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ARTICLE IN PRESS
0142-9612/$ - se
doi:10.1016/j.bi
�CorrespondE-mail addr
Biomaterials 27 (2006) 996–1002
www.elsevier.com/locate/biomaterials
Ability of zirconia double coated with titanium and hydroxyapatite tobond to bone under load-bearing conditions
Takashi Suzukia, Shunsuke Fujibayashia, Yasuaki Nakagawaa,Iwao Nodab, Takashi Nakamuraa,�
aDepartment of Orthopaedic Surgery, Kyoto University Graduate School of Medicine, Shogoin-Kawaharacho 54, Sakyo-ku, Kyoto 606-8507, JapanbBioceram Division, Kyocera Corp., Gamocho-Kawai 10-1, Gamogun, Shiga 529-1595, Japan
Received 3 January 2005; accepted 21 July 2005
Available online 22 August 2005
Abstract
As a preclinical study, we evaluated the ability of hydroxyapatite and titanium on zirconia (HTOZ) to bond to bone under load-
bearing conditions in animal experiments. HTOZ, HA, and Ti on Co–Cr alloy (HTOC) and Ti on Co–Cr alloy (TOC) were
implanted into the weight-bearing portion of the femoral condyles of nine beagle dogs. Femurs were extracted 4, 12, and 52 weeks
after implantation and examined mechanically by pullout testing, and histologically by toluidine blue staining, SEM, and calculation
of the affinity index. The interfacial shear strengths (mean7SD) of the HTOZ, HTOC, and TOC groups were 4.4270.453,
3.9070.903, and 4.0870.790MPa at 4 weeks; 6.8272.64, 6.0071.88, and 6.6371.63MPa at 12 weeks; and 13.9871.94,
11.9571.51, and 10.7870.83MPa at 52 weeks. There were no significant differences in the interfacial shear strengths between the
three groups at any time. Affinity indices (mean7SD) obtained from SEM images of the HTOZ, HTOC, and TOC groups were
49.676.52%, 43.3710.43%, and 23.773.95% at 4 weeks; 55.076.72%, 51.573.07%, and 28.674.09% at 12 weeks; and
59.176.73%, 63.076.40%, and 34.376.72% at 52 weeks. HA-coated implants (HTOZ, HTOC) had significantly higher affinity
indices than non-HA-coated implants (TOC) at all times. HTOZ has the ability to bond to bone equivalent to HTOC and TOC.
HTOZ is an excellent material for components of cementless joint prostheses.
r 2005 Elsevier Ltd. All rights reserved.
Keywords: Zirconia; Cementless; Load-bearing; Total knee arthroplasty
1. Introduction
Many ceramic materials have been used for thecomponents of joint prostheses and, compared withmetallic materials, using ceramic materials such aszirconia as the bearing parts of joint prostheses canreduce polyethylene wear volume [1–6]. Additionally, incomparison to alumina, zirconia has higher wearresistance [1,2,7], and higher bending strength andfracture toughness [8–10]. Because of their goodcombination of mechanical properties and excellentbiocompatibility [11–13], zirconia ceramics are recog-
e front matter r 2005 Elsevier Ltd. All rights reserved.
omaterials.2005.07.026
ing author.
ess: [email protected] (T. Nakamura).
nized as one of the best biomaterials for joint prostheses.However, metallic cobalt–chromium alloys are thestandard materials for the femoral components of totalknee arthroplasty, and ceramic femoral componentshave not been applied as widely in total knee arthro-plasty as in femoral heads for total hip arthroplasty.One of the reasons for this is that there are no ceramicfemoral components of the cementless type for totalknee replacement. In general, ceramic femoral compo-nents such as zirconia and alumina are secured to thefemur using bone cement. In contrast, in cementlessfixation, the metal implants are prepared with roughsurfaces, obtained by using several coatings or byetching, to achieve the mechanical interlocking requiredfor their anchoring. Moreover, to successfully obtain
ARTICLE IN PRESS
Fig. 2. Cross-section of HTOZ, consisting of zirconia ceramic as
substrate, titanium as the deep coating layer, and hydroxyapatite as
the superficial coating layer.
T. Suzuki et al. / Biomaterials 27 (2006) 996–1002 997
early biological fixation, metal surfaces have beenprepared with HA or bioactive glass coatings. AlthoughHA coating is necessary to ensure secure and earlybiological fixation between the ceramic and thesurrounding bone, HA coating of ceramic implants istechnically difficult.To solve this problem, we have developed a new
composite material for cementless ceramic components:hydroxyapatite and titanium on zirconia (HTOZ),which consists of zirconia ceramic as substrate, titaniumas a deep coating layer, and hydroxyapatite as asuperficial coating layer. The basic mechanical proper-ties and biological safety of this material have beenalready reported [14,15]. As a preclinical study, here weevaluated the ability of HTOZ to bond to bone undersuch load-bearing conditions as occur in the clinicalsituation, using an animal model.
2. Materials and methods
2.1. Implant preparation
Three types of trapezoid-shaped implants (8.5� 8.5�
4.3mm) were prepared: HTOZ, HA and Ti on Co–Cr alloy
(HTOC), and Ti on Co–Cr alloy (TOC) (Fig. 1). HTOZ
consisted of zirconia ceramics stabilized with 3mol% Y2O3,
which satisfies the ISO standard criteria [16], as substrate;
titanium (Ti) as a deep coating layer; and hydroxyapatite (HA)
as a superficial coating layer (Fig. 2). HTOC consisted of
Co–Cr alloy (CoCrMo) as substrate, Ti as a deep coating
layer, and HA as a superficial coating layer. TOC consisted of
Co–Cr alloy as substrate and Ti alone as the coating layer.
The details of the methods of preparation of these implants
are described in Refs. [14,15]. Briefly, the initial roughness
(Rmax) of the zirconia was 1.17 mm, and that of the Co–Cy
alloy was 68.5mm. For the Ti surface treatments, HTOZ,
HTOC, and TOC coatings were performed using the inert gas-
shielded arc spray method. Melted titanium was blown onto
the surface of the substrate by the high-speed carrier gas in the
chamber into which argon gas was introduced. The peak
thickness of the Ti coating was determined to be 500 mm and
the surface roughness (Rmax) was approximately 360 mm. ForHTOZ and HTOC, HA coating of the Ti coating was
performed using the flame spray method, with an acetylene
Fig. 1. The three types of trapezoid-shaped implants. From left to
right: HTOZ, HTOC, and TOC.
and oxygen gas flame, and air used as the high-speed carrier
gas for the spray. The thickness of the HA coating was less
than 50 mm (mean 20 mm).
2.2. Surgical procedure
The implants were conventionally sterilized with ethylene
oxide gas and implanted into the weight-bearing portion of the
femoral condyles of nine adult beagle dogs weighing
9.0–11.0 kg. The surgical methods used have been described
previously [17,18]. Briefly, the dogs were anesthetized with
intramuscular administration of ketamine hydrochloride
(50mg/kg), diazepam (5mg), and atropine sulfate (0.5mg).
Just before the operation, pentobarbital sodium (0.5mL/kg)
was injected intravenously, with local administration of a
solution of 1% lidocaine.
The dogs were placed in the supine position and the right
knee exposed via a medial parapatellar approach in the usual
sterile manner. The implantation sites in the weight-bearing
portion of the medial and lateral femoral condyles were
prepared using a specially designed broach with cutting
surfaces, followed by a surgical electronic drill. During drilling,
the hole was continuously cooled with saline. Just before
insertion of the implants, the hole was irrigated with saline
containing isepamicin sulfate to remove any shards of bone.
An implant was then inserted into the hole by tapping in for
press fitting (Fig. 3a).
Two implants were inserted into each femur. The three types
of implants were inserted in a randomized manner to avoid
any position-related differences. Following irrigation, the
fascia and subcutaneous layers were closed with silk sutures
and the skin was closed with skin staples. The same surgical
procedure was repeated to insert further implants into the left
femoral condyles. No postoperative external immobilization
was applied. Thirty-six implants (12 HTOZ, 12 HTOC, and 12
TOC) were inserted into 18 knees of nine dogs. The animals
were housed individually in standard dog cages and fed
standard dog food and water ad lib. The animals were kept in
cages for 2 weeks after the operation and allowed to move
freely under observation. Both hind legs in each animal were
operated on during the same operation so that the animal
would be obliged to stand on the operated legs. Three dogs
were sacrificed at 4, 12, and 52 weeks after the operation with
an overdose of pentobarbital sodium, and both femurs
ARTICLE IN PRESS
Fig. 3. (a) Implants inserted into the load-bearing portion of both
medial and lateral femoral condyles. (b) AP soft X-ray image of the
femur with a HTOZ implant at 4 weeks after implantation.
T. Suzuki et al. / Biomaterials 27 (2006) 996–1002998
retrieved. Six femurs involving 12 implants (four HTOZ, four
HTOC, and four TOC) were prepared for mechanical tests and
histological examinations at each time point. The Kyoto
University guidelines for animal experiments were observed
throughout this study.
2.3. Mechanical testing
Following euthanasia, all the extracted femurs containing
implants were examined by soft X-ray. At each time point,
nine implants (three HTOZ, three HTOC, and three TOC)
were selected at random from 12 implants for pullout tests and
the other three (one HTOZ, one HTOC, and one TOC) were
used for histological examination only. All implant-containing
bone specimens were kept moist after harvesting. After the
specimens were fixed with resin into a cylindrical container, the
superficial bone and cartilage surrounding each implant were
removed minimally using an electronic surgical drill to allow
connection of the implant and a specially designed hook for
the pullout tests.
After the container was set on the base of an Instron-type
autograph (Instron 1123, Instron Japan Ltd., Tokyo, Japan),
the hook was connected to the implant. The implants were
pulled out from the condyles at a crosshead speed of 2.0mm/
min, taking care to ensure that the line of action of the pullout
force was parallel to the long axis of the implant.
The pullout failure load was measured when the implant
was dislodged from the bone. The failure load values were
divided by the bone–implant interface area to obtain the
interfacial shear strength. After the pullout tests, the extracted
implants with surrounding bone were preserved for histologi-
cal examination to examine the separation sites.
2.4. Histological examination
For the histological and morphological examinations, new
bone formation on the coated surface was evaluated by
toluidine blue staining and light microscopy, scanning electron
microscopy (SEM), and measurement of the affinity index. All
specimens from which the implants had not been pulled out,
and some specimens with the implants pulled out, from each
time point were prepared for histological examinations. These
specimens were fixed in 10% phosphate-buffered formalin for
7 d, embedded in polyester resin, then dehydrated in serial
concentrations of ethanol (50%, 70%, 90%, and 99.5% v/v)
changing every 3 d. Sections 500 mm thick were cut with a band
saw (BS-3000N, EXAKT cutting system, Norderstedt, Ger-
many) across the bone–implant interface. The sections were
then ground to a thickness of 100–150 mm using a grinding–-
sliding machine (Microgrinding MG-4000, EXAKT, Norder-
stedt, Germany). For examinations by light microscopy
(ECLIPSE E600, Nikon Ltd., Tokyo, Japan), sections were
stained with toluidine blue. The remaining sections were
coated with gold by sputtering and examined by SEM
(JSM5410LV, JEOL Ltd., Tokyo, Japan).
For quantitative morphological evaluation of the degree of
direct contact between the coating surface and the new bone,
the affinity indices of the specimens with non-pulled-out
implants at each time point were measured from the SEM
photographs using image analysis software (Winroof, Mitani
Ltd., Tokyo, Japan). To calculate the affinity index, the length
of bone in direct contact with the coated surface with no
intervening soft tissue was divided by the total length of the
coated surface, and this value was multiplied by 100 (Fig. 4).
2.5. Statistical analysis
Data were recorded as mean7standard deviation (SD) and
analyzed using a one-way factorial ANOVA with Fisher’s
ARTICLE IN PRESS
Fig. 4. Measurement of affinity indices: the length of bone in direct
contact with the coated surface was divided by the total length of the
coated surface.
T. Suzuki et al. / Biomaterials 27 (2006) 996–1002 999
PLSD testing as the post hoc test. Differences at po0:05 wereconsidered statistically significant.
Fig. 5. Results of mechanical tests. Interfacial shear strength (MPa)
between bone and implants in pullout tests at 4, 12, and 52 weeks.
There was no statistically significant difference in the interfacial shear
strength between the three groups at any time.
3. Results
3.1. Clinical observation
All animals were able to bear their body weight uponstanding within 1 week. When the animals were allowedto walk outside their cages 2 weeks after the operation,all were able to walk. Although there were no infectionsor postoperative complications in the operated animals,mild joint effusion was noted in some animals. Therange of motion of the knee joints was nearly normal inall animals.
3.2. Radiographic findings
Specimens taken from the animals immediately aftereuthanasia were examined by soft X-ray in bothanteroposterior and lateral views. Soft X-ray imagesshowed no breakage or sinking of the implants at anytime points (4, 12, and 52 weeks). No radiolucent zonearound the implant and no sclerotic changes in thesurrounding bone indicating loosening were observedfor any of the three types of implants at any time point.There was no obvious difference between the HA-coatedimplants (HTOZ, HTOC) and the non-HA-coatedimplants (TOC) in the soft X-ray examination (Fig. 3b).
3.3. Mechanical evaluation
The interfacial shear strengths (mean7SD) ofthe HTOZ, HTOC, and TOC implants, obtained bypullout testing, were 4.4270.453, 3.9070.903, and4.0870.790MPa, respectively, at 4 weeks after implan-tation; 6.8272.64, 6.0071.88, and 6.6371.63MPa at12 weeks; and 13.9871.94, 11.9571.51, and 10.7870.830MPa at 52 weeks. The interfacial shear strengthsincreased with time in all three types of implants, andthese values suggest that the implants were firmly
bonded to bone at each time point. Although thestrength of HTOZ bonding was equivalent to or a littlegreater than that of HTOC and TOC at 4, 12, and 52weeks, there was no significant difference in theinterfacial shear strengths between the three groups atany time points (Fig. 5).
3.4. Histological examination
Histological examinations after the pullout tests showedno separation of the coating layer, and all the separationsoccurred in the bone at the bone–implant interface.In the toluidine blue stained sections, at 4 weeks after
implantation, new bone with thin and irregular trabe-culae was observed on the coated surface of all threetypes of implants. At 12 weeks, the new trabecular bonewas somewhat thicker than that at 4 weeks. At 52 weeks,new bone formation with a lamellar pattern on thecoated surface was noted. The direct contact areabetween the new trabecular bone and the coated surface,and new bone formation adjacent to the implants,increased with time. Through all time points, moredirect contact of bone to the coated surface tended to beobserved with the HA-coated implants than the non-HA-coated implants.SEM images of HTOZ (Fig. 6a), HTOC (Fig. 6b),
and TOC (Fig. 6c) at 4 weeks after implantation showednew bone formation on and along the coated surface,similar to the optical microscopy findings. At 12 weeks,new bone appeared to be a little thicker than at 4 weeksfor all three types of implant. However, more directcontact bone on the coated surface was noted with theHA-coated implants than with the non-HA-coatedimplants at both 4 and 12 weeks (Fig. 6d–f). Althoughnew bone formation on the coated surface at 52 weekswas noted in all three types of implants, the new bonewith the non-HA-coated implants appeared to beslightly poorer than that with the HA-coated implants.
ARTICLE IN PRESS
Fig. 6. SEM images at 4 (a: HTOZ; b: HTOC; c: TOC) and 12 weeks (d: HTOZ; e: HTOC; f: TOC). More direct contact bone on the coated surface
was noted with the HA-coated implants than with the non-HA-coated implants at both 4 and 12 weeks.
T. Suzuki et al. / Biomaterials 27 (2006) 996–10021000
3.5. Morphological examination
Affinity indices (mean7SD) obtained from the SEMimages of the specimens involving HTOZ, HTOC, andTOC implants were 49.676.52%, 43.3710.43%,23.773.95%, respectively, at 4 weeks; 55.076.72%,51.573.07%, 28.674.09% at 12 weeks; and 59.176.73%, 63.076.40%, 34.376.72% at 52 weeks. At alltime points, the HA-coated implants had significantlyhigher affinity indices than the non-HA-coated implants(Fig. 7).
4. Discussion
Ceramic femoral components of the cemented typehave been used in our institute for total knee arthro-plasty since 1989. Akagi [19] reported that the clinical
results of surgery with alumina ceramic implants havebeen good, and no aseptic loosening or breakage of theceramic components was observed. Nakamura [20]documented a further study in which zirconia ceramicswere used instead of alumina ceramics, and showedgood clinical results equivalent to the former study.However, there are no ceramic femoral components ofthe cementless type and thus the components have beenfixed with cement in all cases at our institute. Becauseceramic femoral components of the cementless type wereneeded for several cases, HTOZ was developed and thepresent study was performed.At present, there is no established technique to make
porous coatings on ceramics by which the ceramics candirectory bond to bone. Therefore, ceramic jointprostheses fixed without cement have not been popular,except for the ball head for total hip arthroplasty.Bosetti et al. [21] developed zirconia coated with
ARTICLE IN PRESS
Fig. 7. Affinity indices obtained from SEM images of each implant at
4, 12, and 52 weeks. HA-coated implants (HTOZ and HTOC) have
significantly higher affinity indices than the non-HA-coated implant
(TOC) at all times.
T. Suzuki et al. / Biomaterials 27 (2006) 996–1002 1001
bioactive glass and described how the coating enhancedintegration with bone cells on the surface of the zirconiain vitro. Spector et al. [22] reported that oxidizedzirconium femoral components for total knee arthro-plasty reduced the wear volume of polyethylene in vitro.However, there are few studies investigating whetherporous-coated zirconia can directory bond to bone invivo. Therefore, our study is valuable in the realizationof ceramic femoral components for total knee arthro-plasty.The interfacial shear strengths of all three types of
implants, obtained from the pullout tests in this study,were 3.90–4.42MPa at 4 weeks, 6.00–6.82MPa at 12weeks, and 10.78–13.98MPa at 52 weeks. Compared tothe data from similar experiments in previous studies[17,18], the interfacial shear strengths of all three typesof implants in the present study were higher. Thissuggests that all three types of implants bonded firmly tobone. In addition, because the interfacial shear strengthof HTOZ in this study was higher than those in theprevious studies, and was equivalent to those of HTOCand TOC, HTOZ was considered to have sufficientability to bond to bone.With regard to HA coatings, Thomas et al. [23]
demonstrated that HA-coated implants exhibit signifi-cantly greater interfacial shear strengths than uncoatedimplants in pushout tests after 3, 5, 10, and 32 weeks,and they stated that HA coating provided an osteophilicsurface for bone deposition and allows for a more rapiddevelopment of implant–bone attachment. Conversely,Nakashima and Hayashi reported that HA-coatedimplants had higher interfacial shear strengths inpushout tests than non-HA-coated implants at 4 weeks,although there was no significant difference betweenHA-coated and non-HA-coated implants at 12 weeks.Therefore, they described HA coating as enhancingimplant fixation by direct chemical bonding to boneshortly after implantation due to the bioactivity of HA[24,25].
Although there were significant differences in affinityindices, there was no significant difference in theinterfacial shear strength in the pullout tests betweenHA-coated and non-HA-coated implants at any timepoints in this study. As for the mechanical examinations,it was supposed that the strength of interlocking betweenthe bone and the porous structure of the titaniumcoating might exceed the strength of the chemicalattachment between bone and HA, and thus the shearstrength in the pullout tests would partially depend onthe quality of the surrounding bone around the implants.With respect to the histological evaluation, affinity
indices showed significantly greater direct bone in-growth into the HA-coated implants than into thenon-HA-coated implants at all times. This result is asdescribed in previous studies [24,25], and suggests thatHA coating enhances new bone ingrowth into thesurface of the implants due to the good osteoconductionof HA. There were obvious differences in the histolo-gical evaluation despite there being no significantdifference in the mechanical tests. Therefore, we areconvinced that the HA coating is advantageous to earlydirect bonding between bone and implant.The number of samples in this study was limited for
several reasons. First, because this study was apreclinical study using a canine model, it was moreimportant to show the effectiveness of these implantsand illustrate some trends from their use in a total kneereplacement model than to show significance in statis-tical analysis. Second, because of animal welfareconcerns, it was difficult to increase the number ofexperimental animals. Third, in the quantitative mor-phological evaluation in this study, four sections weretaken of each sample and there was considerablevariation in the data obtained for each section, variationthat might have influenced the significance obtainedfrom statistical analysis.Nakashima and Hayashi [24] indicated that HA
coating should induce early bone ingrowth and thesubsequent fixation should depend upon the mechanicalanchoring strength achieved by the rough surface of theimplant. We believe that Ti coating has a macroporousstructure for interlocking with bone, and HA coatinghas good osteoconduction for early bone ingrowth, andthus, both coatings have important roles in the fixationof cementless prostheses to bone.The results of our study showed that HTOZ has
bonding-to-bone ability equivalent to HTOC and TOC,TOC being already in clinical use. It was important thatHTOZ could firmly bond to bone under load-bearingconditions similar to the clinical situation. We areconvinced that HTOZ is an excellent composite materialfor components of cementless joint prostheses. HTOZfemoral components for total knee arthroplasty areexpected to be used clinically and to contribute toimproved future surgical results.
ARTICLE IN PRESST. Suzuki et al. / Biomaterials 27 (2006) 996–10021002
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