16
Degradable, absorbable or resorbable—what is the best grammatical modifier for an implant that is eventually absorbed by the body? Liu Yang , Zheng Yufeng and Hayes Byron Citation: SCIENCE CHINA Materials , 1 ; doi: 10.1007/s40843-017-9023-9 View online: http://engine.scichina.com/doi/10.1007/s40843-017-9023-9 Published by the Science China Press Articles you may be interested in Biomechanical comparison of locking plate and crossing metallic and absorbable screws fixations for intra-articular calcaneal fractures SCIENCE CHINA Life Sciences 59, 958 (2016); Nano-phases and corrosion resistance of C+Mo dual implanted steel Science in China Series E-Technological Sciences 44, 383 (2001); Rapidly in situ forming biodegradable hydrogels by combining alginate and hydroxyapatite nanocrystal SCIENCE CHINA Technological Sciences 53, 272 (2010); Biological effect on sugar beet seeds induced by ion implantation Chinese Science Bulletin 44, 1286 (1999); Special Topic on Bio-based and Biodegradable Polymers SCIENCE CHINA Chemistry 59, 1353 (2016);

lbmd.coe.pku.edu.cnlbmd.coe.pku.edu.cn/PDF/2017SCM.pdf · mater.scichina.com link.springer.com Publishedonline26April 2017 | doi: 10.1007/s40843-017-9023-9 Sci China Mater ,():1–

  • Upload
    vunga

  • View
    213

  • Download
    0

Embed Size (px)

Citation preview

Degradable absorbable or resorbablemdashwhat is the best grammatical modifier for an implantthat is eventually absorbed by the bodyLiu Yang Zheng Yufeng and Hayes ByronCitation SCIENCE CHINA Materials 1 doi 101007s40843-017-9023-9View online httpenginescichinacomdoi101007s40843-017-9023-9Published by the Science China Press

Articles you may be interested in

Biomechanical comparison of locking plate and crossing metallic and absorbable screws fixations for intra-articularcalcaneal fracturesSCIENCE CHINA Life Sciences 59 958 (2016)

Nano-phases and corrosion resistance of C+Mo dual implanted steelScience in China Series E-Technological Sciences 44 383 (2001)

Rapidly in situ forming biodegradable hydrogels by combining alginate and hydroxyapatite nanocrystalSCIENCE CHINA Technological Sciences 53 272 (2010)

Biological effect on sugar beet seeds induced by ion implantationChinese Science Bulletin 44 1286 (1999)

Special Topic on Bio-based and Biodegradable PolymersSCIENCE CHINA Chemistry 59 1353 (2016)

materscichinacom linkspringercom Published online 26 April 2017 | doi 101007s40843-017-9023-9Sci China Mater () 1ndash

Degradable absorbable or resorbablemdashwhat is thebest grammatical modifier for an implant that iseventually absorbed by the bodyYang Liu1 Yufeng Zheng1 and Byron Hayes2

ABSTRACT The adoption of grammatical modifier for im-plants or other kinds of biomaterials eventually absorbed bythe body has been a long-standing confusing issue and thereare diverse terms in the large fields of research which notonly causes the difficulties when searching on the Internetbut also blurs the meaning and boundaries for researchersPrior unification attempts at lawsstandards set the basis forsuch research fields towards researching labeling marketingand instructions for use Considering this the typical gram-matical modifiers ldquobiodegradablerdquo ldquoresorbablerdquo ldquoabsorbablerdquoalong with their noun forms used in the decades of scien-tific research have been reviewed and explained interdiscipli-nary in chemistry ecology materials science biology micro-biology medicine and based on usage customs laws stan-dards and markets The term ldquobiodegradablerdquo has been notonly used in biomaterials but also in ecology waste manage-ment biomedicine and even natural environment Mean-while the term ldquoresorbablerdquo has long been used in biologicalreaction (osteoclast driven bone resorption) but is inappro-priate for implants that do not carry the potential to growback into their original form The term ldquoabsorbablerdquo focusesmore on the host metabolism to the foreign biodegradationproducts of the implanted materialdevice compared with theterm ldquodegradablebiodegradablerdquo Meanwhile the coherenceand normalization of the term ldquoabsorbablerdquo carried by its ownin laws and standards contributes as well In general the au-thors consider the term ldquoabsorbablerdquo to be the best grammat-ical modifier with respect to other adjectives which share thesame inherence A further internationally unified usage isproposed by us

Keywords biodegradation bioabsorption bioresorptionbiodegradable absorbable biomaterials

INTRODUCTION

Current situationTechnologies labeled as absorbable bioabsorbable re-sorbable bioresorbable degradable biodegradable or bysome other similar terms all of which carry the inher-ent underlying potential to allow treated tissue to returnto its native state have been developed for a long timeMore specifically it likely started with the use of sheepgut guitar strings (made of natural collagens recognizedas absorbable polymer today) to approximate woundsover 2000 years ago in the Roman Empire [1] As timeand technology progressed the catgut suture technologybecame significantly refined and synthetic polymers werealso developed both of which led to the absorbable su-tures we find in broad use today Resorbable bioceramictechnologies also entered into use as bone fillers [23] Inaddition the newly evolving biodegradable metals (suchas Mg Fe and Zn and their alloys) are now making theirway into the commercial marketplace [45] All thesedevices carry the promise of fulfilling their intended initialphysicalmechanical function and then undergoing com-positional conversion into components that are eventuallyabsorbed by the bodyMeanwhile numerous terms have been used to describe

the same general concept with the diversity of terms pro-viding self-evidence of either the absence or non-adherenceto standard terminology Compounding this nomenclaturedilemma literature in the field of absorbablebiodegrad-ableresorbable implant materials has been increasing ex-ponentially since the mid-1980s when the synthetic alpha-

1 Department of Materials Science and Engineering College of Engineering Peking University Beijing 100871 China2 Biomaterials Research and Development Medical Product Division WL Gore amp Associates Inc Flagstaff Arizona 86003 USA Corresponding author (email yfzhengpkueducn)

1 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

hydroxyester polymeric resins first became broadly avail-able from commercial suppliers To attain a preliminaryunderstanding of the scope of the confusion surroundinglabeling of these implants all any person has to do is to ini-tiate an Internet search whichmdashin order to confidently ad-dress a single simple conceptmdashbegins as a convoluted as-terisk-filled multi-line querySuch problem not only causes the difficulties when

searching on the Internet but also blurs the meaning andboundaries for researchers The absence of any universalterm recognition unnecessarily complicates communica-tion and confounds the selection of language for researchpapers legal descriptions international trade agreementsas well as the language used in an implantrsquos labelingmarketing and instructions for use Regardless of itsobviousness the problem has been a present and fullyrecognized problem that has persisted for decades Someintermittent attempts have been made by researchers tounify this disparate language into a single preferred term[67] As a result multiple purportedly ldquodefinitiverdquo papershave been published through the years However manyof these papers reflect the perspective of a single authoror society which often leads to conflicts between nomen-clature preferences [8ndash13] for even a single professionalsocietyrsquos breadth of view can be similarly limited by its ownscope Materials that are absorbed by the body do spanmany medical disciplines and the breadth of the technol-ogyrsquos applicability may contribute toward inhibiting anyone professional society from attempting a nomenclatureresolutionmdashas can be evidenced at numerous conferenceswhere one can observe an internal array of presentationsand posters with titles and terminology spanning most (ifnot all) the terms described in the 1st sentence

Standards development in advanceTypically absent from most of these historical nomencla-ture recommendations was any comprehensive consid-eration of the truly broader medical context containedwithin medical dictionaries and the relevant pharma-copeial andor implantable device-related standards [14]Early device and pharmaceutical companies regulatorsand any of the involved standards development organi-zations all had to consciously think about and decide onthe specific terms to include on their labels and in anygoverning standard regulation andor law With implantsthat are eventually absorbed by the body the selection andstandardization of terminology by the United States Phar-macopeia had already occurred and had fully focused onthe term ABSORBABLE by 1939 through its official des-

ignations of both ABSORBABLE and NONABSORBABLEsutures [1516] This same standardized language and clas-sifications remain in place today and have been for decadesembedded in both United States Federal laws and US-Foodand Drug Administration (FDA) regulations [17ndash19] (tobe discussed in later section) as well as in theUnited StatesBritish and European Pharmacopeias [20ndash22] Trying tochange or reverse what has already been both functionaland established in both regulations and law (now fordecades) is both difficult and a questionable undertakingRegardless of this historic and significant establishment ofABSORBABLE as standardized terminology it is possiblethat a simple lack of awareness andor rigorous review bythose involved in the broader research and clinical fieldsmay have become the source for the plethora of similar andanalogously utilized terms we routinely encounter todayThe advances in standard unification of the grammatical

modifier provide insights to the term usage in the researchof such field Due to the fact that many grammatical mod-ifiers have been used in this field for a long time typicalterms have been reviewed and explained interdisciplinaryin chemistry ecology materials science biology microbi-ology medicine and based on usage habits laws standardsand markets Furthermore the international unification ofthe grammatical term usage is proposed

TERMINOLOGYAs stated in the opening sentence multiple terms are be-ing utilized to describe the same general absorbable im-plant concept which includes absorbable bioabsorbableresorbable bioresorbable degradable biodegradable andpotentially other similar themes To provide an improvedunderstanding of the scope of current language diversityan overview of the usage of the aforementioned words wasundertaken to provide data that assisted in both confirmingand clarifying the scope of the problem The results are in-tended to provide a summary understanding of the scopeof confusion (ie how big the problem really is) so as tobetter facilitate identification of an appropriate remedy

Overview of utilization of the terms ldquodegrada-tionrdquoldquobiodegradationrdquo and ldquodegradablerdquoldquobiodegradablerdquoldquoDegradationrdquo and ldquobiodegradationrdquo are both used inpolymers and ceramics for a period of time and had beennoted by Prof D Williams as ldquothe process as deleteriouschange in the chemical structure physical propertiesor appearance of a materialrdquo according to the AmericanSociety for Testing and Materials (ASTM) [23] In theresearch of ldquobiorelatedrdquo polymers International Union

2copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

of Pure and Applied Chemistry (IUPAC) suggested thatldquodegradation indicates progressive loss of the performanceor of the characteristics of a substance or a devicerdquo [14] Itis also a general process since there can be degradationscaused by the action of water named ldquohydrodegradationrdquoor hydrolysis As for biorelated polymers the degradationprocess is limited to macromolecule cleavage and molarmass decrease which distinguishes the degradation ofbiorelated polymer from fragmentation and disintegrationillustrated in bioceramics The term ldquodegradationrdquo wasformerly used in bioceramics by Prof L Hench to describethe decomposition process of calcium phosphate ceramicswhich was followed by host response and tissue repair [3]Thus the definition of ldquodegradationrdquo used in polymers andceramics fields could be interpreted as different inferringmore specifically to chemical processes for bio-relatedpolymers while referring to physical break down from theview of bio-ceramics researchersAs for the term ldquobiodegradationrdquo it is not the simple

addition of the prefix ldquobio-rdquo to ldquodegradationrdquo Fig 1 de-scribes the common usage of ldquobiodegradationrdquo currentlyThe word was firstly introduced as the consumption ofmaterial by bacteria fungi or other biological means inecology waste management biomedicine and even naturalenvironment [24] Some kinds of environmentally friendlyproducts also undergo such process as they can be degraded

by microorganisms and do no harm to the environmentHowever some researchers studying polymers and ceram-ics have defined a more specific scope for ldquobiodegradationrdquoFor polymers especially biorelated polymers the differ-ence between ldquobiodegradationrdquo and ldquodegradationrdquo lies inthe involvement of enzymatic process [1425]mdasha distinc-tion that can be problematic if both modes are active in animplantrsquos degradation process Moreover IUPAC stressedthe importance of proved degradation mechanisms whenusing ldquobiodegradationrdquo otherwise ldquodegradationrdquo should beused instead of ldquobiodegradationrdquo In general ldquodegradationrdquoand ldquobiodegradationrdquo both refer to the chain scission orchain cleavage Nevertheless the meaning of ldquobiodegra-dationrdquo in bioceramics is different since there is no suchprocess as chain scission The degradation process ofso-called ldquoresorbable ceramicsrdquo is claimed to involve eitherdecomposition to small particles as well as dissolved ionswhich participate in the enzymecell mediated reactionand new tissue forms [326ndash28] Despite the exact degra-dation process still needs further investigations the wordldquodegradationrdquo used for ldquoresorbablerdquo ceramics expressesmultiple meanings covering both chemical and physicalreactions in physiological environment such as hydrolysisdecomposition and debris formation According to ProfD Williams the recommended definition of ldquobiodegrada-tionrdquo is the gradual breakdown of a material mediated by

Figure 1 Common use of biodegradation currently

3 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

specific biological activity [23] Another definition as thebiomaterial or medical device involving loss of their in-tegrity or performance when exposed to a physiological orsimulated environment which existed in some ISO Techni-cal Report was not recommended since no specific respectto biological activity mentioned [23]Beyond the category of biomaterials ldquodegradablerdquo in

pure chemistry was defined as qualifier to a substance thatcan undergo physical andor chemical deleterious changesof some properties especially of integrity under stressconditions [14] Thus degradable polymer is consideredwith macromolecules being able to undergo chain scis-sions resulting in a decrease of molar mass [14] BesidesASTM made a standard definition on ldquodegradablerdquo in thescope of soil rock and contained fluids as ldquoin erosioncontrol decomposes under biological chemical processesor ultraviolet stresses associated with typical applicationenvironmentsrdquo [29] Despite no specific emphasis onbiomaterials numerous publications used ldquodegradablerdquo to

modify metals polymers or compounds in tissue engineer-ing drug delivery and gene delivery [30ndash35] Meanwhilein some ASTM standard specifications the definition ofthe adjective ldquobiodegradablerdquo is given as capable of de-composing under natural conditions into elements foundin the nature [36ndash42] The active ASTM entries currentlywith ldquobiodegradationrdquo ldquodegradablerdquo and ldquobiodegradablerdquoin the title are summarized in Table 1 The adoptionsof ldquobiodegradationrdquo ldquodegradablerdquo and ldquobiodegradablerdquoby ASTM are historical generally in the classification ofecology or environmental protectionWhile the above listing provides evidence that the usage

of the term biodegradable is broad it is particularly notablethat almost all of the listed standards are not relevant toimplantable devices Instead the listing primarily reflectsusage directed toward the environmental degradation as-pect that is most commonly recognized within the broadernon-medical oriented population ASTM-F1635 a stan-dard specifically centered on the hydrolytic degradation

Table 1 Summary of the terms ldquobiodegradationrdquo ldquodegradablerdquo and ldquobiodegradablerdquo being utilized in ASTM titles (not limited to implant)

Terminology ASTM titles

ASTM D5864-11 Standard Test Method for Determining Aerobic Aquatic Biodegradation of Lubricants or TheirComponents

ASTM D6954-04(2013) Standard Guide for Exposing and Testing Plastics that Degrade in the Environment by aCombination of Oxidation and Biodegradation

ASTM D5511-12 Standard Test Method for Determining Anaerobic Biodegradation of Plastic Materials Under High-SolidsAnaerobic-Digestion Conditions

ASTM D6139-11 Standard Test Method for Determining the Aerobic Aquatic Biodegradation of Lubricants or TheirComponents Using the Gledhill Shake Flask

ASTM D7991-15 Standard Test Method for Determining Aerobic Biodegradation of Plastics Buried in Sandy MarineSediment under Controlled Laboratory Conditions

ASTM D5338-15 Standard Test Method for Determining Aerobic Biodegradation of Plastic Materials Under ControlledComposting Conditions Incorporating Thermophilic Temperatures

ASTM D6691-09 Standard Test Method for Determining Aerobic Biodegradation of Plastic Materials in the MarineEnvironment by a Defined Microbial Consortium or Natural Sea Water Inoculum

ASTM D5526-12 Standard Test Method for Determining Anaerobic Biodegradation of Plastic Materials Under AcceleratedLandfill Conditions

ASTM D7475-11 Standard Test Method for Determining the Aerobic Degradation and Anaerobic Biodegradation of PlasticMaterials under Accelerated Bioreactor Landfill Conditions

Biodegradation

ASTM D5988-12 Standard Test Method for Determining Aerobic Biodegradation of Plastic Materials in Soil

ASTM F1635-11 Standard Test Method for in vitro Degradation Testing of Hydrolytically Degradable Polymer Resinsand Fabricated Forms for Surgical Implants

ASTM D7444-11 Standard Practice for Heat and Humidity Aging of Oxidatively Degradable PlasticsDegradable

ASTM D3826-98(2013) Standard Practice for Determining Degradation End Point in Degradable Polyethylene andPolypropylene Using a Tensile Test

ASTM D7665-10(2014) Standard Guide for Evaluation of Biodegradable Heat Transfer Fluids

ASTM D8029-16 Standard Specification for Biodegradable Low Aquatic Toxicity Hydraulic FluidsBiodegradable

ASTM D7044-15 Standard Specification for Biodegradable Fire Resistant Hydraulic Fluids

4copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

testing of absorbable polyesters is the sole listed standardfrom ASTM Committee F04mdashMedical and Surgical Im-plants and thereby is directly relevant to implantable de-vices However this standard utilizes the term degradeand its derivatives specifically in reference to the process ofdegradation that occurs as a result of ester hydrolysis Con-versely the same standard uses the term absorbable to de-scribe a class of implants that are eventually absorbed by thebody which it defines as ldquoabsorbable adjmdashin the bodymdashaninitially distinct foreign material or substance that either di-rectly or through intended degradation can pass through orbe assimilated by cells andor tissuerdquo

Overview of utilization of the terms ldquoabsorptionrdquoldquobioab-sorptionrdquo and ldquoabsorbablerdquoldquobioabsorbablerdquoThe term ldquoabsorptionrdquo was recognized by IUPAC as theprocess of penetration and diffusion of a substance (ab-sorbate) into another substance (absorbent) as a result ofthe action of attractive phenomena The IUPAC defini-tion is within the scope of chemistry As for biomaterialsProf D Williams adopted the definition in Dorland Medi-cal Dictionary as the uptake of substances into or across tis-sues [23] For this kind of definition ldquoabsorptionrdquo empha-sizes the interaction of materials and human or animal tis-sue The same connotation is shared by its derivative wordsldquoabsorbablerdquo and ldquobioabsorbablerdquo as capable of being de-graded or dissolved and subsequently metabolized withinan organism [23] Besides the prefix ldquobio-rdquo is abridged as

it is redundant in the field of implantation [43] ASTM hasmade standard definition on ldquoabsorbablerdquo in the field of ab-sorbable polymers as well as absorbablemetals which it de-fines as ldquohellip an initially distinct foreign material or substancethat either directly or through intended degradation can passthrough or be metabolized or assimilated by cells andor tis-sue in the bodyrdquo [43] Table 2 summarizes the currently ac-tive ASTM standards and both United States and EuropeanPharmacopeia implantable device monographs that utilizethe word ldquoabsorbablerdquo in the title Distinctly different fromldquobiodegradablerdquo the utilization of ldquoabsorbablerdquo displays adistinct preference for use in describing this particular classof biomedical materials and devicesAs can be observed in both Table 1 and Table 3 the

well-established terminology for describing sutures is verybroadly based on the term absorbable with historicalapplication of the term to the original gut sutures andeven extending to permanent sutures through the ldquononab-sorbablerdquo descriptorAside from the language of standards organization the

terminology utilized by regulatory agencies is also of par-ticular relevance Through multiple laws and regulationsthe US-FDA is authorized to evaluate medical device man-ufacturers and their products The US Code of FederalRegulations (CFRs) that is specific to sutures legally de-scribes those regulated devices based on composition andthen designates both their product class and needs to meetUSP requirements While Table 3 demonstrates both a US-

Table 2 ldquoAbsorbablerdquo utilized in title entries for implantable device related standards

Terminology Title entries

ISOTS 171372014 Cardiovascular implants and extracorporeal systemsmdashCardiovascular absorbable implants

ISOTR 371372014 Biological evaluation of medical devicesmdashGuidance for absorbable implants

ASTM F3036-13 Standard Guide for Testing Absorbable Stents

ASTM F2902-16 Standard Guide for Assessment of Absorbable Polymeric Implants

ASTM F2502-16 Standard Specification and Test Methods for Absorbable Plates and Screws for Internal Fixation Implants

ASTM F1983-14 Standard Practice for Assessment of Selected Tissue Effects of Absorbable Biomaterials for Implant Applications

ASTM F3160-16 Standard Guide for Metallurgical Characterization of Absorbable Metallic Materials for Medical Implants

United States Pharmacopoeia (USP 39NF 34) monographldquoAbsorbable Surgical Suturerdquo

United States Pharmacopoeia (USP 39NF 34) monographldquoNonabsorbable Surgical Suturerdquo

European Pharmacopoeia (88)ldquoSterile non-absorbable suturesrdquo ndash 1118

European Pharmacopoeia (88)ldquoSterile synthetic absorbable braided suturesrdquo - 1122

Absorbable

European Pharmacopoeia (88)Sterile synthetic absorbable monofilament sutures ndash 1123

5 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Table 3 US-FDA suture product codes and accompanying citation of US CFRsa)

Suture name Regulation Product code

Absorbable polydioxanone surgical (PDS) suture 21 CFR8784840 NEW

Absorbable poly(glycolideL-lactide) surgical suture 21 CFR8784493 GAM

Absorbable gut suture 21 CFR8784830 GAL

Nonabsorbable poly(ethylene terephthalate) suture 21 CFR8785000 GAT

Nonabsorbable polypropylene surgical suture 21 CFR8785010 GAW

Nonabsorbable polyamide surgical suture 21 CFR8785020 GAR

Natural nonabsorbable silk surgical suture 21 CFR8785030 GAP

Stainless steel surgical suture 21 CFR8784495 GAQ

Nonabsorbable expanded polytetrafluoroethylene (ePTFE)surgical suture

21 CFR8785030 NBY

a) Note this table selects abbreviated results obtained from online search for the implant device term ldquosuturerdquo that was conducted on 6 Aug 2016 athttpwwwaccessdatafdagovscriptscdrhcfdocscfPCDclassificationcfm

FDA and a US Code of Federal Regulations preference forabsorbable terminology when referring to sutures Table4 shows an expansion of that preference to include a to-tal of 30 absorbable implant product classifications each ofwhich is assigned to a relevant Federal regulation that uti-lizes the term ldquoabsorbablerdquoIn short ldquoabsorbablerdquo is both a historically well estab-

lished and currently relevant term in both the regulationand standardization of implants that are intentionally ab-sorbed by the body

Overview of utilization of the terms ldquoresorptionrdquoldquobiore-sorptionrdquo and ldquoresorbablerdquoldquobioresorbablerdquoIn the scope of chemistry the term ldquoresorptionrdquo was used toillustrate the total elimination of a substance from its initialplace caused by physical andor chemical phenomena [14]Besides the understanding from pure chemistry ldquoresorp-tionrdquo is more recognized involved in the metabolic activi-ties in vivo For example ldquoresorptionrdquo is considered as theldquoabsorptionrdquo into the circulatory system of cells or tissuewhich usually includes bone resorption tooth resorptionand vanishing twin [44] In the biomedical scope Prof DWilliams used themeaning in DorlandMedical Dictionaryas ldquolysis and assimilation of a substance as of bonerdquo [23]ldquoBioresorptionrdquo is more common when describing the invivo process of a certain foreign material The ISO definedldquobioresorptionrdquo as a process by which biomaterials are de-graded in the physiological environment and the by-prod-uct are eliminated or completely bioabsorbed [23] Thusaccording to this interpretation the bioresorption processincludes material removal in vivo either by cellular activ-ity or not Conversely Taberrsquos Cyclopedic Medical Dictio-nary [45] describes the term ldquoresorbrdquo as themeaning ldquoto ab-

sorb againrdquomdashsomething that live tissue does but not some-thing any implant is known to domdashbe it permanent or ab-sorbableAs for the adjectives ldquobioresorbablerdquo and ldquoresorbablerdquo

there is no difference when used to describe a kind of ma-terials which have the ability of resorption This is ascribedto the fact that ldquoresorptionrdquo itself already has been well rec-ognized as a biological process [23] Currently there is noASTM entries used ldquoresorbablerdquo or ldquobioresorbablerdquo in thetitle

Utilization and comparison of the terms ldquobiodegradablemetalsrdquo and ldquoabsorbable metallic materialsrdquoldquoBiodegradablemetalsrdquo generally include themetalsMg Feand Zn and their alloys and composites They can be de-fined as metals that assist with tissue healing and are thenexpected to gradually corrode and release corrosion prod-ucts in vivowith an appropriate host response and then dis-solve completely with no implant residues [46] As a resultand different from traditional ldquobio-inertrdquometallic biomate-rials (eg Ti and Co based alloys) that release limited cor-rosion products [47] metabolic reactions besides inflam-mation can be expected to occur between the biodegrad-able metal and the host body after implantation Addition-ally the corrosion-based degradation mechanism of thesematerials is inherently different from that of either bioce-ramics or polymers which has resulted in limited to nostandardized guidance available from either ASTM or ISOInstead of the term ldquobiodegradable metalrdquo the recently

published and first absorbable metal related standardASTM F3160 utilizes the more inclusive word ldquoabsorbablerdquowithin the phrase ldquoabsorbable metallic materialsrdquo andagain defines the term as ldquohellip an initially distinct foreign

6copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Table 4 US-FDA absorbable implant related product codes descriptions and accompanying CFRsa)

Product code Device Device class Regulation number Regulation description

OMT Absorbable lung biopsy plug 2 [8784755] Absorbable lung biopsy plug

LMF Agent absorbable hemostatic collagen based 3 [8784490] Absorbable hemostatic agent and dressing

LMG Agent absorbable hemostatic non-collagen based 3 [8784490] Absorbable hemostatic agent and dressing

MRY Appliances and accessories fixation bone absorbable singlemultiple component 2 [8883040] Smooth or threaded metallic bone fixation fastener

PBQ Fixation non-absorbable or absorbable for pelvic use 2 [8844530] Obstetric-gynecologic specialized manual instrument

HQJ Implant absorbable (scleral buckling methods) 2 [8863300] Absorbable implant (scleral buckling method)

OWT Mesh surgical absorbable abdominal hernia 2 [8783300] Surgical mesh

OXM Mesh surgical absorbable fistula 2 [8783300] Surgical mesh

OXI Mesh surgical absorbable large abdominal wall defects 2 [8783300] Surgical mesh

OXL Mesh surgical absorbable organ support 2 [8783300] Surgical mesh

OWW Mesh surgical absorbable orthopaedics reinforcement of tendon 2 [8783300] Surgical mesh

OXF Mesh surgical absorbable plastic and reconstructive surgery 2 [8783300] Surgical mesh

OXC Mesh surgical absorbable staple line reinforcement 2 [8783300] Surgical mesh

OWZ Mesh surgical absorbable thoracic chest wall reconstruction 2 [8783300] Surgical mesh

OWU Mesh surgical non-absorbable diaphragmatic hernia 2 [8783300] Surgical mesh

OWR Mesh surgical non-absorbable facial implants for plastic surgery 2 [8783300] Surgical mesh

OXJ Mesh surgical non-absorbable large abdominal wall defects 2 [8783300] Surgical mesh

OWX Mesh surgical non-absorbable orthopaedics reinforcement of tendon 2 [8783300] Surgical mesh

OXG Mesh surgical non-absorbable plastic and reconstructive surgery 2 [8783300] Surgical mesh

OXD Mesh surgical non-absorbable staple line reinforcement 2 [8783300] Surgical mesh

OXA Mesh surgical non-absorbable thoracic chest wall reconstruction 2 [8783300] Surgical mesh

LBP Replacement ossicular (stapes) using absorbable gelatin material 2 [8743450] Partial ossicular replacement prosthesis

OLL Septal staplerabsorbable staples 2 [8784750] ImplanTABLE staple

MNU Staple absorbable 2 [8883030] Singlemultiple component metallic bone fixationappliances and accessories

GAK Suture absorbable 2 [8784830] Absorbable surgical gut suture

GAL Suture absorbable natural 2 [8784830] Absorbable surgical gut suture

HMO Suture absorbable ophthalmic 3

GAN Suture absorbable synthetic 2 [8784830] Absorbable surgical gut suture

GAM Suture absorbable synthetic polyglycolic acid 2 [8784493] Absorbable poly(glycolidel-lactide) surgical suture

NEW Suture surgical absorbable polydioxanone 2 [8784840] Absorbable polydioxanone surgical suture

a) Note the results obtained from online search for the device term ldquoabsorbablerdquo that was conducted on 6 Aug 2016 at httpwwwaccessdatafdagovscriptscdrhcfdocscfPCDclassifica-tioncfm

7 copy

ScienceChina

Pressand

Springer-VerlagBerlin

Heidelberg 2017

SCIENCECH

INAMaterials

REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

material or substance that either directly or through in-tended degradation can pass through or be metabolized orassimilated by cells andor tissuerdquo The standardrsquos nomen-clature appendix further elaborates on its preference forldquoabsorbablerdquo since the prefix ldquobio-rdquo is redundant in thecontext of implant applications [43]Clearly these two terms of ldquobiodegradable metalsrdquo and

ldquoabsorbable metallic materialsrdquo share the same connota-tion which defines the completemission of an intentionallydegradable material when implanted in vivo In the contextof biodegradable metalsabsorbable metallic materialsthe process includes the corrosion caused by body fluida host response caused by corrosion products followedby dissolutionabsorption and finally improved tissuehealing The ldquobiodegradationrdquo instead of ldquobiocorrosionrdquois used to distinguish this new kind of metals which canfully dissolve in vivo with no implant residues Besidesbiodegradation process the following dynamic process ofdissolutionabsorption also starts in vivo For exampledissolved Mg2+ is considered to enhance the integrin me-diated human-bone-derived cell adhesion and affect newbone formation [48] The metabolic reaction is also crucialand even more important for biodegradable metals as it ishelpful It is another distinction from traditional metalsused for biomedical application In fact the different usagehabit forming of ldquobiodegradablerdquo or ldquoabsorbablerdquoldquobioab-sorbablerdquo may be more related with the study field theresearchers in Taking the ldquoabsorbablerdquo metallic stent asan example (Fig 2) once the ldquoabsorbablerdquo metallic stentwas implanted into blood vessel ldquocorrosionrdquo of biometal

begins The corrosion products including debris hydro-gen (for Mg-based metals) metallic ions and hydroxylconvert the local environment and diffuse into the bloodvessel wall Some corrosion products can be biologicallybeneficial For instance the diffused and absorbed Zn2+

can potentially play a positive role in dealing with athero-sclerosis [49] Along with the corrosion process healingprocesses such as endothelialization may become en-hanced In summary and within the context of absorbablemetals the adjectives ldquodegradablerdquo and ldquoabsorbablerdquo referto the nature of the biodegradation products of the mate-rialdevice being metabolically absorbed an attribute ofthe host (animal or human body) regardless of whetherthe implant degrades corrodes hydrolyzes or dissolves[50ndash52]

Summary quantification of the common TermsFig 3a shows preliminary searching results in Webof Knowledge using ldquodegradablerdquo ldquoabsorbablerdquo or ldquore-sorbablerdquo along with ldquomaterialrdquo as key words Theutilization of ldquodegradablerdquo is a bit more frequently thanldquoabsorbablerdquo but that of ldquoresorbablerdquo steps down Mean-while the counterpart searching result when using ldquobiordquo asprefix to the adjectives along with ldquomaterialrdquo as keywordsare presented in Fig 3b ldquoBiodegradable materialrdquo is themost common utilization which holds 91 among the ex-pression approach This is also due to the fact that besidesthe common utilization in biomaterials ldquobiodegradablerdquois also used in a wide range of applications such as cleanenvironment and ecology [5354]

Figure 2 Different point of views on the biodegradationabsorption process

8copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Figure 3 Searching results in Web of Knowledge from all databases (a) with the total searched publication numbers by ldquodegradablerdquo+ ldquomaterialrdquoldquoabsorbablerdquo+ ldquomaterialrdquo and ldquoresorbablerdquo+ ldquomaterialrdquo as 100 (b) the total searched publication numbers by ldquobiodegradablerdquo+ ldquomaterialrdquo ldquobioab-sorbablerdquo+ ldquomaterialrdquo and ldquobioresorbablerdquo+ ldquomaterialrdquo as 100

DISCUSSION

Expertise inherent biasesAs previously mentioned biomaterial is an interdiscipli-nary field fascinating researchers with specialty from dif-ferent backgrounds Different backgrounds as well as dif-ferent research point of interests may be one of the reasonsfor using different terminologies Materials scientists tendto focus on the materialdevice itself leading to their usageof ldquobiodegradablerdquo to illustrate what happens to the deviceThey pay more attention to the process such as hydroly-sis corrosion debris degradation products and the changeof surface morphology resulting in the researching inter-ests of ldquomaterial biodegradationrdquo In contrast surgeons andbiomedical researchers tend to be concerned more on thehost response and healing process They are curious aboutthe absorption of various degradation products of the im-planted materialdevice and related metabolism mecha-nism and thereby prefer to use the term ldquoabsorbablerdquo toillustrate what happens to the device As known somema-terials may only undergo biodegradation but the corrosionproducts still have no influence on the metabolic activitiesFor example cellulose is considered as ldquodietary fiberrdquowhichcannot be digested and absorbed by human body but is be-nign for human body [55] Some coating tablets for drug ordrug delivery systems made from cellulose and its deriva-tives are quite frequently utilized or investigated [5657]The polymer and derivatives of cellulose can only be de-graded but not be absorbed by human body [58] For suchmaterials the adjective ldquoabsorbablerdquo or ldquobioabsorbablerdquo isnot appropriateOverall once the materialsdevices are implanted into

the human body the ldquobiocorrosionrdquobiodegradationrdquoprocess happens immediately no matter to what degreeat the same time the host will biologically response to the

corrosiondegradation products through the absorptionmetabolism and excretion processes So for the samestory the majority of materials scientists would report itby ldquobiodegradabledegradationrdquo way whereas the majorityof medical doctors would report it by ldquoabsorbableab-sorptionrdquo way In nature the two terms ldquobiodegradablemetalsrdquo and ldquoabsorbable metallic materialsrdquo share the sameconnotation and are mutually replaceable

Connotation and extension of noun forms ldquobiodegradationbioabsorption and bioresorptionrdquo and adjectivesldquobiodegradable bioabsorbable and bioresorbablerdquoThe three noun forms of the terms illustrate the processwhile their adjectival derivatives were used to describe thegroup of materials with such certain capabilities For thestudy on biomaterials polymer researchers use ldquodegrada-tionbiodegradationrdquo when there is proved chain scissionprocess Besides they differentiate ldquobiodegradationrdquo andldquodegradationrdquo by confirmed metabolic activities betweenthe materials and cells or tissues Regarding to the fouradjectives ldquobiodegradablerdquo ldquobioabsorbablerdquo and ldquobiore-sorbablerdquo the term ldquobiocorrodiblerdquo is only used in scientificpapers on iron based materials and some patents on mag-nesium based materials The common usage of termsldquobiodegradablerdquo ldquobioabsorbablerdquo and ldquobioresorbablerdquo withrespect to the biomaterial research area is shown in Table 5The results reveal a widespread usage of ldquobiodegradablerdquo inboth polymers and magnesium based metals Varies typesof materials were reported as biomaterials Besides thereare also reports of ldquobiodegradablerdquo polymers for ecologyand environmental protection which indicates a furtherusage scope of ldquobiodegradablerdquo not only for implants anddevices Besides ldquobioresorbablerdquo is also utilized in all theresearch fields of polymers ceramics andmetals Howeverno current work used ldquobioabsorbablerdquo as grammatical

9 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Table 5 Current reported usage of terms ldquobiodegradablerdquo ldquobioabsorbablerdquo and ldquobioresorbablerdquoTerminology Category Materials Applications

PLA-PEG-biotin PLGA Controlled cell engineering [5960]Porous PLGA Tissue engineering [61ndash63]

PLGA-PEG-PLGA Injective thermosensitive hydrogel [64]PLGA Nerve guidance [65]

Fibronectin (Fn)-coated PLLA P(LLA-CL) Enhanced growth of endothelial cells [6066]PEG tethered PPF [67]

PDMS Drug delivery [68]PGA Tissue engineering [69]

Undefined Coronary stent [70ndash72]PGA Joint resurfacing [73]

Polymers

PHA Ecology and environmental protection [74]CaO-P2O5 glass Bone regeneration [75]β-Whitlockite Bone regeneration [76]

Calcium phosphate hydraulic cement Bone regeneration [77]Calcium

phosphate glass ceramicsBone regeneration [78]

Ceramics

CaO-SiO2-B2O3 glass-ceramics Bone regeneration [79]Pure Mg Implant material [80]

Mg-Ca-based Bone regeneration [81ndash84]Mg-Zn-based Bone regeneration [338586]Mg-Sr-based Bone regeneration [87ndash89]Mg-RE-based Vascular stent [90ndash92]

Mg and its metals

Mg-Ag-based [93]Zn-Mg Zn-Ca Zn-Sr [9495]Zn and its metals Zn-Mg-Sr [96]

Fe [9798]

Biodegradable

Fe and its metals Fe-Mn [99]PLLA PLG PGA Molecule delivery [100]

PGA Suture [101]Undefined Drug-eluting stent [102103]

PLA Neuron attachment [104]Polymers

PLA and PCL reinforced with PGA fibers Bile duct patch [105]Mg-RE based Coronary stent [106ndash109]

Binary Mg alloys [110]Mg and its metalsMg-Al-based [111112]

Zn and its metals Pure Zinc [113114]Fe and its metals Nitrided iron [115]

PLDLA Transforaminal lumbar interbody fusion [116]Alkylene bis(dilactoyl)-methacrylate modified polymer Bone screw augmentation [117]

Undefined Coronary stent [118]PHB Mandibular defects regeneration [119]HA Bone regeneration [120]Ceramics Calcium phosphate [121122]

MgNd2 Stent material [123]Porous Mg Bone substitute [124]Mg-RE Coronary stent [125]Mg-Ca Orthopedic application [126]

Mg and its metals

Mg-based Finite element analysis [127]

Bioabsorbable

Fe and its metals Pure Fe [128]

10copy

ScienceChina

Pressand

Springer-VerlagBerlin

Heidelberg 2017

REVIEWSCIENCE

CHINA

Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

modifier to bioceramics In addition as previouslyillustrated the prefix ldquobiordquo of ldquobioabsorbablerdquo and ldquobiore-sorbablerdquo are abridged hereafter discussion will concen-trate on ldquobiocorrodiblerdquo ldquobiodegradablerdquo ldquoabsorbablerdquo andldquoresorbablerdquoSince absorbable technologies are increasingly utilized

in numerous new and broader implant applications it be-comes more important to not acquiesce in addressing his-torical problems and instead actively move forward towardutilizing standardized language that is both technically ac-curate and unified in itsmeaning Preferred language needsto accurately communicate the concept To achieve the uni-fying goal of harmonized terminology themedical and sci-entific communities need to not solely look at materialschemistry or even biomaterials alone but to instead lookat term selection both across and within the context of thebroader medical disciplinemdashthe location where the resultsof implant technology development actually reaches themarketplace where therapies are brought to those in needNomenclature solutions need to both understand and re-spond to the context of terms across adjacent technologieswhich means to address needs from the perspectives of thebiomaterial researcher the deviceproduct developer thesurgeonclinician user the regulator and last but not leastthe patientgeneral public who is the direct beneficiary ofthe developed technologyA better understanding of these terminologies is neces-

sary and beneficial to the field Therefore the definitionson ldquodegradablerdquo ldquoabsorbablerdquo ldquoresorbablerdquo and relatedterms proposed by different organizations in differentfields have been summarized and discussed with the con-notation and extension of each term being compared andthe criteria being proposed

CONCLUDING REMARKSHerein given both the searching problem on the Internetand ambiguity in meanings the usage of grammaticalmodifiers to describe biomaterials that is eventually ab-sorbed by human body has been enumerated based onusage habits laws standards and markets In summaryldquodegradablerdquoldquobiodegradablerdquo are the most frequently usedgrammatical modifier not only in metals but also poly-mers as such kind of biomaterials ldquoBiodegradationrdquo andldquobiodegradablerdquo define the change of the materialdevicewell in the research of biomaterials but they are alsoadopted in other fields such as ecology and environmentalprotection Meanwhile ldquoresorbablerdquoldquobioresorbablerdquo havelong been recognized in the biological research and theldquoresorptionrdquo itself has been widely accepted as a biological

reaction The utilization of ldquoresorbablerdquoldquobioresorbablerdquowas found to be not as frequent as the counterpartsldquodegradablerdquoldquobiodegradablerdquo and ldquoabsorbablerdquoldquobioab-sorbablerdquo Such usage is accurate for osteoclast driven boneresorption but is inappropriate for implants that do notcarry the potential to grow back into their original formOtherwise despite it is not the most frequently used termldquoabsorbablerdquoldquobioabsorbablerdquo concentrates more on thehost metabolism to the foreign biodegradation productsof the implanted materialdevice compared with ldquodegrad-ablerdquoldquobiodegradablerdquo ldquoAbsorbablerdquo is defined in the scopeof biomaterials by different organizations and their publi-cations and also adopted by ASTM to illustrate ldquoabsorbablepolymerrdquo It is the most historically established the mostbroadly applicable (includes dissolvable devices that donot degrade) the most specific to medical applicationsand is the formal legal descriptor for most implant devicesConsidering the usage history common utilization in lawand standards as well as the scientific meaning in essenceldquoabsorbablerdquo can be better among other grammaticalmodifiers for description of an implant that is eventuallyabsorbed by the body which is recommended by theauthors for a further internationally-unified usage

Received 28 February 2017 accepted 27 March 2017published online 26 April 2017

1 Mackenzie D The history of sutures Med Hist 1973 17 158ndash1682 Hench LL Bioceramics J Am Ceramic Soc 2005 81 1705ndash17283 Hench LL Bioceramics from concept to clinic J AmCeramic Soc

1991 74 1487ndash15104 Windhagen H Radtke K Weizbauer A et al Biodegradable

magnesium-based screw clinically equivalent to titanium screw inhallux valgus surgery short term results of the first prospectiverandomized controlled clinical pilot study BioMed Eng OnLine2013 12 62

5 Schildwaumlchter M Biotronik announces CE mark for magmaristhe first clinically-proven bioresorbable magnesium scaffoldhttpwwwmagmariscomennewsroomjune-15-2016

6 Shalaby SW Burg KJL Bioabsorbable polymers update degrada-tion mechanisms safety and application J App Biomater 1995 6219ndash221

7 Vert M Li SM Spenlehauer G et al Bioresorbability and biocom-patibility of aliphatic polyesters J Mater Sci-Mater Med 1992 3432ndash446

8 Vert M Degradable and bioresorbable polymers in surgery and inpharmacology beliefs and facts J Mater Sci-Mater Med 2009 20437ndash446

9 Benicewicz BC Hopper PK Review polymers for absorbablesurgical suturesmdashPart I J Bioactive Compatible Polym 1990 5453ndash472

10 Barrows HT Synthetic bioabsorbable polymers In Szycher M(Ed) High Performance Biomaterials A Complete Guide toMed-ical and Pharmceutical Applications Boca Raton CRC PRESS1991 243ndash257

11 Weiler A Hoffmann RFG Staumlhelin AC et al Biodegradable

11 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

implants in sports medicine the biological base Arthroscopy-JArthroscopic Related Surgery 2000 16 305ndash321

12 Ikada Y Tsuji H Biodegradable polyesters for medical and ecolog-ical applications Macromol Rapid Commun 2000 21 117ndash132

13 Ashammakhi N Peltoniemi H Waris E et al Developments incraniomaxillofacial surgery use of self-reinforced bioabsorbableosteofixation devices Plast Reconstr Surg 2001 108 167ndash180

14 Vert M Doi Y Hellwich KH et al Terminology for biorelatedpolymers and applications (IUPACRecommendations 2012) PureAppl Chem 2012 84 377ndash410

15 The United States Pharmacopeial Convention The Second Sup-plement to the Pharmacopeia of the United States of America 11thdecennial revision (USP XI-1939 Supplement) 1939

16 Truhlsen SM The recession operation histopathologic responseand suture reaction and absorption Trans Am Ophthalmol Soc1965 63 626ndash677

17 USP in US Law httpwwwusporgprintabout-usplegal-recog-nitionusp-us-law

18 USP develops and publishes standards for drug substances drugproducts excipients and dietary supplements in the United StatesPharmacopeia-National Formulary (USP-NF)

19 United States Public Law 94-295 197620 United States Pharmacopeia httpwwwusporg21 British Pharmacopeia httpswwwpharmacopoeiacom22 European Pharmacopoeia httponlinepheurorgENentryhtm23 Williams DF The Williams Dictionary of Biomaterials Liverpool

Liverpool University Press 199924 httpsenwikipediaorgwikiBiodegradation25 Jones RG Kahovec J Stepto R et al Compendium of Polymer

Terminology and Nomenclature IUPAC Recommendations 2008Cambridge RSC Publishing 2009

26 Higashi S Yamamuro T Nakamura T et al Polymer-hydroxyap-atite composites for biodegradable bone fillers Biomaterials 19867 183ndash187

27 de Groot K Bioceramics of Calcium Phosphate Boca Raton CRCPress 1983

28 Hollinger JO Battistone GC Biodegradable bone repair materialssynthetic polymers and ceramics ClinOrthopRelat Res 1986 207290ndash306

29 ASTMD653-14 Standard Terminology Relating to Soil Rock andContained Fluids ASTM International West Conshohocken PA2014 httpswwwastmorgStandardsD653htm

30 Witte F Hort N Vogt C et al Degradable biomaterials based onmagnesium corrosion Curr Opin Solid State Mater Sci 2008 1263ndash72

31 Lynn DM Langer R Degradable poly(β-amino esters) synthesischaracterization and self-assemblywith plasmidDNA JAmChemSoc 2000 122 10761ndash10768

32 Cima LG Vacanti JP Vacanti C et al Tissue engineering by celltransplantation using degradable polymer substrates J BiomechEng 1991 113 143ndash151

33 Zhang S Zhang X Zhao C et al Research on an Mg-Zn alloy as adegradable biomaterial Acta Biomater 2010 6 626ndash640

34 Anseth KS Metters AT Bryant SJ et al In situ forming degradablenetworks and their application in tissue engineering and drug de-livery J Control Release 2002 78 199ndash209

35 Forrest ML Koerber JT Pack DW A degradable polyethyleniminederivative with low toxicity for highly efficient gene delivery Bio-conjugate Chem 2003 14 934ndash940

36 ASTM E2747-11 Standard Specification for Evaluation and Selec-tion of Onsite Offices for Environmentally Sustainable MeetingsEvents Trade Shows and Conferences ASTM International

West Conshohocken PA 2011 httpswwwastmorgStan-dardsE2747htm

37 ASTM E2745-11 Standard Specification for Evaluation andSelection of Audio Visual (AV) and Production for Environ-mentally Sustainable Meetings Events Trade Shows and Con-ferences ASTM International West Conshohocken PA 2011httpswwwastmorgStandardsE2745htm

38 ASTM E2746-11 Standard Specification for Evaluation andSelection of Communication and Marketing Materials for En-vironmentally Sustainable Meetings Events Trade Shows andConferences ASTM International West Conshohocken PA 2011httpswwwastmorgStandardsE2746htm

39 ASTM E2741-11 Standard Specification for Evaluation and Se-lection of Destinations for Environmentally Sustainable MeetingsEvents Trade Shows and Conferences ASTM InternationalWest Conshohocken PA 2011 httpswwwastmorgStan-dardsE2741htm

40 0 ASTM E2773-11 Standard Specification for Evaluation andSelection of Food and Beverage for Environmentally SustainableMeetings Events Trade Shows and Conferences ASTM Interna-tional West Conshohocken PA 2011 httpswwwastmorgStan-dardsE2773htm

41 ASTM E2742-11 Standard Specification for Evaluation and Selec-tion of Exhibits for Environmentally Sustainable Meetings EventsTrade Shows and Conferences ASTM International West Con-shohocken PA 2011 httpswwwastmorgStandardsE2742htm

42 ASTM E2774-11 Standard Specification for Evaluation and Selec-tion of Venues for Environmentally Sustainable Meetings EventsTrade Shows and Conferences ASTM International West Con-shohocken PA 2011 httpswwwastmorgStandardsE2774htm

43 ASTM F2902-12 Standard Guide for Assessment of AbsorbablePolymeric Implants ASTM International West ConshohockenPA 2012 httpswwwastmorgStandardsF2902htm

44 httpsenwikipediaorgwikiResorption45 Venes D Tabers Cyclopedic Medical Dictionary 22th edition

Philadelphia F A Davis Company 201346 Zheng YF Gu XN Witte F Biodegradable metals Mater Sci Eng-

R-Rep 2014 77 1ndash3447 Hanawa T Metal ion release from metal implants Mater Sci

Eng-C 2004 24 745ndash75248 Zreiqat H Howlett CR Zannettino A et al Mechanisms of mag-

nesium-stimulated adhesion of osteoblastic cells to commonly usedorthopaedic implants J Biomed Mater Res 2002 62 175ndash184

49 Little PJ Bhattacharya R Moreyra AE et al Zinc and cardiovascu-lar disease Nutrition 2010 26 1050ndash1057

50 Seager H Drug-delivery products and the Zydis fast-dissolvingdosage form J Pharm Pharmacol 1998 50 375ndash382

51 Shikinami Y Shape-memory biodegradable and absorbable mate-rial US Patent No 6281262 2001-8-28

52 Huitema TW Knight GW Ransick MH Schulze DR Surgical im-plant with preferential corrosion zone US Patent No 79059022011-3-15

53 Luzier WD Materials derived from biomassbiodegradable mate-rials Proc Natl Acad Sci USA 1992 89 839ndash842

54 Gross RA Kalra B Biodegradable polymers for the environmentScience 2002 297 803ndash807

55 Trumbo P Schlicker S Yates AA et al Dietary reference intakesfor energy carbohydrate fiber fat fatty acids cholesterol proteinand amino acids J Am Diet Assoc 2002 102 1621ndash1630

56 Chambin O Champion D Debray C et al Effects of different cel-lulose derivatives on drug release mechanism studied at a prefor-mulation stage J Control Release 2004 95 101ndash108

12copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

57 Fundueanu G Constantin M Esposito E et al Cellulose acetatebutyrate microcapsules containing dextran ion-exchange resinsas self-propelled drug release system Biomaterials 2005 264337ndash4347

58 Maumlrtson M Viljanto J Hurme T et al Is cellulose sponge degrad-able or stable as implantation material An in vivo subcutaneousstudy in the rat Biomaterials 1999 20 1989ndash1995

59 Patel N Padera R Sanders GH et al Spatially controlled cell en-gineering on biodegradable polymer surfaces The FASEB journal1998 12 1447ndash1454

60 Goldstein A Effect of convection on osteoblastic cell growth andfunction in biodegradable polymer foam scaffolds Biomaterials2001 22 1279ndash1288

61 Wu L Ding J In vitro degradation of three-dimensional porouspoly(DL-lactide-co-glycolide) scaffolds for tissue engineeringBiomaterials 2004 25 5821ndash5830

62 Wu L Ding J Effects of porosity and pore size on in vitro degra-dation of three-dimensional porous poly(DL-lactide-co-glycolide)scaffolds for tissue engineering J Biomed Mater Res 2005 75A767ndash777

63 Pan Z Ding J Poly(lactide-co-glycolide) porous scaffolds for tissueengineering and regenerative medicine Interface Focus 2012 2366ndash377

64 Yu L Zhang Z Zhang H et al Biodegradability and biocompati-bility of thermoreversible hydrogels formed from mixing a sol anda precipitate of block copolymers in water Biomacromolecules2010 11 2169ndash2178

65 Wen X Tresco PA Fabrication and characterization of permeabledegradable poly(DL-lactide-co-glycolide) (PLGA) hollow fiberphase inversion membranes for use as nerve tract guidance chan-nels Biomaterials 2006 27 3800ndash3809

66 Chu CFL Lu A Liszkowski M et al Enhanced growth of animaland human endothelial cells on biodegradable polymers BBA-GenSubjects 1999 1472 479ndash485

67 Jo S Engel PS Mikos AG Synthesis of poly(ethylene glycol)-teth-ered poly(propylene fumarate) and its modification with GRGDpeptide Polymer 2000 41 7595ndash7604

68 Park JH Allen MG Prausnitz MR Biodegradable polymer mi-croneedles fabrication mechanics and transdermal drug deliveryJ Control Release 2005 104 51ndash66

69 Freed LE Vunjak-Novakovic G Biron RJ et al Biodegradablepolymer scaffolds for tissue engineering Nat Biotechnol 1994 12689ndash693

70 Windecker S Serruys PW Wandel S et al Biolimus-eluting stentwith biodegradable polymer versus sirolimus-eluting stent withdurable polymer for coronary revascularisation (LEADERS) arandomised non-inferiority trial Lancet 2008 372 1163ndash1173

71 Stefanini GG Kalesan B Serruys PW et al Long-term clinicaloutcomes of biodegradable polymer biolimus-eluting stents ver-sus durable polymer sirolimus-eluting stents in patients with coro-nary artery disease (LEADERS) 4 year follow-up of a randomisednon-inferiority trial Lancet 2011 378 1940ndash1948

72 Raungaard B Jensen LO Tilsted HH et al Zotarolimus-elutingdurable-polymer-coated stent versus a biolimus-eluting biodegrad-able-polymer-coated stent in unselected patients undergoing per-cutaneous coronary intervention (SORT OUT VI) a randomisednon-inferiority trial Lancet 2015 385 1527ndash1535

73 Freed LE Grande DA Lingbin Z et al Joint resurfacing using allo-graft chondrocytes and synthetic biodegradable polymer scaffoldsJ Biomed Mater Res 1994 28 891ndash899

74 Poirier Y Nawrath C Somerville C Production of polyhydrox-yalkanoates a family of biodegradable plastics and elastomers in

bacteria and plants Nat Biotechnol 1995 13 142ndash15075 Dias A Tsuru K Hayakawa S et al Crystallisation studies of

biodegradable CaO-P2O5 glass with MgO and TiO2 for boneregeneration applications Glass Technol 2004 45 78ndash79

76 Klein CPAT de Groot K Drissen AA et al Interaction ofbiodegradable β-whitlockite ceramics with bone tissue an in vivostudy Biomaterials 1985 6 189ndash192

77 Ikenaga M Hardouin P Lemaicirctre J et al Biomechanical charac-terization of a biodegradable calcium phosphate hydraulic cementa comparison with porous biphasic calcium phosphate ceramics JBiomed Mater Res 1998 40 139ndash144

78 Dias AG Lopes MA Santos JD et al In vivo performance ofbiodegradable calcium phosphate glass ceramics using the rabbitmodel histological and SEM observation J Biomater Appl 200620 253ndash266

79 Lee JH Lee CK Chang BS et al In vivo study of novel biodegrad-able and osteoconductive CaO-SiO2-B2O3 glass-ceramics JBiomed Mater Res 2006 77A 362ndash369

80 Song G Song S A possible biodegradable magnesium implant ma-terial Adv Eng Mater 2007 9 298ndash302

81 Kim WC Kim JG Lee JY et al Influence of Ca on the corrosionproperties of magnesium for biomaterials Mater Lett 2008 624146ndash4148

82 Li Z Gu X Lou S et al The development of binary Mg-Ca alloysfor use as biodegradablematerials within bone Biomaterials 200829 1329ndash1344

83 Wan Y Xiong G Luo H et al Preparation and characterization ofa new biomedical magnesium-calcium alloy Mater Des 2008 292034ndash2037

84 Seong JW Kim WJ Development of biodegradable Mg-Ca alloysheets with enhanced strength and corrosion properties throughthe refinement anduniformdispersion of theMg2Caphase by high-ratio differential speed rolling Acta Biomater 2015 11 531ndash542

85 Zhang S Li J Song Y et al In vitro degradation hemolysis andMC3T3-E1 cell adhesion of biodegradable Mg-Zn alloy Mater SciEng-C 2009 29 1907ndash1912

86 Li J Song Y Zhang S et al In vitro responses of human bone mar-row stromal cells to a fluoridated hydroxyapatite coated biodegrad-able Mg-Zn alloy Biomaterials 2010 31 5782ndash5788

87 Brar HS Wong J Manuel MV Investigation of the mechanical anddegradation properties of Mg-Sr and Mg-Zn-Sr alloys for use aspotential biodegradable implant materials J Mech Behav BiomedMater 2012 7 87ndash95

88 Bornapour M Muja N Shum-Tim D et al Biocompatibility andbiodegradability of Mg-Sr alloys the formation of Sr-substitutedhydroxyapatite Acta Biomater 2013 9 5319ndash5330

89 Gu XN Xie XH Li N et al In vitro and in vivo studies on aMg-Sr binary alloy system developed as a new kind of biodegrad-able metal Acta Biomater 2012 8 2360ndash2374

90 Haumlnzi AC Gerber I Schinhammer M et al On the in vitro andin vivo degradation performance and biological response of newbiodegradableMg-Y-Zn alloys Acta Biomater 2010 6 1824ndash1833

91 Chou DT Hong D Saha P et al In vitro and in vivo corrosioncytocompatibility and mechanical properties of biodegradableMg-Y-Ca-Zr alloys as implant materials Acta Biomater 2013 98518ndash8533

92 Zong Y Yuan G Zhang X et al Comparison of biodegradable be-haviors of AZ31 and Mg-Nd-Zn-Zr alloys in Hanks physiologicalsolution Mater Sci Eng-B 2012 177 395ndash401

93 Tie D Feyerabend FMuumlllerWD et al Antibacterial biodegradableMg-Ag alloys Eur Cell Mater 2013 25 284ndash298

94 VojtěchDKubaacutesek J Seraacutek J et al Mechanical and corrosion prop-

13 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

erties of newly developed biodegradable Zn-based alloys for bonefixation Acta Biomater 2011 7 3515ndash3522

95 Li H Yang H Zheng Y et al Design and characterizations of novelbiodegradable ternary Zn-based alloys with IIA nutrient alloyingelements Mg Ca and Sr Mater Des 2015 83 95ndash102

96 Liu X Sun J Yang Y et al Microstructure mechanical proper-ties in vitro degradation behavior and hemocompatibility of novelZn-Mg-Sr alloys as biodegradable metals Mater Lett 2016 162242ndash245

97 Wu C Qiu H Hu X et al Short-term safety and efficacy of thebiodegradable iron stent in mini-swine coronary arteries ChinMed J (Engl) 2013 126 4752ndash4757

98 Purnama A Hermawan H Champetier S et al Gene expressionprofile of mouse fibroblasts exposed to a biodegradable iron alloyfor stents Acta Biomater 2013 9 8746ndash8753

99 HermawanH Purnama A Dube D et al Fe-Mn alloys for metallicbiodegradable stents degradation and cell viability studies ActaBiomater 2010 6 1852ndash1860

100 Sheridan MH Shea LD Peters MC et al Bioabsorbable polymerscaffolds for tissue engineering capable of sustained growth factordelivery J Control Release 2000 64 91ndash102

101 Shawe S Buchanan F Harkin-Jones E et al A study on the rate ofdegradation of the bioabsorbable polymer polyglycolic acid (PGA)J Mater Sci 2006 41 4832ndash4838

102 Palmerini T Biondi-Zoccai G Della Riva D et al Clinical out-comes with bioabsorbable polymer- versus durable polymer-baseddrug-eluting and bare-metal stents J Am Coll Cardiol 2014 63299ndash307

103 Tanimoto S Serruys PW Thuesen L et al Comparison of in vivoacute stent recoil between the bioabsorbable everolimus-elutingcoronary stent and the everolimus-eluting cobalt chromium coro-nary stent insights from the ABSORB and SPIRIT trials CatheterCardiovasc Interv 2007 70 515ndash523

104 Tsuji H Sasaki H Sato H et al Neuron attachment properties ofcarbon negative-ion implanted bioabsorbable polymer of poly-lac-tic acid Nucl Instr Meth Phys Res Sect B-Beam Interact MaterAtoms 2002 191 815ndash819

105 Aikawa M Miyazawa M Okamoto K et al A novel treatment forbile duct injury with a tissue-engineered bioabsorbable polymerpatch Surgery 2010 147 575ndash580

106 WaksmanR Pakala R Kuchulakanti PK et al Safety and efficacy ofbioabsorbablemagnesium alloy stents in porcine coronary arteriesCatheter Cardiovasc Interv 2006 68 607ndash617

107 Di Mario C Griffiths H Goktekin O et al Drug-eluting bioab-sorbable magnesium stent J Interv Cardiol 2004 17 391ndash395

108 Erbel R Di Mario C Bartunek J et al Temporary scaffoldingof coronary arteries with bioabsorbable magnesium stents aprospective non-randomised multicentre trial Lancet 2007 3691869ndash1875

109 Schranz D Zartner P Michel-Behnke I et al Bioabsorbable metalstents for percutaneous treatment of critical recoarctation of theaorta in a newborn Catheter Cardiovasc Interv 2006 67 671ndash673

110 Gu X Zheng Y Cheng Y et al In vitro corrosion and biocompati-bility of binary magnesium alloys Biomaterials 2009 30 484ndash498

111 Hiromoto S InoueM Taguchi T et al In vitro and in vivo biocom-patibility and corrosion behaviour of a bioabsorbable magnesiumalloy coated with octacalcium phosphate and hydroxyapatite ActaBiomater 2015 11 520ndash530

112 Hiromoto S Tomozawa M Maruyama N Fatigue property of abioabsorbable magnesium alloy with a hydroxyapatite coatingformed by a chemical solution deposition J Mech Behav Biomed-ical Mater 2013 25 1ndash10

113 Bowen PK Drelich J Goldman J Zinc exhibits ideal physiologicalcorrosion behavior for bioabsorbable stents Adv Mater 2013 252577ndash2582

114 Liu X Sun J Yang Y et al In vitro investigation of ultra-pure Znand its mini-tube as potential bioabsorbable stent material MaterLett 2015 161 53ndash56

115 LinW Zhang G Cao P et al Cytotoxicity and its test methodologyfor a bioabsorbable nitrided iron stent J Biomed Mater Res 2015103 764ndash776

116 Coe JD Vaccaro AR Instrumented transforaminal lumbar inter-body fusion with bioresorbable polymer implants and iliac crestautograft Spine 2005 30 S76ndashS83

117 Ignatius AA Augat P Ohnmacht M et al A new bioresorbablepolymer for screw augmentation in the osteosynthesis of osteo-porotic cancellous bone a biomechanical evaluation J BiomedMater Res 2001 58 254ndash260

118 Krucoff MW Kereiakes DJ Petersen JL et al A novel biore-sorbable polymer paclitaxel-eluting stent for the treatment ofsingle and multivessel coronary disease J Am Coll Cardiol 200851 1543ndash1552

119 Kostopoulos L Karring T Guided bone regeneration in mandibu-lar defects in rats using a bioresorbable polymer Clin Oral Im-plants Res 1994 5 66ndash74

120 Dubok VA Bioceramicsmdashyesterday today tomorrow PowderMetall Metal Ceram 2000 39 381ndash394

121 Safronova T Kuznetsov A Korneychuk S et al Calcium phos-phate powders synthesized from solutions with [Ca2+][PO4

3minus]=1for bioresorbable ceramics Cent Eur J Chem 2009 7 184ndash191

122 Bohner M Bioresorbable ceramics In Buchanan FJ (Ed) Degra-dation Rate of Bioresorbable Materials Cambridge WoodheadPublishing 2008 95-114

123 Seitz JM Eifler R Stahl J et al Characterization ofMgNd2 alloy forpotential applications in bioresorbable implantable devices ActaBiomater 2012 8 3852ndash3864

124 WenCE Yamada Y Shimojima K et al Porous bioresorbable mag-nesium as bone substitute MSF 2003 419ndash422 1001ndash1006

125 Campos CM Muramatsu T Iqbal J et al Bioresorbable drug-elut-ing magnesium-alloy scaffold for treatment of coronary artery dis-ease Int J Mol Sci 2013 14 24492ndash24500

126 KirklandNT Birbilis NWalker J et al In-vitro dissolution ofmag-nesium-calcium binary alloys clarifying the unique role of calciumadditions in bioresorbable magnesium implant alloys J BiomedMater Res 2010 95B 91ndash100

127 Gastaldi D Sassi V Petrini L et al Continuum damage model forbioresorbable magnesium alloy devices mdashapplication to coronarystents J Mech Behav Biomed Mater 2011 4 352ndash365

128 Kitabata H Waksman R Warnack B Bioresorbable metal scaffoldfor cardiovascular application current knowledge and future per-spectives Cardiovasc Revasc Med 2014 15 109ndash116

Acknowledgments This work was supported by the National Key Re-search and Development Program of China (2016YFC1102402) NationalNatural Science Foundation of China (NSFC 51431002) and the NSFCand the Research Grants Council (RGC) of Hong Kong Joint ResearchScheme (51361165101 and 5161101031)

Author contributions Liu Y prepared the figures tables organized thereferences and wrote the paper Zheng Y provided the overall concept andrevised the manuscript Hayes B helped with the standard developmentand revised the manuscript All authors participated in the discussion

Conflict of interest The authors declare that they have no conflict ofinterest

14copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Yang Liu received his bachelor degree in materials science and engineering from Harbin engineering University in 2013Then he continued his study as a PhD candidate in Prof Yufeng Zhengrsquos Lab in Peking University His research interestsare mainly focused on the corrosion study of absorbable metallic biomaterials as well as the development of new kind ofMg-based biomaterials

Yufeng Zheng obtained his PhD degree from Harbin Institute of Technology in 1998 He is the National OutstandingYouth and Yangtze River scholar of China His research interests are focused on the development of novel biomaterials andapplication and design of biomedical devices

Byron Hayes an over 35 year employee of WL Gore has been involved in the commercial development of multiple ab-sorbable polymeric implants since the late 1980s Hayes started his standards development activities with ASTM in 2000where he is actively developing standards for polymeric and metallic absorbable implants In 2010 Hayes also becameinvolved with ISO Technical Committees TC150 and TC194 and is now convener of working groups focused on cardiovas-cular and metallic absorbable implants

可降解可吸收再吸收mdashmdash哪个是描述最终被人体吸收生物材料的最好词汇刘洋1 郑玉峰1 拜伦海耶斯2

摘要 关于最终被人体吸收的植入材料领域内文献采用的英文修饰词长期以来混乱且不同不仅造成文献检索困难同时模糊了研究人员的研究边界 此领域在法律法规标准中统一用词的确定为领域内的科学研究产品销售及产品使用说明奠定了基础 我们基于化学生态学材料学生物学微生物学和药学立足于使用习惯法律标准和市场对领域内使用已久的典型修饰词ldquo生物可降解rdquoldquo再吸收rdquo和ldquo可吸收rdquo进行了讨论和解释 总的来说尽管目前绝大多数修饰语实际想表达的意思相同作者认为ldquo可吸收rdquo这一英文修饰语是最恰当的修饰词 同时我们提议进一步规范和统一该领域修饰词的使用

15 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

  • Degradable absorbable or resorbablemdashwhat is the best grammatical modifier for an implant that is eventually absorbed by the body
  • Abstract
  • INTRODUCTION
    • Current situation
    • Standards development in advance
      • TERMINOLOGY
        • Overview of utilization of the terms ldquodegradationrdquoldquobiodegradationrdquo and ldquodegradablerdquoldquobiodegradablerdquo
        • Overview of utilization of the terms ldquoabsorptionrdquoldquobioabsorptionrdquo and ldquoabsorbablerdquoldquobioabsorbablerdquo
        • Overview of utilization of the terms ldquoresorptionrdquoldquobioresorptionrdquo and ldquoresorbablerdquoldquobioresorbablerdquo
        • Utilization and comparison of the terms ldquobiodegradable metalsrdquo and ldquoabsorbable metallic materialsrdquo
        • Summary quantification of the common Terms
          • DISCUSSION
            • Expertise inherent biases
            • Connotation and extension of noun forms ldquobiodegradation bioabsorption and bioresorptionrdquo and adjectives ldquobiodegradable bioabsorbable and bioresorbablerdquo
              • CONCLUDING REMARKS
              • References
              • Acknowledgements

materscichinacom linkspringercom Published online 26 April 2017 | doi 101007s40843-017-9023-9Sci China Mater () 1ndash

Degradable absorbable or resorbablemdashwhat is thebest grammatical modifier for an implant that iseventually absorbed by the bodyYang Liu1 Yufeng Zheng1 and Byron Hayes2

ABSTRACT The adoption of grammatical modifier for im-plants or other kinds of biomaterials eventually absorbed bythe body has been a long-standing confusing issue and thereare diverse terms in the large fields of research which notonly causes the difficulties when searching on the Internetbut also blurs the meaning and boundaries for researchersPrior unification attempts at lawsstandards set the basis forsuch research fields towards researching labeling marketingand instructions for use Considering this the typical gram-matical modifiers ldquobiodegradablerdquo ldquoresorbablerdquo ldquoabsorbablerdquoalong with their noun forms used in the decades of scien-tific research have been reviewed and explained interdiscipli-nary in chemistry ecology materials science biology micro-biology medicine and based on usage customs laws stan-dards and markets The term ldquobiodegradablerdquo has been notonly used in biomaterials but also in ecology waste manage-ment biomedicine and even natural environment Mean-while the term ldquoresorbablerdquo has long been used in biologicalreaction (osteoclast driven bone resorption) but is inappro-priate for implants that do not carry the potential to growback into their original form The term ldquoabsorbablerdquo focusesmore on the host metabolism to the foreign biodegradationproducts of the implanted materialdevice compared with theterm ldquodegradablebiodegradablerdquo Meanwhile the coherenceand normalization of the term ldquoabsorbablerdquo carried by its ownin laws and standards contributes as well In general the au-thors consider the term ldquoabsorbablerdquo to be the best grammat-ical modifier with respect to other adjectives which share thesame inherence A further internationally unified usage isproposed by us

Keywords biodegradation bioabsorption bioresorptionbiodegradable absorbable biomaterials

INTRODUCTION

Current situationTechnologies labeled as absorbable bioabsorbable re-sorbable bioresorbable degradable biodegradable or bysome other similar terms all of which carry the inher-ent underlying potential to allow treated tissue to returnto its native state have been developed for a long timeMore specifically it likely started with the use of sheepgut guitar strings (made of natural collagens recognizedas absorbable polymer today) to approximate woundsover 2000 years ago in the Roman Empire [1] As timeand technology progressed the catgut suture technologybecame significantly refined and synthetic polymers werealso developed both of which led to the absorbable su-tures we find in broad use today Resorbable bioceramictechnologies also entered into use as bone fillers [23] Inaddition the newly evolving biodegradable metals (suchas Mg Fe and Zn and their alloys) are now making theirway into the commercial marketplace [45] All thesedevices carry the promise of fulfilling their intended initialphysicalmechanical function and then undergoing com-positional conversion into components that are eventuallyabsorbed by the bodyMeanwhile numerous terms have been used to describe

the same general concept with the diversity of terms pro-viding self-evidence of either the absence or non-adherenceto standard terminology Compounding this nomenclaturedilemma literature in the field of absorbablebiodegrad-ableresorbable implant materials has been increasing ex-ponentially since the mid-1980s when the synthetic alpha-

1 Department of Materials Science and Engineering College of Engineering Peking University Beijing 100871 China2 Biomaterials Research and Development Medical Product Division WL Gore amp Associates Inc Flagstaff Arizona 86003 USA Corresponding author (email yfzhengpkueducn)

1 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

hydroxyester polymeric resins first became broadly avail-able from commercial suppliers To attain a preliminaryunderstanding of the scope of the confusion surroundinglabeling of these implants all any person has to do is to ini-tiate an Internet search whichmdashin order to confidently ad-dress a single simple conceptmdashbegins as a convoluted as-terisk-filled multi-line querySuch problem not only causes the difficulties when

searching on the Internet but also blurs the meaning andboundaries for researchers The absence of any universalterm recognition unnecessarily complicates communica-tion and confounds the selection of language for researchpapers legal descriptions international trade agreementsas well as the language used in an implantrsquos labelingmarketing and instructions for use Regardless of itsobviousness the problem has been a present and fullyrecognized problem that has persisted for decades Someintermittent attempts have been made by researchers tounify this disparate language into a single preferred term[67] As a result multiple purportedly ldquodefinitiverdquo papershave been published through the years However manyof these papers reflect the perspective of a single authoror society which often leads to conflicts between nomen-clature preferences [8ndash13] for even a single professionalsocietyrsquos breadth of view can be similarly limited by its ownscope Materials that are absorbed by the body do spanmany medical disciplines and the breadth of the technol-ogyrsquos applicability may contribute toward inhibiting anyone professional society from attempting a nomenclatureresolutionmdashas can be evidenced at numerous conferenceswhere one can observe an internal array of presentationsand posters with titles and terminology spanning most (ifnot all) the terms described in the 1st sentence

Standards development in advanceTypically absent from most of these historical nomencla-ture recommendations was any comprehensive consid-eration of the truly broader medical context containedwithin medical dictionaries and the relevant pharma-copeial andor implantable device-related standards [14]Early device and pharmaceutical companies regulatorsand any of the involved standards development organi-zations all had to consciously think about and decide onthe specific terms to include on their labels and in anygoverning standard regulation andor law With implantsthat are eventually absorbed by the body the selection andstandardization of terminology by the United States Phar-macopeia had already occurred and had fully focused onthe term ABSORBABLE by 1939 through its official des-

ignations of both ABSORBABLE and NONABSORBABLEsutures [1516] This same standardized language and clas-sifications remain in place today and have been for decadesembedded in both United States Federal laws and US-Foodand Drug Administration (FDA) regulations [17ndash19] (tobe discussed in later section) as well as in theUnited StatesBritish and European Pharmacopeias [20ndash22] Trying tochange or reverse what has already been both functionaland established in both regulations and law (now fordecades) is both difficult and a questionable undertakingRegardless of this historic and significant establishment ofABSORBABLE as standardized terminology it is possiblethat a simple lack of awareness andor rigorous review bythose involved in the broader research and clinical fieldsmay have become the source for the plethora of similar andanalogously utilized terms we routinely encounter todayThe advances in standard unification of the grammatical

modifier provide insights to the term usage in the researchof such field Due to the fact that many grammatical mod-ifiers have been used in this field for a long time typicalterms have been reviewed and explained interdisciplinaryin chemistry ecology materials science biology microbi-ology medicine and based on usage habits laws standardsand markets Furthermore the international unification ofthe grammatical term usage is proposed

TERMINOLOGYAs stated in the opening sentence multiple terms are be-ing utilized to describe the same general absorbable im-plant concept which includes absorbable bioabsorbableresorbable bioresorbable degradable biodegradable andpotentially other similar themes To provide an improvedunderstanding of the scope of current language diversityan overview of the usage of the aforementioned words wasundertaken to provide data that assisted in both confirmingand clarifying the scope of the problem The results are in-tended to provide a summary understanding of the scopeof confusion (ie how big the problem really is) so as tobetter facilitate identification of an appropriate remedy

Overview of utilization of the terms ldquodegrada-tionrdquoldquobiodegradationrdquo and ldquodegradablerdquoldquobiodegradablerdquoldquoDegradationrdquo and ldquobiodegradationrdquo are both used inpolymers and ceramics for a period of time and had beennoted by Prof D Williams as ldquothe process as deleteriouschange in the chemical structure physical propertiesor appearance of a materialrdquo according to the AmericanSociety for Testing and Materials (ASTM) [23] In theresearch of ldquobiorelatedrdquo polymers International Union

2copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

of Pure and Applied Chemistry (IUPAC) suggested thatldquodegradation indicates progressive loss of the performanceor of the characteristics of a substance or a devicerdquo [14] Itis also a general process since there can be degradationscaused by the action of water named ldquohydrodegradationrdquoor hydrolysis As for biorelated polymers the degradationprocess is limited to macromolecule cleavage and molarmass decrease which distinguishes the degradation ofbiorelated polymer from fragmentation and disintegrationillustrated in bioceramics The term ldquodegradationrdquo wasformerly used in bioceramics by Prof L Hench to describethe decomposition process of calcium phosphate ceramicswhich was followed by host response and tissue repair [3]Thus the definition of ldquodegradationrdquo used in polymers andceramics fields could be interpreted as different inferringmore specifically to chemical processes for bio-relatedpolymers while referring to physical break down from theview of bio-ceramics researchersAs for the term ldquobiodegradationrdquo it is not the simple

addition of the prefix ldquobio-rdquo to ldquodegradationrdquo Fig 1 de-scribes the common usage of ldquobiodegradationrdquo currentlyThe word was firstly introduced as the consumption ofmaterial by bacteria fungi or other biological means inecology waste management biomedicine and even naturalenvironment [24] Some kinds of environmentally friendlyproducts also undergo such process as they can be degraded

by microorganisms and do no harm to the environmentHowever some researchers studying polymers and ceram-ics have defined a more specific scope for ldquobiodegradationrdquoFor polymers especially biorelated polymers the differ-ence between ldquobiodegradationrdquo and ldquodegradationrdquo lies inthe involvement of enzymatic process [1425]mdasha distinc-tion that can be problematic if both modes are active in animplantrsquos degradation process Moreover IUPAC stressedthe importance of proved degradation mechanisms whenusing ldquobiodegradationrdquo otherwise ldquodegradationrdquo should beused instead of ldquobiodegradationrdquo In general ldquodegradationrdquoand ldquobiodegradationrdquo both refer to the chain scission orchain cleavage Nevertheless the meaning of ldquobiodegra-dationrdquo in bioceramics is different since there is no suchprocess as chain scission The degradation process ofso-called ldquoresorbable ceramicsrdquo is claimed to involve eitherdecomposition to small particles as well as dissolved ionswhich participate in the enzymecell mediated reactionand new tissue forms [326ndash28] Despite the exact degra-dation process still needs further investigations the wordldquodegradationrdquo used for ldquoresorbablerdquo ceramics expressesmultiple meanings covering both chemical and physicalreactions in physiological environment such as hydrolysisdecomposition and debris formation According to ProfD Williams the recommended definition of ldquobiodegrada-tionrdquo is the gradual breakdown of a material mediated by

Figure 1 Common use of biodegradation currently

3 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

specific biological activity [23] Another definition as thebiomaterial or medical device involving loss of their in-tegrity or performance when exposed to a physiological orsimulated environment which existed in some ISO Techni-cal Report was not recommended since no specific respectto biological activity mentioned [23]Beyond the category of biomaterials ldquodegradablerdquo in

pure chemistry was defined as qualifier to a substance thatcan undergo physical andor chemical deleterious changesof some properties especially of integrity under stressconditions [14] Thus degradable polymer is consideredwith macromolecules being able to undergo chain scis-sions resulting in a decrease of molar mass [14] BesidesASTM made a standard definition on ldquodegradablerdquo in thescope of soil rock and contained fluids as ldquoin erosioncontrol decomposes under biological chemical processesor ultraviolet stresses associated with typical applicationenvironmentsrdquo [29] Despite no specific emphasis onbiomaterials numerous publications used ldquodegradablerdquo to

modify metals polymers or compounds in tissue engineer-ing drug delivery and gene delivery [30ndash35] Meanwhilein some ASTM standard specifications the definition ofthe adjective ldquobiodegradablerdquo is given as capable of de-composing under natural conditions into elements foundin the nature [36ndash42] The active ASTM entries currentlywith ldquobiodegradationrdquo ldquodegradablerdquo and ldquobiodegradablerdquoin the title are summarized in Table 1 The adoptionsof ldquobiodegradationrdquo ldquodegradablerdquo and ldquobiodegradablerdquoby ASTM are historical generally in the classification ofecology or environmental protectionWhile the above listing provides evidence that the usage

of the term biodegradable is broad it is particularly notablethat almost all of the listed standards are not relevant toimplantable devices Instead the listing primarily reflectsusage directed toward the environmental degradation as-pect that is most commonly recognized within the broadernon-medical oriented population ASTM-F1635 a stan-dard specifically centered on the hydrolytic degradation

Table 1 Summary of the terms ldquobiodegradationrdquo ldquodegradablerdquo and ldquobiodegradablerdquo being utilized in ASTM titles (not limited to implant)

Terminology ASTM titles

ASTM D5864-11 Standard Test Method for Determining Aerobic Aquatic Biodegradation of Lubricants or TheirComponents

ASTM D6954-04(2013) Standard Guide for Exposing and Testing Plastics that Degrade in the Environment by aCombination of Oxidation and Biodegradation

ASTM D5511-12 Standard Test Method for Determining Anaerobic Biodegradation of Plastic Materials Under High-SolidsAnaerobic-Digestion Conditions

ASTM D6139-11 Standard Test Method for Determining the Aerobic Aquatic Biodegradation of Lubricants or TheirComponents Using the Gledhill Shake Flask

ASTM D7991-15 Standard Test Method for Determining Aerobic Biodegradation of Plastics Buried in Sandy MarineSediment under Controlled Laboratory Conditions

ASTM D5338-15 Standard Test Method for Determining Aerobic Biodegradation of Plastic Materials Under ControlledComposting Conditions Incorporating Thermophilic Temperatures

ASTM D6691-09 Standard Test Method for Determining Aerobic Biodegradation of Plastic Materials in the MarineEnvironment by a Defined Microbial Consortium or Natural Sea Water Inoculum

ASTM D5526-12 Standard Test Method for Determining Anaerobic Biodegradation of Plastic Materials Under AcceleratedLandfill Conditions

ASTM D7475-11 Standard Test Method for Determining the Aerobic Degradation and Anaerobic Biodegradation of PlasticMaterials under Accelerated Bioreactor Landfill Conditions

Biodegradation

ASTM D5988-12 Standard Test Method for Determining Aerobic Biodegradation of Plastic Materials in Soil

ASTM F1635-11 Standard Test Method for in vitro Degradation Testing of Hydrolytically Degradable Polymer Resinsand Fabricated Forms for Surgical Implants

ASTM D7444-11 Standard Practice for Heat and Humidity Aging of Oxidatively Degradable PlasticsDegradable

ASTM D3826-98(2013) Standard Practice for Determining Degradation End Point in Degradable Polyethylene andPolypropylene Using a Tensile Test

ASTM D7665-10(2014) Standard Guide for Evaluation of Biodegradable Heat Transfer Fluids

ASTM D8029-16 Standard Specification for Biodegradable Low Aquatic Toxicity Hydraulic FluidsBiodegradable

ASTM D7044-15 Standard Specification for Biodegradable Fire Resistant Hydraulic Fluids

4copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

testing of absorbable polyesters is the sole listed standardfrom ASTM Committee F04mdashMedical and Surgical Im-plants and thereby is directly relevant to implantable de-vices However this standard utilizes the term degradeand its derivatives specifically in reference to the process ofdegradation that occurs as a result of ester hydrolysis Con-versely the same standard uses the term absorbable to de-scribe a class of implants that are eventually absorbed by thebody which it defines as ldquoabsorbable adjmdashin the bodymdashaninitially distinct foreign material or substance that either di-rectly or through intended degradation can pass through orbe assimilated by cells andor tissuerdquo

Overview of utilization of the terms ldquoabsorptionrdquoldquobioab-sorptionrdquo and ldquoabsorbablerdquoldquobioabsorbablerdquoThe term ldquoabsorptionrdquo was recognized by IUPAC as theprocess of penetration and diffusion of a substance (ab-sorbate) into another substance (absorbent) as a result ofthe action of attractive phenomena The IUPAC defini-tion is within the scope of chemistry As for biomaterialsProf D Williams adopted the definition in Dorland Medi-cal Dictionary as the uptake of substances into or across tis-sues [23] For this kind of definition ldquoabsorptionrdquo empha-sizes the interaction of materials and human or animal tis-sue The same connotation is shared by its derivative wordsldquoabsorbablerdquo and ldquobioabsorbablerdquo as capable of being de-graded or dissolved and subsequently metabolized withinan organism [23] Besides the prefix ldquobio-rdquo is abridged as

it is redundant in the field of implantation [43] ASTM hasmade standard definition on ldquoabsorbablerdquo in the field of ab-sorbable polymers as well as absorbablemetals which it de-fines as ldquohellip an initially distinct foreign material or substancethat either directly or through intended degradation can passthrough or be metabolized or assimilated by cells andor tis-sue in the bodyrdquo [43] Table 2 summarizes the currently ac-tive ASTM standards and both United States and EuropeanPharmacopeia implantable device monographs that utilizethe word ldquoabsorbablerdquo in the title Distinctly different fromldquobiodegradablerdquo the utilization of ldquoabsorbablerdquo displays adistinct preference for use in describing this particular classof biomedical materials and devicesAs can be observed in both Table 1 and Table 3 the

well-established terminology for describing sutures is verybroadly based on the term absorbable with historicalapplication of the term to the original gut sutures andeven extending to permanent sutures through the ldquononab-sorbablerdquo descriptorAside from the language of standards organization the

terminology utilized by regulatory agencies is also of par-ticular relevance Through multiple laws and regulationsthe US-FDA is authorized to evaluate medical device man-ufacturers and their products The US Code of FederalRegulations (CFRs) that is specific to sutures legally de-scribes those regulated devices based on composition andthen designates both their product class and needs to meetUSP requirements While Table 3 demonstrates both a US-

Table 2 ldquoAbsorbablerdquo utilized in title entries for implantable device related standards

Terminology Title entries

ISOTS 171372014 Cardiovascular implants and extracorporeal systemsmdashCardiovascular absorbable implants

ISOTR 371372014 Biological evaluation of medical devicesmdashGuidance for absorbable implants

ASTM F3036-13 Standard Guide for Testing Absorbable Stents

ASTM F2902-16 Standard Guide for Assessment of Absorbable Polymeric Implants

ASTM F2502-16 Standard Specification and Test Methods for Absorbable Plates and Screws for Internal Fixation Implants

ASTM F1983-14 Standard Practice for Assessment of Selected Tissue Effects of Absorbable Biomaterials for Implant Applications

ASTM F3160-16 Standard Guide for Metallurgical Characterization of Absorbable Metallic Materials for Medical Implants

United States Pharmacopoeia (USP 39NF 34) monographldquoAbsorbable Surgical Suturerdquo

United States Pharmacopoeia (USP 39NF 34) monographldquoNonabsorbable Surgical Suturerdquo

European Pharmacopoeia (88)ldquoSterile non-absorbable suturesrdquo ndash 1118

European Pharmacopoeia (88)ldquoSterile synthetic absorbable braided suturesrdquo - 1122

Absorbable

European Pharmacopoeia (88)Sterile synthetic absorbable monofilament sutures ndash 1123

5 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Table 3 US-FDA suture product codes and accompanying citation of US CFRsa)

Suture name Regulation Product code

Absorbable polydioxanone surgical (PDS) suture 21 CFR8784840 NEW

Absorbable poly(glycolideL-lactide) surgical suture 21 CFR8784493 GAM

Absorbable gut suture 21 CFR8784830 GAL

Nonabsorbable poly(ethylene terephthalate) suture 21 CFR8785000 GAT

Nonabsorbable polypropylene surgical suture 21 CFR8785010 GAW

Nonabsorbable polyamide surgical suture 21 CFR8785020 GAR

Natural nonabsorbable silk surgical suture 21 CFR8785030 GAP

Stainless steel surgical suture 21 CFR8784495 GAQ

Nonabsorbable expanded polytetrafluoroethylene (ePTFE)surgical suture

21 CFR8785030 NBY

a) Note this table selects abbreviated results obtained from online search for the implant device term ldquosuturerdquo that was conducted on 6 Aug 2016 athttpwwwaccessdatafdagovscriptscdrhcfdocscfPCDclassificationcfm

FDA and a US Code of Federal Regulations preference forabsorbable terminology when referring to sutures Table4 shows an expansion of that preference to include a to-tal of 30 absorbable implant product classifications each ofwhich is assigned to a relevant Federal regulation that uti-lizes the term ldquoabsorbablerdquoIn short ldquoabsorbablerdquo is both a historically well estab-

lished and currently relevant term in both the regulationand standardization of implants that are intentionally ab-sorbed by the body

Overview of utilization of the terms ldquoresorptionrdquoldquobiore-sorptionrdquo and ldquoresorbablerdquoldquobioresorbablerdquoIn the scope of chemistry the term ldquoresorptionrdquo was used toillustrate the total elimination of a substance from its initialplace caused by physical andor chemical phenomena [14]Besides the understanding from pure chemistry ldquoresorp-tionrdquo is more recognized involved in the metabolic activi-ties in vivo For example ldquoresorptionrdquo is considered as theldquoabsorptionrdquo into the circulatory system of cells or tissuewhich usually includes bone resorption tooth resorptionand vanishing twin [44] In the biomedical scope Prof DWilliams used themeaning in DorlandMedical Dictionaryas ldquolysis and assimilation of a substance as of bonerdquo [23]ldquoBioresorptionrdquo is more common when describing the invivo process of a certain foreign material The ISO definedldquobioresorptionrdquo as a process by which biomaterials are de-graded in the physiological environment and the by-prod-uct are eliminated or completely bioabsorbed [23] Thusaccording to this interpretation the bioresorption processincludes material removal in vivo either by cellular activ-ity or not Conversely Taberrsquos Cyclopedic Medical Dictio-nary [45] describes the term ldquoresorbrdquo as themeaning ldquoto ab-

sorb againrdquomdashsomething that live tissue does but not some-thing any implant is known to domdashbe it permanent or ab-sorbableAs for the adjectives ldquobioresorbablerdquo and ldquoresorbablerdquo

there is no difference when used to describe a kind of ma-terials which have the ability of resorption This is ascribedto the fact that ldquoresorptionrdquo itself already has been well rec-ognized as a biological process [23] Currently there is noASTM entries used ldquoresorbablerdquo or ldquobioresorbablerdquo in thetitle

Utilization and comparison of the terms ldquobiodegradablemetalsrdquo and ldquoabsorbable metallic materialsrdquoldquoBiodegradablemetalsrdquo generally include themetalsMg Feand Zn and their alloys and composites They can be de-fined as metals that assist with tissue healing and are thenexpected to gradually corrode and release corrosion prod-ucts in vivowith an appropriate host response and then dis-solve completely with no implant residues [46] As a resultand different from traditional ldquobio-inertrdquometallic biomate-rials (eg Ti and Co based alloys) that release limited cor-rosion products [47] metabolic reactions besides inflam-mation can be expected to occur between the biodegrad-able metal and the host body after implantation Addition-ally the corrosion-based degradation mechanism of thesematerials is inherently different from that of either bioce-ramics or polymers which has resulted in limited to nostandardized guidance available from either ASTM or ISOInstead of the term ldquobiodegradable metalrdquo the recently

published and first absorbable metal related standardASTM F3160 utilizes the more inclusive word ldquoabsorbablerdquowithin the phrase ldquoabsorbable metallic materialsrdquo andagain defines the term as ldquohellip an initially distinct foreign

6copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Table 4 US-FDA absorbable implant related product codes descriptions and accompanying CFRsa)

Product code Device Device class Regulation number Regulation description

OMT Absorbable lung biopsy plug 2 [8784755] Absorbable lung biopsy plug

LMF Agent absorbable hemostatic collagen based 3 [8784490] Absorbable hemostatic agent and dressing

LMG Agent absorbable hemostatic non-collagen based 3 [8784490] Absorbable hemostatic agent and dressing

MRY Appliances and accessories fixation bone absorbable singlemultiple component 2 [8883040] Smooth or threaded metallic bone fixation fastener

PBQ Fixation non-absorbable or absorbable for pelvic use 2 [8844530] Obstetric-gynecologic specialized manual instrument

HQJ Implant absorbable (scleral buckling methods) 2 [8863300] Absorbable implant (scleral buckling method)

OWT Mesh surgical absorbable abdominal hernia 2 [8783300] Surgical mesh

OXM Mesh surgical absorbable fistula 2 [8783300] Surgical mesh

OXI Mesh surgical absorbable large abdominal wall defects 2 [8783300] Surgical mesh

OXL Mesh surgical absorbable organ support 2 [8783300] Surgical mesh

OWW Mesh surgical absorbable orthopaedics reinforcement of tendon 2 [8783300] Surgical mesh

OXF Mesh surgical absorbable plastic and reconstructive surgery 2 [8783300] Surgical mesh

OXC Mesh surgical absorbable staple line reinforcement 2 [8783300] Surgical mesh

OWZ Mesh surgical absorbable thoracic chest wall reconstruction 2 [8783300] Surgical mesh

OWU Mesh surgical non-absorbable diaphragmatic hernia 2 [8783300] Surgical mesh

OWR Mesh surgical non-absorbable facial implants for plastic surgery 2 [8783300] Surgical mesh

OXJ Mesh surgical non-absorbable large abdominal wall defects 2 [8783300] Surgical mesh

OWX Mesh surgical non-absorbable orthopaedics reinforcement of tendon 2 [8783300] Surgical mesh

OXG Mesh surgical non-absorbable plastic and reconstructive surgery 2 [8783300] Surgical mesh

OXD Mesh surgical non-absorbable staple line reinforcement 2 [8783300] Surgical mesh

OXA Mesh surgical non-absorbable thoracic chest wall reconstruction 2 [8783300] Surgical mesh

LBP Replacement ossicular (stapes) using absorbable gelatin material 2 [8743450] Partial ossicular replacement prosthesis

OLL Septal staplerabsorbable staples 2 [8784750] ImplanTABLE staple

MNU Staple absorbable 2 [8883030] Singlemultiple component metallic bone fixationappliances and accessories

GAK Suture absorbable 2 [8784830] Absorbable surgical gut suture

GAL Suture absorbable natural 2 [8784830] Absorbable surgical gut suture

HMO Suture absorbable ophthalmic 3

GAN Suture absorbable synthetic 2 [8784830] Absorbable surgical gut suture

GAM Suture absorbable synthetic polyglycolic acid 2 [8784493] Absorbable poly(glycolidel-lactide) surgical suture

NEW Suture surgical absorbable polydioxanone 2 [8784840] Absorbable polydioxanone surgical suture

a) Note the results obtained from online search for the device term ldquoabsorbablerdquo that was conducted on 6 Aug 2016 at httpwwwaccessdatafdagovscriptscdrhcfdocscfPCDclassifica-tioncfm

7 copy

ScienceChina

Pressand

Springer-VerlagBerlin

Heidelberg 2017

SCIENCECH

INAMaterials

REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

material or substance that either directly or through in-tended degradation can pass through or be metabolized orassimilated by cells andor tissuerdquo The standardrsquos nomen-clature appendix further elaborates on its preference forldquoabsorbablerdquo since the prefix ldquobio-rdquo is redundant in thecontext of implant applications [43]Clearly these two terms of ldquobiodegradable metalsrdquo and

ldquoabsorbable metallic materialsrdquo share the same connota-tion which defines the completemission of an intentionallydegradable material when implanted in vivo In the contextof biodegradable metalsabsorbable metallic materialsthe process includes the corrosion caused by body fluida host response caused by corrosion products followedby dissolutionabsorption and finally improved tissuehealing The ldquobiodegradationrdquo instead of ldquobiocorrosionrdquois used to distinguish this new kind of metals which canfully dissolve in vivo with no implant residues Besidesbiodegradation process the following dynamic process ofdissolutionabsorption also starts in vivo For exampledissolved Mg2+ is considered to enhance the integrin me-diated human-bone-derived cell adhesion and affect newbone formation [48] The metabolic reaction is also crucialand even more important for biodegradable metals as it ishelpful It is another distinction from traditional metalsused for biomedical application In fact the different usagehabit forming of ldquobiodegradablerdquo or ldquoabsorbablerdquoldquobioab-sorbablerdquo may be more related with the study field theresearchers in Taking the ldquoabsorbablerdquo metallic stent asan example (Fig 2) once the ldquoabsorbablerdquo metallic stentwas implanted into blood vessel ldquocorrosionrdquo of biometal

begins The corrosion products including debris hydro-gen (for Mg-based metals) metallic ions and hydroxylconvert the local environment and diffuse into the bloodvessel wall Some corrosion products can be biologicallybeneficial For instance the diffused and absorbed Zn2+

can potentially play a positive role in dealing with athero-sclerosis [49] Along with the corrosion process healingprocesses such as endothelialization may become en-hanced In summary and within the context of absorbablemetals the adjectives ldquodegradablerdquo and ldquoabsorbablerdquo referto the nature of the biodegradation products of the mate-rialdevice being metabolically absorbed an attribute ofthe host (animal or human body) regardless of whetherthe implant degrades corrodes hydrolyzes or dissolves[50ndash52]

Summary quantification of the common TermsFig 3a shows preliminary searching results in Webof Knowledge using ldquodegradablerdquo ldquoabsorbablerdquo or ldquore-sorbablerdquo along with ldquomaterialrdquo as key words Theutilization of ldquodegradablerdquo is a bit more frequently thanldquoabsorbablerdquo but that of ldquoresorbablerdquo steps down Mean-while the counterpart searching result when using ldquobiordquo asprefix to the adjectives along with ldquomaterialrdquo as keywordsare presented in Fig 3b ldquoBiodegradable materialrdquo is themost common utilization which holds 91 among the ex-pression approach This is also due to the fact that besidesthe common utilization in biomaterials ldquobiodegradablerdquois also used in a wide range of applications such as cleanenvironment and ecology [5354]

Figure 2 Different point of views on the biodegradationabsorption process

8copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Figure 3 Searching results in Web of Knowledge from all databases (a) with the total searched publication numbers by ldquodegradablerdquo+ ldquomaterialrdquoldquoabsorbablerdquo+ ldquomaterialrdquo and ldquoresorbablerdquo+ ldquomaterialrdquo as 100 (b) the total searched publication numbers by ldquobiodegradablerdquo+ ldquomaterialrdquo ldquobioab-sorbablerdquo+ ldquomaterialrdquo and ldquobioresorbablerdquo+ ldquomaterialrdquo as 100

DISCUSSION

Expertise inherent biasesAs previously mentioned biomaterial is an interdiscipli-nary field fascinating researchers with specialty from dif-ferent backgrounds Different backgrounds as well as dif-ferent research point of interests may be one of the reasonsfor using different terminologies Materials scientists tendto focus on the materialdevice itself leading to their usageof ldquobiodegradablerdquo to illustrate what happens to the deviceThey pay more attention to the process such as hydroly-sis corrosion debris degradation products and the changeof surface morphology resulting in the researching inter-ests of ldquomaterial biodegradationrdquo In contrast surgeons andbiomedical researchers tend to be concerned more on thehost response and healing process They are curious aboutthe absorption of various degradation products of the im-planted materialdevice and related metabolism mecha-nism and thereby prefer to use the term ldquoabsorbablerdquo toillustrate what happens to the device As known somema-terials may only undergo biodegradation but the corrosionproducts still have no influence on the metabolic activitiesFor example cellulose is considered as ldquodietary fiberrdquowhichcannot be digested and absorbed by human body but is be-nign for human body [55] Some coating tablets for drug ordrug delivery systems made from cellulose and its deriva-tives are quite frequently utilized or investigated [5657]The polymer and derivatives of cellulose can only be de-graded but not be absorbed by human body [58] For suchmaterials the adjective ldquoabsorbablerdquo or ldquobioabsorbablerdquo isnot appropriateOverall once the materialsdevices are implanted into

the human body the ldquobiocorrosionrdquobiodegradationrdquoprocess happens immediately no matter to what degreeat the same time the host will biologically response to the

corrosiondegradation products through the absorptionmetabolism and excretion processes So for the samestory the majority of materials scientists would report itby ldquobiodegradabledegradationrdquo way whereas the majorityof medical doctors would report it by ldquoabsorbableab-sorptionrdquo way In nature the two terms ldquobiodegradablemetalsrdquo and ldquoabsorbable metallic materialsrdquo share the sameconnotation and are mutually replaceable

Connotation and extension of noun forms ldquobiodegradationbioabsorption and bioresorptionrdquo and adjectivesldquobiodegradable bioabsorbable and bioresorbablerdquoThe three noun forms of the terms illustrate the processwhile their adjectival derivatives were used to describe thegroup of materials with such certain capabilities For thestudy on biomaterials polymer researchers use ldquodegrada-tionbiodegradationrdquo when there is proved chain scissionprocess Besides they differentiate ldquobiodegradationrdquo andldquodegradationrdquo by confirmed metabolic activities betweenthe materials and cells or tissues Regarding to the fouradjectives ldquobiodegradablerdquo ldquobioabsorbablerdquo and ldquobiore-sorbablerdquo the term ldquobiocorrodiblerdquo is only used in scientificpapers on iron based materials and some patents on mag-nesium based materials The common usage of termsldquobiodegradablerdquo ldquobioabsorbablerdquo and ldquobioresorbablerdquo withrespect to the biomaterial research area is shown in Table 5The results reveal a widespread usage of ldquobiodegradablerdquo inboth polymers and magnesium based metals Varies typesof materials were reported as biomaterials Besides thereare also reports of ldquobiodegradablerdquo polymers for ecologyand environmental protection which indicates a furtherusage scope of ldquobiodegradablerdquo not only for implants anddevices Besides ldquobioresorbablerdquo is also utilized in all theresearch fields of polymers ceramics andmetals Howeverno current work used ldquobioabsorbablerdquo as grammatical

9 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Table 5 Current reported usage of terms ldquobiodegradablerdquo ldquobioabsorbablerdquo and ldquobioresorbablerdquoTerminology Category Materials Applications

PLA-PEG-biotin PLGA Controlled cell engineering [5960]Porous PLGA Tissue engineering [61ndash63]

PLGA-PEG-PLGA Injective thermosensitive hydrogel [64]PLGA Nerve guidance [65]

Fibronectin (Fn)-coated PLLA P(LLA-CL) Enhanced growth of endothelial cells [6066]PEG tethered PPF [67]

PDMS Drug delivery [68]PGA Tissue engineering [69]

Undefined Coronary stent [70ndash72]PGA Joint resurfacing [73]

Polymers

PHA Ecology and environmental protection [74]CaO-P2O5 glass Bone regeneration [75]β-Whitlockite Bone regeneration [76]

Calcium phosphate hydraulic cement Bone regeneration [77]Calcium

phosphate glass ceramicsBone regeneration [78]

Ceramics

CaO-SiO2-B2O3 glass-ceramics Bone regeneration [79]Pure Mg Implant material [80]

Mg-Ca-based Bone regeneration [81ndash84]Mg-Zn-based Bone regeneration [338586]Mg-Sr-based Bone regeneration [87ndash89]Mg-RE-based Vascular stent [90ndash92]

Mg and its metals

Mg-Ag-based [93]Zn-Mg Zn-Ca Zn-Sr [9495]Zn and its metals Zn-Mg-Sr [96]

Fe [9798]

Biodegradable

Fe and its metals Fe-Mn [99]PLLA PLG PGA Molecule delivery [100]

PGA Suture [101]Undefined Drug-eluting stent [102103]

PLA Neuron attachment [104]Polymers

PLA and PCL reinforced with PGA fibers Bile duct patch [105]Mg-RE based Coronary stent [106ndash109]

Binary Mg alloys [110]Mg and its metalsMg-Al-based [111112]

Zn and its metals Pure Zinc [113114]Fe and its metals Nitrided iron [115]

PLDLA Transforaminal lumbar interbody fusion [116]Alkylene bis(dilactoyl)-methacrylate modified polymer Bone screw augmentation [117]

Undefined Coronary stent [118]PHB Mandibular defects regeneration [119]HA Bone regeneration [120]Ceramics Calcium phosphate [121122]

MgNd2 Stent material [123]Porous Mg Bone substitute [124]Mg-RE Coronary stent [125]Mg-Ca Orthopedic application [126]

Mg and its metals

Mg-based Finite element analysis [127]

Bioabsorbable

Fe and its metals Pure Fe [128]

10copy

ScienceChina

Pressand

Springer-VerlagBerlin

Heidelberg 2017

REVIEWSCIENCE

CHINA

Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

modifier to bioceramics In addition as previouslyillustrated the prefix ldquobiordquo of ldquobioabsorbablerdquo and ldquobiore-sorbablerdquo are abridged hereafter discussion will concen-trate on ldquobiocorrodiblerdquo ldquobiodegradablerdquo ldquoabsorbablerdquo andldquoresorbablerdquoSince absorbable technologies are increasingly utilized

in numerous new and broader implant applications it be-comes more important to not acquiesce in addressing his-torical problems and instead actively move forward towardutilizing standardized language that is both technically ac-curate and unified in itsmeaning Preferred language needsto accurately communicate the concept To achieve the uni-fying goal of harmonized terminology themedical and sci-entific communities need to not solely look at materialschemistry or even biomaterials alone but to instead lookat term selection both across and within the context of thebroader medical disciplinemdashthe location where the resultsof implant technology development actually reaches themarketplace where therapies are brought to those in needNomenclature solutions need to both understand and re-spond to the context of terms across adjacent technologieswhich means to address needs from the perspectives of thebiomaterial researcher the deviceproduct developer thesurgeonclinician user the regulator and last but not leastthe patientgeneral public who is the direct beneficiary ofthe developed technologyA better understanding of these terminologies is neces-

sary and beneficial to the field Therefore the definitionson ldquodegradablerdquo ldquoabsorbablerdquo ldquoresorbablerdquo and relatedterms proposed by different organizations in differentfields have been summarized and discussed with the con-notation and extension of each term being compared andthe criteria being proposed

CONCLUDING REMARKSHerein given both the searching problem on the Internetand ambiguity in meanings the usage of grammaticalmodifiers to describe biomaterials that is eventually ab-sorbed by human body has been enumerated based onusage habits laws standards and markets In summaryldquodegradablerdquoldquobiodegradablerdquo are the most frequently usedgrammatical modifier not only in metals but also poly-mers as such kind of biomaterials ldquoBiodegradationrdquo andldquobiodegradablerdquo define the change of the materialdevicewell in the research of biomaterials but they are alsoadopted in other fields such as ecology and environmentalprotection Meanwhile ldquoresorbablerdquoldquobioresorbablerdquo havelong been recognized in the biological research and theldquoresorptionrdquo itself has been widely accepted as a biological

reaction The utilization of ldquoresorbablerdquoldquobioresorbablerdquowas found to be not as frequent as the counterpartsldquodegradablerdquoldquobiodegradablerdquo and ldquoabsorbablerdquoldquobioab-sorbablerdquo Such usage is accurate for osteoclast driven boneresorption but is inappropriate for implants that do notcarry the potential to grow back into their original formOtherwise despite it is not the most frequently used termldquoabsorbablerdquoldquobioabsorbablerdquo concentrates more on thehost metabolism to the foreign biodegradation productsof the implanted materialdevice compared with ldquodegrad-ablerdquoldquobiodegradablerdquo ldquoAbsorbablerdquo is defined in the scopeof biomaterials by different organizations and their publi-cations and also adopted by ASTM to illustrate ldquoabsorbablepolymerrdquo It is the most historically established the mostbroadly applicable (includes dissolvable devices that donot degrade) the most specific to medical applicationsand is the formal legal descriptor for most implant devicesConsidering the usage history common utilization in lawand standards as well as the scientific meaning in essenceldquoabsorbablerdquo can be better among other grammaticalmodifiers for description of an implant that is eventuallyabsorbed by the body which is recommended by theauthors for a further internationally-unified usage

Received 28 February 2017 accepted 27 March 2017published online 26 April 2017

1 Mackenzie D The history of sutures Med Hist 1973 17 158ndash1682 Hench LL Bioceramics J Am Ceramic Soc 2005 81 1705ndash17283 Hench LL Bioceramics from concept to clinic J AmCeramic Soc

1991 74 1487ndash15104 Windhagen H Radtke K Weizbauer A et al Biodegradable

magnesium-based screw clinically equivalent to titanium screw inhallux valgus surgery short term results of the first prospectiverandomized controlled clinical pilot study BioMed Eng OnLine2013 12 62

5 Schildwaumlchter M Biotronik announces CE mark for magmaristhe first clinically-proven bioresorbable magnesium scaffoldhttpwwwmagmariscomennewsroomjune-15-2016

6 Shalaby SW Burg KJL Bioabsorbable polymers update degrada-tion mechanisms safety and application J App Biomater 1995 6219ndash221

7 Vert M Li SM Spenlehauer G et al Bioresorbability and biocom-patibility of aliphatic polyesters J Mater Sci-Mater Med 1992 3432ndash446

8 Vert M Degradable and bioresorbable polymers in surgery and inpharmacology beliefs and facts J Mater Sci-Mater Med 2009 20437ndash446

9 Benicewicz BC Hopper PK Review polymers for absorbablesurgical suturesmdashPart I J Bioactive Compatible Polym 1990 5453ndash472

10 Barrows HT Synthetic bioabsorbable polymers In Szycher M(Ed) High Performance Biomaterials A Complete Guide toMed-ical and Pharmceutical Applications Boca Raton CRC PRESS1991 243ndash257

11 Weiler A Hoffmann RFG Staumlhelin AC et al Biodegradable

11 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

implants in sports medicine the biological base Arthroscopy-JArthroscopic Related Surgery 2000 16 305ndash321

12 Ikada Y Tsuji H Biodegradable polyesters for medical and ecolog-ical applications Macromol Rapid Commun 2000 21 117ndash132

13 Ashammakhi N Peltoniemi H Waris E et al Developments incraniomaxillofacial surgery use of self-reinforced bioabsorbableosteofixation devices Plast Reconstr Surg 2001 108 167ndash180

14 Vert M Doi Y Hellwich KH et al Terminology for biorelatedpolymers and applications (IUPACRecommendations 2012) PureAppl Chem 2012 84 377ndash410

15 The United States Pharmacopeial Convention The Second Sup-plement to the Pharmacopeia of the United States of America 11thdecennial revision (USP XI-1939 Supplement) 1939

16 Truhlsen SM The recession operation histopathologic responseand suture reaction and absorption Trans Am Ophthalmol Soc1965 63 626ndash677

17 USP in US Law httpwwwusporgprintabout-usplegal-recog-nitionusp-us-law

18 USP develops and publishes standards for drug substances drugproducts excipients and dietary supplements in the United StatesPharmacopeia-National Formulary (USP-NF)

19 United States Public Law 94-295 197620 United States Pharmacopeia httpwwwusporg21 British Pharmacopeia httpswwwpharmacopoeiacom22 European Pharmacopoeia httponlinepheurorgENentryhtm23 Williams DF The Williams Dictionary of Biomaterials Liverpool

Liverpool University Press 199924 httpsenwikipediaorgwikiBiodegradation25 Jones RG Kahovec J Stepto R et al Compendium of Polymer

Terminology and Nomenclature IUPAC Recommendations 2008Cambridge RSC Publishing 2009

26 Higashi S Yamamuro T Nakamura T et al Polymer-hydroxyap-atite composites for biodegradable bone fillers Biomaterials 19867 183ndash187

27 de Groot K Bioceramics of Calcium Phosphate Boca Raton CRCPress 1983

28 Hollinger JO Battistone GC Biodegradable bone repair materialssynthetic polymers and ceramics ClinOrthopRelat Res 1986 207290ndash306

29 ASTMD653-14 Standard Terminology Relating to Soil Rock andContained Fluids ASTM International West Conshohocken PA2014 httpswwwastmorgStandardsD653htm

30 Witte F Hort N Vogt C et al Degradable biomaterials based onmagnesium corrosion Curr Opin Solid State Mater Sci 2008 1263ndash72

31 Lynn DM Langer R Degradable poly(β-amino esters) synthesischaracterization and self-assemblywith plasmidDNA JAmChemSoc 2000 122 10761ndash10768

32 Cima LG Vacanti JP Vacanti C et al Tissue engineering by celltransplantation using degradable polymer substrates J BiomechEng 1991 113 143ndash151

33 Zhang S Zhang X Zhao C et al Research on an Mg-Zn alloy as adegradable biomaterial Acta Biomater 2010 6 626ndash640

34 Anseth KS Metters AT Bryant SJ et al In situ forming degradablenetworks and their application in tissue engineering and drug de-livery J Control Release 2002 78 199ndash209

35 Forrest ML Koerber JT Pack DW A degradable polyethyleniminederivative with low toxicity for highly efficient gene delivery Bio-conjugate Chem 2003 14 934ndash940

36 ASTM E2747-11 Standard Specification for Evaluation and Selec-tion of Onsite Offices for Environmentally Sustainable MeetingsEvents Trade Shows and Conferences ASTM International

West Conshohocken PA 2011 httpswwwastmorgStan-dardsE2747htm

37 ASTM E2745-11 Standard Specification for Evaluation andSelection of Audio Visual (AV) and Production for Environ-mentally Sustainable Meetings Events Trade Shows and Con-ferences ASTM International West Conshohocken PA 2011httpswwwastmorgStandardsE2745htm

38 ASTM E2746-11 Standard Specification for Evaluation andSelection of Communication and Marketing Materials for En-vironmentally Sustainable Meetings Events Trade Shows andConferences ASTM International West Conshohocken PA 2011httpswwwastmorgStandardsE2746htm

39 ASTM E2741-11 Standard Specification for Evaluation and Se-lection of Destinations for Environmentally Sustainable MeetingsEvents Trade Shows and Conferences ASTM InternationalWest Conshohocken PA 2011 httpswwwastmorgStan-dardsE2741htm

40 0 ASTM E2773-11 Standard Specification for Evaluation andSelection of Food and Beverage for Environmentally SustainableMeetings Events Trade Shows and Conferences ASTM Interna-tional West Conshohocken PA 2011 httpswwwastmorgStan-dardsE2773htm

41 ASTM E2742-11 Standard Specification for Evaluation and Selec-tion of Exhibits for Environmentally Sustainable Meetings EventsTrade Shows and Conferences ASTM International West Con-shohocken PA 2011 httpswwwastmorgStandardsE2742htm

42 ASTM E2774-11 Standard Specification for Evaluation and Selec-tion of Venues for Environmentally Sustainable Meetings EventsTrade Shows and Conferences ASTM International West Con-shohocken PA 2011 httpswwwastmorgStandardsE2774htm

43 ASTM F2902-12 Standard Guide for Assessment of AbsorbablePolymeric Implants ASTM International West ConshohockenPA 2012 httpswwwastmorgStandardsF2902htm

44 httpsenwikipediaorgwikiResorption45 Venes D Tabers Cyclopedic Medical Dictionary 22th edition

Philadelphia F A Davis Company 201346 Zheng YF Gu XN Witte F Biodegradable metals Mater Sci Eng-

R-Rep 2014 77 1ndash3447 Hanawa T Metal ion release from metal implants Mater Sci

Eng-C 2004 24 745ndash75248 Zreiqat H Howlett CR Zannettino A et al Mechanisms of mag-

nesium-stimulated adhesion of osteoblastic cells to commonly usedorthopaedic implants J Biomed Mater Res 2002 62 175ndash184

49 Little PJ Bhattacharya R Moreyra AE et al Zinc and cardiovascu-lar disease Nutrition 2010 26 1050ndash1057

50 Seager H Drug-delivery products and the Zydis fast-dissolvingdosage form J Pharm Pharmacol 1998 50 375ndash382

51 Shikinami Y Shape-memory biodegradable and absorbable mate-rial US Patent No 6281262 2001-8-28

52 Huitema TW Knight GW Ransick MH Schulze DR Surgical im-plant with preferential corrosion zone US Patent No 79059022011-3-15

53 Luzier WD Materials derived from biomassbiodegradable mate-rials Proc Natl Acad Sci USA 1992 89 839ndash842

54 Gross RA Kalra B Biodegradable polymers for the environmentScience 2002 297 803ndash807

55 Trumbo P Schlicker S Yates AA et al Dietary reference intakesfor energy carbohydrate fiber fat fatty acids cholesterol proteinand amino acids J Am Diet Assoc 2002 102 1621ndash1630

56 Chambin O Champion D Debray C et al Effects of different cel-lulose derivatives on drug release mechanism studied at a prefor-mulation stage J Control Release 2004 95 101ndash108

12copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

57 Fundueanu G Constantin M Esposito E et al Cellulose acetatebutyrate microcapsules containing dextran ion-exchange resinsas self-propelled drug release system Biomaterials 2005 264337ndash4347

58 Maumlrtson M Viljanto J Hurme T et al Is cellulose sponge degrad-able or stable as implantation material An in vivo subcutaneousstudy in the rat Biomaterials 1999 20 1989ndash1995

59 Patel N Padera R Sanders GH et al Spatially controlled cell en-gineering on biodegradable polymer surfaces The FASEB journal1998 12 1447ndash1454

60 Goldstein A Effect of convection on osteoblastic cell growth andfunction in biodegradable polymer foam scaffolds Biomaterials2001 22 1279ndash1288

61 Wu L Ding J In vitro degradation of three-dimensional porouspoly(DL-lactide-co-glycolide) scaffolds for tissue engineeringBiomaterials 2004 25 5821ndash5830

62 Wu L Ding J Effects of porosity and pore size on in vitro degra-dation of three-dimensional porous poly(DL-lactide-co-glycolide)scaffolds for tissue engineering J Biomed Mater Res 2005 75A767ndash777

63 Pan Z Ding J Poly(lactide-co-glycolide) porous scaffolds for tissueengineering and regenerative medicine Interface Focus 2012 2366ndash377

64 Yu L Zhang Z Zhang H et al Biodegradability and biocompati-bility of thermoreversible hydrogels formed from mixing a sol anda precipitate of block copolymers in water Biomacromolecules2010 11 2169ndash2178

65 Wen X Tresco PA Fabrication and characterization of permeabledegradable poly(DL-lactide-co-glycolide) (PLGA) hollow fiberphase inversion membranes for use as nerve tract guidance chan-nels Biomaterials 2006 27 3800ndash3809

66 Chu CFL Lu A Liszkowski M et al Enhanced growth of animaland human endothelial cells on biodegradable polymers BBA-GenSubjects 1999 1472 479ndash485

67 Jo S Engel PS Mikos AG Synthesis of poly(ethylene glycol)-teth-ered poly(propylene fumarate) and its modification with GRGDpeptide Polymer 2000 41 7595ndash7604

68 Park JH Allen MG Prausnitz MR Biodegradable polymer mi-croneedles fabrication mechanics and transdermal drug deliveryJ Control Release 2005 104 51ndash66

69 Freed LE Vunjak-Novakovic G Biron RJ et al Biodegradablepolymer scaffolds for tissue engineering Nat Biotechnol 1994 12689ndash693

70 Windecker S Serruys PW Wandel S et al Biolimus-eluting stentwith biodegradable polymer versus sirolimus-eluting stent withdurable polymer for coronary revascularisation (LEADERS) arandomised non-inferiority trial Lancet 2008 372 1163ndash1173

71 Stefanini GG Kalesan B Serruys PW et al Long-term clinicaloutcomes of biodegradable polymer biolimus-eluting stents ver-sus durable polymer sirolimus-eluting stents in patients with coro-nary artery disease (LEADERS) 4 year follow-up of a randomisednon-inferiority trial Lancet 2011 378 1940ndash1948

72 Raungaard B Jensen LO Tilsted HH et al Zotarolimus-elutingdurable-polymer-coated stent versus a biolimus-eluting biodegrad-able-polymer-coated stent in unselected patients undergoing per-cutaneous coronary intervention (SORT OUT VI) a randomisednon-inferiority trial Lancet 2015 385 1527ndash1535

73 Freed LE Grande DA Lingbin Z et al Joint resurfacing using allo-graft chondrocytes and synthetic biodegradable polymer scaffoldsJ Biomed Mater Res 1994 28 891ndash899

74 Poirier Y Nawrath C Somerville C Production of polyhydrox-yalkanoates a family of biodegradable plastics and elastomers in

bacteria and plants Nat Biotechnol 1995 13 142ndash15075 Dias A Tsuru K Hayakawa S et al Crystallisation studies of

biodegradable CaO-P2O5 glass with MgO and TiO2 for boneregeneration applications Glass Technol 2004 45 78ndash79

76 Klein CPAT de Groot K Drissen AA et al Interaction ofbiodegradable β-whitlockite ceramics with bone tissue an in vivostudy Biomaterials 1985 6 189ndash192

77 Ikenaga M Hardouin P Lemaicirctre J et al Biomechanical charac-terization of a biodegradable calcium phosphate hydraulic cementa comparison with porous biphasic calcium phosphate ceramics JBiomed Mater Res 1998 40 139ndash144

78 Dias AG Lopes MA Santos JD et al In vivo performance ofbiodegradable calcium phosphate glass ceramics using the rabbitmodel histological and SEM observation J Biomater Appl 200620 253ndash266

79 Lee JH Lee CK Chang BS et al In vivo study of novel biodegrad-able and osteoconductive CaO-SiO2-B2O3 glass-ceramics JBiomed Mater Res 2006 77A 362ndash369

80 Song G Song S A possible biodegradable magnesium implant ma-terial Adv Eng Mater 2007 9 298ndash302

81 Kim WC Kim JG Lee JY et al Influence of Ca on the corrosionproperties of magnesium for biomaterials Mater Lett 2008 624146ndash4148

82 Li Z Gu X Lou S et al The development of binary Mg-Ca alloysfor use as biodegradablematerials within bone Biomaterials 200829 1329ndash1344

83 Wan Y Xiong G Luo H et al Preparation and characterization ofa new biomedical magnesium-calcium alloy Mater Des 2008 292034ndash2037

84 Seong JW Kim WJ Development of biodegradable Mg-Ca alloysheets with enhanced strength and corrosion properties throughthe refinement anduniformdispersion of theMg2Caphase by high-ratio differential speed rolling Acta Biomater 2015 11 531ndash542

85 Zhang S Li J Song Y et al In vitro degradation hemolysis andMC3T3-E1 cell adhesion of biodegradable Mg-Zn alloy Mater SciEng-C 2009 29 1907ndash1912

86 Li J Song Y Zhang S et al In vitro responses of human bone mar-row stromal cells to a fluoridated hydroxyapatite coated biodegrad-able Mg-Zn alloy Biomaterials 2010 31 5782ndash5788

87 Brar HS Wong J Manuel MV Investigation of the mechanical anddegradation properties of Mg-Sr and Mg-Zn-Sr alloys for use aspotential biodegradable implant materials J Mech Behav BiomedMater 2012 7 87ndash95

88 Bornapour M Muja N Shum-Tim D et al Biocompatibility andbiodegradability of Mg-Sr alloys the formation of Sr-substitutedhydroxyapatite Acta Biomater 2013 9 5319ndash5330

89 Gu XN Xie XH Li N et al In vitro and in vivo studies on aMg-Sr binary alloy system developed as a new kind of biodegrad-able metal Acta Biomater 2012 8 2360ndash2374

90 Haumlnzi AC Gerber I Schinhammer M et al On the in vitro andin vivo degradation performance and biological response of newbiodegradableMg-Y-Zn alloys Acta Biomater 2010 6 1824ndash1833

91 Chou DT Hong D Saha P et al In vitro and in vivo corrosioncytocompatibility and mechanical properties of biodegradableMg-Y-Ca-Zr alloys as implant materials Acta Biomater 2013 98518ndash8533

92 Zong Y Yuan G Zhang X et al Comparison of biodegradable be-haviors of AZ31 and Mg-Nd-Zn-Zr alloys in Hanks physiologicalsolution Mater Sci Eng-B 2012 177 395ndash401

93 Tie D Feyerabend FMuumlllerWD et al Antibacterial biodegradableMg-Ag alloys Eur Cell Mater 2013 25 284ndash298

94 VojtěchDKubaacutesek J Seraacutek J et al Mechanical and corrosion prop-

13 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

erties of newly developed biodegradable Zn-based alloys for bonefixation Acta Biomater 2011 7 3515ndash3522

95 Li H Yang H Zheng Y et al Design and characterizations of novelbiodegradable ternary Zn-based alloys with IIA nutrient alloyingelements Mg Ca and Sr Mater Des 2015 83 95ndash102

96 Liu X Sun J Yang Y et al Microstructure mechanical proper-ties in vitro degradation behavior and hemocompatibility of novelZn-Mg-Sr alloys as biodegradable metals Mater Lett 2016 162242ndash245

97 Wu C Qiu H Hu X et al Short-term safety and efficacy of thebiodegradable iron stent in mini-swine coronary arteries ChinMed J (Engl) 2013 126 4752ndash4757

98 Purnama A Hermawan H Champetier S et al Gene expressionprofile of mouse fibroblasts exposed to a biodegradable iron alloyfor stents Acta Biomater 2013 9 8746ndash8753

99 HermawanH Purnama A Dube D et al Fe-Mn alloys for metallicbiodegradable stents degradation and cell viability studies ActaBiomater 2010 6 1852ndash1860

100 Sheridan MH Shea LD Peters MC et al Bioabsorbable polymerscaffolds for tissue engineering capable of sustained growth factordelivery J Control Release 2000 64 91ndash102

101 Shawe S Buchanan F Harkin-Jones E et al A study on the rate ofdegradation of the bioabsorbable polymer polyglycolic acid (PGA)J Mater Sci 2006 41 4832ndash4838

102 Palmerini T Biondi-Zoccai G Della Riva D et al Clinical out-comes with bioabsorbable polymer- versus durable polymer-baseddrug-eluting and bare-metal stents J Am Coll Cardiol 2014 63299ndash307

103 Tanimoto S Serruys PW Thuesen L et al Comparison of in vivoacute stent recoil between the bioabsorbable everolimus-elutingcoronary stent and the everolimus-eluting cobalt chromium coro-nary stent insights from the ABSORB and SPIRIT trials CatheterCardiovasc Interv 2007 70 515ndash523

104 Tsuji H Sasaki H Sato H et al Neuron attachment properties ofcarbon negative-ion implanted bioabsorbable polymer of poly-lac-tic acid Nucl Instr Meth Phys Res Sect B-Beam Interact MaterAtoms 2002 191 815ndash819

105 Aikawa M Miyazawa M Okamoto K et al A novel treatment forbile duct injury with a tissue-engineered bioabsorbable polymerpatch Surgery 2010 147 575ndash580

106 WaksmanR Pakala R Kuchulakanti PK et al Safety and efficacy ofbioabsorbablemagnesium alloy stents in porcine coronary arteriesCatheter Cardiovasc Interv 2006 68 607ndash617

107 Di Mario C Griffiths H Goktekin O et al Drug-eluting bioab-sorbable magnesium stent J Interv Cardiol 2004 17 391ndash395

108 Erbel R Di Mario C Bartunek J et al Temporary scaffoldingof coronary arteries with bioabsorbable magnesium stents aprospective non-randomised multicentre trial Lancet 2007 3691869ndash1875

109 Schranz D Zartner P Michel-Behnke I et al Bioabsorbable metalstents for percutaneous treatment of critical recoarctation of theaorta in a newborn Catheter Cardiovasc Interv 2006 67 671ndash673

110 Gu X Zheng Y Cheng Y et al In vitro corrosion and biocompati-bility of binary magnesium alloys Biomaterials 2009 30 484ndash498

111 Hiromoto S InoueM Taguchi T et al In vitro and in vivo biocom-patibility and corrosion behaviour of a bioabsorbable magnesiumalloy coated with octacalcium phosphate and hydroxyapatite ActaBiomater 2015 11 520ndash530

112 Hiromoto S Tomozawa M Maruyama N Fatigue property of abioabsorbable magnesium alloy with a hydroxyapatite coatingformed by a chemical solution deposition J Mech Behav Biomed-ical Mater 2013 25 1ndash10

113 Bowen PK Drelich J Goldman J Zinc exhibits ideal physiologicalcorrosion behavior for bioabsorbable stents Adv Mater 2013 252577ndash2582

114 Liu X Sun J Yang Y et al In vitro investigation of ultra-pure Znand its mini-tube as potential bioabsorbable stent material MaterLett 2015 161 53ndash56

115 LinW Zhang G Cao P et al Cytotoxicity and its test methodologyfor a bioabsorbable nitrided iron stent J Biomed Mater Res 2015103 764ndash776

116 Coe JD Vaccaro AR Instrumented transforaminal lumbar inter-body fusion with bioresorbable polymer implants and iliac crestautograft Spine 2005 30 S76ndashS83

117 Ignatius AA Augat P Ohnmacht M et al A new bioresorbablepolymer for screw augmentation in the osteosynthesis of osteo-porotic cancellous bone a biomechanical evaluation J BiomedMater Res 2001 58 254ndash260

118 Krucoff MW Kereiakes DJ Petersen JL et al A novel biore-sorbable polymer paclitaxel-eluting stent for the treatment ofsingle and multivessel coronary disease J Am Coll Cardiol 200851 1543ndash1552

119 Kostopoulos L Karring T Guided bone regeneration in mandibu-lar defects in rats using a bioresorbable polymer Clin Oral Im-plants Res 1994 5 66ndash74

120 Dubok VA Bioceramicsmdashyesterday today tomorrow PowderMetall Metal Ceram 2000 39 381ndash394

121 Safronova T Kuznetsov A Korneychuk S et al Calcium phos-phate powders synthesized from solutions with [Ca2+][PO4

3minus]=1for bioresorbable ceramics Cent Eur J Chem 2009 7 184ndash191

122 Bohner M Bioresorbable ceramics In Buchanan FJ (Ed) Degra-dation Rate of Bioresorbable Materials Cambridge WoodheadPublishing 2008 95-114

123 Seitz JM Eifler R Stahl J et al Characterization ofMgNd2 alloy forpotential applications in bioresorbable implantable devices ActaBiomater 2012 8 3852ndash3864

124 WenCE Yamada Y Shimojima K et al Porous bioresorbable mag-nesium as bone substitute MSF 2003 419ndash422 1001ndash1006

125 Campos CM Muramatsu T Iqbal J et al Bioresorbable drug-elut-ing magnesium-alloy scaffold for treatment of coronary artery dis-ease Int J Mol Sci 2013 14 24492ndash24500

126 KirklandNT Birbilis NWalker J et al In-vitro dissolution ofmag-nesium-calcium binary alloys clarifying the unique role of calciumadditions in bioresorbable magnesium implant alloys J BiomedMater Res 2010 95B 91ndash100

127 Gastaldi D Sassi V Petrini L et al Continuum damage model forbioresorbable magnesium alloy devices mdashapplication to coronarystents J Mech Behav Biomed Mater 2011 4 352ndash365

128 Kitabata H Waksman R Warnack B Bioresorbable metal scaffoldfor cardiovascular application current knowledge and future per-spectives Cardiovasc Revasc Med 2014 15 109ndash116

Acknowledgments This work was supported by the National Key Re-search and Development Program of China (2016YFC1102402) NationalNatural Science Foundation of China (NSFC 51431002) and the NSFCand the Research Grants Council (RGC) of Hong Kong Joint ResearchScheme (51361165101 and 5161101031)

Author contributions Liu Y prepared the figures tables organized thereferences and wrote the paper Zheng Y provided the overall concept andrevised the manuscript Hayes B helped with the standard developmentand revised the manuscript All authors participated in the discussion

Conflict of interest The authors declare that they have no conflict ofinterest

14copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Yang Liu received his bachelor degree in materials science and engineering from Harbin engineering University in 2013Then he continued his study as a PhD candidate in Prof Yufeng Zhengrsquos Lab in Peking University His research interestsare mainly focused on the corrosion study of absorbable metallic biomaterials as well as the development of new kind ofMg-based biomaterials

Yufeng Zheng obtained his PhD degree from Harbin Institute of Technology in 1998 He is the National OutstandingYouth and Yangtze River scholar of China His research interests are focused on the development of novel biomaterials andapplication and design of biomedical devices

Byron Hayes an over 35 year employee of WL Gore has been involved in the commercial development of multiple ab-sorbable polymeric implants since the late 1980s Hayes started his standards development activities with ASTM in 2000where he is actively developing standards for polymeric and metallic absorbable implants In 2010 Hayes also becameinvolved with ISO Technical Committees TC150 and TC194 and is now convener of working groups focused on cardiovas-cular and metallic absorbable implants

可降解可吸收再吸收mdashmdash哪个是描述最终被人体吸收生物材料的最好词汇刘洋1 郑玉峰1 拜伦海耶斯2

摘要 关于最终被人体吸收的植入材料领域内文献采用的英文修饰词长期以来混乱且不同不仅造成文献检索困难同时模糊了研究人员的研究边界 此领域在法律法规标准中统一用词的确定为领域内的科学研究产品销售及产品使用说明奠定了基础 我们基于化学生态学材料学生物学微生物学和药学立足于使用习惯法律标准和市场对领域内使用已久的典型修饰词ldquo生物可降解rdquoldquo再吸收rdquo和ldquo可吸收rdquo进行了讨论和解释 总的来说尽管目前绝大多数修饰语实际想表达的意思相同作者认为ldquo可吸收rdquo这一英文修饰语是最恰当的修饰词 同时我们提议进一步规范和统一该领域修饰词的使用

15 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

  • Degradable absorbable or resorbablemdashwhat is the best grammatical modifier for an implant that is eventually absorbed by the body
  • Abstract
  • INTRODUCTION
    • Current situation
    • Standards development in advance
      • TERMINOLOGY
        • Overview of utilization of the terms ldquodegradationrdquoldquobiodegradationrdquo and ldquodegradablerdquoldquobiodegradablerdquo
        • Overview of utilization of the terms ldquoabsorptionrdquoldquobioabsorptionrdquo and ldquoabsorbablerdquoldquobioabsorbablerdquo
        • Overview of utilization of the terms ldquoresorptionrdquoldquobioresorptionrdquo and ldquoresorbablerdquoldquobioresorbablerdquo
        • Utilization and comparison of the terms ldquobiodegradable metalsrdquo and ldquoabsorbable metallic materialsrdquo
        • Summary quantification of the common Terms
          • DISCUSSION
            • Expertise inherent biases
            • Connotation and extension of noun forms ldquobiodegradation bioabsorption and bioresorptionrdquo and adjectives ldquobiodegradable bioabsorbable and bioresorbablerdquo
              • CONCLUDING REMARKS
              • References
              • Acknowledgements

hydroxyester polymeric resins first became broadly avail-able from commercial suppliers To attain a preliminaryunderstanding of the scope of the confusion surroundinglabeling of these implants all any person has to do is to ini-tiate an Internet search whichmdashin order to confidently ad-dress a single simple conceptmdashbegins as a convoluted as-terisk-filled multi-line querySuch problem not only causes the difficulties when

searching on the Internet but also blurs the meaning andboundaries for researchers The absence of any universalterm recognition unnecessarily complicates communica-tion and confounds the selection of language for researchpapers legal descriptions international trade agreementsas well as the language used in an implantrsquos labelingmarketing and instructions for use Regardless of itsobviousness the problem has been a present and fullyrecognized problem that has persisted for decades Someintermittent attempts have been made by researchers tounify this disparate language into a single preferred term[67] As a result multiple purportedly ldquodefinitiverdquo papershave been published through the years However manyof these papers reflect the perspective of a single authoror society which often leads to conflicts between nomen-clature preferences [8ndash13] for even a single professionalsocietyrsquos breadth of view can be similarly limited by its ownscope Materials that are absorbed by the body do spanmany medical disciplines and the breadth of the technol-ogyrsquos applicability may contribute toward inhibiting anyone professional society from attempting a nomenclatureresolutionmdashas can be evidenced at numerous conferenceswhere one can observe an internal array of presentationsand posters with titles and terminology spanning most (ifnot all) the terms described in the 1st sentence

Standards development in advanceTypically absent from most of these historical nomencla-ture recommendations was any comprehensive consid-eration of the truly broader medical context containedwithin medical dictionaries and the relevant pharma-copeial andor implantable device-related standards [14]Early device and pharmaceutical companies regulatorsand any of the involved standards development organi-zations all had to consciously think about and decide onthe specific terms to include on their labels and in anygoverning standard regulation andor law With implantsthat are eventually absorbed by the body the selection andstandardization of terminology by the United States Phar-macopeia had already occurred and had fully focused onthe term ABSORBABLE by 1939 through its official des-

ignations of both ABSORBABLE and NONABSORBABLEsutures [1516] This same standardized language and clas-sifications remain in place today and have been for decadesembedded in both United States Federal laws and US-Foodand Drug Administration (FDA) regulations [17ndash19] (tobe discussed in later section) as well as in theUnited StatesBritish and European Pharmacopeias [20ndash22] Trying tochange or reverse what has already been both functionaland established in both regulations and law (now fordecades) is both difficult and a questionable undertakingRegardless of this historic and significant establishment ofABSORBABLE as standardized terminology it is possiblethat a simple lack of awareness andor rigorous review bythose involved in the broader research and clinical fieldsmay have become the source for the plethora of similar andanalogously utilized terms we routinely encounter todayThe advances in standard unification of the grammatical

modifier provide insights to the term usage in the researchof such field Due to the fact that many grammatical mod-ifiers have been used in this field for a long time typicalterms have been reviewed and explained interdisciplinaryin chemistry ecology materials science biology microbi-ology medicine and based on usage habits laws standardsand markets Furthermore the international unification ofthe grammatical term usage is proposed

TERMINOLOGYAs stated in the opening sentence multiple terms are be-ing utilized to describe the same general absorbable im-plant concept which includes absorbable bioabsorbableresorbable bioresorbable degradable biodegradable andpotentially other similar themes To provide an improvedunderstanding of the scope of current language diversityan overview of the usage of the aforementioned words wasundertaken to provide data that assisted in both confirmingand clarifying the scope of the problem The results are in-tended to provide a summary understanding of the scopeof confusion (ie how big the problem really is) so as tobetter facilitate identification of an appropriate remedy

Overview of utilization of the terms ldquodegrada-tionrdquoldquobiodegradationrdquo and ldquodegradablerdquoldquobiodegradablerdquoldquoDegradationrdquo and ldquobiodegradationrdquo are both used inpolymers and ceramics for a period of time and had beennoted by Prof D Williams as ldquothe process as deleteriouschange in the chemical structure physical propertiesor appearance of a materialrdquo according to the AmericanSociety for Testing and Materials (ASTM) [23] In theresearch of ldquobiorelatedrdquo polymers International Union

2copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

of Pure and Applied Chemistry (IUPAC) suggested thatldquodegradation indicates progressive loss of the performanceor of the characteristics of a substance or a devicerdquo [14] Itis also a general process since there can be degradationscaused by the action of water named ldquohydrodegradationrdquoor hydrolysis As for biorelated polymers the degradationprocess is limited to macromolecule cleavage and molarmass decrease which distinguishes the degradation ofbiorelated polymer from fragmentation and disintegrationillustrated in bioceramics The term ldquodegradationrdquo wasformerly used in bioceramics by Prof L Hench to describethe decomposition process of calcium phosphate ceramicswhich was followed by host response and tissue repair [3]Thus the definition of ldquodegradationrdquo used in polymers andceramics fields could be interpreted as different inferringmore specifically to chemical processes for bio-relatedpolymers while referring to physical break down from theview of bio-ceramics researchersAs for the term ldquobiodegradationrdquo it is not the simple

addition of the prefix ldquobio-rdquo to ldquodegradationrdquo Fig 1 de-scribes the common usage of ldquobiodegradationrdquo currentlyThe word was firstly introduced as the consumption ofmaterial by bacteria fungi or other biological means inecology waste management biomedicine and even naturalenvironment [24] Some kinds of environmentally friendlyproducts also undergo such process as they can be degraded

by microorganisms and do no harm to the environmentHowever some researchers studying polymers and ceram-ics have defined a more specific scope for ldquobiodegradationrdquoFor polymers especially biorelated polymers the differ-ence between ldquobiodegradationrdquo and ldquodegradationrdquo lies inthe involvement of enzymatic process [1425]mdasha distinc-tion that can be problematic if both modes are active in animplantrsquos degradation process Moreover IUPAC stressedthe importance of proved degradation mechanisms whenusing ldquobiodegradationrdquo otherwise ldquodegradationrdquo should beused instead of ldquobiodegradationrdquo In general ldquodegradationrdquoand ldquobiodegradationrdquo both refer to the chain scission orchain cleavage Nevertheless the meaning of ldquobiodegra-dationrdquo in bioceramics is different since there is no suchprocess as chain scission The degradation process ofso-called ldquoresorbable ceramicsrdquo is claimed to involve eitherdecomposition to small particles as well as dissolved ionswhich participate in the enzymecell mediated reactionand new tissue forms [326ndash28] Despite the exact degra-dation process still needs further investigations the wordldquodegradationrdquo used for ldquoresorbablerdquo ceramics expressesmultiple meanings covering both chemical and physicalreactions in physiological environment such as hydrolysisdecomposition and debris formation According to ProfD Williams the recommended definition of ldquobiodegrada-tionrdquo is the gradual breakdown of a material mediated by

Figure 1 Common use of biodegradation currently

3 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

specific biological activity [23] Another definition as thebiomaterial or medical device involving loss of their in-tegrity or performance when exposed to a physiological orsimulated environment which existed in some ISO Techni-cal Report was not recommended since no specific respectto biological activity mentioned [23]Beyond the category of biomaterials ldquodegradablerdquo in

pure chemistry was defined as qualifier to a substance thatcan undergo physical andor chemical deleterious changesof some properties especially of integrity under stressconditions [14] Thus degradable polymer is consideredwith macromolecules being able to undergo chain scis-sions resulting in a decrease of molar mass [14] BesidesASTM made a standard definition on ldquodegradablerdquo in thescope of soil rock and contained fluids as ldquoin erosioncontrol decomposes under biological chemical processesor ultraviolet stresses associated with typical applicationenvironmentsrdquo [29] Despite no specific emphasis onbiomaterials numerous publications used ldquodegradablerdquo to

modify metals polymers or compounds in tissue engineer-ing drug delivery and gene delivery [30ndash35] Meanwhilein some ASTM standard specifications the definition ofthe adjective ldquobiodegradablerdquo is given as capable of de-composing under natural conditions into elements foundin the nature [36ndash42] The active ASTM entries currentlywith ldquobiodegradationrdquo ldquodegradablerdquo and ldquobiodegradablerdquoin the title are summarized in Table 1 The adoptionsof ldquobiodegradationrdquo ldquodegradablerdquo and ldquobiodegradablerdquoby ASTM are historical generally in the classification ofecology or environmental protectionWhile the above listing provides evidence that the usage

of the term biodegradable is broad it is particularly notablethat almost all of the listed standards are not relevant toimplantable devices Instead the listing primarily reflectsusage directed toward the environmental degradation as-pect that is most commonly recognized within the broadernon-medical oriented population ASTM-F1635 a stan-dard specifically centered on the hydrolytic degradation

Table 1 Summary of the terms ldquobiodegradationrdquo ldquodegradablerdquo and ldquobiodegradablerdquo being utilized in ASTM titles (not limited to implant)

Terminology ASTM titles

ASTM D5864-11 Standard Test Method for Determining Aerobic Aquatic Biodegradation of Lubricants or TheirComponents

ASTM D6954-04(2013) Standard Guide for Exposing and Testing Plastics that Degrade in the Environment by aCombination of Oxidation and Biodegradation

ASTM D5511-12 Standard Test Method for Determining Anaerobic Biodegradation of Plastic Materials Under High-SolidsAnaerobic-Digestion Conditions

ASTM D6139-11 Standard Test Method for Determining the Aerobic Aquatic Biodegradation of Lubricants or TheirComponents Using the Gledhill Shake Flask

ASTM D7991-15 Standard Test Method for Determining Aerobic Biodegradation of Plastics Buried in Sandy MarineSediment under Controlled Laboratory Conditions

ASTM D5338-15 Standard Test Method for Determining Aerobic Biodegradation of Plastic Materials Under ControlledComposting Conditions Incorporating Thermophilic Temperatures

ASTM D6691-09 Standard Test Method for Determining Aerobic Biodegradation of Plastic Materials in the MarineEnvironment by a Defined Microbial Consortium or Natural Sea Water Inoculum

ASTM D5526-12 Standard Test Method for Determining Anaerobic Biodegradation of Plastic Materials Under AcceleratedLandfill Conditions

ASTM D7475-11 Standard Test Method for Determining the Aerobic Degradation and Anaerobic Biodegradation of PlasticMaterials under Accelerated Bioreactor Landfill Conditions

Biodegradation

ASTM D5988-12 Standard Test Method for Determining Aerobic Biodegradation of Plastic Materials in Soil

ASTM F1635-11 Standard Test Method for in vitro Degradation Testing of Hydrolytically Degradable Polymer Resinsand Fabricated Forms for Surgical Implants

ASTM D7444-11 Standard Practice for Heat and Humidity Aging of Oxidatively Degradable PlasticsDegradable

ASTM D3826-98(2013) Standard Practice for Determining Degradation End Point in Degradable Polyethylene andPolypropylene Using a Tensile Test

ASTM D7665-10(2014) Standard Guide for Evaluation of Biodegradable Heat Transfer Fluids

ASTM D8029-16 Standard Specification for Biodegradable Low Aquatic Toxicity Hydraulic FluidsBiodegradable

ASTM D7044-15 Standard Specification for Biodegradable Fire Resistant Hydraulic Fluids

4copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

testing of absorbable polyesters is the sole listed standardfrom ASTM Committee F04mdashMedical and Surgical Im-plants and thereby is directly relevant to implantable de-vices However this standard utilizes the term degradeand its derivatives specifically in reference to the process ofdegradation that occurs as a result of ester hydrolysis Con-versely the same standard uses the term absorbable to de-scribe a class of implants that are eventually absorbed by thebody which it defines as ldquoabsorbable adjmdashin the bodymdashaninitially distinct foreign material or substance that either di-rectly or through intended degradation can pass through orbe assimilated by cells andor tissuerdquo

Overview of utilization of the terms ldquoabsorptionrdquoldquobioab-sorptionrdquo and ldquoabsorbablerdquoldquobioabsorbablerdquoThe term ldquoabsorptionrdquo was recognized by IUPAC as theprocess of penetration and diffusion of a substance (ab-sorbate) into another substance (absorbent) as a result ofthe action of attractive phenomena The IUPAC defini-tion is within the scope of chemistry As for biomaterialsProf D Williams adopted the definition in Dorland Medi-cal Dictionary as the uptake of substances into or across tis-sues [23] For this kind of definition ldquoabsorptionrdquo empha-sizes the interaction of materials and human or animal tis-sue The same connotation is shared by its derivative wordsldquoabsorbablerdquo and ldquobioabsorbablerdquo as capable of being de-graded or dissolved and subsequently metabolized withinan organism [23] Besides the prefix ldquobio-rdquo is abridged as

it is redundant in the field of implantation [43] ASTM hasmade standard definition on ldquoabsorbablerdquo in the field of ab-sorbable polymers as well as absorbablemetals which it de-fines as ldquohellip an initially distinct foreign material or substancethat either directly or through intended degradation can passthrough or be metabolized or assimilated by cells andor tis-sue in the bodyrdquo [43] Table 2 summarizes the currently ac-tive ASTM standards and both United States and EuropeanPharmacopeia implantable device monographs that utilizethe word ldquoabsorbablerdquo in the title Distinctly different fromldquobiodegradablerdquo the utilization of ldquoabsorbablerdquo displays adistinct preference for use in describing this particular classof biomedical materials and devicesAs can be observed in both Table 1 and Table 3 the

well-established terminology for describing sutures is verybroadly based on the term absorbable with historicalapplication of the term to the original gut sutures andeven extending to permanent sutures through the ldquononab-sorbablerdquo descriptorAside from the language of standards organization the

terminology utilized by regulatory agencies is also of par-ticular relevance Through multiple laws and regulationsthe US-FDA is authorized to evaluate medical device man-ufacturers and their products The US Code of FederalRegulations (CFRs) that is specific to sutures legally de-scribes those regulated devices based on composition andthen designates both their product class and needs to meetUSP requirements While Table 3 demonstrates both a US-

Table 2 ldquoAbsorbablerdquo utilized in title entries for implantable device related standards

Terminology Title entries

ISOTS 171372014 Cardiovascular implants and extracorporeal systemsmdashCardiovascular absorbable implants

ISOTR 371372014 Biological evaluation of medical devicesmdashGuidance for absorbable implants

ASTM F3036-13 Standard Guide for Testing Absorbable Stents

ASTM F2902-16 Standard Guide for Assessment of Absorbable Polymeric Implants

ASTM F2502-16 Standard Specification and Test Methods for Absorbable Plates and Screws for Internal Fixation Implants

ASTM F1983-14 Standard Practice for Assessment of Selected Tissue Effects of Absorbable Biomaterials for Implant Applications

ASTM F3160-16 Standard Guide for Metallurgical Characterization of Absorbable Metallic Materials for Medical Implants

United States Pharmacopoeia (USP 39NF 34) monographldquoAbsorbable Surgical Suturerdquo

United States Pharmacopoeia (USP 39NF 34) monographldquoNonabsorbable Surgical Suturerdquo

European Pharmacopoeia (88)ldquoSterile non-absorbable suturesrdquo ndash 1118

European Pharmacopoeia (88)ldquoSterile synthetic absorbable braided suturesrdquo - 1122

Absorbable

European Pharmacopoeia (88)Sterile synthetic absorbable monofilament sutures ndash 1123

5 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Table 3 US-FDA suture product codes and accompanying citation of US CFRsa)

Suture name Regulation Product code

Absorbable polydioxanone surgical (PDS) suture 21 CFR8784840 NEW

Absorbable poly(glycolideL-lactide) surgical suture 21 CFR8784493 GAM

Absorbable gut suture 21 CFR8784830 GAL

Nonabsorbable poly(ethylene terephthalate) suture 21 CFR8785000 GAT

Nonabsorbable polypropylene surgical suture 21 CFR8785010 GAW

Nonabsorbable polyamide surgical suture 21 CFR8785020 GAR

Natural nonabsorbable silk surgical suture 21 CFR8785030 GAP

Stainless steel surgical suture 21 CFR8784495 GAQ

Nonabsorbable expanded polytetrafluoroethylene (ePTFE)surgical suture

21 CFR8785030 NBY

a) Note this table selects abbreviated results obtained from online search for the implant device term ldquosuturerdquo that was conducted on 6 Aug 2016 athttpwwwaccessdatafdagovscriptscdrhcfdocscfPCDclassificationcfm

FDA and a US Code of Federal Regulations preference forabsorbable terminology when referring to sutures Table4 shows an expansion of that preference to include a to-tal of 30 absorbable implant product classifications each ofwhich is assigned to a relevant Federal regulation that uti-lizes the term ldquoabsorbablerdquoIn short ldquoabsorbablerdquo is both a historically well estab-

lished and currently relevant term in both the regulationand standardization of implants that are intentionally ab-sorbed by the body

Overview of utilization of the terms ldquoresorptionrdquoldquobiore-sorptionrdquo and ldquoresorbablerdquoldquobioresorbablerdquoIn the scope of chemistry the term ldquoresorptionrdquo was used toillustrate the total elimination of a substance from its initialplace caused by physical andor chemical phenomena [14]Besides the understanding from pure chemistry ldquoresorp-tionrdquo is more recognized involved in the metabolic activi-ties in vivo For example ldquoresorptionrdquo is considered as theldquoabsorptionrdquo into the circulatory system of cells or tissuewhich usually includes bone resorption tooth resorptionand vanishing twin [44] In the biomedical scope Prof DWilliams used themeaning in DorlandMedical Dictionaryas ldquolysis and assimilation of a substance as of bonerdquo [23]ldquoBioresorptionrdquo is more common when describing the invivo process of a certain foreign material The ISO definedldquobioresorptionrdquo as a process by which biomaterials are de-graded in the physiological environment and the by-prod-uct are eliminated or completely bioabsorbed [23] Thusaccording to this interpretation the bioresorption processincludes material removal in vivo either by cellular activ-ity or not Conversely Taberrsquos Cyclopedic Medical Dictio-nary [45] describes the term ldquoresorbrdquo as themeaning ldquoto ab-

sorb againrdquomdashsomething that live tissue does but not some-thing any implant is known to domdashbe it permanent or ab-sorbableAs for the adjectives ldquobioresorbablerdquo and ldquoresorbablerdquo

there is no difference when used to describe a kind of ma-terials which have the ability of resorption This is ascribedto the fact that ldquoresorptionrdquo itself already has been well rec-ognized as a biological process [23] Currently there is noASTM entries used ldquoresorbablerdquo or ldquobioresorbablerdquo in thetitle

Utilization and comparison of the terms ldquobiodegradablemetalsrdquo and ldquoabsorbable metallic materialsrdquoldquoBiodegradablemetalsrdquo generally include themetalsMg Feand Zn and their alloys and composites They can be de-fined as metals that assist with tissue healing and are thenexpected to gradually corrode and release corrosion prod-ucts in vivowith an appropriate host response and then dis-solve completely with no implant residues [46] As a resultand different from traditional ldquobio-inertrdquometallic biomate-rials (eg Ti and Co based alloys) that release limited cor-rosion products [47] metabolic reactions besides inflam-mation can be expected to occur between the biodegrad-able metal and the host body after implantation Addition-ally the corrosion-based degradation mechanism of thesematerials is inherently different from that of either bioce-ramics or polymers which has resulted in limited to nostandardized guidance available from either ASTM or ISOInstead of the term ldquobiodegradable metalrdquo the recently

published and first absorbable metal related standardASTM F3160 utilizes the more inclusive word ldquoabsorbablerdquowithin the phrase ldquoabsorbable metallic materialsrdquo andagain defines the term as ldquohellip an initially distinct foreign

6copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Table 4 US-FDA absorbable implant related product codes descriptions and accompanying CFRsa)

Product code Device Device class Regulation number Regulation description

OMT Absorbable lung biopsy plug 2 [8784755] Absorbable lung biopsy plug

LMF Agent absorbable hemostatic collagen based 3 [8784490] Absorbable hemostatic agent and dressing

LMG Agent absorbable hemostatic non-collagen based 3 [8784490] Absorbable hemostatic agent and dressing

MRY Appliances and accessories fixation bone absorbable singlemultiple component 2 [8883040] Smooth or threaded metallic bone fixation fastener

PBQ Fixation non-absorbable or absorbable for pelvic use 2 [8844530] Obstetric-gynecologic specialized manual instrument

HQJ Implant absorbable (scleral buckling methods) 2 [8863300] Absorbable implant (scleral buckling method)

OWT Mesh surgical absorbable abdominal hernia 2 [8783300] Surgical mesh

OXM Mesh surgical absorbable fistula 2 [8783300] Surgical mesh

OXI Mesh surgical absorbable large abdominal wall defects 2 [8783300] Surgical mesh

OXL Mesh surgical absorbable organ support 2 [8783300] Surgical mesh

OWW Mesh surgical absorbable orthopaedics reinforcement of tendon 2 [8783300] Surgical mesh

OXF Mesh surgical absorbable plastic and reconstructive surgery 2 [8783300] Surgical mesh

OXC Mesh surgical absorbable staple line reinforcement 2 [8783300] Surgical mesh

OWZ Mesh surgical absorbable thoracic chest wall reconstruction 2 [8783300] Surgical mesh

OWU Mesh surgical non-absorbable diaphragmatic hernia 2 [8783300] Surgical mesh

OWR Mesh surgical non-absorbable facial implants for plastic surgery 2 [8783300] Surgical mesh

OXJ Mesh surgical non-absorbable large abdominal wall defects 2 [8783300] Surgical mesh

OWX Mesh surgical non-absorbable orthopaedics reinforcement of tendon 2 [8783300] Surgical mesh

OXG Mesh surgical non-absorbable plastic and reconstructive surgery 2 [8783300] Surgical mesh

OXD Mesh surgical non-absorbable staple line reinforcement 2 [8783300] Surgical mesh

OXA Mesh surgical non-absorbable thoracic chest wall reconstruction 2 [8783300] Surgical mesh

LBP Replacement ossicular (stapes) using absorbable gelatin material 2 [8743450] Partial ossicular replacement prosthesis

OLL Septal staplerabsorbable staples 2 [8784750] ImplanTABLE staple

MNU Staple absorbable 2 [8883030] Singlemultiple component metallic bone fixationappliances and accessories

GAK Suture absorbable 2 [8784830] Absorbable surgical gut suture

GAL Suture absorbable natural 2 [8784830] Absorbable surgical gut suture

HMO Suture absorbable ophthalmic 3

GAN Suture absorbable synthetic 2 [8784830] Absorbable surgical gut suture

GAM Suture absorbable synthetic polyglycolic acid 2 [8784493] Absorbable poly(glycolidel-lactide) surgical suture

NEW Suture surgical absorbable polydioxanone 2 [8784840] Absorbable polydioxanone surgical suture

a) Note the results obtained from online search for the device term ldquoabsorbablerdquo that was conducted on 6 Aug 2016 at httpwwwaccessdatafdagovscriptscdrhcfdocscfPCDclassifica-tioncfm

7 copy

ScienceChina

Pressand

Springer-VerlagBerlin

Heidelberg 2017

SCIENCECH

INAMaterials

REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

material or substance that either directly or through in-tended degradation can pass through or be metabolized orassimilated by cells andor tissuerdquo The standardrsquos nomen-clature appendix further elaborates on its preference forldquoabsorbablerdquo since the prefix ldquobio-rdquo is redundant in thecontext of implant applications [43]Clearly these two terms of ldquobiodegradable metalsrdquo and

ldquoabsorbable metallic materialsrdquo share the same connota-tion which defines the completemission of an intentionallydegradable material when implanted in vivo In the contextof biodegradable metalsabsorbable metallic materialsthe process includes the corrosion caused by body fluida host response caused by corrosion products followedby dissolutionabsorption and finally improved tissuehealing The ldquobiodegradationrdquo instead of ldquobiocorrosionrdquois used to distinguish this new kind of metals which canfully dissolve in vivo with no implant residues Besidesbiodegradation process the following dynamic process ofdissolutionabsorption also starts in vivo For exampledissolved Mg2+ is considered to enhance the integrin me-diated human-bone-derived cell adhesion and affect newbone formation [48] The metabolic reaction is also crucialand even more important for biodegradable metals as it ishelpful It is another distinction from traditional metalsused for biomedical application In fact the different usagehabit forming of ldquobiodegradablerdquo or ldquoabsorbablerdquoldquobioab-sorbablerdquo may be more related with the study field theresearchers in Taking the ldquoabsorbablerdquo metallic stent asan example (Fig 2) once the ldquoabsorbablerdquo metallic stentwas implanted into blood vessel ldquocorrosionrdquo of biometal

begins The corrosion products including debris hydro-gen (for Mg-based metals) metallic ions and hydroxylconvert the local environment and diffuse into the bloodvessel wall Some corrosion products can be biologicallybeneficial For instance the diffused and absorbed Zn2+

can potentially play a positive role in dealing with athero-sclerosis [49] Along with the corrosion process healingprocesses such as endothelialization may become en-hanced In summary and within the context of absorbablemetals the adjectives ldquodegradablerdquo and ldquoabsorbablerdquo referto the nature of the biodegradation products of the mate-rialdevice being metabolically absorbed an attribute ofthe host (animal or human body) regardless of whetherthe implant degrades corrodes hydrolyzes or dissolves[50ndash52]

Summary quantification of the common TermsFig 3a shows preliminary searching results in Webof Knowledge using ldquodegradablerdquo ldquoabsorbablerdquo or ldquore-sorbablerdquo along with ldquomaterialrdquo as key words Theutilization of ldquodegradablerdquo is a bit more frequently thanldquoabsorbablerdquo but that of ldquoresorbablerdquo steps down Mean-while the counterpart searching result when using ldquobiordquo asprefix to the adjectives along with ldquomaterialrdquo as keywordsare presented in Fig 3b ldquoBiodegradable materialrdquo is themost common utilization which holds 91 among the ex-pression approach This is also due to the fact that besidesthe common utilization in biomaterials ldquobiodegradablerdquois also used in a wide range of applications such as cleanenvironment and ecology [5354]

Figure 2 Different point of views on the biodegradationabsorption process

8copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Figure 3 Searching results in Web of Knowledge from all databases (a) with the total searched publication numbers by ldquodegradablerdquo+ ldquomaterialrdquoldquoabsorbablerdquo+ ldquomaterialrdquo and ldquoresorbablerdquo+ ldquomaterialrdquo as 100 (b) the total searched publication numbers by ldquobiodegradablerdquo+ ldquomaterialrdquo ldquobioab-sorbablerdquo+ ldquomaterialrdquo and ldquobioresorbablerdquo+ ldquomaterialrdquo as 100

DISCUSSION

Expertise inherent biasesAs previously mentioned biomaterial is an interdiscipli-nary field fascinating researchers with specialty from dif-ferent backgrounds Different backgrounds as well as dif-ferent research point of interests may be one of the reasonsfor using different terminologies Materials scientists tendto focus on the materialdevice itself leading to their usageof ldquobiodegradablerdquo to illustrate what happens to the deviceThey pay more attention to the process such as hydroly-sis corrosion debris degradation products and the changeof surface morphology resulting in the researching inter-ests of ldquomaterial biodegradationrdquo In contrast surgeons andbiomedical researchers tend to be concerned more on thehost response and healing process They are curious aboutthe absorption of various degradation products of the im-planted materialdevice and related metabolism mecha-nism and thereby prefer to use the term ldquoabsorbablerdquo toillustrate what happens to the device As known somema-terials may only undergo biodegradation but the corrosionproducts still have no influence on the metabolic activitiesFor example cellulose is considered as ldquodietary fiberrdquowhichcannot be digested and absorbed by human body but is be-nign for human body [55] Some coating tablets for drug ordrug delivery systems made from cellulose and its deriva-tives are quite frequently utilized or investigated [5657]The polymer and derivatives of cellulose can only be de-graded but not be absorbed by human body [58] For suchmaterials the adjective ldquoabsorbablerdquo or ldquobioabsorbablerdquo isnot appropriateOverall once the materialsdevices are implanted into

the human body the ldquobiocorrosionrdquobiodegradationrdquoprocess happens immediately no matter to what degreeat the same time the host will biologically response to the

corrosiondegradation products through the absorptionmetabolism and excretion processes So for the samestory the majority of materials scientists would report itby ldquobiodegradabledegradationrdquo way whereas the majorityof medical doctors would report it by ldquoabsorbableab-sorptionrdquo way In nature the two terms ldquobiodegradablemetalsrdquo and ldquoabsorbable metallic materialsrdquo share the sameconnotation and are mutually replaceable

Connotation and extension of noun forms ldquobiodegradationbioabsorption and bioresorptionrdquo and adjectivesldquobiodegradable bioabsorbable and bioresorbablerdquoThe three noun forms of the terms illustrate the processwhile their adjectival derivatives were used to describe thegroup of materials with such certain capabilities For thestudy on biomaterials polymer researchers use ldquodegrada-tionbiodegradationrdquo when there is proved chain scissionprocess Besides they differentiate ldquobiodegradationrdquo andldquodegradationrdquo by confirmed metabolic activities betweenthe materials and cells or tissues Regarding to the fouradjectives ldquobiodegradablerdquo ldquobioabsorbablerdquo and ldquobiore-sorbablerdquo the term ldquobiocorrodiblerdquo is only used in scientificpapers on iron based materials and some patents on mag-nesium based materials The common usage of termsldquobiodegradablerdquo ldquobioabsorbablerdquo and ldquobioresorbablerdquo withrespect to the biomaterial research area is shown in Table 5The results reveal a widespread usage of ldquobiodegradablerdquo inboth polymers and magnesium based metals Varies typesof materials were reported as biomaterials Besides thereare also reports of ldquobiodegradablerdquo polymers for ecologyand environmental protection which indicates a furtherusage scope of ldquobiodegradablerdquo not only for implants anddevices Besides ldquobioresorbablerdquo is also utilized in all theresearch fields of polymers ceramics andmetals Howeverno current work used ldquobioabsorbablerdquo as grammatical

9 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Table 5 Current reported usage of terms ldquobiodegradablerdquo ldquobioabsorbablerdquo and ldquobioresorbablerdquoTerminology Category Materials Applications

PLA-PEG-biotin PLGA Controlled cell engineering [5960]Porous PLGA Tissue engineering [61ndash63]

PLGA-PEG-PLGA Injective thermosensitive hydrogel [64]PLGA Nerve guidance [65]

Fibronectin (Fn)-coated PLLA P(LLA-CL) Enhanced growth of endothelial cells [6066]PEG tethered PPF [67]

PDMS Drug delivery [68]PGA Tissue engineering [69]

Undefined Coronary stent [70ndash72]PGA Joint resurfacing [73]

Polymers

PHA Ecology and environmental protection [74]CaO-P2O5 glass Bone regeneration [75]β-Whitlockite Bone regeneration [76]

Calcium phosphate hydraulic cement Bone regeneration [77]Calcium

phosphate glass ceramicsBone regeneration [78]

Ceramics

CaO-SiO2-B2O3 glass-ceramics Bone regeneration [79]Pure Mg Implant material [80]

Mg-Ca-based Bone regeneration [81ndash84]Mg-Zn-based Bone regeneration [338586]Mg-Sr-based Bone regeneration [87ndash89]Mg-RE-based Vascular stent [90ndash92]

Mg and its metals

Mg-Ag-based [93]Zn-Mg Zn-Ca Zn-Sr [9495]Zn and its metals Zn-Mg-Sr [96]

Fe [9798]

Biodegradable

Fe and its metals Fe-Mn [99]PLLA PLG PGA Molecule delivery [100]

PGA Suture [101]Undefined Drug-eluting stent [102103]

PLA Neuron attachment [104]Polymers

PLA and PCL reinforced with PGA fibers Bile duct patch [105]Mg-RE based Coronary stent [106ndash109]

Binary Mg alloys [110]Mg and its metalsMg-Al-based [111112]

Zn and its metals Pure Zinc [113114]Fe and its metals Nitrided iron [115]

PLDLA Transforaminal lumbar interbody fusion [116]Alkylene bis(dilactoyl)-methacrylate modified polymer Bone screw augmentation [117]

Undefined Coronary stent [118]PHB Mandibular defects regeneration [119]HA Bone regeneration [120]Ceramics Calcium phosphate [121122]

MgNd2 Stent material [123]Porous Mg Bone substitute [124]Mg-RE Coronary stent [125]Mg-Ca Orthopedic application [126]

Mg and its metals

Mg-based Finite element analysis [127]

Bioabsorbable

Fe and its metals Pure Fe [128]

10copy

ScienceChina

Pressand

Springer-VerlagBerlin

Heidelberg 2017

REVIEWSCIENCE

CHINA

Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

modifier to bioceramics In addition as previouslyillustrated the prefix ldquobiordquo of ldquobioabsorbablerdquo and ldquobiore-sorbablerdquo are abridged hereafter discussion will concen-trate on ldquobiocorrodiblerdquo ldquobiodegradablerdquo ldquoabsorbablerdquo andldquoresorbablerdquoSince absorbable technologies are increasingly utilized

in numerous new and broader implant applications it be-comes more important to not acquiesce in addressing his-torical problems and instead actively move forward towardutilizing standardized language that is both technically ac-curate and unified in itsmeaning Preferred language needsto accurately communicate the concept To achieve the uni-fying goal of harmonized terminology themedical and sci-entific communities need to not solely look at materialschemistry or even biomaterials alone but to instead lookat term selection both across and within the context of thebroader medical disciplinemdashthe location where the resultsof implant technology development actually reaches themarketplace where therapies are brought to those in needNomenclature solutions need to both understand and re-spond to the context of terms across adjacent technologieswhich means to address needs from the perspectives of thebiomaterial researcher the deviceproduct developer thesurgeonclinician user the regulator and last but not leastthe patientgeneral public who is the direct beneficiary ofthe developed technologyA better understanding of these terminologies is neces-

sary and beneficial to the field Therefore the definitionson ldquodegradablerdquo ldquoabsorbablerdquo ldquoresorbablerdquo and relatedterms proposed by different organizations in differentfields have been summarized and discussed with the con-notation and extension of each term being compared andthe criteria being proposed

CONCLUDING REMARKSHerein given both the searching problem on the Internetand ambiguity in meanings the usage of grammaticalmodifiers to describe biomaterials that is eventually ab-sorbed by human body has been enumerated based onusage habits laws standards and markets In summaryldquodegradablerdquoldquobiodegradablerdquo are the most frequently usedgrammatical modifier not only in metals but also poly-mers as such kind of biomaterials ldquoBiodegradationrdquo andldquobiodegradablerdquo define the change of the materialdevicewell in the research of biomaterials but they are alsoadopted in other fields such as ecology and environmentalprotection Meanwhile ldquoresorbablerdquoldquobioresorbablerdquo havelong been recognized in the biological research and theldquoresorptionrdquo itself has been widely accepted as a biological

reaction The utilization of ldquoresorbablerdquoldquobioresorbablerdquowas found to be not as frequent as the counterpartsldquodegradablerdquoldquobiodegradablerdquo and ldquoabsorbablerdquoldquobioab-sorbablerdquo Such usage is accurate for osteoclast driven boneresorption but is inappropriate for implants that do notcarry the potential to grow back into their original formOtherwise despite it is not the most frequently used termldquoabsorbablerdquoldquobioabsorbablerdquo concentrates more on thehost metabolism to the foreign biodegradation productsof the implanted materialdevice compared with ldquodegrad-ablerdquoldquobiodegradablerdquo ldquoAbsorbablerdquo is defined in the scopeof biomaterials by different organizations and their publi-cations and also adopted by ASTM to illustrate ldquoabsorbablepolymerrdquo It is the most historically established the mostbroadly applicable (includes dissolvable devices that donot degrade) the most specific to medical applicationsand is the formal legal descriptor for most implant devicesConsidering the usage history common utilization in lawand standards as well as the scientific meaning in essenceldquoabsorbablerdquo can be better among other grammaticalmodifiers for description of an implant that is eventuallyabsorbed by the body which is recommended by theauthors for a further internationally-unified usage

Received 28 February 2017 accepted 27 March 2017published online 26 April 2017

1 Mackenzie D The history of sutures Med Hist 1973 17 158ndash1682 Hench LL Bioceramics J Am Ceramic Soc 2005 81 1705ndash17283 Hench LL Bioceramics from concept to clinic J AmCeramic Soc

1991 74 1487ndash15104 Windhagen H Radtke K Weizbauer A et al Biodegradable

magnesium-based screw clinically equivalent to titanium screw inhallux valgus surgery short term results of the first prospectiverandomized controlled clinical pilot study BioMed Eng OnLine2013 12 62

5 Schildwaumlchter M Biotronik announces CE mark for magmaristhe first clinically-proven bioresorbable magnesium scaffoldhttpwwwmagmariscomennewsroomjune-15-2016

6 Shalaby SW Burg KJL Bioabsorbable polymers update degrada-tion mechanisms safety and application J App Biomater 1995 6219ndash221

7 Vert M Li SM Spenlehauer G et al Bioresorbability and biocom-patibility of aliphatic polyesters J Mater Sci-Mater Med 1992 3432ndash446

8 Vert M Degradable and bioresorbable polymers in surgery and inpharmacology beliefs and facts J Mater Sci-Mater Med 2009 20437ndash446

9 Benicewicz BC Hopper PK Review polymers for absorbablesurgical suturesmdashPart I J Bioactive Compatible Polym 1990 5453ndash472

10 Barrows HT Synthetic bioabsorbable polymers In Szycher M(Ed) High Performance Biomaterials A Complete Guide toMed-ical and Pharmceutical Applications Boca Raton CRC PRESS1991 243ndash257

11 Weiler A Hoffmann RFG Staumlhelin AC et al Biodegradable

11 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

implants in sports medicine the biological base Arthroscopy-JArthroscopic Related Surgery 2000 16 305ndash321

12 Ikada Y Tsuji H Biodegradable polyesters for medical and ecolog-ical applications Macromol Rapid Commun 2000 21 117ndash132

13 Ashammakhi N Peltoniemi H Waris E et al Developments incraniomaxillofacial surgery use of self-reinforced bioabsorbableosteofixation devices Plast Reconstr Surg 2001 108 167ndash180

14 Vert M Doi Y Hellwich KH et al Terminology for biorelatedpolymers and applications (IUPACRecommendations 2012) PureAppl Chem 2012 84 377ndash410

15 The United States Pharmacopeial Convention The Second Sup-plement to the Pharmacopeia of the United States of America 11thdecennial revision (USP XI-1939 Supplement) 1939

16 Truhlsen SM The recession operation histopathologic responseand suture reaction and absorption Trans Am Ophthalmol Soc1965 63 626ndash677

17 USP in US Law httpwwwusporgprintabout-usplegal-recog-nitionusp-us-law

18 USP develops and publishes standards for drug substances drugproducts excipients and dietary supplements in the United StatesPharmacopeia-National Formulary (USP-NF)

19 United States Public Law 94-295 197620 United States Pharmacopeia httpwwwusporg21 British Pharmacopeia httpswwwpharmacopoeiacom22 European Pharmacopoeia httponlinepheurorgENentryhtm23 Williams DF The Williams Dictionary of Biomaterials Liverpool

Liverpool University Press 199924 httpsenwikipediaorgwikiBiodegradation25 Jones RG Kahovec J Stepto R et al Compendium of Polymer

Terminology and Nomenclature IUPAC Recommendations 2008Cambridge RSC Publishing 2009

26 Higashi S Yamamuro T Nakamura T et al Polymer-hydroxyap-atite composites for biodegradable bone fillers Biomaterials 19867 183ndash187

27 de Groot K Bioceramics of Calcium Phosphate Boca Raton CRCPress 1983

28 Hollinger JO Battistone GC Biodegradable bone repair materialssynthetic polymers and ceramics ClinOrthopRelat Res 1986 207290ndash306

29 ASTMD653-14 Standard Terminology Relating to Soil Rock andContained Fluids ASTM International West Conshohocken PA2014 httpswwwastmorgStandardsD653htm

30 Witte F Hort N Vogt C et al Degradable biomaterials based onmagnesium corrosion Curr Opin Solid State Mater Sci 2008 1263ndash72

31 Lynn DM Langer R Degradable poly(β-amino esters) synthesischaracterization and self-assemblywith plasmidDNA JAmChemSoc 2000 122 10761ndash10768

32 Cima LG Vacanti JP Vacanti C et al Tissue engineering by celltransplantation using degradable polymer substrates J BiomechEng 1991 113 143ndash151

33 Zhang S Zhang X Zhao C et al Research on an Mg-Zn alloy as adegradable biomaterial Acta Biomater 2010 6 626ndash640

34 Anseth KS Metters AT Bryant SJ et al In situ forming degradablenetworks and their application in tissue engineering and drug de-livery J Control Release 2002 78 199ndash209

35 Forrest ML Koerber JT Pack DW A degradable polyethyleniminederivative with low toxicity for highly efficient gene delivery Bio-conjugate Chem 2003 14 934ndash940

36 ASTM E2747-11 Standard Specification for Evaluation and Selec-tion of Onsite Offices for Environmentally Sustainable MeetingsEvents Trade Shows and Conferences ASTM International

West Conshohocken PA 2011 httpswwwastmorgStan-dardsE2747htm

37 ASTM E2745-11 Standard Specification for Evaluation andSelection of Audio Visual (AV) and Production for Environ-mentally Sustainable Meetings Events Trade Shows and Con-ferences ASTM International West Conshohocken PA 2011httpswwwastmorgStandardsE2745htm

38 ASTM E2746-11 Standard Specification for Evaluation andSelection of Communication and Marketing Materials for En-vironmentally Sustainable Meetings Events Trade Shows andConferences ASTM International West Conshohocken PA 2011httpswwwastmorgStandardsE2746htm

39 ASTM E2741-11 Standard Specification for Evaluation and Se-lection of Destinations for Environmentally Sustainable MeetingsEvents Trade Shows and Conferences ASTM InternationalWest Conshohocken PA 2011 httpswwwastmorgStan-dardsE2741htm

40 0 ASTM E2773-11 Standard Specification for Evaluation andSelection of Food and Beverage for Environmentally SustainableMeetings Events Trade Shows and Conferences ASTM Interna-tional West Conshohocken PA 2011 httpswwwastmorgStan-dardsE2773htm

41 ASTM E2742-11 Standard Specification for Evaluation and Selec-tion of Exhibits for Environmentally Sustainable Meetings EventsTrade Shows and Conferences ASTM International West Con-shohocken PA 2011 httpswwwastmorgStandardsE2742htm

42 ASTM E2774-11 Standard Specification for Evaluation and Selec-tion of Venues for Environmentally Sustainable Meetings EventsTrade Shows and Conferences ASTM International West Con-shohocken PA 2011 httpswwwastmorgStandardsE2774htm

43 ASTM F2902-12 Standard Guide for Assessment of AbsorbablePolymeric Implants ASTM International West ConshohockenPA 2012 httpswwwastmorgStandardsF2902htm

44 httpsenwikipediaorgwikiResorption45 Venes D Tabers Cyclopedic Medical Dictionary 22th edition

Philadelphia F A Davis Company 201346 Zheng YF Gu XN Witte F Biodegradable metals Mater Sci Eng-

R-Rep 2014 77 1ndash3447 Hanawa T Metal ion release from metal implants Mater Sci

Eng-C 2004 24 745ndash75248 Zreiqat H Howlett CR Zannettino A et al Mechanisms of mag-

nesium-stimulated adhesion of osteoblastic cells to commonly usedorthopaedic implants J Biomed Mater Res 2002 62 175ndash184

49 Little PJ Bhattacharya R Moreyra AE et al Zinc and cardiovascu-lar disease Nutrition 2010 26 1050ndash1057

50 Seager H Drug-delivery products and the Zydis fast-dissolvingdosage form J Pharm Pharmacol 1998 50 375ndash382

51 Shikinami Y Shape-memory biodegradable and absorbable mate-rial US Patent No 6281262 2001-8-28

52 Huitema TW Knight GW Ransick MH Schulze DR Surgical im-plant with preferential corrosion zone US Patent No 79059022011-3-15

53 Luzier WD Materials derived from biomassbiodegradable mate-rials Proc Natl Acad Sci USA 1992 89 839ndash842

54 Gross RA Kalra B Biodegradable polymers for the environmentScience 2002 297 803ndash807

55 Trumbo P Schlicker S Yates AA et al Dietary reference intakesfor energy carbohydrate fiber fat fatty acids cholesterol proteinand amino acids J Am Diet Assoc 2002 102 1621ndash1630

56 Chambin O Champion D Debray C et al Effects of different cel-lulose derivatives on drug release mechanism studied at a prefor-mulation stage J Control Release 2004 95 101ndash108

12copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

57 Fundueanu G Constantin M Esposito E et al Cellulose acetatebutyrate microcapsules containing dextran ion-exchange resinsas self-propelled drug release system Biomaterials 2005 264337ndash4347

58 Maumlrtson M Viljanto J Hurme T et al Is cellulose sponge degrad-able or stable as implantation material An in vivo subcutaneousstudy in the rat Biomaterials 1999 20 1989ndash1995

59 Patel N Padera R Sanders GH et al Spatially controlled cell en-gineering on biodegradable polymer surfaces The FASEB journal1998 12 1447ndash1454

60 Goldstein A Effect of convection on osteoblastic cell growth andfunction in biodegradable polymer foam scaffolds Biomaterials2001 22 1279ndash1288

61 Wu L Ding J In vitro degradation of three-dimensional porouspoly(DL-lactide-co-glycolide) scaffolds for tissue engineeringBiomaterials 2004 25 5821ndash5830

62 Wu L Ding J Effects of porosity and pore size on in vitro degra-dation of three-dimensional porous poly(DL-lactide-co-glycolide)scaffolds for tissue engineering J Biomed Mater Res 2005 75A767ndash777

63 Pan Z Ding J Poly(lactide-co-glycolide) porous scaffolds for tissueengineering and regenerative medicine Interface Focus 2012 2366ndash377

64 Yu L Zhang Z Zhang H et al Biodegradability and biocompati-bility of thermoreversible hydrogels formed from mixing a sol anda precipitate of block copolymers in water Biomacromolecules2010 11 2169ndash2178

65 Wen X Tresco PA Fabrication and characterization of permeabledegradable poly(DL-lactide-co-glycolide) (PLGA) hollow fiberphase inversion membranes for use as nerve tract guidance chan-nels Biomaterials 2006 27 3800ndash3809

66 Chu CFL Lu A Liszkowski M et al Enhanced growth of animaland human endothelial cells on biodegradable polymers BBA-GenSubjects 1999 1472 479ndash485

67 Jo S Engel PS Mikos AG Synthesis of poly(ethylene glycol)-teth-ered poly(propylene fumarate) and its modification with GRGDpeptide Polymer 2000 41 7595ndash7604

68 Park JH Allen MG Prausnitz MR Biodegradable polymer mi-croneedles fabrication mechanics and transdermal drug deliveryJ Control Release 2005 104 51ndash66

69 Freed LE Vunjak-Novakovic G Biron RJ et al Biodegradablepolymer scaffolds for tissue engineering Nat Biotechnol 1994 12689ndash693

70 Windecker S Serruys PW Wandel S et al Biolimus-eluting stentwith biodegradable polymer versus sirolimus-eluting stent withdurable polymer for coronary revascularisation (LEADERS) arandomised non-inferiority trial Lancet 2008 372 1163ndash1173

71 Stefanini GG Kalesan B Serruys PW et al Long-term clinicaloutcomes of biodegradable polymer biolimus-eluting stents ver-sus durable polymer sirolimus-eluting stents in patients with coro-nary artery disease (LEADERS) 4 year follow-up of a randomisednon-inferiority trial Lancet 2011 378 1940ndash1948

72 Raungaard B Jensen LO Tilsted HH et al Zotarolimus-elutingdurable-polymer-coated stent versus a biolimus-eluting biodegrad-able-polymer-coated stent in unselected patients undergoing per-cutaneous coronary intervention (SORT OUT VI) a randomisednon-inferiority trial Lancet 2015 385 1527ndash1535

73 Freed LE Grande DA Lingbin Z et al Joint resurfacing using allo-graft chondrocytes and synthetic biodegradable polymer scaffoldsJ Biomed Mater Res 1994 28 891ndash899

74 Poirier Y Nawrath C Somerville C Production of polyhydrox-yalkanoates a family of biodegradable plastics and elastomers in

bacteria and plants Nat Biotechnol 1995 13 142ndash15075 Dias A Tsuru K Hayakawa S et al Crystallisation studies of

biodegradable CaO-P2O5 glass with MgO and TiO2 for boneregeneration applications Glass Technol 2004 45 78ndash79

76 Klein CPAT de Groot K Drissen AA et al Interaction ofbiodegradable β-whitlockite ceramics with bone tissue an in vivostudy Biomaterials 1985 6 189ndash192

77 Ikenaga M Hardouin P Lemaicirctre J et al Biomechanical charac-terization of a biodegradable calcium phosphate hydraulic cementa comparison with porous biphasic calcium phosphate ceramics JBiomed Mater Res 1998 40 139ndash144

78 Dias AG Lopes MA Santos JD et al In vivo performance ofbiodegradable calcium phosphate glass ceramics using the rabbitmodel histological and SEM observation J Biomater Appl 200620 253ndash266

79 Lee JH Lee CK Chang BS et al In vivo study of novel biodegrad-able and osteoconductive CaO-SiO2-B2O3 glass-ceramics JBiomed Mater Res 2006 77A 362ndash369

80 Song G Song S A possible biodegradable magnesium implant ma-terial Adv Eng Mater 2007 9 298ndash302

81 Kim WC Kim JG Lee JY et al Influence of Ca on the corrosionproperties of magnesium for biomaterials Mater Lett 2008 624146ndash4148

82 Li Z Gu X Lou S et al The development of binary Mg-Ca alloysfor use as biodegradablematerials within bone Biomaterials 200829 1329ndash1344

83 Wan Y Xiong G Luo H et al Preparation and characterization ofa new biomedical magnesium-calcium alloy Mater Des 2008 292034ndash2037

84 Seong JW Kim WJ Development of biodegradable Mg-Ca alloysheets with enhanced strength and corrosion properties throughthe refinement anduniformdispersion of theMg2Caphase by high-ratio differential speed rolling Acta Biomater 2015 11 531ndash542

85 Zhang S Li J Song Y et al In vitro degradation hemolysis andMC3T3-E1 cell adhesion of biodegradable Mg-Zn alloy Mater SciEng-C 2009 29 1907ndash1912

86 Li J Song Y Zhang S et al In vitro responses of human bone mar-row stromal cells to a fluoridated hydroxyapatite coated biodegrad-able Mg-Zn alloy Biomaterials 2010 31 5782ndash5788

87 Brar HS Wong J Manuel MV Investigation of the mechanical anddegradation properties of Mg-Sr and Mg-Zn-Sr alloys for use aspotential biodegradable implant materials J Mech Behav BiomedMater 2012 7 87ndash95

88 Bornapour M Muja N Shum-Tim D et al Biocompatibility andbiodegradability of Mg-Sr alloys the formation of Sr-substitutedhydroxyapatite Acta Biomater 2013 9 5319ndash5330

89 Gu XN Xie XH Li N et al In vitro and in vivo studies on aMg-Sr binary alloy system developed as a new kind of biodegrad-able metal Acta Biomater 2012 8 2360ndash2374

90 Haumlnzi AC Gerber I Schinhammer M et al On the in vitro andin vivo degradation performance and biological response of newbiodegradableMg-Y-Zn alloys Acta Biomater 2010 6 1824ndash1833

91 Chou DT Hong D Saha P et al In vitro and in vivo corrosioncytocompatibility and mechanical properties of biodegradableMg-Y-Ca-Zr alloys as implant materials Acta Biomater 2013 98518ndash8533

92 Zong Y Yuan G Zhang X et al Comparison of biodegradable be-haviors of AZ31 and Mg-Nd-Zn-Zr alloys in Hanks physiologicalsolution Mater Sci Eng-B 2012 177 395ndash401

93 Tie D Feyerabend FMuumlllerWD et al Antibacterial biodegradableMg-Ag alloys Eur Cell Mater 2013 25 284ndash298

94 VojtěchDKubaacutesek J Seraacutek J et al Mechanical and corrosion prop-

13 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

erties of newly developed biodegradable Zn-based alloys for bonefixation Acta Biomater 2011 7 3515ndash3522

95 Li H Yang H Zheng Y et al Design and characterizations of novelbiodegradable ternary Zn-based alloys with IIA nutrient alloyingelements Mg Ca and Sr Mater Des 2015 83 95ndash102

96 Liu X Sun J Yang Y et al Microstructure mechanical proper-ties in vitro degradation behavior and hemocompatibility of novelZn-Mg-Sr alloys as biodegradable metals Mater Lett 2016 162242ndash245

97 Wu C Qiu H Hu X et al Short-term safety and efficacy of thebiodegradable iron stent in mini-swine coronary arteries ChinMed J (Engl) 2013 126 4752ndash4757

98 Purnama A Hermawan H Champetier S et al Gene expressionprofile of mouse fibroblasts exposed to a biodegradable iron alloyfor stents Acta Biomater 2013 9 8746ndash8753

99 HermawanH Purnama A Dube D et al Fe-Mn alloys for metallicbiodegradable stents degradation and cell viability studies ActaBiomater 2010 6 1852ndash1860

100 Sheridan MH Shea LD Peters MC et al Bioabsorbable polymerscaffolds for tissue engineering capable of sustained growth factordelivery J Control Release 2000 64 91ndash102

101 Shawe S Buchanan F Harkin-Jones E et al A study on the rate ofdegradation of the bioabsorbable polymer polyglycolic acid (PGA)J Mater Sci 2006 41 4832ndash4838

102 Palmerini T Biondi-Zoccai G Della Riva D et al Clinical out-comes with bioabsorbable polymer- versus durable polymer-baseddrug-eluting and bare-metal stents J Am Coll Cardiol 2014 63299ndash307

103 Tanimoto S Serruys PW Thuesen L et al Comparison of in vivoacute stent recoil between the bioabsorbable everolimus-elutingcoronary stent and the everolimus-eluting cobalt chromium coro-nary stent insights from the ABSORB and SPIRIT trials CatheterCardiovasc Interv 2007 70 515ndash523

104 Tsuji H Sasaki H Sato H et al Neuron attachment properties ofcarbon negative-ion implanted bioabsorbable polymer of poly-lac-tic acid Nucl Instr Meth Phys Res Sect B-Beam Interact MaterAtoms 2002 191 815ndash819

105 Aikawa M Miyazawa M Okamoto K et al A novel treatment forbile duct injury with a tissue-engineered bioabsorbable polymerpatch Surgery 2010 147 575ndash580

106 WaksmanR Pakala R Kuchulakanti PK et al Safety and efficacy ofbioabsorbablemagnesium alloy stents in porcine coronary arteriesCatheter Cardiovasc Interv 2006 68 607ndash617

107 Di Mario C Griffiths H Goktekin O et al Drug-eluting bioab-sorbable magnesium stent J Interv Cardiol 2004 17 391ndash395

108 Erbel R Di Mario C Bartunek J et al Temporary scaffoldingof coronary arteries with bioabsorbable magnesium stents aprospective non-randomised multicentre trial Lancet 2007 3691869ndash1875

109 Schranz D Zartner P Michel-Behnke I et al Bioabsorbable metalstents for percutaneous treatment of critical recoarctation of theaorta in a newborn Catheter Cardiovasc Interv 2006 67 671ndash673

110 Gu X Zheng Y Cheng Y et al In vitro corrosion and biocompati-bility of binary magnesium alloys Biomaterials 2009 30 484ndash498

111 Hiromoto S InoueM Taguchi T et al In vitro and in vivo biocom-patibility and corrosion behaviour of a bioabsorbable magnesiumalloy coated with octacalcium phosphate and hydroxyapatite ActaBiomater 2015 11 520ndash530

112 Hiromoto S Tomozawa M Maruyama N Fatigue property of abioabsorbable magnesium alloy with a hydroxyapatite coatingformed by a chemical solution deposition J Mech Behav Biomed-ical Mater 2013 25 1ndash10

113 Bowen PK Drelich J Goldman J Zinc exhibits ideal physiologicalcorrosion behavior for bioabsorbable stents Adv Mater 2013 252577ndash2582

114 Liu X Sun J Yang Y et al In vitro investigation of ultra-pure Znand its mini-tube as potential bioabsorbable stent material MaterLett 2015 161 53ndash56

115 LinW Zhang G Cao P et al Cytotoxicity and its test methodologyfor a bioabsorbable nitrided iron stent J Biomed Mater Res 2015103 764ndash776

116 Coe JD Vaccaro AR Instrumented transforaminal lumbar inter-body fusion with bioresorbable polymer implants and iliac crestautograft Spine 2005 30 S76ndashS83

117 Ignatius AA Augat P Ohnmacht M et al A new bioresorbablepolymer for screw augmentation in the osteosynthesis of osteo-porotic cancellous bone a biomechanical evaluation J BiomedMater Res 2001 58 254ndash260

118 Krucoff MW Kereiakes DJ Petersen JL et al A novel biore-sorbable polymer paclitaxel-eluting stent for the treatment ofsingle and multivessel coronary disease J Am Coll Cardiol 200851 1543ndash1552

119 Kostopoulos L Karring T Guided bone regeneration in mandibu-lar defects in rats using a bioresorbable polymer Clin Oral Im-plants Res 1994 5 66ndash74

120 Dubok VA Bioceramicsmdashyesterday today tomorrow PowderMetall Metal Ceram 2000 39 381ndash394

121 Safronova T Kuznetsov A Korneychuk S et al Calcium phos-phate powders synthesized from solutions with [Ca2+][PO4

3minus]=1for bioresorbable ceramics Cent Eur J Chem 2009 7 184ndash191

122 Bohner M Bioresorbable ceramics In Buchanan FJ (Ed) Degra-dation Rate of Bioresorbable Materials Cambridge WoodheadPublishing 2008 95-114

123 Seitz JM Eifler R Stahl J et al Characterization ofMgNd2 alloy forpotential applications in bioresorbable implantable devices ActaBiomater 2012 8 3852ndash3864

124 WenCE Yamada Y Shimojima K et al Porous bioresorbable mag-nesium as bone substitute MSF 2003 419ndash422 1001ndash1006

125 Campos CM Muramatsu T Iqbal J et al Bioresorbable drug-elut-ing magnesium-alloy scaffold for treatment of coronary artery dis-ease Int J Mol Sci 2013 14 24492ndash24500

126 KirklandNT Birbilis NWalker J et al In-vitro dissolution ofmag-nesium-calcium binary alloys clarifying the unique role of calciumadditions in bioresorbable magnesium implant alloys J BiomedMater Res 2010 95B 91ndash100

127 Gastaldi D Sassi V Petrini L et al Continuum damage model forbioresorbable magnesium alloy devices mdashapplication to coronarystents J Mech Behav Biomed Mater 2011 4 352ndash365

128 Kitabata H Waksman R Warnack B Bioresorbable metal scaffoldfor cardiovascular application current knowledge and future per-spectives Cardiovasc Revasc Med 2014 15 109ndash116

Acknowledgments This work was supported by the National Key Re-search and Development Program of China (2016YFC1102402) NationalNatural Science Foundation of China (NSFC 51431002) and the NSFCand the Research Grants Council (RGC) of Hong Kong Joint ResearchScheme (51361165101 and 5161101031)

Author contributions Liu Y prepared the figures tables organized thereferences and wrote the paper Zheng Y provided the overall concept andrevised the manuscript Hayes B helped with the standard developmentand revised the manuscript All authors participated in the discussion

Conflict of interest The authors declare that they have no conflict ofinterest

14copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Yang Liu received his bachelor degree in materials science and engineering from Harbin engineering University in 2013Then he continued his study as a PhD candidate in Prof Yufeng Zhengrsquos Lab in Peking University His research interestsare mainly focused on the corrosion study of absorbable metallic biomaterials as well as the development of new kind ofMg-based biomaterials

Yufeng Zheng obtained his PhD degree from Harbin Institute of Technology in 1998 He is the National OutstandingYouth and Yangtze River scholar of China His research interests are focused on the development of novel biomaterials andapplication and design of biomedical devices

Byron Hayes an over 35 year employee of WL Gore has been involved in the commercial development of multiple ab-sorbable polymeric implants since the late 1980s Hayes started his standards development activities with ASTM in 2000where he is actively developing standards for polymeric and metallic absorbable implants In 2010 Hayes also becameinvolved with ISO Technical Committees TC150 and TC194 and is now convener of working groups focused on cardiovas-cular and metallic absorbable implants

可降解可吸收再吸收mdashmdash哪个是描述最终被人体吸收生物材料的最好词汇刘洋1 郑玉峰1 拜伦海耶斯2

摘要 关于最终被人体吸收的植入材料领域内文献采用的英文修饰词长期以来混乱且不同不仅造成文献检索困难同时模糊了研究人员的研究边界 此领域在法律法规标准中统一用词的确定为领域内的科学研究产品销售及产品使用说明奠定了基础 我们基于化学生态学材料学生物学微生物学和药学立足于使用习惯法律标准和市场对领域内使用已久的典型修饰词ldquo生物可降解rdquoldquo再吸收rdquo和ldquo可吸收rdquo进行了讨论和解释 总的来说尽管目前绝大多数修饰语实际想表达的意思相同作者认为ldquo可吸收rdquo这一英文修饰语是最恰当的修饰词 同时我们提议进一步规范和统一该领域修饰词的使用

15 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

  • Degradable absorbable or resorbablemdashwhat is the best grammatical modifier for an implant that is eventually absorbed by the body
  • Abstract
  • INTRODUCTION
    • Current situation
    • Standards development in advance
      • TERMINOLOGY
        • Overview of utilization of the terms ldquodegradationrdquoldquobiodegradationrdquo and ldquodegradablerdquoldquobiodegradablerdquo
        • Overview of utilization of the terms ldquoabsorptionrdquoldquobioabsorptionrdquo and ldquoabsorbablerdquoldquobioabsorbablerdquo
        • Overview of utilization of the terms ldquoresorptionrdquoldquobioresorptionrdquo and ldquoresorbablerdquoldquobioresorbablerdquo
        • Utilization and comparison of the terms ldquobiodegradable metalsrdquo and ldquoabsorbable metallic materialsrdquo
        • Summary quantification of the common Terms
          • DISCUSSION
            • Expertise inherent biases
            • Connotation and extension of noun forms ldquobiodegradation bioabsorption and bioresorptionrdquo and adjectives ldquobiodegradable bioabsorbable and bioresorbablerdquo
              • CONCLUDING REMARKS
              • References
              • Acknowledgements

of Pure and Applied Chemistry (IUPAC) suggested thatldquodegradation indicates progressive loss of the performanceor of the characteristics of a substance or a devicerdquo [14] Itis also a general process since there can be degradationscaused by the action of water named ldquohydrodegradationrdquoor hydrolysis As for biorelated polymers the degradationprocess is limited to macromolecule cleavage and molarmass decrease which distinguishes the degradation ofbiorelated polymer from fragmentation and disintegrationillustrated in bioceramics The term ldquodegradationrdquo wasformerly used in bioceramics by Prof L Hench to describethe decomposition process of calcium phosphate ceramicswhich was followed by host response and tissue repair [3]Thus the definition of ldquodegradationrdquo used in polymers andceramics fields could be interpreted as different inferringmore specifically to chemical processes for bio-relatedpolymers while referring to physical break down from theview of bio-ceramics researchersAs for the term ldquobiodegradationrdquo it is not the simple

addition of the prefix ldquobio-rdquo to ldquodegradationrdquo Fig 1 de-scribes the common usage of ldquobiodegradationrdquo currentlyThe word was firstly introduced as the consumption ofmaterial by bacteria fungi or other biological means inecology waste management biomedicine and even naturalenvironment [24] Some kinds of environmentally friendlyproducts also undergo such process as they can be degraded

by microorganisms and do no harm to the environmentHowever some researchers studying polymers and ceram-ics have defined a more specific scope for ldquobiodegradationrdquoFor polymers especially biorelated polymers the differ-ence between ldquobiodegradationrdquo and ldquodegradationrdquo lies inthe involvement of enzymatic process [1425]mdasha distinc-tion that can be problematic if both modes are active in animplantrsquos degradation process Moreover IUPAC stressedthe importance of proved degradation mechanisms whenusing ldquobiodegradationrdquo otherwise ldquodegradationrdquo should beused instead of ldquobiodegradationrdquo In general ldquodegradationrdquoand ldquobiodegradationrdquo both refer to the chain scission orchain cleavage Nevertheless the meaning of ldquobiodegra-dationrdquo in bioceramics is different since there is no suchprocess as chain scission The degradation process ofso-called ldquoresorbable ceramicsrdquo is claimed to involve eitherdecomposition to small particles as well as dissolved ionswhich participate in the enzymecell mediated reactionand new tissue forms [326ndash28] Despite the exact degra-dation process still needs further investigations the wordldquodegradationrdquo used for ldquoresorbablerdquo ceramics expressesmultiple meanings covering both chemical and physicalreactions in physiological environment such as hydrolysisdecomposition and debris formation According to ProfD Williams the recommended definition of ldquobiodegrada-tionrdquo is the gradual breakdown of a material mediated by

Figure 1 Common use of biodegradation currently

3 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

specific biological activity [23] Another definition as thebiomaterial or medical device involving loss of their in-tegrity or performance when exposed to a physiological orsimulated environment which existed in some ISO Techni-cal Report was not recommended since no specific respectto biological activity mentioned [23]Beyond the category of biomaterials ldquodegradablerdquo in

pure chemistry was defined as qualifier to a substance thatcan undergo physical andor chemical deleterious changesof some properties especially of integrity under stressconditions [14] Thus degradable polymer is consideredwith macromolecules being able to undergo chain scis-sions resulting in a decrease of molar mass [14] BesidesASTM made a standard definition on ldquodegradablerdquo in thescope of soil rock and contained fluids as ldquoin erosioncontrol decomposes under biological chemical processesor ultraviolet stresses associated with typical applicationenvironmentsrdquo [29] Despite no specific emphasis onbiomaterials numerous publications used ldquodegradablerdquo to

modify metals polymers or compounds in tissue engineer-ing drug delivery and gene delivery [30ndash35] Meanwhilein some ASTM standard specifications the definition ofthe adjective ldquobiodegradablerdquo is given as capable of de-composing under natural conditions into elements foundin the nature [36ndash42] The active ASTM entries currentlywith ldquobiodegradationrdquo ldquodegradablerdquo and ldquobiodegradablerdquoin the title are summarized in Table 1 The adoptionsof ldquobiodegradationrdquo ldquodegradablerdquo and ldquobiodegradablerdquoby ASTM are historical generally in the classification ofecology or environmental protectionWhile the above listing provides evidence that the usage

of the term biodegradable is broad it is particularly notablethat almost all of the listed standards are not relevant toimplantable devices Instead the listing primarily reflectsusage directed toward the environmental degradation as-pect that is most commonly recognized within the broadernon-medical oriented population ASTM-F1635 a stan-dard specifically centered on the hydrolytic degradation

Table 1 Summary of the terms ldquobiodegradationrdquo ldquodegradablerdquo and ldquobiodegradablerdquo being utilized in ASTM titles (not limited to implant)

Terminology ASTM titles

ASTM D5864-11 Standard Test Method for Determining Aerobic Aquatic Biodegradation of Lubricants or TheirComponents

ASTM D6954-04(2013) Standard Guide for Exposing and Testing Plastics that Degrade in the Environment by aCombination of Oxidation and Biodegradation

ASTM D5511-12 Standard Test Method for Determining Anaerobic Biodegradation of Plastic Materials Under High-SolidsAnaerobic-Digestion Conditions

ASTM D6139-11 Standard Test Method for Determining the Aerobic Aquatic Biodegradation of Lubricants or TheirComponents Using the Gledhill Shake Flask

ASTM D7991-15 Standard Test Method for Determining Aerobic Biodegradation of Plastics Buried in Sandy MarineSediment under Controlled Laboratory Conditions

ASTM D5338-15 Standard Test Method for Determining Aerobic Biodegradation of Plastic Materials Under ControlledComposting Conditions Incorporating Thermophilic Temperatures

ASTM D6691-09 Standard Test Method for Determining Aerobic Biodegradation of Plastic Materials in the MarineEnvironment by a Defined Microbial Consortium or Natural Sea Water Inoculum

ASTM D5526-12 Standard Test Method for Determining Anaerobic Biodegradation of Plastic Materials Under AcceleratedLandfill Conditions

ASTM D7475-11 Standard Test Method for Determining the Aerobic Degradation and Anaerobic Biodegradation of PlasticMaterials under Accelerated Bioreactor Landfill Conditions

Biodegradation

ASTM D5988-12 Standard Test Method for Determining Aerobic Biodegradation of Plastic Materials in Soil

ASTM F1635-11 Standard Test Method for in vitro Degradation Testing of Hydrolytically Degradable Polymer Resinsand Fabricated Forms for Surgical Implants

ASTM D7444-11 Standard Practice for Heat and Humidity Aging of Oxidatively Degradable PlasticsDegradable

ASTM D3826-98(2013) Standard Practice for Determining Degradation End Point in Degradable Polyethylene andPolypropylene Using a Tensile Test

ASTM D7665-10(2014) Standard Guide for Evaluation of Biodegradable Heat Transfer Fluids

ASTM D8029-16 Standard Specification for Biodegradable Low Aquatic Toxicity Hydraulic FluidsBiodegradable

ASTM D7044-15 Standard Specification for Biodegradable Fire Resistant Hydraulic Fluids

4copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

testing of absorbable polyesters is the sole listed standardfrom ASTM Committee F04mdashMedical and Surgical Im-plants and thereby is directly relevant to implantable de-vices However this standard utilizes the term degradeand its derivatives specifically in reference to the process ofdegradation that occurs as a result of ester hydrolysis Con-versely the same standard uses the term absorbable to de-scribe a class of implants that are eventually absorbed by thebody which it defines as ldquoabsorbable adjmdashin the bodymdashaninitially distinct foreign material or substance that either di-rectly or through intended degradation can pass through orbe assimilated by cells andor tissuerdquo

Overview of utilization of the terms ldquoabsorptionrdquoldquobioab-sorptionrdquo and ldquoabsorbablerdquoldquobioabsorbablerdquoThe term ldquoabsorptionrdquo was recognized by IUPAC as theprocess of penetration and diffusion of a substance (ab-sorbate) into another substance (absorbent) as a result ofthe action of attractive phenomena The IUPAC defini-tion is within the scope of chemistry As for biomaterialsProf D Williams adopted the definition in Dorland Medi-cal Dictionary as the uptake of substances into or across tis-sues [23] For this kind of definition ldquoabsorptionrdquo empha-sizes the interaction of materials and human or animal tis-sue The same connotation is shared by its derivative wordsldquoabsorbablerdquo and ldquobioabsorbablerdquo as capable of being de-graded or dissolved and subsequently metabolized withinan organism [23] Besides the prefix ldquobio-rdquo is abridged as

it is redundant in the field of implantation [43] ASTM hasmade standard definition on ldquoabsorbablerdquo in the field of ab-sorbable polymers as well as absorbablemetals which it de-fines as ldquohellip an initially distinct foreign material or substancethat either directly or through intended degradation can passthrough or be metabolized or assimilated by cells andor tis-sue in the bodyrdquo [43] Table 2 summarizes the currently ac-tive ASTM standards and both United States and EuropeanPharmacopeia implantable device monographs that utilizethe word ldquoabsorbablerdquo in the title Distinctly different fromldquobiodegradablerdquo the utilization of ldquoabsorbablerdquo displays adistinct preference for use in describing this particular classof biomedical materials and devicesAs can be observed in both Table 1 and Table 3 the

well-established terminology for describing sutures is verybroadly based on the term absorbable with historicalapplication of the term to the original gut sutures andeven extending to permanent sutures through the ldquononab-sorbablerdquo descriptorAside from the language of standards organization the

terminology utilized by regulatory agencies is also of par-ticular relevance Through multiple laws and regulationsthe US-FDA is authorized to evaluate medical device man-ufacturers and their products The US Code of FederalRegulations (CFRs) that is specific to sutures legally de-scribes those regulated devices based on composition andthen designates both their product class and needs to meetUSP requirements While Table 3 demonstrates both a US-

Table 2 ldquoAbsorbablerdquo utilized in title entries for implantable device related standards

Terminology Title entries

ISOTS 171372014 Cardiovascular implants and extracorporeal systemsmdashCardiovascular absorbable implants

ISOTR 371372014 Biological evaluation of medical devicesmdashGuidance for absorbable implants

ASTM F3036-13 Standard Guide for Testing Absorbable Stents

ASTM F2902-16 Standard Guide for Assessment of Absorbable Polymeric Implants

ASTM F2502-16 Standard Specification and Test Methods for Absorbable Plates and Screws for Internal Fixation Implants

ASTM F1983-14 Standard Practice for Assessment of Selected Tissue Effects of Absorbable Biomaterials for Implant Applications

ASTM F3160-16 Standard Guide for Metallurgical Characterization of Absorbable Metallic Materials for Medical Implants

United States Pharmacopoeia (USP 39NF 34) monographldquoAbsorbable Surgical Suturerdquo

United States Pharmacopoeia (USP 39NF 34) monographldquoNonabsorbable Surgical Suturerdquo

European Pharmacopoeia (88)ldquoSterile non-absorbable suturesrdquo ndash 1118

European Pharmacopoeia (88)ldquoSterile synthetic absorbable braided suturesrdquo - 1122

Absorbable

European Pharmacopoeia (88)Sterile synthetic absorbable monofilament sutures ndash 1123

5 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Table 3 US-FDA suture product codes and accompanying citation of US CFRsa)

Suture name Regulation Product code

Absorbable polydioxanone surgical (PDS) suture 21 CFR8784840 NEW

Absorbable poly(glycolideL-lactide) surgical suture 21 CFR8784493 GAM

Absorbable gut suture 21 CFR8784830 GAL

Nonabsorbable poly(ethylene terephthalate) suture 21 CFR8785000 GAT

Nonabsorbable polypropylene surgical suture 21 CFR8785010 GAW

Nonabsorbable polyamide surgical suture 21 CFR8785020 GAR

Natural nonabsorbable silk surgical suture 21 CFR8785030 GAP

Stainless steel surgical suture 21 CFR8784495 GAQ

Nonabsorbable expanded polytetrafluoroethylene (ePTFE)surgical suture

21 CFR8785030 NBY

a) Note this table selects abbreviated results obtained from online search for the implant device term ldquosuturerdquo that was conducted on 6 Aug 2016 athttpwwwaccessdatafdagovscriptscdrhcfdocscfPCDclassificationcfm

FDA and a US Code of Federal Regulations preference forabsorbable terminology when referring to sutures Table4 shows an expansion of that preference to include a to-tal of 30 absorbable implant product classifications each ofwhich is assigned to a relevant Federal regulation that uti-lizes the term ldquoabsorbablerdquoIn short ldquoabsorbablerdquo is both a historically well estab-

lished and currently relevant term in both the regulationand standardization of implants that are intentionally ab-sorbed by the body

Overview of utilization of the terms ldquoresorptionrdquoldquobiore-sorptionrdquo and ldquoresorbablerdquoldquobioresorbablerdquoIn the scope of chemistry the term ldquoresorptionrdquo was used toillustrate the total elimination of a substance from its initialplace caused by physical andor chemical phenomena [14]Besides the understanding from pure chemistry ldquoresorp-tionrdquo is more recognized involved in the metabolic activi-ties in vivo For example ldquoresorptionrdquo is considered as theldquoabsorptionrdquo into the circulatory system of cells or tissuewhich usually includes bone resorption tooth resorptionand vanishing twin [44] In the biomedical scope Prof DWilliams used themeaning in DorlandMedical Dictionaryas ldquolysis and assimilation of a substance as of bonerdquo [23]ldquoBioresorptionrdquo is more common when describing the invivo process of a certain foreign material The ISO definedldquobioresorptionrdquo as a process by which biomaterials are de-graded in the physiological environment and the by-prod-uct are eliminated or completely bioabsorbed [23] Thusaccording to this interpretation the bioresorption processincludes material removal in vivo either by cellular activ-ity or not Conversely Taberrsquos Cyclopedic Medical Dictio-nary [45] describes the term ldquoresorbrdquo as themeaning ldquoto ab-

sorb againrdquomdashsomething that live tissue does but not some-thing any implant is known to domdashbe it permanent or ab-sorbableAs for the adjectives ldquobioresorbablerdquo and ldquoresorbablerdquo

there is no difference when used to describe a kind of ma-terials which have the ability of resorption This is ascribedto the fact that ldquoresorptionrdquo itself already has been well rec-ognized as a biological process [23] Currently there is noASTM entries used ldquoresorbablerdquo or ldquobioresorbablerdquo in thetitle

Utilization and comparison of the terms ldquobiodegradablemetalsrdquo and ldquoabsorbable metallic materialsrdquoldquoBiodegradablemetalsrdquo generally include themetalsMg Feand Zn and their alloys and composites They can be de-fined as metals that assist with tissue healing and are thenexpected to gradually corrode and release corrosion prod-ucts in vivowith an appropriate host response and then dis-solve completely with no implant residues [46] As a resultand different from traditional ldquobio-inertrdquometallic biomate-rials (eg Ti and Co based alloys) that release limited cor-rosion products [47] metabolic reactions besides inflam-mation can be expected to occur between the biodegrad-able metal and the host body after implantation Addition-ally the corrosion-based degradation mechanism of thesematerials is inherently different from that of either bioce-ramics or polymers which has resulted in limited to nostandardized guidance available from either ASTM or ISOInstead of the term ldquobiodegradable metalrdquo the recently

published and first absorbable metal related standardASTM F3160 utilizes the more inclusive word ldquoabsorbablerdquowithin the phrase ldquoabsorbable metallic materialsrdquo andagain defines the term as ldquohellip an initially distinct foreign

6copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Table 4 US-FDA absorbable implant related product codes descriptions and accompanying CFRsa)

Product code Device Device class Regulation number Regulation description

OMT Absorbable lung biopsy plug 2 [8784755] Absorbable lung biopsy plug

LMF Agent absorbable hemostatic collagen based 3 [8784490] Absorbable hemostatic agent and dressing

LMG Agent absorbable hemostatic non-collagen based 3 [8784490] Absorbable hemostatic agent and dressing

MRY Appliances and accessories fixation bone absorbable singlemultiple component 2 [8883040] Smooth or threaded metallic bone fixation fastener

PBQ Fixation non-absorbable or absorbable for pelvic use 2 [8844530] Obstetric-gynecologic specialized manual instrument

HQJ Implant absorbable (scleral buckling methods) 2 [8863300] Absorbable implant (scleral buckling method)

OWT Mesh surgical absorbable abdominal hernia 2 [8783300] Surgical mesh

OXM Mesh surgical absorbable fistula 2 [8783300] Surgical mesh

OXI Mesh surgical absorbable large abdominal wall defects 2 [8783300] Surgical mesh

OXL Mesh surgical absorbable organ support 2 [8783300] Surgical mesh

OWW Mesh surgical absorbable orthopaedics reinforcement of tendon 2 [8783300] Surgical mesh

OXF Mesh surgical absorbable plastic and reconstructive surgery 2 [8783300] Surgical mesh

OXC Mesh surgical absorbable staple line reinforcement 2 [8783300] Surgical mesh

OWZ Mesh surgical absorbable thoracic chest wall reconstruction 2 [8783300] Surgical mesh

OWU Mesh surgical non-absorbable diaphragmatic hernia 2 [8783300] Surgical mesh

OWR Mesh surgical non-absorbable facial implants for plastic surgery 2 [8783300] Surgical mesh

OXJ Mesh surgical non-absorbable large abdominal wall defects 2 [8783300] Surgical mesh

OWX Mesh surgical non-absorbable orthopaedics reinforcement of tendon 2 [8783300] Surgical mesh

OXG Mesh surgical non-absorbable plastic and reconstructive surgery 2 [8783300] Surgical mesh

OXD Mesh surgical non-absorbable staple line reinforcement 2 [8783300] Surgical mesh

OXA Mesh surgical non-absorbable thoracic chest wall reconstruction 2 [8783300] Surgical mesh

LBP Replacement ossicular (stapes) using absorbable gelatin material 2 [8743450] Partial ossicular replacement prosthesis

OLL Septal staplerabsorbable staples 2 [8784750] ImplanTABLE staple

MNU Staple absorbable 2 [8883030] Singlemultiple component metallic bone fixationappliances and accessories

GAK Suture absorbable 2 [8784830] Absorbable surgical gut suture

GAL Suture absorbable natural 2 [8784830] Absorbable surgical gut suture

HMO Suture absorbable ophthalmic 3

GAN Suture absorbable synthetic 2 [8784830] Absorbable surgical gut suture

GAM Suture absorbable synthetic polyglycolic acid 2 [8784493] Absorbable poly(glycolidel-lactide) surgical suture

NEW Suture surgical absorbable polydioxanone 2 [8784840] Absorbable polydioxanone surgical suture

a) Note the results obtained from online search for the device term ldquoabsorbablerdquo that was conducted on 6 Aug 2016 at httpwwwaccessdatafdagovscriptscdrhcfdocscfPCDclassifica-tioncfm

7 copy

ScienceChina

Pressand

Springer-VerlagBerlin

Heidelberg 2017

SCIENCECH

INAMaterials

REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

material or substance that either directly or through in-tended degradation can pass through or be metabolized orassimilated by cells andor tissuerdquo The standardrsquos nomen-clature appendix further elaborates on its preference forldquoabsorbablerdquo since the prefix ldquobio-rdquo is redundant in thecontext of implant applications [43]Clearly these two terms of ldquobiodegradable metalsrdquo and

ldquoabsorbable metallic materialsrdquo share the same connota-tion which defines the completemission of an intentionallydegradable material when implanted in vivo In the contextof biodegradable metalsabsorbable metallic materialsthe process includes the corrosion caused by body fluida host response caused by corrosion products followedby dissolutionabsorption and finally improved tissuehealing The ldquobiodegradationrdquo instead of ldquobiocorrosionrdquois used to distinguish this new kind of metals which canfully dissolve in vivo with no implant residues Besidesbiodegradation process the following dynamic process ofdissolutionabsorption also starts in vivo For exampledissolved Mg2+ is considered to enhance the integrin me-diated human-bone-derived cell adhesion and affect newbone formation [48] The metabolic reaction is also crucialand even more important for biodegradable metals as it ishelpful It is another distinction from traditional metalsused for biomedical application In fact the different usagehabit forming of ldquobiodegradablerdquo or ldquoabsorbablerdquoldquobioab-sorbablerdquo may be more related with the study field theresearchers in Taking the ldquoabsorbablerdquo metallic stent asan example (Fig 2) once the ldquoabsorbablerdquo metallic stentwas implanted into blood vessel ldquocorrosionrdquo of biometal

begins The corrosion products including debris hydro-gen (for Mg-based metals) metallic ions and hydroxylconvert the local environment and diffuse into the bloodvessel wall Some corrosion products can be biologicallybeneficial For instance the diffused and absorbed Zn2+

can potentially play a positive role in dealing with athero-sclerosis [49] Along with the corrosion process healingprocesses such as endothelialization may become en-hanced In summary and within the context of absorbablemetals the adjectives ldquodegradablerdquo and ldquoabsorbablerdquo referto the nature of the biodegradation products of the mate-rialdevice being metabolically absorbed an attribute ofthe host (animal or human body) regardless of whetherthe implant degrades corrodes hydrolyzes or dissolves[50ndash52]

Summary quantification of the common TermsFig 3a shows preliminary searching results in Webof Knowledge using ldquodegradablerdquo ldquoabsorbablerdquo or ldquore-sorbablerdquo along with ldquomaterialrdquo as key words Theutilization of ldquodegradablerdquo is a bit more frequently thanldquoabsorbablerdquo but that of ldquoresorbablerdquo steps down Mean-while the counterpart searching result when using ldquobiordquo asprefix to the adjectives along with ldquomaterialrdquo as keywordsare presented in Fig 3b ldquoBiodegradable materialrdquo is themost common utilization which holds 91 among the ex-pression approach This is also due to the fact that besidesthe common utilization in biomaterials ldquobiodegradablerdquois also used in a wide range of applications such as cleanenvironment and ecology [5354]

Figure 2 Different point of views on the biodegradationabsorption process

8copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Figure 3 Searching results in Web of Knowledge from all databases (a) with the total searched publication numbers by ldquodegradablerdquo+ ldquomaterialrdquoldquoabsorbablerdquo+ ldquomaterialrdquo and ldquoresorbablerdquo+ ldquomaterialrdquo as 100 (b) the total searched publication numbers by ldquobiodegradablerdquo+ ldquomaterialrdquo ldquobioab-sorbablerdquo+ ldquomaterialrdquo and ldquobioresorbablerdquo+ ldquomaterialrdquo as 100

DISCUSSION

Expertise inherent biasesAs previously mentioned biomaterial is an interdiscipli-nary field fascinating researchers with specialty from dif-ferent backgrounds Different backgrounds as well as dif-ferent research point of interests may be one of the reasonsfor using different terminologies Materials scientists tendto focus on the materialdevice itself leading to their usageof ldquobiodegradablerdquo to illustrate what happens to the deviceThey pay more attention to the process such as hydroly-sis corrosion debris degradation products and the changeof surface morphology resulting in the researching inter-ests of ldquomaterial biodegradationrdquo In contrast surgeons andbiomedical researchers tend to be concerned more on thehost response and healing process They are curious aboutthe absorption of various degradation products of the im-planted materialdevice and related metabolism mecha-nism and thereby prefer to use the term ldquoabsorbablerdquo toillustrate what happens to the device As known somema-terials may only undergo biodegradation but the corrosionproducts still have no influence on the metabolic activitiesFor example cellulose is considered as ldquodietary fiberrdquowhichcannot be digested and absorbed by human body but is be-nign for human body [55] Some coating tablets for drug ordrug delivery systems made from cellulose and its deriva-tives are quite frequently utilized or investigated [5657]The polymer and derivatives of cellulose can only be de-graded but not be absorbed by human body [58] For suchmaterials the adjective ldquoabsorbablerdquo or ldquobioabsorbablerdquo isnot appropriateOverall once the materialsdevices are implanted into

the human body the ldquobiocorrosionrdquobiodegradationrdquoprocess happens immediately no matter to what degreeat the same time the host will biologically response to the

corrosiondegradation products through the absorptionmetabolism and excretion processes So for the samestory the majority of materials scientists would report itby ldquobiodegradabledegradationrdquo way whereas the majorityof medical doctors would report it by ldquoabsorbableab-sorptionrdquo way In nature the two terms ldquobiodegradablemetalsrdquo and ldquoabsorbable metallic materialsrdquo share the sameconnotation and are mutually replaceable

Connotation and extension of noun forms ldquobiodegradationbioabsorption and bioresorptionrdquo and adjectivesldquobiodegradable bioabsorbable and bioresorbablerdquoThe three noun forms of the terms illustrate the processwhile their adjectival derivatives were used to describe thegroup of materials with such certain capabilities For thestudy on biomaterials polymer researchers use ldquodegrada-tionbiodegradationrdquo when there is proved chain scissionprocess Besides they differentiate ldquobiodegradationrdquo andldquodegradationrdquo by confirmed metabolic activities betweenthe materials and cells or tissues Regarding to the fouradjectives ldquobiodegradablerdquo ldquobioabsorbablerdquo and ldquobiore-sorbablerdquo the term ldquobiocorrodiblerdquo is only used in scientificpapers on iron based materials and some patents on mag-nesium based materials The common usage of termsldquobiodegradablerdquo ldquobioabsorbablerdquo and ldquobioresorbablerdquo withrespect to the biomaterial research area is shown in Table 5The results reveal a widespread usage of ldquobiodegradablerdquo inboth polymers and magnesium based metals Varies typesof materials were reported as biomaterials Besides thereare also reports of ldquobiodegradablerdquo polymers for ecologyand environmental protection which indicates a furtherusage scope of ldquobiodegradablerdquo not only for implants anddevices Besides ldquobioresorbablerdquo is also utilized in all theresearch fields of polymers ceramics andmetals Howeverno current work used ldquobioabsorbablerdquo as grammatical

9 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Table 5 Current reported usage of terms ldquobiodegradablerdquo ldquobioabsorbablerdquo and ldquobioresorbablerdquoTerminology Category Materials Applications

PLA-PEG-biotin PLGA Controlled cell engineering [5960]Porous PLGA Tissue engineering [61ndash63]

PLGA-PEG-PLGA Injective thermosensitive hydrogel [64]PLGA Nerve guidance [65]

Fibronectin (Fn)-coated PLLA P(LLA-CL) Enhanced growth of endothelial cells [6066]PEG tethered PPF [67]

PDMS Drug delivery [68]PGA Tissue engineering [69]

Undefined Coronary stent [70ndash72]PGA Joint resurfacing [73]

Polymers

PHA Ecology and environmental protection [74]CaO-P2O5 glass Bone regeneration [75]β-Whitlockite Bone regeneration [76]

Calcium phosphate hydraulic cement Bone regeneration [77]Calcium

phosphate glass ceramicsBone regeneration [78]

Ceramics

CaO-SiO2-B2O3 glass-ceramics Bone regeneration [79]Pure Mg Implant material [80]

Mg-Ca-based Bone regeneration [81ndash84]Mg-Zn-based Bone regeneration [338586]Mg-Sr-based Bone regeneration [87ndash89]Mg-RE-based Vascular stent [90ndash92]

Mg and its metals

Mg-Ag-based [93]Zn-Mg Zn-Ca Zn-Sr [9495]Zn and its metals Zn-Mg-Sr [96]

Fe [9798]

Biodegradable

Fe and its metals Fe-Mn [99]PLLA PLG PGA Molecule delivery [100]

PGA Suture [101]Undefined Drug-eluting stent [102103]

PLA Neuron attachment [104]Polymers

PLA and PCL reinforced with PGA fibers Bile duct patch [105]Mg-RE based Coronary stent [106ndash109]

Binary Mg alloys [110]Mg and its metalsMg-Al-based [111112]

Zn and its metals Pure Zinc [113114]Fe and its metals Nitrided iron [115]

PLDLA Transforaminal lumbar interbody fusion [116]Alkylene bis(dilactoyl)-methacrylate modified polymer Bone screw augmentation [117]

Undefined Coronary stent [118]PHB Mandibular defects regeneration [119]HA Bone regeneration [120]Ceramics Calcium phosphate [121122]

MgNd2 Stent material [123]Porous Mg Bone substitute [124]Mg-RE Coronary stent [125]Mg-Ca Orthopedic application [126]

Mg and its metals

Mg-based Finite element analysis [127]

Bioabsorbable

Fe and its metals Pure Fe [128]

10copy

ScienceChina

Pressand

Springer-VerlagBerlin

Heidelberg 2017

REVIEWSCIENCE

CHINA

Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

modifier to bioceramics In addition as previouslyillustrated the prefix ldquobiordquo of ldquobioabsorbablerdquo and ldquobiore-sorbablerdquo are abridged hereafter discussion will concen-trate on ldquobiocorrodiblerdquo ldquobiodegradablerdquo ldquoabsorbablerdquo andldquoresorbablerdquoSince absorbable technologies are increasingly utilized

in numerous new and broader implant applications it be-comes more important to not acquiesce in addressing his-torical problems and instead actively move forward towardutilizing standardized language that is both technically ac-curate and unified in itsmeaning Preferred language needsto accurately communicate the concept To achieve the uni-fying goal of harmonized terminology themedical and sci-entific communities need to not solely look at materialschemistry or even biomaterials alone but to instead lookat term selection both across and within the context of thebroader medical disciplinemdashthe location where the resultsof implant technology development actually reaches themarketplace where therapies are brought to those in needNomenclature solutions need to both understand and re-spond to the context of terms across adjacent technologieswhich means to address needs from the perspectives of thebiomaterial researcher the deviceproduct developer thesurgeonclinician user the regulator and last but not leastthe patientgeneral public who is the direct beneficiary ofthe developed technologyA better understanding of these terminologies is neces-

sary and beneficial to the field Therefore the definitionson ldquodegradablerdquo ldquoabsorbablerdquo ldquoresorbablerdquo and relatedterms proposed by different organizations in differentfields have been summarized and discussed with the con-notation and extension of each term being compared andthe criteria being proposed

CONCLUDING REMARKSHerein given both the searching problem on the Internetand ambiguity in meanings the usage of grammaticalmodifiers to describe biomaterials that is eventually ab-sorbed by human body has been enumerated based onusage habits laws standards and markets In summaryldquodegradablerdquoldquobiodegradablerdquo are the most frequently usedgrammatical modifier not only in metals but also poly-mers as such kind of biomaterials ldquoBiodegradationrdquo andldquobiodegradablerdquo define the change of the materialdevicewell in the research of biomaterials but they are alsoadopted in other fields such as ecology and environmentalprotection Meanwhile ldquoresorbablerdquoldquobioresorbablerdquo havelong been recognized in the biological research and theldquoresorptionrdquo itself has been widely accepted as a biological

reaction The utilization of ldquoresorbablerdquoldquobioresorbablerdquowas found to be not as frequent as the counterpartsldquodegradablerdquoldquobiodegradablerdquo and ldquoabsorbablerdquoldquobioab-sorbablerdquo Such usage is accurate for osteoclast driven boneresorption but is inappropriate for implants that do notcarry the potential to grow back into their original formOtherwise despite it is not the most frequently used termldquoabsorbablerdquoldquobioabsorbablerdquo concentrates more on thehost metabolism to the foreign biodegradation productsof the implanted materialdevice compared with ldquodegrad-ablerdquoldquobiodegradablerdquo ldquoAbsorbablerdquo is defined in the scopeof biomaterials by different organizations and their publi-cations and also adopted by ASTM to illustrate ldquoabsorbablepolymerrdquo It is the most historically established the mostbroadly applicable (includes dissolvable devices that donot degrade) the most specific to medical applicationsand is the formal legal descriptor for most implant devicesConsidering the usage history common utilization in lawand standards as well as the scientific meaning in essenceldquoabsorbablerdquo can be better among other grammaticalmodifiers for description of an implant that is eventuallyabsorbed by the body which is recommended by theauthors for a further internationally-unified usage

Received 28 February 2017 accepted 27 March 2017published online 26 April 2017

1 Mackenzie D The history of sutures Med Hist 1973 17 158ndash1682 Hench LL Bioceramics J Am Ceramic Soc 2005 81 1705ndash17283 Hench LL Bioceramics from concept to clinic J AmCeramic Soc

1991 74 1487ndash15104 Windhagen H Radtke K Weizbauer A et al Biodegradable

magnesium-based screw clinically equivalent to titanium screw inhallux valgus surgery short term results of the first prospectiverandomized controlled clinical pilot study BioMed Eng OnLine2013 12 62

5 Schildwaumlchter M Biotronik announces CE mark for magmaristhe first clinically-proven bioresorbable magnesium scaffoldhttpwwwmagmariscomennewsroomjune-15-2016

6 Shalaby SW Burg KJL Bioabsorbable polymers update degrada-tion mechanisms safety and application J App Biomater 1995 6219ndash221

7 Vert M Li SM Spenlehauer G et al Bioresorbability and biocom-patibility of aliphatic polyesters J Mater Sci-Mater Med 1992 3432ndash446

8 Vert M Degradable and bioresorbable polymers in surgery and inpharmacology beliefs and facts J Mater Sci-Mater Med 2009 20437ndash446

9 Benicewicz BC Hopper PK Review polymers for absorbablesurgical suturesmdashPart I J Bioactive Compatible Polym 1990 5453ndash472

10 Barrows HT Synthetic bioabsorbable polymers In Szycher M(Ed) High Performance Biomaterials A Complete Guide toMed-ical and Pharmceutical Applications Boca Raton CRC PRESS1991 243ndash257

11 Weiler A Hoffmann RFG Staumlhelin AC et al Biodegradable

11 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

implants in sports medicine the biological base Arthroscopy-JArthroscopic Related Surgery 2000 16 305ndash321

12 Ikada Y Tsuji H Biodegradable polyesters for medical and ecolog-ical applications Macromol Rapid Commun 2000 21 117ndash132

13 Ashammakhi N Peltoniemi H Waris E et al Developments incraniomaxillofacial surgery use of self-reinforced bioabsorbableosteofixation devices Plast Reconstr Surg 2001 108 167ndash180

14 Vert M Doi Y Hellwich KH et al Terminology for biorelatedpolymers and applications (IUPACRecommendations 2012) PureAppl Chem 2012 84 377ndash410

15 The United States Pharmacopeial Convention The Second Sup-plement to the Pharmacopeia of the United States of America 11thdecennial revision (USP XI-1939 Supplement) 1939

16 Truhlsen SM The recession operation histopathologic responseand suture reaction and absorption Trans Am Ophthalmol Soc1965 63 626ndash677

17 USP in US Law httpwwwusporgprintabout-usplegal-recog-nitionusp-us-law

18 USP develops and publishes standards for drug substances drugproducts excipients and dietary supplements in the United StatesPharmacopeia-National Formulary (USP-NF)

19 United States Public Law 94-295 197620 United States Pharmacopeia httpwwwusporg21 British Pharmacopeia httpswwwpharmacopoeiacom22 European Pharmacopoeia httponlinepheurorgENentryhtm23 Williams DF The Williams Dictionary of Biomaterials Liverpool

Liverpool University Press 199924 httpsenwikipediaorgwikiBiodegradation25 Jones RG Kahovec J Stepto R et al Compendium of Polymer

Terminology and Nomenclature IUPAC Recommendations 2008Cambridge RSC Publishing 2009

26 Higashi S Yamamuro T Nakamura T et al Polymer-hydroxyap-atite composites for biodegradable bone fillers Biomaterials 19867 183ndash187

27 de Groot K Bioceramics of Calcium Phosphate Boca Raton CRCPress 1983

28 Hollinger JO Battistone GC Biodegradable bone repair materialssynthetic polymers and ceramics ClinOrthopRelat Res 1986 207290ndash306

29 ASTMD653-14 Standard Terminology Relating to Soil Rock andContained Fluids ASTM International West Conshohocken PA2014 httpswwwastmorgStandardsD653htm

30 Witte F Hort N Vogt C et al Degradable biomaterials based onmagnesium corrosion Curr Opin Solid State Mater Sci 2008 1263ndash72

31 Lynn DM Langer R Degradable poly(β-amino esters) synthesischaracterization and self-assemblywith plasmidDNA JAmChemSoc 2000 122 10761ndash10768

32 Cima LG Vacanti JP Vacanti C et al Tissue engineering by celltransplantation using degradable polymer substrates J BiomechEng 1991 113 143ndash151

33 Zhang S Zhang X Zhao C et al Research on an Mg-Zn alloy as adegradable biomaterial Acta Biomater 2010 6 626ndash640

34 Anseth KS Metters AT Bryant SJ et al In situ forming degradablenetworks and their application in tissue engineering and drug de-livery J Control Release 2002 78 199ndash209

35 Forrest ML Koerber JT Pack DW A degradable polyethyleniminederivative with low toxicity for highly efficient gene delivery Bio-conjugate Chem 2003 14 934ndash940

36 ASTM E2747-11 Standard Specification for Evaluation and Selec-tion of Onsite Offices for Environmentally Sustainable MeetingsEvents Trade Shows and Conferences ASTM International

West Conshohocken PA 2011 httpswwwastmorgStan-dardsE2747htm

37 ASTM E2745-11 Standard Specification for Evaluation andSelection of Audio Visual (AV) and Production for Environ-mentally Sustainable Meetings Events Trade Shows and Con-ferences ASTM International West Conshohocken PA 2011httpswwwastmorgStandardsE2745htm

38 ASTM E2746-11 Standard Specification for Evaluation andSelection of Communication and Marketing Materials for En-vironmentally Sustainable Meetings Events Trade Shows andConferences ASTM International West Conshohocken PA 2011httpswwwastmorgStandardsE2746htm

39 ASTM E2741-11 Standard Specification for Evaluation and Se-lection of Destinations for Environmentally Sustainable MeetingsEvents Trade Shows and Conferences ASTM InternationalWest Conshohocken PA 2011 httpswwwastmorgStan-dardsE2741htm

40 0 ASTM E2773-11 Standard Specification for Evaluation andSelection of Food and Beverage for Environmentally SustainableMeetings Events Trade Shows and Conferences ASTM Interna-tional West Conshohocken PA 2011 httpswwwastmorgStan-dardsE2773htm

41 ASTM E2742-11 Standard Specification for Evaluation and Selec-tion of Exhibits for Environmentally Sustainable Meetings EventsTrade Shows and Conferences ASTM International West Con-shohocken PA 2011 httpswwwastmorgStandardsE2742htm

42 ASTM E2774-11 Standard Specification for Evaluation and Selec-tion of Venues for Environmentally Sustainable Meetings EventsTrade Shows and Conferences ASTM International West Con-shohocken PA 2011 httpswwwastmorgStandardsE2774htm

43 ASTM F2902-12 Standard Guide for Assessment of AbsorbablePolymeric Implants ASTM International West ConshohockenPA 2012 httpswwwastmorgStandardsF2902htm

44 httpsenwikipediaorgwikiResorption45 Venes D Tabers Cyclopedic Medical Dictionary 22th edition

Philadelphia F A Davis Company 201346 Zheng YF Gu XN Witte F Biodegradable metals Mater Sci Eng-

R-Rep 2014 77 1ndash3447 Hanawa T Metal ion release from metal implants Mater Sci

Eng-C 2004 24 745ndash75248 Zreiqat H Howlett CR Zannettino A et al Mechanisms of mag-

nesium-stimulated adhesion of osteoblastic cells to commonly usedorthopaedic implants J Biomed Mater Res 2002 62 175ndash184

49 Little PJ Bhattacharya R Moreyra AE et al Zinc and cardiovascu-lar disease Nutrition 2010 26 1050ndash1057

50 Seager H Drug-delivery products and the Zydis fast-dissolvingdosage form J Pharm Pharmacol 1998 50 375ndash382

51 Shikinami Y Shape-memory biodegradable and absorbable mate-rial US Patent No 6281262 2001-8-28

52 Huitema TW Knight GW Ransick MH Schulze DR Surgical im-plant with preferential corrosion zone US Patent No 79059022011-3-15

53 Luzier WD Materials derived from biomassbiodegradable mate-rials Proc Natl Acad Sci USA 1992 89 839ndash842

54 Gross RA Kalra B Biodegradable polymers for the environmentScience 2002 297 803ndash807

55 Trumbo P Schlicker S Yates AA et al Dietary reference intakesfor energy carbohydrate fiber fat fatty acids cholesterol proteinand amino acids J Am Diet Assoc 2002 102 1621ndash1630

56 Chambin O Champion D Debray C et al Effects of different cel-lulose derivatives on drug release mechanism studied at a prefor-mulation stage J Control Release 2004 95 101ndash108

12copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

57 Fundueanu G Constantin M Esposito E et al Cellulose acetatebutyrate microcapsules containing dextran ion-exchange resinsas self-propelled drug release system Biomaterials 2005 264337ndash4347

58 Maumlrtson M Viljanto J Hurme T et al Is cellulose sponge degrad-able or stable as implantation material An in vivo subcutaneousstudy in the rat Biomaterials 1999 20 1989ndash1995

59 Patel N Padera R Sanders GH et al Spatially controlled cell en-gineering on biodegradable polymer surfaces The FASEB journal1998 12 1447ndash1454

60 Goldstein A Effect of convection on osteoblastic cell growth andfunction in biodegradable polymer foam scaffolds Biomaterials2001 22 1279ndash1288

61 Wu L Ding J In vitro degradation of three-dimensional porouspoly(DL-lactide-co-glycolide) scaffolds for tissue engineeringBiomaterials 2004 25 5821ndash5830

62 Wu L Ding J Effects of porosity and pore size on in vitro degra-dation of three-dimensional porous poly(DL-lactide-co-glycolide)scaffolds for tissue engineering J Biomed Mater Res 2005 75A767ndash777

63 Pan Z Ding J Poly(lactide-co-glycolide) porous scaffolds for tissueengineering and regenerative medicine Interface Focus 2012 2366ndash377

64 Yu L Zhang Z Zhang H et al Biodegradability and biocompati-bility of thermoreversible hydrogels formed from mixing a sol anda precipitate of block copolymers in water Biomacromolecules2010 11 2169ndash2178

65 Wen X Tresco PA Fabrication and characterization of permeabledegradable poly(DL-lactide-co-glycolide) (PLGA) hollow fiberphase inversion membranes for use as nerve tract guidance chan-nels Biomaterials 2006 27 3800ndash3809

66 Chu CFL Lu A Liszkowski M et al Enhanced growth of animaland human endothelial cells on biodegradable polymers BBA-GenSubjects 1999 1472 479ndash485

67 Jo S Engel PS Mikos AG Synthesis of poly(ethylene glycol)-teth-ered poly(propylene fumarate) and its modification with GRGDpeptide Polymer 2000 41 7595ndash7604

68 Park JH Allen MG Prausnitz MR Biodegradable polymer mi-croneedles fabrication mechanics and transdermal drug deliveryJ Control Release 2005 104 51ndash66

69 Freed LE Vunjak-Novakovic G Biron RJ et al Biodegradablepolymer scaffolds for tissue engineering Nat Biotechnol 1994 12689ndash693

70 Windecker S Serruys PW Wandel S et al Biolimus-eluting stentwith biodegradable polymer versus sirolimus-eluting stent withdurable polymer for coronary revascularisation (LEADERS) arandomised non-inferiority trial Lancet 2008 372 1163ndash1173

71 Stefanini GG Kalesan B Serruys PW et al Long-term clinicaloutcomes of biodegradable polymer biolimus-eluting stents ver-sus durable polymer sirolimus-eluting stents in patients with coro-nary artery disease (LEADERS) 4 year follow-up of a randomisednon-inferiority trial Lancet 2011 378 1940ndash1948

72 Raungaard B Jensen LO Tilsted HH et al Zotarolimus-elutingdurable-polymer-coated stent versus a biolimus-eluting biodegrad-able-polymer-coated stent in unselected patients undergoing per-cutaneous coronary intervention (SORT OUT VI) a randomisednon-inferiority trial Lancet 2015 385 1527ndash1535

73 Freed LE Grande DA Lingbin Z et al Joint resurfacing using allo-graft chondrocytes and synthetic biodegradable polymer scaffoldsJ Biomed Mater Res 1994 28 891ndash899

74 Poirier Y Nawrath C Somerville C Production of polyhydrox-yalkanoates a family of biodegradable plastics and elastomers in

bacteria and plants Nat Biotechnol 1995 13 142ndash15075 Dias A Tsuru K Hayakawa S et al Crystallisation studies of

biodegradable CaO-P2O5 glass with MgO and TiO2 for boneregeneration applications Glass Technol 2004 45 78ndash79

76 Klein CPAT de Groot K Drissen AA et al Interaction ofbiodegradable β-whitlockite ceramics with bone tissue an in vivostudy Biomaterials 1985 6 189ndash192

77 Ikenaga M Hardouin P Lemaicirctre J et al Biomechanical charac-terization of a biodegradable calcium phosphate hydraulic cementa comparison with porous biphasic calcium phosphate ceramics JBiomed Mater Res 1998 40 139ndash144

78 Dias AG Lopes MA Santos JD et al In vivo performance ofbiodegradable calcium phosphate glass ceramics using the rabbitmodel histological and SEM observation J Biomater Appl 200620 253ndash266

79 Lee JH Lee CK Chang BS et al In vivo study of novel biodegrad-able and osteoconductive CaO-SiO2-B2O3 glass-ceramics JBiomed Mater Res 2006 77A 362ndash369

80 Song G Song S A possible biodegradable magnesium implant ma-terial Adv Eng Mater 2007 9 298ndash302

81 Kim WC Kim JG Lee JY et al Influence of Ca on the corrosionproperties of magnesium for biomaterials Mater Lett 2008 624146ndash4148

82 Li Z Gu X Lou S et al The development of binary Mg-Ca alloysfor use as biodegradablematerials within bone Biomaterials 200829 1329ndash1344

83 Wan Y Xiong G Luo H et al Preparation and characterization ofa new biomedical magnesium-calcium alloy Mater Des 2008 292034ndash2037

84 Seong JW Kim WJ Development of biodegradable Mg-Ca alloysheets with enhanced strength and corrosion properties throughthe refinement anduniformdispersion of theMg2Caphase by high-ratio differential speed rolling Acta Biomater 2015 11 531ndash542

85 Zhang S Li J Song Y et al In vitro degradation hemolysis andMC3T3-E1 cell adhesion of biodegradable Mg-Zn alloy Mater SciEng-C 2009 29 1907ndash1912

86 Li J Song Y Zhang S et al In vitro responses of human bone mar-row stromal cells to a fluoridated hydroxyapatite coated biodegrad-able Mg-Zn alloy Biomaterials 2010 31 5782ndash5788

87 Brar HS Wong J Manuel MV Investigation of the mechanical anddegradation properties of Mg-Sr and Mg-Zn-Sr alloys for use aspotential biodegradable implant materials J Mech Behav BiomedMater 2012 7 87ndash95

88 Bornapour M Muja N Shum-Tim D et al Biocompatibility andbiodegradability of Mg-Sr alloys the formation of Sr-substitutedhydroxyapatite Acta Biomater 2013 9 5319ndash5330

89 Gu XN Xie XH Li N et al In vitro and in vivo studies on aMg-Sr binary alloy system developed as a new kind of biodegrad-able metal Acta Biomater 2012 8 2360ndash2374

90 Haumlnzi AC Gerber I Schinhammer M et al On the in vitro andin vivo degradation performance and biological response of newbiodegradableMg-Y-Zn alloys Acta Biomater 2010 6 1824ndash1833

91 Chou DT Hong D Saha P et al In vitro and in vivo corrosioncytocompatibility and mechanical properties of biodegradableMg-Y-Ca-Zr alloys as implant materials Acta Biomater 2013 98518ndash8533

92 Zong Y Yuan G Zhang X et al Comparison of biodegradable be-haviors of AZ31 and Mg-Nd-Zn-Zr alloys in Hanks physiologicalsolution Mater Sci Eng-B 2012 177 395ndash401

93 Tie D Feyerabend FMuumlllerWD et al Antibacterial biodegradableMg-Ag alloys Eur Cell Mater 2013 25 284ndash298

94 VojtěchDKubaacutesek J Seraacutek J et al Mechanical and corrosion prop-

13 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

erties of newly developed biodegradable Zn-based alloys for bonefixation Acta Biomater 2011 7 3515ndash3522

95 Li H Yang H Zheng Y et al Design and characterizations of novelbiodegradable ternary Zn-based alloys with IIA nutrient alloyingelements Mg Ca and Sr Mater Des 2015 83 95ndash102

96 Liu X Sun J Yang Y et al Microstructure mechanical proper-ties in vitro degradation behavior and hemocompatibility of novelZn-Mg-Sr alloys as biodegradable metals Mater Lett 2016 162242ndash245

97 Wu C Qiu H Hu X et al Short-term safety and efficacy of thebiodegradable iron stent in mini-swine coronary arteries ChinMed J (Engl) 2013 126 4752ndash4757

98 Purnama A Hermawan H Champetier S et al Gene expressionprofile of mouse fibroblasts exposed to a biodegradable iron alloyfor stents Acta Biomater 2013 9 8746ndash8753

99 HermawanH Purnama A Dube D et al Fe-Mn alloys for metallicbiodegradable stents degradation and cell viability studies ActaBiomater 2010 6 1852ndash1860

100 Sheridan MH Shea LD Peters MC et al Bioabsorbable polymerscaffolds for tissue engineering capable of sustained growth factordelivery J Control Release 2000 64 91ndash102

101 Shawe S Buchanan F Harkin-Jones E et al A study on the rate ofdegradation of the bioabsorbable polymer polyglycolic acid (PGA)J Mater Sci 2006 41 4832ndash4838

102 Palmerini T Biondi-Zoccai G Della Riva D et al Clinical out-comes with bioabsorbable polymer- versus durable polymer-baseddrug-eluting and bare-metal stents J Am Coll Cardiol 2014 63299ndash307

103 Tanimoto S Serruys PW Thuesen L et al Comparison of in vivoacute stent recoil between the bioabsorbable everolimus-elutingcoronary stent and the everolimus-eluting cobalt chromium coro-nary stent insights from the ABSORB and SPIRIT trials CatheterCardiovasc Interv 2007 70 515ndash523

104 Tsuji H Sasaki H Sato H et al Neuron attachment properties ofcarbon negative-ion implanted bioabsorbable polymer of poly-lac-tic acid Nucl Instr Meth Phys Res Sect B-Beam Interact MaterAtoms 2002 191 815ndash819

105 Aikawa M Miyazawa M Okamoto K et al A novel treatment forbile duct injury with a tissue-engineered bioabsorbable polymerpatch Surgery 2010 147 575ndash580

106 WaksmanR Pakala R Kuchulakanti PK et al Safety and efficacy ofbioabsorbablemagnesium alloy stents in porcine coronary arteriesCatheter Cardiovasc Interv 2006 68 607ndash617

107 Di Mario C Griffiths H Goktekin O et al Drug-eluting bioab-sorbable magnesium stent J Interv Cardiol 2004 17 391ndash395

108 Erbel R Di Mario C Bartunek J et al Temporary scaffoldingof coronary arteries with bioabsorbable magnesium stents aprospective non-randomised multicentre trial Lancet 2007 3691869ndash1875

109 Schranz D Zartner P Michel-Behnke I et al Bioabsorbable metalstents for percutaneous treatment of critical recoarctation of theaorta in a newborn Catheter Cardiovasc Interv 2006 67 671ndash673

110 Gu X Zheng Y Cheng Y et al In vitro corrosion and biocompati-bility of binary magnesium alloys Biomaterials 2009 30 484ndash498

111 Hiromoto S InoueM Taguchi T et al In vitro and in vivo biocom-patibility and corrosion behaviour of a bioabsorbable magnesiumalloy coated with octacalcium phosphate and hydroxyapatite ActaBiomater 2015 11 520ndash530

112 Hiromoto S Tomozawa M Maruyama N Fatigue property of abioabsorbable magnesium alloy with a hydroxyapatite coatingformed by a chemical solution deposition J Mech Behav Biomed-ical Mater 2013 25 1ndash10

113 Bowen PK Drelich J Goldman J Zinc exhibits ideal physiologicalcorrosion behavior for bioabsorbable stents Adv Mater 2013 252577ndash2582

114 Liu X Sun J Yang Y et al In vitro investigation of ultra-pure Znand its mini-tube as potential bioabsorbable stent material MaterLett 2015 161 53ndash56

115 LinW Zhang G Cao P et al Cytotoxicity and its test methodologyfor a bioabsorbable nitrided iron stent J Biomed Mater Res 2015103 764ndash776

116 Coe JD Vaccaro AR Instrumented transforaminal lumbar inter-body fusion with bioresorbable polymer implants and iliac crestautograft Spine 2005 30 S76ndashS83

117 Ignatius AA Augat P Ohnmacht M et al A new bioresorbablepolymer for screw augmentation in the osteosynthesis of osteo-porotic cancellous bone a biomechanical evaluation J BiomedMater Res 2001 58 254ndash260

118 Krucoff MW Kereiakes DJ Petersen JL et al A novel biore-sorbable polymer paclitaxel-eluting stent for the treatment ofsingle and multivessel coronary disease J Am Coll Cardiol 200851 1543ndash1552

119 Kostopoulos L Karring T Guided bone regeneration in mandibu-lar defects in rats using a bioresorbable polymer Clin Oral Im-plants Res 1994 5 66ndash74

120 Dubok VA Bioceramicsmdashyesterday today tomorrow PowderMetall Metal Ceram 2000 39 381ndash394

121 Safronova T Kuznetsov A Korneychuk S et al Calcium phos-phate powders synthesized from solutions with [Ca2+][PO4

3minus]=1for bioresorbable ceramics Cent Eur J Chem 2009 7 184ndash191

122 Bohner M Bioresorbable ceramics In Buchanan FJ (Ed) Degra-dation Rate of Bioresorbable Materials Cambridge WoodheadPublishing 2008 95-114

123 Seitz JM Eifler R Stahl J et al Characterization ofMgNd2 alloy forpotential applications in bioresorbable implantable devices ActaBiomater 2012 8 3852ndash3864

124 WenCE Yamada Y Shimojima K et al Porous bioresorbable mag-nesium as bone substitute MSF 2003 419ndash422 1001ndash1006

125 Campos CM Muramatsu T Iqbal J et al Bioresorbable drug-elut-ing magnesium-alloy scaffold for treatment of coronary artery dis-ease Int J Mol Sci 2013 14 24492ndash24500

126 KirklandNT Birbilis NWalker J et al In-vitro dissolution ofmag-nesium-calcium binary alloys clarifying the unique role of calciumadditions in bioresorbable magnesium implant alloys J BiomedMater Res 2010 95B 91ndash100

127 Gastaldi D Sassi V Petrini L et al Continuum damage model forbioresorbable magnesium alloy devices mdashapplication to coronarystents J Mech Behav Biomed Mater 2011 4 352ndash365

128 Kitabata H Waksman R Warnack B Bioresorbable metal scaffoldfor cardiovascular application current knowledge and future per-spectives Cardiovasc Revasc Med 2014 15 109ndash116

Acknowledgments This work was supported by the National Key Re-search and Development Program of China (2016YFC1102402) NationalNatural Science Foundation of China (NSFC 51431002) and the NSFCand the Research Grants Council (RGC) of Hong Kong Joint ResearchScheme (51361165101 and 5161101031)

Author contributions Liu Y prepared the figures tables organized thereferences and wrote the paper Zheng Y provided the overall concept andrevised the manuscript Hayes B helped with the standard developmentand revised the manuscript All authors participated in the discussion

Conflict of interest The authors declare that they have no conflict ofinterest

14copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Yang Liu received his bachelor degree in materials science and engineering from Harbin engineering University in 2013Then he continued his study as a PhD candidate in Prof Yufeng Zhengrsquos Lab in Peking University His research interestsare mainly focused on the corrosion study of absorbable metallic biomaterials as well as the development of new kind ofMg-based biomaterials

Yufeng Zheng obtained his PhD degree from Harbin Institute of Technology in 1998 He is the National OutstandingYouth and Yangtze River scholar of China His research interests are focused on the development of novel biomaterials andapplication and design of biomedical devices

Byron Hayes an over 35 year employee of WL Gore has been involved in the commercial development of multiple ab-sorbable polymeric implants since the late 1980s Hayes started his standards development activities with ASTM in 2000where he is actively developing standards for polymeric and metallic absorbable implants In 2010 Hayes also becameinvolved with ISO Technical Committees TC150 and TC194 and is now convener of working groups focused on cardiovas-cular and metallic absorbable implants

可降解可吸收再吸收mdashmdash哪个是描述最终被人体吸收生物材料的最好词汇刘洋1 郑玉峰1 拜伦海耶斯2

摘要 关于最终被人体吸收的植入材料领域内文献采用的英文修饰词长期以来混乱且不同不仅造成文献检索困难同时模糊了研究人员的研究边界 此领域在法律法规标准中统一用词的确定为领域内的科学研究产品销售及产品使用说明奠定了基础 我们基于化学生态学材料学生物学微生物学和药学立足于使用习惯法律标准和市场对领域内使用已久的典型修饰词ldquo生物可降解rdquoldquo再吸收rdquo和ldquo可吸收rdquo进行了讨论和解释 总的来说尽管目前绝大多数修饰语实际想表达的意思相同作者认为ldquo可吸收rdquo这一英文修饰语是最恰当的修饰词 同时我们提议进一步规范和统一该领域修饰词的使用

15 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

  • Degradable absorbable or resorbablemdashwhat is the best grammatical modifier for an implant that is eventually absorbed by the body
  • Abstract
  • INTRODUCTION
    • Current situation
    • Standards development in advance
      • TERMINOLOGY
        • Overview of utilization of the terms ldquodegradationrdquoldquobiodegradationrdquo and ldquodegradablerdquoldquobiodegradablerdquo
        • Overview of utilization of the terms ldquoabsorptionrdquoldquobioabsorptionrdquo and ldquoabsorbablerdquoldquobioabsorbablerdquo
        • Overview of utilization of the terms ldquoresorptionrdquoldquobioresorptionrdquo and ldquoresorbablerdquoldquobioresorbablerdquo
        • Utilization and comparison of the terms ldquobiodegradable metalsrdquo and ldquoabsorbable metallic materialsrdquo
        • Summary quantification of the common Terms
          • DISCUSSION
            • Expertise inherent biases
            • Connotation and extension of noun forms ldquobiodegradation bioabsorption and bioresorptionrdquo and adjectives ldquobiodegradable bioabsorbable and bioresorbablerdquo
              • CONCLUDING REMARKS
              • References
              • Acknowledgements

specific biological activity [23] Another definition as thebiomaterial or medical device involving loss of their in-tegrity or performance when exposed to a physiological orsimulated environment which existed in some ISO Techni-cal Report was not recommended since no specific respectto biological activity mentioned [23]Beyond the category of biomaterials ldquodegradablerdquo in

pure chemistry was defined as qualifier to a substance thatcan undergo physical andor chemical deleterious changesof some properties especially of integrity under stressconditions [14] Thus degradable polymer is consideredwith macromolecules being able to undergo chain scis-sions resulting in a decrease of molar mass [14] BesidesASTM made a standard definition on ldquodegradablerdquo in thescope of soil rock and contained fluids as ldquoin erosioncontrol decomposes under biological chemical processesor ultraviolet stresses associated with typical applicationenvironmentsrdquo [29] Despite no specific emphasis onbiomaterials numerous publications used ldquodegradablerdquo to

modify metals polymers or compounds in tissue engineer-ing drug delivery and gene delivery [30ndash35] Meanwhilein some ASTM standard specifications the definition ofthe adjective ldquobiodegradablerdquo is given as capable of de-composing under natural conditions into elements foundin the nature [36ndash42] The active ASTM entries currentlywith ldquobiodegradationrdquo ldquodegradablerdquo and ldquobiodegradablerdquoin the title are summarized in Table 1 The adoptionsof ldquobiodegradationrdquo ldquodegradablerdquo and ldquobiodegradablerdquoby ASTM are historical generally in the classification ofecology or environmental protectionWhile the above listing provides evidence that the usage

of the term biodegradable is broad it is particularly notablethat almost all of the listed standards are not relevant toimplantable devices Instead the listing primarily reflectsusage directed toward the environmental degradation as-pect that is most commonly recognized within the broadernon-medical oriented population ASTM-F1635 a stan-dard specifically centered on the hydrolytic degradation

Table 1 Summary of the terms ldquobiodegradationrdquo ldquodegradablerdquo and ldquobiodegradablerdquo being utilized in ASTM titles (not limited to implant)

Terminology ASTM titles

ASTM D5864-11 Standard Test Method for Determining Aerobic Aquatic Biodegradation of Lubricants or TheirComponents

ASTM D6954-04(2013) Standard Guide for Exposing and Testing Plastics that Degrade in the Environment by aCombination of Oxidation and Biodegradation

ASTM D5511-12 Standard Test Method for Determining Anaerobic Biodegradation of Plastic Materials Under High-SolidsAnaerobic-Digestion Conditions

ASTM D6139-11 Standard Test Method for Determining the Aerobic Aquatic Biodegradation of Lubricants or TheirComponents Using the Gledhill Shake Flask

ASTM D7991-15 Standard Test Method for Determining Aerobic Biodegradation of Plastics Buried in Sandy MarineSediment under Controlled Laboratory Conditions

ASTM D5338-15 Standard Test Method for Determining Aerobic Biodegradation of Plastic Materials Under ControlledComposting Conditions Incorporating Thermophilic Temperatures

ASTM D6691-09 Standard Test Method for Determining Aerobic Biodegradation of Plastic Materials in the MarineEnvironment by a Defined Microbial Consortium or Natural Sea Water Inoculum

ASTM D5526-12 Standard Test Method for Determining Anaerobic Biodegradation of Plastic Materials Under AcceleratedLandfill Conditions

ASTM D7475-11 Standard Test Method for Determining the Aerobic Degradation and Anaerobic Biodegradation of PlasticMaterials under Accelerated Bioreactor Landfill Conditions

Biodegradation

ASTM D5988-12 Standard Test Method for Determining Aerobic Biodegradation of Plastic Materials in Soil

ASTM F1635-11 Standard Test Method for in vitro Degradation Testing of Hydrolytically Degradable Polymer Resinsand Fabricated Forms for Surgical Implants

ASTM D7444-11 Standard Practice for Heat and Humidity Aging of Oxidatively Degradable PlasticsDegradable

ASTM D3826-98(2013) Standard Practice for Determining Degradation End Point in Degradable Polyethylene andPolypropylene Using a Tensile Test

ASTM D7665-10(2014) Standard Guide for Evaluation of Biodegradable Heat Transfer Fluids

ASTM D8029-16 Standard Specification for Biodegradable Low Aquatic Toxicity Hydraulic FluidsBiodegradable

ASTM D7044-15 Standard Specification for Biodegradable Fire Resistant Hydraulic Fluids

4copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

testing of absorbable polyesters is the sole listed standardfrom ASTM Committee F04mdashMedical and Surgical Im-plants and thereby is directly relevant to implantable de-vices However this standard utilizes the term degradeand its derivatives specifically in reference to the process ofdegradation that occurs as a result of ester hydrolysis Con-versely the same standard uses the term absorbable to de-scribe a class of implants that are eventually absorbed by thebody which it defines as ldquoabsorbable adjmdashin the bodymdashaninitially distinct foreign material or substance that either di-rectly or through intended degradation can pass through orbe assimilated by cells andor tissuerdquo

Overview of utilization of the terms ldquoabsorptionrdquoldquobioab-sorptionrdquo and ldquoabsorbablerdquoldquobioabsorbablerdquoThe term ldquoabsorptionrdquo was recognized by IUPAC as theprocess of penetration and diffusion of a substance (ab-sorbate) into another substance (absorbent) as a result ofthe action of attractive phenomena The IUPAC defini-tion is within the scope of chemistry As for biomaterialsProf D Williams adopted the definition in Dorland Medi-cal Dictionary as the uptake of substances into or across tis-sues [23] For this kind of definition ldquoabsorptionrdquo empha-sizes the interaction of materials and human or animal tis-sue The same connotation is shared by its derivative wordsldquoabsorbablerdquo and ldquobioabsorbablerdquo as capable of being de-graded or dissolved and subsequently metabolized withinan organism [23] Besides the prefix ldquobio-rdquo is abridged as

it is redundant in the field of implantation [43] ASTM hasmade standard definition on ldquoabsorbablerdquo in the field of ab-sorbable polymers as well as absorbablemetals which it de-fines as ldquohellip an initially distinct foreign material or substancethat either directly or through intended degradation can passthrough or be metabolized or assimilated by cells andor tis-sue in the bodyrdquo [43] Table 2 summarizes the currently ac-tive ASTM standards and both United States and EuropeanPharmacopeia implantable device monographs that utilizethe word ldquoabsorbablerdquo in the title Distinctly different fromldquobiodegradablerdquo the utilization of ldquoabsorbablerdquo displays adistinct preference for use in describing this particular classof biomedical materials and devicesAs can be observed in both Table 1 and Table 3 the

well-established terminology for describing sutures is verybroadly based on the term absorbable with historicalapplication of the term to the original gut sutures andeven extending to permanent sutures through the ldquononab-sorbablerdquo descriptorAside from the language of standards organization the

terminology utilized by regulatory agencies is also of par-ticular relevance Through multiple laws and regulationsthe US-FDA is authorized to evaluate medical device man-ufacturers and their products The US Code of FederalRegulations (CFRs) that is specific to sutures legally de-scribes those regulated devices based on composition andthen designates both their product class and needs to meetUSP requirements While Table 3 demonstrates both a US-

Table 2 ldquoAbsorbablerdquo utilized in title entries for implantable device related standards

Terminology Title entries

ISOTS 171372014 Cardiovascular implants and extracorporeal systemsmdashCardiovascular absorbable implants

ISOTR 371372014 Biological evaluation of medical devicesmdashGuidance for absorbable implants

ASTM F3036-13 Standard Guide for Testing Absorbable Stents

ASTM F2902-16 Standard Guide for Assessment of Absorbable Polymeric Implants

ASTM F2502-16 Standard Specification and Test Methods for Absorbable Plates and Screws for Internal Fixation Implants

ASTM F1983-14 Standard Practice for Assessment of Selected Tissue Effects of Absorbable Biomaterials for Implant Applications

ASTM F3160-16 Standard Guide for Metallurgical Characterization of Absorbable Metallic Materials for Medical Implants

United States Pharmacopoeia (USP 39NF 34) monographldquoAbsorbable Surgical Suturerdquo

United States Pharmacopoeia (USP 39NF 34) monographldquoNonabsorbable Surgical Suturerdquo

European Pharmacopoeia (88)ldquoSterile non-absorbable suturesrdquo ndash 1118

European Pharmacopoeia (88)ldquoSterile synthetic absorbable braided suturesrdquo - 1122

Absorbable

European Pharmacopoeia (88)Sterile synthetic absorbable monofilament sutures ndash 1123

5 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Table 3 US-FDA suture product codes and accompanying citation of US CFRsa)

Suture name Regulation Product code

Absorbable polydioxanone surgical (PDS) suture 21 CFR8784840 NEW

Absorbable poly(glycolideL-lactide) surgical suture 21 CFR8784493 GAM

Absorbable gut suture 21 CFR8784830 GAL

Nonabsorbable poly(ethylene terephthalate) suture 21 CFR8785000 GAT

Nonabsorbable polypropylene surgical suture 21 CFR8785010 GAW

Nonabsorbable polyamide surgical suture 21 CFR8785020 GAR

Natural nonabsorbable silk surgical suture 21 CFR8785030 GAP

Stainless steel surgical suture 21 CFR8784495 GAQ

Nonabsorbable expanded polytetrafluoroethylene (ePTFE)surgical suture

21 CFR8785030 NBY

a) Note this table selects abbreviated results obtained from online search for the implant device term ldquosuturerdquo that was conducted on 6 Aug 2016 athttpwwwaccessdatafdagovscriptscdrhcfdocscfPCDclassificationcfm

FDA and a US Code of Federal Regulations preference forabsorbable terminology when referring to sutures Table4 shows an expansion of that preference to include a to-tal of 30 absorbable implant product classifications each ofwhich is assigned to a relevant Federal regulation that uti-lizes the term ldquoabsorbablerdquoIn short ldquoabsorbablerdquo is both a historically well estab-

lished and currently relevant term in both the regulationand standardization of implants that are intentionally ab-sorbed by the body

Overview of utilization of the terms ldquoresorptionrdquoldquobiore-sorptionrdquo and ldquoresorbablerdquoldquobioresorbablerdquoIn the scope of chemistry the term ldquoresorptionrdquo was used toillustrate the total elimination of a substance from its initialplace caused by physical andor chemical phenomena [14]Besides the understanding from pure chemistry ldquoresorp-tionrdquo is more recognized involved in the metabolic activi-ties in vivo For example ldquoresorptionrdquo is considered as theldquoabsorptionrdquo into the circulatory system of cells or tissuewhich usually includes bone resorption tooth resorptionand vanishing twin [44] In the biomedical scope Prof DWilliams used themeaning in DorlandMedical Dictionaryas ldquolysis and assimilation of a substance as of bonerdquo [23]ldquoBioresorptionrdquo is more common when describing the invivo process of a certain foreign material The ISO definedldquobioresorptionrdquo as a process by which biomaterials are de-graded in the physiological environment and the by-prod-uct are eliminated or completely bioabsorbed [23] Thusaccording to this interpretation the bioresorption processincludes material removal in vivo either by cellular activ-ity or not Conversely Taberrsquos Cyclopedic Medical Dictio-nary [45] describes the term ldquoresorbrdquo as themeaning ldquoto ab-

sorb againrdquomdashsomething that live tissue does but not some-thing any implant is known to domdashbe it permanent or ab-sorbableAs for the adjectives ldquobioresorbablerdquo and ldquoresorbablerdquo

there is no difference when used to describe a kind of ma-terials which have the ability of resorption This is ascribedto the fact that ldquoresorptionrdquo itself already has been well rec-ognized as a biological process [23] Currently there is noASTM entries used ldquoresorbablerdquo or ldquobioresorbablerdquo in thetitle

Utilization and comparison of the terms ldquobiodegradablemetalsrdquo and ldquoabsorbable metallic materialsrdquoldquoBiodegradablemetalsrdquo generally include themetalsMg Feand Zn and their alloys and composites They can be de-fined as metals that assist with tissue healing and are thenexpected to gradually corrode and release corrosion prod-ucts in vivowith an appropriate host response and then dis-solve completely with no implant residues [46] As a resultand different from traditional ldquobio-inertrdquometallic biomate-rials (eg Ti and Co based alloys) that release limited cor-rosion products [47] metabolic reactions besides inflam-mation can be expected to occur between the biodegrad-able metal and the host body after implantation Addition-ally the corrosion-based degradation mechanism of thesematerials is inherently different from that of either bioce-ramics or polymers which has resulted in limited to nostandardized guidance available from either ASTM or ISOInstead of the term ldquobiodegradable metalrdquo the recently

published and first absorbable metal related standardASTM F3160 utilizes the more inclusive word ldquoabsorbablerdquowithin the phrase ldquoabsorbable metallic materialsrdquo andagain defines the term as ldquohellip an initially distinct foreign

6copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Table 4 US-FDA absorbable implant related product codes descriptions and accompanying CFRsa)

Product code Device Device class Regulation number Regulation description

OMT Absorbable lung biopsy plug 2 [8784755] Absorbable lung biopsy plug

LMF Agent absorbable hemostatic collagen based 3 [8784490] Absorbable hemostatic agent and dressing

LMG Agent absorbable hemostatic non-collagen based 3 [8784490] Absorbable hemostatic agent and dressing

MRY Appliances and accessories fixation bone absorbable singlemultiple component 2 [8883040] Smooth or threaded metallic bone fixation fastener

PBQ Fixation non-absorbable or absorbable for pelvic use 2 [8844530] Obstetric-gynecologic specialized manual instrument

HQJ Implant absorbable (scleral buckling methods) 2 [8863300] Absorbable implant (scleral buckling method)

OWT Mesh surgical absorbable abdominal hernia 2 [8783300] Surgical mesh

OXM Mesh surgical absorbable fistula 2 [8783300] Surgical mesh

OXI Mesh surgical absorbable large abdominal wall defects 2 [8783300] Surgical mesh

OXL Mesh surgical absorbable organ support 2 [8783300] Surgical mesh

OWW Mesh surgical absorbable orthopaedics reinforcement of tendon 2 [8783300] Surgical mesh

OXF Mesh surgical absorbable plastic and reconstructive surgery 2 [8783300] Surgical mesh

OXC Mesh surgical absorbable staple line reinforcement 2 [8783300] Surgical mesh

OWZ Mesh surgical absorbable thoracic chest wall reconstruction 2 [8783300] Surgical mesh

OWU Mesh surgical non-absorbable diaphragmatic hernia 2 [8783300] Surgical mesh

OWR Mesh surgical non-absorbable facial implants for plastic surgery 2 [8783300] Surgical mesh

OXJ Mesh surgical non-absorbable large abdominal wall defects 2 [8783300] Surgical mesh

OWX Mesh surgical non-absorbable orthopaedics reinforcement of tendon 2 [8783300] Surgical mesh

OXG Mesh surgical non-absorbable plastic and reconstructive surgery 2 [8783300] Surgical mesh

OXD Mesh surgical non-absorbable staple line reinforcement 2 [8783300] Surgical mesh

OXA Mesh surgical non-absorbable thoracic chest wall reconstruction 2 [8783300] Surgical mesh

LBP Replacement ossicular (stapes) using absorbable gelatin material 2 [8743450] Partial ossicular replacement prosthesis

OLL Septal staplerabsorbable staples 2 [8784750] ImplanTABLE staple

MNU Staple absorbable 2 [8883030] Singlemultiple component metallic bone fixationappliances and accessories

GAK Suture absorbable 2 [8784830] Absorbable surgical gut suture

GAL Suture absorbable natural 2 [8784830] Absorbable surgical gut suture

HMO Suture absorbable ophthalmic 3

GAN Suture absorbable synthetic 2 [8784830] Absorbable surgical gut suture

GAM Suture absorbable synthetic polyglycolic acid 2 [8784493] Absorbable poly(glycolidel-lactide) surgical suture

NEW Suture surgical absorbable polydioxanone 2 [8784840] Absorbable polydioxanone surgical suture

a) Note the results obtained from online search for the device term ldquoabsorbablerdquo that was conducted on 6 Aug 2016 at httpwwwaccessdatafdagovscriptscdrhcfdocscfPCDclassifica-tioncfm

7 copy

ScienceChina

Pressand

Springer-VerlagBerlin

Heidelberg 2017

SCIENCECH

INAMaterials

REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

material or substance that either directly or through in-tended degradation can pass through or be metabolized orassimilated by cells andor tissuerdquo The standardrsquos nomen-clature appendix further elaborates on its preference forldquoabsorbablerdquo since the prefix ldquobio-rdquo is redundant in thecontext of implant applications [43]Clearly these two terms of ldquobiodegradable metalsrdquo and

ldquoabsorbable metallic materialsrdquo share the same connota-tion which defines the completemission of an intentionallydegradable material when implanted in vivo In the contextof biodegradable metalsabsorbable metallic materialsthe process includes the corrosion caused by body fluida host response caused by corrosion products followedby dissolutionabsorption and finally improved tissuehealing The ldquobiodegradationrdquo instead of ldquobiocorrosionrdquois used to distinguish this new kind of metals which canfully dissolve in vivo with no implant residues Besidesbiodegradation process the following dynamic process ofdissolutionabsorption also starts in vivo For exampledissolved Mg2+ is considered to enhance the integrin me-diated human-bone-derived cell adhesion and affect newbone formation [48] The metabolic reaction is also crucialand even more important for biodegradable metals as it ishelpful It is another distinction from traditional metalsused for biomedical application In fact the different usagehabit forming of ldquobiodegradablerdquo or ldquoabsorbablerdquoldquobioab-sorbablerdquo may be more related with the study field theresearchers in Taking the ldquoabsorbablerdquo metallic stent asan example (Fig 2) once the ldquoabsorbablerdquo metallic stentwas implanted into blood vessel ldquocorrosionrdquo of biometal

begins The corrosion products including debris hydro-gen (for Mg-based metals) metallic ions and hydroxylconvert the local environment and diffuse into the bloodvessel wall Some corrosion products can be biologicallybeneficial For instance the diffused and absorbed Zn2+

can potentially play a positive role in dealing with athero-sclerosis [49] Along with the corrosion process healingprocesses such as endothelialization may become en-hanced In summary and within the context of absorbablemetals the adjectives ldquodegradablerdquo and ldquoabsorbablerdquo referto the nature of the biodegradation products of the mate-rialdevice being metabolically absorbed an attribute ofthe host (animal or human body) regardless of whetherthe implant degrades corrodes hydrolyzes or dissolves[50ndash52]

Summary quantification of the common TermsFig 3a shows preliminary searching results in Webof Knowledge using ldquodegradablerdquo ldquoabsorbablerdquo or ldquore-sorbablerdquo along with ldquomaterialrdquo as key words Theutilization of ldquodegradablerdquo is a bit more frequently thanldquoabsorbablerdquo but that of ldquoresorbablerdquo steps down Mean-while the counterpart searching result when using ldquobiordquo asprefix to the adjectives along with ldquomaterialrdquo as keywordsare presented in Fig 3b ldquoBiodegradable materialrdquo is themost common utilization which holds 91 among the ex-pression approach This is also due to the fact that besidesthe common utilization in biomaterials ldquobiodegradablerdquois also used in a wide range of applications such as cleanenvironment and ecology [5354]

Figure 2 Different point of views on the biodegradationabsorption process

8copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Figure 3 Searching results in Web of Knowledge from all databases (a) with the total searched publication numbers by ldquodegradablerdquo+ ldquomaterialrdquoldquoabsorbablerdquo+ ldquomaterialrdquo and ldquoresorbablerdquo+ ldquomaterialrdquo as 100 (b) the total searched publication numbers by ldquobiodegradablerdquo+ ldquomaterialrdquo ldquobioab-sorbablerdquo+ ldquomaterialrdquo and ldquobioresorbablerdquo+ ldquomaterialrdquo as 100

DISCUSSION

Expertise inherent biasesAs previously mentioned biomaterial is an interdiscipli-nary field fascinating researchers with specialty from dif-ferent backgrounds Different backgrounds as well as dif-ferent research point of interests may be one of the reasonsfor using different terminologies Materials scientists tendto focus on the materialdevice itself leading to their usageof ldquobiodegradablerdquo to illustrate what happens to the deviceThey pay more attention to the process such as hydroly-sis corrosion debris degradation products and the changeof surface morphology resulting in the researching inter-ests of ldquomaterial biodegradationrdquo In contrast surgeons andbiomedical researchers tend to be concerned more on thehost response and healing process They are curious aboutthe absorption of various degradation products of the im-planted materialdevice and related metabolism mecha-nism and thereby prefer to use the term ldquoabsorbablerdquo toillustrate what happens to the device As known somema-terials may only undergo biodegradation but the corrosionproducts still have no influence on the metabolic activitiesFor example cellulose is considered as ldquodietary fiberrdquowhichcannot be digested and absorbed by human body but is be-nign for human body [55] Some coating tablets for drug ordrug delivery systems made from cellulose and its deriva-tives are quite frequently utilized or investigated [5657]The polymer and derivatives of cellulose can only be de-graded but not be absorbed by human body [58] For suchmaterials the adjective ldquoabsorbablerdquo or ldquobioabsorbablerdquo isnot appropriateOverall once the materialsdevices are implanted into

the human body the ldquobiocorrosionrdquobiodegradationrdquoprocess happens immediately no matter to what degreeat the same time the host will biologically response to the

corrosiondegradation products through the absorptionmetabolism and excretion processes So for the samestory the majority of materials scientists would report itby ldquobiodegradabledegradationrdquo way whereas the majorityof medical doctors would report it by ldquoabsorbableab-sorptionrdquo way In nature the two terms ldquobiodegradablemetalsrdquo and ldquoabsorbable metallic materialsrdquo share the sameconnotation and are mutually replaceable

Connotation and extension of noun forms ldquobiodegradationbioabsorption and bioresorptionrdquo and adjectivesldquobiodegradable bioabsorbable and bioresorbablerdquoThe three noun forms of the terms illustrate the processwhile their adjectival derivatives were used to describe thegroup of materials with such certain capabilities For thestudy on biomaterials polymer researchers use ldquodegrada-tionbiodegradationrdquo when there is proved chain scissionprocess Besides they differentiate ldquobiodegradationrdquo andldquodegradationrdquo by confirmed metabolic activities betweenthe materials and cells or tissues Regarding to the fouradjectives ldquobiodegradablerdquo ldquobioabsorbablerdquo and ldquobiore-sorbablerdquo the term ldquobiocorrodiblerdquo is only used in scientificpapers on iron based materials and some patents on mag-nesium based materials The common usage of termsldquobiodegradablerdquo ldquobioabsorbablerdquo and ldquobioresorbablerdquo withrespect to the biomaterial research area is shown in Table 5The results reveal a widespread usage of ldquobiodegradablerdquo inboth polymers and magnesium based metals Varies typesof materials were reported as biomaterials Besides thereare also reports of ldquobiodegradablerdquo polymers for ecologyand environmental protection which indicates a furtherusage scope of ldquobiodegradablerdquo not only for implants anddevices Besides ldquobioresorbablerdquo is also utilized in all theresearch fields of polymers ceramics andmetals Howeverno current work used ldquobioabsorbablerdquo as grammatical

9 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Table 5 Current reported usage of terms ldquobiodegradablerdquo ldquobioabsorbablerdquo and ldquobioresorbablerdquoTerminology Category Materials Applications

PLA-PEG-biotin PLGA Controlled cell engineering [5960]Porous PLGA Tissue engineering [61ndash63]

PLGA-PEG-PLGA Injective thermosensitive hydrogel [64]PLGA Nerve guidance [65]

Fibronectin (Fn)-coated PLLA P(LLA-CL) Enhanced growth of endothelial cells [6066]PEG tethered PPF [67]

PDMS Drug delivery [68]PGA Tissue engineering [69]

Undefined Coronary stent [70ndash72]PGA Joint resurfacing [73]

Polymers

PHA Ecology and environmental protection [74]CaO-P2O5 glass Bone regeneration [75]β-Whitlockite Bone regeneration [76]

Calcium phosphate hydraulic cement Bone regeneration [77]Calcium

phosphate glass ceramicsBone regeneration [78]

Ceramics

CaO-SiO2-B2O3 glass-ceramics Bone regeneration [79]Pure Mg Implant material [80]

Mg-Ca-based Bone regeneration [81ndash84]Mg-Zn-based Bone regeneration [338586]Mg-Sr-based Bone regeneration [87ndash89]Mg-RE-based Vascular stent [90ndash92]

Mg and its metals

Mg-Ag-based [93]Zn-Mg Zn-Ca Zn-Sr [9495]Zn and its metals Zn-Mg-Sr [96]

Fe [9798]

Biodegradable

Fe and its metals Fe-Mn [99]PLLA PLG PGA Molecule delivery [100]

PGA Suture [101]Undefined Drug-eluting stent [102103]

PLA Neuron attachment [104]Polymers

PLA and PCL reinforced with PGA fibers Bile duct patch [105]Mg-RE based Coronary stent [106ndash109]

Binary Mg alloys [110]Mg and its metalsMg-Al-based [111112]

Zn and its metals Pure Zinc [113114]Fe and its metals Nitrided iron [115]

PLDLA Transforaminal lumbar interbody fusion [116]Alkylene bis(dilactoyl)-methacrylate modified polymer Bone screw augmentation [117]

Undefined Coronary stent [118]PHB Mandibular defects regeneration [119]HA Bone regeneration [120]Ceramics Calcium phosphate [121122]

MgNd2 Stent material [123]Porous Mg Bone substitute [124]Mg-RE Coronary stent [125]Mg-Ca Orthopedic application [126]

Mg and its metals

Mg-based Finite element analysis [127]

Bioabsorbable

Fe and its metals Pure Fe [128]

10copy

ScienceChina

Pressand

Springer-VerlagBerlin

Heidelberg 2017

REVIEWSCIENCE

CHINA

Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

modifier to bioceramics In addition as previouslyillustrated the prefix ldquobiordquo of ldquobioabsorbablerdquo and ldquobiore-sorbablerdquo are abridged hereafter discussion will concen-trate on ldquobiocorrodiblerdquo ldquobiodegradablerdquo ldquoabsorbablerdquo andldquoresorbablerdquoSince absorbable technologies are increasingly utilized

in numerous new and broader implant applications it be-comes more important to not acquiesce in addressing his-torical problems and instead actively move forward towardutilizing standardized language that is both technically ac-curate and unified in itsmeaning Preferred language needsto accurately communicate the concept To achieve the uni-fying goal of harmonized terminology themedical and sci-entific communities need to not solely look at materialschemistry or even biomaterials alone but to instead lookat term selection both across and within the context of thebroader medical disciplinemdashthe location where the resultsof implant technology development actually reaches themarketplace where therapies are brought to those in needNomenclature solutions need to both understand and re-spond to the context of terms across adjacent technologieswhich means to address needs from the perspectives of thebiomaterial researcher the deviceproduct developer thesurgeonclinician user the regulator and last but not leastthe patientgeneral public who is the direct beneficiary ofthe developed technologyA better understanding of these terminologies is neces-

sary and beneficial to the field Therefore the definitionson ldquodegradablerdquo ldquoabsorbablerdquo ldquoresorbablerdquo and relatedterms proposed by different organizations in differentfields have been summarized and discussed with the con-notation and extension of each term being compared andthe criteria being proposed

CONCLUDING REMARKSHerein given both the searching problem on the Internetand ambiguity in meanings the usage of grammaticalmodifiers to describe biomaterials that is eventually ab-sorbed by human body has been enumerated based onusage habits laws standards and markets In summaryldquodegradablerdquoldquobiodegradablerdquo are the most frequently usedgrammatical modifier not only in metals but also poly-mers as such kind of biomaterials ldquoBiodegradationrdquo andldquobiodegradablerdquo define the change of the materialdevicewell in the research of biomaterials but they are alsoadopted in other fields such as ecology and environmentalprotection Meanwhile ldquoresorbablerdquoldquobioresorbablerdquo havelong been recognized in the biological research and theldquoresorptionrdquo itself has been widely accepted as a biological

reaction The utilization of ldquoresorbablerdquoldquobioresorbablerdquowas found to be not as frequent as the counterpartsldquodegradablerdquoldquobiodegradablerdquo and ldquoabsorbablerdquoldquobioab-sorbablerdquo Such usage is accurate for osteoclast driven boneresorption but is inappropriate for implants that do notcarry the potential to grow back into their original formOtherwise despite it is not the most frequently used termldquoabsorbablerdquoldquobioabsorbablerdquo concentrates more on thehost metabolism to the foreign biodegradation productsof the implanted materialdevice compared with ldquodegrad-ablerdquoldquobiodegradablerdquo ldquoAbsorbablerdquo is defined in the scopeof biomaterials by different organizations and their publi-cations and also adopted by ASTM to illustrate ldquoabsorbablepolymerrdquo It is the most historically established the mostbroadly applicable (includes dissolvable devices that donot degrade) the most specific to medical applicationsand is the formal legal descriptor for most implant devicesConsidering the usage history common utilization in lawand standards as well as the scientific meaning in essenceldquoabsorbablerdquo can be better among other grammaticalmodifiers for description of an implant that is eventuallyabsorbed by the body which is recommended by theauthors for a further internationally-unified usage

Received 28 February 2017 accepted 27 March 2017published online 26 April 2017

1 Mackenzie D The history of sutures Med Hist 1973 17 158ndash1682 Hench LL Bioceramics J Am Ceramic Soc 2005 81 1705ndash17283 Hench LL Bioceramics from concept to clinic J AmCeramic Soc

1991 74 1487ndash15104 Windhagen H Radtke K Weizbauer A et al Biodegradable

magnesium-based screw clinically equivalent to titanium screw inhallux valgus surgery short term results of the first prospectiverandomized controlled clinical pilot study BioMed Eng OnLine2013 12 62

5 Schildwaumlchter M Biotronik announces CE mark for magmaristhe first clinically-proven bioresorbable magnesium scaffoldhttpwwwmagmariscomennewsroomjune-15-2016

6 Shalaby SW Burg KJL Bioabsorbable polymers update degrada-tion mechanisms safety and application J App Biomater 1995 6219ndash221

7 Vert M Li SM Spenlehauer G et al Bioresorbability and biocom-patibility of aliphatic polyesters J Mater Sci-Mater Med 1992 3432ndash446

8 Vert M Degradable and bioresorbable polymers in surgery and inpharmacology beliefs and facts J Mater Sci-Mater Med 2009 20437ndash446

9 Benicewicz BC Hopper PK Review polymers for absorbablesurgical suturesmdashPart I J Bioactive Compatible Polym 1990 5453ndash472

10 Barrows HT Synthetic bioabsorbable polymers In Szycher M(Ed) High Performance Biomaterials A Complete Guide toMed-ical and Pharmceutical Applications Boca Raton CRC PRESS1991 243ndash257

11 Weiler A Hoffmann RFG Staumlhelin AC et al Biodegradable

11 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

implants in sports medicine the biological base Arthroscopy-JArthroscopic Related Surgery 2000 16 305ndash321

12 Ikada Y Tsuji H Biodegradable polyesters for medical and ecolog-ical applications Macromol Rapid Commun 2000 21 117ndash132

13 Ashammakhi N Peltoniemi H Waris E et al Developments incraniomaxillofacial surgery use of self-reinforced bioabsorbableosteofixation devices Plast Reconstr Surg 2001 108 167ndash180

14 Vert M Doi Y Hellwich KH et al Terminology for biorelatedpolymers and applications (IUPACRecommendations 2012) PureAppl Chem 2012 84 377ndash410

15 The United States Pharmacopeial Convention The Second Sup-plement to the Pharmacopeia of the United States of America 11thdecennial revision (USP XI-1939 Supplement) 1939

16 Truhlsen SM The recession operation histopathologic responseand suture reaction and absorption Trans Am Ophthalmol Soc1965 63 626ndash677

17 USP in US Law httpwwwusporgprintabout-usplegal-recog-nitionusp-us-law

18 USP develops and publishes standards for drug substances drugproducts excipients and dietary supplements in the United StatesPharmacopeia-National Formulary (USP-NF)

19 United States Public Law 94-295 197620 United States Pharmacopeia httpwwwusporg21 British Pharmacopeia httpswwwpharmacopoeiacom22 European Pharmacopoeia httponlinepheurorgENentryhtm23 Williams DF The Williams Dictionary of Biomaterials Liverpool

Liverpool University Press 199924 httpsenwikipediaorgwikiBiodegradation25 Jones RG Kahovec J Stepto R et al Compendium of Polymer

Terminology and Nomenclature IUPAC Recommendations 2008Cambridge RSC Publishing 2009

26 Higashi S Yamamuro T Nakamura T et al Polymer-hydroxyap-atite composites for biodegradable bone fillers Biomaterials 19867 183ndash187

27 de Groot K Bioceramics of Calcium Phosphate Boca Raton CRCPress 1983

28 Hollinger JO Battistone GC Biodegradable bone repair materialssynthetic polymers and ceramics ClinOrthopRelat Res 1986 207290ndash306

29 ASTMD653-14 Standard Terminology Relating to Soil Rock andContained Fluids ASTM International West Conshohocken PA2014 httpswwwastmorgStandardsD653htm

30 Witte F Hort N Vogt C et al Degradable biomaterials based onmagnesium corrosion Curr Opin Solid State Mater Sci 2008 1263ndash72

31 Lynn DM Langer R Degradable poly(β-amino esters) synthesischaracterization and self-assemblywith plasmidDNA JAmChemSoc 2000 122 10761ndash10768

32 Cima LG Vacanti JP Vacanti C et al Tissue engineering by celltransplantation using degradable polymer substrates J BiomechEng 1991 113 143ndash151

33 Zhang S Zhang X Zhao C et al Research on an Mg-Zn alloy as adegradable biomaterial Acta Biomater 2010 6 626ndash640

34 Anseth KS Metters AT Bryant SJ et al In situ forming degradablenetworks and their application in tissue engineering and drug de-livery J Control Release 2002 78 199ndash209

35 Forrest ML Koerber JT Pack DW A degradable polyethyleniminederivative with low toxicity for highly efficient gene delivery Bio-conjugate Chem 2003 14 934ndash940

36 ASTM E2747-11 Standard Specification for Evaluation and Selec-tion of Onsite Offices for Environmentally Sustainable MeetingsEvents Trade Shows and Conferences ASTM International

West Conshohocken PA 2011 httpswwwastmorgStan-dardsE2747htm

37 ASTM E2745-11 Standard Specification for Evaluation andSelection of Audio Visual (AV) and Production for Environ-mentally Sustainable Meetings Events Trade Shows and Con-ferences ASTM International West Conshohocken PA 2011httpswwwastmorgStandardsE2745htm

38 ASTM E2746-11 Standard Specification for Evaluation andSelection of Communication and Marketing Materials for En-vironmentally Sustainable Meetings Events Trade Shows andConferences ASTM International West Conshohocken PA 2011httpswwwastmorgStandardsE2746htm

39 ASTM E2741-11 Standard Specification for Evaluation and Se-lection of Destinations for Environmentally Sustainable MeetingsEvents Trade Shows and Conferences ASTM InternationalWest Conshohocken PA 2011 httpswwwastmorgStan-dardsE2741htm

40 0 ASTM E2773-11 Standard Specification for Evaluation andSelection of Food and Beverage for Environmentally SustainableMeetings Events Trade Shows and Conferences ASTM Interna-tional West Conshohocken PA 2011 httpswwwastmorgStan-dardsE2773htm

41 ASTM E2742-11 Standard Specification for Evaluation and Selec-tion of Exhibits for Environmentally Sustainable Meetings EventsTrade Shows and Conferences ASTM International West Con-shohocken PA 2011 httpswwwastmorgStandardsE2742htm

42 ASTM E2774-11 Standard Specification for Evaluation and Selec-tion of Venues for Environmentally Sustainable Meetings EventsTrade Shows and Conferences ASTM International West Con-shohocken PA 2011 httpswwwastmorgStandardsE2774htm

43 ASTM F2902-12 Standard Guide for Assessment of AbsorbablePolymeric Implants ASTM International West ConshohockenPA 2012 httpswwwastmorgStandardsF2902htm

44 httpsenwikipediaorgwikiResorption45 Venes D Tabers Cyclopedic Medical Dictionary 22th edition

Philadelphia F A Davis Company 201346 Zheng YF Gu XN Witte F Biodegradable metals Mater Sci Eng-

R-Rep 2014 77 1ndash3447 Hanawa T Metal ion release from metal implants Mater Sci

Eng-C 2004 24 745ndash75248 Zreiqat H Howlett CR Zannettino A et al Mechanisms of mag-

nesium-stimulated adhesion of osteoblastic cells to commonly usedorthopaedic implants J Biomed Mater Res 2002 62 175ndash184

49 Little PJ Bhattacharya R Moreyra AE et al Zinc and cardiovascu-lar disease Nutrition 2010 26 1050ndash1057

50 Seager H Drug-delivery products and the Zydis fast-dissolvingdosage form J Pharm Pharmacol 1998 50 375ndash382

51 Shikinami Y Shape-memory biodegradable and absorbable mate-rial US Patent No 6281262 2001-8-28

52 Huitema TW Knight GW Ransick MH Schulze DR Surgical im-plant with preferential corrosion zone US Patent No 79059022011-3-15

53 Luzier WD Materials derived from biomassbiodegradable mate-rials Proc Natl Acad Sci USA 1992 89 839ndash842

54 Gross RA Kalra B Biodegradable polymers for the environmentScience 2002 297 803ndash807

55 Trumbo P Schlicker S Yates AA et al Dietary reference intakesfor energy carbohydrate fiber fat fatty acids cholesterol proteinand amino acids J Am Diet Assoc 2002 102 1621ndash1630

56 Chambin O Champion D Debray C et al Effects of different cel-lulose derivatives on drug release mechanism studied at a prefor-mulation stage J Control Release 2004 95 101ndash108

12copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

57 Fundueanu G Constantin M Esposito E et al Cellulose acetatebutyrate microcapsules containing dextran ion-exchange resinsas self-propelled drug release system Biomaterials 2005 264337ndash4347

58 Maumlrtson M Viljanto J Hurme T et al Is cellulose sponge degrad-able or stable as implantation material An in vivo subcutaneousstudy in the rat Biomaterials 1999 20 1989ndash1995

59 Patel N Padera R Sanders GH et al Spatially controlled cell en-gineering on biodegradable polymer surfaces The FASEB journal1998 12 1447ndash1454

60 Goldstein A Effect of convection on osteoblastic cell growth andfunction in biodegradable polymer foam scaffolds Biomaterials2001 22 1279ndash1288

61 Wu L Ding J In vitro degradation of three-dimensional porouspoly(DL-lactide-co-glycolide) scaffolds for tissue engineeringBiomaterials 2004 25 5821ndash5830

62 Wu L Ding J Effects of porosity and pore size on in vitro degra-dation of three-dimensional porous poly(DL-lactide-co-glycolide)scaffolds for tissue engineering J Biomed Mater Res 2005 75A767ndash777

63 Pan Z Ding J Poly(lactide-co-glycolide) porous scaffolds for tissueengineering and regenerative medicine Interface Focus 2012 2366ndash377

64 Yu L Zhang Z Zhang H et al Biodegradability and biocompati-bility of thermoreversible hydrogels formed from mixing a sol anda precipitate of block copolymers in water Biomacromolecules2010 11 2169ndash2178

65 Wen X Tresco PA Fabrication and characterization of permeabledegradable poly(DL-lactide-co-glycolide) (PLGA) hollow fiberphase inversion membranes for use as nerve tract guidance chan-nels Biomaterials 2006 27 3800ndash3809

66 Chu CFL Lu A Liszkowski M et al Enhanced growth of animaland human endothelial cells on biodegradable polymers BBA-GenSubjects 1999 1472 479ndash485

67 Jo S Engel PS Mikos AG Synthesis of poly(ethylene glycol)-teth-ered poly(propylene fumarate) and its modification with GRGDpeptide Polymer 2000 41 7595ndash7604

68 Park JH Allen MG Prausnitz MR Biodegradable polymer mi-croneedles fabrication mechanics and transdermal drug deliveryJ Control Release 2005 104 51ndash66

69 Freed LE Vunjak-Novakovic G Biron RJ et al Biodegradablepolymer scaffolds for tissue engineering Nat Biotechnol 1994 12689ndash693

70 Windecker S Serruys PW Wandel S et al Biolimus-eluting stentwith biodegradable polymer versus sirolimus-eluting stent withdurable polymer for coronary revascularisation (LEADERS) arandomised non-inferiority trial Lancet 2008 372 1163ndash1173

71 Stefanini GG Kalesan B Serruys PW et al Long-term clinicaloutcomes of biodegradable polymer biolimus-eluting stents ver-sus durable polymer sirolimus-eluting stents in patients with coro-nary artery disease (LEADERS) 4 year follow-up of a randomisednon-inferiority trial Lancet 2011 378 1940ndash1948

72 Raungaard B Jensen LO Tilsted HH et al Zotarolimus-elutingdurable-polymer-coated stent versus a biolimus-eluting biodegrad-able-polymer-coated stent in unselected patients undergoing per-cutaneous coronary intervention (SORT OUT VI) a randomisednon-inferiority trial Lancet 2015 385 1527ndash1535

73 Freed LE Grande DA Lingbin Z et al Joint resurfacing using allo-graft chondrocytes and synthetic biodegradable polymer scaffoldsJ Biomed Mater Res 1994 28 891ndash899

74 Poirier Y Nawrath C Somerville C Production of polyhydrox-yalkanoates a family of biodegradable plastics and elastomers in

bacteria and plants Nat Biotechnol 1995 13 142ndash15075 Dias A Tsuru K Hayakawa S et al Crystallisation studies of

biodegradable CaO-P2O5 glass with MgO and TiO2 for boneregeneration applications Glass Technol 2004 45 78ndash79

76 Klein CPAT de Groot K Drissen AA et al Interaction ofbiodegradable β-whitlockite ceramics with bone tissue an in vivostudy Biomaterials 1985 6 189ndash192

77 Ikenaga M Hardouin P Lemaicirctre J et al Biomechanical charac-terization of a biodegradable calcium phosphate hydraulic cementa comparison with porous biphasic calcium phosphate ceramics JBiomed Mater Res 1998 40 139ndash144

78 Dias AG Lopes MA Santos JD et al In vivo performance ofbiodegradable calcium phosphate glass ceramics using the rabbitmodel histological and SEM observation J Biomater Appl 200620 253ndash266

79 Lee JH Lee CK Chang BS et al In vivo study of novel biodegrad-able and osteoconductive CaO-SiO2-B2O3 glass-ceramics JBiomed Mater Res 2006 77A 362ndash369

80 Song G Song S A possible biodegradable magnesium implant ma-terial Adv Eng Mater 2007 9 298ndash302

81 Kim WC Kim JG Lee JY et al Influence of Ca on the corrosionproperties of magnesium for biomaterials Mater Lett 2008 624146ndash4148

82 Li Z Gu X Lou S et al The development of binary Mg-Ca alloysfor use as biodegradablematerials within bone Biomaterials 200829 1329ndash1344

83 Wan Y Xiong G Luo H et al Preparation and characterization ofa new biomedical magnesium-calcium alloy Mater Des 2008 292034ndash2037

84 Seong JW Kim WJ Development of biodegradable Mg-Ca alloysheets with enhanced strength and corrosion properties throughthe refinement anduniformdispersion of theMg2Caphase by high-ratio differential speed rolling Acta Biomater 2015 11 531ndash542

85 Zhang S Li J Song Y et al In vitro degradation hemolysis andMC3T3-E1 cell adhesion of biodegradable Mg-Zn alloy Mater SciEng-C 2009 29 1907ndash1912

86 Li J Song Y Zhang S et al In vitro responses of human bone mar-row stromal cells to a fluoridated hydroxyapatite coated biodegrad-able Mg-Zn alloy Biomaterials 2010 31 5782ndash5788

87 Brar HS Wong J Manuel MV Investigation of the mechanical anddegradation properties of Mg-Sr and Mg-Zn-Sr alloys for use aspotential biodegradable implant materials J Mech Behav BiomedMater 2012 7 87ndash95

88 Bornapour M Muja N Shum-Tim D et al Biocompatibility andbiodegradability of Mg-Sr alloys the formation of Sr-substitutedhydroxyapatite Acta Biomater 2013 9 5319ndash5330

89 Gu XN Xie XH Li N et al In vitro and in vivo studies on aMg-Sr binary alloy system developed as a new kind of biodegrad-able metal Acta Biomater 2012 8 2360ndash2374

90 Haumlnzi AC Gerber I Schinhammer M et al On the in vitro andin vivo degradation performance and biological response of newbiodegradableMg-Y-Zn alloys Acta Biomater 2010 6 1824ndash1833

91 Chou DT Hong D Saha P et al In vitro and in vivo corrosioncytocompatibility and mechanical properties of biodegradableMg-Y-Ca-Zr alloys as implant materials Acta Biomater 2013 98518ndash8533

92 Zong Y Yuan G Zhang X et al Comparison of biodegradable be-haviors of AZ31 and Mg-Nd-Zn-Zr alloys in Hanks physiologicalsolution Mater Sci Eng-B 2012 177 395ndash401

93 Tie D Feyerabend FMuumlllerWD et al Antibacterial biodegradableMg-Ag alloys Eur Cell Mater 2013 25 284ndash298

94 VojtěchDKubaacutesek J Seraacutek J et al Mechanical and corrosion prop-

13 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

erties of newly developed biodegradable Zn-based alloys for bonefixation Acta Biomater 2011 7 3515ndash3522

95 Li H Yang H Zheng Y et al Design and characterizations of novelbiodegradable ternary Zn-based alloys with IIA nutrient alloyingelements Mg Ca and Sr Mater Des 2015 83 95ndash102

96 Liu X Sun J Yang Y et al Microstructure mechanical proper-ties in vitro degradation behavior and hemocompatibility of novelZn-Mg-Sr alloys as biodegradable metals Mater Lett 2016 162242ndash245

97 Wu C Qiu H Hu X et al Short-term safety and efficacy of thebiodegradable iron stent in mini-swine coronary arteries ChinMed J (Engl) 2013 126 4752ndash4757

98 Purnama A Hermawan H Champetier S et al Gene expressionprofile of mouse fibroblasts exposed to a biodegradable iron alloyfor stents Acta Biomater 2013 9 8746ndash8753

99 HermawanH Purnama A Dube D et al Fe-Mn alloys for metallicbiodegradable stents degradation and cell viability studies ActaBiomater 2010 6 1852ndash1860

100 Sheridan MH Shea LD Peters MC et al Bioabsorbable polymerscaffolds for tissue engineering capable of sustained growth factordelivery J Control Release 2000 64 91ndash102

101 Shawe S Buchanan F Harkin-Jones E et al A study on the rate ofdegradation of the bioabsorbable polymer polyglycolic acid (PGA)J Mater Sci 2006 41 4832ndash4838

102 Palmerini T Biondi-Zoccai G Della Riva D et al Clinical out-comes with bioabsorbable polymer- versus durable polymer-baseddrug-eluting and bare-metal stents J Am Coll Cardiol 2014 63299ndash307

103 Tanimoto S Serruys PW Thuesen L et al Comparison of in vivoacute stent recoil between the bioabsorbable everolimus-elutingcoronary stent and the everolimus-eluting cobalt chromium coro-nary stent insights from the ABSORB and SPIRIT trials CatheterCardiovasc Interv 2007 70 515ndash523

104 Tsuji H Sasaki H Sato H et al Neuron attachment properties ofcarbon negative-ion implanted bioabsorbable polymer of poly-lac-tic acid Nucl Instr Meth Phys Res Sect B-Beam Interact MaterAtoms 2002 191 815ndash819

105 Aikawa M Miyazawa M Okamoto K et al A novel treatment forbile duct injury with a tissue-engineered bioabsorbable polymerpatch Surgery 2010 147 575ndash580

106 WaksmanR Pakala R Kuchulakanti PK et al Safety and efficacy ofbioabsorbablemagnesium alloy stents in porcine coronary arteriesCatheter Cardiovasc Interv 2006 68 607ndash617

107 Di Mario C Griffiths H Goktekin O et al Drug-eluting bioab-sorbable magnesium stent J Interv Cardiol 2004 17 391ndash395

108 Erbel R Di Mario C Bartunek J et al Temporary scaffoldingof coronary arteries with bioabsorbable magnesium stents aprospective non-randomised multicentre trial Lancet 2007 3691869ndash1875

109 Schranz D Zartner P Michel-Behnke I et al Bioabsorbable metalstents for percutaneous treatment of critical recoarctation of theaorta in a newborn Catheter Cardiovasc Interv 2006 67 671ndash673

110 Gu X Zheng Y Cheng Y et al In vitro corrosion and biocompati-bility of binary magnesium alloys Biomaterials 2009 30 484ndash498

111 Hiromoto S InoueM Taguchi T et al In vitro and in vivo biocom-patibility and corrosion behaviour of a bioabsorbable magnesiumalloy coated with octacalcium phosphate and hydroxyapatite ActaBiomater 2015 11 520ndash530

112 Hiromoto S Tomozawa M Maruyama N Fatigue property of abioabsorbable magnesium alloy with a hydroxyapatite coatingformed by a chemical solution deposition J Mech Behav Biomed-ical Mater 2013 25 1ndash10

113 Bowen PK Drelich J Goldman J Zinc exhibits ideal physiologicalcorrosion behavior for bioabsorbable stents Adv Mater 2013 252577ndash2582

114 Liu X Sun J Yang Y et al In vitro investigation of ultra-pure Znand its mini-tube as potential bioabsorbable stent material MaterLett 2015 161 53ndash56

115 LinW Zhang G Cao P et al Cytotoxicity and its test methodologyfor a bioabsorbable nitrided iron stent J Biomed Mater Res 2015103 764ndash776

116 Coe JD Vaccaro AR Instrumented transforaminal lumbar inter-body fusion with bioresorbable polymer implants and iliac crestautograft Spine 2005 30 S76ndashS83

117 Ignatius AA Augat P Ohnmacht M et al A new bioresorbablepolymer for screw augmentation in the osteosynthesis of osteo-porotic cancellous bone a biomechanical evaluation J BiomedMater Res 2001 58 254ndash260

118 Krucoff MW Kereiakes DJ Petersen JL et al A novel biore-sorbable polymer paclitaxel-eluting stent for the treatment ofsingle and multivessel coronary disease J Am Coll Cardiol 200851 1543ndash1552

119 Kostopoulos L Karring T Guided bone regeneration in mandibu-lar defects in rats using a bioresorbable polymer Clin Oral Im-plants Res 1994 5 66ndash74

120 Dubok VA Bioceramicsmdashyesterday today tomorrow PowderMetall Metal Ceram 2000 39 381ndash394

121 Safronova T Kuznetsov A Korneychuk S et al Calcium phos-phate powders synthesized from solutions with [Ca2+][PO4

3minus]=1for bioresorbable ceramics Cent Eur J Chem 2009 7 184ndash191

122 Bohner M Bioresorbable ceramics In Buchanan FJ (Ed) Degra-dation Rate of Bioresorbable Materials Cambridge WoodheadPublishing 2008 95-114

123 Seitz JM Eifler R Stahl J et al Characterization ofMgNd2 alloy forpotential applications in bioresorbable implantable devices ActaBiomater 2012 8 3852ndash3864

124 WenCE Yamada Y Shimojima K et al Porous bioresorbable mag-nesium as bone substitute MSF 2003 419ndash422 1001ndash1006

125 Campos CM Muramatsu T Iqbal J et al Bioresorbable drug-elut-ing magnesium-alloy scaffold for treatment of coronary artery dis-ease Int J Mol Sci 2013 14 24492ndash24500

126 KirklandNT Birbilis NWalker J et al In-vitro dissolution ofmag-nesium-calcium binary alloys clarifying the unique role of calciumadditions in bioresorbable magnesium implant alloys J BiomedMater Res 2010 95B 91ndash100

127 Gastaldi D Sassi V Petrini L et al Continuum damage model forbioresorbable magnesium alloy devices mdashapplication to coronarystents J Mech Behav Biomed Mater 2011 4 352ndash365

128 Kitabata H Waksman R Warnack B Bioresorbable metal scaffoldfor cardiovascular application current knowledge and future per-spectives Cardiovasc Revasc Med 2014 15 109ndash116

Acknowledgments This work was supported by the National Key Re-search and Development Program of China (2016YFC1102402) NationalNatural Science Foundation of China (NSFC 51431002) and the NSFCand the Research Grants Council (RGC) of Hong Kong Joint ResearchScheme (51361165101 and 5161101031)

Author contributions Liu Y prepared the figures tables organized thereferences and wrote the paper Zheng Y provided the overall concept andrevised the manuscript Hayes B helped with the standard developmentand revised the manuscript All authors participated in the discussion

Conflict of interest The authors declare that they have no conflict ofinterest

14copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Yang Liu received his bachelor degree in materials science and engineering from Harbin engineering University in 2013Then he continued his study as a PhD candidate in Prof Yufeng Zhengrsquos Lab in Peking University His research interestsare mainly focused on the corrosion study of absorbable metallic biomaterials as well as the development of new kind ofMg-based biomaterials

Yufeng Zheng obtained his PhD degree from Harbin Institute of Technology in 1998 He is the National OutstandingYouth and Yangtze River scholar of China His research interests are focused on the development of novel biomaterials andapplication and design of biomedical devices

Byron Hayes an over 35 year employee of WL Gore has been involved in the commercial development of multiple ab-sorbable polymeric implants since the late 1980s Hayes started his standards development activities with ASTM in 2000where he is actively developing standards for polymeric and metallic absorbable implants In 2010 Hayes also becameinvolved with ISO Technical Committees TC150 and TC194 and is now convener of working groups focused on cardiovas-cular and metallic absorbable implants

可降解可吸收再吸收mdashmdash哪个是描述最终被人体吸收生物材料的最好词汇刘洋1 郑玉峰1 拜伦海耶斯2

摘要 关于最终被人体吸收的植入材料领域内文献采用的英文修饰词长期以来混乱且不同不仅造成文献检索困难同时模糊了研究人员的研究边界 此领域在法律法规标准中统一用词的确定为领域内的科学研究产品销售及产品使用说明奠定了基础 我们基于化学生态学材料学生物学微生物学和药学立足于使用习惯法律标准和市场对领域内使用已久的典型修饰词ldquo生物可降解rdquoldquo再吸收rdquo和ldquo可吸收rdquo进行了讨论和解释 总的来说尽管目前绝大多数修饰语实际想表达的意思相同作者认为ldquo可吸收rdquo这一英文修饰语是最恰当的修饰词 同时我们提议进一步规范和统一该领域修饰词的使用

15 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

  • Degradable absorbable or resorbablemdashwhat is the best grammatical modifier for an implant that is eventually absorbed by the body
  • Abstract
  • INTRODUCTION
    • Current situation
    • Standards development in advance
      • TERMINOLOGY
        • Overview of utilization of the terms ldquodegradationrdquoldquobiodegradationrdquo and ldquodegradablerdquoldquobiodegradablerdquo
        • Overview of utilization of the terms ldquoabsorptionrdquoldquobioabsorptionrdquo and ldquoabsorbablerdquoldquobioabsorbablerdquo
        • Overview of utilization of the terms ldquoresorptionrdquoldquobioresorptionrdquo and ldquoresorbablerdquoldquobioresorbablerdquo
        • Utilization and comparison of the terms ldquobiodegradable metalsrdquo and ldquoabsorbable metallic materialsrdquo
        • Summary quantification of the common Terms
          • DISCUSSION
            • Expertise inherent biases
            • Connotation and extension of noun forms ldquobiodegradation bioabsorption and bioresorptionrdquo and adjectives ldquobiodegradable bioabsorbable and bioresorbablerdquo
              • CONCLUDING REMARKS
              • References
              • Acknowledgements

testing of absorbable polyesters is the sole listed standardfrom ASTM Committee F04mdashMedical and Surgical Im-plants and thereby is directly relevant to implantable de-vices However this standard utilizes the term degradeand its derivatives specifically in reference to the process ofdegradation that occurs as a result of ester hydrolysis Con-versely the same standard uses the term absorbable to de-scribe a class of implants that are eventually absorbed by thebody which it defines as ldquoabsorbable adjmdashin the bodymdashaninitially distinct foreign material or substance that either di-rectly or through intended degradation can pass through orbe assimilated by cells andor tissuerdquo

Overview of utilization of the terms ldquoabsorptionrdquoldquobioab-sorptionrdquo and ldquoabsorbablerdquoldquobioabsorbablerdquoThe term ldquoabsorptionrdquo was recognized by IUPAC as theprocess of penetration and diffusion of a substance (ab-sorbate) into another substance (absorbent) as a result ofthe action of attractive phenomena The IUPAC defini-tion is within the scope of chemistry As for biomaterialsProf D Williams adopted the definition in Dorland Medi-cal Dictionary as the uptake of substances into or across tis-sues [23] For this kind of definition ldquoabsorptionrdquo empha-sizes the interaction of materials and human or animal tis-sue The same connotation is shared by its derivative wordsldquoabsorbablerdquo and ldquobioabsorbablerdquo as capable of being de-graded or dissolved and subsequently metabolized withinan organism [23] Besides the prefix ldquobio-rdquo is abridged as

it is redundant in the field of implantation [43] ASTM hasmade standard definition on ldquoabsorbablerdquo in the field of ab-sorbable polymers as well as absorbablemetals which it de-fines as ldquohellip an initially distinct foreign material or substancethat either directly or through intended degradation can passthrough or be metabolized or assimilated by cells andor tis-sue in the bodyrdquo [43] Table 2 summarizes the currently ac-tive ASTM standards and both United States and EuropeanPharmacopeia implantable device monographs that utilizethe word ldquoabsorbablerdquo in the title Distinctly different fromldquobiodegradablerdquo the utilization of ldquoabsorbablerdquo displays adistinct preference for use in describing this particular classof biomedical materials and devicesAs can be observed in both Table 1 and Table 3 the

well-established terminology for describing sutures is verybroadly based on the term absorbable with historicalapplication of the term to the original gut sutures andeven extending to permanent sutures through the ldquononab-sorbablerdquo descriptorAside from the language of standards organization the

terminology utilized by regulatory agencies is also of par-ticular relevance Through multiple laws and regulationsthe US-FDA is authorized to evaluate medical device man-ufacturers and their products The US Code of FederalRegulations (CFRs) that is specific to sutures legally de-scribes those regulated devices based on composition andthen designates both their product class and needs to meetUSP requirements While Table 3 demonstrates both a US-

Table 2 ldquoAbsorbablerdquo utilized in title entries for implantable device related standards

Terminology Title entries

ISOTS 171372014 Cardiovascular implants and extracorporeal systemsmdashCardiovascular absorbable implants

ISOTR 371372014 Biological evaluation of medical devicesmdashGuidance for absorbable implants

ASTM F3036-13 Standard Guide for Testing Absorbable Stents

ASTM F2902-16 Standard Guide for Assessment of Absorbable Polymeric Implants

ASTM F2502-16 Standard Specification and Test Methods for Absorbable Plates and Screws for Internal Fixation Implants

ASTM F1983-14 Standard Practice for Assessment of Selected Tissue Effects of Absorbable Biomaterials for Implant Applications

ASTM F3160-16 Standard Guide for Metallurgical Characterization of Absorbable Metallic Materials for Medical Implants

United States Pharmacopoeia (USP 39NF 34) monographldquoAbsorbable Surgical Suturerdquo

United States Pharmacopoeia (USP 39NF 34) monographldquoNonabsorbable Surgical Suturerdquo

European Pharmacopoeia (88)ldquoSterile non-absorbable suturesrdquo ndash 1118

European Pharmacopoeia (88)ldquoSterile synthetic absorbable braided suturesrdquo - 1122

Absorbable

European Pharmacopoeia (88)Sterile synthetic absorbable monofilament sutures ndash 1123

5 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Table 3 US-FDA suture product codes and accompanying citation of US CFRsa)

Suture name Regulation Product code

Absorbable polydioxanone surgical (PDS) suture 21 CFR8784840 NEW

Absorbable poly(glycolideL-lactide) surgical suture 21 CFR8784493 GAM

Absorbable gut suture 21 CFR8784830 GAL

Nonabsorbable poly(ethylene terephthalate) suture 21 CFR8785000 GAT

Nonabsorbable polypropylene surgical suture 21 CFR8785010 GAW

Nonabsorbable polyamide surgical suture 21 CFR8785020 GAR

Natural nonabsorbable silk surgical suture 21 CFR8785030 GAP

Stainless steel surgical suture 21 CFR8784495 GAQ

Nonabsorbable expanded polytetrafluoroethylene (ePTFE)surgical suture

21 CFR8785030 NBY

a) Note this table selects abbreviated results obtained from online search for the implant device term ldquosuturerdquo that was conducted on 6 Aug 2016 athttpwwwaccessdatafdagovscriptscdrhcfdocscfPCDclassificationcfm

FDA and a US Code of Federal Regulations preference forabsorbable terminology when referring to sutures Table4 shows an expansion of that preference to include a to-tal of 30 absorbable implant product classifications each ofwhich is assigned to a relevant Federal regulation that uti-lizes the term ldquoabsorbablerdquoIn short ldquoabsorbablerdquo is both a historically well estab-

lished and currently relevant term in both the regulationand standardization of implants that are intentionally ab-sorbed by the body

Overview of utilization of the terms ldquoresorptionrdquoldquobiore-sorptionrdquo and ldquoresorbablerdquoldquobioresorbablerdquoIn the scope of chemistry the term ldquoresorptionrdquo was used toillustrate the total elimination of a substance from its initialplace caused by physical andor chemical phenomena [14]Besides the understanding from pure chemistry ldquoresorp-tionrdquo is more recognized involved in the metabolic activi-ties in vivo For example ldquoresorptionrdquo is considered as theldquoabsorptionrdquo into the circulatory system of cells or tissuewhich usually includes bone resorption tooth resorptionand vanishing twin [44] In the biomedical scope Prof DWilliams used themeaning in DorlandMedical Dictionaryas ldquolysis and assimilation of a substance as of bonerdquo [23]ldquoBioresorptionrdquo is more common when describing the invivo process of a certain foreign material The ISO definedldquobioresorptionrdquo as a process by which biomaterials are de-graded in the physiological environment and the by-prod-uct are eliminated or completely bioabsorbed [23] Thusaccording to this interpretation the bioresorption processincludes material removal in vivo either by cellular activ-ity or not Conversely Taberrsquos Cyclopedic Medical Dictio-nary [45] describes the term ldquoresorbrdquo as themeaning ldquoto ab-

sorb againrdquomdashsomething that live tissue does but not some-thing any implant is known to domdashbe it permanent or ab-sorbableAs for the adjectives ldquobioresorbablerdquo and ldquoresorbablerdquo

there is no difference when used to describe a kind of ma-terials which have the ability of resorption This is ascribedto the fact that ldquoresorptionrdquo itself already has been well rec-ognized as a biological process [23] Currently there is noASTM entries used ldquoresorbablerdquo or ldquobioresorbablerdquo in thetitle

Utilization and comparison of the terms ldquobiodegradablemetalsrdquo and ldquoabsorbable metallic materialsrdquoldquoBiodegradablemetalsrdquo generally include themetalsMg Feand Zn and their alloys and composites They can be de-fined as metals that assist with tissue healing and are thenexpected to gradually corrode and release corrosion prod-ucts in vivowith an appropriate host response and then dis-solve completely with no implant residues [46] As a resultand different from traditional ldquobio-inertrdquometallic biomate-rials (eg Ti and Co based alloys) that release limited cor-rosion products [47] metabolic reactions besides inflam-mation can be expected to occur between the biodegrad-able metal and the host body after implantation Addition-ally the corrosion-based degradation mechanism of thesematerials is inherently different from that of either bioce-ramics or polymers which has resulted in limited to nostandardized guidance available from either ASTM or ISOInstead of the term ldquobiodegradable metalrdquo the recently

published and first absorbable metal related standardASTM F3160 utilizes the more inclusive word ldquoabsorbablerdquowithin the phrase ldquoabsorbable metallic materialsrdquo andagain defines the term as ldquohellip an initially distinct foreign

6copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Table 4 US-FDA absorbable implant related product codes descriptions and accompanying CFRsa)

Product code Device Device class Regulation number Regulation description

OMT Absorbable lung biopsy plug 2 [8784755] Absorbable lung biopsy plug

LMF Agent absorbable hemostatic collagen based 3 [8784490] Absorbable hemostatic agent and dressing

LMG Agent absorbable hemostatic non-collagen based 3 [8784490] Absorbable hemostatic agent and dressing

MRY Appliances and accessories fixation bone absorbable singlemultiple component 2 [8883040] Smooth or threaded metallic bone fixation fastener

PBQ Fixation non-absorbable or absorbable for pelvic use 2 [8844530] Obstetric-gynecologic specialized manual instrument

HQJ Implant absorbable (scleral buckling methods) 2 [8863300] Absorbable implant (scleral buckling method)

OWT Mesh surgical absorbable abdominal hernia 2 [8783300] Surgical mesh

OXM Mesh surgical absorbable fistula 2 [8783300] Surgical mesh

OXI Mesh surgical absorbable large abdominal wall defects 2 [8783300] Surgical mesh

OXL Mesh surgical absorbable organ support 2 [8783300] Surgical mesh

OWW Mesh surgical absorbable orthopaedics reinforcement of tendon 2 [8783300] Surgical mesh

OXF Mesh surgical absorbable plastic and reconstructive surgery 2 [8783300] Surgical mesh

OXC Mesh surgical absorbable staple line reinforcement 2 [8783300] Surgical mesh

OWZ Mesh surgical absorbable thoracic chest wall reconstruction 2 [8783300] Surgical mesh

OWU Mesh surgical non-absorbable diaphragmatic hernia 2 [8783300] Surgical mesh

OWR Mesh surgical non-absorbable facial implants for plastic surgery 2 [8783300] Surgical mesh

OXJ Mesh surgical non-absorbable large abdominal wall defects 2 [8783300] Surgical mesh

OWX Mesh surgical non-absorbable orthopaedics reinforcement of tendon 2 [8783300] Surgical mesh

OXG Mesh surgical non-absorbable plastic and reconstructive surgery 2 [8783300] Surgical mesh

OXD Mesh surgical non-absorbable staple line reinforcement 2 [8783300] Surgical mesh

OXA Mesh surgical non-absorbable thoracic chest wall reconstruction 2 [8783300] Surgical mesh

LBP Replacement ossicular (stapes) using absorbable gelatin material 2 [8743450] Partial ossicular replacement prosthesis

OLL Septal staplerabsorbable staples 2 [8784750] ImplanTABLE staple

MNU Staple absorbable 2 [8883030] Singlemultiple component metallic bone fixationappliances and accessories

GAK Suture absorbable 2 [8784830] Absorbable surgical gut suture

GAL Suture absorbable natural 2 [8784830] Absorbable surgical gut suture

HMO Suture absorbable ophthalmic 3

GAN Suture absorbable synthetic 2 [8784830] Absorbable surgical gut suture

GAM Suture absorbable synthetic polyglycolic acid 2 [8784493] Absorbable poly(glycolidel-lactide) surgical suture

NEW Suture surgical absorbable polydioxanone 2 [8784840] Absorbable polydioxanone surgical suture

a) Note the results obtained from online search for the device term ldquoabsorbablerdquo that was conducted on 6 Aug 2016 at httpwwwaccessdatafdagovscriptscdrhcfdocscfPCDclassifica-tioncfm

7 copy

ScienceChina

Pressand

Springer-VerlagBerlin

Heidelberg 2017

SCIENCECH

INAMaterials

REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

material or substance that either directly or through in-tended degradation can pass through or be metabolized orassimilated by cells andor tissuerdquo The standardrsquos nomen-clature appendix further elaborates on its preference forldquoabsorbablerdquo since the prefix ldquobio-rdquo is redundant in thecontext of implant applications [43]Clearly these two terms of ldquobiodegradable metalsrdquo and

ldquoabsorbable metallic materialsrdquo share the same connota-tion which defines the completemission of an intentionallydegradable material when implanted in vivo In the contextof biodegradable metalsabsorbable metallic materialsthe process includes the corrosion caused by body fluida host response caused by corrosion products followedby dissolutionabsorption and finally improved tissuehealing The ldquobiodegradationrdquo instead of ldquobiocorrosionrdquois used to distinguish this new kind of metals which canfully dissolve in vivo with no implant residues Besidesbiodegradation process the following dynamic process ofdissolutionabsorption also starts in vivo For exampledissolved Mg2+ is considered to enhance the integrin me-diated human-bone-derived cell adhesion and affect newbone formation [48] The metabolic reaction is also crucialand even more important for biodegradable metals as it ishelpful It is another distinction from traditional metalsused for biomedical application In fact the different usagehabit forming of ldquobiodegradablerdquo or ldquoabsorbablerdquoldquobioab-sorbablerdquo may be more related with the study field theresearchers in Taking the ldquoabsorbablerdquo metallic stent asan example (Fig 2) once the ldquoabsorbablerdquo metallic stentwas implanted into blood vessel ldquocorrosionrdquo of biometal

begins The corrosion products including debris hydro-gen (for Mg-based metals) metallic ions and hydroxylconvert the local environment and diffuse into the bloodvessel wall Some corrosion products can be biologicallybeneficial For instance the diffused and absorbed Zn2+

can potentially play a positive role in dealing with athero-sclerosis [49] Along with the corrosion process healingprocesses such as endothelialization may become en-hanced In summary and within the context of absorbablemetals the adjectives ldquodegradablerdquo and ldquoabsorbablerdquo referto the nature of the biodegradation products of the mate-rialdevice being metabolically absorbed an attribute ofthe host (animal or human body) regardless of whetherthe implant degrades corrodes hydrolyzes or dissolves[50ndash52]

Summary quantification of the common TermsFig 3a shows preliminary searching results in Webof Knowledge using ldquodegradablerdquo ldquoabsorbablerdquo or ldquore-sorbablerdquo along with ldquomaterialrdquo as key words Theutilization of ldquodegradablerdquo is a bit more frequently thanldquoabsorbablerdquo but that of ldquoresorbablerdquo steps down Mean-while the counterpart searching result when using ldquobiordquo asprefix to the adjectives along with ldquomaterialrdquo as keywordsare presented in Fig 3b ldquoBiodegradable materialrdquo is themost common utilization which holds 91 among the ex-pression approach This is also due to the fact that besidesthe common utilization in biomaterials ldquobiodegradablerdquois also used in a wide range of applications such as cleanenvironment and ecology [5354]

Figure 2 Different point of views on the biodegradationabsorption process

8copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Figure 3 Searching results in Web of Knowledge from all databases (a) with the total searched publication numbers by ldquodegradablerdquo+ ldquomaterialrdquoldquoabsorbablerdquo+ ldquomaterialrdquo and ldquoresorbablerdquo+ ldquomaterialrdquo as 100 (b) the total searched publication numbers by ldquobiodegradablerdquo+ ldquomaterialrdquo ldquobioab-sorbablerdquo+ ldquomaterialrdquo and ldquobioresorbablerdquo+ ldquomaterialrdquo as 100

DISCUSSION

Expertise inherent biasesAs previously mentioned biomaterial is an interdiscipli-nary field fascinating researchers with specialty from dif-ferent backgrounds Different backgrounds as well as dif-ferent research point of interests may be one of the reasonsfor using different terminologies Materials scientists tendto focus on the materialdevice itself leading to their usageof ldquobiodegradablerdquo to illustrate what happens to the deviceThey pay more attention to the process such as hydroly-sis corrosion debris degradation products and the changeof surface morphology resulting in the researching inter-ests of ldquomaterial biodegradationrdquo In contrast surgeons andbiomedical researchers tend to be concerned more on thehost response and healing process They are curious aboutthe absorption of various degradation products of the im-planted materialdevice and related metabolism mecha-nism and thereby prefer to use the term ldquoabsorbablerdquo toillustrate what happens to the device As known somema-terials may only undergo biodegradation but the corrosionproducts still have no influence on the metabolic activitiesFor example cellulose is considered as ldquodietary fiberrdquowhichcannot be digested and absorbed by human body but is be-nign for human body [55] Some coating tablets for drug ordrug delivery systems made from cellulose and its deriva-tives are quite frequently utilized or investigated [5657]The polymer and derivatives of cellulose can only be de-graded but not be absorbed by human body [58] For suchmaterials the adjective ldquoabsorbablerdquo or ldquobioabsorbablerdquo isnot appropriateOverall once the materialsdevices are implanted into

the human body the ldquobiocorrosionrdquobiodegradationrdquoprocess happens immediately no matter to what degreeat the same time the host will biologically response to the

corrosiondegradation products through the absorptionmetabolism and excretion processes So for the samestory the majority of materials scientists would report itby ldquobiodegradabledegradationrdquo way whereas the majorityof medical doctors would report it by ldquoabsorbableab-sorptionrdquo way In nature the two terms ldquobiodegradablemetalsrdquo and ldquoabsorbable metallic materialsrdquo share the sameconnotation and are mutually replaceable

Connotation and extension of noun forms ldquobiodegradationbioabsorption and bioresorptionrdquo and adjectivesldquobiodegradable bioabsorbable and bioresorbablerdquoThe three noun forms of the terms illustrate the processwhile their adjectival derivatives were used to describe thegroup of materials with such certain capabilities For thestudy on biomaterials polymer researchers use ldquodegrada-tionbiodegradationrdquo when there is proved chain scissionprocess Besides they differentiate ldquobiodegradationrdquo andldquodegradationrdquo by confirmed metabolic activities betweenthe materials and cells or tissues Regarding to the fouradjectives ldquobiodegradablerdquo ldquobioabsorbablerdquo and ldquobiore-sorbablerdquo the term ldquobiocorrodiblerdquo is only used in scientificpapers on iron based materials and some patents on mag-nesium based materials The common usage of termsldquobiodegradablerdquo ldquobioabsorbablerdquo and ldquobioresorbablerdquo withrespect to the biomaterial research area is shown in Table 5The results reveal a widespread usage of ldquobiodegradablerdquo inboth polymers and magnesium based metals Varies typesof materials were reported as biomaterials Besides thereare also reports of ldquobiodegradablerdquo polymers for ecologyand environmental protection which indicates a furtherusage scope of ldquobiodegradablerdquo not only for implants anddevices Besides ldquobioresorbablerdquo is also utilized in all theresearch fields of polymers ceramics andmetals Howeverno current work used ldquobioabsorbablerdquo as grammatical

9 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Table 5 Current reported usage of terms ldquobiodegradablerdquo ldquobioabsorbablerdquo and ldquobioresorbablerdquoTerminology Category Materials Applications

PLA-PEG-biotin PLGA Controlled cell engineering [5960]Porous PLGA Tissue engineering [61ndash63]

PLGA-PEG-PLGA Injective thermosensitive hydrogel [64]PLGA Nerve guidance [65]

Fibronectin (Fn)-coated PLLA P(LLA-CL) Enhanced growth of endothelial cells [6066]PEG tethered PPF [67]

PDMS Drug delivery [68]PGA Tissue engineering [69]

Undefined Coronary stent [70ndash72]PGA Joint resurfacing [73]

Polymers

PHA Ecology and environmental protection [74]CaO-P2O5 glass Bone regeneration [75]β-Whitlockite Bone regeneration [76]

Calcium phosphate hydraulic cement Bone regeneration [77]Calcium

phosphate glass ceramicsBone regeneration [78]

Ceramics

CaO-SiO2-B2O3 glass-ceramics Bone regeneration [79]Pure Mg Implant material [80]

Mg-Ca-based Bone regeneration [81ndash84]Mg-Zn-based Bone regeneration [338586]Mg-Sr-based Bone regeneration [87ndash89]Mg-RE-based Vascular stent [90ndash92]

Mg and its metals

Mg-Ag-based [93]Zn-Mg Zn-Ca Zn-Sr [9495]Zn and its metals Zn-Mg-Sr [96]

Fe [9798]

Biodegradable

Fe and its metals Fe-Mn [99]PLLA PLG PGA Molecule delivery [100]

PGA Suture [101]Undefined Drug-eluting stent [102103]

PLA Neuron attachment [104]Polymers

PLA and PCL reinforced with PGA fibers Bile duct patch [105]Mg-RE based Coronary stent [106ndash109]

Binary Mg alloys [110]Mg and its metalsMg-Al-based [111112]

Zn and its metals Pure Zinc [113114]Fe and its metals Nitrided iron [115]

PLDLA Transforaminal lumbar interbody fusion [116]Alkylene bis(dilactoyl)-methacrylate modified polymer Bone screw augmentation [117]

Undefined Coronary stent [118]PHB Mandibular defects regeneration [119]HA Bone regeneration [120]Ceramics Calcium phosphate [121122]

MgNd2 Stent material [123]Porous Mg Bone substitute [124]Mg-RE Coronary stent [125]Mg-Ca Orthopedic application [126]

Mg and its metals

Mg-based Finite element analysis [127]

Bioabsorbable

Fe and its metals Pure Fe [128]

10copy

ScienceChina

Pressand

Springer-VerlagBerlin

Heidelberg 2017

REVIEWSCIENCE

CHINA

Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

modifier to bioceramics In addition as previouslyillustrated the prefix ldquobiordquo of ldquobioabsorbablerdquo and ldquobiore-sorbablerdquo are abridged hereafter discussion will concen-trate on ldquobiocorrodiblerdquo ldquobiodegradablerdquo ldquoabsorbablerdquo andldquoresorbablerdquoSince absorbable technologies are increasingly utilized

in numerous new and broader implant applications it be-comes more important to not acquiesce in addressing his-torical problems and instead actively move forward towardutilizing standardized language that is both technically ac-curate and unified in itsmeaning Preferred language needsto accurately communicate the concept To achieve the uni-fying goal of harmonized terminology themedical and sci-entific communities need to not solely look at materialschemistry or even biomaterials alone but to instead lookat term selection both across and within the context of thebroader medical disciplinemdashthe location where the resultsof implant technology development actually reaches themarketplace where therapies are brought to those in needNomenclature solutions need to both understand and re-spond to the context of terms across adjacent technologieswhich means to address needs from the perspectives of thebiomaterial researcher the deviceproduct developer thesurgeonclinician user the regulator and last but not leastthe patientgeneral public who is the direct beneficiary ofthe developed technologyA better understanding of these terminologies is neces-

sary and beneficial to the field Therefore the definitionson ldquodegradablerdquo ldquoabsorbablerdquo ldquoresorbablerdquo and relatedterms proposed by different organizations in differentfields have been summarized and discussed with the con-notation and extension of each term being compared andthe criteria being proposed

CONCLUDING REMARKSHerein given both the searching problem on the Internetand ambiguity in meanings the usage of grammaticalmodifiers to describe biomaterials that is eventually ab-sorbed by human body has been enumerated based onusage habits laws standards and markets In summaryldquodegradablerdquoldquobiodegradablerdquo are the most frequently usedgrammatical modifier not only in metals but also poly-mers as such kind of biomaterials ldquoBiodegradationrdquo andldquobiodegradablerdquo define the change of the materialdevicewell in the research of biomaterials but they are alsoadopted in other fields such as ecology and environmentalprotection Meanwhile ldquoresorbablerdquoldquobioresorbablerdquo havelong been recognized in the biological research and theldquoresorptionrdquo itself has been widely accepted as a biological

reaction The utilization of ldquoresorbablerdquoldquobioresorbablerdquowas found to be not as frequent as the counterpartsldquodegradablerdquoldquobiodegradablerdquo and ldquoabsorbablerdquoldquobioab-sorbablerdquo Such usage is accurate for osteoclast driven boneresorption but is inappropriate for implants that do notcarry the potential to grow back into their original formOtherwise despite it is not the most frequently used termldquoabsorbablerdquoldquobioabsorbablerdquo concentrates more on thehost metabolism to the foreign biodegradation productsof the implanted materialdevice compared with ldquodegrad-ablerdquoldquobiodegradablerdquo ldquoAbsorbablerdquo is defined in the scopeof biomaterials by different organizations and their publi-cations and also adopted by ASTM to illustrate ldquoabsorbablepolymerrdquo It is the most historically established the mostbroadly applicable (includes dissolvable devices that donot degrade) the most specific to medical applicationsand is the formal legal descriptor for most implant devicesConsidering the usage history common utilization in lawand standards as well as the scientific meaning in essenceldquoabsorbablerdquo can be better among other grammaticalmodifiers for description of an implant that is eventuallyabsorbed by the body which is recommended by theauthors for a further internationally-unified usage

Received 28 February 2017 accepted 27 March 2017published online 26 April 2017

1 Mackenzie D The history of sutures Med Hist 1973 17 158ndash1682 Hench LL Bioceramics J Am Ceramic Soc 2005 81 1705ndash17283 Hench LL Bioceramics from concept to clinic J AmCeramic Soc

1991 74 1487ndash15104 Windhagen H Radtke K Weizbauer A et al Biodegradable

magnesium-based screw clinically equivalent to titanium screw inhallux valgus surgery short term results of the first prospectiverandomized controlled clinical pilot study BioMed Eng OnLine2013 12 62

5 Schildwaumlchter M Biotronik announces CE mark for magmaristhe first clinically-proven bioresorbable magnesium scaffoldhttpwwwmagmariscomennewsroomjune-15-2016

6 Shalaby SW Burg KJL Bioabsorbable polymers update degrada-tion mechanisms safety and application J App Biomater 1995 6219ndash221

7 Vert M Li SM Spenlehauer G et al Bioresorbability and biocom-patibility of aliphatic polyesters J Mater Sci-Mater Med 1992 3432ndash446

8 Vert M Degradable and bioresorbable polymers in surgery and inpharmacology beliefs and facts J Mater Sci-Mater Med 2009 20437ndash446

9 Benicewicz BC Hopper PK Review polymers for absorbablesurgical suturesmdashPart I J Bioactive Compatible Polym 1990 5453ndash472

10 Barrows HT Synthetic bioabsorbable polymers In Szycher M(Ed) High Performance Biomaterials A Complete Guide toMed-ical and Pharmceutical Applications Boca Raton CRC PRESS1991 243ndash257

11 Weiler A Hoffmann RFG Staumlhelin AC et al Biodegradable

11 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

implants in sports medicine the biological base Arthroscopy-JArthroscopic Related Surgery 2000 16 305ndash321

12 Ikada Y Tsuji H Biodegradable polyesters for medical and ecolog-ical applications Macromol Rapid Commun 2000 21 117ndash132

13 Ashammakhi N Peltoniemi H Waris E et al Developments incraniomaxillofacial surgery use of self-reinforced bioabsorbableosteofixation devices Plast Reconstr Surg 2001 108 167ndash180

14 Vert M Doi Y Hellwich KH et al Terminology for biorelatedpolymers and applications (IUPACRecommendations 2012) PureAppl Chem 2012 84 377ndash410

15 The United States Pharmacopeial Convention The Second Sup-plement to the Pharmacopeia of the United States of America 11thdecennial revision (USP XI-1939 Supplement) 1939

16 Truhlsen SM The recession operation histopathologic responseand suture reaction and absorption Trans Am Ophthalmol Soc1965 63 626ndash677

17 USP in US Law httpwwwusporgprintabout-usplegal-recog-nitionusp-us-law

18 USP develops and publishes standards for drug substances drugproducts excipients and dietary supplements in the United StatesPharmacopeia-National Formulary (USP-NF)

19 United States Public Law 94-295 197620 United States Pharmacopeia httpwwwusporg21 British Pharmacopeia httpswwwpharmacopoeiacom22 European Pharmacopoeia httponlinepheurorgENentryhtm23 Williams DF The Williams Dictionary of Biomaterials Liverpool

Liverpool University Press 199924 httpsenwikipediaorgwikiBiodegradation25 Jones RG Kahovec J Stepto R et al Compendium of Polymer

Terminology and Nomenclature IUPAC Recommendations 2008Cambridge RSC Publishing 2009

26 Higashi S Yamamuro T Nakamura T et al Polymer-hydroxyap-atite composites for biodegradable bone fillers Biomaterials 19867 183ndash187

27 de Groot K Bioceramics of Calcium Phosphate Boca Raton CRCPress 1983

28 Hollinger JO Battistone GC Biodegradable bone repair materialssynthetic polymers and ceramics ClinOrthopRelat Res 1986 207290ndash306

29 ASTMD653-14 Standard Terminology Relating to Soil Rock andContained Fluids ASTM International West Conshohocken PA2014 httpswwwastmorgStandardsD653htm

30 Witte F Hort N Vogt C et al Degradable biomaterials based onmagnesium corrosion Curr Opin Solid State Mater Sci 2008 1263ndash72

31 Lynn DM Langer R Degradable poly(β-amino esters) synthesischaracterization and self-assemblywith plasmidDNA JAmChemSoc 2000 122 10761ndash10768

32 Cima LG Vacanti JP Vacanti C et al Tissue engineering by celltransplantation using degradable polymer substrates J BiomechEng 1991 113 143ndash151

33 Zhang S Zhang X Zhao C et al Research on an Mg-Zn alloy as adegradable biomaterial Acta Biomater 2010 6 626ndash640

34 Anseth KS Metters AT Bryant SJ et al In situ forming degradablenetworks and their application in tissue engineering and drug de-livery J Control Release 2002 78 199ndash209

35 Forrest ML Koerber JT Pack DW A degradable polyethyleniminederivative with low toxicity for highly efficient gene delivery Bio-conjugate Chem 2003 14 934ndash940

36 ASTM E2747-11 Standard Specification for Evaluation and Selec-tion of Onsite Offices for Environmentally Sustainable MeetingsEvents Trade Shows and Conferences ASTM International

West Conshohocken PA 2011 httpswwwastmorgStan-dardsE2747htm

37 ASTM E2745-11 Standard Specification for Evaluation andSelection of Audio Visual (AV) and Production for Environ-mentally Sustainable Meetings Events Trade Shows and Con-ferences ASTM International West Conshohocken PA 2011httpswwwastmorgStandardsE2745htm

38 ASTM E2746-11 Standard Specification for Evaluation andSelection of Communication and Marketing Materials for En-vironmentally Sustainable Meetings Events Trade Shows andConferences ASTM International West Conshohocken PA 2011httpswwwastmorgStandardsE2746htm

39 ASTM E2741-11 Standard Specification for Evaluation and Se-lection of Destinations for Environmentally Sustainable MeetingsEvents Trade Shows and Conferences ASTM InternationalWest Conshohocken PA 2011 httpswwwastmorgStan-dardsE2741htm

40 0 ASTM E2773-11 Standard Specification for Evaluation andSelection of Food and Beverage for Environmentally SustainableMeetings Events Trade Shows and Conferences ASTM Interna-tional West Conshohocken PA 2011 httpswwwastmorgStan-dardsE2773htm

41 ASTM E2742-11 Standard Specification for Evaluation and Selec-tion of Exhibits for Environmentally Sustainable Meetings EventsTrade Shows and Conferences ASTM International West Con-shohocken PA 2011 httpswwwastmorgStandardsE2742htm

42 ASTM E2774-11 Standard Specification for Evaluation and Selec-tion of Venues for Environmentally Sustainable Meetings EventsTrade Shows and Conferences ASTM International West Con-shohocken PA 2011 httpswwwastmorgStandardsE2774htm

43 ASTM F2902-12 Standard Guide for Assessment of AbsorbablePolymeric Implants ASTM International West ConshohockenPA 2012 httpswwwastmorgStandardsF2902htm

44 httpsenwikipediaorgwikiResorption45 Venes D Tabers Cyclopedic Medical Dictionary 22th edition

Philadelphia F A Davis Company 201346 Zheng YF Gu XN Witte F Biodegradable metals Mater Sci Eng-

R-Rep 2014 77 1ndash3447 Hanawa T Metal ion release from metal implants Mater Sci

Eng-C 2004 24 745ndash75248 Zreiqat H Howlett CR Zannettino A et al Mechanisms of mag-

nesium-stimulated adhesion of osteoblastic cells to commonly usedorthopaedic implants J Biomed Mater Res 2002 62 175ndash184

49 Little PJ Bhattacharya R Moreyra AE et al Zinc and cardiovascu-lar disease Nutrition 2010 26 1050ndash1057

50 Seager H Drug-delivery products and the Zydis fast-dissolvingdosage form J Pharm Pharmacol 1998 50 375ndash382

51 Shikinami Y Shape-memory biodegradable and absorbable mate-rial US Patent No 6281262 2001-8-28

52 Huitema TW Knight GW Ransick MH Schulze DR Surgical im-plant with preferential corrosion zone US Patent No 79059022011-3-15

53 Luzier WD Materials derived from biomassbiodegradable mate-rials Proc Natl Acad Sci USA 1992 89 839ndash842

54 Gross RA Kalra B Biodegradable polymers for the environmentScience 2002 297 803ndash807

55 Trumbo P Schlicker S Yates AA et al Dietary reference intakesfor energy carbohydrate fiber fat fatty acids cholesterol proteinand amino acids J Am Diet Assoc 2002 102 1621ndash1630

56 Chambin O Champion D Debray C et al Effects of different cel-lulose derivatives on drug release mechanism studied at a prefor-mulation stage J Control Release 2004 95 101ndash108

12copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

57 Fundueanu G Constantin M Esposito E et al Cellulose acetatebutyrate microcapsules containing dextran ion-exchange resinsas self-propelled drug release system Biomaterials 2005 264337ndash4347

58 Maumlrtson M Viljanto J Hurme T et al Is cellulose sponge degrad-able or stable as implantation material An in vivo subcutaneousstudy in the rat Biomaterials 1999 20 1989ndash1995

59 Patel N Padera R Sanders GH et al Spatially controlled cell en-gineering on biodegradable polymer surfaces The FASEB journal1998 12 1447ndash1454

60 Goldstein A Effect of convection on osteoblastic cell growth andfunction in biodegradable polymer foam scaffolds Biomaterials2001 22 1279ndash1288

61 Wu L Ding J In vitro degradation of three-dimensional porouspoly(DL-lactide-co-glycolide) scaffolds for tissue engineeringBiomaterials 2004 25 5821ndash5830

62 Wu L Ding J Effects of porosity and pore size on in vitro degra-dation of three-dimensional porous poly(DL-lactide-co-glycolide)scaffolds for tissue engineering J Biomed Mater Res 2005 75A767ndash777

63 Pan Z Ding J Poly(lactide-co-glycolide) porous scaffolds for tissueengineering and regenerative medicine Interface Focus 2012 2366ndash377

64 Yu L Zhang Z Zhang H et al Biodegradability and biocompati-bility of thermoreversible hydrogels formed from mixing a sol anda precipitate of block copolymers in water Biomacromolecules2010 11 2169ndash2178

65 Wen X Tresco PA Fabrication and characterization of permeabledegradable poly(DL-lactide-co-glycolide) (PLGA) hollow fiberphase inversion membranes for use as nerve tract guidance chan-nels Biomaterials 2006 27 3800ndash3809

66 Chu CFL Lu A Liszkowski M et al Enhanced growth of animaland human endothelial cells on biodegradable polymers BBA-GenSubjects 1999 1472 479ndash485

67 Jo S Engel PS Mikos AG Synthesis of poly(ethylene glycol)-teth-ered poly(propylene fumarate) and its modification with GRGDpeptide Polymer 2000 41 7595ndash7604

68 Park JH Allen MG Prausnitz MR Biodegradable polymer mi-croneedles fabrication mechanics and transdermal drug deliveryJ Control Release 2005 104 51ndash66

69 Freed LE Vunjak-Novakovic G Biron RJ et al Biodegradablepolymer scaffolds for tissue engineering Nat Biotechnol 1994 12689ndash693

70 Windecker S Serruys PW Wandel S et al Biolimus-eluting stentwith biodegradable polymer versus sirolimus-eluting stent withdurable polymer for coronary revascularisation (LEADERS) arandomised non-inferiority trial Lancet 2008 372 1163ndash1173

71 Stefanini GG Kalesan B Serruys PW et al Long-term clinicaloutcomes of biodegradable polymer biolimus-eluting stents ver-sus durable polymer sirolimus-eluting stents in patients with coro-nary artery disease (LEADERS) 4 year follow-up of a randomisednon-inferiority trial Lancet 2011 378 1940ndash1948

72 Raungaard B Jensen LO Tilsted HH et al Zotarolimus-elutingdurable-polymer-coated stent versus a biolimus-eluting biodegrad-able-polymer-coated stent in unselected patients undergoing per-cutaneous coronary intervention (SORT OUT VI) a randomisednon-inferiority trial Lancet 2015 385 1527ndash1535

73 Freed LE Grande DA Lingbin Z et al Joint resurfacing using allo-graft chondrocytes and synthetic biodegradable polymer scaffoldsJ Biomed Mater Res 1994 28 891ndash899

74 Poirier Y Nawrath C Somerville C Production of polyhydrox-yalkanoates a family of biodegradable plastics and elastomers in

bacteria and plants Nat Biotechnol 1995 13 142ndash15075 Dias A Tsuru K Hayakawa S et al Crystallisation studies of

biodegradable CaO-P2O5 glass with MgO and TiO2 for boneregeneration applications Glass Technol 2004 45 78ndash79

76 Klein CPAT de Groot K Drissen AA et al Interaction ofbiodegradable β-whitlockite ceramics with bone tissue an in vivostudy Biomaterials 1985 6 189ndash192

77 Ikenaga M Hardouin P Lemaicirctre J et al Biomechanical charac-terization of a biodegradable calcium phosphate hydraulic cementa comparison with porous biphasic calcium phosphate ceramics JBiomed Mater Res 1998 40 139ndash144

78 Dias AG Lopes MA Santos JD et al In vivo performance ofbiodegradable calcium phosphate glass ceramics using the rabbitmodel histological and SEM observation J Biomater Appl 200620 253ndash266

79 Lee JH Lee CK Chang BS et al In vivo study of novel biodegrad-able and osteoconductive CaO-SiO2-B2O3 glass-ceramics JBiomed Mater Res 2006 77A 362ndash369

80 Song G Song S A possible biodegradable magnesium implant ma-terial Adv Eng Mater 2007 9 298ndash302

81 Kim WC Kim JG Lee JY et al Influence of Ca on the corrosionproperties of magnesium for biomaterials Mater Lett 2008 624146ndash4148

82 Li Z Gu X Lou S et al The development of binary Mg-Ca alloysfor use as biodegradablematerials within bone Biomaterials 200829 1329ndash1344

83 Wan Y Xiong G Luo H et al Preparation and characterization ofa new biomedical magnesium-calcium alloy Mater Des 2008 292034ndash2037

84 Seong JW Kim WJ Development of biodegradable Mg-Ca alloysheets with enhanced strength and corrosion properties throughthe refinement anduniformdispersion of theMg2Caphase by high-ratio differential speed rolling Acta Biomater 2015 11 531ndash542

85 Zhang S Li J Song Y et al In vitro degradation hemolysis andMC3T3-E1 cell adhesion of biodegradable Mg-Zn alloy Mater SciEng-C 2009 29 1907ndash1912

86 Li J Song Y Zhang S et al In vitro responses of human bone mar-row stromal cells to a fluoridated hydroxyapatite coated biodegrad-able Mg-Zn alloy Biomaterials 2010 31 5782ndash5788

87 Brar HS Wong J Manuel MV Investigation of the mechanical anddegradation properties of Mg-Sr and Mg-Zn-Sr alloys for use aspotential biodegradable implant materials J Mech Behav BiomedMater 2012 7 87ndash95

88 Bornapour M Muja N Shum-Tim D et al Biocompatibility andbiodegradability of Mg-Sr alloys the formation of Sr-substitutedhydroxyapatite Acta Biomater 2013 9 5319ndash5330

89 Gu XN Xie XH Li N et al In vitro and in vivo studies on aMg-Sr binary alloy system developed as a new kind of biodegrad-able metal Acta Biomater 2012 8 2360ndash2374

90 Haumlnzi AC Gerber I Schinhammer M et al On the in vitro andin vivo degradation performance and biological response of newbiodegradableMg-Y-Zn alloys Acta Biomater 2010 6 1824ndash1833

91 Chou DT Hong D Saha P et al In vitro and in vivo corrosioncytocompatibility and mechanical properties of biodegradableMg-Y-Ca-Zr alloys as implant materials Acta Biomater 2013 98518ndash8533

92 Zong Y Yuan G Zhang X et al Comparison of biodegradable be-haviors of AZ31 and Mg-Nd-Zn-Zr alloys in Hanks physiologicalsolution Mater Sci Eng-B 2012 177 395ndash401

93 Tie D Feyerabend FMuumlllerWD et al Antibacterial biodegradableMg-Ag alloys Eur Cell Mater 2013 25 284ndash298

94 VojtěchDKubaacutesek J Seraacutek J et al Mechanical and corrosion prop-

13 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

erties of newly developed biodegradable Zn-based alloys for bonefixation Acta Biomater 2011 7 3515ndash3522

95 Li H Yang H Zheng Y et al Design and characterizations of novelbiodegradable ternary Zn-based alloys with IIA nutrient alloyingelements Mg Ca and Sr Mater Des 2015 83 95ndash102

96 Liu X Sun J Yang Y et al Microstructure mechanical proper-ties in vitro degradation behavior and hemocompatibility of novelZn-Mg-Sr alloys as biodegradable metals Mater Lett 2016 162242ndash245

97 Wu C Qiu H Hu X et al Short-term safety and efficacy of thebiodegradable iron stent in mini-swine coronary arteries ChinMed J (Engl) 2013 126 4752ndash4757

98 Purnama A Hermawan H Champetier S et al Gene expressionprofile of mouse fibroblasts exposed to a biodegradable iron alloyfor stents Acta Biomater 2013 9 8746ndash8753

99 HermawanH Purnama A Dube D et al Fe-Mn alloys for metallicbiodegradable stents degradation and cell viability studies ActaBiomater 2010 6 1852ndash1860

100 Sheridan MH Shea LD Peters MC et al Bioabsorbable polymerscaffolds for tissue engineering capable of sustained growth factordelivery J Control Release 2000 64 91ndash102

101 Shawe S Buchanan F Harkin-Jones E et al A study on the rate ofdegradation of the bioabsorbable polymer polyglycolic acid (PGA)J Mater Sci 2006 41 4832ndash4838

102 Palmerini T Biondi-Zoccai G Della Riva D et al Clinical out-comes with bioabsorbable polymer- versus durable polymer-baseddrug-eluting and bare-metal stents J Am Coll Cardiol 2014 63299ndash307

103 Tanimoto S Serruys PW Thuesen L et al Comparison of in vivoacute stent recoil between the bioabsorbable everolimus-elutingcoronary stent and the everolimus-eluting cobalt chromium coro-nary stent insights from the ABSORB and SPIRIT trials CatheterCardiovasc Interv 2007 70 515ndash523

104 Tsuji H Sasaki H Sato H et al Neuron attachment properties ofcarbon negative-ion implanted bioabsorbable polymer of poly-lac-tic acid Nucl Instr Meth Phys Res Sect B-Beam Interact MaterAtoms 2002 191 815ndash819

105 Aikawa M Miyazawa M Okamoto K et al A novel treatment forbile duct injury with a tissue-engineered bioabsorbable polymerpatch Surgery 2010 147 575ndash580

106 WaksmanR Pakala R Kuchulakanti PK et al Safety and efficacy ofbioabsorbablemagnesium alloy stents in porcine coronary arteriesCatheter Cardiovasc Interv 2006 68 607ndash617

107 Di Mario C Griffiths H Goktekin O et al Drug-eluting bioab-sorbable magnesium stent J Interv Cardiol 2004 17 391ndash395

108 Erbel R Di Mario C Bartunek J et al Temporary scaffoldingof coronary arteries with bioabsorbable magnesium stents aprospective non-randomised multicentre trial Lancet 2007 3691869ndash1875

109 Schranz D Zartner P Michel-Behnke I et al Bioabsorbable metalstents for percutaneous treatment of critical recoarctation of theaorta in a newborn Catheter Cardiovasc Interv 2006 67 671ndash673

110 Gu X Zheng Y Cheng Y et al In vitro corrosion and biocompati-bility of binary magnesium alloys Biomaterials 2009 30 484ndash498

111 Hiromoto S InoueM Taguchi T et al In vitro and in vivo biocom-patibility and corrosion behaviour of a bioabsorbable magnesiumalloy coated with octacalcium phosphate and hydroxyapatite ActaBiomater 2015 11 520ndash530

112 Hiromoto S Tomozawa M Maruyama N Fatigue property of abioabsorbable magnesium alloy with a hydroxyapatite coatingformed by a chemical solution deposition J Mech Behav Biomed-ical Mater 2013 25 1ndash10

113 Bowen PK Drelich J Goldman J Zinc exhibits ideal physiologicalcorrosion behavior for bioabsorbable stents Adv Mater 2013 252577ndash2582

114 Liu X Sun J Yang Y et al In vitro investigation of ultra-pure Znand its mini-tube as potential bioabsorbable stent material MaterLett 2015 161 53ndash56

115 LinW Zhang G Cao P et al Cytotoxicity and its test methodologyfor a bioabsorbable nitrided iron stent J Biomed Mater Res 2015103 764ndash776

116 Coe JD Vaccaro AR Instrumented transforaminal lumbar inter-body fusion with bioresorbable polymer implants and iliac crestautograft Spine 2005 30 S76ndashS83

117 Ignatius AA Augat P Ohnmacht M et al A new bioresorbablepolymer for screw augmentation in the osteosynthesis of osteo-porotic cancellous bone a biomechanical evaluation J BiomedMater Res 2001 58 254ndash260

118 Krucoff MW Kereiakes DJ Petersen JL et al A novel biore-sorbable polymer paclitaxel-eluting stent for the treatment ofsingle and multivessel coronary disease J Am Coll Cardiol 200851 1543ndash1552

119 Kostopoulos L Karring T Guided bone regeneration in mandibu-lar defects in rats using a bioresorbable polymer Clin Oral Im-plants Res 1994 5 66ndash74

120 Dubok VA Bioceramicsmdashyesterday today tomorrow PowderMetall Metal Ceram 2000 39 381ndash394

121 Safronova T Kuznetsov A Korneychuk S et al Calcium phos-phate powders synthesized from solutions with [Ca2+][PO4

3minus]=1for bioresorbable ceramics Cent Eur J Chem 2009 7 184ndash191

122 Bohner M Bioresorbable ceramics In Buchanan FJ (Ed) Degra-dation Rate of Bioresorbable Materials Cambridge WoodheadPublishing 2008 95-114

123 Seitz JM Eifler R Stahl J et al Characterization ofMgNd2 alloy forpotential applications in bioresorbable implantable devices ActaBiomater 2012 8 3852ndash3864

124 WenCE Yamada Y Shimojima K et al Porous bioresorbable mag-nesium as bone substitute MSF 2003 419ndash422 1001ndash1006

125 Campos CM Muramatsu T Iqbal J et al Bioresorbable drug-elut-ing magnesium-alloy scaffold for treatment of coronary artery dis-ease Int J Mol Sci 2013 14 24492ndash24500

126 KirklandNT Birbilis NWalker J et al In-vitro dissolution ofmag-nesium-calcium binary alloys clarifying the unique role of calciumadditions in bioresorbable magnesium implant alloys J BiomedMater Res 2010 95B 91ndash100

127 Gastaldi D Sassi V Petrini L et al Continuum damage model forbioresorbable magnesium alloy devices mdashapplication to coronarystents J Mech Behav Biomed Mater 2011 4 352ndash365

128 Kitabata H Waksman R Warnack B Bioresorbable metal scaffoldfor cardiovascular application current knowledge and future per-spectives Cardiovasc Revasc Med 2014 15 109ndash116

Acknowledgments This work was supported by the National Key Re-search and Development Program of China (2016YFC1102402) NationalNatural Science Foundation of China (NSFC 51431002) and the NSFCand the Research Grants Council (RGC) of Hong Kong Joint ResearchScheme (51361165101 and 5161101031)

Author contributions Liu Y prepared the figures tables organized thereferences and wrote the paper Zheng Y provided the overall concept andrevised the manuscript Hayes B helped with the standard developmentand revised the manuscript All authors participated in the discussion

Conflict of interest The authors declare that they have no conflict ofinterest

14copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Yang Liu received his bachelor degree in materials science and engineering from Harbin engineering University in 2013Then he continued his study as a PhD candidate in Prof Yufeng Zhengrsquos Lab in Peking University His research interestsare mainly focused on the corrosion study of absorbable metallic biomaterials as well as the development of new kind ofMg-based biomaterials

Yufeng Zheng obtained his PhD degree from Harbin Institute of Technology in 1998 He is the National OutstandingYouth and Yangtze River scholar of China His research interests are focused on the development of novel biomaterials andapplication and design of biomedical devices

Byron Hayes an over 35 year employee of WL Gore has been involved in the commercial development of multiple ab-sorbable polymeric implants since the late 1980s Hayes started his standards development activities with ASTM in 2000where he is actively developing standards for polymeric and metallic absorbable implants In 2010 Hayes also becameinvolved with ISO Technical Committees TC150 and TC194 and is now convener of working groups focused on cardiovas-cular and metallic absorbable implants

可降解可吸收再吸收mdashmdash哪个是描述最终被人体吸收生物材料的最好词汇刘洋1 郑玉峰1 拜伦海耶斯2

摘要 关于最终被人体吸收的植入材料领域内文献采用的英文修饰词长期以来混乱且不同不仅造成文献检索困难同时模糊了研究人员的研究边界 此领域在法律法规标准中统一用词的确定为领域内的科学研究产品销售及产品使用说明奠定了基础 我们基于化学生态学材料学生物学微生物学和药学立足于使用习惯法律标准和市场对领域内使用已久的典型修饰词ldquo生物可降解rdquoldquo再吸收rdquo和ldquo可吸收rdquo进行了讨论和解释 总的来说尽管目前绝大多数修饰语实际想表达的意思相同作者认为ldquo可吸收rdquo这一英文修饰语是最恰当的修饰词 同时我们提议进一步规范和统一该领域修饰词的使用

15 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

  • Degradable absorbable or resorbablemdashwhat is the best grammatical modifier for an implant that is eventually absorbed by the body
  • Abstract
  • INTRODUCTION
    • Current situation
    • Standards development in advance
      • TERMINOLOGY
        • Overview of utilization of the terms ldquodegradationrdquoldquobiodegradationrdquo and ldquodegradablerdquoldquobiodegradablerdquo
        • Overview of utilization of the terms ldquoabsorptionrdquoldquobioabsorptionrdquo and ldquoabsorbablerdquoldquobioabsorbablerdquo
        • Overview of utilization of the terms ldquoresorptionrdquoldquobioresorptionrdquo and ldquoresorbablerdquoldquobioresorbablerdquo
        • Utilization and comparison of the terms ldquobiodegradable metalsrdquo and ldquoabsorbable metallic materialsrdquo
        • Summary quantification of the common Terms
          • DISCUSSION
            • Expertise inherent biases
            • Connotation and extension of noun forms ldquobiodegradation bioabsorption and bioresorptionrdquo and adjectives ldquobiodegradable bioabsorbable and bioresorbablerdquo
              • CONCLUDING REMARKS
              • References
              • Acknowledgements

Table 3 US-FDA suture product codes and accompanying citation of US CFRsa)

Suture name Regulation Product code

Absorbable polydioxanone surgical (PDS) suture 21 CFR8784840 NEW

Absorbable poly(glycolideL-lactide) surgical suture 21 CFR8784493 GAM

Absorbable gut suture 21 CFR8784830 GAL

Nonabsorbable poly(ethylene terephthalate) suture 21 CFR8785000 GAT

Nonabsorbable polypropylene surgical suture 21 CFR8785010 GAW

Nonabsorbable polyamide surgical suture 21 CFR8785020 GAR

Natural nonabsorbable silk surgical suture 21 CFR8785030 GAP

Stainless steel surgical suture 21 CFR8784495 GAQ

Nonabsorbable expanded polytetrafluoroethylene (ePTFE)surgical suture

21 CFR8785030 NBY

a) Note this table selects abbreviated results obtained from online search for the implant device term ldquosuturerdquo that was conducted on 6 Aug 2016 athttpwwwaccessdatafdagovscriptscdrhcfdocscfPCDclassificationcfm

FDA and a US Code of Federal Regulations preference forabsorbable terminology when referring to sutures Table4 shows an expansion of that preference to include a to-tal of 30 absorbable implant product classifications each ofwhich is assigned to a relevant Federal regulation that uti-lizes the term ldquoabsorbablerdquoIn short ldquoabsorbablerdquo is both a historically well estab-

lished and currently relevant term in both the regulationand standardization of implants that are intentionally ab-sorbed by the body

Overview of utilization of the terms ldquoresorptionrdquoldquobiore-sorptionrdquo and ldquoresorbablerdquoldquobioresorbablerdquoIn the scope of chemistry the term ldquoresorptionrdquo was used toillustrate the total elimination of a substance from its initialplace caused by physical andor chemical phenomena [14]Besides the understanding from pure chemistry ldquoresorp-tionrdquo is more recognized involved in the metabolic activi-ties in vivo For example ldquoresorptionrdquo is considered as theldquoabsorptionrdquo into the circulatory system of cells or tissuewhich usually includes bone resorption tooth resorptionand vanishing twin [44] In the biomedical scope Prof DWilliams used themeaning in DorlandMedical Dictionaryas ldquolysis and assimilation of a substance as of bonerdquo [23]ldquoBioresorptionrdquo is more common when describing the invivo process of a certain foreign material The ISO definedldquobioresorptionrdquo as a process by which biomaterials are de-graded in the physiological environment and the by-prod-uct are eliminated or completely bioabsorbed [23] Thusaccording to this interpretation the bioresorption processincludes material removal in vivo either by cellular activ-ity or not Conversely Taberrsquos Cyclopedic Medical Dictio-nary [45] describes the term ldquoresorbrdquo as themeaning ldquoto ab-

sorb againrdquomdashsomething that live tissue does but not some-thing any implant is known to domdashbe it permanent or ab-sorbableAs for the adjectives ldquobioresorbablerdquo and ldquoresorbablerdquo

there is no difference when used to describe a kind of ma-terials which have the ability of resorption This is ascribedto the fact that ldquoresorptionrdquo itself already has been well rec-ognized as a biological process [23] Currently there is noASTM entries used ldquoresorbablerdquo or ldquobioresorbablerdquo in thetitle

Utilization and comparison of the terms ldquobiodegradablemetalsrdquo and ldquoabsorbable metallic materialsrdquoldquoBiodegradablemetalsrdquo generally include themetalsMg Feand Zn and their alloys and composites They can be de-fined as metals that assist with tissue healing and are thenexpected to gradually corrode and release corrosion prod-ucts in vivowith an appropriate host response and then dis-solve completely with no implant residues [46] As a resultand different from traditional ldquobio-inertrdquometallic biomate-rials (eg Ti and Co based alloys) that release limited cor-rosion products [47] metabolic reactions besides inflam-mation can be expected to occur between the biodegrad-able metal and the host body after implantation Addition-ally the corrosion-based degradation mechanism of thesematerials is inherently different from that of either bioce-ramics or polymers which has resulted in limited to nostandardized guidance available from either ASTM or ISOInstead of the term ldquobiodegradable metalrdquo the recently

published and first absorbable metal related standardASTM F3160 utilizes the more inclusive word ldquoabsorbablerdquowithin the phrase ldquoabsorbable metallic materialsrdquo andagain defines the term as ldquohellip an initially distinct foreign

6copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Table 4 US-FDA absorbable implant related product codes descriptions and accompanying CFRsa)

Product code Device Device class Regulation number Regulation description

OMT Absorbable lung biopsy plug 2 [8784755] Absorbable lung biopsy plug

LMF Agent absorbable hemostatic collagen based 3 [8784490] Absorbable hemostatic agent and dressing

LMG Agent absorbable hemostatic non-collagen based 3 [8784490] Absorbable hemostatic agent and dressing

MRY Appliances and accessories fixation bone absorbable singlemultiple component 2 [8883040] Smooth or threaded metallic bone fixation fastener

PBQ Fixation non-absorbable or absorbable for pelvic use 2 [8844530] Obstetric-gynecologic specialized manual instrument

HQJ Implant absorbable (scleral buckling methods) 2 [8863300] Absorbable implant (scleral buckling method)

OWT Mesh surgical absorbable abdominal hernia 2 [8783300] Surgical mesh

OXM Mesh surgical absorbable fistula 2 [8783300] Surgical mesh

OXI Mesh surgical absorbable large abdominal wall defects 2 [8783300] Surgical mesh

OXL Mesh surgical absorbable organ support 2 [8783300] Surgical mesh

OWW Mesh surgical absorbable orthopaedics reinforcement of tendon 2 [8783300] Surgical mesh

OXF Mesh surgical absorbable plastic and reconstructive surgery 2 [8783300] Surgical mesh

OXC Mesh surgical absorbable staple line reinforcement 2 [8783300] Surgical mesh

OWZ Mesh surgical absorbable thoracic chest wall reconstruction 2 [8783300] Surgical mesh

OWU Mesh surgical non-absorbable diaphragmatic hernia 2 [8783300] Surgical mesh

OWR Mesh surgical non-absorbable facial implants for plastic surgery 2 [8783300] Surgical mesh

OXJ Mesh surgical non-absorbable large abdominal wall defects 2 [8783300] Surgical mesh

OWX Mesh surgical non-absorbable orthopaedics reinforcement of tendon 2 [8783300] Surgical mesh

OXG Mesh surgical non-absorbable plastic and reconstructive surgery 2 [8783300] Surgical mesh

OXD Mesh surgical non-absorbable staple line reinforcement 2 [8783300] Surgical mesh

OXA Mesh surgical non-absorbable thoracic chest wall reconstruction 2 [8783300] Surgical mesh

LBP Replacement ossicular (stapes) using absorbable gelatin material 2 [8743450] Partial ossicular replacement prosthesis

OLL Septal staplerabsorbable staples 2 [8784750] ImplanTABLE staple

MNU Staple absorbable 2 [8883030] Singlemultiple component metallic bone fixationappliances and accessories

GAK Suture absorbable 2 [8784830] Absorbable surgical gut suture

GAL Suture absorbable natural 2 [8784830] Absorbable surgical gut suture

HMO Suture absorbable ophthalmic 3

GAN Suture absorbable synthetic 2 [8784830] Absorbable surgical gut suture

GAM Suture absorbable synthetic polyglycolic acid 2 [8784493] Absorbable poly(glycolidel-lactide) surgical suture

NEW Suture surgical absorbable polydioxanone 2 [8784840] Absorbable polydioxanone surgical suture

a) Note the results obtained from online search for the device term ldquoabsorbablerdquo that was conducted on 6 Aug 2016 at httpwwwaccessdatafdagovscriptscdrhcfdocscfPCDclassifica-tioncfm

7 copy

ScienceChina

Pressand

Springer-VerlagBerlin

Heidelberg 2017

SCIENCECH

INAMaterials

REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

material or substance that either directly or through in-tended degradation can pass through or be metabolized orassimilated by cells andor tissuerdquo The standardrsquos nomen-clature appendix further elaborates on its preference forldquoabsorbablerdquo since the prefix ldquobio-rdquo is redundant in thecontext of implant applications [43]Clearly these two terms of ldquobiodegradable metalsrdquo and

ldquoabsorbable metallic materialsrdquo share the same connota-tion which defines the completemission of an intentionallydegradable material when implanted in vivo In the contextof biodegradable metalsabsorbable metallic materialsthe process includes the corrosion caused by body fluida host response caused by corrosion products followedby dissolutionabsorption and finally improved tissuehealing The ldquobiodegradationrdquo instead of ldquobiocorrosionrdquois used to distinguish this new kind of metals which canfully dissolve in vivo with no implant residues Besidesbiodegradation process the following dynamic process ofdissolutionabsorption also starts in vivo For exampledissolved Mg2+ is considered to enhance the integrin me-diated human-bone-derived cell adhesion and affect newbone formation [48] The metabolic reaction is also crucialand even more important for biodegradable metals as it ishelpful It is another distinction from traditional metalsused for biomedical application In fact the different usagehabit forming of ldquobiodegradablerdquo or ldquoabsorbablerdquoldquobioab-sorbablerdquo may be more related with the study field theresearchers in Taking the ldquoabsorbablerdquo metallic stent asan example (Fig 2) once the ldquoabsorbablerdquo metallic stentwas implanted into blood vessel ldquocorrosionrdquo of biometal

begins The corrosion products including debris hydro-gen (for Mg-based metals) metallic ions and hydroxylconvert the local environment and diffuse into the bloodvessel wall Some corrosion products can be biologicallybeneficial For instance the diffused and absorbed Zn2+

can potentially play a positive role in dealing with athero-sclerosis [49] Along with the corrosion process healingprocesses such as endothelialization may become en-hanced In summary and within the context of absorbablemetals the adjectives ldquodegradablerdquo and ldquoabsorbablerdquo referto the nature of the biodegradation products of the mate-rialdevice being metabolically absorbed an attribute ofthe host (animal or human body) regardless of whetherthe implant degrades corrodes hydrolyzes or dissolves[50ndash52]

Summary quantification of the common TermsFig 3a shows preliminary searching results in Webof Knowledge using ldquodegradablerdquo ldquoabsorbablerdquo or ldquore-sorbablerdquo along with ldquomaterialrdquo as key words Theutilization of ldquodegradablerdquo is a bit more frequently thanldquoabsorbablerdquo but that of ldquoresorbablerdquo steps down Mean-while the counterpart searching result when using ldquobiordquo asprefix to the adjectives along with ldquomaterialrdquo as keywordsare presented in Fig 3b ldquoBiodegradable materialrdquo is themost common utilization which holds 91 among the ex-pression approach This is also due to the fact that besidesthe common utilization in biomaterials ldquobiodegradablerdquois also used in a wide range of applications such as cleanenvironment and ecology [5354]

Figure 2 Different point of views on the biodegradationabsorption process

8copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Figure 3 Searching results in Web of Knowledge from all databases (a) with the total searched publication numbers by ldquodegradablerdquo+ ldquomaterialrdquoldquoabsorbablerdquo+ ldquomaterialrdquo and ldquoresorbablerdquo+ ldquomaterialrdquo as 100 (b) the total searched publication numbers by ldquobiodegradablerdquo+ ldquomaterialrdquo ldquobioab-sorbablerdquo+ ldquomaterialrdquo and ldquobioresorbablerdquo+ ldquomaterialrdquo as 100

DISCUSSION

Expertise inherent biasesAs previously mentioned biomaterial is an interdiscipli-nary field fascinating researchers with specialty from dif-ferent backgrounds Different backgrounds as well as dif-ferent research point of interests may be one of the reasonsfor using different terminologies Materials scientists tendto focus on the materialdevice itself leading to their usageof ldquobiodegradablerdquo to illustrate what happens to the deviceThey pay more attention to the process such as hydroly-sis corrosion debris degradation products and the changeof surface morphology resulting in the researching inter-ests of ldquomaterial biodegradationrdquo In contrast surgeons andbiomedical researchers tend to be concerned more on thehost response and healing process They are curious aboutthe absorption of various degradation products of the im-planted materialdevice and related metabolism mecha-nism and thereby prefer to use the term ldquoabsorbablerdquo toillustrate what happens to the device As known somema-terials may only undergo biodegradation but the corrosionproducts still have no influence on the metabolic activitiesFor example cellulose is considered as ldquodietary fiberrdquowhichcannot be digested and absorbed by human body but is be-nign for human body [55] Some coating tablets for drug ordrug delivery systems made from cellulose and its deriva-tives are quite frequently utilized or investigated [5657]The polymer and derivatives of cellulose can only be de-graded but not be absorbed by human body [58] For suchmaterials the adjective ldquoabsorbablerdquo or ldquobioabsorbablerdquo isnot appropriateOverall once the materialsdevices are implanted into

the human body the ldquobiocorrosionrdquobiodegradationrdquoprocess happens immediately no matter to what degreeat the same time the host will biologically response to the

corrosiondegradation products through the absorptionmetabolism and excretion processes So for the samestory the majority of materials scientists would report itby ldquobiodegradabledegradationrdquo way whereas the majorityof medical doctors would report it by ldquoabsorbableab-sorptionrdquo way In nature the two terms ldquobiodegradablemetalsrdquo and ldquoabsorbable metallic materialsrdquo share the sameconnotation and are mutually replaceable

Connotation and extension of noun forms ldquobiodegradationbioabsorption and bioresorptionrdquo and adjectivesldquobiodegradable bioabsorbable and bioresorbablerdquoThe three noun forms of the terms illustrate the processwhile their adjectival derivatives were used to describe thegroup of materials with such certain capabilities For thestudy on biomaterials polymer researchers use ldquodegrada-tionbiodegradationrdquo when there is proved chain scissionprocess Besides they differentiate ldquobiodegradationrdquo andldquodegradationrdquo by confirmed metabolic activities betweenthe materials and cells or tissues Regarding to the fouradjectives ldquobiodegradablerdquo ldquobioabsorbablerdquo and ldquobiore-sorbablerdquo the term ldquobiocorrodiblerdquo is only used in scientificpapers on iron based materials and some patents on mag-nesium based materials The common usage of termsldquobiodegradablerdquo ldquobioabsorbablerdquo and ldquobioresorbablerdquo withrespect to the biomaterial research area is shown in Table 5The results reveal a widespread usage of ldquobiodegradablerdquo inboth polymers and magnesium based metals Varies typesof materials were reported as biomaterials Besides thereare also reports of ldquobiodegradablerdquo polymers for ecologyand environmental protection which indicates a furtherusage scope of ldquobiodegradablerdquo not only for implants anddevices Besides ldquobioresorbablerdquo is also utilized in all theresearch fields of polymers ceramics andmetals Howeverno current work used ldquobioabsorbablerdquo as grammatical

9 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Table 5 Current reported usage of terms ldquobiodegradablerdquo ldquobioabsorbablerdquo and ldquobioresorbablerdquoTerminology Category Materials Applications

PLA-PEG-biotin PLGA Controlled cell engineering [5960]Porous PLGA Tissue engineering [61ndash63]

PLGA-PEG-PLGA Injective thermosensitive hydrogel [64]PLGA Nerve guidance [65]

Fibronectin (Fn)-coated PLLA P(LLA-CL) Enhanced growth of endothelial cells [6066]PEG tethered PPF [67]

PDMS Drug delivery [68]PGA Tissue engineering [69]

Undefined Coronary stent [70ndash72]PGA Joint resurfacing [73]

Polymers

PHA Ecology and environmental protection [74]CaO-P2O5 glass Bone regeneration [75]β-Whitlockite Bone regeneration [76]

Calcium phosphate hydraulic cement Bone regeneration [77]Calcium

phosphate glass ceramicsBone regeneration [78]

Ceramics

CaO-SiO2-B2O3 glass-ceramics Bone regeneration [79]Pure Mg Implant material [80]

Mg-Ca-based Bone regeneration [81ndash84]Mg-Zn-based Bone regeneration [338586]Mg-Sr-based Bone regeneration [87ndash89]Mg-RE-based Vascular stent [90ndash92]

Mg and its metals

Mg-Ag-based [93]Zn-Mg Zn-Ca Zn-Sr [9495]Zn and its metals Zn-Mg-Sr [96]

Fe [9798]

Biodegradable

Fe and its metals Fe-Mn [99]PLLA PLG PGA Molecule delivery [100]

PGA Suture [101]Undefined Drug-eluting stent [102103]

PLA Neuron attachment [104]Polymers

PLA and PCL reinforced with PGA fibers Bile duct patch [105]Mg-RE based Coronary stent [106ndash109]

Binary Mg alloys [110]Mg and its metalsMg-Al-based [111112]

Zn and its metals Pure Zinc [113114]Fe and its metals Nitrided iron [115]

PLDLA Transforaminal lumbar interbody fusion [116]Alkylene bis(dilactoyl)-methacrylate modified polymer Bone screw augmentation [117]

Undefined Coronary stent [118]PHB Mandibular defects regeneration [119]HA Bone regeneration [120]Ceramics Calcium phosphate [121122]

MgNd2 Stent material [123]Porous Mg Bone substitute [124]Mg-RE Coronary stent [125]Mg-Ca Orthopedic application [126]

Mg and its metals

Mg-based Finite element analysis [127]

Bioabsorbable

Fe and its metals Pure Fe [128]

10copy

ScienceChina

Pressand

Springer-VerlagBerlin

Heidelberg 2017

REVIEWSCIENCE

CHINA

Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

modifier to bioceramics In addition as previouslyillustrated the prefix ldquobiordquo of ldquobioabsorbablerdquo and ldquobiore-sorbablerdquo are abridged hereafter discussion will concen-trate on ldquobiocorrodiblerdquo ldquobiodegradablerdquo ldquoabsorbablerdquo andldquoresorbablerdquoSince absorbable technologies are increasingly utilized

in numerous new and broader implant applications it be-comes more important to not acquiesce in addressing his-torical problems and instead actively move forward towardutilizing standardized language that is both technically ac-curate and unified in itsmeaning Preferred language needsto accurately communicate the concept To achieve the uni-fying goal of harmonized terminology themedical and sci-entific communities need to not solely look at materialschemistry or even biomaterials alone but to instead lookat term selection both across and within the context of thebroader medical disciplinemdashthe location where the resultsof implant technology development actually reaches themarketplace where therapies are brought to those in needNomenclature solutions need to both understand and re-spond to the context of terms across adjacent technologieswhich means to address needs from the perspectives of thebiomaterial researcher the deviceproduct developer thesurgeonclinician user the regulator and last but not leastthe patientgeneral public who is the direct beneficiary ofthe developed technologyA better understanding of these terminologies is neces-

sary and beneficial to the field Therefore the definitionson ldquodegradablerdquo ldquoabsorbablerdquo ldquoresorbablerdquo and relatedterms proposed by different organizations in differentfields have been summarized and discussed with the con-notation and extension of each term being compared andthe criteria being proposed

CONCLUDING REMARKSHerein given both the searching problem on the Internetand ambiguity in meanings the usage of grammaticalmodifiers to describe biomaterials that is eventually ab-sorbed by human body has been enumerated based onusage habits laws standards and markets In summaryldquodegradablerdquoldquobiodegradablerdquo are the most frequently usedgrammatical modifier not only in metals but also poly-mers as such kind of biomaterials ldquoBiodegradationrdquo andldquobiodegradablerdquo define the change of the materialdevicewell in the research of biomaterials but they are alsoadopted in other fields such as ecology and environmentalprotection Meanwhile ldquoresorbablerdquoldquobioresorbablerdquo havelong been recognized in the biological research and theldquoresorptionrdquo itself has been widely accepted as a biological

reaction The utilization of ldquoresorbablerdquoldquobioresorbablerdquowas found to be not as frequent as the counterpartsldquodegradablerdquoldquobiodegradablerdquo and ldquoabsorbablerdquoldquobioab-sorbablerdquo Such usage is accurate for osteoclast driven boneresorption but is inappropriate for implants that do notcarry the potential to grow back into their original formOtherwise despite it is not the most frequently used termldquoabsorbablerdquoldquobioabsorbablerdquo concentrates more on thehost metabolism to the foreign biodegradation productsof the implanted materialdevice compared with ldquodegrad-ablerdquoldquobiodegradablerdquo ldquoAbsorbablerdquo is defined in the scopeof biomaterials by different organizations and their publi-cations and also adopted by ASTM to illustrate ldquoabsorbablepolymerrdquo It is the most historically established the mostbroadly applicable (includes dissolvable devices that donot degrade) the most specific to medical applicationsand is the formal legal descriptor for most implant devicesConsidering the usage history common utilization in lawand standards as well as the scientific meaning in essenceldquoabsorbablerdquo can be better among other grammaticalmodifiers for description of an implant that is eventuallyabsorbed by the body which is recommended by theauthors for a further internationally-unified usage

Received 28 February 2017 accepted 27 March 2017published online 26 April 2017

1 Mackenzie D The history of sutures Med Hist 1973 17 158ndash1682 Hench LL Bioceramics J Am Ceramic Soc 2005 81 1705ndash17283 Hench LL Bioceramics from concept to clinic J AmCeramic Soc

1991 74 1487ndash15104 Windhagen H Radtke K Weizbauer A et al Biodegradable

magnesium-based screw clinically equivalent to titanium screw inhallux valgus surgery short term results of the first prospectiverandomized controlled clinical pilot study BioMed Eng OnLine2013 12 62

5 Schildwaumlchter M Biotronik announces CE mark for magmaristhe first clinically-proven bioresorbable magnesium scaffoldhttpwwwmagmariscomennewsroomjune-15-2016

6 Shalaby SW Burg KJL Bioabsorbable polymers update degrada-tion mechanisms safety and application J App Biomater 1995 6219ndash221

7 Vert M Li SM Spenlehauer G et al Bioresorbability and biocom-patibility of aliphatic polyesters J Mater Sci-Mater Med 1992 3432ndash446

8 Vert M Degradable and bioresorbable polymers in surgery and inpharmacology beliefs and facts J Mater Sci-Mater Med 2009 20437ndash446

9 Benicewicz BC Hopper PK Review polymers for absorbablesurgical suturesmdashPart I J Bioactive Compatible Polym 1990 5453ndash472

10 Barrows HT Synthetic bioabsorbable polymers In Szycher M(Ed) High Performance Biomaterials A Complete Guide toMed-ical and Pharmceutical Applications Boca Raton CRC PRESS1991 243ndash257

11 Weiler A Hoffmann RFG Staumlhelin AC et al Biodegradable

11 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

implants in sports medicine the biological base Arthroscopy-JArthroscopic Related Surgery 2000 16 305ndash321

12 Ikada Y Tsuji H Biodegradable polyesters for medical and ecolog-ical applications Macromol Rapid Commun 2000 21 117ndash132

13 Ashammakhi N Peltoniemi H Waris E et al Developments incraniomaxillofacial surgery use of self-reinforced bioabsorbableosteofixation devices Plast Reconstr Surg 2001 108 167ndash180

14 Vert M Doi Y Hellwich KH et al Terminology for biorelatedpolymers and applications (IUPACRecommendations 2012) PureAppl Chem 2012 84 377ndash410

15 The United States Pharmacopeial Convention The Second Sup-plement to the Pharmacopeia of the United States of America 11thdecennial revision (USP XI-1939 Supplement) 1939

16 Truhlsen SM The recession operation histopathologic responseand suture reaction and absorption Trans Am Ophthalmol Soc1965 63 626ndash677

17 USP in US Law httpwwwusporgprintabout-usplegal-recog-nitionusp-us-law

18 USP develops and publishes standards for drug substances drugproducts excipients and dietary supplements in the United StatesPharmacopeia-National Formulary (USP-NF)

19 United States Public Law 94-295 197620 United States Pharmacopeia httpwwwusporg21 British Pharmacopeia httpswwwpharmacopoeiacom22 European Pharmacopoeia httponlinepheurorgENentryhtm23 Williams DF The Williams Dictionary of Biomaterials Liverpool

Liverpool University Press 199924 httpsenwikipediaorgwikiBiodegradation25 Jones RG Kahovec J Stepto R et al Compendium of Polymer

Terminology and Nomenclature IUPAC Recommendations 2008Cambridge RSC Publishing 2009

26 Higashi S Yamamuro T Nakamura T et al Polymer-hydroxyap-atite composites for biodegradable bone fillers Biomaterials 19867 183ndash187

27 de Groot K Bioceramics of Calcium Phosphate Boca Raton CRCPress 1983

28 Hollinger JO Battistone GC Biodegradable bone repair materialssynthetic polymers and ceramics ClinOrthopRelat Res 1986 207290ndash306

29 ASTMD653-14 Standard Terminology Relating to Soil Rock andContained Fluids ASTM International West Conshohocken PA2014 httpswwwastmorgStandardsD653htm

30 Witte F Hort N Vogt C et al Degradable biomaterials based onmagnesium corrosion Curr Opin Solid State Mater Sci 2008 1263ndash72

31 Lynn DM Langer R Degradable poly(β-amino esters) synthesischaracterization and self-assemblywith plasmidDNA JAmChemSoc 2000 122 10761ndash10768

32 Cima LG Vacanti JP Vacanti C et al Tissue engineering by celltransplantation using degradable polymer substrates J BiomechEng 1991 113 143ndash151

33 Zhang S Zhang X Zhao C et al Research on an Mg-Zn alloy as adegradable biomaterial Acta Biomater 2010 6 626ndash640

34 Anseth KS Metters AT Bryant SJ et al In situ forming degradablenetworks and their application in tissue engineering and drug de-livery J Control Release 2002 78 199ndash209

35 Forrest ML Koerber JT Pack DW A degradable polyethyleniminederivative with low toxicity for highly efficient gene delivery Bio-conjugate Chem 2003 14 934ndash940

36 ASTM E2747-11 Standard Specification for Evaluation and Selec-tion of Onsite Offices for Environmentally Sustainable MeetingsEvents Trade Shows and Conferences ASTM International

West Conshohocken PA 2011 httpswwwastmorgStan-dardsE2747htm

37 ASTM E2745-11 Standard Specification for Evaluation andSelection of Audio Visual (AV) and Production for Environ-mentally Sustainable Meetings Events Trade Shows and Con-ferences ASTM International West Conshohocken PA 2011httpswwwastmorgStandardsE2745htm

38 ASTM E2746-11 Standard Specification for Evaluation andSelection of Communication and Marketing Materials for En-vironmentally Sustainable Meetings Events Trade Shows andConferences ASTM International West Conshohocken PA 2011httpswwwastmorgStandardsE2746htm

39 ASTM E2741-11 Standard Specification for Evaluation and Se-lection of Destinations for Environmentally Sustainable MeetingsEvents Trade Shows and Conferences ASTM InternationalWest Conshohocken PA 2011 httpswwwastmorgStan-dardsE2741htm

40 0 ASTM E2773-11 Standard Specification for Evaluation andSelection of Food and Beverage for Environmentally SustainableMeetings Events Trade Shows and Conferences ASTM Interna-tional West Conshohocken PA 2011 httpswwwastmorgStan-dardsE2773htm

41 ASTM E2742-11 Standard Specification for Evaluation and Selec-tion of Exhibits for Environmentally Sustainable Meetings EventsTrade Shows and Conferences ASTM International West Con-shohocken PA 2011 httpswwwastmorgStandardsE2742htm

42 ASTM E2774-11 Standard Specification for Evaluation and Selec-tion of Venues for Environmentally Sustainable Meetings EventsTrade Shows and Conferences ASTM International West Con-shohocken PA 2011 httpswwwastmorgStandardsE2774htm

43 ASTM F2902-12 Standard Guide for Assessment of AbsorbablePolymeric Implants ASTM International West ConshohockenPA 2012 httpswwwastmorgStandardsF2902htm

44 httpsenwikipediaorgwikiResorption45 Venes D Tabers Cyclopedic Medical Dictionary 22th edition

Philadelphia F A Davis Company 201346 Zheng YF Gu XN Witte F Biodegradable metals Mater Sci Eng-

R-Rep 2014 77 1ndash3447 Hanawa T Metal ion release from metal implants Mater Sci

Eng-C 2004 24 745ndash75248 Zreiqat H Howlett CR Zannettino A et al Mechanisms of mag-

nesium-stimulated adhesion of osteoblastic cells to commonly usedorthopaedic implants J Biomed Mater Res 2002 62 175ndash184

49 Little PJ Bhattacharya R Moreyra AE et al Zinc and cardiovascu-lar disease Nutrition 2010 26 1050ndash1057

50 Seager H Drug-delivery products and the Zydis fast-dissolvingdosage form J Pharm Pharmacol 1998 50 375ndash382

51 Shikinami Y Shape-memory biodegradable and absorbable mate-rial US Patent No 6281262 2001-8-28

52 Huitema TW Knight GW Ransick MH Schulze DR Surgical im-plant with preferential corrosion zone US Patent No 79059022011-3-15

53 Luzier WD Materials derived from biomassbiodegradable mate-rials Proc Natl Acad Sci USA 1992 89 839ndash842

54 Gross RA Kalra B Biodegradable polymers for the environmentScience 2002 297 803ndash807

55 Trumbo P Schlicker S Yates AA et al Dietary reference intakesfor energy carbohydrate fiber fat fatty acids cholesterol proteinand amino acids J Am Diet Assoc 2002 102 1621ndash1630

56 Chambin O Champion D Debray C et al Effects of different cel-lulose derivatives on drug release mechanism studied at a prefor-mulation stage J Control Release 2004 95 101ndash108

12copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

57 Fundueanu G Constantin M Esposito E et al Cellulose acetatebutyrate microcapsules containing dextran ion-exchange resinsas self-propelled drug release system Biomaterials 2005 264337ndash4347

58 Maumlrtson M Viljanto J Hurme T et al Is cellulose sponge degrad-able or stable as implantation material An in vivo subcutaneousstudy in the rat Biomaterials 1999 20 1989ndash1995

59 Patel N Padera R Sanders GH et al Spatially controlled cell en-gineering on biodegradable polymer surfaces The FASEB journal1998 12 1447ndash1454

60 Goldstein A Effect of convection on osteoblastic cell growth andfunction in biodegradable polymer foam scaffolds Biomaterials2001 22 1279ndash1288

61 Wu L Ding J In vitro degradation of three-dimensional porouspoly(DL-lactide-co-glycolide) scaffolds for tissue engineeringBiomaterials 2004 25 5821ndash5830

62 Wu L Ding J Effects of porosity and pore size on in vitro degra-dation of three-dimensional porous poly(DL-lactide-co-glycolide)scaffolds for tissue engineering J Biomed Mater Res 2005 75A767ndash777

63 Pan Z Ding J Poly(lactide-co-glycolide) porous scaffolds for tissueengineering and regenerative medicine Interface Focus 2012 2366ndash377

64 Yu L Zhang Z Zhang H et al Biodegradability and biocompati-bility of thermoreversible hydrogels formed from mixing a sol anda precipitate of block copolymers in water Biomacromolecules2010 11 2169ndash2178

65 Wen X Tresco PA Fabrication and characterization of permeabledegradable poly(DL-lactide-co-glycolide) (PLGA) hollow fiberphase inversion membranes for use as nerve tract guidance chan-nels Biomaterials 2006 27 3800ndash3809

66 Chu CFL Lu A Liszkowski M et al Enhanced growth of animaland human endothelial cells on biodegradable polymers BBA-GenSubjects 1999 1472 479ndash485

67 Jo S Engel PS Mikos AG Synthesis of poly(ethylene glycol)-teth-ered poly(propylene fumarate) and its modification with GRGDpeptide Polymer 2000 41 7595ndash7604

68 Park JH Allen MG Prausnitz MR Biodegradable polymer mi-croneedles fabrication mechanics and transdermal drug deliveryJ Control Release 2005 104 51ndash66

69 Freed LE Vunjak-Novakovic G Biron RJ et al Biodegradablepolymer scaffolds for tissue engineering Nat Biotechnol 1994 12689ndash693

70 Windecker S Serruys PW Wandel S et al Biolimus-eluting stentwith biodegradable polymer versus sirolimus-eluting stent withdurable polymer for coronary revascularisation (LEADERS) arandomised non-inferiority trial Lancet 2008 372 1163ndash1173

71 Stefanini GG Kalesan B Serruys PW et al Long-term clinicaloutcomes of biodegradable polymer biolimus-eluting stents ver-sus durable polymer sirolimus-eluting stents in patients with coro-nary artery disease (LEADERS) 4 year follow-up of a randomisednon-inferiority trial Lancet 2011 378 1940ndash1948

72 Raungaard B Jensen LO Tilsted HH et al Zotarolimus-elutingdurable-polymer-coated stent versus a biolimus-eluting biodegrad-able-polymer-coated stent in unselected patients undergoing per-cutaneous coronary intervention (SORT OUT VI) a randomisednon-inferiority trial Lancet 2015 385 1527ndash1535

73 Freed LE Grande DA Lingbin Z et al Joint resurfacing using allo-graft chondrocytes and synthetic biodegradable polymer scaffoldsJ Biomed Mater Res 1994 28 891ndash899

74 Poirier Y Nawrath C Somerville C Production of polyhydrox-yalkanoates a family of biodegradable plastics and elastomers in

bacteria and plants Nat Biotechnol 1995 13 142ndash15075 Dias A Tsuru K Hayakawa S et al Crystallisation studies of

biodegradable CaO-P2O5 glass with MgO and TiO2 for boneregeneration applications Glass Technol 2004 45 78ndash79

76 Klein CPAT de Groot K Drissen AA et al Interaction ofbiodegradable β-whitlockite ceramics with bone tissue an in vivostudy Biomaterials 1985 6 189ndash192

77 Ikenaga M Hardouin P Lemaicirctre J et al Biomechanical charac-terization of a biodegradable calcium phosphate hydraulic cementa comparison with porous biphasic calcium phosphate ceramics JBiomed Mater Res 1998 40 139ndash144

78 Dias AG Lopes MA Santos JD et al In vivo performance ofbiodegradable calcium phosphate glass ceramics using the rabbitmodel histological and SEM observation J Biomater Appl 200620 253ndash266

79 Lee JH Lee CK Chang BS et al In vivo study of novel biodegrad-able and osteoconductive CaO-SiO2-B2O3 glass-ceramics JBiomed Mater Res 2006 77A 362ndash369

80 Song G Song S A possible biodegradable magnesium implant ma-terial Adv Eng Mater 2007 9 298ndash302

81 Kim WC Kim JG Lee JY et al Influence of Ca on the corrosionproperties of magnesium for biomaterials Mater Lett 2008 624146ndash4148

82 Li Z Gu X Lou S et al The development of binary Mg-Ca alloysfor use as biodegradablematerials within bone Biomaterials 200829 1329ndash1344

83 Wan Y Xiong G Luo H et al Preparation and characterization ofa new biomedical magnesium-calcium alloy Mater Des 2008 292034ndash2037

84 Seong JW Kim WJ Development of biodegradable Mg-Ca alloysheets with enhanced strength and corrosion properties throughthe refinement anduniformdispersion of theMg2Caphase by high-ratio differential speed rolling Acta Biomater 2015 11 531ndash542

85 Zhang S Li J Song Y et al In vitro degradation hemolysis andMC3T3-E1 cell adhesion of biodegradable Mg-Zn alloy Mater SciEng-C 2009 29 1907ndash1912

86 Li J Song Y Zhang S et al In vitro responses of human bone mar-row stromal cells to a fluoridated hydroxyapatite coated biodegrad-able Mg-Zn alloy Biomaterials 2010 31 5782ndash5788

87 Brar HS Wong J Manuel MV Investigation of the mechanical anddegradation properties of Mg-Sr and Mg-Zn-Sr alloys for use aspotential biodegradable implant materials J Mech Behav BiomedMater 2012 7 87ndash95

88 Bornapour M Muja N Shum-Tim D et al Biocompatibility andbiodegradability of Mg-Sr alloys the formation of Sr-substitutedhydroxyapatite Acta Biomater 2013 9 5319ndash5330

89 Gu XN Xie XH Li N et al In vitro and in vivo studies on aMg-Sr binary alloy system developed as a new kind of biodegrad-able metal Acta Biomater 2012 8 2360ndash2374

90 Haumlnzi AC Gerber I Schinhammer M et al On the in vitro andin vivo degradation performance and biological response of newbiodegradableMg-Y-Zn alloys Acta Biomater 2010 6 1824ndash1833

91 Chou DT Hong D Saha P et al In vitro and in vivo corrosioncytocompatibility and mechanical properties of biodegradableMg-Y-Ca-Zr alloys as implant materials Acta Biomater 2013 98518ndash8533

92 Zong Y Yuan G Zhang X et al Comparison of biodegradable be-haviors of AZ31 and Mg-Nd-Zn-Zr alloys in Hanks physiologicalsolution Mater Sci Eng-B 2012 177 395ndash401

93 Tie D Feyerabend FMuumlllerWD et al Antibacterial biodegradableMg-Ag alloys Eur Cell Mater 2013 25 284ndash298

94 VojtěchDKubaacutesek J Seraacutek J et al Mechanical and corrosion prop-

13 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

erties of newly developed biodegradable Zn-based alloys for bonefixation Acta Biomater 2011 7 3515ndash3522

95 Li H Yang H Zheng Y et al Design and characterizations of novelbiodegradable ternary Zn-based alloys with IIA nutrient alloyingelements Mg Ca and Sr Mater Des 2015 83 95ndash102

96 Liu X Sun J Yang Y et al Microstructure mechanical proper-ties in vitro degradation behavior and hemocompatibility of novelZn-Mg-Sr alloys as biodegradable metals Mater Lett 2016 162242ndash245

97 Wu C Qiu H Hu X et al Short-term safety and efficacy of thebiodegradable iron stent in mini-swine coronary arteries ChinMed J (Engl) 2013 126 4752ndash4757

98 Purnama A Hermawan H Champetier S et al Gene expressionprofile of mouse fibroblasts exposed to a biodegradable iron alloyfor stents Acta Biomater 2013 9 8746ndash8753

99 HermawanH Purnama A Dube D et al Fe-Mn alloys for metallicbiodegradable stents degradation and cell viability studies ActaBiomater 2010 6 1852ndash1860

100 Sheridan MH Shea LD Peters MC et al Bioabsorbable polymerscaffolds for tissue engineering capable of sustained growth factordelivery J Control Release 2000 64 91ndash102

101 Shawe S Buchanan F Harkin-Jones E et al A study on the rate ofdegradation of the bioabsorbable polymer polyglycolic acid (PGA)J Mater Sci 2006 41 4832ndash4838

102 Palmerini T Biondi-Zoccai G Della Riva D et al Clinical out-comes with bioabsorbable polymer- versus durable polymer-baseddrug-eluting and bare-metal stents J Am Coll Cardiol 2014 63299ndash307

103 Tanimoto S Serruys PW Thuesen L et al Comparison of in vivoacute stent recoil between the bioabsorbable everolimus-elutingcoronary stent and the everolimus-eluting cobalt chromium coro-nary stent insights from the ABSORB and SPIRIT trials CatheterCardiovasc Interv 2007 70 515ndash523

104 Tsuji H Sasaki H Sato H et al Neuron attachment properties ofcarbon negative-ion implanted bioabsorbable polymer of poly-lac-tic acid Nucl Instr Meth Phys Res Sect B-Beam Interact MaterAtoms 2002 191 815ndash819

105 Aikawa M Miyazawa M Okamoto K et al A novel treatment forbile duct injury with a tissue-engineered bioabsorbable polymerpatch Surgery 2010 147 575ndash580

106 WaksmanR Pakala R Kuchulakanti PK et al Safety and efficacy ofbioabsorbablemagnesium alloy stents in porcine coronary arteriesCatheter Cardiovasc Interv 2006 68 607ndash617

107 Di Mario C Griffiths H Goktekin O et al Drug-eluting bioab-sorbable magnesium stent J Interv Cardiol 2004 17 391ndash395

108 Erbel R Di Mario C Bartunek J et al Temporary scaffoldingof coronary arteries with bioabsorbable magnesium stents aprospective non-randomised multicentre trial Lancet 2007 3691869ndash1875

109 Schranz D Zartner P Michel-Behnke I et al Bioabsorbable metalstents for percutaneous treatment of critical recoarctation of theaorta in a newborn Catheter Cardiovasc Interv 2006 67 671ndash673

110 Gu X Zheng Y Cheng Y et al In vitro corrosion and biocompati-bility of binary magnesium alloys Biomaterials 2009 30 484ndash498

111 Hiromoto S InoueM Taguchi T et al In vitro and in vivo biocom-patibility and corrosion behaviour of a bioabsorbable magnesiumalloy coated with octacalcium phosphate and hydroxyapatite ActaBiomater 2015 11 520ndash530

112 Hiromoto S Tomozawa M Maruyama N Fatigue property of abioabsorbable magnesium alloy with a hydroxyapatite coatingformed by a chemical solution deposition J Mech Behav Biomed-ical Mater 2013 25 1ndash10

113 Bowen PK Drelich J Goldman J Zinc exhibits ideal physiologicalcorrosion behavior for bioabsorbable stents Adv Mater 2013 252577ndash2582

114 Liu X Sun J Yang Y et al In vitro investigation of ultra-pure Znand its mini-tube as potential bioabsorbable stent material MaterLett 2015 161 53ndash56

115 LinW Zhang G Cao P et al Cytotoxicity and its test methodologyfor a bioabsorbable nitrided iron stent J Biomed Mater Res 2015103 764ndash776

116 Coe JD Vaccaro AR Instrumented transforaminal lumbar inter-body fusion with bioresorbable polymer implants and iliac crestautograft Spine 2005 30 S76ndashS83

117 Ignatius AA Augat P Ohnmacht M et al A new bioresorbablepolymer for screw augmentation in the osteosynthesis of osteo-porotic cancellous bone a biomechanical evaluation J BiomedMater Res 2001 58 254ndash260

118 Krucoff MW Kereiakes DJ Petersen JL et al A novel biore-sorbable polymer paclitaxel-eluting stent for the treatment ofsingle and multivessel coronary disease J Am Coll Cardiol 200851 1543ndash1552

119 Kostopoulos L Karring T Guided bone regeneration in mandibu-lar defects in rats using a bioresorbable polymer Clin Oral Im-plants Res 1994 5 66ndash74

120 Dubok VA Bioceramicsmdashyesterday today tomorrow PowderMetall Metal Ceram 2000 39 381ndash394

121 Safronova T Kuznetsov A Korneychuk S et al Calcium phos-phate powders synthesized from solutions with [Ca2+][PO4

3minus]=1for bioresorbable ceramics Cent Eur J Chem 2009 7 184ndash191

122 Bohner M Bioresorbable ceramics In Buchanan FJ (Ed) Degra-dation Rate of Bioresorbable Materials Cambridge WoodheadPublishing 2008 95-114

123 Seitz JM Eifler R Stahl J et al Characterization ofMgNd2 alloy forpotential applications in bioresorbable implantable devices ActaBiomater 2012 8 3852ndash3864

124 WenCE Yamada Y Shimojima K et al Porous bioresorbable mag-nesium as bone substitute MSF 2003 419ndash422 1001ndash1006

125 Campos CM Muramatsu T Iqbal J et al Bioresorbable drug-elut-ing magnesium-alloy scaffold for treatment of coronary artery dis-ease Int J Mol Sci 2013 14 24492ndash24500

126 KirklandNT Birbilis NWalker J et al In-vitro dissolution ofmag-nesium-calcium binary alloys clarifying the unique role of calciumadditions in bioresorbable magnesium implant alloys J BiomedMater Res 2010 95B 91ndash100

127 Gastaldi D Sassi V Petrini L et al Continuum damage model forbioresorbable magnesium alloy devices mdashapplication to coronarystents J Mech Behav Biomed Mater 2011 4 352ndash365

128 Kitabata H Waksman R Warnack B Bioresorbable metal scaffoldfor cardiovascular application current knowledge and future per-spectives Cardiovasc Revasc Med 2014 15 109ndash116

Acknowledgments This work was supported by the National Key Re-search and Development Program of China (2016YFC1102402) NationalNatural Science Foundation of China (NSFC 51431002) and the NSFCand the Research Grants Council (RGC) of Hong Kong Joint ResearchScheme (51361165101 and 5161101031)

Author contributions Liu Y prepared the figures tables organized thereferences and wrote the paper Zheng Y provided the overall concept andrevised the manuscript Hayes B helped with the standard developmentand revised the manuscript All authors participated in the discussion

Conflict of interest The authors declare that they have no conflict ofinterest

14copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Yang Liu received his bachelor degree in materials science and engineering from Harbin engineering University in 2013Then he continued his study as a PhD candidate in Prof Yufeng Zhengrsquos Lab in Peking University His research interestsare mainly focused on the corrosion study of absorbable metallic biomaterials as well as the development of new kind ofMg-based biomaterials

Yufeng Zheng obtained his PhD degree from Harbin Institute of Technology in 1998 He is the National OutstandingYouth and Yangtze River scholar of China His research interests are focused on the development of novel biomaterials andapplication and design of biomedical devices

Byron Hayes an over 35 year employee of WL Gore has been involved in the commercial development of multiple ab-sorbable polymeric implants since the late 1980s Hayes started his standards development activities with ASTM in 2000where he is actively developing standards for polymeric and metallic absorbable implants In 2010 Hayes also becameinvolved with ISO Technical Committees TC150 and TC194 and is now convener of working groups focused on cardiovas-cular and metallic absorbable implants

可降解可吸收再吸收mdashmdash哪个是描述最终被人体吸收生物材料的最好词汇刘洋1 郑玉峰1 拜伦海耶斯2

摘要 关于最终被人体吸收的植入材料领域内文献采用的英文修饰词长期以来混乱且不同不仅造成文献检索困难同时模糊了研究人员的研究边界 此领域在法律法规标准中统一用词的确定为领域内的科学研究产品销售及产品使用说明奠定了基础 我们基于化学生态学材料学生物学微生物学和药学立足于使用习惯法律标准和市场对领域内使用已久的典型修饰词ldquo生物可降解rdquoldquo再吸收rdquo和ldquo可吸收rdquo进行了讨论和解释 总的来说尽管目前绝大多数修饰语实际想表达的意思相同作者认为ldquo可吸收rdquo这一英文修饰语是最恰当的修饰词 同时我们提议进一步规范和统一该领域修饰词的使用

15 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

  • Degradable absorbable or resorbablemdashwhat is the best grammatical modifier for an implant that is eventually absorbed by the body
  • Abstract
  • INTRODUCTION
    • Current situation
    • Standards development in advance
      • TERMINOLOGY
        • Overview of utilization of the terms ldquodegradationrdquoldquobiodegradationrdquo and ldquodegradablerdquoldquobiodegradablerdquo
        • Overview of utilization of the terms ldquoabsorptionrdquoldquobioabsorptionrdquo and ldquoabsorbablerdquoldquobioabsorbablerdquo
        • Overview of utilization of the terms ldquoresorptionrdquoldquobioresorptionrdquo and ldquoresorbablerdquoldquobioresorbablerdquo
        • Utilization and comparison of the terms ldquobiodegradable metalsrdquo and ldquoabsorbable metallic materialsrdquo
        • Summary quantification of the common Terms
          • DISCUSSION
            • Expertise inherent biases
            • Connotation and extension of noun forms ldquobiodegradation bioabsorption and bioresorptionrdquo and adjectives ldquobiodegradable bioabsorbable and bioresorbablerdquo
              • CONCLUDING REMARKS
              • References
              • Acknowledgements

Table 4 US-FDA absorbable implant related product codes descriptions and accompanying CFRsa)

Product code Device Device class Regulation number Regulation description

OMT Absorbable lung biopsy plug 2 [8784755] Absorbable lung biopsy plug

LMF Agent absorbable hemostatic collagen based 3 [8784490] Absorbable hemostatic agent and dressing

LMG Agent absorbable hemostatic non-collagen based 3 [8784490] Absorbable hemostatic agent and dressing

MRY Appliances and accessories fixation bone absorbable singlemultiple component 2 [8883040] Smooth or threaded metallic bone fixation fastener

PBQ Fixation non-absorbable or absorbable for pelvic use 2 [8844530] Obstetric-gynecologic specialized manual instrument

HQJ Implant absorbable (scleral buckling methods) 2 [8863300] Absorbable implant (scleral buckling method)

OWT Mesh surgical absorbable abdominal hernia 2 [8783300] Surgical mesh

OXM Mesh surgical absorbable fistula 2 [8783300] Surgical mesh

OXI Mesh surgical absorbable large abdominal wall defects 2 [8783300] Surgical mesh

OXL Mesh surgical absorbable organ support 2 [8783300] Surgical mesh

OWW Mesh surgical absorbable orthopaedics reinforcement of tendon 2 [8783300] Surgical mesh

OXF Mesh surgical absorbable plastic and reconstructive surgery 2 [8783300] Surgical mesh

OXC Mesh surgical absorbable staple line reinforcement 2 [8783300] Surgical mesh

OWZ Mesh surgical absorbable thoracic chest wall reconstruction 2 [8783300] Surgical mesh

OWU Mesh surgical non-absorbable diaphragmatic hernia 2 [8783300] Surgical mesh

OWR Mesh surgical non-absorbable facial implants for plastic surgery 2 [8783300] Surgical mesh

OXJ Mesh surgical non-absorbable large abdominal wall defects 2 [8783300] Surgical mesh

OWX Mesh surgical non-absorbable orthopaedics reinforcement of tendon 2 [8783300] Surgical mesh

OXG Mesh surgical non-absorbable plastic and reconstructive surgery 2 [8783300] Surgical mesh

OXD Mesh surgical non-absorbable staple line reinforcement 2 [8783300] Surgical mesh

OXA Mesh surgical non-absorbable thoracic chest wall reconstruction 2 [8783300] Surgical mesh

LBP Replacement ossicular (stapes) using absorbable gelatin material 2 [8743450] Partial ossicular replacement prosthesis

OLL Septal staplerabsorbable staples 2 [8784750] ImplanTABLE staple

MNU Staple absorbable 2 [8883030] Singlemultiple component metallic bone fixationappliances and accessories

GAK Suture absorbable 2 [8784830] Absorbable surgical gut suture

GAL Suture absorbable natural 2 [8784830] Absorbable surgical gut suture

HMO Suture absorbable ophthalmic 3

GAN Suture absorbable synthetic 2 [8784830] Absorbable surgical gut suture

GAM Suture absorbable synthetic polyglycolic acid 2 [8784493] Absorbable poly(glycolidel-lactide) surgical suture

NEW Suture surgical absorbable polydioxanone 2 [8784840] Absorbable polydioxanone surgical suture

a) Note the results obtained from online search for the device term ldquoabsorbablerdquo that was conducted on 6 Aug 2016 at httpwwwaccessdatafdagovscriptscdrhcfdocscfPCDclassifica-tioncfm

7 copy

ScienceChina

Pressand

Springer-VerlagBerlin

Heidelberg 2017

SCIENCECH

INAMaterials

REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

material or substance that either directly or through in-tended degradation can pass through or be metabolized orassimilated by cells andor tissuerdquo The standardrsquos nomen-clature appendix further elaborates on its preference forldquoabsorbablerdquo since the prefix ldquobio-rdquo is redundant in thecontext of implant applications [43]Clearly these two terms of ldquobiodegradable metalsrdquo and

ldquoabsorbable metallic materialsrdquo share the same connota-tion which defines the completemission of an intentionallydegradable material when implanted in vivo In the contextof biodegradable metalsabsorbable metallic materialsthe process includes the corrosion caused by body fluida host response caused by corrosion products followedby dissolutionabsorption and finally improved tissuehealing The ldquobiodegradationrdquo instead of ldquobiocorrosionrdquois used to distinguish this new kind of metals which canfully dissolve in vivo with no implant residues Besidesbiodegradation process the following dynamic process ofdissolutionabsorption also starts in vivo For exampledissolved Mg2+ is considered to enhance the integrin me-diated human-bone-derived cell adhesion and affect newbone formation [48] The metabolic reaction is also crucialand even more important for biodegradable metals as it ishelpful It is another distinction from traditional metalsused for biomedical application In fact the different usagehabit forming of ldquobiodegradablerdquo or ldquoabsorbablerdquoldquobioab-sorbablerdquo may be more related with the study field theresearchers in Taking the ldquoabsorbablerdquo metallic stent asan example (Fig 2) once the ldquoabsorbablerdquo metallic stentwas implanted into blood vessel ldquocorrosionrdquo of biometal

begins The corrosion products including debris hydro-gen (for Mg-based metals) metallic ions and hydroxylconvert the local environment and diffuse into the bloodvessel wall Some corrosion products can be biologicallybeneficial For instance the diffused and absorbed Zn2+

can potentially play a positive role in dealing with athero-sclerosis [49] Along with the corrosion process healingprocesses such as endothelialization may become en-hanced In summary and within the context of absorbablemetals the adjectives ldquodegradablerdquo and ldquoabsorbablerdquo referto the nature of the biodegradation products of the mate-rialdevice being metabolically absorbed an attribute ofthe host (animal or human body) regardless of whetherthe implant degrades corrodes hydrolyzes or dissolves[50ndash52]

Summary quantification of the common TermsFig 3a shows preliminary searching results in Webof Knowledge using ldquodegradablerdquo ldquoabsorbablerdquo or ldquore-sorbablerdquo along with ldquomaterialrdquo as key words Theutilization of ldquodegradablerdquo is a bit more frequently thanldquoabsorbablerdquo but that of ldquoresorbablerdquo steps down Mean-while the counterpart searching result when using ldquobiordquo asprefix to the adjectives along with ldquomaterialrdquo as keywordsare presented in Fig 3b ldquoBiodegradable materialrdquo is themost common utilization which holds 91 among the ex-pression approach This is also due to the fact that besidesthe common utilization in biomaterials ldquobiodegradablerdquois also used in a wide range of applications such as cleanenvironment and ecology [5354]

Figure 2 Different point of views on the biodegradationabsorption process

8copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Figure 3 Searching results in Web of Knowledge from all databases (a) with the total searched publication numbers by ldquodegradablerdquo+ ldquomaterialrdquoldquoabsorbablerdquo+ ldquomaterialrdquo and ldquoresorbablerdquo+ ldquomaterialrdquo as 100 (b) the total searched publication numbers by ldquobiodegradablerdquo+ ldquomaterialrdquo ldquobioab-sorbablerdquo+ ldquomaterialrdquo and ldquobioresorbablerdquo+ ldquomaterialrdquo as 100

DISCUSSION

Expertise inherent biasesAs previously mentioned biomaterial is an interdiscipli-nary field fascinating researchers with specialty from dif-ferent backgrounds Different backgrounds as well as dif-ferent research point of interests may be one of the reasonsfor using different terminologies Materials scientists tendto focus on the materialdevice itself leading to their usageof ldquobiodegradablerdquo to illustrate what happens to the deviceThey pay more attention to the process such as hydroly-sis corrosion debris degradation products and the changeof surface morphology resulting in the researching inter-ests of ldquomaterial biodegradationrdquo In contrast surgeons andbiomedical researchers tend to be concerned more on thehost response and healing process They are curious aboutthe absorption of various degradation products of the im-planted materialdevice and related metabolism mecha-nism and thereby prefer to use the term ldquoabsorbablerdquo toillustrate what happens to the device As known somema-terials may only undergo biodegradation but the corrosionproducts still have no influence on the metabolic activitiesFor example cellulose is considered as ldquodietary fiberrdquowhichcannot be digested and absorbed by human body but is be-nign for human body [55] Some coating tablets for drug ordrug delivery systems made from cellulose and its deriva-tives are quite frequently utilized or investigated [5657]The polymer and derivatives of cellulose can only be de-graded but not be absorbed by human body [58] For suchmaterials the adjective ldquoabsorbablerdquo or ldquobioabsorbablerdquo isnot appropriateOverall once the materialsdevices are implanted into

the human body the ldquobiocorrosionrdquobiodegradationrdquoprocess happens immediately no matter to what degreeat the same time the host will biologically response to the

corrosiondegradation products through the absorptionmetabolism and excretion processes So for the samestory the majority of materials scientists would report itby ldquobiodegradabledegradationrdquo way whereas the majorityof medical doctors would report it by ldquoabsorbableab-sorptionrdquo way In nature the two terms ldquobiodegradablemetalsrdquo and ldquoabsorbable metallic materialsrdquo share the sameconnotation and are mutually replaceable

Connotation and extension of noun forms ldquobiodegradationbioabsorption and bioresorptionrdquo and adjectivesldquobiodegradable bioabsorbable and bioresorbablerdquoThe three noun forms of the terms illustrate the processwhile their adjectival derivatives were used to describe thegroup of materials with such certain capabilities For thestudy on biomaterials polymer researchers use ldquodegrada-tionbiodegradationrdquo when there is proved chain scissionprocess Besides they differentiate ldquobiodegradationrdquo andldquodegradationrdquo by confirmed metabolic activities betweenthe materials and cells or tissues Regarding to the fouradjectives ldquobiodegradablerdquo ldquobioabsorbablerdquo and ldquobiore-sorbablerdquo the term ldquobiocorrodiblerdquo is only used in scientificpapers on iron based materials and some patents on mag-nesium based materials The common usage of termsldquobiodegradablerdquo ldquobioabsorbablerdquo and ldquobioresorbablerdquo withrespect to the biomaterial research area is shown in Table 5The results reveal a widespread usage of ldquobiodegradablerdquo inboth polymers and magnesium based metals Varies typesof materials were reported as biomaterials Besides thereare also reports of ldquobiodegradablerdquo polymers for ecologyand environmental protection which indicates a furtherusage scope of ldquobiodegradablerdquo not only for implants anddevices Besides ldquobioresorbablerdquo is also utilized in all theresearch fields of polymers ceramics andmetals Howeverno current work used ldquobioabsorbablerdquo as grammatical

9 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Table 5 Current reported usage of terms ldquobiodegradablerdquo ldquobioabsorbablerdquo and ldquobioresorbablerdquoTerminology Category Materials Applications

PLA-PEG-biotin PLGA Controlled cell engineering [5960]Porous PLGA Tissue engineering [61ndash63]

PLGA-PEG-PLGA Injective thermosensitive hydrogel [64]PLGA Nerve guidance [65]

Fibronectin (Fn)-coated PLLA P(LLA-CL) Enhanced growth of endothelial cells [6066]PEG tethered PPF [67]

PDMS Drug delivery [68]PGA Tissue engineering [69]

Undefined Coronary stent [70ndash72]PGA Joint resurfacing [73]

Polymers

PHA Ecology and environmental protection [74]CaO-P2O5 glass Bone regeneration [75]β-Whitlockite Bone regeneration [76]

Calcium phosphate hydraulic cement Bone regeneration [77]Calcium

phosphate glass ceramicsBone regeneration [78]

Ceramics

CaO-SiO2-B2O3 glass-ceramics Bone regeneration [79]Pure Mg Implant material [80]

Mg-Ca-based Bone regeneration [81ndash84]Mg-Zn-based Bone regeneration [338586]Mg-Sr-based Bone regeneration [87ndash89]Mg-RE-based Vascular stent [90ndash92]

Mg and its metals

Mg-Ag-based [93]Zn-Mg Zn-Ca Zn-Sr [9495]Zn and its metals Zn-Mg-Sr [96]

Fe [9798]

Biodegradable

Fe and its metals Fe-Mn [99]PLLA PLG PGA Molecule delivery [100]

PGA Suture [101]Undefined Drug-eluting stent [102103]

PLA Neuron attachment [104]Polymers

PLA and PCL reinforced with PGA fibers Bile duct patch [105]Mg-RE based Coronary stent [106ndash109]

Binary Mg alloys [110]Mg and its metalsMg-Al-based [111112]

Zn and its metals Pure Zinc [113114]Fe and its metals Nitrided iron [115]

PLDLA Transforaminal lumbar interbody fusion [116]Alkylene bis(dilactoyl)-methacrylate modified polymer Bone screw augmentation [117]

Undefined Coronary stent [118]PHB Mandibular defects regeneration [119]HA Bone regeneration [120]Ceramics Calcium phosphate [121122]

MgNd2 Stent material [123]Porous Mg Bone substitute [124]Mg-RE Coronary stent [125]Mg-Ca Orthopedic application [126]

Mg and its metals

Mg-based Finite element analysis [127]

Bioabsorbable

Fe and its metals Pure Fe [128]

10copy

ScienceChina

Pressand

Springer-VerlagBerlin

Heidelberg 2017

REVIEWSCIENCE

CHINA

Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

modifier to bioceramics In addition as previouslyillustrated the prefix ldquobiordquo of ldquobioabsorbablerdquo and ldquobiore-sorbablerdquo are abridged hereafter discussion will concen-trate on ldquobiocorrodiblerdquo ldquobiodegradablerdquo ldquoabsorbablerdquo andldquoresorbablerdquoSince absorbable technologies are increasingly utilized

in numerous new and broader implant applications it be-comes more important to not acquiesce in addressing his-torical problems and instead actively move forward towardutilizing standardized language that is both technically ac-curate and unified in itsmeaning Preferred language needsto accurately communicate the concept To achieve the uni-fying goal of harmonized terminology themedical and sci-entific communities need to not solely look at materialschemistry or even biomaterials alone but to instead lookat term selection both across and within the context of thebroader medical disciplinemdashthe location where the resultsof implant technology development actually reaches themarketplace where therapies are brought to those in needNomenclature solutions need to both understand and re-spond to the context of terms across adjacent technologieswhich means to address needs from the perspectives of thebiomaterial researcher the deviceproduct developer thesurgeonclinician user the regulator and last but not leastthe patientgeneral public who is the direct beneficiary ofthe developed technologyA better understanding of these terminologies is neces-

sary and beneficial to the field Therefore the definitionson ldquodegradablerdquo ldquoabsorbablerdquo ldquoresorbablerdquo and relatedterms proposed by different organizations in differentfields have been summarized and discussed with the con-notation and extension of each term being compared andthe criteria being proposed

CONCLUDING REMARKSHerein given both the searching problem on the Internetand ambiguity in meanings the usage of grammaticalmodifiers to describe biomaterials that is eventually ab-sorbed by human body has been enumerated based onusage habits laws standards and markets In summaryldquodegradablerdquoldquobiodegradablerdquo are the most frequently usedgrammatical modifier not only in metals but also poly-mers as such kind of biomaterials ldquoBiodegradationrdquo andldquobiodegradablerdquo define the change of the materialdevicewell in the research of biomaterials but they are alsoadopted in other fields such as ecology and environmentalprotection Meanwhile ldquoresorbablerdquoldquobioresorbablerdquo havelong been recognized in the biological research and theldquoresorptionrdquo itself has been widely accepted as a biological

reaction The utilization of ldquoresorbablerdquoldquobioresorbablerdquowas found to be not as frequent as the counterpartsldquodegradablerdquoldquobiodegradablerdquo and ldquoabsorbablerdquoldquobioab-sorbablerdquo Such usage is accurate for osteoclast driven boneresorption but is inappropriate for implants that do notcarry the potential to grow back into their original formOtherwise despite it is not the most frequently used termldquoabsorbablerdquoldquobioabsorbablerdquo concentrates more on thehost metabolism to the foreign biodegradation productsof the implanted materialdevice compared with ldquodegrad-ablerdquoldquobiodegradablerdquo ldquoAbsorbablerdquo is defined in the scopeof biomaterials by different organizations and their publi-cations and also adopted by ASTM to illustrate ldquoabsorbablepolymerrdquo It is the most historically established the mostbroadly applicable (includes dissolvable devices that donot degrade) the most specific to medical applicationsand is the formal legal descriptor for most implant devicesConsidering the usage history common utilization in lawand standards as well as the scientific meaning in essenceldquoabsorbablerdquo can be better among other grammaticalmodifiers for description of an implant that is eventuallyabsorbed by the body which is recommended by theauthors for a further internationally-unified usage

Received 28 February 2017 accepted 27 March 2017published online 26 April 2017

1 Mackenzie D The history of sutures Med Hist 1973 17 158ndash1682 Hench LL Bioceramics J Am Ceramic Soc 2005 81 1705ndash17283 Hench LL Bioceramics from concept to clinic J AmCeramic Soc

1991 74 1487ndash15104 Windhagen H Radtke K Weizbauer A et al Biodegradable

magnesium-based screw clinically equivalent to titanium screw inhallux valgus surgery short term results of the first prospectiverandomized controlled clinical pilot study BioMed Eng OnLine2013 12 62

5 Schildwaumlchter M Biotronik announces CE mark for magmaristhe first clinically-proven bioresorbable magnesium scaffoldhttpwwwmagmariscomennewsroomjune-15-2016

6 Shalaby SW Burg KJL Bioabsorbable polymers update degrada-tion mechanisms safety and application J App Biomater 1995 6219ndash221

7 Vert M Li SM Spenlehauer G et al Bioresorbability and biocom-patibility of aliphatic polyesters J Mater Sci-Mater Med 1992 3432ndash446

8 Vert M Degradable and bioresorbable polymers in surgery and inpharmacology beliefs and facts J Mater Sci-Mater Med 2009 20437ndash446

9 Benicewicz BC Hopper PK Review polymers for absorbablesurgical suturesmdashPart I J Bioactive Compatible Polym 1990 5453ndash472

10 Barrows HT Synthetic bioabsorbable polymers In Szycher M(Ed) High Performance Biomaterials A Complete Guide toMed-ical and Pharmceutical Applications Boca Raton CRC PRESS1991 243ndash257

11 Weiler A Hoffmann RFG Staumlhelin AC et al Biodegradable

11 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

implants in sports medicine the biological base Arthroscopy-JArthroscopic Related Surgery 2000 16 305ndash321

12 Ikada Y Tsuji H Biodegradable polyesters for medical and ecolog-ical applications Macromol Rapid Commun 2000 21 117ndash132

13 Ashammakhi N Peltoniemi H Waris E et al Developments incraniomaxillofacial surgery use of self-reinforced bioabsorbableosteofixation devices Plast Reconstr Surg 2001 108 167ndash180

14 Vert M Doi Y Hellwich KH et al Terminology for biorelatedpolymers and applications (IUPACRecommendations 2012) PureAppl Chem 2012 84 377ndash410

15 The United States Pharmacopeial Convention The Second Sup-plement to the Pharmacopeia of the United States of America 11thdecennial revision (USP XI-1939 Supplement) 1939

16 Truhlsen SM The recession operation histopathologic responseand suture reaction and absorption Trans Am Ophthalmol Soc1965 63 626ndash677

17 USP in US Law httpwwwusporgprintabout-usplegal-recog-nitionusp-us-law

18 USP develops and publishes standards for drug substances drugproducts excipients and dietary supplements in the United StatesPharmacopeia-National Formulary (USP-NF)

19 United States Public Law 94-295 197620 United States Pharmacopeia httpwwwusporg21 British Pharmacopeia httpswwwpharmacopoeiacom22 European Pharmacopoeia httponlinepheurorgENentryhtm23 Williams DF The Williams Dictionary of Biomaterials Liverpool

Liverpool University Press 199924 httpsenwikipediaorgwikiBiodegradation25 Jones RG Kahovec J Stepto R et al Compendium of Polymer

Terminology and Nomenclature IUPAC Recommendations 2008Cambridge RSC Publishing 2009

26 Higashi S Yamamuro T Nakamura T et al Polymer-hydroxyap-atite composites for biodegradable bone fillers Biomaterials 19867 183ndash187

27 de Groot K Bioceramics of Calcium Phosphate Boca Raton CRCPress 1983

28 Hollinger JO Battistone GC Biodegradable bone repair materialssynthetic polymers and ceramics ClinOrthopRelat Res 1986 207290ndash306

29 ASTMD653-14 Standard Terminology Relating to Soil Rock andContained Fluids ASTM International West Conshohocken PA2014 httpswwwastmorgStandardsD653htm

30 Witte F Hort N Vogt C et al Degradable biomaterials based onmagnesium corrosion Curr Opin Solid State Mater Sci 2008 1263ndash72

31 Lynn DM Langer R Degradable poly(β-amino esters) synthesischaracterization and self-assemblywith plasmidDNA JAmChemSoc 2000 122 10761ndash10768

32 Cima LG Vacanti JP Vacanti C et al Tissue engineering by celltransplantation using degradable polymer substrates J BiomechEng 1991 113 143ndash151

33 Zhang S Zhang X Zhao C et al Research on an Mg-Zn alloy as adegradable biomaterial Acta Biomater 2010 6 626ndash640

34 Anseth KS Metters AT Bryant SJ et al In situ forming degradablenetworks and their application in tissue engineering and drug de-livery J Control Release 2002 78 199ndash209

35 Forrest ML Koerber JT Pack DW A degradable polyethyleniminederivative with low toxicity for highly efficient gene delivery Bio-conjugate Chem 2003 14 934ndash940

36 ASTM E2747-11 Standard Specification for Evaluation and Selec-tion of Onsite Offices for Environmentally Sustainable MeetingsEvents Trade Shows and Conferences ASTM International

West Conshohocken PA 2011 httpswwwastmorgStan-dardsE2747htm

37 ASTM E2745-11 Standard Specification for Evaluation andSelection of Audio Visual (AV) and Production for Environ-mentally Sustainable Meetings Events Trade Shows and Con-ferences ASTM International West Conshohocken PA 2011httpswwwastmorgStandardsE2745htm

38 ASTM E2746-11 Standard Specification for Evaluation andSelection of Communication and Marketing Materials for En-vironmentally Sustainable Meetings Events Trade Shows andConferences ASTM International West Conshohocken PA 2011httpswwwastmorgStandardsE2746htm

39 ASTM E2741-11 Standard Specification for Evaluation and Se-lection of Destinations for Environmentally Sustainable MeetingsEvents Trade Shows and Conferences ASTM InternationalWest Conshohocken PA 2011 httpswwwastmorgStan-dardsE2741htm

40 0 ASTM E2773-11 Standard Specification for Evaluation andSelection of Food and Beverage for Environmentally SustainableMeetings Events Trade Shows and Conferences ASTM Interna-tional West Conshohocken PA 2011 httpswwwastmorgStan-dardsE2773htm

41 ASTM E2742-11 Standard Specification for Evaluation and Selec-tion of Exhibits for Environmentally Sustainable Meetings EventsTrade Shows and Conferences ASTM International West Con-shohocken PA 2011 httpswwwastmorgStandardsE2742htm

42 ASTM E2774-11 Standard Specification for Evaluation and Selec-tion of Venues for Environmentally Sustainable Meetings EventsTrade Shows and Conferences ASTM International West Con-shohocken PA 2011 httpswwwastmorgStandardsE2774htm

43 ASTM F2902-12 Standard Guide for Assessment of AbsorbablePolymeric Implants ASTM International West ConshohockenPA 2012 httpswwwastmorgStandardsF2902htm

44 httpsenwikipediaorgwikiResorption45 Venes D Tabers Cyclopedic Medical Dictionary 22th edition

Philadelphia F A Davis Company 201346 Zheng YF Gu XN Witte F Biodegradable metals Mater Sci Eng-

R-Rep 2014 77 1ndash3447 Hanawa T Metal ion release from metal implants Mater Sci

Eng-C 2004 24 745ndash75248 Zreiqat H Howlett CR Zannettino A et al Mechanisms of mag-

nesium-stimulated adhesion of osteoblastic cells to commonly usedorthopaedic implants J Biomed Mater Res 2002 62 175ndash184

49 Little PJ Bhattacharya R Moreyra AE et al Zinc and cardiovascu-lar disease Nutrition 2010 26 1050ndash1057

50 Seager H Drug-delivery products and the Zydis fast-dissolvingdosage form J Pharm Pharmacol 1998 50 375ndash382

51 Shikinami Y Shape-memory biodegradable and absorbable mate-rial US Patent No 6281262 2001-8-28

52 Huitema TW Knight GW Ransick MH Schulze DR Surgical im-plant with preferential corrosion zone US Patent No 79059022011-3-15

53 Luzier WD Materials derived from biomassbiodegradable mate-rials Proc Natl Acad Sci USA 1992 89 839ndash842

54 Gross RA Kalra B Biodegradable polymers for the environmentScience 2002 297 803ndash807

55 Trumbo P Schlicker S Yates AA et al Dietary reference intakesfor energy carbohydrate fiber fat fatty acids cholesterol proteinand amino acids J Am Diet Assoc 2002 102 1621ndash1630

56 Chambin O Champion D Debray C et al Effects of different cel-lulose derivatives on drug release mechanism studied at a prefor-mulation stage J Control Release 2004 95 101ndash108

12copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

57 Fundueanu G Constantin M Esposito E et al Cellulose acetatebutyrate microcapsules containing dextran ion-exchange resinsas self-propelled drug release system Biomaterials 2005 264337ndash4347

58 Maumlrtson M Viljanto J Hurme T et al Is cellulose sponge degrad-able or stable as implantation material An in vivo subcutaneousstudy in the rat Biomaterials 1999 20 1989ndash1995

59 Patel N Padera R Sanders GH et al Spatially controlled cell en-gineering on biodegradable polymer surfaces The FASEB journal1998 12 1447ndash1454

60 Goldstein A Effect of convection on osteoblastic cell growth andfunction in biodegradable polymer foam scaffolds Biomaterials2001 22 1279ndash1288

61 Wu L Ding J In vitro degradation of three-dimensional porouspoly(DL-lactide-co-glycolide) scaffolds for tissue engineeringBiomaterials 2004 25 5821ndash5830

62 Wu L Ding J Effects of porosity and pore size on in vitro degra-dation of three-dimensional porous poly(DL-lactide-co-glycolide)scaffolds for tissue engineering J Biomed Mater Res 2005 75A767ndash777

63 Pan Z Ding J Poly(lactide-co-glycolide) porous scaffolds for tissueengineering and regenerative medicine Interface Focus 2012 2366ndash377

64 Yu L Zhang Z Zhang H et al Biodegradability and biocompati-bility of thermoreversible hydrogels formed from mixing a sol anda precipitate of block copolymers in water Biomacromolecules2010 11 2169ndash2178

65 Wen X Tresco PA Fabrication and characterization of permeabledegradable poly(DL-lactide-co-glycolide) (PLGA) hollow fiberphase inversion membranes for use as nerve tract guidance chan-nels Biomaterials 2006 27 3800ndash3809

66 Chu CFL Lu A Liszkowski M et al Enhanced growth of animaland human endothelial cells on biodegradable polymers BBA-GenSubjects 1999 1472 479ndash485

67 Jo S Engel PS Mikos AG Synthesis of poly(ethylene glycol)-teth-ered poly(propylene fumarate) and its modification with GRGDpeptide Polymer 2000 41 7595ndash7604

68 Park JH Allen MG Prausnitz MR Biodegradable polymer mi-croneedles fabrication mechanics and transdermal drug deliveryJ Control Release 2005 104 51ndash66

69 Freed LE Vunjak-Novakovic G Biron RJ et al Biodegradablepolymer scaffolds for tissue engineering Nat Biotechnol 1994 12689ndash693

70 Windecker S Serruys PW Wandel S et al Biolimus-eluting stentwith biodegradable polymer versus sirolimus-eluting stent withdurable polymer for coronary revascularisation (LEADERS) arandomised non-inferiority trial Lancet 2008 372 1163ndash1173

71 Stefanini GG Kalesan B Serruys PW et al Long-term clinicaloutcomes of biodegradable polymer biolimus-eluting stents ver-sus durable polymer sirolimus-eluting stents in patients with coro-nary artery disease (LEADERS) 4 year follow-up of a randomisednon-inferiority trial Lancet 2011 378 1940ndash1948

72 Raungaard B Jensen LO Tilsted HH et al Zotarolimus-elutingdurable-polymer-coated stent versus a biolimus-eluting biodegrad-able-polymer-coated stent in unselected patients undergoing per-cutaneous coronary intervention (SORT OUT VI) a randomisednon-inferiority trial Lancet 2015 385 1527ndash1535

73 Freed LE Grande DA Lingbin Z et al Joint resurfacing using allo-graft chondrocytes and synthetic biodegradable polymer scaffoldsJ Biomed Mater Res 1994 28 891ndash899

74 Poirier Y Nawrath C Somerville C Production of polyhydrox-yalkanoates a family of biodegradable plastics and elastomers in

bacteria and plants Nat Biotechnol 1995 13 142ndash15075 Dias A Tsuru K Hayakawa S et al Crystallisation studies of

biodegradable CaO-P2O5 glass with MgO and TiO2 for boneregeneration applications Glass Technol 2004 45 78ndash79

76 Klein CPAT de Groot K Drissen AA et al Interaction ofbiodegradable β-whitlockite ceramics with bone tissue an in vivostudy Biomaterials 1985 6 189ndash192

77 Ikenaga M Hardouin P Lemaicirctre J et al Biomechanical charac-terization of a biodegradable calcium phosphate hydraulic cementa comparison with porous biphasic calcium phosphate ceramics JBiomed Mater Res 1998 40 139ndash144

78 Dias AG Lopes MA Santos JD et al In vivo performance ofbiodegradable calcium phosphate glass ceramics using the rabbitmodel histological and SEM observation J Biomater Appl 200620 253ndash266

79 Lee JH Lee CK Chang BS et al In vivo study of novel biodegrad-able and osteoconductive CaO-SiO2-B2O3 glass-ceramics JBiomed Mater Res 2006 77A 362ndash369

80 Song G Song S A possible biodegradable magnesium implant ma-terial Adv Eng Mater 2007 9 298ndash302

81 Kim WC Kim JG Lee JY et al Influence of Ca on the corrosionproperties of magnesium for biomaterials Mater Lett 2008 624146ndash4148

82 Li Z Gu X Lou S et al The development of binary Mg-Ca alloysfor use as biodegradablematerials within bone Biomaterials 200829 1329ndash1344

83 Wan Y Xiong G Luo H et al Preparation and characterization ofa new biomedical magnesium-calcium alloy Mater Des 2008 292034ndash2037

84 Seong JW Kim WJ Development of biodegradable Mg-Ca alloysheets with enhanced strength and corrosion properties throughthe refinement anduniformdispersion of theMg2Caphase by high-ratio differential speed rolling Acta Biomater 2015 11 531ndash542

85 Zhang S Li J Song Y et al In vitro degradation hemolysis andMC3T3-E1 cell adhesion of biodegradable Mg-Zn alloy Mater SciEng-C 2009 29 1907ndash1912

86 Li J Song Y Zhang S et al In vitro responses of human bone mar-row stromal cells to a fluoridated hydroxyapatite coated biodegrad-able Mg-Zn alloy Biomaterials 2010 31 5782ndash5788

87 Brar HS Wong J Manuel MV Investigation of the mechanical anddegradation properties of Mg-Sr and Mg-Zn-Sr alloys for use aspotential biodegradable implant materials J Mech Behav BiomedMater 2012 7 87ndash95

88 Bornapour M Muja N Shum-Tim D et al Biocompatibility andbiodegradability of Mg-Sr alloys the formation of Sr-substitutedhydroxyapatite Acta Biomater 2013 9 5319ndash5330

89 Gu XN Xie XH Li N et al In vitro and in vivo studies on aMg-Sr binary alloy system developed as a new kind of biodegrad-able metal Acta Biomater 2012 8 2360ndash2374

90 Haumlnzi AC Gerber I Schinhammer M et al On the in vitro andin vivo degradation performance and biological response of newbiodegradableMg-Y-Zn alloys Acta Biomater 2010 6 1824ndash1833

91 Chou DT Hong D Saha P et al In vitro and in vivo corrosioncytocompatibility and mechanical properties of biodegradableMg-Y-Ca-Zr alloys as implant materials Acta Biomater 2013 98518ndash8533

92 Zong Y Yuan G Zhang X et al Comparison of biodegradable be-haviors of AZ31 and Mg-Nd-Zn-Zr alloys in Hanks physiologicalsolution Mater Sci Eng-B 2012 177 395ndash401

93 Tie D Feyerabend FMuumlllerWD et al Antibacterial biodegradableMg-Ag alloys Eur Cell Mater 2013 25 284ndash298

94 VojtěchDKubaacutesek J Seraacutek J et al Mechanical and corrosion prop-

13 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

erties of newly developed biodegradable Zn-based alloys for bonefixation Acta Biomater 2011 7 3515ndash3522

95 Li H Yang H Zheng Y et al Design and characterizations of novelbiodegradable ternary Zn-based alloys with IIA nutrient alloyingelements Mg Ca and Sr Mater Des 2015 83 95ndash102

96 Liu X Sun J Yang Y et al Microstructure mechanical proper-ties in vitro degradation behavior and hemocompatibility of novelZn-Mg-Sr alloys as biodegradable metals Mater Lett 2016 162242ndash245

97 Wu C Qiu H Hu X et al Short-term safety and efficacy of thebiodegradable iron stent in mini-swine coronary arteries ChinMed J (Engl) 2013 126 4752ndash4757

98 Purnama A Hermawan H Champetier S et al Gene expressionprofile of mouse fibroblasts exposed to a biodegradable iron alloyfor stents Acta Biomater 2013 9 8746ndash8753

99 HermawanH Purnama A Dube D et al Fe-Mn alloys for metallicbiodegradable stents degradation and cell viability studies ActaBiomater 2010 6 1852ndash1860

100 Sheridan MH Shea LD Peters MC et al Bioabsorbable polymerscaffolds for tissue engineering capable of sustained growth factordelivery J Control Release 2000 64 91ndash102

101 Shawe S Buchanan F Harkin-Jones E et al A study on the rate ofdegradation of the bioabsorbable polymer polyglycolic acid (PGA)J Mater Sci 2006 41 4832ndash4838

102 Palmerini T Biondi-Zoccai G Della Riva D et al Clinical out-comes with bioabsorbable polymer- versus durable polymer-baseddrug-eluting and bare-metal stents J Am Coll Cardiol 2014 63299ndash307

103 Tanimoto S Serruys PW Thuesen L et al Comparison of in vivoacute stent recoil between the bioabsorbable everolimus-elutingcoronary stent and the everolimus-eluting cobalt chromium coro-nary stent insights from the ABSORB and SPIRIT trials CatheterCardiovasc Interv 2007 70 515ndash523

104 Tsuji H Sasaki H Sato H et al Neuron attachment properties ofcarbon negative-ion implanted bioabsorbable polymer of poly-lac-tic acid Nucl Instr Meth Phys Res Sect B-Beam Interact MaterAtoms 2002 191 815ndash819

105 Aikawa M Miyazawa M Okamoto K et al A novel treatment forbile duct injury with a tissue-engineered bioabsorbable polymerpatch Surgery 2010 147 575ndash580

106 WaksmanR Pakala R Kuchulakanti PK et al Safety and efficacy ofbioabsorbablemagnesium alloy stents in porcine coronary arteriesCatheter Cardiovasc Interv 2006 68 607ndash617

107 Di Mario C Griffiths H Goktekin O et al Drug-eluting bioab-sorbable magnesium stent J Interv Cardiol 2004 17 391ndash395

108 Erbel R Di Mario C Bartunek J et al Temporary scaffoldingof coronary arteries with bioabsorbable magnesium stents aprospective non-randomised multicentre trial Lancet 2007 3691869ndash1875

109 Schranz D Zartner P Michel-Behnke I et al Bioabsorbable metalstents for percutaneous treatment of critical recoarctation of theaorta in a newborn Catheter Cardiovasc Interv 2006 67 671ndash673

110 Gu X Zheng Y Cheng Y et al In vitro corrosion and biocompati-bility of binary magnesium alloys Biomaterials 2009 30 484ndash498

111 Hiromoto S InoueM Taguchi T et al In vitro and in vivo biocom-patibility and corrosion behaviour of a bioabsorbable magnesiumalloy coated with octacalcium phosphate and hydroxyapatite ActaBiomater 2015 11 520ndash530

112 Hiromoto S Tomozawa M Maruyama N Fatigue property of abioabsorbable magnesium alloy with a hydroxyapatite coatingformed by a chemical solution deposition J Mech Behav Biomed-ical Mater 2013 25 1ndash10

113 Bowen PK Drelich J Goldman J Zinc exhibits ideal physiologicalcorrosion behavior for bioabsorbable stents Adv Mater 2013 252577ndash2582

114 Liu X Sun J Yang Y et al In vitro investigation of ultra-pure Znand its mini-tube as potential bioabsorbable stent material MaterLett 2015 161 53ndash56

115 LinW Zhang G Cao P et al Cytotoxicity and its test methodologyfor a bioabsorbable nitrided iron stent J Biomed Mater Res 2015103 764ndash776

116 Coe JD Vaccaro AR Instrumented transforaminal lumbar inter-body fusion with bioresorbable polymer implants and iliac crestautograft Spine 2005 30 S76ndashS83

117 Ignatius AA Augat P Ohnmacht M et al A new bioresorbablepolymer for screw augmentation in the osteosynthesis of osteo-porotic cancellous bone a biomechanical evaluation J BiomedMater Res 2001 58 254ndash260

118 Krucoff MW Kereiakes DJ Petersen JL et al A novel biore-sorbable polymer paclitaxel-eluting stent for the treatment ofsingle and multivessel coronary disease J Am Coll Cardiol 200851 1543ndash1552

119 Kostopoulos L Karring T Guided bone regeneration in mandibu-lar defects in rats using a bioresorbable polymer Clin Oral Im-plants Res 1994 5 66ndash74

120 Dubok VA Bioceramicsmdashyesterday today tomorrow PowderMetall Metal Ceram 2000 39 381ndash394

121 Safronova T Kuznetsov A Korneychuk S et al Calcium phos-phate powders synthesized from solutions with [Ca2+][PO4

3minus]=1for bioresorbable ceramics Cent Eur J Chem 2009 7 184ndash191

122 Bohner M Bioresorbable ceramics In Buchanan FJ (Ed) Degra-dation Rate of Bioresorbable Materials Cambridge WoodheadPublishing 2008 95-114

123 Seitz JM Eifler R Stahl J et al Characterization ofMgNd2 alloy forpotential applications in bioresorbable implantable devices ActaBiomater 2012 8 3852ndash3864

124 WenCE Yamada Y Shimojima K et al Porous bioresorbable mag-nesium as bone substitute MSF 2003 419ndash422 1001ndash1006

125 Campos CM Muramatsu T Iqbal J et al Bioresorbable drug-elut-ing magnesium-alloy scaffold for treatment of coronary artery dis-ease Int J Mol Sci 2013 14 24492ndash24500

126 KirklandNT Birbilis NWalker J et al In-vitro dissolution ofmag-nesium-calcium binary alloys clarifying the unique role of calciumadditions in bioresorbable magnesium implant alloys J BiomedMater Res 2010 95B 91ndash100

127 Gastaldi D Sassi V Petrini L et al Continuum damage model forbioresorbable magnesium alloy devices mdashapplication to coronarystents J Mech Behav Biomed Mater 2011 4 352ndash365

128 Kitabata H Waksman R Warnack B Bioresorbable metal scaffoldfor cardiovascular application current knowledge and future per-spectives Cardiovasc Revasc Med 2014 15 109ndash116

Acknowledgments This work was supported by the National Key Re-search and Development Program of China (2016YFC1102402) NationalNatural Science Foundation of China (NSFC 51431002) and the NSFCand the Research Grants Council (RGC) of Hong Kong Joint ResearchScheme (51361165101 and 5161101031)

Author contributions Liu Y prepared the figures tables organized thereferences and wrote the paper Zheng Y provided the overall concept andrevised the manuscript Hayes B helped with the standard developmentand revised the manuscript All authors participated in the discussion

Conflict of interest The authors declare that they have no conflict ofinterest

14copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Yang Liu received his bachelor degree in materials science and engineering from Harbin engineering University in 2013Then he continued his study as a PhD candidate in Prof Yufeng Zhengrsquos Lab in Peking University His research interestsare mainly focused on the corrosion study of absorbable metallic biomaterials as well as the development of new kind ofMg-based biomaterials

Yufeng Zheng obtained his PhD degree from Harbin Institute of Technology in 1998 He is the National OutstandingYouth and Yangtze River scholar of China His research interests are focused on the development of novel biomaterials andapplication and design of biomedical devices

Byron Hayes an over 35 year employee of WL Gore has been involved in the commercial development of multiple ab-sorbable polymeric implants since the late 1980s Hayes started his standards development activities with ASTM in 2000where he is actively developing standards for polymeric and metallic absorbable implants In 2010 Hayes also becameinvolved with ISO Technical Committees TC150 and TC194 and is now convener of working groups focused on cardiovas-cular and metallic absorbable implants

可降解可吸收再吸收mdashmdash哪个是描述最终被人体吸收生物材料的最好词汇刘洋1 郑玉峰1 拜伦海耶斯2

摘要 关于最终被人体吸收的植入材料领域内文献采用的英文修饰词长期以来混乱且不同不仅造成文献检索困难同时模糊了研究人员的研究边界 此领域在法律法规标准中统一用词的确定为领域内的科学研究产品销售及产品使用说明奠定了基础 我们基于化学生态学材料学生物学微生物学和药学立足于使用习惯法律标准和市场对领域内使用已久的典型修饰词ldquo生物可降解rdquoldquo再吸收rdquo和ldquo可吸收rdquo进行了讨论和解释 总的来说尽管目前绝大多数修饰语实际想表达的意思相同作者认为ldquo可吸收rdquo这一英文修饰语是最恰当的修饰词 同时我们提议进一步规范和统一该领域修饰词的使用

15 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

  • Degradable absorbable or resorbablemdashwhat is the best grammatical modifier for an implant that is eventually absorbed by the body
  • Abstract
  • INTRODUCTION
    • Current situation
    • Standards development in advance
      • TERMINOLOGY
        • Overview of utilization of the terms ldquodegradationrdquoldquobiodegradationrdquo and ldquodegradablerdquoldquobiodegradablerdquo
        • Overview of utilization of the terms ldquoabsorptionrdquoldquobioabsorptionrdquo and ldquoabsorbablerdquoldquobioabsorbablerdquo
        • Overview of utilization of the terms ldquoresorptionrdquoldquobioresorptionrdquo and ldquoresorbablerdquoldquobioresorbablerdquo
        • Utilization and comparison of the terms ldquobiodegradable metalsrdquo and ldquoabsorbable metallic materialsrdquo
        • Summary quantification of the common Terms
          • DISCUSSION
            • Expertise inherent biases
            • Connotation and extension of noun forms ldquobiodegradation bioabsorption and bioresorptionrdquo and adjectives ldquobiodegradable bioabsorbable and bioresorbablerdquo
              • CONCLUDING REMARKS
              • References
              • Acknowledgements

material or substance that either directly or through in-tended degradation can pass through or be metabolized orassimilated by cells andor tissuerdquo The standardrsquos nomen-clature appendix further elaborates on its preference forldquoabsorbablerdquo since the prefix ldquobio-rdquo is redundant in thecontext of implant applications [43]Clearly these two terms of ldquobiodegradable metalsrdquo and

ldquoabsorbable metallic materialsrdquo share the same connota-tion which defines the completemission of an intentionallydegradable material when implanted in vivo In the contextof biodegradable metalsabsorbable metallic materialsthe process includes the corrosion caused by body fluida host response caused by corrosion products followedby dissolutionabsorption and finally improved tissuehealing The ldquobiodegradationrdquo instead of ldquobiocorrosionrdquois used to distinguish this new kind of metals which canfully dissolve in vivo with no implant residues Besidesbiodegradation process the following dynamic process ofdissolutionabsorption also starts in vivo For exampledissolved Mg2+ is considered to enhance the integrin me-diated human-bone-derived cell adhesion and affect newbone formation [48] The metabolic reaction is also crucialand even more important for biodegradable metals as it ishelpful It is another distinction from traditional metalsused for biomedical application In fact the different usagehabit forming of ldquobiodegradablerdquo or ldquoabsorbablerdquoldquobioab-sorbablerdquo may be more related with the study field theresearchers in Taking the ldquoabsorbablerdquo metallic stent asan example (Fig 2) once the ldquoabsorbablerdquo metallic stentwas implanted into blood vessel ldquocorrosionrdquo of biometal

begins The corrosion products including debris hydro-gen (for Mg-based metals) metallic ions and hydroxylconvert the local environment and diffuse into the bloodvessel wall Some corrosion products can be biologicallybeneficial For instance the diffused and absorbed Zn2+

can potentially play a positive role in dealing with athero-sclerosis [49] Along with the corrosion process healingprocesses such as endothelialization may become en-hanced In summary and within the context of absorbablemetals the adjectives ldquodegradablerdquo and ldquoabsorbablerdquo referto the nature of the biodegradation products of the mate-rialdevice being metabolically absorbed an attribute ofthe host (animal or human body) regardless of whetherthe implant degrades corrodes hydrolyzes or dissolves[50ndash52]

Summary quantification of the common TermsFig 3a shows preliminary searching results in Webof Knowledge using ldquodegradablerdquo ldquoabsorbablerdquo or ldquore-sorbablerdquo along with ldquomaterialrdquo as key words Theutilization of ldquodegradablerdquo is a bit more frequently thanldquoabsorbablerdquo but that of ldquoresorbablerdquo steps down Mean-while the counterpart searching result when using ldquobiordquo asprefix to the adjectives along with ldquomaterialrdquo as keywordsare presented in Fig 3b ldquoBiodegradable materialrdquo is themost common utilization which holds 91 among the ex-pression approach This is also due to the fact that besidesthe common utilization in biomaterials ldquobiodegradablerdquois also used in a wide range of applications such as cleanenvironment and ecology [5354]

Figure 2 Different point of views on the biodegradationabsorption process

8copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Figure 3 Searching results in Web of Knowledge from all databases (a) with the total searched publication numbers by ldquodegradablerdquo+ ldquomaterialrdquoldquoabsorbablerdquo+ ldquomaterialrdquo and ldquoresorbablerdquo+ ldquomaterialrdquo as 100 (b) the total searched publication numbers by ldquobiodegradablerdquo+ ldquomaterialrdquo ldquobioab-sorbablerdquo+ ldquomaterialrdquo and ldquobioresorbablerdquo+ ldquomaterialrdquo as 100

DISCUSSION

Expertise inherent biasesAs previously mentioned biomaterial is an interdiscipli-nary field fascinating researchers with specialty from dif-ferent backgrounds Different backgrounds as well as dif-ferent research point of interests may be one of the reasonsfor using different terminologies Materials scientists tendto focus on the materialdevice itself leading to their usageof ldquobiodegradablerdquo to illustrate what happens to the deviceThey pay more attention to the process such as hydroly-sis corrosion debris degradation products and the changeof surface morphology resulting in the researching inter-ests of ldquomaterial biodegradationrdquo In contrast surgeons andbiomedical researchers tend to be concerned more on thehost response and healing process They are curious aboutthe absorption of various degradation products of the im-planted materialdevice and related metabolism mecha-nism and thereby prefer to use the term ldquoabsorbablerdquo toillustrate what happens to the device As known somema-terials may only undergo biodegradation but the corrosionproducts still have no influence on the metabolic activitiesFor example cellulose is considered as ldquodietary fiberrdquowhichcannot be digested and absorbed by human body but is be-nign for human body [55] Some coating tablets for drug ordrug delivery systems made from cellulose and its deriva-tives are quite frequently utilized or investigated [5657]The polymer and derivatives of cellulose can only be de-graded but not be absorbed by human body [58] For suchmaterials the adjective ldquoabsorbablerdquo or ldquobioabsorbablerdquo isnot appropriateOverall once the materialsdevices are implanted into

the human body the ldquobiocorrosionrdquobiodegradationrdquoprocess happens immediately no matter to what degreeat the same time the host will biologically response to the

corrosiondegradation products through the absorptionmetabolism and excretion processes So for the samestory the majority of materials scientists would report itby ldquobiodegradabledegradationrdquo way whereas the majorityof medical doctors would report it by ldquoabsorbableab-sorptionrdquo way In nature the two terms ldquobiodegradablemetalsrdquo and ldquoabsorbable metallic materialsrdquo share the sameconnotation and are mutually replaceable

Connotation and extension of noun forms ldquobiodegradationbioabsorption and bioresorptionrdquo and adjectivesldquobiodegradable bioabsorbable and bioresorbablerdquoThe three noun forms of the terms illustrate the processwhile their adjectival derivatives were used to describe thegroup of materials with such certain capabilities For thestudy on biomaterials polymer researchers use ldquodegrada-tionbiodegradationrdquo when there is proved chain scissionprocess Besides they differentiate ldquobiodegradationrdquo andldquodegradationrdquo by confirmed metabolic activities betweenthe materials and cells or tissues Regarding to the fouradjectives ldquobiodegradablerdquo ldquobioabsorbablerdquo and ldquobiore-sorbablerdquo the term ldquobiocorrodiblerdquo is only used in scientificpapers on iron based materials and some patents on mag-nesium based materials The common usage of termsldquobiodegradablerdquo ldquobioabsorbablerdquo and ldquobioresorbablerdquo withrespect to the biomaterial research area is shown in Table 5The results reveal a widespread usage of ldquobiodegradablerdquo inboth polymers and magnesium based metals Varies typesof materials were reported as biomaterials Besides thereare also reports of ldquobiodegradablerdquo polymers for ecologyand environmental protection which indicates a furtherusage scope of ldquobiodegradablerdquo not only for implants anddevices Besides ldquobioresorbablerdquo is also utilized in all theresearch fields of polymers ceramics andmetals Howeverno current work used ldquobioabsorbablerdquo as grammatical

9 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Table 5 Current reported usage of terms ldquobiodegradablerdquo ldquobioabsorbablerdquo and ldquobioresorbablerdquoTerminology Category Materials Applications

PLA-PEG-biotin PLGA Controlled cell engineering [5960]Porous PLGA Tissue engineering [61ndash63]

PLGA-PEG-PLGA Injective thermosensitive hydrogel [64]PLGA Nerve guidance [65]

Fibronectin (Fn)-coated PLLA P(LLA-CL) Enhanced growth of endothelial cells [6066]PEG tethered PPF [67]

PDMS Drug delivery [68]PGA Tissue engineering [69]

Undefined Coronary stent [70ndash72]PGA Joint resurfacing [73]

Polymers

PHA Ecology and environmental protection [74]CaO-P2O5 glass Bone regeneration [75]β-Whitlockite Bone regeneration [76]

Calcium phosphate hydraulic cement Bone regeneration [77]Calcium

phosphate glass ceramicsBone regeneration [78]

Ceramics

CaO-SiO2-B2O3 glass-ceramics Bone regeneration [79]Pure Mg Implant material [80]

Mg-Ca-based Bone regeneration [81ndash84]Mg-Zn-based Bone regeneration [338586]Mg-Sr-based Bone regeneration [87ndash89]Mg-RE-based Vascular stent [90ndash92]

Mg and its metals

Mg-Ag-based [93]Zn-Mg Zn-Ca Zn-Sr [9495]Zn and its metals Zn-Mg-Sr [96]

Fe [9798]

Biodegradable

Fe and its metals Fe-Mn [99]PLLA PLG PGA Molecule delivery [100]

PGA Suture [101]Undefined Drug-eluting stent [102103]

PLA Neuron attachment [104]Polymers

PLA and PCL reinforced with PGA fibers Bile duct patch [105]Mg-RE based Coronary stent [106ndash109]

Binary Mg alloys [110]Mg and its metalsMg-Al-based [111112]

Zn and its metals Pure Zinc [113114]Fe and its metals Nitrided iron [115]

PLDLA Transforaminal lumbar interbody fusion [116]Alkylene bis(dilactoyl)-methacrylate modified polymer Bone screw augmentation [117]

Undefined Coronary stent [118]PHB Mandibular defects regeneration [119]HA Bone regeneration [120]Ceramics Calcium phosphate [121122]

MgNd2 Stent material [123]Porous Mg Bone substitute [124]Mg-RE Coronary stent [125]Mg-Ca Orthopedic application [126]

Mg and its metals

Mg-based Finite element analysis [127]

Bioabsorbable

Fe and its metals Pure Fe [128]

10copy

ScienceChina

Pressand

Springer-VerlagBerlin

Heidelberg 2017

REVIEWSCIENCE

CHINA

Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

modifier to bioceramics In addition as previouslyillustrated the prefix ldquobiordquo of ldquobioabsorbablerdquo and ldquobiore-sorbablerdquo are abridged hereafter discussion will concen-trate on ldquobiocorrodiblerdquo ldquobiodegradablerdquo ldquoabsorbablerdquo andldquoresorbablerdquoSince absorbable technologies are increasingly utilized

in numerous new and broader implant applications it be-comes more important to not acquiesce in addressing his-torical problems and instead actively move forward towardutilizing standardized language that is both technically ac-curate and unified in itsmeaning Preferred language needsto accurately communicate the concept To achieve the uni-fying goal of harmonized terminology themedical and sci-entific communities need to not solely look at materialschemistry or even biomaterials alone but to instead lookat term selection both across and within the context of thebroader medical disciplinemdashthe location where the resultsof implant technology development actually reaches themarketplace where therapies are brought to those in needNomenclature solutions need to both understand and re-spond to the context of terms across adjacent technologieswhich means to address needs from the perspectives of thebiomaterial researcher the deviceproduct developer thesurgeonclinician user the regulator and last but not leastthe patientgeneral public who is the direct beneficiary ofthe developed technologyA better understanding of these terminologies is neces-

sary and beneficial to the field Therefore the definitionson ldquodegradablerdquo ldquoabsorbablerdquo ldquoresorbablerdquo and relatedterms proposed by different organizations in differentfields have been summarized and discussed with the con-notation and extension of each term being compared andthe criteria being proposed

CONCLUDING REMARKSHerein given both the searching problem on the Internetand ambiguity in meanings the usage of grammaticalmodifiers to describe biomaterials that is eventually ab-sorbed by human body has been enumerated based onusage habits laws standards and markets In summaryldquodegradablerdquoldquobiodegradablerdquo are the most frequently usedgrammatical modifier not only in metals but also poly-mers as such kind of biomaterials ldquoBiodegradationrdquo andldquobiodegradablerdquo define the change of the materialdevicewell in the research of biomaterials but they are alsoadopted in other fields such as ecology and environmentalprotection Meanwhile ldquoresorbablerdquoldquobioresorbablerdquo havelong been recognized in the biological research and theldquoresorptionrdquo itself has been widely accepted as a biological

reaction The utilization of ldquoresorbablerdquoldquobioresorbablerdquowas found to be not as frequent as the counterpartsldquodegradablerdquoldquobiodegradablerdquo and ldquoabsorbablerdquoldquobioab-sorbablerdquo Such usage is accurate for osteoclast driven boneresorption but is inappropriate for implants that do notcarry the potential to grow back into their original formOtherwise despite it is not the most frequently used termldquoabsorbablerdquoldquobioabsorbablerdquo concentrates more on thehost metabolism to the foreign biodegradation productsof the implanted materialdevice compared with ldquodegrad-ablerdquoldquobiodegradablerdquo ldquoAbsorbablerdquo is defined in the scopeof biomaterials by different organizations and their publi-cations and also adopted by ASTM to illustrate ldquoabsorbablepolymerrdquo It is the most historically established the mostbroadly applicable (includes dissolvable devices that donot degrade) the most specific to medical applicationsand is the formal legal descriptor for most implant devicesConsidering the usage history common utilization in lawand standards as well as the scientific meaning in essenceldquoabsorbablerdquo can be better among other grammaticalmodifiers for description of an implant that is eventuallyabsorbed by the body which is recommended by theauthors for a further internationally-unified usage

Received 28 February 2017 accepted 27 March 2017published online 26 April 2017

1 Mackenzie D The history of sutures Med Hist 1973 17 158ndash1682 Hench LL Bioceramics J Am Ceramic Soc 2005 81 1705ndash17283 Hench LL Bioceramics from concept to clinic J AmCeramic Soc

1991 74 1487ndash15104 Windhagen H Radtke K Weizbauer A et al Biodegradable

magnesium-based screw clinically equivalent to titanium screw inhallux valgus surgery short term results of the first prospectiverandomized controlled clinical pilot study BioMed Eng OnLine2013 12 62

5 Schildwaumlchter M Biotronik announces CE mark for magmaristhe first clinically-proven bioresorbable magnesium scaffoldhttpwwwmagmariscomennewsroomjune-15-2016

6 Shalaby SW Burg KJL Bioabsorbable polymers update degrada-tion mechanisms safety and application J App Biomater 1995 6219ndash221

7 Vert M Li SM Spenlehauer G et al Bioresorbability and biocom-patibility of aliphatic polyesters J Mater Sci-Mater Med 1992 3432ndash446

8 Vert M Degradable and bioresorbable polymers in surgery and inpharmacology beliefs and facts J Mater Sci-Mater Med 2009 20437ndash446

9 Benicewicz BC Hopper PK Review polymers for absorbablesurgical suturesmdashPart I J Bioactive Compatible Polym 1990 5453ndash472

10 Barrows HT Synthetic bioabsorbable polymers In Szycher M(Ed) High Performance Biomaterials A Complete Guide toMed-ical and Pharmceutical Applications Boca Raton CRC PRESS1991 243ndash257

11 Weiler A Hoffmann RFG Staumlhelin AC et al Biodegradable

11 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

implants in sports medicine the biological base Arthroscopy-JArthroscopic Related Surgery 2000 16 305ndash321

12 Ikada Y Tsuji H Biodegradable polyesters for medical and ecolog-ical applications Macromol Rapid Commun 2000 21 117ndash132

13 Ashammakhi N Peltoniemi H Waris E et al Developments incraniomaxillofacial surgery use of self-reinforced bioabsorbableosteofixation devices Plast Reconstr Surg 2001 108 167ndash180

14 Vert M Doi Y Hellwich KH et al Terminology for biorelatedpolymers and applications (IUPACRecommendations 2012) PureAppl Chem 2012 84 377ndash410

15 The United States Pharmacopeial Convention The Second Sup-plement to the Pharmacopeia of the United States of America 11thdecennial revision (USP XI-1939 Supplement) 1939

16 Truhlsen SM The recession operation histopathologic responseand suture reaction and absorption Trans Am Ophthalmol Soc1965 63 626ndash677

17 USP in US Law httpwwwusporgprintabout-usplegal-recog-nitionusp-us-law

18 USP develops and publishes standards for drug substances drugproducts excipients and dietary supplements in the United StatesPharmacopeia-National Formulary (USP-NF)

19 United States Public Law 94-295 197620 United States Pharmacopeia httpwwwusporg21 British Pharmacopeia httpswwwpharmacopoeiacom22 European Pharmacopoeia httponlinepheurorgENentryhtm23 Williams DF The Williams Dictionary of Biomaterials Liverpool

Liverpool University Press 199924 httpsenwikipediaorgwikiBiodegradation25 Jones RG Kahovec J Stepto R et al Compendium of Polymer

Terminology and Nomenclature IUPAC Recommendations 2008Cambridge RSC Publishing 2009

26 Higashi S Yamamuro T Nakamura T et al Polymer-hydroxyap-atite composites for biodegradable bone fillers Biomaterials 19867 183ndash187

27 de Groot K Bioceramics of Calcium Phosphate Boca Raton CRCPress 1983

28 Hollinger JO Battistone GC Biodegradable bone repair materialssynthetic polymers and ceramics ClinOrthopRelat Res 1986 207290ndash306

29 ASTMD653-14 Standard Terminology Relating to Soil Rock andContained Fluids ASTM International West Conshohocken PA2014 httpswwwastmorgStandardsD653htm

30 Witte F Hort N Vogt C et al Degradable biomaterials based onmagnesium corrosion Curr Opin Solid State Mater Sci 2008 1263ndash72

31 Lynn DM Langer R Degradable poly(β-amino esters) synthesischaracterization and self-assemblywith plasmidDNA JAmChemSoc 2000 122 10761ndash10768

32 Cima LG Vacanti JP Vacanti C et al Tissue engineering by celltransplantation using degradable polymer substrates J BiomechEng 1991 113 143ndash151

33 Zhang S Zhang X Zhao C et al Research on an Mg-Zn alloy as adegradable biomaterial Acta Biomater 2010 6 626ndash640

34 Anseth KS Metters AT Bryant SJ et al In situ forming degradablenetworks and their application in tissue engineering and drug de-livery J Control Release 2002 78 199ndash209

35 Forrest ML Koerber JT Pack DW A degradable polyethyleniminederivative with low toxicity for highly efficient gene delivery Bio-conjugate Chem 2003 14 934ndash940

36 ASTM E2747-11 Standard Specification for Evaluation and Selec-tion of Onsite Offices for Environmentally Sustainable MeetingsEvents Trade Shows and Conferences ASTM International

West Conshohocken PA 2011 httpswwwastmorgStan-dardsE2747htm

37 ASTM E2745-11 Standard Specification for Evaluation andSelection of Audio Visual (AV) and Production for Environ-mentally Sustainable Meetings Events Trade Shows and Con-ferences ASTM International West Conshohocken PA 2011httpswwwastmorgStandardsE2745htm

38 ASTM E2746-11 Standard Specification for Evaluation andSelection of Communication and Marketing Materials for En-vironmentally Sustainable Meetings Events Trade Shows andConferences ASTM International West Conshohocken PA 2011httpswwwastmorgStandardsE2746htm

39 ASTM E2741-11 Standard Specification for Evaluation and Se-lection of Destinations for Environmentally Sustainable MeetingsEvents Trade Shows and Conferences ASTM InternationalWest Conshohocken PA 2011 httpswwwastmorgStan-dardsE2741htm

40 0 ASTM E2773-11 Standard Specification for Evaluation andSelection of Food and Beverage for Environmentally SustainableMeetings Events Trade Shows and Conferences ASTM Interna-tional West Conshohocken PA 2011 httpswwwastmorgStan-dardsE2773htm

41 ASTM E2742-11 Standard Specification for Evaluation and Selec-tion of Exhibits for Environmentally Sustainable Meetings EventsTrade Shows and Conferences ASTM International West Con-shohocken PA 2011 httpswwwastmorgStandardsE2742htm

42 ASTM E2774-11 Standard Specification for Evaluation and Selec-tion of Venues for Environmentally Sustainable Meetings EventsTrade Shows and Conferences ASTM International West Con-shohocken PA 2011 httpswwwastmorgStandardsE2774htm

43 ASTM F2902-12 Standard Guide for Assessment of AbsorbablePolymeric Implants ASTM International West ConshohockenPA 2012 httpswwwastmorgStandardsF2902htm

44 httpsenwikipediaorgwikiResorption45 Venes D Tabers Cyclopedic Medical Dictionary 22th edition

Philadelphia F A Davis Company 201346 Zheng YF Gu XN Witte F Biodegradable metals Mater Sci Eng-

R-Rep 2014 77 1ndash3447 Hanawa T Metal ion release from metal implants Mater Sci

Eng-C 2004 24 745ndash75248 Zreiqat H Howlett CR Zannettino A et al Mechanisms of mag-

nesium-stimulated adhesion of osteoblastic cells to commonly usedorthopaedic implants J Biomed Mater Res 2002 62 175ndash184

49 Little PJ Bhattacharya R Moreyra AE et al Zinc and cardiovascu-lar disease Nutrition 2010 26 1050ndash1057

50 Seager H Drug-delivery products and the Zydis fast-dissolvingdosage form J Pharm Pharmacol 1998 50 375ndash382

51 Shikinami Y Shape-memory biodegradable and absorbable mate-rial US Patent No 6281262 2001-8-28

52 Huitema TW Knight GW Ransick MH Schulze DR Surgical im-plant with preferential corrosion zone US Patent No 79059022011-3-15

53 Luzier WD Materials derived from biomassbiodegradable mate-rials Proc Natl Acad Sci USA 1992 89 839ndash842

54 Gross RA Kalra B Biodegradable polymers for the environmentScience 2002 297 803ndash807

55 Trumbo P Schlicker S Yates AA et al Dietary reference intakesfor energy carbohydrate fiber fat fatty acids cholesterol proteinand amino acids J Am Diet Assoc 2002 102 1621ndash1630

56 Chambin O Champion D Debray C et al Effects of different cel-lulose derivatives on drug release mechanism studied at a prefor-mulation stage J Control Release 2004 95 101ndash108

12copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

57 Fundueanu G Constantin M Esposito E et al Cellulose acetatebutyrate microcapsules containing dextran ion-exchange resinsas self-propelled drug release system Biomaterials 2005 264337ndash4347

58 Maumlrtson M Viljanto J Hurme T et al Is cellulose sponge degrad-able or stable as implantation material An in vivo subcutaneousstudy in the rat Biomaterials 1999 20 1989ndash1995

59 Patel N Padera R Sanders GH et al Spatially controlled cell en-gineering on biodegradable polymer surfaces The FASEB journal1998 12 1447ndash1454

60 Goldstein A Effect of convection on osteoblastic cell growth andfunction in biodegradable polymer foam scaffolds Biomaterials2001 22 1279ndash1288

61 Wu L Ding J In vitro degradation of three-dimensional porouspoly(DL-lactide-co-glycolide) scaffolds for tissue engineeringBiomaterials 2004 25 5821ndash5830

62 Wu L Ding J Effects of porosity and pore size on in vitro degra-dation of three-dimensional porous poly(DL-lactide-co-glycolide)scaffolds for tissue engineering J Biomed Mater Res 2005 75A767ndash777

63 Pan Z Ding J Poly(lactide-co-glycolide) porous scaffolds for tissueengineering and regenerative medicine Interface Focus 2012 2366ndash377

64 Yu L Zhang Z Zhang H et al Biodegradability and biocompati-bility of thermoreversible hydrogels formed from mixing a sol anda precipitate of block copolymers in water Biomacromolecules2010 11 2169ndash2178

65 Wen X Tresco PA Fabrication and characterization of permeabledegradable poly(DL-lactide-co-glycolide) (PLGA) hollow fiberphase inversion membranes for use as nerve tract guidance chan-nels Biomaterials 2006 27 3800ndash3809

66 Chu CFL Lu A Liszkowski M et al Enhanced growth of animaland human endothelial cells on biodegradable polymers BBA-GenSubjects 1999 1472 479ndash485

67 Jo S Engel PS Mikos AG Synthesis of poly(ethylene glycol)-teth-ered poly(propylene fumarate) and its modification with GRGDpeptide Polymer 2000 41 7595ndash7604

68 Park JH Allen MG Prausnitz MR Biodegradable polymer mi-croneedles fabrication mechanics and transdermal drug deliveryJ Control Release 2005 104 51ndash66

69 Freed LE Vunjak-Novakovic G Biron RJ et al Biodegradablepolymer scaffolds for tissue engineering Nat Biotechnol 1994 12689ndash693

70 Windecker S Serruys PW Wandel S et al Biolimus-eluting stentwith biodegradable polymer versus sirolimus-eluting stent withdurable polymer for coronary revascularisation (LEADERS) arandomised non-inferiority trial Lancet 2008 372 1163ndash1173

71 Stefanini GG Kalesan B Serruys PW et al Long-term clinicaloutcomes of biodegradable polymer biolimus-eluting stents ver-sus durable polymer sirolimus-eluting stents in patients with coro-nary artery disease (LEADERS) 4 year follow-up of a randomisednon-inferiority trial Lancet 2011 378 1940ndash1948

72 Raungaard B Jensen LO Tilsted HH et al Zotarolimus-elutingdurable-polymer-coated stent versus a biolimus-eluting biodegrad-able-polymer-coated stent in unselected patients undergoing per-cutaneous coronary intervention (SORT OUT VI) a randomisednon-inferiority trial Lancet 2015 385 1527ndash1535

73 Freed LE Grande DA Lingbin Z et al Joint resurfacing using allo-graft chondrocytes and synthetic biodegradable polymer scaffoldsJ Biomed Mater Res 1994 28 891ndash899

74 Poirier Y Nawrath C Somerville C Production of polyhydrox-yalkanoates a family of biodegradable plastics and elastomers in

bacteria and plants Nat Biotechnol 1995 13 142ndash15075 Dias A Tsuru K Hayakawa S et al Crystallisation studies of

biodegradable CaO-P2O5 glass with MgO and TiO2 for boneregeneration applications Glass Technol 2004 45 78ndash79

76 Klein CPAT de Groot K Drissen AA et al Interaction ofbiodegradable β-whitlockite ceramics with bone tissue an in vivostudy Biomaterials 1985 6 189ndash192

77 Ikenaga M Hardouin P Lemaicirctre J et al Biomechanical charac-terization of a biodegradable calcium phosphate hydraulic cementa comparison with porous biphasic calcium phosphate ceramics JBiomed Mater Res 1998 40 139ndash144

78 Dias AG Lopes MA Santos JD et al In vivo performance ofbiodegradable calcium phosphate glass ceramics using the rabbitmodel histological and SEM observation J Biomater Appl 200620 253ndash266

79 Lee JH Lee CK Chang BS et al In vivo study of novel biodegrad-able and osteoconductive CaO-SiO2-B2O3 glass-ceramics JBiomed Mater Res 2006 77A 362ndash369

80 Song G Song S A possible biodegradable magnesium implant ma-terial Adv Eng Mater 2007 9 298ndash302

81 Kim WC Kim JG Lee JY et al Influence of Ca on the corrosionproperties of magnesium for biomaterials Mater Lett 2008 624146ndash4148

82 Li Z Gu X Lou S et al The development of binary Mg-Ca alloysfor use as biodegradablematerials within bone Biomaterials 200829 1329ndash1344

83 Wan Y Xiong G Luo H et al Preparation and characterization ofa new biomedical magnesium-calcium alloy Mater Des 2008 292034ndash2037

84 Seong JW Kim WJ Development of biodegradable Mg-Ca alloysheets with enhanced strength and corrosion properties throughthe refinement anduniformdispersion of theMg2Caphase by high-ratio differential speed rolling Acta Biomater 2015 11 531ndash542

85 Zhang S Li J Song Y et al In vitro degradation hemolysis andMC3T3-E1 cell adhesion of biodegradable Mg-Zn alloy Mater SciEng-C 2009 29 1907ndash1912

86 Li J Song Y Zhang S et al In vitro responses of human bone mar-row stromal cells to a fluoridated hydroxyapatite coated biodegrad-able Mg-Zn alloy Biomaterials 2010 31 5782ndash5788

87 Brar HS Wong J Manuel MV Investigation of the mechanical anddegradation properties of Mg-Sr and Mg-Zn-Sr alloys for use aspotential biodegradable implant materials J Mech Behav BiomedMater 2012 7 87ndash95

88 Bornapour M Muja N Shum-Tim D et al Biocompatibility andbiodegradability of Mg-Sr alloys the formation of Sr-substitutedhydroxyapatite Acta Biomater 2013 9 5319ndash5330

89 Gu XN Xie XH Li N et al In vitro and in vivo studies on aMg-Sr binary alloy system developed as a new kind of biodegrad-able metal Acta Biomater 2012 8 2360ndash2374

90 Haumlnzi AC Gerber I Schinhammer M et al On the in vitro andin vivo degradation performance and biological response of newbiodegradableMg-Y-Zn alloys Acta Biomater 2010 6 1824ndash1833

91 Chou DT Hong D Saha P et al In vitro and in vivo corrosioncytocompatibility and mechanical properties of biodegradableMg-Y-Ca-Zr alloys as implant materials Acta Biomater 2013 98518ndash8533

92 Zong Y Yuan G Zhang X et al Comparison of biodegradable be-haviors of AZ31 and Mg-Nd-Zn-Zr alloys in Hanks physiologicalsolution Mater Sci Eng-B 2012 177 395ndash401

93 Tie D Feyerabend FMuumlllerWD et al Antibacterial biodegradableMg-Ag alloys Eur Cell Mater 2013 25 284ndash298

94 VojtěchDKubaacutesek J Seraacutek J et al Mechanical and corrosion prop-

13 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

erties of newly developed biodegradable Zn-based alloys for bonefixation Acta Biomater 2011 7 3515ndash3522

95 Li H Yang H Zheng Y et al Design and characterizations of novelbiodegradable ternary Zn-based alloys with IIA nutrient alloyingelements Mg Ca and Sr Mater Des 2015 83 95ndash102

96 Liu X Sun J Yang Y et al Microstructure mechanical proper-ties in vitro degradation behavior and hemocompatibility of novelZn-Mg-Sr alloys as biodegradable metals Mater Lett 2016 162242ndash245

97 Wu C Qiu H Hu X et al Short-term safety and efficacy of thebiodegradable iron stent in mini-swine coronary arteries ChinMed J (Engl) 2013 126 4752ndash4757

98 Purnama A Hermawan H Champetier S et al Gene expressionprofile of mouse fibroblasts exposed to a biodegradable iron alloyfor stents Acta Biomater 2013 9 8746ndash8753

99 HermawanH Purnama A Dube D et al Fe-Mn alloys for metallicbiodegradable stents degradation and cell viability studies ActaBiomater 2010 6 1852ndash1860

100 Sheridan MH Shea LD Peters MC et al Bioabsorbable polymerscaffolds for tissue engineering capable of sustained growth factordelivery J Control Release 2000 64 91ndash102

101 Shawe S Buchanan F Harkin-Jones E et al A study on the rate ofdegradation of the bioabsorbable polymer polyglycolic acid (PGA)J Mater Sci 2006 41 4832ndash4838

102 Palmerini T Biondi-Zoccai G Della Riva D et al Clinical out-comes with bioabsorbable polymer- versus durable polymer-baseddrug-eluting and bare-metal stents J Am Coll Cardiol 2014 63299ndash307

103 Tanimoto S Serruys PW Thuesen L et al Comparison of in vivoacute stent recoil between the bioabsorbable everolimus-elutingcoronary stent and the everolimus-eluting cobalt chromium coro-nary stent insights from the ABSORB and SPIRIT trials CatheterCardiovasc Interv 2007 70 515ndash523

104 Tsuji H Sasaki H Sato H et al Neuron attachment properties ofcarbon negative-ion implanted bioabsorbable polymer of poly-lac-tic acid Nucl Instr Meth Phys Res Sect B-Beam Interact MaterAtoms 2002 191 815ndash819

105 Aikawa M Miyazawa M Okamoto K et al A novel treatment forbile duct injury with a tissue-engineered bioabsorbable polymerpatch Surgery 2010 147 575ndash580

106 WaksmanR Pakala R Kuchulakanti PK et al Safety and efficacy ofbioabsorbablemagnesium alloy stents in porcine coronary arteriesCatheter Cardiovasc Interv 2006 68 607ndash617

107 Di Mario C Griffiths H Goktekin O et al Drug-eluting bioab-sorbable magnesium stent J Interv Cardiol 2004 17 391ndash395

108 Erbel R Di Mario C Bartunek J et al Temporary scaffoldingof coronary arteries with bioabsorbable magnesium stents aprospective non-randomised multicentre trial Lancet 2007 3691869ndash1875

109 Schranz D Zartner P Michel-Behnke I et al Bioabsorbable metalstents for percutaneous treatment of critical recoarctation of theaorta in a newborn Catheter Cardiovasc Interv 2006 67 671ndash673

110 Gu X Zheng Y Cheng Y et al In vitro corrosion and biocompati-bility of binary magnesium alloys Biomaterials 2009 30 484ndash498

111 Hiromoto S InoueM Taguchi T et al In vitro and in vivo biocom-patibility and corrosion behaviour of a bioabsorbable magnesiumalloy coated with octacalcium phosphate and hydroxyapatite ActaBiomater 2015 11 520ndash530

112 Hiromoto S Tomozawa M Maruyama N Fatigue property of abioabsorbable magnesium alloy with a hydroxyapatite coatingformed by a chemical solution deposition J Mech Behav Biomed-ical Mater 2013 25 1ndash10

113 Bowen PK Drelich J Goldman J Zinc exhibits ideal physiologicalcorrosion behavior for bioabsorbable stents Adv Mater 2013 252577ndash2582

114 Liu X Sun J Yang Y et al In vitro investigation of ultra-pure Znand its mini-tube as potential bioabsorbable stent material MaterLett 2015 161 53ndash56

115 LinW Zhang G Cao P et al Cytotoxicity and its test methodologyfor a bioabsorbable nitrided iron stent J Biomed Mater Res 2015103 764ndash776

116 Coe JD Vaccaro AR Instrumented transforaminal lumbar inter-body fusion with bioresorbable polymer implants and iliac crestautograft Spine 2005 30 S76ndashS83

117 Ignatius AA Augat P Ohnmacht M et al A new bioresorbablepolymer for screw augmentation in the osteosynthesis of osteo-porotic cancellous bone a biomechanical evaluation J BiomedMater Res 2001 58 254ndash260

118 Krucoff MW Kereiakes DJ Petersen JL et al A novel biore-sorbable polymer paclitaxel-eluting stent for the treatment ofsingle and multivessel coronary disease J Am Coll Cardiol 200851 1543ndash1552

119 Kostopoulos L Karring T Guided bone regeneration in mandibu-lar defects in rats using a bioresorbable polymer Clin Oral Im-plants Res 1994 5 66ndash74

120 Dubok VA Bioceramicsmdashyesterday today tomorrow PowderMetall Metal Ceram 2000 39 381ndash394

121 Safronova T Kuznetsov A Korneychuk S et al Calcium phos-phate powders synthesized from solutions with [Ca2+][PO4

3minus]=1for bioresorbable ceramics Cent Eur J Chem 2009 7 184ndash191

122 Bohner M Bioresorbable ceramics In Buchanan FJ (Ed) Degra-dation Rate of Bioresorbable Materials Cambridge WoodheadPublishing 2008 95-114

123 Seitz JM Eifler R Stahl J et al Characterization ofMgNd2 alloy forpotential applications in bioresorbable implantable devices ActaBiomater 2012 8 3852ndash3864

124 WenCE Yamada Y Shimojima K et al Porous bioresorbable mag-nesium as bone substitute MSF 2003 419ndash422 1001ndash1006

125 Campos CM Muramatsu T Iqbal J et al Bioresorbable drug-elut-ing magnesium-alloy scaffold for treatment of coronary artery dis-ease Int J Mol Sci 2013 14 24492ndash24500

126 KirklandNT Birbilis NWalker J et al In-vitro dissolution ofmag-nesium-calcium binary alloys clarifying the unique role of calciumadditions in bioresorbable magnesium implant alloys J BiomedMater Res 2010 95B 91ndash100

127 Gastaldi D Sassi V Petrini L et al Continuum damage model forbioresorbable magnesium alloy devices mdashapplication to coronarystents J Mech Behav Biomed Mater 2011 4 352ndash365

128 Kitabata H Waksman R Warnack B Bioresorbable metal scaffoldfor cardiovascular application current knowledge and future per-spectives Cardiovasc Revasc Med 2014 15 109ndash116

Acknowledgments This work was supported by the National Key Re-search and Development Program of China (2016YFC1102402) NationalNatural Science Foundation of China (NSFC 51431002) and the NSFCand the Research Grants Council (RGC) of Hong Kong Joint ResearchScheme (51361165101 and 5161101031)

Author contributions Liu Y prepared the figures tables organized thereferences and wrote the paper Zheng Y provided the overall concept andrevised the manuscript Hayes B helped with the standard developmentand revised the manuscript All authors participated in the discussion

Conflict of interest The authors declare that they have no conflict ofinterest

14copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Yang Liu received his bachelor degree in materials science and engineering from Harbin engineering University in 2013Then he continued his study as a PhD candidate in Prof Yufeng Zhengrsquos Lab in Peking University His research interestsare mainly focused on the corrosion study of absorbable metallic biomaterials as well as the development of new kind ofMg-based biomaterials

Yufeng Zheng obtained his PhD degree from Harbin Institute of Technology in 1998 He is the National OutstandingYouth and Yangtze River scholar of China His research interests are focused on the development of novel biomaterials andapplication and design of biomedical devices

Byron Hayes an over 35 year employee of WL Gore has been involved in the commercial development of multiple ab-sorbable polymeric implants since the late 1980s Hayes started his standards development activities with ASTM in 2000where he is actively developing standards for polymeric and metallic absorbable implants In 2010 Hayes also becameinvolved with ISO Technical Committees TC150 and TC194 and is now convener of working groups focused on cardiovas-cular and metallic absorbable implants

可降解可吸收再吸收mdashmdash哪个是描述最终被人体吸收生物材料的最好词汇刘洋1 郑玉峰1 拜伦海耶斯2

摘要 关于最终被人体吸收的植入材料领域内文献采用的英文修饰词长期以来混乱且不同不仅造成文献检索困难同时模糊了研究人员的研究边界 此领域在法律法规标准中统一用词的确定为领域内的科学研究产品销售及产品使用说明奠定了基础 我们基于化学生态学材料学生物学微生物学和药学立足于使用习惯法律标准和市场对领域内使用已久的典型修饰词ldquo生物可降解rdquoldquo再吸收rdquo和ldquo可吸收rdquo进行了讨论和解释 总的来说尽管目前绝大多数修饰语实际想表达的意思相同作者认为ldquo可吸收rdquo这一英文修饰语是最恰当的修饰词 同时我们提议进一步规范和统一该领域修饰词的使用

15 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

  • Degradable absorbable or resorbablemdashwhat is the best grammatical modifier for an implant that is eventually absorbed by the body
  • Abstract
  • INTRODUCTION
    • Current situation
    • Standards development in advance
      • TERMINOLOGY
        • Overview of utilization of the terms ldquodegradationrdquoldquobiodegradationrdquo and ldquodegradablerdquoldquobiodegradablerdquo
        • Overview of utilization of the terms ldquoabsorptionrdquoldquobioabsorptionrdquo and ldquoabsorbablerdquoldquobioabsorbablerdquo
        • Overview of utilization of the terms ldquoresorptionrdquoldquobioresorptionrdquo and ldquoresorbablerdquoldquobioresorbablerdquo
        • Utilization and comparison of the terms ldquobiodegradable metalsrdquo and ldquoabsorbable metallic materialsrdquo
        • Summary quantification of the common Terms
          • DISCUSSION
            • Expertise inherent biases
            • Connotation and extension of noun forms ldquobiodegradation bioabsorption and bioresorptionrdquo and adjectives ldquobiodegradable bioabsorbable and bioresorbablerdquo
              • CONCLUDING REMARKS
              • References
              • Acknowledgements

Figure 3 Searching results in Web of Knowledge from all databases (a) with the total searched publication numbers by ldquodegradablerdquo+ ldquomaterialrdquoldquoabsorbablerdquo+ ldquomaterialrdquo and ldquoresorbablerdquo+ ldquomaterialrdquo as 100 (b) the total searched publication numbers by ldquobiodegradablerdquo+ ldquomaterialrdquo ldquobioab-sorbablerdquo+ ldquomaterialrdquo and ldquobioresorbablerdquo+ ldquomaterialrdquo as 100

DISCUSSION

Expertise inherent biasesAs previously mentioned biomaterial is an interdiscipli-nary field fascinating researchers with specialty from dif-ferent backgrounds Different backgrounds as well as dif-ferent research point of interests may be one of the reasonsfor using different terminologies Materials scientists tendto focus on the materialdevice itself leading to their usageof ldquobiodegradablerdquo to illustrate what happens to the deviceThey pay more attention to the process such as hydroly-sis corrosion debris degradation products and the changeof surface morphology resulting in the researching inter-ests of ldquomaterial biodegradationrdquo In contrast surgeons andbiomedical researchers tend to be concerned more on thehost response and healing process They are curious aboutthe absorption of various degradation products of the im-planted materialdevice and related metabolism mecha-nism and thereby prefer to use the term ldquoabsorbablerdquo toillustrate what happens to the device As known somema-terials may only undergo biodegradation but the corrosionproducts still have no influence on the metabolic activitiesFor example cellulose is considered as ldquodietary fiberrdquowhichcannot be digested and absorbed by human body but is be-nign for human body [55] Some coating tablets for drug ordrug delivery systems made from cellulose and its deriva-tives are quite frequently utilized or investigated [5657]The polymer and derivatives of cellulose can only be de-graded but not be absorbed by human body [58] For suchmaterials the adjective ldquoabsorbablerdquo or ldquobioabsorbablerdquo isnot appropriateOverall once the materialsdevices are implanted into

the human body the ldquobiocorrosionrdquobiodegradationrdquoprocess happens immediately no matter to what degreeat the same time the host will biologically response to the

corrosiondegradation products through the absorptionmetabolism and excretion processes So for the samestory the majority of materials scientists would report itby ldquobiodegradabledegradationrdquo way whereas the majorityof medical doctors would report it by ldquoabsorbableab-sorptionrdquo way In nature the two terms ldquobiodegradablemetalsrdquo and ldquoabsorbable metallic materialsrdquo share the sameconnotation and are mutually replaceable

Connotation and extension of noun forms ldquobiodegradationbioabsorption and bioresorptionrdquo and adjectivesldquobiodegradable bioabsorbable and bioresorbablerdquoThe three noun forms of the terms illustrate the processwhile their adjectival derivatives were used to describe thegroup of materials with such certain capabilities For thestudy on biomaterials polymer researchers use ldquodegrada-tionbiodegradationrdquo when there is proved chain scissionprocess Besides they differentiate ldquobiodegradationrdquo andldquodegradationrdquo by confirmed metabolic activities betweenthe materials and cells or tissues Regarding to the fouradjectives ldquobiodegradablerdquo ldquobioabsorbablerdquo and ldquobiore-sorbablerdquo the term ldquobiocorrodiblerdquo is only used in scientificpapers on iron based materials and some patents on mag-nesium based materials The common usage of termsldquobiodegradablerdquo ldquobioabsorbablerdquo and ldquobioresorbablerdquo withrespect to the biomaterial research area is shown in Table 5The results reveal a widespread usage of ldquobiodegradablerdquo inboth polymers and magnesium based metals Varies typesof materials were reported as biomaterials Besides thereare also reports of ldquobiodegradablerdquo polymers for ecologyand environmental protection which indicates a furtherusage scope of ldquobiodegradablerdquo not only for implants anddevices Besides ldquobioresorbablerdquo is also utilized in all theresearch fields of polymers ceramics andmetals Howeverno current work used ldquobioabsorbablerdquo as grammatical

9 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Table 5 Current reported usage of terms ldquobiodegradablerdquo ldquobioabsorbablerdquo and ldquobioresorbablerdquoTerminology Category Materials Applications

PLA-PEG-biotin PLGA Controlled cell engineering [5960]Porous PLGA Tissue engineering [61ndash63]

PLGA-PEG-PLGA Injective thermosensitive hydrogel [64]PLGA Nerve guidance [65]

Fibronectin (Fn)-coated PLLA P(LLA-CL) Enhanced growth of endothelial cells [6066]PEG tethered PPF [67]

PDMS Drug delivery [68]PGA Tissue engineering [69]

Undefined Coronary stent [70ndash72]PGA Joint resurfacing [73]

Polymers

PHA Ecology and environmental protection [74]CaO-P2O5 glass Bone regeneration [75]β-Whitlockite Bone regeneration [76]

Calcium phosphate hydraulic cement Bone regeneration [77]Calcium

phosphate glass ceramicsBone regeneration [78]

Ceramics

CaO-SiO2-B2O3 glass-ceramics Bone regeneration [79]Pure Mg Implant material [80]

Mg-Ca-based Bone regeneration [81ndash84]Mg-Zn-based Bone regeneration [338586]Mg-Sr-based Bone regeneration [87ndash89]Mg-RE-based Vascular stent [90ndash92]

Mg and its metals

Mg-Ag-based [93]Zn-Mg Zn-Ca Zn-Sr [9495]Zn and its metals Zn-Mg-Sr [96]

Fe [9798]

Biodegradable

Fe and its metals Fe-Mn [99]PLLA PLG PGA Molecule delivery [100]

PGA Suture [101]Undefined Drug-eluting stent [102103]

PLA Neuron attachment [104]Polymers

PLA and PCL reinforced with PGA fibers Bile duct patch [105]Mg-RE based Coronary stent [106ndash109]

Binary Mg alloys [110]Mg and its metalsMg-Al-based [111112]

Zn and its metals Pure Zinc [113114]Fe and its metals Nitrided iron [115]

PLDLA Transforaminal lumbar interbody fusion [116]Alkylene bis(dilactoyl)-methacrylate modified polymer Bone screw augmentation [117]

Undefined Coronary stent [118]PHB Mandibular defects regeneration [119]HA Bone regeneration [120]Ceramics Calcium phosphate [121122]

MgNd2 Stent material [123]Porous Mg Bone substitute [124]Mg-RE Coronary stent [125]Mg-Ca Orthopedic application [126]

Mg and its metals

Mg-based Finite element analysis [127]

Bioabsorbable

Fe and its metals Pure Fe [128]

10copy

ScienceChina

Pressand

Springer-VerlagBerlin

Heidelberg 2017

REVIEWSCIENCE

CHINA

Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

modifier to bioceramics In addition as previouslyillustrated the prefix ldquobiordquo of ldquobioabsorbablerdquo and ldquobiore-sorbablerdquo are abridged hereafter discussion will concen-trate on ldquobiocorrodiblerdquo ldquobiodegradablerdquo ldquoabsorbablerdquo andldquoresorbablerdquoSince absorbable technologies are increasingly utilized

in numerous new and broader implant applications it be-comes more important to not acquiesce in addressing his-torical problems and instead actively move forward towardutilizing standardized language that is both technically ac-curate and unified in itsmeaning Preferred language needsto accurately communicate the concept To achieve the uni-fying goal of harmonized terminology themedical and sci-entific communities need to not solely look at materialschemistry or even biomaterials alone but to instead lookat term selection both across and within the context of thebroader medical disciplinemdashthe location where the resultsof implant technology development actually reaches themarketplace where therapies are brought to those in needNomenclature solutions need to both understand and re-spond to the context of terms across adjacent technologieswhich means to address needs from the perspectives of thebiomaterial researcher the deviceproduct developer thesurgeonclinician user the regulator and last but not leastthe patientgeneral public who is the direct beneficiary ofthe developed technologyA better understanding of these terminologies is neces-

sary and beneficial to the field Therefore the definitionson ldquodegradablerdquo ldquoabsorbablerdquo ldquoresorbablerdquo and relatedterms proposed by different organizations in differentfields have been summarized and discussed with the con-notation and extension of each term being compared andthe criteria being proposed

CONCLUDING REMARKSHerein given both the searching problem on the Internetand ambiguity in meanings the usage of grammaticalmodifiers to describe biomaterials that is eventually ab-sorbed by human body has been enumerated based onusage habits laws standards and markets In summaryldquodegradablerdquoldquobiodegradablerdquo are the most frequently usedgrammatical modifier not only in metals but also poly-mers as such kind of biomaterials ldquoBiodegradationrdquo andldquobiodegradablerdquo define the change of the materialdevicewell in the research of biomaterials but they are alsoadopted in other fields such as ecology and environmentalprotection Meanwhile ldquoresorbablerdquoldquobioresorbablerdquo havelong been recognized in the biological research and theldquoresorptionrdquo itself has been widely accepted as a biological

reaction The utilization of ldquoresorbablerdquoldquobioresorbablerdquowas found to be not as frequent as the counterpartsldquodegradablerdquoldquobiodegradablerdquo and ldquoabsorbablerdquoldquobioab-sorbablerdquo Such usage is accurate for osteoclast driven boneresorption but is inappropriate for implants that do notcarry the potential to grow back into their original formOtherwise despite it is not the most frequently used termldquoabsorbablerdquoldquobioabsorbablerdquo concentrates more on thehost metabolism to the foreign biodegradation productsof the implanted materialdevice compared with ldquodegrad-ablerdquoldquobiodegradablerdquo ldquoAbsorbablerdquo is defined in the scopeof biomaterials by different organizations and their publi-cations and also adopted by ASTM to illustrate ldquoabsorbablepolymerrdquo It is the most historically established the mostbroadly applicable (includes dissolvable devices that donot degrade) the most specific to medical applicationsand is the formal legal descriptor for most implant devicesConsidering the usage history common utilization in lawand standards as well as the scientific meaning in essenceldquoabsorbablerdquo can be better among other grammaticalmodifiers for description of an implant that is eventuallyabsorbed by the body which is recommended by theauthors for a further internationally-unified usage

Received 28 February 2017 accepted 27 March 2017published online 26 April 2017

1 Mackenzie D The history of sutures Med Hist 1973 17 158ndash1682 Hench LL Bioceramics J Am Ceramic Soc 2005 81 1705ndash17283 Hench LL Bioceramics from concept to clinic J AmCeramic Soc

1991 74 1487ndash15104 Windhagen H Radtke K Weizbauer A et al Biodegradable

magnesium-based screw clinically equivalent to titanium screw inhallux valgus surgery short term results of the first prospectiverandomized controlled clinical pilot study BioMed Eng OnLine2013 12 62

5 Schildwaumlchter M Biotronik announces CE mark for magmaristhe first clinically-proven bioresorbable magnesium scaffoldhttpwwwmagmariscomennewsroomjune-15-2016

6 Shalaby SW Burg KJL Bioabsorbable polymers update degrada-tion mechanisms safety and application J App Biomater 1995 6219ndash221

7 Vert M Li SM Spenlehauer G et al Bioresorbability and biocom-patibility of aliphatic polyesters J Mater Sci-Mater Med 1992 3432ndash446

8 Vert M Degradable and bioresorbable polymers in surgery and inpharmacology beliefs and facts J Mater Sci-Mater Med 2009 20437ndash446

9 Benicewicz BC Hopper PK Review polymers for absorbablesurgical suturesmdashPart I J Bioactive Compatible Polym 1990 5453ndash472

10 Barrows HT Synthetic bioabsorbable polymers In Szycher M(Ed) High Performance Biomaterials A Complete Guide toMed-ical and Pharmceutical Applications Boca Raton CRC PRESS1991 243ndash257

11 Weiler A Hoffmann RFG Staumlhelin AC et al Biodegradable

11 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

implants in sports medicine the biological base Arthroscopy-JArthroscopic Related Surgery 2000 16 305ndash321

12 Ikada Y Tsuji H Biodegradable polyesters for medical and ecolog-ical applications Macromol Rapid Commun 2000 21 117ndash132

13 Ashammakhi N Peltoniemi H Waris E et al Developments incraniomaxillofacial surgery use of self-reinforced bioabsorbableosteofixation devices Plast Reconstr Surg 2001 108 167ndash180

14 Vert M Doi Y Hellwich KH et al Terminology for biorelatedpolymers and applications (IUPACRecommendations 2012) PureAppl Chem 2012 84 377ndash410

15 The United States Pharmacopeial Convention The Second Sup-plement to the Pharmacopeia of the United States of America 11thdecennial revision (USP XI-1939 Supplement) 1939

16 Truhlsen SM The recession operation histopathologic responseand suture reaction and absorption Trans Am Ophthalmol Soc1965 63 626ndash677

17 USP in US Law httpwwwusporgprintabout-usplegal-recog-nitionusp-us-law

18 USP develops and publishes standards for drug substances drugproducts excipients and dietary supplements in the United StatesPharmacopeia-National Formulary (USP-NF)

19 United States Public Law 94-295 197620 United States Pharmacopeia httpwwwusporg21 British Pharmacopeia httpswwwpharmacopoeiacom22 European Pharmacopoeia httponlinepheurorgENentryhtm23 Williams DF The Williams Dictionary of Biomaterials Liverpool

Liverpool University Press 199924 httpsenwikipediaorgwikiBiodegradation25 Jones RG Kahovec J Stepto R et al Compendium of Polymer

Terminology and Nomenclature IUPAC Recommendations 2008Cambridge RSC Publishing 2009

26 Higashi S Yamamuro T Nakamura T et al Polymer-hydroxyap-atite composites for biodegradable bone fillers Biomaterials 19867 183ndash187

27 de Groot K Bioceramics of Calcium Phosphate Boca Raton CRCPress 1983

28 Hollinger JO Battistone GC Biodegradable bone repair materialssynthetic polymers and ceramics ClinOrthopRelat Res 1986 207290ndash306

29 ASTMD653-14 Standard Terminology Relating to Soil Rock andContained Fluids ASTM International West Conshohocken PA2014 httpswwwastmorgStandardsD653htm

30 Witte F Hort N Vogt C et al Degradable biomaterials based onmagnesium corrosion Curr Opin Solid State Mater Sci 2008 1263ndash72

31 Lynn DM Langer R Degradable poly(β-amino esters) synthesischaracterization and self-assemblywith plasmidDNA JAmChemSoc 2000 122 10761ndash10768

32 Cima LG Vacanti JP Vacanti C et al Tissue engineering by celltransplantation using degradable polymer substrates J BiomechEng 1991 113 143ndash151

33 Zhang S Zhang X Zhao C et al Research on an Mg-Zn alloy as adegradable biomaterial Acta Biomater 2010 6 626ndash640

34 Anseth KS Metters AT Bryant SJ et al In situ forming degradablenetworks and their application in tissue engineering and drug de-livery J Control Release 2002 78 199ndash209

35 Forrest ML Koerber JT Pack DW A degradable polyethyleniminederivative with low toxicity for highly efficient gene delivery Bio-conjugate Chem 2003 14 934ndash940

36 ASTM E2747-11 Standard Specification for Evaluation and Selec-tion of Onsite Offices for Environmentally Sustainable MeetingsEvents Trade Shows and Conferences ASTM International

West Conshohocken PA 2011 httpswwwastmorgStan-dardsE2747htm

37 ASTM E2745-11 Standard Specification for Evaluation andSelection of Audio Visual (AV) and Production for Environ-mentally Sustainable Meetings Events Trade Shows and Con-ferences ASTM International West Conshohocken PA 2011httpswwwastmorgStandardsE2745htm

38 ASTM E2746-11 Standard Specification for Evaluation andSelection of Communication and Marketing Materials for En-vironmentally Sustainable Meetings Events Trade Shows andConferences ASTM International West Conshohocken PA 2011httpswwwastmorgStandardsE2746htm

39 ASTM E2741-11 Standard Specification for Evaluation and Se-lection of Destinations for Environmentally Sustainable MeetingsEvents Trade Shows and Conferences ASTM InternationalWest Conshohocken PA 2011 httpswwwastmorgStan-dardsE2741htm

40 0 ASTM E2773-11 Standard Specification for Evaluation andSelection of Food and Beverage for Environmentally SustainableMeetings Events Trade Shows and Conferences ASTM Interna-tional West Conshohocken PA 2011 httpswwwastmorgStan-dardsE2773htm

41 ASTM E2742-11 Standard Specification for Evaluation and Selec-tion of Exhibits for Environmentally Sustainable Meetings EventsTrade Shows and Conferences ASTM International West Con-shohocken PA 2011 httpswwwastmorgStandardsE2742htm

42 ASTM E2774-11 Standard Specification for Evaluation and Selec-tion of Venues for Environmentally Sustainable Meetings EventsTrade Shows and Conferences ASTM International West Con-shohocken PA 2011 httpswwwastmorgStandardsE2774htm

43 ASTM F2902-12 Standard Guide for Assessment of AbsorbablePolymeric Implants ASTM International West ConshohockenPA 2012 httpswwwastmorgStandardsF2902htm

44 httpsenwikipediaorgwikiResorption45 Venes D Tabers Cyclopedic Medical Dictionary 22th edition

Philadelphia F A Davis Company 201346 Zheng YF Gu XN Witte F Biodegradable metals Mater Sci Eng-

R-Rep 2014 77 1ndash3447 Hanawa T Metal ion release from metal implants Mater Sci

Eng-C 2004 24 745ndash75248 Zreiqat H Howlett CR Zannettino A et al Mechanisms of mag-

nesium-stimulated adhesion of osteoblastic cells to commonly usedorthopaedic implants J Biomed Mater Res 2002 62 175ndash184

49 Little PJ Bhattacharya R Moreyra AE et al Zinc and cardiovascu-lar disease Nutrition 2010 26 1050ndash1057

50 Seager H Drug-delivery products and the Zydis fast-dissolvingdosage form J Pharm Pharmacol 1998 50 375ndash382

51 Shikinami Y Shape-memory biodegradable and absorbable mate-rial US Patent No 6281262 2001-8-28

52 Huitema TW Knight GW Ransick MH Schulze DR Surgical im-plant with preferential corrosion zone US Patent No 79059022011-3-15

53 Luzier WD Materials derived from biomassbiodegradable mate-rials Proc Natl Acad Sci USA 1992 89 839ndash842

54 Gross RA Kalra B Biodegradable polymers for the environmentScience 2002 297 803ndash807

55 Trumbo P Schlicker S Yates AA et al Dietary reference intakesfor energy carbohydrate fiber fat fatty acids cholesterol proteinand amino acids J Am Diet Assoc 2002 102 1621ndash1630

56 Chambin O Champion D Debray C et al Effects of different cel-lulose derivatives on drug release mechanism studied at a prefor-mulation stage J Control Release 2004 95 101ndash108

12copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

57 Fundueanu G Constantin M Esposito E et al Cellulose acetatebutyrate microcapsules containing dextran ion-exchange resinsas self-propelled drug release system Biomaterials 2005 264337ndash4347

58 Maumlrtson M Viljanto J Hurme T et al Is cellulose sponge degrad-able or stable as implantation material An in vivo subcutaneousstudy in the rat Biomaterials 1999 20 1989ndash1995

59 Patel N Padera R Sanders GH et al Spatially controlled cell en-gineering on biodegradable polymer surfaces The FASEB journal1998 12 1447ndash1454

60 Goldstein A Effect of convection on osteoblastic cell growth andfunction in biodegradable polymer foam scaffolds Biomaterials2001 22 1279ndash1288

61 Wu L Ding J In vitro degradation of three-dimensional porouspoly(DL-lactide-co-glycolide) scaffolds for tissue engineeringBiomaterials 2004 25 5821ndash5830

62 Wu L Ding J Effects of porosity and pore size on in vitro degra-dation of three-dimensional porous poly(DL-lactide-co-glycolide)scaffolds for tissue engineering J Biomed Mater Res 2005 75A767ndash777

63 Pan Z Ding J Poly(lactide-co-glycolide) porous scaffolds for tissueengineering and regenerative medicine Interface Focus 2012 2366ndash377

64 Yu L Zhang Z Zhang H et al Biodegradability and biocompati-bility of thermoreversible hydrogels formed from mixing a sol anda precipitate of block copolymers in water Biomacromolecules2010 11 2169ndash2178

65 Wen X Tresco PA Fabrication and characterization of permeabledegradable poly(DL-lactide-co-glycolide) (PLGA) hollow fiberphase inversion membranes for use as nerve tract guidance chan-nels Biomaterials 2006 27 3800ndash3809

66 Chu CFL Lu A Liszkowski M et al Enhanced growth of animaland human endothelial cells on biodegradable polymers BBA-GenSubjects 1999 1472 479ndash485

67 Jo S Engel PS Mikos AG Synthesis of poly(ethylene glycol)-teth-ered poly(propylene fumarate) and its modification with GRGDpeptide Polymer 2000 41 7595ndash7604

68 Park JH Allen MG Prausnitz MR Biodegradable polymer mi-croneedles fabrication mechanics and transdermal drug deliveryJ Control Release 2005 104 51ndash66

69 Freed LE Vunjak-Novakovic G Biron RJ et al Biodegradablepolymer scaffolds for tissue engineering Nat Biotechnol 1994 12689ndash693

70 Windecker S Serruys PW Wandel S et al Biolimus-eluting stentwith biodegradable polymer versus sirolimus-eluting stent withdurable polymer for coronary revascularisation (LEADERS) arandomised non-inferiority trial Lancet 2008 372 1163ndash1173

71 Stefanini GG Kalesan B Serruys PW et al Long-term clinicaloutcomes of biodegradable polymer biolimus-eluting stents ver-sus durable polymer sirolimus-eluting stents in patients with coro-nary artery disease (LEADERS) 4 year follow-up of a randomisednon-inferiority trial Lancet 2011 378 1940ndash1948

72 Raungaard B Jensen LO Tilsted HH et al Zotarolimus-elutingdurable-polymer-coated stent versus a biolimus-eluting biodegrad-able-polymer-coated stent in unselected patients undergoing per-cutaneous coronary intervention (SORT OUT VI) a randomisednon-inferiority trial Lancet 2015 385 1527ndash1535

73 Freed LE Grande DA Lingbin Z et al Joint resurfacing using allo-graft chondrocytes and synthetic biodegradable polymer scaffoldsJ Biomed Mater Res 1994 28 891ndash899

74 Poirier Y Nawrath C Somerville C Production of polyhydrox-yalkanoates a family of biodegradable plastics and elastomers in

bacteria and plants Nat Biotechnol 1995 13 142ndash15075 Dias A Tsuru K Hayakawa S et al Crystallisation studies of

biodegradable CaO-P2O5 glass with MgO and TiO2 for boneregeneration applications Glass Technol 2004 45 78ndash79

76 Klein CPAT de Groot K Drissen AA et al Interaction ofbiodegradable β-whitlockite ceramics with bone tissue an in vivostudy Biomaterials 1985 6 189ndash192

77 Ikenaga M Hardouin P Lemaicirctre J et al Biomechanical charac-terization of a biodegradable calcium phosphate hydraulic cementa comparison with porous biphasic calcium phosphate ceramics JBiomed Mater Res 1998 40 139ndash144

78 Dias AG Lopes MA Santos JD et al In vivo performance ofbiodegradable calcium phosphate glass ceramics using the rabbitmodel histological and SEM observation J Biomater Appl 200620 253ndash266

79 Lee JH Lee CK Chang BS et al In vivo study of novel biodegrad-able and osteoconductive CaO-SiO2-B2O3 glass-ceramics JBiomed Mater Res 2006 77A 362ndash369

80 Song G Song S A possible biodegradable magnesium implant ma-terial Adv Eng Mater 2007 9 298ndash302

81 Kim WC Kim JG Lee JY et al Influence of Ca on the corrosionproperties of magnesium for biomaterials Mater Lett 2008 624146ndash4148

82 Li Z Gu X Lou S et al The development of binary Mg-Ca alloysfor use as biodegradablematerials within bone Biomaterials 200829 1329ndash1344

83 Wan Y Xiong G Luo H et al Preparation and characterization ofa new biomedical magnesium-calcium alloy Mater Des 2008 292034ndash2037

84 Seong JW Kim WJ Development of biodegradable Mg-Ca alloysheets with enhanced strength and corrosion properties throughthe refinement anduniformdispersion of theMg2Caphase by high-ratio differential speed rolling Acta Biomater 2015 11 531ndash542

85 Zhang S Li J Song Y et al In vitro degradation hemolysis andMC3T3-E1 cell adhesion of biodegradable Mg-Zn alloy Mater SciEng-C 2009 29 1907ndash1912

86 Li J Song Y Zhang S et al In vitro responses of human bone mar-row stromal cells to a fluoridated hydroxyapatite coated biodegrad-able Mg-Zn alloy Biomaterials 2010 31 5782ndash5788

87 Brar HS Wong J Manuel MV Investigation of the mechanical anddegradation properties of Mg-Sr and Mg-Zn-Sr alloys for use aspotential biodegradable implant materials J Mech Behav BiomedMater 2012 7 87ndash95

88 Bornapour M Muja N Shum-Tim D et al Biocompatibility andbiodegradability of Mg-Sr alloys the formation of Sr-substitutedhydroxyapatite Acta Biomater 2013 9 5319ndash5330

89 Gu XN Xie XH Li N et al In vitro and in vivo studies on aMg-Sr binary alloy system developed as a new kind of biodegrad-able metal Acta Biomater 2012 8 2360ndash2374

90 Haumlnzi AC Gerber I Schinhammer M et al On the in vitro andin vivo degradation performance and biological response of newbiodegradableMg-Y-Zn alloys Acta Biomater 2010 6 1824ndash1833

91 Chou DT Hong D Saha P et al In vitro and in vivo corrosioncytocompatibility and mechanical properties of biodegradableMg-Y-Ca-Zr alloys as implant materials Acta Biomater 2013 98518ndash8533

92 Zong Y Yuan G Zhang X et al Comparison of biodegradable be-haviors of AZ31 and Mg-Nd-Zn-Zr alloys in Hanks physiologicalsolution Mater Sci Eng-B 2012 177 395ndash401

93 Tie D Feyerabend FMuumlllerWD et al Antibacterial biodegradableMg-Ag alloys Eur Cell Mater 2013 25 284ndash298

94 VojtěchDKubaacutesek J Seraacutek J et al Mechanical and corrosion prop-

13 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

erties of newly developed biodegradable Zn-based alloys for bonefixation Acta Biomater 2011 7 3515ndash3522

95 Li H Yang H Zheng Y et al Design and characterizations of novelbiodegradable ternary Zn-based alloys with IIA nutrient alloyingelements Mg Ca and Sr Mater Des 2015 83 95ndash102

96 Liu X Sun J Yang Y et al Microstructure mechanical proper-ties in vitro degradation behavior and hemocompatibility of novelZn-Mg-Sr alloys as biodegradable metals Mater Lett 2016 162242ndash245

97 Wu C Qiu H Hu X et al Short-term safety and efficacy of thebiodegradable iron stent in mini-swine coronary arteries ChinMed J (Engl) 2013 126 4752ndash4757

98 Purnama A Hermawan H Champetier S et al Gene expressionprofile of mouse fibroblasts exposed to a biodegradable iron alloyfor stents Acta Biomater 2013 9 8746ndash8753

99 HermawanH Purnama A Dube D et al Fe-Mn alloys for metallicbiodegradable stents degradation and cell viability studies ActaBiomater 2010 6 1852ndash1860

100 Sheridan MH Shea LD Peters MC et al Bioabsorbable polymerscaffolds for tissue engineering capable of sustained growth factordelivery J Control Release 2000 64 91ndash102

101 Shawe S Buchanan F Harkin-Jones E et al A study on the rate ofdegradation of the bioabsorbable polymer polyglycolic acid (PGA)J Mater Sci 2006 41 4832ndash4838

102 Palmerini T Biondi-Zoccai G Della Riva D et al Clinical out-comes with bioabsorbable polymer- versus durable polymer-baseddrug-eluting and bare-metal stents J Am Coll Cardiol 2014 63299ndash307

103 Tanimoto S Serruys PW Thuesen L et al Comparison of in vivoacute stent recoil between the bioabsorbable everolimus-elutingcoronary stent and the everolimus-eluting cobalt chromium coro-nary stent insights from the ABSORB and SPIRIT trials CatheterCardiovasc Interv 2007 70 515ndash523

104 Tsuji H Sasaki H Sato H et al Neuron attachment properties ofcarbon negative-ion implanted bioabsorbable polymer of poly-lac-tic acid Nucl Instr Meth Phys Res Sect B-Beam Interact MaterAtoms 2002 191 815ndash819

105 Aikawa M Miyazawa M Okamoto K et al A novel treatment forbile duct injury with a tissue-engineered bioabsorbable polymerpatch Surgery 2010 147 575ndash580

106 WaksmanR Pakala R Kuchulakanti PK et al Safety and efficacy ofbioabsorbablemagnesium alloy stents in porcine coronary arteriesCatheter Cardiovasc Interv 2006 68 607ndash617

107 Di Mario C Griffiths H Goktekin O et al Drug-eluting bioab-sorbable magnesium stent J Interv Cardiol 2004 17 391ndash395

108 Erbel R Di Mario C Bartunek J et al Temporary scaffoldingof coronary arteries with bioabsorbable magnesium stents aprospective non-randomised multicentre trial Lancet 2007 3691869ndash1875

109 Schranz D Zartner P Michel-Behnke I et al Bioabsorbable metalstents for percutaneous treatment of critical recoarctation of theaorta in a newborn Catheter Cardiovasc Interv 2006 67 671ndash673

110 Gu X Zheng Y Cheng Y et al In vitro corrosion and biocompati-bility of binary magnesium alloys Biomaterials 2009 30 484ndash498

111 Hiromoto S InoueM Taguchi T et al In vitro and in vivo biocom-patibility and corrosion behaviour of a bioabsorbable magnesiumalloy coated with octacalcium phosphate and hydroxyapatite ActaBiomater 2015 11 520ndash530

112 Hiromoto S Tomozawa M Maruyama N Fatigue property of abioabsorbable magnesium alloy with a hydroxyapatite coatingformed by a chemical solution deposition J Mech Behav Biomed-ical Mater 2013 25 1ndash10

113 Bowen PK Drelich J Goldman J Zinc exhibits ideal physiologicalcorrosion behavior for bioabsorbable stents Adv Mater 2013 252577ndash2582

114 Liu X Sun J Yang Y et al In vitro investigation of ultra-pure Znand its mini-tube as potential bioabsorbable stent material MaterLett 2015 161 53ndash56

115 LinW Zhang G Cao P et al Cytotoxicity and its test methodologyfor a bioabsorbable nitrided iron stent J Biomed Mater Res 2015103 764ndash776

116 Coe JD Vaccaro AR Instrumented transforaminal lumbar inter-body fusion with bioresorbable polymer implants and iliac crestautograft Spine 2005 30 S76ndashS83

117 Ignatius AA Augat P Ohnmacht M et al A new bioresorbablepolymer for screw augmentation in the osteosynthesis of osteo-porotic cancellous bone a biomechanical evaluation J BiomedMater Res 2001 58 254ndash260

118 Krucoff MW Kereiakes DJ Petersen JL et al A novel biore-sorbable polymer paclitaxel-eluting stent for the treatment ofsingle and multivessel coronary disease J Am Coll Cardiol 200851 1543ndash1552

119 Kostopoulos L Karring T Guided bone regeneration in mandibu-lar defects in rats using a bioresorbable polymer Clin Oral Im-plants Res 1994 5 66ndash74

120 Dubok VA Bioceramicsmdashyesterday today tomorrow PowderMetall Metal Ceram 2000 39 381ndash394

121 Safronova T Kuznetsov A Korneychuk S et al Calcium phos-phate powders synthesized from solutions with [Ca2+][PO4

3minus]=1for bioresorbable ceramics Cent Eur J Chem 2009 7 184ndash191

122 Bohner M Bioresorbable ceramics In Buchanan FJ (Ed) Degra-dation Rate of Bioresorbable Materials Cambridge WoodheadPublishing 2008 95-114

123 Seitz JM Eifler R Stahl J et al Characterization ofMgNd2 alloy forpotential applications in bioresorbable implantable devices ActaBiomater 2012 8 3852ndash3864

124 WenCE Yamada Y Shimojima K et al Porous bioresorbable mag-nesium as bone substitute MSF 2003 419ndash422 1001ndash1006

125 Campos CM Muramatsu T Iqbal J et al Bioresorbable drug-elut-ing magnesium-alloy scaffold for treatment of coronary artery dis-ease Int J Mol Sci 2013 14 24492ndash24500

126 KirklandNT Birbilis NWalker J et al In-vitro dissolution ofmag-nesium-calcium binary alloys clarifying the unique role of calciumadditions in bioresorbable magnesium implant alloys J BiomedMater Res 2010 95B 91ndash100

127 Gastaldi D Sassi V Petrini L et al Continuum damage model forbioresorbable magnesium alloy devices mdashapplication to coronarystents J Mech Behav Biomed Mater 2011 4 352ndash365

128 Kitabata H Waksman R Warnack B Bioresorbable metal scaffoldfor cardiovascular application current knowledge and future per-spectives Cardiovasc Revasc Med 2014 15 109ndash116

Acknowledgments This work was supported by the National Key Re-search and Development Program of China (2016YFC1102402) NationalNatural Science Foundation of China (NSFC 51431002) and the NSFCand the Research Grants Council (RGC) of Hong Kong Joint ResearchScheme (51361165101 and 5161101031)

Author contributions Liu Y prepared the figures tables organized thereferences and wrote the paper Zheng Y provided the overall concept andrevised the manuscript Hayes B helped with the standard developmentand revised the manuscript All authors participated in the discussion

Conflict of interest The authors declare that they have no conflict ofinterest

14copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Yang Liu received his bachelor degree in materials science and engineering from Harbin engineering University in 2013Then he continued his study as a PhD candidate in Prof Yufeng Zhengrsquos Lab in Peking University His research interestsare mainly focused on the corrosion study of absorbable metallic biomaterials as well as the development of new kind ofMg-based biomaterials

Yufeng Zheng obtained his PhD degree from Harbin Institute of Technology in 1998 He is the National OutstandingYouth and Yangtze River scholar of China His research interests are focused on the development of novel biomaterials andapplication and design of biomedical devices

Byron Hayes an over 35 year employee of WL Gore has been involved in the commercial development of multiple ab-sorbable polymeric implants since the late 1980s Hayes started his standards development activities with ASTM in 2000where he is actively developing standards for polymeric and metallic absorbable implants In 2010 Hayes also becameinvolved with ISO Technical Committees TC150 and TC194 and is now convener of working groups focused on cardiovas-cular and metallic absorbable implants

可降解可吸收再吸收mdashmdash哪个是描述最终被人体吸收生物材料的最好词汇刘洋1 郑玉峰1 拜伦海耶斯2

摘要 关于最终被人体吸收的植入材料领域内文献采用的英文修饰词长期以来混乱且不同不仅造成文献检索困难同时模糊了研究人员的研究边界 此领域在法律法规标准中统一用词的确定为领域内的科学研究产品销售及产品使用说明奠定了基础 我们基于化学生态学材料学生物学微生物学和药学立足于使用习惯法律标准和市场对领域内使用已久的典型修饰词ldquo生物可降解rdquoldquo再吸收rdquo和ldquo可吸收rdquo进行了讨论和解释 总的来说尽管目前绝大多数修饰语实际想表达的意思相同作者认为ldquo可吸收rdquo这一英文修饰语是最恰当的修饰词 同时我们提议进一步规范和统一该领域修饰词的使用

15 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

  • Degradable absorbable or resorbablemdashwhat is the best grammatical modifier for an implant that is eventually absorbed by the body
  • Abstract
  • INTRODUCTION
    • Current situation
    • Standards development in advance
      • TERMINOLOGY
        • Overview of utilization of the terms ldquodegradationrdquoldquobiodegradationrdquo and ldquodegradablerdquoldquobiodegradablerdquo
        • Overview of utilization of the terms ldquoabsorptionrdquoldquobioabsorptionrdquo and ldquoabsorbablerdquoldquobioabsorbablerdquo
        • Overview of utilization of the terms ldquoresorptionrdquoldquobioresorptionrdquo and ldquoresorbablerdquoldquobioresorbablerdquo
        • Utilization and comparison of the terms ldquobiodegradable metalsrdquo and ldquoabsorbable metallic materialsrdquo
        • Summary quantification of the common Terms
          • DISCUSSION
            • Expertise inherent biases
            • Connotation and extension of noun forms ldquobiodegradation bioabsorption and bioresorptionrdquo and adjectives ldquobiodegradable bioabsorbable and bioresorbablerdquo
              • CONCLUDING REMARKS
              • References
              • Acknowledgements

Table 5 Current reported usage of terms ldquobiodegradablerdquo ldquobioabsorbablerdquo and ldquobioresorbablerdquoTerminology Category Materials Applications

PLA-PEG-biotin PLGA Controlled cell engineering [5960]Porous PLGA Tissue engineering [61ndash63]

PLGA-PEG-PLGA Injective thermosensitive hydrogel [64]PLGA Nerve guidance [65]

Fibronectin (Fn)-coated PLLA P(LLA-CL) Enhanced growth of endothelial cells [6066]PEG tethered PPF [67]

PDMS Drug delivery [68]PGA Tissue engineering [69]

Undefined Coronary stent [70ndash72]PGA Joint resurfacing [73]

Polymers

PHA Ecology and environmental protection [74]CaO-P2O5 glass Bone regeneration [75]β-Whitlockite Bone regeneration [76]

Calcium phosphate hydraulic cement Bone regeneration [77]Calcium

phosphate glass ceramicsBone regeneration [78]

Ceramics

CaO-SiO2-B2O3 glass-ceramics Bone regeneration [79]Pure Mg Implant material [80]

Mg-Ca-based Bone regeneration [81ndash84]Mg-Zn-based Bone regeneration [338586]Mg-Sr-based Bone regeneration [87ndash89]Mg-RE-based Vascular stent [90ndash92]

Mg and its metals

Mg-Ag-based [93]Zn-Mg Zn-Ca Zn-Sr [9495]Zn and its metals Zn-Mg-Sr [96]

Fe [9798]

Biodegradable

Fe and its metals Fe-Mn [99]PLLA PLG PGA Molecule delivery [100]

PGA Suture [101]Undefined Drug-eluting stent [102103]

PLA Neuron attachment [104]Polymers

PLA and PCL reinforced with PGA fibers Bile duct patch [105]Mg-RE based Coronary stent [106ndash109]

Binary Mg alloys [110]Mg and its metalsMg-Al-based [111112]

Zn and its metals Pure Zinc [113114]Fe and its metals Nitrided iron [115]

PLDLA Transforaminal lumbar interbody fusion [116]Alkylene bis(dilactoyl)-methacrylate modified polymer Bone screw augmentation [117]

Undefined Coronary stent [118]PHB Mandibular defects regeneration [119]HA Bone regeneration [120]Ceramics Calcium phosphate [121122]

MgNd2 Stent material [123]Porous Mg Bone substitute [124]Mg-RE Coronary stent [125]Mg-Ca Orthopedic application [126]

Mg and its metals

Mg-based Finite element analysis [127]

Bioabsorbable

Fe and its metals Pure Fe [128]

10copy

ScienceChina

Pressand

Springer-VerlagBerlin

Heidelberg 2017

REVIEWSCIENCE

CHINA

Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

modifier to bioceramics In addition as previouslyillustrated the prefix ldquobiordquo of ldquobioabsorbablerdquo and ldquobiore-sorbablerdquo are abridged hereafter discussion will concen-trate on ldquobiocorrodiblerdquo ldquobiodegradablerdquo ldquoabsorbablerdquo andldquoresorbablerdquoSince absorbable technologies are increasingly utilized

in numerous new and broader implant applications it be-comes more important to not acquiesce in addressing his-torical problems and instead actively move forward towardutilizing standardized language that is both technically ac-curate and unified in itsmeaning Preferred language needsto accurately communicate the concept To achieve the uni-fying goal of harmonized terminology themedical and sci-entific communities need to not solely look at materialschemistry or even biomaterials alone but to instead lookat term selection both across and within the context of thebroader medical disciplinemdashthe location where the resultsof implant technology development actually reaches themarketplace where therapies are brought to those in needNomenclature solutions need to both understand and re-spond to the context of terms across adjacent technologieswhich means to address needs from the perspectives of thebiomaterial researcher the deviceproduct developer thesurgeonclinician user the regulator and last but not leastthe patientgeneral public who is the direct beneficiary ofthe developed technologyA better understanding of these terminologies is neces-

sary and beneficial to the field Therefore the definitionson ldquodegradablerdquo ldquoabsorbablerdquo ldquoresorbablerdquo and relatedterms proposed by different organizations in differentfields have been summarized and discussed with the con-notation and extension of each term being compared andthe criteria being proposed

CONCLUDING REMARKSHerein given both the searching problem on the Internetand ambiguity in meanings the usage of grammaticalmodifiers to describe biomaterials that is eventually ab-sorbed by human body has been enumerated based onusage habits laws standards and markets In summaryldquodegradablerdquoldquobiodegradablerdquo are the most frequently usedgrammatical modifier not only in metals but also poly-mers as such kind of biomaterials ldquoBiodegradationrdquo andldquobiodegradablerdquo define the change of the materialdevicewell in the research of biomaterials but they are alsoadopted in other fields such as ecology and environmentalprotection Meanwhile ldquoresorbablerdquoldquobioresorbablerdquo havelong been recognized in the biological research and theldquoresorptionrdquo itself has been widely accepted as a biological

reaction The utilization of ldquoresorbablerdquoldquobioresorbablerdquowas found to be not as frequent as the counterpartsldquodegradablerdquoldquobiodegradablerdquo and ldquoabsorbablerdquoldquobioab-sorbablerdquo Such usage is accurate for osteoclast driven boneresorption but is inappropriate for implants that do notcarry the potential to grow back into their original formOtherwise despite it is not the most frequently used termldquoabsorbablerdquoldquobioabsorbablerdquo concentrates more on thehost metabolism to the foreign biodegradation productsof the implanted materialdevice compared with ldquodegrad-ablerdquoldquobiodegradablerdquo ldquoAbsorbablerdquo is defined in the scopeof biomaterials by different organizations and their publi-cations and also adopted by ASTM to illustrate ldquoabsorbablepolymerrdquo It is the most historically established the mostbroadly applicable (includes dissolvable devices that donot degrade) the most specific to medical applicationsand is the formal legal descriptor for most implant devicesConsidering the usage history common utilization in lawand standards as well as the scientific meaning in essenceldquoabsorbablerdquo can be better among other grammaticalmodifiers for description of an implant that is eventuallyabsorbed by the body which is recommended by theauthors for a further internationally-unified usage

Received 28 February 2017 accepted 27 March 2017published online 26 April 2017

1 Mackenzie D The history of sutures Med Hist 1973 17 158ndash1682 Hench LL Bioceramics J Am Ceramic Soc 2005 81 1705ndash17283 Hench LL Bioceramics from concept to clinic J AmCeramic Soc

1991 74 1487ndash15104 Windhagen H Radtke K Weizbauer A et al Biodegradable

magnesium-based screw clinically equivalent to titanium screw inhallux valgus surgery short term results of the first prospectiverandomized controlled clinical pilot study BioMed Eng OnLine2013 12 62

5 Schildwaumlchter M Biotronik announces CE mark for magmaristhe first clinically-proven bioresorbable magnesium scaffoldhttpwwwmagmariscomennewsroomjune-15-2016

6 Shalaby SW Burg KJL Bioabsorbable polymers update degrada-tion mechanisms safety and application J App Biomater 1995 6219ndash221

7 Vert M Li SM Spenlehauer G et al Bioresorbability and biocom-patibility of aliphatic polyesters J Mater Sci-Mater Med 1992 3432ndash446

8 Vert M Degradable and bioresorbable polymers in surgery and inpharmacology beliefs and facts J Mater Sci-Mater Med 2009 20437ndash446

9 Benicewicz BC Hopper PK Review polymers for absorbablesurgical suturesmdashPart I J Bioactive Compatible Polym 1990 5453ndash472

10 Barrows HT Synthetic bioabsorbable polymers In Szycher M(Ed) High Performance Biomaterials A Complete Guide toMed-ical and Pharmceutical Applications Boca Raton CRC PRESS1991 243ndash257

11 Weiler A Hoffmann RFG Staumlhelin AC et al Biodegradable

11 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

implants in sports medicine the biological base Arthroscopy-JArthroscopic Related Surgery 2000 16 305ndash321

12 Ikada Y Tsuji H Biodegradable polyesters for medical and ecolog-ical applications Macromol Rapid Commun 2000 21 117ndash132

13 Ashammakhi N Peltoniemi H Waris E et al Developments incraniomaxillofacial surgery use of self-reinforced bioabsorbableosteofixation devices Plast Reconstr Surg 2001 108 167ndash180

14 Vert M Doi Y Hellwich KH et al Terminology for biorelatedpolymers and applications (IUPACRecommendations 2012) PureAppl Chem 2012 84 377ndash410

15 The United States Pharmacopeial Convention The Second Sup-plement to the Pharmacopeia of the United States of America 11thdecennial revision (USP XI-1939 Supplement) 1939

16 Truhlsen SM The recession operation histopathologic responseand suture reaction and absorption Trans Am Ophthalmol Soc1965 63 626ndash677

17 USP in US Law httpwwwusporgprintabout-usplegal-recog-nitionusp-us-law

18 USP develops and publishes standards for drug substances drugproducts excipients and dietary supplements in the United StatesPharmacopeia-National Formulary (USP-NF)

19 United States Public Law 94-295 197620 United States Pharmacopeia httpwwwusporg21 British Pharmacopeia httpswwwpharmacopoeiacom22 European Pharmacopoeia httponlinepheurorgENentryhtm23 Williams DF The Williams Dictionary of Biomaterials Liverpool

Liverpool University Press 199924 httpsenwikipediaorgwikiBiodegradation25 Jones RG Kahovec J Stepto R et al Compendium of Polymer

Terminology and Nomenclature IUPAC Recommendations 2008Cambridge RSC Publishing 2009

26 Higashi S Yamamuro T Nakamura T et al Polymer-hydroxyap-atite composites for biodegradable bone fillers Biomaterials 19867 183ndash187

27 de Groot K Bioceramics of Calcium Phosphate Boca Raton CRCPress 1983

28 Hollinger JO Battistone GC Biodegradable bone repair materialssynthetic polymers and ceramics ClinOrthopRelat Res 1986 207290ndash306

29 ASTMD653-14 Standard Terminology Relating to Soil Rock andContained Fluids ASTM International West Conshohocken PA2014 httpswwwastmorgStandardsD653htm

30 Witte F Hort N Vogt C et al Degradable biomaterials based onmagnesium corrosion Curr Opin Solid State Mater Sci 2008 1263ndash72

31 Lynn DM Langer R Degradable poly(β-amino esters) synthesischaracterization and self-assemblywith plasmidDNA JAmChemSoc 2000 122 10761ndash10768

32 Cima LG Vacanti JP Vacanti C et al Tissue engineering by celltransplantation using degradable polymer substrates J BiomechEng 1991 113 143ndash151

33 Zhang S Zhang X Zhao C et al Research on an Mg-Zn alloy as adegradable biomaterial Acta Biomater 2010 6 626ndash640

34 Anseth KS Metters AT Bryant SJ et al In situ forming degradablenetworks and their application in tissue engineering and drug de-livery J Control Release 2002 78 199ndash209

35 Forrest ML Koerber JT Pack DW A degradable polyethyleniminederivative with low toxicity for highly efficient gene delivery Bio-conjugate Chem 2003 14 934ndash940

36 ASTM E2747-11 Standard Specification for Evaluation and Selec-tion of Onsite Offices for Environmentally Sustainable MeetingsEvents Trade Shows and Conferences ASTM International

West Conshohocken PA 2011 httpswwwastmorgStan-dardsE2747htm

37 ASTM E2745-11 Standard Specification for Evaluation andSelection of Audio Visual (AV) and Production for Environ-mentally Sustainable Meetings Events Trade Shows and Con-ferences ASTM International West Conshohocken PA 2011httpswwwastmorgStandardsE2745htm

38 ASTM E2746-11 Standard Specification for Evaluation andSelection of Communication and Marketing Materials for En-vironmentally Sustainable Meetings Events Trade Shows andConferences ASTM International West Conshohocken PA 2011httpswwwastmorgStandardsE2746htm

39 ASTM E2741-11 Standard Specification for Evaluation and Se-lection of Destinations for Environmentally Sustainable MeetingsEvents Trade Shows and Conferences ASTM InternationalWest Conshohocken PA 2011 httpswwwastmorgStan-dardsE2741htm

40 0 ASTM E2773-11 Standard Specification for Evaluation andSelection of Food and Beverage for Environmentally SustainableMeetings Events Trade Shows and Conferences ASTM Interna-tional West Conshohocken PA 2011 httpswwwastmorgStan-dardsE2773htm

41 ASTM E2742-11 Standard Specification for Evaluation and Selec-tion of Exhibits for Environmentally Sustainable Meetings EventsTrade Shows and Conferences ASTM International West Con-shohocken PA 2011 httpswwwastmorgStandardsE2742htm

42 ASTM E2774-11 Standard Specification for Evaluation and Selec-tion of Venues for Environmentally Sustainable Meetings EventsTrade Shows and Conferences ASTM International West Con-shohocken PA 2011 httpswwwastmorgStandardsE2774htm

43 ASTM F2902-12 Standard Guide for Assessment of AbsorbablePolymeric Implants ASTM International West ConshohockenPA 2012 httpswwwastmorgStandardsF2902htm

44 httpsenwikipediaorgwikiResorption45 Venes D Tabers Cyclopedic Medical Dictionary 22th edition

Philadelphia F A Davis Company 201346 Zheng YF Gu XN Witte F Biodegradable metals Mater Sci Eng-

R-Rep 2014 77 1ndash3447 Hanawa T Metal ion release from metal implants Mater Sci

Eng-C 2004 24 745ndash75248 Zreiqat H Howlett CR Zannettino A et al Mechanisms of mag-

nesium-stimulated adhesion of osteoblastic cells to commonly usedorthopaedic implants J Biomed Mater Res 2002 62 175ndash184

49 Little PJ Bhattacharya R Moreyra AE et al Zinc and cardiovascu-lar disease Nutrition 2010 26 1050ndash1057

50 Seager H Drug-delivery products and the Zydis fast-dissolvingdosage form J Pharm Pharmacol 1998 50 375ndash382

51 Shikinami Y Shape-memory biodegradable and absorbable mate-rial US Patent No 6281262 2001-8-28

52 Huitema TW Knight GW Ransick MH Schulze DR Surgical im-plant with preferential corrosion zone US Patent No 79059022011-3-15

53 Luzier WD Materials derived from biomassbiodegradable mate-rials Proc Natl Acad Sci USA 1992 89 839ndash842

54 Gross RA Kalra B Biodegradable polymers for the environmentScience 2002 297 803ndash807

55 Trumbo P Schlicker S Yates AA et al Dietary reference intakesfor energy carbohydrate fiber fat fatty acids cholesterol proteinand amino acids J Am Diet Assoc 2002 102 1621ndash1630

56 Chambin O Champion D Debray C et al Effects of different cel-lulose derivatives on drug release mechanism studied at a prefor-mulation stage J Control Release 2004 95 101ndash108

12copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

57 Fundueanu G Constantin M Esposito E et al Cellulose acetatebutyrate microcapsules containing dextran ion-exchange resinsas self-propelled drug release system Biomaterials 2005 264337ndash4347

58 Maumlrtson M Viljanto J Hurme T et al Is cellulose sponge degrad-able or stable as implantation material An in vivo subcutaneousstudy in the rat Biomaterials 1999 20 1989ndash1995

59 Patel N Padera R Sanders GH et al Spatially controlled cell en-gineering on biodegradable polymer surfaces The FASEB journal1998 12 1447ndash1454

60 Goldstein A Effect of convection on osteoblastic cell growth andfunction in biodegradable polymer foam scaffolds Biomaterials2001 22 1279ndash1288

61 Wu L Ding J In vitro degradation of three-dimensional porouspoly(DL-lactide-co-glycolide) scaffolds for tissue engineeringBiomaterials 2004 25 5821ndash5830

62 Wu L Ding J Effects of porosity and pore size on in vitro degra-dation of three-dimensional porous poly(DL-lactide-co-glycolide)scaffolds for tissue engineering J Biomed Mater Res 2005 75A767ndash777

63 Pan Z Ding J Poly(lactide-co-glycolide) porous scaffolds for tissueengineering and regenerative medicine Interface Focus 2012 2366ndash377

64 Yu L Zhang Z Zhang H et al Biodegradability and biocompati-bility of thermoreversible hydrogels formed from mixing a sol anda precipitate of block copolymers in water Biomacromolecules2010 11 2169ndash2178

65 Wen X Tresco PA Fabrication and characterization of permeabledegradable poly(DL-lactide-co-glycolide) (PLGA) hollow fiberphase inversion membranes for use as nerve tract guidance chan-nels Biomaterials 2006 27 3800ndash3809

66 Chu CFL Lu A Liszkowski M et al Enhanced growth of animaland human endothelial cells on biodegradable polymers BBA-GenSubjects 1999 1472 479ndash485

67 Jo S Engel PS Mikos AG Synthesis of poly(ethylene glycol)-teth-ered poly(propylene fumarate) and its modification with GRGDpeptide Polymer 2000 41 7595ndash7604

68 Park JH Allen MG Prausnitz MR Biodegradable polymer mi-croneedles fabrication mechanics and transdermal drug deliveryJ Control Release 2005 104 51ndash66

69 Freed LE Vunjak-Novakovic G Biron RJ et al Biodegradablepolymer scaffolds for tissue engineering Nat Biotechnol 1994 12689ndash693

70 Windecker S Serruys PW Wandel S et al Biolimus-eluting stentwith biodegradable polymer versus sirolimus-eluting stent withdurable polymer for coronary revascularisation (LEADERS) arandomised non-inferiority trial Lancet 2008 372 1163ndash1173

71 Stefanini GG Kalesan B Serruys PW et al Long-term clinicaloutcomes of biodegradable polymer biolimus-eluting stents ver-sus durable polymer sirolimus-eluting stents in patients with coro-nary artery disease (LEADERS) 4 year follow-up of a randomisednon-inferiority trial Lancet 2011 378 1940ndash1948

72 Raungaard B Jensen LO Tilsted HH et al Zotarolimus-elutingdurable-polymer-coated stent versus a biolimus-eluting biodegrad-able-polymer-coated stent in unselected patients undergoing per-cutaneous coronary intervention (SORT OUT VI) a randomisednon-inferiority trial Lancet 2015 385 1527ndash1535

73 Freed LE Grande DA Lingbin Z et al Joint resurfacing using allo-graft chondrocytes and synthetic biodegradable polymer scaffoldsJ Biomed Mater Res 1994 28 891ndash899

74 Poirier Y Nawrath C Somerville C Production of polyhydrox-yalkanoates a family of biodegradable plastics and elastomers in

bacteria and plants Nat Biotechnol 1995 13 142ndash15075 Dias A Tsuru K Hayakawa S et al Crystallisation studies of

biodegradable CaO-P2O5 glass with MgO and TiO2 for boneregeneration applications Glass Technol 2004 45 78ndash79

76 Klein CPAT de Groot K Drissen AA et al Interaction ofbiodegradable β-whitlockite ceramics with bone tissue an in vivostudy Biomaterials 1985 6 189ndash192

77 Ikenaga M Hardouin P Lemaicirctre J et al Biomechanical charac-terization of a biodegradable calcium phosphate hydraulic cementa comparison with porous biphasic calcium phosphate ceramics JBiomed Mater Res 1998 40 139ndash144

78 Dias AG Lopes MA Santos JD et al In vivo performance ofbiodegradable calcium phosphate glass ceramics using the rabbitmodel histological and SEM observation J Biomater Appl 200620 253ndash266

79 Lee JH Lee CK Chang BS et al In vivo study of novel biodegrad-able and osteoconductive CaO-SiO2-B2O3 glass-ceramics JBiomed Mater Res 2006 77A 362ndash369

80 Song G Song S A possible biodegradable magnesium implant ma-terial Adv Eng Mater 2007 9 298ndash302

81 Kim WC Kim JG Lee JY et al Influence of Ca on the corrosionproperties of magnesium for biomaterials Mater Lett 2008 624146ndash4148

82 Li Z Gu X Lou S et al The development of binary Mg-Ca alloysfor use as biodegradablematerials within bone Biomaterials 200829 1329ndash1344

83 Wan Y Xiong G Luo H et al Preparation and characterization ofa new biomedical magnesium-calcium alloy Mater Des 2008 292034ndash2037

84 Seong JW Kim WJ Development of biodegradable Mg-Ca alloysheets with enhanced strength and corrosion properties throughthe refinement anduniformdispersion of theMg2Caphase by high-ratio differential speed rolling Acta Biomater 2015 11 531ndash542

85 Zhang S Li J Song Y et al In vitro degradation hemolysis andMC3T3-E1 cell adhesion of biodegradable Mg-Zn alloy Mater SciEng-C 2009 29 1907ndash1912

86 Li J Song Y Zhang S et al In vitro responses of human bone mar-row stromal cells to a fluoridated hydroxyapatite coated biodegrad-able Mg-Zn alloy Biomaterials 2010 31 5782ndash5788

87 Brar HS Wong J Manuel MV Investigation of the mechanical anddegradation properties of Mg-Sr and Mg-Zn-Sr alloys for use aspotential biodegradable implant materials J Mech Behav BiomedMater 2012 7 87ndash95

88 Bornapour M Muja N Shum-Tim D et al Biocompatibility andbiodegradability of Mg-Sr alloys the formation of Sr-substitutedhydroxyapatite Acta Biomater 2013 9 5319ndash5330

89 Gu XN Xie XH Li N et al In vitro and in vivo studies on aMg-Sr binary alloy system developed as a new kind of biodegrad-able metal Acta Biomater 2012 8 2360ndash2374

90 Haumlnzi AC Gerber I Schinhammer M et al On the in vitro andin vivo degradation performance and biological response of newbiodegradableMg-Y-Zn alloys Acta Biomater 2010 6 1824ndash1833

91 Chou DT Hong D Saha P et al In vitro and in vivo corrosioncytocompatibility and mechanical properties of biodegradableMg-Y-Ca-Zr alloys as implant materials Acta Biomater 2013 98518ndash8533

92 Zong Y Yuan G Zhang X et al Comparison of biodegradable be-haviors of AZ31 and Mg-Nd-Zn-Zr alloys in Hanks physiologicalsolution Mater Sci Eng-B 2012 177 395ndash401

93 Tie D Feyerabend FMuumlllerWD et al Antibacterial biodegradableMg-Ag alloys Eur Cell Mater 2013 25 284ndash298

94 VojtěchDKubaacutesek J Seraacutek J et al Mechanical and corrosion prop-

13 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

erties of newly developed biodegradable Zn-based alloys for bonefixation Acta Biomater 2011 7 3515ndash3522

95 Li H Yang H Zheng Y et al Design and characterizations of novelbiodegradable ternary Zn-based alloys with IIA nutrient alloyingelements Mg Ca and Sr Mater Des 2015 83 95ndash102

96 Liu X Sun J Yang Y et al Microstructure mechanical proper-ties in vitro degradation behavior and hemocompatibility of novelZn-Mg-Sr alloys as biodegradable metals Mater Lett 2016 162242ndash245

97 Wu C Qiu H Hu X et al Short-term safety and efficacy of thebiodegradable iron stent in mini-swine coronary arteries ChinMed J (Engl) 2013 126 4752ndash4757

98 Purnama A Hermawan H Champetier S et al Gene expressionprofile of mouse fibroblasts exposed to a biodegradable iron alloyfor stents Acta Biomater 2013 9 8746ndash8753

99 HermawanH Purnama A Dube D et al Fe-Mn alloys for metallicbiodegradable stents degradation and cell viability studies ActaBiomater 2010 6 1852ndash1860

100 Sheridan MH Shea LD Peters MC et al Bioabsorbable polymerscaffolds for tissue engineering capable of sustained growth factordelivery J Control Release 2000 64 91ndash102

101 Shawe S Buchanan F Harkin-Jones E et al A study on the rate ofdegradation of the bioabsorbable polymer polyglycolic acid (PGA)J Mater Sci 2006 41 4832ndash4838

102 Palmerini T Biondi-Zoccai G Della Riva D et al Clinical out-comes with bioabsorbable polymer- versus durable polymer-baseddrug-eluting and bare-metal stents J Am Coll Cardiol 2014 63299ndash307

103 Tanimoto S Serruys PW Thuesen L et al Comparison of in vivoacute stent recoil between the bioabsorbable everolimus-elutingcoronary stent and the everolimus-eluting cobalt chromium coro-nary stent insights from the ABSORB and SPIRIT trials CatheterCardiovasc Interv 2007 70 515ndash523

104 Tsuji H Sasaki H Sato H et al Neuron attachment properties ofcarbon negative-ion implanted bioabsorbable polymer of poly-lac-tic acid Nucl Instr Meth Phys Res Sect B-Beam Interact MaterAtoms 2002 191 815ndash819

105 Aikawa M Miyazawa M Okamoto K et al A novel treatment forbile duct injury with a tissue-engineered bioabsorbable polymerpatch Surgery 2010 147 575ndash580

106 WaksmanR Pakala R Kuchulakanti PK et al Safety and efficacy ofbioabsorbablemagnesium alloy stents in porcine coronary arteriesCatheter Cardiovasc Interv 2006 68 607ndash617

107 Di Mario C Griffiths H Goktekin O et al Drug-eluting bioab-sorbable magnesium stent J Interv Cardiol 2004 17 391ndash395

108 Erbel R Di Mario C Bartunek J et al Temporary scaffoldingof coronary arteries with bioabsorbable magnesium stents aprospective non-randomised multicentre trial Lancet 2007 3691869ndash1875

109 Schranz D Zartner P Michel-Behnke I et al Bioabsorbable metalstents for percutaneous treatment of critical recoarctation of theaorta in a newborn Catheter Cardiovasc Interv 2006 67 671ndash673

110 Gu X Zheng Y Cheng Y et al In vitro corrosion and biocompati-bility of binary magnesium alloys Biomaterials 2009 30 484ndash498

111 Hiromoto S InoueM Taguchi T et al In vitro and in vivo biocom-patibility and corrosion behaviour of a bioabsorbable magnesiumalloy coated with octacalcium phosphate and hydroxyapatite ActaBiomater 2015 11 520ndash530

112 Hiromoto S Tomozawa M Maruyama N Fatigue property of abioabsorbable magnesium alloy with a hydroxyapatite coatingformed by a chemical solution deposition J Mech Behav Biomed-ical Mater 2013 25 1ndash10

113 Bowen PK Drelich J Goldman J Zinc exhibits ideal physiologicalcorrosion behavior for bioabsorbable stents Adv Mater 2013 252577ndash2582

114 Liu X Sun J Yang Y et al In vitro investigation of ultra-pure Znand its mini-tube as potential bioabsorbable stent material MaterLett 2015 161 53ndash56

115 LinW Zhang G Cao P et al Cytotoxicity and its test methodologyfor a bioabsorbable nitrided iron stent J Biomed Mater Res 2015103 764ndash776

116 Coe JD Vaccaro AR Instrumented transforaminal lumbar inter-body fusion with bioresorbable polymer implants and iliac crestautograft Spine 2005 30 S76ndashS83

117 Ignatius AA Augat P Ohnmacht M et al A new bioresorbablepolymer for screw augmentation in the osteosynthesis of osteo-porotic cancellous bone a biomechanical evaluation J BiomedMater Res 2001 58 254ndash260

118 Krucoff MW Kereiakes DJ Petersen JL et al A novel biore-sorbable polymer paclitaxel-eluting stent for the treatment ofsingle and multivessel coronary disease J Am Coll Cardiol 200851 1543ndash1552

119 Kostopoulos L Karring T Guided bone regeneration in mandibu-lar defects in rats using a bioresorbable polymer Clin Oral Im-plants Res 1994 5 66ndash74

120 Dubok VA Bioceramicsmdashyesterday today tomorrow PowderMetall Metal Ceram 2000 39 381ndash394

121 Safronova T Kuznetsov A Korneychuk S et al Calcium phos-phate powders synthesized from solutions with [Ca2+][PO4

3minus]=1for bioresorbable ceramics Cent Eur J Chem 2009 7 184ndash191

122 Bohner M Bioresorbable ceramics In Buchanan FJ (Ed) Degra-dation Rate of Bioresorbable Materials Cambridge WoodheadPublishing 2008 95-114

123 Seitz JM Eifler R Stahl J et al Characterization ofMgNd2 alloy forpotential applications in bioresorbable implantable devices ActaBiomater 2012 8 3852ndash3864

124 WenCE Yamada Y Shimojima K et al Porous bioresorbable mag-nesium as bone substitute MSF 2003 419ndash422 1001ndash1006

125 Campos CM Muramatsu T Iqbal J et al Bioresorbable drug-elut-ing magnesium-alloy scaffold for treatment of coronary artery dis-ease Int J Mol Sci 2013 14 24492ndash24500

126 KirklandNT Birbilis NWalker J et al In-vitro dissolution ofmag-nesium-calcium binary alloys clarifying the unique role of calciumadditions in bioresorbable magnesium implant alloys J BiomedMater Res 2010 95B 91ndash100

127 Gastaldi D Sassi V Petrini L et al Continuum damage model forbioresorbable magnesium alloy devices mdashapplication to coronarystents J Mech Behav Biomed Mater 2011 4 352ndash365

128 Kitabata H Waksman R Warnack B Bioresorbable metal scaffoldfor cardiovascular application current knowledge and future per-spectives Cardiovasc Revasc Med 2014 15 109ndash116

Acknowledgments This work was supported by the National Key Re-search and Development Program of China (2016YFC1102402) NationalNatural Science Foundation of China (NSFC 51431002) and the NSFCand the Research Grants Council (RGC) of Hong Kong Joint ResearchScheme (51361165101 and 5161101031)

Author contributions Liu Y prepared the figures tables organized thereferences and wrote the paper Zheng Y provided the overall concept andrevised the manuscript Hayes B helped with the standard developmentand revised the manuscript All authors participated in the discussion

Conflict of interest The authors declare that they have no conflict ofinterest

14copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Yang Liu received his bachelor degree in materials science and engineering from Harbin engineering University in 2013Then he continued his study as a PhD candidate in Prof Yufeng Zhengrsquos Lab in Peking University His research interestsare mainly focused on the corrosion study of absorbable metallic biomaterials as well as the development of new kind ofMg-based biomaterials

Yufeng Zheng obtained his PhD degree from Harbin Institute of Technology in 1998 He is the National OutstandingYouth and Yangtze River scholar of China His research interests are focused on the development of novel biomaterials andapplication and design of biomedical devices

Byron Hayes an over 35 year employee of WL Gore has been involved in the commercial development of multiple ab-sorbable polymeric implants since the late 1980s Hayes started his standards development activities with ASTM in 2000where he is actively developing standards for polymeric and metallic absorbable implants In 2010 Hayes also becameinvolved with ISO Technical Committees TC150 and TC194 and is now convener of working groups focused on cardiovas-cular and metallic absorbable implants

可降解可吸收再吸收mdashmdash哪个是描述最终被人体吸收生物材料的最好词汇刘洋1 郑玉峰1 拜伦海耶斯2

摘要 关于最终被人体吸收的植入材料领域内文献采用的英文修饰词长期以来混乱且不同不仅造成文献检索困难同时模糊了研究人员的研究边界 此领域在法律法规标准中统一用词的确定为领域内的科学研究产品销售及产品使用说明奠定了基础 我们基于化学生态学材料学生物学微生物学和药学立足于使用习惯法律标准和市场对领域内使用已久的典型修饰词ldquo生物可降解rdquoldquo再吸收rdquo和ldquo可吸收rdquo进行了讨论和解释 总的来说尽管目前绝大多数修饰语实际想表达的意思相同作者认为ldquo可吸收rdquo这一英文修饰语是最恰当的修饰词 同时我们提议进一步规范和统一该领域修饰词的使用

15 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

  • Degradable absorbable or resorbablemdashwhat is the best grammatical modifier for an implant that is eventually absorbed by the body
  • Abstract
  • INTRODUCTION
    • Current situation
    • Standards development in advance
      • TERMINOLOGY
        • Overview of utilization of the terms ldquodegradationrdquoldquobiodegradationrdquo and ldquodegradablerdquoldquobiodegradablerdquo
        • Overview of utilization of the terms ldquoabsorptionrdquoldquobioabsorptionrdquo and ldquoabsorbablerdquoldquobioabsorbablerdquo
        • Overview of utilization of the terms ldquoresorptionrdquoldquobioresorptionrdquo and ldquoresorbablerdquoldquobioresorbablerdquo
        • Utilization and comparison of the terms ldquobiodegradable metalsrdquo and ldquoabsorbable metallic materialsrdquo
        • Summary quantification of the common Terms
          • DISCUSSION
            • Expertise inherent biases
            • Connotation and extension of noun forms ldquobiodegradation bioabsorption and bioresorptionrdquo and adjectives ldquobiodegradable bioabsorbable and bioresorbablerdquo
              • CONCLUDING REMARKS
              • References
              • Acknowledgements

modifier to bioceramics In addition as previouslyillustrated the prefix ldquobiordquo of ldquobioabsorbablerdquo and ldquobiore-sorbablerdquo are abridged hereafter discussion will concen-trate on ldquobiocorrodiblerdquo ldquobiodegradablerdquo ldquoabsorbablerdquo andldquoresorbablerdquoSince absorbable technologies are increasingly utilized

in numerous new and broader implant applications it be-comes more important to not acquiesce in addressing his-torical problems and instead actively move forward towardutilizing standardized language that is both technically ac-curate and unified in itsmeaning Preferred language needsto accurately communicate the concept To achieve the uni-fying goal of harmonized terminology themedical and sci-entific communities need to not solely look at materialschemistry or even biomaterials alone but to instead lookat term selection both across and within the context of thebroader medical disciplinemdashthe location where the resultsof implant technology development actually reaches themarketplace where therapies are brought to those in needNomenclature solutions need to both understand and re-spond to the context of terms across adjacent technologieswhich means to address needs from the perspectives of thebiomaterial researcher the deviceproduct developer thesurgeonclinician user the regulator and last but not leastthe patientgeneral public who is the direct beneficiary ofthe developed technologyA better understanding of these terminologies is neces-

sary and beneficial to the field Therefore the definitionson ldquodegradablerdquo ldquoabsorbablerdquo ldquoresorbablerdquo and relatedterms proposed by different organizations in differentfields have been summarized and discussed with the con-notation and extension of each term being compared andthe criteria being proposed

CONCLUDING REMARKSHerein given both the searching problem on the Internetand ambiguity in meanings the usage of grammaticalmodifiers to describe biomaterials that is eventually ab-sorbed by human body has been enumerated based onusage habits laws standards and markets In summaryldquodegradablerdquoldquobiodegradablerdquo are the most frequently usedgrammatical modifier not only in metals but also poly-mers as such kind of biomaterials ldquoBiodegradationrdquo andldquobiodegradablerdquo define the change of the materialdevicewell in the research of biomaterials but they are alsoadopted in other fields such as ecology and environmentalprotection Meanwhile ldquoresorbablerdquoldquobioresorbablerdquo havelong been recognized in the biological research and theldquoresorptionrdquo itself has been widely accepted as a biological

reaction The utilization of ldquoresorbablerdquoldquobioresorbablerdquowas found to be not as frequent as the counterpartsldquodegradablerdquoldquobiodegradablerdquo and ldquoabsorbablerdquoldquobioab-sorbablerdquo Such usage is accurate for osteoclast driven boneresorption but is inappropriate for implants that do notcarry the potential to grow back into their original formOtherwise despite it is not the most frequently used termldquoabsorbablerdquoldquobioabsorbablerdquo concentrates more on thehost metabolism to the foreign biodegradation productsof the implanted materialdevice compared with ldquodegrad-ablerdquoldquobiodegradablerdquo ldquoAbsorbablerdquo is defined in the scopeof biomaterials by different organizations and their publi-cations and also adopted by ASTM to illustrate ldquoabsorbablepolymerrdquo It is the most historically established the mostbroadly applicable (includes dissolvable devices that donot degrade) the most specific to medical applicationsand is the formal legal descriptor for most implant devicesConsidering the usage history common utilization in lawand standards as well as the scientific meaning in essenceldquoabsorbablerdquo can be better among other grammaticalmodifiers for description of an implant that is eventuallyabsorbed by the body which is recommended by theauthors for a further internationally-unified usage

Received 28 February 2017 accepted 27 March 2017published online 26 April 2017

1 Mackenzie D The history of sutures Med Hist 1973 17 158ndash1682 Hench LL Bioceramics J Am Ceramic Soc 2005 81 1705ndash17283 Hench LL Bioceramics from concept to clinic J AmCeramic Soc

1991 74 1487ndash15104 Windhagen H Radtke K Weizbauer A et al Biodegradable

magnesium-based screw clinically equivalent to titanium screw inhallux valgus surgery short term results of the first prospectiverandomized controlled clinical pilot study BioMed Eng OnLine2013 12 62

5 Schildwaumlchter M Biotronik announces CE mark for magmaristhe first clinically-proven bioresorbable magnesium scaffoldhttpwwwmagmariscomennewsroomjune-15-2016

6 Shalaby SW Burg KJL Bioabsorbable polymers update degrada-tion mechanisms safety and application J App Biomater 1995 6219ndash221

7 Vert M Li SM Spenlehauer G et al Bioresorbability and biocom-patibility of aliphatic polyesters J Mater Sci-Mater Med 1992 3432ndash446

8 Vert M Degradable and bioresorbable polymers in surgery and inpharmacology beliefs and facts J Mater Sci-Mater Med 2009 20437ndash446

9 Benicewicz BC Hopper PK Review polymers for absorbablesurgical suturesmdashPart I J Bioactive Compatible Polym 1990 5453ndash472

10 Barrows HT Synthetic bioabsorbable polymers In Szycher M(Ed) High Performance Biomaterials A Complete Guide toMed-ical and Pharmceutical Applications Boca Raton CRC PRESS1991 243ndash257

11 Weiler A Hoffmann RFG Staumlhelin AC et al Biodegradable

11 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

implants in sports medicine the biological base Arthroscopy-JArthroscopic Related Surgery 2000 16 305ndash321

12 Ikada Y Tsuji H Biodegradable polyesters for medical and ecolog-ical applications Macromol Rapid Commun 2000 21 117ndash132

13 Ashammakhi N Peltoniemi H Waris E et al Developments incraniomaxillofacial surgery use of self-reinforced bioabsorbableosteofixation devices Plast Reconstr Surg 2001 108 167ndash180

14 Vert M Doi Y Hellwich KH et al Terminology for biorelatedpolymers and applications (IUPACRecommendations 2012) PureAppl Chem 2012 84 377ndash410

15 The United States Pharmacopeial Convention The Second Sup-plement to the Pharmacopeia of the United States of America 11thdecennial revision (USP XI-1939 Supplement) 1939

16 Truhlsen SM The recession operation histopathologic responseand suture reaction and absorption Trans Am Ophthalmol Soc1965 63 626ndash677

17 USP in US Law httpwwwusporgprintabout-usplegal-recog-nitionusp-us-law

18 USP develops and publishes standards for drug substances drugproducts excipients and dietary supplements in the United StatesPharmacopeia-National Formulary (USP-NF)

19 United States Public Law 94-295 197620 United States Pharmacopeia httpwwwusporg21 British Pharmacopeia httpswwwpharmacopoeiacom22 European Pharmacopoeia httponlinepheurorgENentryhtm23 Williams DF The Williams Dictionary of Biomaterials Liverpool

Liverpool University Press 199924 httpsenwikipediaorgwikiBiodegradation25 Jones RG Kahovec J Stepto R et al Compendium of Polymer

Terminology and Nomenclature IUPAC Recommendations 2008Cambridge RSC Publishing 2009

26 Higashi S Yamamuro T Nakamura T et al Polymer-hydroxyap-atite composites for biodegradable bone fillers Biomaterials 19867 183ndash187

27 de Groot K Bioceramics of Calcium Phosphate Boca Raton CRCPress 1983

28 Hollinger JO Battistone GC Biodegradable bone repair materialssynthetic polymers and ceramics ClinOrthopRelat Res 1986 207290ndash306

29 ASTMD653-14 Standard Terminology Relating to Soil Rock andContained Fluids ASTM International West Conshohocken PA2014 httpswwwastmorgStandardsD653htm

30 Witte F Hort N Vogt C et al Degradable biomaterials based onmagnesium corrosion Curr Opin Solid State Mater Sci 2008 1263ndash72

31 Lynn DM Langer R Degradable poly(β-amino esters) synthesischaracterization and self-assemblywith plasmidDNA JAmChemSoc 2000 122 10761ndash10768

32 Cima LG Vacanti JP Vacanti C et al Tissue engineering by celltransplantation using degradable polymer substrates J BiomechEng 1991 113 143ndash151

33 Zhang S Zhang X Zhao C et al Research on an Mg-Zn alloy as adegradable biomaterial Acta Biomater 2010 6 626ndash640

34 Anseth KS Metters AT Bryant SJ et al In situ forming degradablenetworks and their application in tissue engineering and drug de-livery J Control Release 2002 78 199ndash209

35 Forrest ML Koerber JT Pack DW A degradable polyethyleniminederivative with low toxicity for highly efficient gene delivery Bio-conjugate Chem 2003 14 934ndash940

36 ASTM E2747-11 Standard Specification for Evaluation and Selec-tion of Onsite Offices for Environmentally Sustainable MeetingsEvents Trade Shows and Conferences ASTM International

West Conshohocken PA 2011 httpswwwastmorgStan-dardsE2747htm

37 ASTM E2745-11 Standard Specification for Evaluation andSelection of Audio Visual (AV) and Production for Environ-mentally Sustainable Meetings Events Trade Shows and Con-ferences ASTM International West Conshohocken PA 2011httpswwwastmorgStandardsE2745htm

38 ASTM E2746-11 Standard Specification for Evaluation andSelection of Communication and Marketing Materials for En-vironmentally Sustainable Meetings Events Trade Shows andConferences ASTM International West Conshohocken PA 2011httpswwwastmorgStandardsE2746htm

39 ASTM E2741-11 Standard Specification for Evaluation and Se-lection of Destinations for Environmentally Sustainable MeetingsEvents Trade Shows and Conferences ASTM InternationalWest Conshohocken PA 2011 httpswwwastmorgStan-dardsE2741htm

40 0 ASTM E2773-11 Standard Specification for Evaluation andSelection of Food and Beverage for Environmentally SustainableMeetings Events Trade Shows and Conferences ASTM Interna-tional West Conshohocken PA 2011 httpswwwastmorgStan-dardsE2773htm

41 ASTM E2742-11 Standard Specification for Evaluation and Selec-tion of Exhibits for Environmentally Sustainable Meetings EventsTrade Shows and Conferences ASTM International West Con-shohocken PA 2011 httpswwwastmorgStandardsE2742htm

42 ASTM E2774-11 Standard Specification for Evaluation and Selec-tion of Venues for Environmentally Sustainable Meetings EventsTrade Shows and Conferences ASTM International West Con-shohocken PA 2011 httpswwwastmorgStandardsE2774htm

43 ASTM F2902-12 Standard Guide for Assessment of AbsorbablePolymeric Implants ASTM International West ConshohockenPA 2012 httpswwwastmorgStandardsF2902htm

44 httpsenwikipediaorgwikiResorption45 Venes D Tabers Cyclopedic Medical Dictionary 22th edition

Philadelphia F A Davis Company 201346 Zheng YF Gu XN Witte F Biodegradable metals Mater Sci Eng-

R-Rep 2014 77 1ndash3447 Hanawa T Metal ion release from metal implants Mater Sci

Eng-C 2004 24 745ndash75248 Zreiqat H Howlett CR Zannettino A et al Mechanisms of mag-

nesium-stimulated adhesion of osteoblastic cells to commonly usedorthopaedic implants J Biomed Mater Res 2002 62 175ndash184

49 Little PJ Bhattacharya R Moreyra AE et al Zinc and cardiovascu-lar disease Nutrition 2010 26 1050ndash1057

50 Seager H Drug-delivery products and the Zydis fast-dissolvingdosage form J Pharm Pharmacol 1998 50 375ndash382

51 Shikinami Y Shape-memory biodegradable and absorbable mate-rial US Patent No 6281262 2001-8-28

52 Huitema TW Knight GW Ransick MH Schulze DR Surgical im-plant with preferential corrosion zone US Patent No 79059022011-3-15

53 Luzier WD Materials derived from biomassbiodegradable mate-rials Proc Natl Acad Sci USA 1992 89 839ndash842

54 Gross RA Kalra B Biodegradable polymers for the environmentScience 2002 297 803ndash807

55 Trumbo P Schlicker S Yates AA et al Dietary reference intakesfor energy carbohydrate fiber fat fatty acids cholesterol proteinand amino acids J Am Diet Assoc 2002 102 1621ndash1630

56 Chambin O Champion D Debray C et al Effects of different cel-lulose derivatives on drug release mechanism studied at a prefor-mulation stage J Control Release 2004 95 101ndash108

12copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

57 Fundueanu G Constantin M Esposito E et al Cellulose acetatebutyrate microcapsules containing dextran ion-exchange resinsas self-propelled drug release system Biomaterials 2005 264337ndash4347

58 Maumlrtson M Viljanto J Hurme T et al Is cellulose sponge degrad-able or stable as implantation material An in vivo subcutaneousstudy in the rat Biomaterials 1999 20 1989ndash1995

59 Patel N Padera R Sanders GH et al Spatially controlled cell en-gineering on biodegradable polymer surfaces The FASEB journal1998 12 1447ndash1454

60 Goldstein A Effect of convection on osteoblastic cell growth andfunction in biodegradable polymer foam scaffolds Biomaterials2001 22 1279ndash1288

61 Wu L Ding J In vitro degradation of three-dimensional porouspoly(DL-lactide-co-glycolide) scaffolds for tissue engineeringBiomaterials 2004 25 5821ndash5830

62 Wu L Ding J Effects of porosity and pore size on in vitro degra-dation of three-dimensional porous poly(DL-lactide-co-glycolide)scaffolds for tissue engineering J Biomed Mater Res 2005 75A767ndash777

63 Pan Z Ding J Poly(lactide-co-glycolide) porous scaffolds for tissueengineering and regenerative medicine Interface Focus 2012 2366ndash377

64 Yu L Zhang Z Zhang H et al Biodegradability and biocompati-bility of thermoreversible hydrogels formed from mixing a sol anda precipitate of block copolymers in water Biomacromolecules2010 11 2169ndash2178

65 Wen X Tresco PA Fabrication and characterization of permeabledegradable poly(DL-lactide-co-glycolide) (PLGA) hollow fiberphase inversion membranes for use as nerve tract guidance chan-nels Biomaterials 2006 27 3800ndash3809

66 Chu CFL Lu A Liszkowski M et al Enhanced growth of animaland human endothelial cells on biodegradable polymers BBA-GenSubjects 1999 1472 479ndash485

67 Jo S Engel PS Mikos AG Synthesis of poly(ethylene glycol)-teth-ered poly(propylene fumarate) and its modification with GRGDpeptide Polymer 2000 41 7595ndash7604

68 Park JH Allen MG Prausnitz MR Biodegradable polymer mi-croneedles fabrication mechanics and transdermal drug deliveryJ Control Release 2005 104 51ndash66

69 Freed LE Vunjak-Novakovic G Biron RJ et al Biodegradablepolymer scaffolds for tissue engineering Nat Biotechnol 1994 12689ndash693

70 Windecker S Serruys PW Wandel S et al Biolimus-eluting stentwith biodegradable polymer versus sirolimus-eluting stent withdurable polymer for coronary revascularisation (LEADERS) arandomised non-inferiority trial Lancet 2008 372 1163ndash1173

71 Stefanini GG Kalesan B Serruys PW et al Long-term clinicaloutcomes of biodegradable polymer biolimus-eluting stents ver-sus durable polymer sirolimus-eluting stents in patients with coro-nary artery disease (LEADERS) 4 year follow-up of a randomisednon-inferiority trial Lancet 2011 378 1940ndash1948

72 Raungaard B Jensen LO Tilsted HH et al Zotarolimus-elutingdurable-polymer-coated stent versus a biolimus-eluting biodegrad-able-polymer-coated stent in unselected patients undergoing per-cutaneous coronary intervention (SORT OUT VI) a randomisednon-inferiority trial Lancet 2015 385 1527ndash1535

73 Freed LE Grande DA Lingbin Z et al Joint resurfacing using allo-graft chondrocytes and synthetic biodegradable polymer scaffoldsJ Biomed Mater Res 1994 28 891ndash899

74 Poirier Y Nawrath C Somerville C Production of polyhydrox-yalkanoates a family of biodegradable plastics and elastomers in

bacteria and plants Nat Biotechnol 1995 13 142ndash15075 Dias A Tsuru K Hayakawa S et al Crystallisation studies of

biodegradable CaO-P2O5 glass with MgO and TiO2 for boneregeneration applications Glass Technol 2004 45 78ndash79

76 Klein CPAT de Groot K Drissen AA et al Interaction ofbiodegradable β-whitlockite ceramics with bone tissue an in vivostudy Biomaterials 1985 6 189ndash192

77 Ikenaga M Hardouin P Lemaicirctre J et al Biomechanical charac-terization of a biodegradable calcium phosphate hydraulic cementa comparison with porous biphasic calcium phosphate ceramics JBiomed Mater Res 1998 40 139ndash144

78 Dias AG Lopes MA Santos JD et al In vivo performance ofbiodegradable calcium phosphate glass ceramics using the rabbitmodel histological and SEM observation J Biomater Appl 200620 253ndash266

79 Lee JH Lee CK Chang BS et al In vivo study of novel biodegrad-able and osteoconductive CaO-SiO2-B2O3 glass-ceramics JBiomed Mater Res 2006 77A 362ndash369

80 Song G Song S A possible biodegradable magnesium implant ma-terial Adv Eng Mater 2007 9 298ndash302

81 Kim WC Kim JG Lee JY et al Influence of Ca on the corrosionproperties of magnesium for biomaterials Mater Lett 2008 624146ndash4148

82 Li Z Gu X Lou S et al The development of binary Mg-Ca alloysfor use as biodegradablematerials within bone Biomaterials 200829 1329ndash1344

83 Wan Y Xiong G Luo H et al Preparation and characterization ofa new biomedical magnesium-calcium alloy Mater Des 2008 292034ndash2037

84 Seong JW Kim WJ Development of biodegradable Mg-Ca alloysheets with enhanced strength and corrosion properties throughthe refinement anduniformdispersion of theMg2Caphase by high-ratio differential speed rolling Acta Biomater 2015 11 531ndash542

85 Zhang S Li J Song Y et al In vitro degradation hemolysis andMC3T3-E1 cell adhesion of biodegradable Mg-Zn alloy Mater SciEng-C 2009 29 1907ndash1912

86 Li J Song Y Zhang S et al In vitro responses of human bone mar-row stromal cells to a fluoridated hydroxyapatite coated biodegrad-able Mg-Zn alloy Biomaterials 2010 31 5782ndash5788

87 Brar HS Wong J Manuel MV Investigation of the mechanical anddegradation properties of Mg-Sr and Mg-Zn-Sr alloys for use aspotential biodegradable implant materials J Mech Behav BiomedMater 2012 7 87ndash95

88 Bornapour M Muja N Shum-Tim D et al Biocompatibility andbiodegradability of Mg-Sr alloys the formation of Sr-substitutedhydroxyapatite Acta Biomater 2013 9 5319ndash5330

89 Gu XN Xie XH Li N et al In vitro and in vivo studies on aMg-Sr binary alloy system developed as a new kind of biodegrad-able metal Acta Biomater 2012 8 2360ndash2374

90 Haumlnzi AC Gerber I Schinhammer M et al On the in vitro andin vivo degradation performance and biological response of newbiodegradableMg-Y-Zn alloys Acta Biomater 2010 6 1824ndash1833

91 Chou DT Hong D Saha P et al In vitro and in vivo corrosioncytocompatibility and mechanical properties of biodegradableMg-Y-Ca-Zr alloys as implant materials Acta Biomater 2013 98518ndash8533

92 Zong Y Yuan G Zhang X et al Comparison of biodegradable be-haviors of AZ31 and Mg-Nd-Zn-Zr alloys in Hanks physiologicalsolution Mater Sci Eng-B 2012 177 395ndash401

93 Tie D Feyerabend FMuumlllerWD et al Antibacterial biodegradableMg-Ag alloys Eur Cell Mater 2013 25 284ndash298

94 VojtěchDKubaacutesek J Seraacutek J et al Mechanical and corrosion prop-

13 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

erties of newly developed biodegradable Zn-based alloys for bonefixation Acta Biomater 2011 7 3515ndash3522

95 Li H Yang H Zheng Y et al Design and characterizations of novelbiodegradable ternary Zn-based alloys with IIA nutrient alloyingelements Mg Ca and Sr Mater Des 2015 83 95ndash102

96 Liu X Sun J Yang Y et al Microstructure mechanical proper-ties in vitro degradation behavior and hemocompatibility of novelZn-Mg-Sr alloys as biodegradable metals Mater Lett 2016 162242ndash245

97 Wu C Qiu H Hu X et al Short-term safety and efficacy of thebiodegradable iron stent in mini-swine coronary arteries ChinMed J (Engl) 2013 126 4752ndash4757

98 Purnama A Hermawan H Champetier S et al Gene expressionprofile of mouse fibroblasts exposed to a biodegradable iron alloyfor stents Acta Biomater 2013 9 8746ndash8753

99 HermawanH Purnama A Dube D et al Fe-Mn alloys for metallicbiodegradable stents degradation and cell viability studies ActaBiomater 2010 6 1852ndash1860

100 Sheridan MH Shea LD Peters MC et al Bioabsorbable polymerscaffolds for tissue engineering capable of sustained growth factordelivery J Control Release 2000 64 91ndash102

101 Shawe S Buchanan F Harkin-Jones E et al A study on the rate ofdegradation of the bioabsorbable polymer polyglycolic acid (PGA)J Mater Sci 2006 41 4832ndash4838

102 Palmerini T Biondi-Zoccai G Della Riva D et al Clinical out-comes with bioabsorbable polymer- versus durable polymer-baseddrug-eluting and bare-metal stents J Am Coll Cardiol 2014 63299ndash307

103 Tanimoto S Serruys PW Thuesen L et al Comparison of in vivoacute stent recoil between the bioabsorbable everolimus-elutingcoronary stent and the everolimus-eluting cobalt chromium coro-nary stent insights from the ABSORB and SPIRIT trials CatheterCardiovasc Interv 2007 70 515ndash523

104 Tsuji H Sasaki H Sato H et al Neuron attachment properties ofcarbon negative-ion implanted bioabsorbable polymer of poly-lac-tic acid Nucl Instr Meth Phys Res Sect B-Beam Interact MaterAtoms 2002 191 815ndash819

105 Aikawa M Miyazawa M Okamoto K et al A novel treatment forbile duct injury with a tissue-engineered bioabsorbable polymerpatch Surgery 2010 147 575ndash580

106 WaksmanR Pakala R Kuchulakanti PK et al Safety and efficacy ofbioabsorbablemagnesium alloy stents in porcine coronary arteriesCatheter Cardiovasc Interv 2006 68 607ndash617

107 Di Mario C Griffiths H Goktekin O et al Drug-eluting bioab-sorbable magnesium stent J Interv Cardiol 2004 17 391ndash395

108 Erbel R Di Mario C Bartunek J et al Temporary scaffoldingof coronary arteries with bioabsorbable magnesium stents aprospective non-randomised multicentre trial Lancet 2007 3691869ndash1875

109 Schranz D Zartner P Michel-Behnke I et al Bioabsorbable metalstents for percutaneous treatment of critical recoarctation of theaorta in a newborn Catheter Cardiovasc Interv 2006 67 671ndash673

110 Gu X Zheng Y Cheng Y et al In vitro corrosion and biocompati-bility of binary magnesium alloys Biomaterials 2009 30 484ndash498

111 Hiromoto S InoueM Taguchi T et al In vitro and in vivo biocom-patibility and corrosion behaviour of a bioabsorbable magnesiumalloy coated with octacalcium phosphate and hydroxyapatite ActaBiomater 2015 11 520ndash530

112 Hiromoto S Tomozawa M Maruyama N Fatigue property of abioabsorbable magnesium alloy with a hydroxyapatite coatingformed by a chemical solution deposition J Mech Behav Biomed-ical Mater 2013 25 1ndash10

113 Bowen PK Drelich J Goldman J Zinc exhibits ideal physiologicalcorrosion behavior for bioabsorbable stents Adv Mater 2013 252577ndash2582

114 Liu X Sun J Yang Y et al In vitro investigation of ultra-pure Znand its mini-tube as potential bioabsorbable stent material MaterLett 2015 161 53ndash56

115 LinW Zhang G Cao P et al Cytotoxicity and its test methodologyfor a bioabsorbable nitrided iron stent J Biomed Mater Res 2015103 764ndash776

116 Coe JD Vaccaro AR Instrumented transforaminal lumbar inter-body fusion with bioresorbable polymer implants and iliac crestautograft Spine 2005 30 S76ndashS83

117 Ignatius AA Augat P Ohnmacht M et al A new bioresorbablepolymer for screw augmentation in the osteosynthesis of osteo-porotic cancellous bone a biomechanical evaluation J BiomedMater Res 2001 58 254ndash260

118 Krucoff MW Kereiakes DJ Petersen JL et al A novel biore-sorbable polymer paclitaxel-eluting stent for the treatment ofsingle and multivessel coronary disease J Am Coll Cardiol 200851 1543ndash1552

119 Kostopoulos L Karring T Guided bone regeneration in mandibu-lar defects in rats using a bioresorbable polymer Clin Oral Im-plants Res 1994 5 66ndash74

120 Dubok VA Bioceramicsmdashyesterday today tomorrow PowderMetall Metal Ceram 2000 39 381ndash394

121 Safronova T Kuznetsov A Korneychuk S et al Calcium phos-phate powders synthesized from solutions with [Ca2+][PO4

3minus]=1for bioresorbable ceramics Cent Eur J Chem 2009 7 184ndash191

122 Bohner M Bioresorbable ceramics In Buchanan FJ (Ed) Degra-dation Rate of Bioresorbable Materials Cambridge WoodheadPublishing 2008 95-114

123 Seitz JM Eifler R Stahl J et al Characterization ofMgNd2 alloy forpotential applications in bioresorbable implantable devices ActaBiomater 2012 8 3852ndash3864

124 WenCE Yamada Y Shimojima K et al Porous bioresorbable mag-nesium as bone substitute MSF 2003 419ndash422 1001ndash1006

125 Campos CM Muramatsu T Iqbal J et al Bioresorbable drug-elut-ing magnesium-alloy scaffold for treatment of coronary artery dis-ease Int J Mol Sci 2013 14 24492ndash24500

126 KirklandNT Birbilis NWalker J et al In-vitro dissolution ofmag-nesium-calcium binary alloys clarifying the unique role of calciumadditions in bioresorbable magnesium implant alloys J BiomedMater Res 2010 95B 91ndash100

127 Gastaldi D Sassi V Petrini L et al Continuum damage model forbioresorbable magnesium alloy devices mdashapplication to coronarystents J Mech Behav Biomed Mater 2011 4 352ndash365

128 Kitabata H Waksman R Warnack B Bioresorbable metal scaffoldfor cardiovascular application current knowledge and future per-spectives Cardiovasc Revasc Med 2014 15 109ndash116

Acknowledgments This work was supported by the National Key Re-search and Development Program of China (2016YFC1102402) NationalNatural Science Foundation of China (NSFC 51431002) and the NSFCand the Research Grants Council (RGC) of Hong Kong Joint ResearchScheme (51361165101 and 5161101031)

Author contributions Liu Y prepared the figures tables organized thereferences and wrote the paper Zheng Y provided the overall concept andrevised the manuscript Hayes B helped with the standard developmentand revised the manuscript All authors participated in the discussion

Conflict of interest The authors declare that they have no conflict ofinterest

14copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Yang Liu received his bachelor degree in materials science and engineering from Harbin engineering University in 2013Then he continued his study as a PhD candidate in Prof Yufeng Zhengrsquos Lab in Peking University His research interestsare mainly focused on the corrosion study of absorbable metallic biomaterials as well as the development of new kind ofMg-based biomaterials

Yufeng Zheng obtained his PhD degree from Harbin Institute of Technology in 1998 He is the National OutstandingYouth and Yangtze River scholar of China His research interests are focused on the development of novel biomaterials andapplication and design of biomedical devices

Byron Hayes an over 35 year employee of WL Gore has been involved in the commercial development of multiple ab-sorbable polymeric implants since the late 1980s Hayes started his standards development activities with ASTM in 2000where he is actively developing standards for polymeric and metallic absorbable implants In 2010 Hayes also becameinvolved with ISO Technical Committees TC150 and TC194 and is now convener of working groups focused on cardiovas-cular and metallic absorbable implants

可降解可吸收再吸收mdashmdash哪个是描述最终被人体吸收生物材料的最好词汇刘洋1 郑玉峰1 拜伦海耶斯2

摘要 关于最终被人体吸收的植入材料领域内文献采用的英文修饰词长期以来混乱且不同不仅造成文献检索困难同时模糊了研究人员的研究边界 此领域在法律法规标准中统一用词的确定为领域内的科学研究产品销售及产品使用说明奠定了基础 我们基于化学生态学材料学生物学微生物学和药学立足于使用习惯法律标准和市场对领域内使用已久的典型修饰词ldquo生物可降解rdquoldquo再吸收rdquo和ldquo可吸收rdquo进行了讨论和解释 总的来说尽管目前绝大多数修饰语实际想表达的意思相同作者认为ldquo可吸收rdquo这一英文修饰语是最恰当的修饰词 同时我们提议进一步规范和统一该领域修饰词的使用

15 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

  • Degradable absorbable or resorbablemdashwhat is the best grammatical modifier for an implant that is eventually absorbed by the body
  • Abstract
  • INTRODUCTION
    • Current situation
    • Standards development in advance
      • TERMINOLOGY
        • Overview of utilization of the terms ldquodegradationrdquoldquobiodegradationrdquo and ldquodegradablerdquoldquobiodegradablerdquo
        • Overview of utilization of the terms ldquoabsorptionrdquoldquobioabsorptionrdquo and ldquoabsorbablerdquoldquobioabsorbablerdquo
        • Overview of utilization of the terms ldquoresorptionrdquoldquobioresorptionrdquo and ldquoresorbablerdquoldquobioresorbablerdquo
        • Utilization and comparison of the terms ldquobiodegradable metalsrdquo and ldquoabsorbable metallic materialsrdquo
        • Summary quantification of the common Terms
          • DISCUSSION
            • Expertise inherent biases
            • Connotation and extension of noun forms ldquobiodegradation bioabsorption and bioresorptionrdquo and adjectives ldquobiodegradable bioabsorbable and bioresorbablerdquo
              • CONCLUDING REMARKS
              • References
              • Acknowledgements

implants in sports medicine the biological base Arthroscopy-JArthroscopic Related Surgery 2000 16 305ndash321

12 Ikada Y Tsuji H Biodegradable polyesters for medical and ecolog-ical applications Macromol Rapid Commun 2000 21 117ndash132

13 Ashammakhi N Peltoniemi H Waris E et al Developments incraniomaxillofacial surgery use of self-reinforced bioabsorbableosteofixation devices Plast Reconstr Surg 2001 108 167ndash180

14 Vert M Doi Y Hellwich KH et al Terminology for biorelatedpolymers and applications (IUPACRecommendations 2012) PureAppl Chem 2012 84 377ndash410

15 The United States Pharmacopeial Convention The Second Sup-plement to the Pharmacopeia of the United States of America 11thdecennial revision (USP XI-1939 Supplement) 1939

16 Truhlsen SM The recession operation histopathologic responseand suture reaction and absorption Trans Am Ophthalmol Soc1965 63 626ndash677

17 USP in US Law httpwwwusporgprintabout-usplegal-recog-nitionusp-us-law

18 USP develops and publishes standards for drug substances drugproducts excipients and dietary supplements in the United StatesPharmacopeia-National Formulary (USP-NF)

19 United States Public Law 94-295 197620 United States Pharmacopeia httpwwwusporg21 British Pharmacopeia httpswwwpharmacopoeiacom22 European Pharmacopoeia httponlinepheurorgENentryhtm23 Williams DF The Williams Dictionary of Biomaterials Liverpool

Liverpool University Press 199924 httpsenwikipediaorgwikiBiodegradation25 Jones RG Kahovec J Stepto R et al Compendium of Polymer

Terminology and Nomenclature IUPAC Recommendations 2008Cambridge RSC Publishing 2009

26 Higashi S Yamamuro T Nakamura T et al Polymer-hydroxyap-atite composites for biodegradable bone fillers Biomaterials 19867 183ndash187

27 de Groot K Bioceramics of Calcium Phosphate Boca Raton CRCPress 1983

28 Hollinger JO Battistone GC Biodegradable bone repair materialssynthetic polymers and ceramics ClinOrthopRelat Res 1986 207290ndash306

29 ASTMD653-14 Standard Terminology Relating to Soil Rock andContained Fluids ASTM International West Conshohocken PA2014 httpswwwastmorgStandardsD653htm

30 Witte F Hort N Vogt C et al Degradable biomaterials based onmagnesium corrosion Curr Opin Solid State Mater Sci 2008 1263ndash72

31 Lynn DM Langer R Degradable poly(β-amino esters) synthesischaracterization and self-assemblywith plasmidDNA JAmChemSoc 2000 122 10761ndash10768

32 Cima LG Vacanti JP Vacanti C et al Tissue engineering by celltransplantation using degradable polymer substrates J BiomechEng 1991 113 143ndash151

33 Zhang S Zhang X Zhao C et al Research on an Mg-Zn alloy as adegradable biomaterial Acta Biomater 2010 6 626ndash640

34 Anseth KS Metters AT Bryant SJ et al In situ forming degradablenetworks and their application in tissue engineering and drug de-livery J Control Release 2002 78 199ndash209

35 Forrest ML Koerber JT Pack DW A degradable polyethyleniminederivative with low toxicity for highly efficient gene delivery Bio-conjugate Chem 2003 14 934ndash940

36 ASTM E2747-11 Standard Specification for Evaluation and Selec-tion of Onsite Offices for Environmentally Sustainable MeetingsEvents Trade Shows and Conferences ASTM International

West Conshohocken PA 2011 httpswwwastmorgStan-dardsE2747htm

37 ASTM E2745-11 Standard Specification for Evaluation andSelection of Audio Visual (AV) and Production for Environ-mentally Sustainable Meetings Events Trade Shows and Con-ferences ASTM International West Conshohocken PA 2011httpswwwastmorgStandardsE2745htm

38 ASTM E2746-11 Standard Specification for Evaluation andSelection of Communication and Marketing Materials for En-vironmentally Sustainable Meetings Events Trade Shows andConferences ASTM International West Conshohocken PA 2011httpswwwastmorgStandardsE2746htm

39 ASTM E2741-11 Standard Specification for Evaluation and Se-lection of Destinations for Environmentally Sustainable MeetingsEvents Trade Shows and Conferences ASTM InternationalWest Conshohocken PA 2011 httpswwwastmorgStan-dardsE2741htm

40 0 ASTM E2773-11 Standard Specification for Evaluation andSelection of Food and Beverage for Environmentally SustainableMeetings Events Trade Shows and Conferences ASTM Interna-tional West Conshohocken PA 2011 httpswwwastmorgStan-dardsE2773htm

41 ASTM E2742-11 Standard Specification for Evaluation and Selec-tion of Exhibits for Environmentally Sustainable Meetings EventsTrade Shows and Conferences ASTM International West Con-shohocken PA 2011 httpswwwastmorgStandardsE2742htm

42 ASTM E2774-11 Standard Specification for Evaluation and Selec-tion of Venues for Environmentally Sustainable Meetings EventsTrade Shows and Conferences ASTM International West Con-shohocken PA 2011 httpswwwastmorgStandardsE2774htm

43 ASTM F2902-12 Standard Guide for Assessment of AbsorbablePolymeric Implants ASTM International West ConshohockenPA 2012 httpswwwastmorgStandardsF2902htm

44 httpsenwikipediaorgwikiResorption45 Venes D Tabers Cyclopedic Medical Dictionary 22th edition

Philadelphia F A Davis Company 201346 Zheng YF Gu XN Witte F Biodegradable metals Mater Sci Eng-

R-Rep 2014 77 1ndash3447 Hanawa T Metal ion release from metal implants Mater Sci

Eng-C 2004 24 745ndash75248 Zreiqat H Howlett CR Zannettino A et al Mechanisms of mag-

nesium-stimulated adhesion of osteoblastic cells to commonly usedorthopaedic implants J Biomed Mater Res 2002 62 175ndash184

49 Little PJ Bhattacharya R Moreyra AE et al Zinc and cardiovascu-lar disease Nutrition 2010 26 1050ndash1057

50 Seager H Drug-delivery products and the Zydis fast-dissolvingdosage form J Pharm Pharmacol 1998 50 375ndash382

51 Shikinami Y Shape-memory biodegradable and absorbable mate-rial US Patent No 6281262 2001-8-28

52 Huitema TW Knight GW Ransick MH Schulze DR Surgical im-plant with preferential corrosion zone US Patent No 79059022011-3-15

53 Luzier WD Materials derived from biomassbiodegradable mate-rials Proc Natl Acad Sci USA 1992 89 839ndash842

54 Gross RA Kalra B Biodegradable polymers for the environmentScience 2002 297 803ndash807

55 Trumbo P Schlicker S Yates AA et al Dietary reference intakesfor energy carbohydrate fiber fat fatty acids cholesterol proteinand amino acids J Am Diet Assoc 2002 102 1621ndash1630

56 Chambin O Champion D Debray C et al Effects of different cel-lulose derivatives on drug release mechanism studied at a prefor-mulation stage J Control Release 2004 95 101ndash108

12copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

57 Fundueanu G Constantin M Esposito E et al Cellulose acetatebutyrate microcapsules containing dextran ion-exchange resinsas self-propelled drug release system Biomaterials 2005 264337ndash4347

58 Maumlrtson M Viljanto J Hurme T et al Is cellulose sponge degrad-able or stable as implantation material An in vivo subcutaneousstudy in the rat Biomaterials 1999 20 1989ndash1995

59 Patel N Padera R Sanders GH et al Spatially controlled cell en-gineering on biodegradable polymer surfaces The FASEB journal1998 12 1447ndash1454

60 Goldstein A Effect of convection on osteoblastic cell growth andfunction in biodegradable polymer foam scaffolds Biomaterials2001 22 1279ndash1288

61 Wu L Ding J In vitro degradation of three-dimensional porouspoly(DL-lactide-co-glycolide) scaffolds for tissue engineeringBiomaterials 2004 25 5821ndash5830

62 Wu L Ding J Effects of porosity and pore size on in vitro degra-dation of three-dimensional porous poly(DL-lactide-co-glycolide)scaffolds for tissue engineering J Biomed Mater Res 2005 75A767ndash777

63 Pan Z Ding J Poly(lactide-co-glycolide) porous scaffolds for tissueengineering and regenerative medicine Interface Focus 2012 2366ndash377

64 Yu L Zhang Z Zhang H et al Biodegradability and biocompati-bility of thermoreversible hydrogels formed from mixing a sol anda precipitate of block copolymers in water Biomacromolecules2010 11 2169ndash2178

65 Wen X Tresco PA Fabrication and characterization of permeabledegradable poly(DL-lactide-co-glycolide) (PLGA) hollow fiberphase inversion membranes for use as nerve tract guidance chan-nels Biomaterials 2006 27 3800ndash3809

66 Chu CFL Lu A Liszkowski M et al Enhanced growth of animaland human endothelial cells on biodegradable polymers BBA-GenSubjects 1999 1472 479ndash485

67 Jo S Engel PS Mikos AG Synthesis of poly(ethylene glycol)-teth-ered poly(propylene fumarate) and its modification with GRGDpeptide Polymer 2000 41 7595ndash7604

68 Park JH Allen MG Prausnitz MR Biodegradable polymer mi-croneedles fabrication mechanics and transdermal drug deliveryJ Control Release 2005 104 51ndash66

69 Freed LE Vunjak-Novakovic G Biron RJ et al Biodegradablepolymer scaffolds for tissue engineering Nat Biotechnol 1994 12689ndash693

70 Windecker S Serruys PW Wandel S et al Biolimus-eluting stentwith biodegradable polymer versus sirolimus-eluting stent withdurable polymer for coronary revascularisation (LEADERS) arandomised non-inferiority trial Lancet 2008 372 1163ndash1173

71 Stefanini GG Kalesan B Serruys PW et al Long-term clinicaloutcomes of biodegradable polymer biolimus-eluting stents ver-sus durable polymer sirolimus-eluting stents in patients with coro-nary artery disease (LEADERS) 4 year follow-up of a randomisednon-inferiority trial Lancet 2011 378 1940ndash1948

72 Raungaard B Jensen LO Tilsted HH et al Zotarolimus-elutingdurable-polymer-coated stent versus a biolimus-eluting biodegrad-able-polymer-coated stent in unselected patients undergoing per-cutaneous coronary intervention (SORT OUT VI) a randomisednon-inferiority trial Lancet 2015 385 1527ndash1535

73 Freed LE Grande DA Lingbin Z et al Joint resurfacing using allo-graft chondrocytes and synthetic biodegradable polymer scaffoldsJ Biomed Mater Res 1994 28 891ndash899

74 Poirier Y Nawrath C Somerville C Production of polyhydrox-yalkanoates a family of biodegradable plastics and elastomers in

bacteria and plants Nat Biotechnol 1995 13 142ndash15075 Dias A Tsuru K Hayakawa S et al Crystallisation studies of

biodegradable CaO-P2O5 glass with MgO and TiO2 for boneregeneration applications Glass Technol 2004 45 78ndash79

76 Klein CPAT de Groot K Drissen AA et al Interaction ofbiodegradable β-whitlockite ceramics with bone tissue an in vivostudy Biomaterials 1985 6 189ndash192

77 Ikenaga M Hardouin P Lemaicirctre J et al Biomechanical charac-terization of a biodegradable calcium phosphate hydraulic cementa comparison with porous biphasic calcium phosphate ceramics JBiomed Mater Res 1998 40 139ndash144

78 Dias AG Lopes MA Santos JD et al In vivo performance ofbiodegradable calcium phosphate glass ceramics using the rabbitmodel histological and SEM observation J Biomater Appl 200620 253ndash266

79 Lee JH Lee CK Chang BS et al In vivo study of novel biodegrad-able and osteoconductive CaO-SiO2-B2O3 glass-ceramics JBiomed Mater Res 2006 77A 362ndash369

80 Song G Song S A possible biodegradable magnesium implant ma-terial Adv Eng Mater 2007 9 298ndash302

81 Kim WC Kim JG Lee JY et al Influence of Ca on the corrosionproperties of magnesium for biomaterials Mater Lett 2008 624146ndash4148

82 Li Z Gu X Lou S et al The development of binary Mg-Ca alloysfor use as biodegradablematerials within bone Biomaterials 200829 1329ndash1344

83 Wan Y Xiong G Luo H et al Preparation and characterization ofa new biomedical magnesium-calcium alloy Mater Des 2008 292034ndash2037

84 Seong JW Kim WJ Development of biodegradable Mg-Ca alloysheets with enhanced strength and corrosion properties throughthe refinement anduniformdispersion of theMg2Caphase by high-ratio differential speed rolling Acta Biomater 2015 11 531ndash542

85 Zhang S Li J Song Y et al In vitro degradation hemolysis andMC3T3-E1 cell adhesion of biodegradable Mg-Zn alloy Mater SciEng-C 2009 29 1907ndash1912

86 Li J Song Y Zhang S et al In vitro responses of human bone mar-row stromal cells to a fluoridated hydroxyapatite coated biodegrad-able Mg-Zn alloy Biomaterials 2010 31 5782ndash5788

87 Brar HS Wong J Manuel MV Investigation of the mechanical anddegradation properties of Mg-Sr and Mg-Zn-Sr alloys for use aspotential biodegradable implant materials J Mech Behav BiomedMater 2012 7 87ndash95

88 Bornapour M Muja N Shum-Tim D et al Biocompatibility andbiodegradability of Mg-Sr alloys the formation of Sr-substitutedhydroxyapatite Acta Biomater 2013 9 5319ndash5330

89 Gu XN Xie XH Li N et al In vitro and in vivo studies on aMg-Sr binary alloy system developed as a new kind of biodegrad-able metal Acta Biomater 2012 8 2360ndash2374

90 Haumlnzi AC Gerber I Schinhammer M et al On the in vitro andin vivo degradation performance and biological response of newbiodegradableMg-Y-Zn alloys Acta Biomater 2010 6 1824ndash1833

91 Chou DT Hong D Saha P et al In vitro and in vivo corrosioncytocompatibility and mechanical properties of biodegradableMg-Y-Ca-Zr alloys as implant materials Acta Biomater 2013 98518ndash8533

92 Zong Y Yuan G Zhang X et al Comparison of biodegradable be-haviors of AZ31 and Mg-Nd-Zn-Zr alloys in Hanks physiologicalsolution Mater Sci Eng-B 2012 177 395ndash401

93 Tie D Feyerabend FMuumlllerWD et al Antibacterial biodegradableMg-Ag alloys Eur Cell Mater 2013 25 284ndash298

94 VojtěchDKubaacutesek J Seraacutek J et al Mechanical and corrosion prop-

13 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

erties of newly developed biodegradable Zn-based alloys for bonefixation Acta Biomater 2011 7 3515ndash3522

95 Li H Yang H Zheng Y et al Design and characterizations of novelbiodegradable ternary Zn-based alloys with IIA nutrient alloyingelements Mg Ca and Sr Mater Des 2015 83 95ndash102

96 Liu X Sun J Yang Y et al Microstructure mechanical proper-ties in vitro degradation behavior and hemocompatibility of novelZn-Mg-Sr alloys as biodegradable metals Mater Lett 2016 162242ndash245

97 Wu C Qiu H Hu X et al Short-term safety and efficacy of thebiodegradable iron stent in mini-swine coronary arteries ChinMed J (Engl) 2013 126 4752ndash4757

98 Purnama A Hermawan H Champetier S et al Gene expressionprofile of mouse fibroblasts exposed to a biodegradable iron alloyfor stents Acta Biomater 2013 9 8746ndash8753

99 HermawanH Purnama A Dube D et al Fe-Mn alloys for metallicbiodegradable stents degradation and cell viability studies ActaBiomater 2010 6 1852ndash1860

100 Sheridan MH Shea LD Peters MC et al Bioabsorbable polymerscaffolds for tissue engineering capable of sustained growth factordelivery J Control Release 2000 64 91ndash102

101 Shawe S Buchanan F Harkin-Jones E et al A study on the rate ofdegradation of the bioabsorbable polymer polyglycolic acid (PGA)J Mater Sci 2006 41 4832ndash4838

102 Palmerini T Biondi-Zoccai G Della Riva D et al Clinical out-comes with bioabsorbable polymer- versus durable polymer-baseddrug-eluting and bare-metal stents J Am Coll Cardiol 2014 63299ndash307

103 Tanimoto S Serruys PW Thuesen L et al Comparison of in vivoacute stent recoil between the bioabsorbable everolimus-elutingcoronary stent and the everolimus-eluting cobalt chromium coro-nary stent insights from the ABSORB and SPIRIT trials CatheterCardiovasc Interv 2007 70 515ndash523

104 Tsuji H Sasaki H Sato H et al Neuron attachment properties ofcarbon negative-ion implanted bioabsorbable polymer of poly-lac-tic acid Nucl Instr Meth Phys Res Sect B-Beam Interact MaterAtoms 2002 191 815ndash819

105 Aikawa M Miyazawa M Okamoto K et al A novel treatment forbile duct injury with a tissue-engineered bioabsorbable polymerpatch Surgery 2010 147 575ndash580

106 WaksmanR Pakala R Kuchulakanti PK et al Safety and efficacy ofbioabsorbablemagnesium alloy stents in porcine coronary arteriesCatheter Cardiovasc Interv 2006 68 607ndash617

107 Di Mario C Griffiths H Goktekin O et al Drug-eluting bioab-sorbable magnesium stent J Interv Cardiol 2004 17 391ndash395

108 Erbel R Di Mario C Bartunek J et al Temporary scaffoldingof coronary arteries with bioabsorbable magnesium stents aprospective non-randomised multicentre trial Lancet 2007 3691869ndash1875

109 Schranz D Zartner P Michel-Behnke I et al Bioabsorbable metalstents for percutaneous treatment of critical recoarctation of theaorta in a newborn Catheter Cardiovasc Interv 2006 67 671ndash673

110 Gu X Zheng Y Cheng Y et al In vitro corrosion and biocompati-bility of binary magnesium alloys Biomaterials 2009 30 484ndash498

111 Hiromoto S InoueM Taguchi T et al In vitro and in vivo biocom-patibility and corrosion behaviour of a bioabsorbable magnesiumalloy coated with octacalcium phosphate and hydroxyapatite ActaBiomater 2015 11 520ndash530

112 Hiromoto S Tomozawa M Maruyama N Fatigue property of abioabsorbable magnesium alloy with a hydroxyapatite coatingformed by a chemical solution deposition J Mech Behav Biomed-ical Mater 2013 25 1ndash10

113 Bowen PK Drelich J Goldman J Zinc exhibits ideal physiologicalcorrosion behavior for bioabsorbable stents Adv Mater 2013 252577ndash2582

114 Liu X Sun J Yang Y et al In vitro investigation of ultra-pure Znand its mini-tube as potential bioabsorbable stent material MaterLett 2015 161 53ndash56

115 LinW Zhang G Cao P et al Cytotoxicity and its test methodologyfor a bioabsorbable nitrided iron stent J Biomed Mater Res 2015103 764ndash776

116 Coe JD Vaccaro AR Instrumented transforaminal lumbar inter-body fusion with bioresorbable polymer implants and iliac crestautograft Spine 2005 30 S76ndashS83

117 Ignatius AA Augat P Ohnmacht M et al A new bioresorbablepolymer for screw augmentation in the osteosynthesis of osteo-porotic cancellous bone a biomechanical evaluation J BiomedMater Res 2001 58 254ndash260

118 Krucoff MW Kereiakes DJ Petersen JL et al A novel biore-sorbable polymer paclitaxel-eluting stent for the treatment ofsingle and multivessel coronary disease J Am Coll Cardiol 200851 1543ndash1552

119 Kostopoulos L Karring T Guided bone regeneration in mandibu-lar defects in rats using a bioresorbable polymer Clin Oral Im-plants Res 1994 5 66ndash74

120 Dubok VA Bioceramicsmdashyesterday today tomorrow PowderMetall Metal Ceram 2000 39 381ndash394

121 Safronova T Kuznetsov A Korneychuk S et al Calcium phos-phate powders synthesized from solutions with [Ca2+][PO4

3minus]=1for bioresorbable ceramics Cent Eur J Chem 2009 7 184ndash191

122 Bohner M Bioresorbable ceramics In Buchanan FJ (Ed) Degra-dation Rate of Bioresorbable Materials Cambridge WoodheadPublishing 2008 95-114

123 Seitz JM Eifler R Stahl J et al Characterization ofMgNd2 alloy forpotential applications in bioresorbable implantable devices ActaBiomater 2012 8 3852ndash3864

124 WenCE Yamada Y Shimojima K et al Porous bioresorbable mag-nesium as bone substitute MSF 2003 419ndash422 1001ndash1006

125 Campos CM Muramatsu T Iqbal J et al Bioresorbable drug-elut-ing magnesium-alloy scaffold for treatment of coronary artery dis-ease Int J Mol Sci 2013 14 24492ndash24500

126 KirklandNT Birbilis NWalker J et al In-vitro dissolution ofmag-nesium-calcium binary alloys clarifying the unique role of calciumadditions in bioresorbable magnesium implant alloys J BiomedMater Res 2010 95B 91ndash100

127 Gastaldi D Sassi V Petrini L et al Continuum damage model forbioresorbable magnesium alloy devices mdashapplication to coronarystents J Mech Behav Biomed Mater 2011 4 352ndash365

128 Kitabata H Waksman R Warnack B Bioresorbable metal scaffoldfor cardiovascular application current knowledge and future per-spectives Cardiovasc Revasc Med 2014 15 109ndash116

Acknowledgments This work was supported by the National Key Re-search and Development Program of China (2016YFC1102402) NationalNatural Science Foundation of China (NSFC 51431002) and the NSFCand the Research Grants Council (RGC) of Hong Kong Joint ResearchScheme (51361165101 and 5161101031)

Author contributions Liu Y prepared the figures tables organized thereferences and wrote the paper Zheng Y provided the overall concept andrevised the manuscript Hayes B helped with the standard developmentand revised the manuscript All authors participated in the discussion

Conflict of interest The authors declare that they have no conflict ofinterest

14copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Yang Liu received his bachelor degree in materials science and engineering from Harbin engineering University in 2013Then he continued his study as a PhD candidate in Prof Yufeng Zhengrsquos Lab in Peking University His research interestsare mainly focused on the corrosion study of absorbable metallic biomaterials as well as the development of new kind ofMg-based biomaterials

Yufeng Zheng obtained his PhD degree from Harbin Institute of Technology in 1998 He is the National OutstandingYouth and Yangtze River scholar of China His research interests are focused on the development of novel biomaterials andapplication and design of biomedical devices

Byron Hayes an over 35 year employee of WL Gore has been involved in the commercial development of multiple ab-sorbable polymeric implants since the late 1980s Hayes started his standards development activities with ASTM in 2000where he is actively developing standards for polymeric and metallic absorbable implants In 2010 Hayes also becameinvolved with ISO Technical Committees TC150 and TC194 and is now convener of working groups focused on cardiovas-cular and metallic absorbable implants

可降解可吸收再吸收mdashmdash哪个是描述最终被人体吸收生物材料的最好词汇刘洋1 郑玉峰1 拜伦海耶斯2

摘要 关于最终被人体吸收的植入材料领域内文献采用的英文修饰词长期以来混乱且不同不仅造成文献检索困难同时模糊了研究人员的研究边界 此领域在法律法规标准中统一用词的确定为领域内的科学研究产品销售及产品使用说明奠定了基础 我们基于化学生态学材料学生物学微生物学和药学立足于使用习惯法律标准和市场对领域内使用已久的典型修饰词ldquo生物可降解rdquoldquo再吸收rdquo和ldquo可吸收rdquo进行了讨论和解释 总的来说尽管目前绝大多数修饰语实际想表达的意思相同作者认为ldquo可吸收rdquo这一英文修饰语是最恰当的修饰词 同时我们提议进一步规范和统一该领域修饰词的使用

15 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

  • Degradable absorbable or resorbablemdashwhat is the best grammatical modifier for an implant that is eventually absorbed by the body
  • Abstract
  • INTRODUCTION
    • Current situation
    • Standards development in advance
      • TERMINOLOGY
        • Overview of utilization of the terms ldquodegradationrdquoldquobiodegradationrdquo and ldquodegradablerdquoldquobiodegradablerdquo
        • Overview of utilization of the terms ldquoabsorptionrdquoldquobioabsorptionrdquo and ldquoabsorbablerdquoldquobioabsorbablerdquo
        • Overview of utilization of the terms ldquoresorptionrdquoldquobioresorptionrdquo and ldquoresorbablerdquoldquobioresorbablerdquo
        • Utilization and comparison of the terms ldquobiodegradable metalsrdquo and ldquoabsorbable metallic materialsrdquo
        • Summary quantification of the common Terms
          • DISCUSSION
            • Expertise inherent biases
            • Connotation and extension of noun forms ldquobiodegradation bioabsorption and bioresorptionrdquo and adjectives ldquobiodegradable bioabsorbable and bioresorbablerdquo
              • CONCLUDING REMARKS
              • References
              • Acknowledgements

57 Fundueanu G Constantin M Esposito E et al Cellulose acetatebutyrate microcapsules containing dextran ion-exchange resinsas self-propelled drug release system Biomaterials 2005 264337ndash4347

58 Maumlrtson M Viljanto J Hurme T et al Is cellulose sponge degrad-able or stable as implantation material An in vivo subcutaneousstudy in the rat Biomaterials 1999 20 1989ndash1995

59 Patel N Padera R Sanders GH et al Spatially controlled cell en-gineering on biodegradable polymer surfaces The FASEB journal1998 12 1447ndash1454

60 Goldstein A Effect of convection on osteoblastic cell growth andfunction in biodegradable polymer foam scaffolds Biomaterials2001 22 1279ndash1288

61 Wu L Ding J In vitro degradation of three-dimensional porouspoly(DL-lactide-co-glycolide) scaffolds for tissue engineeringBiomaterials 2004 25 5821ndash5830

62 Wu L Ding J Effects of porosity and pore size on in vitro degra-dation of three-dimensional porous poly(DL-lactide-co-glycolide)scaffolds for tissue engineering J Biomed Mater Res 2005 75A767ndash777

63 Pan Z Ding J Poly(lactide-co-glycolide) porous scaffolds for tissueengineering and regenerative medicine Interface Focus 2012 2366ndash377

64 Yu L Zhang Z Zhang H et al Biodegradability and biocompati-bility of thermoreversible hydrogels formed from mixing a sol anda precipitate of block copolymers in water Biomacromolecules2010 11 2169ndash2178

65 Wen X Tresco PA Fabrication and characterization of permeabledegradable poly(DL-lactide-co-glycolide) (PLGA) hollow fiberphase inversion membranes for use as nerve tract guidance chan-nels Biomaterials 2006 27 3800ndash3809

66 Chu CFL Lu A Liszkowski M et al Enhanced growth of animaland human endothelial cells on biodegradable polymers BBA-GenSubjects 1999 1472 479ndash485

67 Jo S Engel PS Mikos AG Synthesis of poly(ethylene glycol)-teth-ered poly(propylene fumarate) and its modification with GRGDpeptide Polymer 2000 41 7595ndash7604

68 Park JH Allen MG Prausnitz MR Biodegradable polymer mi-croneedles fabrication mechanics and transdermal drug deliveryJ Control Release 2005 104 51ndash66

69 Freed LE Vunjak-Novakovic G Biron RJ et al Biodegradablepolymer scaffolds for tissue engineering Nat Biotechnol 1994 12689ndash693

70 Windecker S Serruys PW Wandel S et al Biolimus-eluting stentwith biodegradable polymer versus sirolimus-eluting stent withdurable polymer for coronary revascularisation (LEADERS) arandomised non-inferiority trial Lancet 2008 372 1163ndash1173

71 Stefanini GG Kalesan B Serruys PW et al Long-term clinicaloutcomes of biodegradable polymer biolimus-eluting stents ver-sus durable polymer sirolimus-eluting stents in patients with coro-nary artery disease (LEADERS) 4 year follow-up of a randomisednon-inferiority trial Lancet 2011 378 1940ndash1948

72 Raungaard B Jensen LO Tilsted HH et al Zotarolimus-elutingdurable-polymer-coated stent versus a biolimus-eluting biodegrad-able-polymer-coated stent in unselected patients undergoing per-cutaneous coronary intervention (SORT OUT VI) a randomisednon-inferiority trial Lancet 2015 385 1527ndash1535

73 Freed LE Grande DA Lingbin Z et al Joint resurfacing using allo-graft chondrocytes and synthetic biodegradable polymer scaffoldsJ Biomed Mater Res 1994 28 891ndash899

74 Poirier Y Nawrath C Somerville C Production of polyhydrox-yalkanoates a family of biodegradable plastics and elastomers in

bacteria and plants Nat Biotechnol 1995 13 142ndash15075 Dias A Tsuru K Hayakawa S et al Crystallisation studies of

biodegradable CaO-P2O5 glass with MgO and TiO2 for boneregeneration applications Glass Technol 2004 45 78ndash79

76 Klein CPAT de Groot K Drissen AA et al Interaction ofbiodegradable β-whitlockite ceramics with bone tissue an in vivostudy Biomaterials 1985 6 189ndash192

77 Ikenaga M Hardouin P Lemaicirctre J et al Biomechanical charac-terization of a biodegradable calcium phosphate hydraulic cementa comparison with porous biphasic calcium phosphate ceramics JBiomed Mater Res 1998 40 139ndash144

78 Dias AG Lopes MA Santos JD et al In vivo performance ofbiodegradable calcium phosphate glass ceramics using the rabbitmodel histological and SEM observation J Biomater Appl 200620 253ndash266

79 Lee JH Lee CK Chang BS et al In vivo study of novel biodegrad-able and osteoconductive CaO-SiO2-B2O3 glass-ceramics JBiomed Mater Res 2006 77A 362ndash369

80 Song G Song S A possible biodegradable magnesium implant ma-terial Adv Eng Mater 2007 9 298ndash302

81 Kim WC Kim JG Lee JY et al Influence of Ca on the corrosionproperties of magnesium for biomaterials Mater Lett 2008 624146ndash4148

82 Li Z Gu X Lou S et al The development of binary Mg-Ca alloysfor use as biodegradablematerials within bone Biomaterials 200829 1329ndash1344

83 Wan Y Xiong G Luo H et al Preparation and characterization ofa new biomedical magnesium-calcium alloy Mater Des 2008 292034ndash2037

84 Seong JW Kim WJ Development of biodegradable Mg-Ca alloysheets with enhanced strength and corrosion properties throughthe refinement anduniformdispersion of theMg2Caphase by high-ratio differential speed rolling Acta Biomater 2015 11 531ndash542

85 Zhang S Li J Song Y et al In vitro degradation hemolysis andMC3T3-E1 cell adhesion of biodegradable Mg-Zn alloy Mater SciEng-C 2009 29 1907ndash1912

86 Li J Song Y Zhang S et al In vitro responses of human bone mar-row stromal cells to a fluoridated hydroxyapatite coated biodegrad-able Mg-Zn alloy Biomaterials 2010 31 5782ndash5788

87 Brar HS Wong J Manuel MV Investigation of the mechanical anddegradation properties of Mg-Sr and Mg-Zn-Sr alloys for use aspotential biodegradable implant materials J Mech Behav BiomedMater 2012 7 87ndash95

88 Bornapour M Muja N Shum-Tim D et al Biocompatibility andbiodegradability of Mg-Sr alloys the formation of Sr-substitutedhydroxyapatite Acta Biomater 2013 9 5319ndash5330

89 Gu XN Xie XH Li N et al In vitro and in vivo studies on aMg-Sr binary alloy system developed as a new kind of biodegrad-able metal Acta Biomater 2012 8 2360ndash2374

90 Haumlnzi AC Gerber I Schinhammer M et al On the in vitro andin vivo degradation performance and biological response of newbiodegradableMg-Y-Zn alloys Acta Biomater 2010 6 1824ndash1833

91 Chou DT Hong D Saha P et al In vitro and in vivo corrosioncytocompatibility and mechanical properties of biodegradableMg-Y-Ca-Zr alloys as implant materials Acta Biomater 2013 98518ndash8533

92 Zong Y Yuan G Zhang X et al Comparison of biodegradable be-haviors of AZ31 and Mg-Nd-Zn-Zr alloys in Hanks physiologicalsolution Mater Sci Eng-B 2012 177 395ndash401

93 Tie D Feyerabend FMuumlllerWD et al Antibacterial biodegradableMg-Ag alloys Eur Cell Mater 2013 25 284ndash298

94 VojtěchDKubaacutesek J Seraacutek J et al Mechanical and corrosion prop-

13 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

erties of newly developed biodegradable Zn-based alloys for bonefixation Acta Biomater 2011 7 3515ndash3522

95 Li H Yang H Zheng Y et al Design and characterizations of novelbiodegradable ternary Zn-based alloys with IIA nutrient alloyingelements Mg Ca and Sr Mater Des 2015 83 95ndash102

96 Liu X Sun J Yang Y et al Microstructure mechanical proper-ties in vitro degradation behavior and hemocompatibility of novelZn-Mg-Sr alloys as biodegradable metals Mater Lett 2016 162242ndash245

97 Wu C Qiu H Hu X et al Short-term safety and efficacy of thebiodegradable iron stent in mini-swine coronary arteries ChinMed J (Engl) 2013 126 4752ndash4757

98 Purnama A Hermawan H Champetier S et al Gene expressionprofile of mouse fibroblasts exposed to a biodegradable iron alloyfor stents Acta Biomater 2013 9 8746ndash8753

99 HermawanH Purnama A Dube D et al Fe-Mn alloys for metallicbiodegradable stents degradation and cell viability studies ActaBiomater 2010 6 1852ndash1860

100 Sheridan MH Shea LD Peters MC et al Bioabsorbable polymerscaffolds for tissue engineering capable of sustained growth factordelivery J Control Release 2000 64 91ndash102

101 Shawe S Buchanan F Harkin-Jones E et al A study on the rate ofdegradation of the bioabsorbable polymer polyglycolic acid (PGA)J Mater Sci 2006 41 4832ndash4838

102 Palmerini T Biondi-Zoccai G Della Riva D et al Clinical out-comes with bioabsorbable polymer- versus durable polymer-baseddrug-eluting and bare-metal stents J Am Coll Cardiol 2014 63299ndash307

103 Tanimoto S Serruys PW Thuesen L et al Comparison of in vivoacute stent recoil between the bioabsorbable everolimus-elutingcoronary stent and the everolimus-eluting cobalt chromium coro-nary stent insights from the ABSORB and SPIRIT trials CatheterCardiovasc Interv 2007 70 515ndash523

104 Tsuji H Sasaki H Sato H et al Neuron attachment properties ofcarbon negative-ion implanted bioabsorbable polymer of poly-lac-tic acid Nucl Instr Meth Phys Res Sect B-Beam Interact MaterAtoms 2002 191 815ndash819

105 Aikawa M Miyazawa M Okamoto K et al A novel treatment forbile duct injury with a tissue-engineered bioabsorbable polymerpatch Surgery 2010 147 575ndash580

106 WaksmanR Pakala R Kuchulakanti PK et al Safety and efficacy ofbioabsorbablemagnesium alloy stents in porcine coronary arteriesCatheter Cardiovasc Interv 2006 68 607ndash617

107 Di Mario C Griffiths H Goktekin O et al Drug-eluting bioab-sorbable magnesium stent J Interv Cardiol 2004 17 391ndash395

108 Erbel R Di Mario C Bartunek J et al Temporary scaffoldingof coronary arteries with bioabsorbable magnesium stents aprospective non-randomised multicentre trial Lancet 2007 3691869ndash1875

109 Schranz D Zartner P Michel-Behnke I et al Bioabsorbable metalstents for percutaneous treatment of critical recoarctation of theaorta in a newborn Catheter Cardiovasc Interv 2006 67 671ndash673

110 Gu X Zheng Y Cheng Y et al In vitro corrosion and biocompati-bility of binary magnesium alloys Biomaterials 2009 30 484ndash498

111 Hiromoto S InoueM Taguchi T et al In vitro and in vivo biocom-patibility and corrosion behaviour of a bioabsorbable magnesiumalloy coated with octacalcium phosphate and hydroxyapatite ActaBiomater 2015 11 520ndash530

112 Hiromoto S Tomozawa M Maruyama N Fatigue property of abioabsorbable magnesium alloy with a hydroxyapatite coatingformed by a chemical solution deposition J Mech Behav Biomed-ical Mater 2013 25 1ndash10

113 Bowen PK Drelich J Goldman J Zinc exhibits ideal physiologicalcorrosion behavior for bioabsorbable stents Adv Mater 2013 252577ndash2582

114 Liu X Sun J Yang Y et al In vitro investigation of ultra-pure Znand its mini-tube as potential bioabsorbable stent material MaterLett 2015 161 53ndash56

115 LinW Zhang G Cao P et al Cytotoxicity and its test methodologyfor a bioabsorbable nitrided iron stent J Biomed Mater Res 2015103 764ndash776

116 Coe JD Vaccaro AR Instrumented transforaminal lumbar inter-body fusion with bioresorbable polymer implants and iliac crestautograft Spine 2005 30 S76ndashS83

117 Ignatius AA Augat P Ohnmacht M et al A new bioresorbablepolymer for screw augmentation in the osteosynthesis of osteo-porotic cancellous bone a biomechanical evaluation J BiomedMater Res 2001 58 254ndash260

118 Krucoff MW Kereiakes DJ Petersen JL et al A novel biore-sorbable polymer paclitaxel-eluting stent for the treatment ofsingle and multivessel coronary disease J Am Coll Cardiol 200851 1543ndash1552

119 Kostopoulos L Karring T Guided bone regeneration in mandibu-lar defects in rats using a bioresorbable polymer Clin Oral Im-plants Res 1994 5 66ndash74

120 Dubok VA Bioceramicsmdashyesterday today tomorrow PowderMetall Metal Ceram 2000 39 381ndash394

121 Safronova T Kuznetsov A Korneychuk S et al Calcium phos-phate powders synthesized from solutions with [Ca2+][PO4

3minus]=1for bioresorbable ceramics Cent Eur J Chem 2009 7 184ndash191

122 Bohner M Bioresorbable ceramics In Buchanan FJ (Ed) Degra-dation Rate of Bioresorbable Materials Cambridge WoodheadPublishing 2008 95-114

123 Seitz JM Eifler R Stahl J et al Characterization ofMgNd2 alloy forpotential applications in bioresorbable implantable devices ActaBiomater 2012 8 3852ndash3864

124 WenCE Yamada Y Shimojima K et al Porous bioresorbable mag-nesium as bone substitute MSF 2003 419ndash422 1001ndash1006

125 Campos CM Muramatsu T Iqbal J et al Bioresorbable drug-elut-ing magnesium-alloy scaffold for treatment of coronary artery dis-ease Int J Mol Sci 2013 14 24492ndash24500

126 KirklandNT Birbilis NWalker J et al In-vitro dissolution ofmag-nesium-calcium binary alloys clarifying the unique role of calciumadditions in bioresorbable magnesium implant alloys J BiomedMater Res 2010 95B 91ndash100

127 Gastaldi D Sassi V Petrini L et al Continuum damage model forbioresorbable magnesium alloy devices mdashapplication to coronarystents J Mech Behav Biomed Mater 2011 4 352ndash365

128 Kitabata H Waksman R Warnack B Bioresorbable metal scaffoldfor cardiovascular application current knowledge and future per-spectives Cardiovasc Revasc Med 2014 15 109ndash116

Acknowledgments This work was supported by the National Key Re-search and Development Program of China (2016YFC1102402) NationalNatural Science Foundation of China (NSFC 51431002) and the NSFCand the Research Grants Council (RGC) of Hong Kong Joint ResearchScheme (51361165101 and 5161101031)

Author contributions Liu Y prepared the figures tables organized thereferences and wrote the paper Zheng Y provided the overall concept andrevised the manuscript Hayes B helped with the standard developmentand revised the manuscript All authors participated in the discussion

Conflict of interest The authors declare that they have no conflict ofinterest

14copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Yang Liu received his bachelor degree in materials science and engineering from Harbin engineering University in 2013Then he continued his study as a PhD candidate in Prof Yufeng Zhengrsquos Lab in Peking University His research interestsare mainly focused on the corrosion study of absorbable metallic biomaterials as well as the development of new kind ofMg-based biomaterials

Yufeng Zheng obtained his PhD degree from Harbin Institute of Technology in 1998 He is the National OutstandingYouth and Yangtze River scholar of China His research interests are focused on the development of novel biomaterials andapplication and design of biomedical devices

Byron Hayes an over 35 year employee of WL Gore has been involved in the commercial development of multiple ab-sorbable polymeric implants since the late 1980s Hayes started his standards development activities with ASTM in 2000where he is actively developing standards for polymeric and metallic absorbable implants In 2010 Hayes also becameinvolved with ISO Technical Committees TC150 and TC194 and is now convener of working groups focused on cardiovas-cular and metallic absorbable implants

可降解可吸收再吸收mdashmdash哪个是描述最终被人体吸收生物材料的最好词汇刘洋1 郑玉峰1 拜伦海耶斯2

摘要 关于最终被人体吸收的植入材料领域内文献采用的英文修饰词长期以来混乱且不同不仅造成文献检索困难同时模糊了研究人员的研究边界 此领域在法律法规标准中统一用词的确定为领域内的科学研究产品销售及产品使用说明奠定了基础 我们基于化学生态学材料学生物学微生物学和药学立足于使用习惯法律标准和市场对领域内使用已久的典型修饰词ldquo生物可降解rdquoldquo再吸收rdquo和ldquo可吸收rdquo进行了讨论和解释 总的来说尽管目前绝大多数修饰语实际想表达的意思相同作者认为ldquo可吸收rdquo这一英文修饰语是最恰当的修饰词 同时我们提议进一步规范和统一该领域修饰词的使用

15 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

  • Degradable absorbable or resorbablemdashwhat is the best grammatical modifier for an implant that is eventually absorbed by the body
  • Abstract
  • INTRODUCTION
    • Current situation
    • Standards development in advance
      • TERMINOLOGY
        • Overview of utilization of the terms ldquodegradationrdquoldquobiodegradationrdquo and ldquodegradablerdquoldquobiodegradablerdquo
        • Overview of utilization of the terms ldquoabsorptionrdquoldquobioabsorptionrdquo and ldquoabsorbablerdquoldquobioabsorbablerdquo
        • Overview of utilization of the terms ldquoresorptionrdquoldquobioresorptionrdquo and ldquoresorbablerdquoldquobioresorbablerdquo
        • Utilization and comparison of the terms ldquobiodegradable metalsrdquo and ldquoabsorbable metallic materialsrdquo
        • Summary quantification of the common Terms
          • DISCUSSION
            • Expertise inherent biases
            • Connotation and extension of noun forms ldquobiodegradation bioabsorption and bioresorptionrdquo and adjectives ldquobiodegradable bioabsorbable and bioresorbablerdquo
              • CONCLUDING REMARKS
              • References
              • Acknowledgements

erties of newly developed biodegradable Zn-based alloys for bonefixation Acta Biomater 2011 7 3515ndash3522

95 Li H Yang H Zheng Y et al Design and characterizations of novelbiodegradable ternary Zn-based alloys with IIA nutrient alloyingelements Mg Ca and Sr Mater Des 2015 83 95ndash102

96 Liu X Sun J Yang Y et al Microstructure mechanical proper-ties in vitro degradation behavior and hemocompatibility of novelZn-Mg-Sr alloys as biodegradable metals Mater Lett 2016 162242ndash245

97 Wu C Qiu H Hu X et al Short-term safety and efficacy of thebiodegradable iron stent in mini-swine coronary arteries ChinMed J (Engl) 2013 126 4752ndash4757

98 Purnama A Hermawan H Champetier S et al Gene expressionprofile of mouse fibroblasts exposed to a biodegradable iron alloyfor stents Acta Biomater 2013 9 8746ndash8753

99 HermawanH Purnama A Dube D et al Fe-Mn alloys for metallicbiodegradable stents degradation and cell viability studies ActaBiomater 2010 6 1852ndash1860

100 Sheridan MH Shea LD Peters MC et al Bioabsorbable polymerscaffolds for tissue engineering capable of sustained growth factordelivery J Control Release 2000 64 91ndash102

101 Shawe S Buchanan F Harkin-Jones E et al A study on the rate ofdegradation of the bioabsorbable polymer polyglycolic acid (PGA)J Mater Sci 2006 41 4832ndash4838

102 Palmerini T Biondi-Zoccai G Della Riva D et al Clinical out-comes with bioabsorbable polymer- versus durable polymer-baseddrug-eluting and bare-metal stents J Am Coll Cardiol 2014 63299ndash307

103 Tanimoto S Serruys PW Thuesen L et al Comparison of in vivoacute stent recoil between the bioabsorbable everolimus-elutingcoronary stent and the everolimus-eluting cobalt chromium coro-nary stent insights from the ABSORB and SPIRIT trials CatheterCardiovasc Interv 2007 70 515ndash523

104 Tsuji H Sasaki H Sato H et al Neuron attachment properties ofcarbon negative-ion implanted bioabsorbable polymer of poly-lac-tic acid Nucl Instr Meth Phys Res Sect B-Beam Interact MaterAtoms 2002 191 815ndash819

105 Aikawa M Miyazawa M Okamoto K et al A novel treatment forbile duct injury with a tissue-engineered bioabsorbable polymerpatch Surgery 2010 147 575ndash580

106 WaksmanR Pakala R Kuchulakanti PK et al Safety and efficacy ofbioabsorbablemagnesium alloy stents in porcine coronary arteriesCatheter Cardiovasc Interv 2006 68 607ndash617

107 Di Mario C Griffiths H Goktekin O et al Drug-eluting bioab-sorbable magnesium stent J Interv Cardiol 2004 17 391ndash395

108 Erbel R Di Mario C Bartunek J et al Temporary scaffoldingof coronary arteries with bioabsorbable magnesium stents aprospective non-randomised multicentre trial Lancet 2007 3691869ndash1875

109 Schranz D Zartner P Michel-Behnke I et al Bioabsorbable metalstents for percutaneous treatment of critical recoarctation of theaorta in a newborn Catheter Cardiovasc Interv 2006 67 671ndash673

110 Gu X Zheng Y Cheng Y et al In vitro corrosion and biocompati-bility of binary magnesium alloys Biomaterials 2009 30 484ndash498

111 Hiromoto S InoueM Taguchi T et al In vitro and in vivo biocom-patibility and corrosion behaviour of a bioabsorbable magnesiumalloy coated with octacalcium phosphate and hydroxyapatite ActaBiomater 2015 11 520ndash530

112 Hiromoto S Tomozawa M Maruyama N Fatigue property of abioabsorbable magnesium alloy with a hydroxyapatite coatingformed by a chemical solution deposition J Mech Behav Biomed-ical Mater 2013 25 1ndash10

113 Bowen PK Drelich J Goldman J Zinc exhibits ideal physiologicalcorrosion behavior for bioabsorbable stents Adv Mater 2013 252577ndash2582

114 Liu X Sun J Yang Y et al In vitro investigation of ultra-pure Znand its mini-tube as potential bioabsorbable stent material MaterLett 2015 161 53ndash56

115 LinW Zhang G Cao P et al Cytotoxicity and its test methodologyfor a bioabsorbable nitrided iron stent J Biomed Mater Res 2015103 764ndash776

116 Coe JD Vaccaro AR Instrumented transforaminal lumbar inter-body fusion with bioresorbable polymer implants and iliac crestautograft Spine 2005 30 S76ndashS83

117 Ignatius AA Augat P Ohnmacht M et al A new bioresorbablepolymer for screw augmentation in the osteosynthesis of osteo-porotic cancellous bone a biomechanical evaluation J BiomedMater Res 2001 58 254ndash260

118 Krucoff MW Kereiakes DJ Petersen JL et al A novel biore-sorbable polymer paclitaxel-eluting stent for the treatment ofsingle and multivessel coronary disease J Am Coll Cardiol 200851 1543ndash1552

119 Kostopoulos L Karring T Guided bone regeneration in mandibu-lar defects in rats using a bioresorbable polymer Clin Oral Im-plants Res 1994 5 66ndash74

120 Dubok VA Bioceramicsmdashyesterday today tomorrow PowderMetall Metal Ceram 2000 39 381ndash394

121 Safronova T Kuznetsov A Korneychuk S et al Calcium phos-phate powders synthesized from solutions with [Ca2+][PO4

3minus]=1for bioresorbable ceramics Cent Eur J Chem 2009 7 184ndash191

122 Bohner M Bioresorbable ceramics In Buchanan FJ (Ed) Degra-dation Rate of Bioresorbable Materials Cambridge WoodheadPublishing 2008 95-114

123 Seitz JM Eifler R Stahl J et al Characterization ofMgNd2 alloy forpotential applications in bioresorbable implantable devices ActaBiomater 2012 8 3852ndash3864

124 WenCE Yamada Y Shimojima K et al Porous bioresorbable mag-nesium as bone substitute MSF 2003 419ndash422 1001ndash1006

125 Campos CM Muramatsu T Iqbal J et al Bioresorbable drug-elut-ing magnesium-alloy scaffold for treatment of coronary artery dis-ease Int J Mol Sci 2013 14 24492ndash24500

126 KirklandNT Birbilis NWalker J et al In-vitro dissolution ofmag-nesium-calcium binary alloys clarifying the unique role of calciumadditions in bioresorbable magnesium implant alloys J BiomedMater Res 2010 95B 91ndash100

127 Gastaldi D Sassi V Petrini L et al Continuum damage model forbioresorbable magnesium alloy devices mdashapplication to coronarystents J Mech Behav Biomed Mater 2011 4 352ndash365

128 Kitabata H Waksman R Warnack B Bioresorbable metal scaffoldfor cardiovascular application current knowledge and future per-spectives Cardiovasc Revasc Med 2014 15 109ndash116

Acknowledgments This work was supported by the National Key Re-search and Development Program of China (2016YFC1102402) NationalNatural Science Foundation of China (NSFC 51431002) and the NSFCand the Research Grants Council (RGC) of Hong Kong Joint ResearchScheme (51361165101 and 5161101031)

Author contributions Liu Y prepared the figures tables organized thereferences and wrote the paper Zheng Y provided the overall concept andrevised the manuscript Hayes B helped with the standard developmentand revised the manuscript All authors participated in the discussion

Conflict of interest The authors declare that they have no conflict ofinterest

14copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

REVIEW SCIENCE CHINA Materials

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

Yang Liu received his bachelor degree in materials science and engineering from Harbin engineering University in 2013Then he continued his study as a PhD candidate in Prof Yufeng Zhengrsquos Lab in Peking University His research interestsare mainly focused on the corrosion study of absorbable metallic biomaterials as well as the development of new kind ofMg-based biomaterials

Yufeng Zheng obtained his PhD degree from Harbin Institute of Technology in 1998 He is the National OutstandingYouth and Yangtze River scholar of China His research interests are focused on the development of novel biomaterials andapplication and design of biomedical devices

Byron Hayes an over 35 year employee of WL Gore has been involved in the commercial development of multiple ab-sorbable polymeric implants since the late 1980s Hayes started his standards development activities with ASTM in 2000where he is actively developing standards for polymeric and metallic absorbable implants In 2010 Hayes also becameinvolved with ISO Technical Committees TC150 and TC194 and is now convener of working groups focused on cardiovas-cular and metallic absorbable implants

可降解可吸收再吸收mdashmdash哪个是描述最终被人体吸收生物材料的最好词汇刘洋1 郑玉峰1 拜伦海耶斯2

摘要 关于最终被人体吸收的植入材料领域内文献采用的英文修饰词长期以来混乱且不同不仅造成文献检索困难同时模糊了研究人员的研究边界 此领域在法律法规标准中统一用词的确定为领域内的科学研究产品销售及产品使用说明奠定了基础 我们基于化学生态学材料学生物学微生物学和药学立足于使用习惯法律标准和市场对领域内使用已久的典型修饰词ldquo生物可降解rdquoldquo再吸收rdquo和ldquo可吸收rdquo进行了讨论和解释 总的来说尽管目前绝大多数修饰语实际想表达的意思相同作者认为ldquo可吸收rdquo这一英文修饰语是最恰当的修饰词 同时我们提议进一步规范和统一该领域修饰词的使用

15 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

  • Degradable absorbable or resorbablemdashwhat is the best grammatical modifier for an implant that is eventually absorbed by the body
  • Abstract
  • INTRODUCTION
    • Current situation
    • Standards development in advance
      • TERMINOLOGY
        • Overview of utilization of the terms ldquodegradationrdquoldquobiodegradationrdquo and ldquodegradablerdquoldquobiodegradablerdquo
        • Overview of utilization of the terms ldquoabsorptionrdquoldquobioabsorptionrdquo and ldquoabsorbablerdquoldquobioabsorbablerdquo
        • Overview of utilization of the terms ldquoresorptionrdquoldquobioresorptionrdquo and ldquoresorbablerdquoldquobioresorbablerdquo
        • Utilization and comparison of the terms ldquobiodegradable metalsrdquo and ldquoabsorbable metallic materialsrdquo
        • Summary quantification of the common Terms
          • DISCUSSION
            • Expertise inherent biases
            • Connotation and extension of noun forms ldquobiodegradation bioabsorption and bioresorptionrdquo and adjectives ldquobiodegradable bioabsorbable and bioresorbablerdquo
              • CONCLUDING REMARKS
              • References
              • Acknowledgements

Yang Liu received his bachelor degree in materials science and engineering from Harbin engineering University in 2013Then he continued his study as a PhD candidate in Prof Yufeng Zhengrsquos Lab in Peking University His research interestsare mainly focused on the corrosion study of absorbable metallic biomaterials as well as the development of new kind ofMg-based biomaterials

Yufeng Zheng obtained his PhD degree from Harbin Institute of Technology in 1998 He is the National OutstandingYouth and Yangtze River scholar of China His research interests are focused on the development of novel biomaterials andapplication and design of biomedical devices

Byron Hayes an over 35 year employee of WL Gore has been involved in the commercial development of multiple ab-sorbable polymeric implants since the late 1980s Hayes started his standards development activities with ASTM in 2000where he is actively developing standards for polymeric and metallic absorbable implants In 2010 Hayes also becameinvolved with ISO Technical Committees TC150 and TC194 and is now convener of working groups focused on cardiovas-cular and metallic absorbable implants

可降解可吸收再吸收mdashmdash哪个是描述最终被人体吸收生物材料的最好词汇刘洋1 郑玉峰1 拜伦海耶斯2

摘要 关于最终被人体吸收的植入材料领域内文献采用的英文修饰词长期以来混乱且不同不仅造成文献检索困难同时模糊了研究人员的研究边界 此领域在法律法规标准中统一用词的确定为领域内的科学研究产品销售及产品使用说明奠定了基础 我们基于化学生态学材料学生物学微生物学和药学立足于使用习惯法律标准和市场对领域内使用已久的典型修饰词ldquo生物可降解rdquoldquo再吸收rdquo和ldquo可吸收rdquo进行了讨论和解释 总的来说尽管目前绝大多数修饰语实际想表达的意思相同作者认为ldquo可吸收rdquo这一英文修饰语是最恰当的修饰词 同时我们提议进一步规范和统一该领域修饰词的使用

15 copy Science China Press and Springer-Verlag Berlin Heidelberg 2017

SCIENCE CHINA Materials REVIEW

Downloaded to IP 2231043888 On 2017-04-26 161110 httpenginescichinacomdoi101007s40843-017-9023-9

  • Degradable absorbable or resorbablemdashwhat is the best grammatical modifier for an implant that is eventually absorbed by the body
  • Abstract
  • INTRODUCTION
    • Current situation
    • Standards development in advance
      • TERMINOLOGY
        • Overview of utilization of the terms ldquodegradationrdquoldquobiodegradationrdquo and ldquodegradablerdquoldquobiodegradablerdquo
        • Overview of utilization of the terms ldquoabsorptionrdquoldquobioabsorptionrdquo and ldquoabsorbablerdquoldquobioabsorbablerdquo
        • Overview of utilization of the terms ldquoresorptionrdquoldquobioresorptionrdquo and ldquoresorbablerdquoldquobioresorbablerdquo
        • Utilization and comparison of the terms ldquobiodegradable metalsrdquo and ldquoabsorbable metallic materialsrdquo
        • Summary quantification of the common Terms
          • DISCUSSION
            • Expertise inherent biases
            • Connotation and extension of noun forms ldquobiodegradation bioabsorption and bioresorptionrdquo and adjectives ldquobiodegradable bioabsorbable and bioresorbablerdquo
              • CONCLUDING REMARKS
              • References
              • Acknowledgements