Histomorphological evaluation of loaded plate-form and root-form implants in Macaca mulatta monkeys

Michael McCrackenJack E. LemonsMarjorie JeffcoatDavid L. KothMichael E. Fritz

Authors’ affiliationsM. McCracken, J. E. Lemons, M. Jeffcoat,D. L. Koth, University of Alabama School ofDentistry, Birmingham, Alabama.M. E. Fritz, Yerkes Regional Primate Center,Atlanta, Georgia, USA

Correspondence to:Dr Michael McCrackenBox 49, SDB1530 3rd Ave S.Birmingham, AL 35294USATel: π1 (205) 934 1593Fax: π1 (205) 975 6108

Date:Accepted 19 March 2001

To cite this article:McCracken M, Lemons J, Jeffcoat M, Koth D, FritzM. Histomorphological evaluation of loaded plate-form and root-form implants in Macaca mulattamonkeysClin. Oral Impl. Res, 13, 2002; 214–220

Copyright C Blackwell Munksgaard 2002

ISSN 0905-7161

214

Histomorphological evaluation ofloaded plate-form and root-formimplants in Macaca mulatta monkeys

Key words: endosseous implants, primate, root-form implant, blade implant, titanium,osseointegration

Abstract: As part of a long-term evaluation of endosteal dental implants in primates, thispaper describes the histological response to plate-form and root-form implants. Thirty-sixprimates received 48 mandibular distal abutment implants. After healing, the implants wererestored with fixed partial dentures, which remained in function for two years. A subset ofthe group was ligated at the gingival sulcus to biologically stress tissues supporting theimplants. Crestal bone height around implants was quantified using digital subtractionradiographic techniques. The ligated implants lost more crestal bone than non-ligatedimplants, as shown by ANOVA (P , 0.05). After retrieval, implants were embedded andsectioned for histomorphometric analysis including measurement of per centosseointegration. Both plate-form and root-form non-ligated implants demonstrated about60% osseointegration. When ligated, plate-form implants dropped to an average integrationof only 34%, while root-form implants maintained 62% integration, a significant difference.These data show that in this primate model, plate-form and root-form implants maintainedintegration while in function for two years. When stressed with ligation, root-form implantsmaintained relative amounts of osseointegration, while per cent osseointegration of plate-form implants decreased.

Surgical reconstructive procedures withinthe musculoskeletal system have beenhighly successful in terms of restoring nor-mal anatomical form and function. End-osteal implant devices, such as dental im-plants, offer a relatively unique oppor-tunity for research because the biomaterialto tissue interface initially develops underpassive functional loading conditions.

A large and growing evidence base sug-gests that dental implants can be placedwith a high degree of predictability. Theevidence indicates that implant successafter five years approaches 95% in the an-terior mandible (Albrektsson et al. 1988;Albrektsson & Lekholm 1989; Zarb &Schmitt 1990; Saadoun & LeGall 1992).

Predictability appears to be influenced bylocation of the implant, quantity and den-sity of bone, and host factors such as load-ing and smoking (Johns et al. 1992; Wedg-wood et al. 1992; Meffert 1993; Minsket al. 1996; Jones et al. 1997).

Many of the early endosteal dental im-plants were plate-form designs. These gen-erally involved single-stage restorativetechniques and, in some situations, rela-tively uncontrolled surgical placement. Forexample, some implants were altered phys-ically by the clinician to provide implantstability in the osteotomy site. These im-plants generally functioned with a fibrousor fibro–osseous interface (Weiss 1986).

Literature reports examining these early

McCracken et al . Blade vs. plate implants in primates

blade implants are mixed. Fritz &Smithloff, in a study of single-stage bladeimplants, documented a 50% implant sur-vival rate after 15years (Smithloff & Fritz1987). In a retrospective radiographicanalysis, Telsey reported a 90% survivalrate of blade implants after five years (Tel-sey et al. 1991). Weiss has supported theuse of plate-type implants (Weiss 1988). Ka-pur reports an 86% success rate with man-dibular distal abutment plate-form im-plants at 42months in a study of patientstreated within a Veterans’ Administrationhospital (Kapur et al. 1987).

With the development of controlled sur-gical protocols and handling procedures,more recent reports indicate that plate-formimplantscanfunctionwith directbone inte-gration (Lemons 1988; Steflik et al. 1992).Since plate-form implants can be placed inareas which may not readily accommodatea root-form implant (Lemons 1987; Linkowet al. 1995), plate-form implants with abony interface could be of considerable im-portance to the overall future of implantsystems.

This paper focuses on one aspect of alongitudinal study of dental implants inprimates. The purpose of this report is tocompare the histomorphology of root-formand plate-form implants after two years ofloaded function in primates. We tested thehypothesis that endosteal implants dif-fering only in geometric design will elicitsimilar tissue reactions in Macaca mulattamonkeys.

Material and methods

To test our hypothesis, clinical radio-graphic crestal bone height and linear os-seointegration of histological specimenswere measured. Plate-form and root-formimplants were all two-stage systems; allwere loaded with fixed partial dentures. Asubgroup of implants was biologicallystressed along the periodontium with liga-tures.

Implant material and design

Titanium (cp grade II) was selected as animplant material because of its docu-mented clinical success as an implant ma-terial. Titanium exhibits an excellentstrength to weight ratio, forms a tenaciousoxide, elicits little or no inflammatory re-

215 | Clin. Oral Impl. Res. 13, 2002 / 214–220

sponse, and can be machined or coined toa variety of shapes for clinical use (Laut-enschlager & Monaghan 1993; Wataha1996).

In this study, the root-form and plate-form implants were designed to test thehost response to different geometries of im-plants. Other variables of the implants ––load-bearing area in the occluso-gingival di-rection, materials and surface character-istics –– were characterized and standard-ized.

Plate-form implants (Oratronics Inc.,New York, NY, USA) were fabricated fromunalloyed titanium (ASTM F-4 67) usingstandard coining technology. Mill stock,metallic microstructure, chemistry andsurface quality were evaluated to confirmsimilar characteristics of the root-form andplate-form implants (Kilpadi & Lemons1994; Kilpadi et al. 1998a).

Plate-form implants were 7¿12¿1.6mm in depth, length and width and in-cluded two vent openings. Plate-form im-plants were designed for initial stabilizationusing endosteal pins placed at 45 degreesthrough the superior aspect of the plate;thesepinswere removedat thesecond-stagesurgery. The dimension of the plate-formduplicated the vertical load-bearing surfacearea of the root-form implants (Kilpadi et al.1994; Kilpadi & Lemons 1994).

Plate-form implants were passivated ac-cording to ASTM standards (ASTM F-4 86).This included cleaning, submersion in30% nitric acid for 20min, and ultrasoniccleaning in deionized water. Implants werepackaged in glass containers and sterilizedusing dry heat at 400æF for 4h. Surfacechemistry and critical surface tension wereevaluated and compared to root-form im-plants to ensure consistency (Kilpadi et al.1998a, 1998b).

Root-form implants (Osseodent; Colla-gen Corporation, Palo Alto, CA, USA) werepassivated, gamma radiation sterilized, andpackaged by the manufacturer. Threadedroot-form implants were made from asingle lot shipment of unalloyed titanium(ASTM F4 67). Nominal dimensions of theimplants were 3.75¿7mm. Surface areawas determined using calibrated micro-graphs and engineering drawings. The load-bearing area of the implant was the inferiorpart of the crestal body, the underside ofthe threads and the base of the implantwhich would resist an occlusal-gingivalload. Both implant types provided a load-

bearing area of approximately 29mm2. Thecollar and abutment surfaces of both im-plant types were identical.

Animal model and study design

A detailed description of animal treatment,extractions and surgical implant placementcan be found in a previous article (Fritzet al. 1994). Sections of this protocol aresummarized below.

Thirty-six adult male Macaca mulattamonkeys were selected for the study; ani-mals were housed and maintained at theYerkes Regional Primate Research Center.Primates received dental prophylaxis oncea month, which was sufficient to preventattachment loss around natural teeth (Of-fenbacher et al. 1987; Fritz et al. 1994).Their diet consisted of water-softenedmonkey feed and soft fruit.

Each posterior segment of 36 animals (72segments) received one of three treatmentsin accordance with a randomized blockstatistical design: (1) extraction of man-dibular molars and placement of a threadedroot-form implant, (2) extraction of man-dibular molars and placement of a plate-form implant, or (3) extraction of mandibu-lar molars except for a second molar. Allsegments were restored with a full gold,high-noble, fixed partial denture. Fixed par-tial dentures supported by natural teethserved as controls.

Mandibular molars were extracted undergeneral anesthesia supplemented with lo-cal anesthesia (2% lidocaine with1 :100000 epinephrine). Postoperative anal-gesics (banamine 50mg/ml and buprenor-phine 0.3mg) and antibiotics (penicillin Gprocaine, 300000units) were also adminis-tered. Implants were placed six monthsafter extractions.

Implants were placed so that the centerof the abutment platform was 12mm dis-tal to the second premolar using standardimplant placement techniques. Plate-formimplant osteotomies were prepared with ahigh-efficiency low-speed circular saw,which did not elevate the temperature inthe bone (Koth et al. 1992).

Clinical treatment

Implants were maintained by brushing andmonthly instrumentation with plasticscalers (Noblepharma Inc., Westmont, IL,USA). Diet, healing and cleaning werestandardized according to a published pro-tocol (Eke et al. 1996).


Implants were loaded with a fixed partialdenture three months after implant place-ment. The control sites – natural teeth –also received fixed partial dentures. Pros-theses were waxed to anatomic form andcast in high-noble alloy following standarddental laboratory techniques.

Of 72 possible original sites in 36 ani-mals, 24 sites were natural teeth, 24 wereplate-form implants, and 24 were root-form implants. One root-form and fourplate-form implants failed to integrate, andone plate-form specimen was damagedduring histological preparation. After twoyears of function, 20 randomly selected im-plants were ligated with a silk suture tocreate peri-implantitis. Ligatures remainedfor six months.

Quantitative subtraction radiographictechniques were used to determine boneloss around the implants. Details of thistechnique and its application to the pri-mates can be found in previous reports ofthis primate population (Jeffcoat et al.1987, 1992; Jeffcoat & Reddy 1993; Fritzet al. 1994, 1996). Briefly, standardizedradiographs were taken at implant place-ment and at subsequent intervals deter-mined by the study protocol, using exteriorfixation of the source to object by meansof ear rods (modified cephalostat). Analuminum wedge was used as a standardreference to assess density changes withinthe bone. The baseline radiograph was di-gitized and subtracted from subsequentradiographs to isolate changes in bonemass and dimension. Also, changes in thecrestal bone height on the mesial and distalside of each implant were measured fromthe digitized images. For the purpose ofthis paper, mesial and distal measurementswere averaged to yield change in crestalbone height. Radiographic analyses will bepresented in detail in a subsequent paper.

Specimen retrieval and analysis

After two years of function, implants wereremoved en bloc from the primate man-dibles. Specimens were embedded inPMMA resin and sectioned through themiddle of the implant body in a buccoling-ual direction. Samples were attached toglass slides with cyanoacrylate cement.Using an Buehler Isomet Low Speed Sawwith a diamond blade, samples were cut toa uniform thickness and polished with a


series of abrasive papers and pastes to lessthan 40mm in thickness.

Samples were stained and counterstainedwith Sanderson’s Quick bone stain and vanGieson’s bone stain for implant-to-bone in-terfacial measurements.

Osseointegration was quantified usingthe MicroVu (Micro-Vu, Windsor, CA,USA) automated measuring system and as-sociated microcomputer. This instrumen-tation features a linear measuring accuracyof 5mm, and a repeatability of 1mm. Resol-ution is 0.5mm. The video camera has aspatial resolution of 811¿508pixels.Specimens were examined at ¿100 magni-fication. Tissue was considered osseointe-grated if there was no visible gap or fibroustissue between the bone and the adjacentimplant and no visible connective tissuebetween the bone and the implant, orwithin approximately 10mm.

Two measurements were made relativeto the percentage of biomaterial-to-bone in-tegration: (1) histological quantification ofthe amount of mineralized bone directlyadjacent to the biomaterial along the re-gion of implant-to-bone contact, and (2)radiographic measurements of bone heightrelative to the implant abutment.

Interface integration measurements

Fig.1. Per cent osseointegration of implants. The plate-form ligated group was statistically different from othergroups (P,0.001).

were made starting at the height of thecrest of bone in the specimen. It is import-ant to note that this part of the evaluationdid not account for loss of crestal boneheight when calculating the percentage oflinear osseointegration per cent. This em-phasized the specimen-specific interfacedimensions and condition of the implant,rather than the position of the implant inthe ridge. Data on crestal bone loss are pro-vided as a separate variable.

The length of bone contacting the im-plant was measured, as well as the lengthof the implant surface. The bone lengthwas divided by the implant surface lengthto yield per cent osseointegration for thesample. Measurements were repeatedthree times and averaged for a final value.

After measurements were completed,the code was revealed to identify whichimplants had been ligated. Analysis of thedata was performed using two-way ANO-VA of independent variables, Implant typeand Ligation, affecting dependent variables,Per cent osseointegration and Crestal boneloss (Statistica; Statsoft Inc., Tulsa, OK,USA). Duncan’s post hoc analysis was usedto determine between-group significance.Results were considered significant at theP,0.05 level.


Fig.2. Crestal bone loss around implants. Ligated implants lost significantly more crestal bone than non-ligatedimplants (P,0.05).

Results

The root-form group had a mean osseoin-tegration of 59%, with a range of 38–83%,while the plate-form group had a mean os-seointegration of 56% and a range of 49–69%. The root-form ligated group had amean osseointegration of 62%, with arange of 42–87%, while the plate-form lig-ated group had a mean osseointegration of33% and a range of 0–56%. The plate-formligated group was significantly differentfrom other groups (P,0.001). The meanper cent osseointegration and associatedstandard errors are displayed in Figure1.

Radiographic analysis showed a changein crestal bone height. Results are shownin Figure2. Ligated implants lost1.54∫0.29mm of crestal bone after thetime of ligature placement, while non-lig-ated implants lost 0.56∫0.22mm of

Table 1. Crestal bone loss by group

Group Crestal bone loss(mm ∫ SE)

Plate-form 0.28 ∫ 0.13

Root-form 0.71 ∫ 0.32

Root-form ligated 1.33 ∫ 0.30

Plate-form ligated 1.72 ∫ 0.47


crestal bone. These groups were statisti-cally different, as shown by ANOVA, withP,0.05.

Crestal bone loss of each group is shownin Table1. The mean crestal bone lossaround non-ligated root-form implants was0.71mm, while the mean crestal bone lossaround plate-form implants was 0.28mm.The mean crestal bone loss around ligatedroot-form implants was 1.33mm, whilemean crestal bone loss around ligatedplate-form implants was 1.72mm. No indi-vidual group was statistically differentfrom any other group, nor did statisticalanalysis show a correlation between achange in radiographic crestal bone heightand per cent osseointegration, as definedand measured in this study. Photomicro-graphs of histological specimens of ligatedimplants are shown in Figures3 and 4.

Discussion

In a previous paper that reported findingsfrom this group of primates, Fritz et al.demonstrated clinical and radiographic evi-dence of osseointegration of both plate- androot-form implants (Fritz et al. 1996).These findings are now confirmed by his-

Fig.3. Root-form implant, ligated. This typical threa-ded root-form implant demonstrates some evidenceof bone loss around the first thread of the implant,as well as inflammation. However, vertical bone lossis not dramatic.

tological analysis of the implants after twoyears of function.

Fritz et al. also reported a loss of crestalbone height around the implants twelvemonths after placement. Using digital sub-traction radiography, they concluded thatroot-form implants lost an average of0.38mm of crestal bone, while plate-formimplants lost significantly less crestalbone, only 0.1mm.

The trend noted in the above studycontinued and the data presented in thispaper provides a comparison of radio-graphic and histomorphometric out-comes. When evaluated after 24monthsof function, the plate-form implants lost0.28mm of bone, while the root-form im-plants lost 0.71mm of bone. Althoughthis difference was not significant (PΩ0.48), over half the samples were re-moved from these groups to conduct lig-ation experiments, reducing statisticalpower.

When ligated, the mean crestal boneheight around implants decreased signifi-cantly, as expected. What is more interest-ing is the behavior of the interface belowthe crest of the bone. All implants lostcrestal bone height when ligated, but alongthe midline in a buccal-lingual plane, theroot-form implants maintained local osseo-


Fig.4. Blade implant, ligated. This implant de-monstrates a typical response for blade implantswhich were ligated to induce inflammation. The le-vel of bone apposition, which approaches the neck ofthe implant in non-ligated cases, has moved towardthe apex of the implant. A fibrous connective tissueappears to fill the space between the implant and thebone. Bone loss is markedly linear, along the implantinterface.

integration, while the plate-form implantstended to lose local osseointegration.

After six months of ligation, the plate-form implants in this study declined dra-matically in per cent osseointegrationalong this section of the implant. Severalspecimens in this group dropped below20% interfacial contact. This was not dueto an increase in the marrow spaces foundin normal bone. The ligated implantstended toward a fibrous tissue downgrowthfrom the oral epithelium along the junc-tion between the implant and bone. In con-trast, root-form implants, when ligated,showed no comparable decrease in per centosseointegration. Since the implants werecontrolled for material characteristics andplacement techniques, the major differencebetween the implants was geometry.

Several theories may explain why theligated plate-form implants demonstratedless osseointegration than other groups. Ifit is assumed that the loss of integration of


an implant occurs in a manner somewhatsimilar to the loss of a natural tooth – adegeneration of bone secondary to bacterialactivity and inflammation – then greateraccess to the implant-bone junction mayaccelerate bony degeneration. Under func-tion, implants move slightly (Bidez et al.1986; Ko et al. 1992; Misch & Bidez 1994).Because of geometrical considerations, theamount of movement at the neck of aplate-form implant might open up a biggergap compared to a threaded implant. Thesituation is analogous to putting a bevel onthe finish line of a crown preparation(Hunter & Hunter 1990; Padilla & Bailey1992). Functional loading of plate-form im-plants may create a bigger gap, allowingmore bacterial invasion. Alternatively, thelarger gap may cause a greater microstrainat the plate–form interface. If this localstrain were above normal capacity levels,complicated by the biological stress of theligature, it may lead to loss of integration.

Asecond possibility is that theplate-formimplants, with a transition from the abut-ment platform to the smaller rectangularimplant body, simply move more than root-form implants. This micromovement maylead toa lossof support (Bidezet al.1986; Bi-dez & Misch 1992; Ko et al. 1992; Misch &Bidez 1994). Perhaps this does not present aproblemina situationoforalhealth, butcanlead to a loss of osseointegration when peri-implantitis is present.

A third possibility is the character of theload applied to the implant to bone inter-face. In the case of these plate-form im-plants, an axial load applied to the implantproduces a shear force at the interface.Bone is weakest in shear (Bidez & Misch1992). Because of the threads of the root-form implant, the thread geometry mayload the bone more in compression. Thisis not true around the collar of the implant,but root-form threaded implants typicallylose crestal bone down to the first threadof the implant. Although this study doesnot support conclusions in this area, thetendency of implants to lose crestal bonein areas of shear warrants further research.

Conclusions

In this study, plate-form and root-form im-plants were placed in primates and loadedfor two years. Some implants were biolo-

gically stressed for six months with a liga-ture to create peri-implantitis. Ligated im-plants lost more crestal bone than non-lig-ated implants. Histological evaluationdemonstrated significantly less osseoin-tegration associated with ligated plate-form implants, with an average of 34% os-seointegration. Other implant groups –root-form, plate-form and root-form lig-ated – demonstrated a typical osseointegr-ation rate of about 60%.

Resume

Ce manuscript decrit la reponse histologique a long termeau niveau des implants-plateau ou racine. Trente-six pri-mates ont recu 48 implants comme pilier distal au niveaude la mandibule. Apres guerison, les implants ont ete char-ges avec des protheses partielles fixees qui sont restees enfonction durant deux annees. Un sous-groupe a ete ligatureau niveau des sulci gingivaux afin d’augmenter l’accumu-lation de plaque dentaire au niveau de ces implants. Lahauteur osseuse crestale autour des implants a ete quanti-fee en utilisant des techniques de soustraction radiologi-que. Les implants ligatures ont perdu davantage d’oscrestal que les non-ligatures (ANOVA: P,0.05). Apres leuravulsion les implants ont ete enfouis dans des blocs et de-coupespouruneanalysehistomorphometrique evaluant lamesure de l’osteointegration. Les deux types d’implantavaient une osteintegration d’environ 60%. Lorsqu’il yavait une ligature, les implants-plateau avaient une dimi-nution de l’integration allant jusqu’a 34% tandis que ceuxen forme racine maintenaient une integration de 62%. Cesdonnees ontmontreque danscemodeledeprimate, les im-plants-plateau et -racine maintenaient une integration du-rant leur mise en fonction de deux annees. Lorsqu’une liga-ture etait placee les implants-racine maintenaient unebonne quantite d’osteontegration tandis que cette derniereetait significativement inferieure lorsque les implants-pla-teau etaient utilises.

Zusammenfassung

Diese Arbeit ist Teil einer Langzeitstudie über enossaleZahnimplantaten an Primaten und beschreibt die histolo-gische Antwort auf scheiben- und wurzelförmige mplant-ate. 36 Primaten erhielten 48 seitliche Unterkieferimpl-antate. Nach der Heilphase wurden die mplantate mitfestsitzenden Teilprothesen versorgt, die während zweiJahren in Funktion verblieben. Ein Teil der Gruppe erhi-elt im den Sulcus eine Ligatur, um die dem mplantatangrenzendenden Gewebe einer biologischen Stressitu-ation auszusetzen. Die Höhe des Alveolarknochens umdie mplantate wurde mit Hilfe der digitalen Subtrak-tionsradiographie quantitativ erfasst. Die mplantate miteiner Ligatur verloren mehr Alveolarknochen als dienichtligierten mplantate (ANOVA; P,0.05). Nach derEntnahme wurden die mplantate eingebettet und histolo-gische Schnitte angefertigt. Diese dienten der histomor-phometrischen Analyse und der Bestimmung des Osseo-


integrationsgrades in Prozenten. Sowohl die scheiben-, implantes distales mandibulares con pilar. Tras la cicatri-wie auch die wurzelförmigen mplantate zeigten ohne zacion, los implates se restauraron con dentaduras parcia-Ligaturen eine 60%-ige Osseointegration. Wurden aber les fijas, que permanecieron en function durante 2 anos.Ligaturen angelegt, so reduzierte sich der Grad der Osseo- A un subconjunto del grupo se les coloco una ligadura enintegration bei den scheibenförmigen mplantaten auf el surco gingival para estresar los tejidos que soportan los34%, bei den wurzelförmigen mplantate auf 62%, es han- implantes. Se cuantifico la altura de la cresta osea alrede-delte sich um einen signifikanten Unterschied. Die Re- dor de los implantes usando tecnicas radiograficas de sus-sultate dieses Primatenmodells zeigen, dass die scheiben- traccion digital. Los implantes ligados perdieron mas hue-und wurzelförmigen mplantate während einer Funk- so crestal que los implantes no ligados, como se muestrationszeit von zwei Jahren ihre Osseointegration been ANOVA (P,0.05). Tras la retirada, los implantes seibehalten. Werden die Gewebe aber mit Ligaturen zur ex- embebieron y seccionaron para analisis histomorfometri-perimentellen Entzündung gebracht, können die wurz- co incluyendo mediciones del porcentaje de osteointegra-elförmigen mplantate ihren Osseontegrationsgrad cion. Tanto los implantes con forma de placa como losbeibehalten, bei den scheibenförmigen mplantaten nahm de forma de raız no ligados mostraron un 60 por cientoer ab. de osteointegracion. Cuando se ligaron, los implantes con

forma de placa bajaron a una media de integracion de soloel 34 por ciento, mientras que los implantes con formade raız mantuvieron el 62 por ciento de integracion, unadiferencia significativa. Estos datos muestran que en estemodelo de primates, lo implantes con forma de placa yResumenforma de raız mantuvieron la integracion en funcion du-rante 2 anos. Al estresarse con ligaduras, los implantes

Como parte de una evaluacion a largo plazo de implantes con forma de raız mantuvieron unas cantidades relativasdentales endooseos en primates, este trabajo describe la de osteointegracion, mientras que el porcentaje de inte-respuesta histologica a implantes con forma de placa y gracion de los implantes con forma de placa disminuyo.con forma de raız. Treinta y seis primates recibieron 48

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Documents

Histomorphological evaluation of loaded plate-form and root-form implants in Macaca mulatta monkeys