<<

Materials Express

2158-5849/2014/4/001/012 Copyright © 2014 by American Scientific Publishers All rights reserved. doi:10.1166/mex.2014.1148 Printed in the United States of America www.aspbs.com/mex

Implantable zirconia bioceramics for repair and replacement: A chronological review

Adeel Afzal Affiliated Colleges at Hafr Al-Batin, King Fahd University of Petroleum and Minerals, P.O. Box 1803, Hafr Al-Batin, 31991, Saudi Arabia; Interdisciplinary Research Centre in Biomedical Materials, COMSATS Institute of Information Technology, Defense Road, Off. Raiwind Road, Lahore, 54000, Pakistan

ABSTRACT Bone tissue engineering applies scientific principles to repair, regenerate, and restore the functions of defected hard tissues or to replace them with purposely built . In the past few decades, the design, construc- Review tion and modification of biomaterials possessing desirable properties—those mimicking natural bone—remained the center of attention. Consequently,IP: 192.168.39.211 zirconia is foundOn: Thu, to be 23 the Sep material 2021 18:24:00 of choice for bone repair and replace- ment applications due to its uniqueCopyright: biomechanical American properties. Scientific This Publishers paper aims to present a succinct review of Delivered by Ingenta the applications of zirconia based biomaterials in bone tissue engineering; for instance, as implantable bioce- ramic, as coating or thin film on other metallic implants, as porous bone scaffold and substitute material, and as a radio-opacifying agent in bone cements. The evolution of zirconia as an essential material in biomedical applications, especially those concerning bone repair and replacement, is presented in a chronological order. Particular emphasis is placed on recent progress and drawbacks of zirconia and its composites in terms of their mechanical and biological properties. It is concluded that zirconia certainly enjoys the best combination of mechanical strength, fracture toughness, biocompatibility, and bioactivity; however, its properties can be fur- ther improved either by suitable surface modification or through combination with other bioactive and glasses. Keywords: Biocompatibility, Bone, , Nanocomposite, Osseointegration, Zirconia.

CONTENTS 1. INTRODUCTION 1. Introduction ...... 1 Zirconia (ZrO2 is an extremely capable ceramic that has 2. Zirconia Ceramics in Bone Tissue Engineering ...... 2 been used as structural and functional material in sev- 2.1. Zirconia Ceramics in Orthopedic Implants ...... 2 eral industrial and biomedical applications.1 2 It exists in 2.2. Zirconia Ceramic Thin Films and Coatings three polymorphic forms at ambient pressure: (1) mon- for Orthopedic Implants ...... 4 oclinic at < 1,170 C; (2) tetragonal at 1,170–2,370 C 2.3. Zirconia Ceramic Scaffolds and Bone > Graft Substitutes ...... 5 temperature range; and (3) cubic at 2,370 C, until it 3–6 2.4. Zirconia Ceramics in Bone Cements ...... 6 melts at 2,706 C. In addition to its polymorphic crys- 3. Challenges and Recent Trends ...... 7 talline structure, zirconia possesses a unique combination 4. Concluding Remarks ...... 7 of physicochemical characteristics such as (a) its biocom- Acknowledgments ...... 7 patibility and bioactivity: zirconia is biocompatible and References and Notes ...... 7 promotes cell proliferation and differentiation in osteogenic pathways;7–10 (b) its osseointegration: bone attachment on zirconia surface and the formation of a direct inter- Emails: [email protected], [email protected] face between bone and zirconia has been demonstrated

Mater. Express, Vol. 4, No. 1, 2014 1 Materials Express Implantable zirconia bioceramics for bone repair and replacement Afzal

in several studies, that is often comparable to or even this field. Figure 1 shows a pictographic representation of better than titania implants;11–16 (c) its radiopaqueness: the applications of zirconia in bone tissue engineering, as that makes it clearly visible in radiographs, thus making discussed in this review paper. Finally, the drawbacks and it possible to monitor its function;17–19 and above all, resulting research trends are also discussed. (d) its mechanical strength and toughness: that is ascribed to the transformation toughening mechanism of zirconia 2. ZIRCONIA CERAMICS IN BONE ceramics; 20–25 i.e., when external stress is applied, the TISSUE ENGINEERING cracks initiate and propagate, and the metastable tetrago- 43 nal phase transforms into monoclinic polymorph around Since 1970s, zirconia received great attention as a and close to the crack tip causing volume expansion biomedical material due to its chemical and biologi- and compressive stresses, which effectively inhibit crack cal inertness and superior properties, as mentioned ear- propagation. lier. The early stage investigations on zirconia based biomaterials focused on its orthopedic applications, specif- Besides, it has been known since long that zirconia 44–49 does not accumulate in the body tissues, muscles, or ically as femoral heads for total hip replacements. after implantation,26–29 which reduces its local or Later, zirconia was included in composites used as bone 50–53 54–57 systematic toxic effects as compared to those caused by graft substitutes, bone cements, and in dental 633–42 58 titania implants.30–32 Because of these desirable character- implants and prostheses. Piconi and Maccauro istics and its excellent stability, shock and wear resistance, reviewed the performance and prospects of zirconia as a in addition, zirconia is preferred in many biomedical appli- ceramic in 1999. They concluded that tetrag- cations especially in orthopedics and dentistry. In the past onal zirconia polycrystals (TZP) are best suited for ortho- few years, a number of reviews have been published on pedic applications due to their excellent physicochemical clinical trials and success of zirconia in dental implants and mechanical properties. and prostheses.633–42 That is why the dental applications Over the years, it has been found that zirconia of zirconia bioceramics are not discussed in this paper. polymorphs are highly sensitive to synthetic methods 6 59 60 The readers are therefore referred to the aforementioned and processing techniques. However, both of the reviews for more insight on zirconia bioceramics in den- metastable zirconia polymorphs, i.e., tetragonal and cubic IP: 192.168.39.211 On: Thu,zirconia, 23 Sep can2021 be synthesized18:24:00 and partially stabilized at room tistry. On the other hand, zirconia inCopyright: orthopedic American applica- Scientific Publishers tions has not been reviewed or little has been published on temperature by doping zirconia lattice with other Delivered by Ingenta zirconia and its composites as bone replacement materials such as calcia (CaO), magnesia (MgO), ceria (CeO2 , and 61–67 to regenerate, repair, and/or strengthen bone in this form. yttria (Y2O3 . Numerous partially stabilized zirconia This article therefore aims to present an overview of (PSZ) compositions are known today that possess excel- Review ≥ 68 69 the recent advances and critical assessment of the suc- lent flexural strength (usually 1,000 MPa), and high ≥ 1/2 68 70 cess of zirconia powders, scaffolds, coatings, and implants, fracture toughness (usually 8MPam . The appli- which have been used for bone replacement and regenera- cations of partially stabilized zirconia ceramic as a bioma- tion. This review paper is principally divided into different terial are discussed in the following sub-sections. sections depending upon the application of zirconia as a biomaterial, and each section discusses selected examples 2.1. Zirconia Ceramics in Orthopedic Implants of the mechanical properties, bioactivity, and osseointegra- Early microscopic and radiographic studies in animals tion of zirconia bioceramics in a chronological order to confirmed that zirconia implants possessed good biocom- provide readers a clear understanding of the progress in patibility, and that bone apposition could occur directly

Adeel Afzal studied Chemistry at Quaid-i-Azam University (Islamabad, Pakistan) and received M.Sc. (Chemistry) and M.Phil. (Organic Chemistry) degrees in 2002 and 2004, respectively. He earned Ph.D. (Dr. rer. Nat. in Chemistry) in 2007 from University of Vienna (Austria). He specialized in design, synthesis and fabrication of synthetic antibodies based on molecularly imprinted polymers and ceramic thin films, and metal nanoparticles as artificial receptor layers for mass-sensitive chemical sensors. Later, he served different higher education institutions, research centres and industries in Pakistan. From 2010–2012, he worked as Postdoctoral Researcher at University of Bari (Italy) and developed high tem- perature metal oxide semiconductor gas sensors and nanomaterials for catalytic applications. In 2012, he joined KFUPM Affiliated Colleges at Hafr Al-Batin (Saudi Arabia) as Assis- tant Professor of Chemistry. His research interests include synthesis, characterization and applications of nanomaterials, polymers and nanocomposites, development of chemical sensors, biomedical materials and diagnostics.

2 Mater. Express, Vol. 4, 2014 Implantable zirconia bioceramics for bone repair and replacement Materials Express Afzal

Fig. 1. Biomedical uses of zirconia ceramics in modern bone replacement and repair applications. These include application of zirconia bioceramics as orthopedic implants, thin films and coatings on other metallic implants, porous bone scaffolds and substitute materials, and bone cements. Review

IP: 192.168.39.211 On: Thu, 23 Sep 2021 18:24:00 on the implant surface without leaving any gaps or cel- response towards zirconia implants with modified surfaces Copyright: American Scientific Publishers lular infiltrate at the interface. 71 72 However, regardlessDelivered bywas Ingenta similar to that of titanium implants, thus showing of the amount of intensive research on ceramic zirco- comparable osseointegration capability. nia biomaterials, relatively little was known about the In 2009, Att et al. 77 monitored osteoblast activity on effects of surface modification on bone tissue response to UV treated zirconia (Y-PSZ) implants. They found that implantable zirconia bioceramics and their stability until UV treatment enhanced osteoblast attachment and prolif- recently. Therefore, attempts were made to modify zirco- eration, and facilitated subsequent mineralization process. nia surface and investigate its influence on biological and Figure 2 demonstrates enhanced bioactivity of UV treated mechanical properties of zirconia. zirconia disks. UV light transformed hydrophobic zirconia In 2004, Hao et al.73 tested a CO laser to mod- surfaces to hydrophilic status and progressively reduced 2 78 ify the surface of magnesia partially stabilized zirconia the amount of surface carbon. In a later study, Han et al. (MgO-PSZ) ceramic and found out that MgO-PSZ surfaces utilized alumina-sandblasted discs of yttrium stabilized tetragonal zirconia polycrystals (Y-TZP) to investigate the rich in hydroxyl groups facilitate apatite formation, when response of osteoblast like cells. They observed a more soaked for 14 days in simulated body fluids (SBF). A year pronounced differentiation and proliferation of osteoblast later, Sennerby et al.74 used a slurry containing zirconia like cells on zirconia, when combined with bone morpho- powder and a pore-former75 to modify the surface of zir- genetic protein-2 (BMP-2). conia implants, and observed stronger bone tissue response In 2012, Lee et al. 79 also reported enhanced osseoin- towards greater surface roughness of surface modified tegration and early bone formation around alumina- implants as compared to non-modified zirconia implants. sandblasted tetragonal zirconia implants with the In a histomorphometric comparative study by Lee simulation of recombinant human BMP (rhBMP-2) gel. 76 et al. different types of implants based on compos- On the other side, in a recent study by Kohal et al.80 to ite hydroxyapatite, titania or zirconia were tested and it examine in vivo and in vitro response of osteoblasts and was found that zirconia implants surface modified with bone tissue, it was observed that cell proliferation and hydroxyapatite and fluorapatite provided the highest bone- osseointegration proceeded more slowly on sandblasted to-implant contact after 4 and 12 weeks of healing period. and acid etched zirconia (TZP) implants as compared to Depprich et al. 12 13 also investigated the osseointegration, commercial titania implants, although surface modified i.e., the formation of direct bone-to-implant interface, on zirconia was accepted by osteoblastic hFOB 1.19 cells and yttria stabilized tetragonal zirconia (Y-PSZ) implants mod- it demonstrated sufficient osseointegration with rat bone ified by acid etching. They concluded that bone tissue tissues after 28 days of healing.

Mater. Express, Vol. 4, 2014 3 Materials Express Implantable zirconia bioceramics for bone repair and replacement Afzal

Fig. 2. Increased osteoblast affinity of zirconia disks by UV light treatment. Initial spread and cytoskeletal arrangement of rat bone marrow-derived osteoblasts 3 h after seeding onto untreated and UV treated zirconia surfaces. Representative confocal microscopic images with dual staining of DAPI for nuclei (green) and rhodamine phalloidin for actin filaments (red) are shown. Cell morphometric evaluations for the area and perimeter of osteoblasts were performed using the images (histograms). Data are mean ± SD (n = 10). Adapted with permission from [77], Att, et al.; Enhanced osteoblast function on ultraviolet light-treated zirconia; Biomaterials 30, 1273 (2009). © 2009, Elsevier.

Similarly, a couple of other contradicting reports could et al.91 tested the osteoblast behavior towards nanostruc- be found in literature on bioactivity and osseointegra- tured monoclinic zirconia coatings prepared via plasma tion of zirconia implants in comparison with commercial spraying technique. They observed excellent bioactivity or biological grade titania implants.81 82 Nonetheless, in vitro, and bone-like apatite precipitates on the coating in light of the majority of data reported in recent surface after 6 days of soaking in SBF. The cellular differ- literature, it may be concluded that suitably surface modi- entiation tests also revealed effective attachment, adhesion, fied zirconia implants perform excellently both in vivo and and proliferation of osteoblast-like MG63 cells to the sur- in vitro,83 84 and often better thanIP: titania192.168.39.211 controls.10 85–87On: Thu,face 23 Sep of the 2021 monoclinic 18:24:00 zirconia coating. Copyright: American ScientificFurthermore, Publishers zirconia has been coupled with bioactive Delivered by Ingenta 2.2. Zirconia Ceramic Thin Films and Coatings hydroxyapatite (HAp) to prepare ZrO2/HAp composite for Orthopedic Implants coatings for orthopedic implants in the past decade. 92–95 The physical properties of zirconia and the success of zir- These composite coatings possessed better mechanical Review properties and biocompatibility as compared to pris- conia implants also introduced them as coatings for other 96 metallic implants. In 2006, Liu et al. 88 deposited zirco- tine ZrO2 or HAp. Wang et al. in 2010, fabricated nia thin films via filtered cathodic arc system with oxygen nanocomposite coatings on titanium via electrodeposition plasma. These ceramic films composed of stoichiometric method. These coatings comprised of fluorinated HAp and zirconia nanoparticles demonstrated bone-like apatite for- zirconia, and exhibited high bonding strength, low disso- 96 mation on the surface, when immersed in SBF, attributable lution rate, and good in vitro bioactivity. to the nanoscale surface structure. Zirconia thin films also revealed favorable bioactivity and cytocompatibility as observed by growth and proliferation of bone mar- row mesenchymal stem (BMMS) cells. Figure 3 shows the surface morphology of BMMS cells grown on the surface of thin films. These ceramic thin films can be used to coat metallic bone replacements (implants) to enhance their biocompatibility and osseointegration. In a later study, it was also confirmed that zirco- nia coatings could enhance implants’ osseointegration capability.89 As stated earlier, UV light improves hydrophilicity and bioactivity of zirconia ceramics.77 Hsu et al.90 prepared monoclinic zirconia thin films via micro-arc oxidation and Fig. 3. Bone marrow mesenchymal stem (BMMS) cells seeded on exposed them to UV light. They also confirmed the pres- zirconia thin films after 4 days. Adapted with permission from [88],

ence of hydrophilic groups and eventual improvement in Liu, et al.; Bioactivity and cytocompatibility of zirconia (ZrO2) films the bioactivity of monoclinic zirconia through enhanced fabricated by cathodic arc deposition; Biomaterials 27, 3904 (2006). apatite formation after UV treatment. In 2010, Wang © 2006, Elsevier.

4 Mater. Express, Vol. 4, 2014 Implantable zirconia bioceramics for bone repair and replacement Materials Express Afzal

Recently, multicomponent calcia-zirconia-silica com- posite coatings have also been demonstrated to have good bioactivity, excellent bonding strength with the sub- strate, and low degradation rate.97 But the effects of such coatings on osseointegration and cytotoxicity of bone implants are still unknown and demand further investigations. Nonetheless, these results suggest that zir- conia based thin films and coatings can be utilized for possible applications in bone tissue replacement.

2.3. Zirconia Ceramic Scaffolds and Bone Graft Substitutes Porous bone scaffolds and substitute materials are typi- cally used in bone tissue engineering to fill bone defects and to regenerate bone tissue.98–105 The porous morpholo- gies of biodegradable polymers, ceramics, and polymer- ceramic nanocomposite scaffolds have been widely studied and applied in bone tissue engineering.102 106–111 Zirco- nia, thanks to its favorable biomechanical properties,112 is also exploited as a novel bone substitute material. In 2006, Chen et al.113 developed a procedure for fabricating zir- conia based porous scaffolds by combining replication and electrospray methods. Thus, obtained zirconia scaffolds were mechanically superior and exhibited higher stiffness Review Fig. 4. The microstructure of the struts of ZrO foams produced by as compared to those prepared via conventional slurry dip 2 the replication technique combined with (a) electrospraying and (b) coating method. The improvementIP: 192.168.39.211 in mechanicalrelia- On: Thu,slurry 23 Sep dipping, 2021 respectively. 18:24:00 The population of micropores is much bility of zirconia scaffolds was attributedCopyright: to considerably American Scientificlower in thePublishers struts of foams prepared by electrospraying (a) than in reduced dimensions and population of microcracksDelivered and by thoseIngenta prepared by slurry dipping (b). Reprinted with permission from micropores, as shown in Figure 4. [113], Chen, et al.; Improved mechanical reliability of bone tissue engi- It is well known that nanocrystalline calcium phosphate neering (zirconia) scaffolds by electrospraying; J. Am. Ceram. Soc. 89, 1534 (2006). © 2006, The American Ceramic Society. (CaP) powders such as HAp and -or-tricalcium phos- phates (-or-TCP), if reinforced with zirconia, exhibit exceptional bending and compressive strengths, stiffness, strength of zirconia/HAp scaffolds, having porosity in the micro hardness, and fracture toughness. 114–119 On the range of 72–91%, could be increased from 2.5 to 13.8 MPa other hand, HAp coatings and-or reinforcements enhance by varying the amount of zirconia from 50–100 wt.%. the biological activity and osseointegration capability of In 2011, Jang et al.137 also produced multicom- 120–123 zirconia ceramics. Owing to the complimenting ponent, continuously porous TCP/TCP-(t-ZrO2 /t-ZrO2 properties of HAp and zirconia, several works have been composites through multi-pass extrusion method as artifi- produced on the synthesis, characterization, , and cial bone graft substitutes for cortical bone. They obtained phase stability of zirconia and hydroxyapatite composite exceptional compressive strength (53 MPa), biocompat- bone scaffolds and substitutes in the past.124–130 ibility, and cell proliferation behavior. A year later, It has been demonstrated that bone in growth and Mondal et al.138 fabricated porous scaffolds composed apposition is greater in microporous HAp scaffolds as of tetragonal zirconia, biphasic calcium phosphate, and compared to zirconia scaffolds of similar porosity;131–133 poly(caprolactone) multilayers by a similar extrusion pro- however, zirconia is mechanically tough and contributes cess. These scaffolds exhibited excellent cell viability strength to HAp as well as TCP ceramics.134 For example, and attachment with high porosity (78%) and compres- Matsumoto et al.135 in 2011, achieved excellent results sive strength (12.7 MPa). Furthermore, a multicomponent with microporous zirconia/HAp composite scaffolds con- porous scaffold composed of chitosan, nanoscale silica and taining yttria stabilized zirconia and HAp in 70/30 ratio. zirconia was developed by Pattnaik et al.139 who reported These composite scaffolds had strength equal to cortical that the presence on zirconia in the scaffold facilitated bone, and exhibited high protein adsorption, cell and tissue protein adsorption, biomineralization, and biodegradation affinity.135 Figure 5 presents the stained and SEM images processes, and that these scaffolds were not cytotoxic to of the histological section showing direct bonding of bones rat osteoprogenitor cells.139 to HAp, and zirconia/HAp composite scaffolds. A later In a recent study, Lin et al.140 reported mesoporous study by the same group136 established that compressive bioactive glass coated zirconia scaffolds with higher

Mater. Express, Vol. 4, 2014 5 Materials Express Implantable zirconia bioceramics for bone repair and replacement Afzal

IP: 192.168.39.211 On: Thu, 23 Sep 2021 18:24:00 Copyright: American Scientific Publishers Delivered by Ingenta Review

Fig. 5. Representative histological sections of specimens. HE stained samples (a)–(c) and SEM observations of samples (d)–(g)—((a) and (d): ZrO2; ∗ (b), (e), and (g): ZrO2/HAp-L; (c) and (f): HAp-L; : sample; B: bone; F: fibrous tissue). Reprinted with permission from [135], Matsumoto, et al.; Zirconia–hydroxyapatite composite material with micro porous structure; Dent. Mater. 27, e205 (2011). © 2011, Elsevier.

compressive strength, good biocompatibility and cell via- that radio-opacifying additives such as BaSO4 and ZrO2 bility. It is therefore suggested that zirconia certainly had adverse effects on biocompatibility and mechanical instructs strength, stiffness, and toughness to bone scaf- properties of PMMA bone cements. However, examples folds that is important for load bearing applications. in pertinent literature demonstrate that zirconia improves However, its biological properties such as adhesion to hard the tensile and compressive strengths as well as fracture tissue, and bioactivity may be improved by combining toughness of acrylic bone cements.142 145 it with a suitable bioactive material. In this bargain, zir- For instance, Kotha et al.146 in 2009, reported that conia/HAp and zirconia/TCP composite scaffolds present PMMA based acrylic bone cements reinforced with an optimum solution for bone regeneration and repair 5 vol.% of PMMA coated zirconia fibers (diameter: applications. 30 m) demonstrated 41% improvement in the fracture toughness. At the same time, it was also revealed in an 2.4. Zirconia Ceramics in Bone Cements alternate study by Gillani et al.147 that bone cements Zirconia is used as additives in commercial bone cements composed of zirconia nanoparticles, MMA monomer, and due to its radiopaqueness, toughness, and biocompatibility. PMMA beads exhibited greater cytocompatibility and It is often mixed with methylmethacrylate (MMA) osteoblast activity due to nanoscaling of zirconia addi- monomers, poly(methylmethacrylate) (PMMA), and initia- tives. Yet other reports suggest that on an average, 40-fold tor to form readily polymerizable bone cement.59 141–144 increase in the mean fatigue life of acrylic (PMMA) In a recent review by Arora et al.144 it was suggested bone cements as compared to the commercial benchmark

6 Mater. Express, Vol. 4, 2014 Implantable zirconia bioceramics for bone repair and replacement Materials Express Afzal

Similarly, in the past, many researchers discussed that a combination of bioactive phosphosilicate glasses with partially stabilized tetragonal zirconia ceramics could display desirable osseointegration as well as biome- chanical properties.159–164 However, as stated earlier, majority of research focused on mixing zirconia with HAp, and -or-TCP ceramics to achieve bet- ter results.120–123 Often, exceptional enhancements in mechanical properties137 with optimum biocompatibility and bioactivity have been recorded,135 136 which direct the use of zirconia-HAp/TCP composites in bone tissue engineering applications.

4. CONCLUDING REMARKS Zirconia holds unique and reliable combination of physic- Fig. 6. The mean fatigue life of specimens prepared from a commer- ochemical properties. Its biocompatibility and sufficient cial benchmark (Osteobond™, OB), and cements containing 0, 5, 10, biological activity enable its use in biomedical applica- 15 and 20 vol.% straight zirconia fibers and 10 vol.% variable diam- tions, especially in the field of bone tissue engineering. eter zirconia fibers (VDFs). Error bars span one standard deviation. Appropriate surface modification of zirconia and increased Adapted with permission from [148], Kane, et al.; Improved fatigue life of acrylic bone cements reinforced with zirconia fibers; J. Mech. surface roughness lead to better anchorage of osteoblast Behav. Biomed. Mater. 3, 504 (2010). © 2010, Elsevier. like cells, good bone-to-implant contact, and rapid bone like apatite formation. Similarly, zirconia based compos- ites reinforced with alumina and-or with HAp, TCP, bio- Review (Osteobond™, OB) can be achieved by reinforcing it with glass perform better than pristine zirconia both in vivo and 15–20 vol.% of sintered, straight zirconia fibers,148 as in vitro. However, it should be stressed that mechanical shown in Figure 6. IP: 192.168.39.211 On: Thu,properties 23 Sep 2021 of zirconia 18:24:00 are not compromised in achieving Copyright: American Scientifichigh surface Publishers roughness and superior bioactivity during the Delivered by Ingenta surface modification or composite formation procedures. 3. CHALLENGES AND RECENT TRENDS In future, further research on studying the effects of In late 1990s, the catastrophic failure of many zirconia aging, fatigue life, and long-term phase stability of zirco- ceramic femoral heads caused a huge concern for the nia ceramics should confirm the enduring significance of biomedical scientists and researchers. As a consequence, zirconia as bone repair and-or replacement material. Fur- a few orthopedic experts even turned to cobalt-chromium thermore, contradicting reports in literature indicate that 149 as the material of choice in total hip arthroplasty. the behavioral mechanism of zirconia and its composites However, the subsequent characterizations of the failed is still largely unknown; for instance, minor details regard- femoral heads confirmed that failure of zirconia implants ing changes in microstructure, phase percentage and sta- was caused by increased transformation of the tetrago- bility, surface chemistry, porosity etc. as a function of load nal zirconia to the monoclinic phase and decreased sur- applied and time passed both in vivo and in vitro must 150–152 face hardness in consequence, which rendered these be studied for suitable evaluation of the performance and implants less favorable in total hip arthroplasty. These life-time of implantable zirconia bioceramics. results asked for development of alternative approaches and new composite bioceramics to add value to zirconia Acknowledgments: The financial support provided by 153–155 implants. the Higher Education Commission (HEC, Pakistan) is 153 In 2006, Chevalier identified the development of gratefully acknowledged. Adeel Afzal appreciates his alumina–zirconia composite ceramics as a practical alter- colleagues at the Interdisciplinary Research Centre in native to monolithic zirconia and to reduce the long- Biomedical Materials (IRCBM, Pakistan) for their com- term effects of aging. In a recent study, Roualdes mitment, extended collaboration and continuous assistance 156 et al. demonstrated that sintered ceramics composed in biomedical materials research. of nanosized alumina and zirconia powders were bio- compatible, and did not exhibit inflammation and wear debris during in vivo histological examinations, which References and Notes makes them favorable for clinical applications. Further- 1. A. Eichler; Tetragonal Y-doped zirconia: Structure and ion conduc- tivity; Phys. Rev. B 64, 174103 (2001). more, recent reports suggest that bone binding ability 2. S. Shukla and S. Seal; Mechanisms of room temperature metastable of alumina–zirconia ceramic composites can be further tetragonal phase stabilisation in zirconia; Int. Mater. Rev. 50, 45 improved by the combination of HAp coatings. 157 158 (2005).

Mater. Express, Vol. 4, 2014 7 Materials Express Implantable zirconia bioceramics for bone repair and replacement Afzal

3. R. H. French, S. J. Glass, F. S. Ohuchi, Y.-N. Xu, and W. Y. Ching; 22. A. H. Heuer; Transformation toughening in ZrO2-containing ceram- Experimental and theoretical determination of the electronic struc- ics; J. Am. Ceram. Soc. 70, 689 (1987).

ture and optical properties of three phases of ZrO2; Phys. Rev. B 23. R. H. Hannink, P. M. Kelly, and B. C. Muddle; Transformation 49, 5133 (1994). toughening in zirconia-containing ceramics; J. Am. Ceram. Soc. 4. J. P. Goff, W. Hayes, S. Hull, M. T. Hutchings, and K. N. Clausen; 83, 461 (2000). Defect structure of yttria-stabilized zirconia and its influence on the 24. J. Chai, F. C. S. Chu, T. W. Chow, and B. M. H. Liang; Chemi- ionic conductivity at elevated temperatures; Phys. Rev. B 59, 14202 cal solubility and flexural strength of zirconia-based ceramics; Int. (1999). J. Prosthodont. 20, 587 (2007). 5. I. Denry and J. R. Kelly; State of the art of zirconia for dental 25. K. Kvam and S. Karlsson; Solubility and strength of zirconia-based applications. Dent. Mater. 24, 299 (2008). dental materials after artificial aging; J. Prosthet. Dent. 110, 281 6. B. Al-Amleh, K. Lyons, and M. Swain; Clinical trials in zirconia: (2013). a systematic review; J. Oral Rehabil. 37, 641 (2010). 26. J. Harms and E. Mäusle; Tissue reaction to ceramic implant mate- 7. Y. Ichikawa, Y. Akagawa, H. Nikai, and H. Tsuru; Tissue compat- rial; J. Biomed. Mater. Res. 13, 67 (1979). ibility and stability of a new zirconia ceramic in vivo; J. Prosthet. 27. R. C. Garvie, C. Urbani, D. R. Kennedy, and J. C. McNeuer; Bio- Dent. 68, 322 (1992). compatibility of magnesia-partially stabilized zirconia (Mg-PSZ) 8. Y. Josset, Z. Oum’Hamed, A. Zarrinpour, M. Lorenzato, J.-J. ceramics; J. Mater. Sci. 19, 3224 (1984). Adnet, and D. Laurent-Maquin; In vitro reactions of human 28. C. Piconi, G. Maccauro, F. Muratori, and E. Brach Del Prever; osteoblasts in culture with zirconia and alumina ceramics; Alumina and zirconia ceramics in joint replacements; J. Appl. Bio- J. Biomed. Mater. Res. 47, 481 (1999). mater. Biomech. JABB 1, 19 (2003). 9. L. Rimondini, L. Cerroni, A. Carrassi, and P. Torricelli; P. Bacterial 29. P. F. Manicone, P. Rossi Iommetti, and L. Raffaelli; An overview colonization of zirconia ceramic surfaces: An in vitro and in vivo of zirconia ceramics: basic properties and clinical applications; study; Int. J. Oral Maxillofac. Implants 17, 793 (2002). J. Dent. 35, 819 (2007). 10. B. Stadlinger, M. Hennig, U. Eckelt, E. Kuhlisch, and R. Mai; 30. D. Weingart, S. Steinemann, W. Schilli, J. R. Strub, U. Hellerich, Comparison of zirconia and titanium implants after a short healing J. Assenmacher, and J. Simpson; Titanium deposition in regional period. A pilot study in minipigs; Int. J. Oral Maxillofac. Surg. lymph nodes after insertion of titanium screw implants in maxillo- 39, 585 (2010). facial region; Int. J. Oral Maxillofac. Surg. 23, 450 (1994). 11. Y. Akagawa, Y. Ichikawa, H. Nikai, and H. Tsuru; Interface his- 31. K. W. Frisken, G. W. Dandie, S. Lugowski, and G. Jordan; A study tology of unloaded and early loaded partially stabilized zirco- of titanium release into body organs following the insertion of sin- nia endosseous implant in initial bone healing; J. Prosthet. Dent. gle threaded screw implants into the mandibles of sheep; Aust. 69, 599 (1993). Dent. J. 47, 214 (2002). 12. R. Depprich, H. Zipprich, M. Ommerborn,IP: 192.168.39.211 E. Mahn, L. Lammers, On: Thu, 32.23 U.Sep Meyer, 2021 M. 18:24:00 Bühner, A. Büchter, B. Kruse-Lösler, T. Stamm, and J. Handschel, C. Naujoks, H.-P. Wiesmann,Copyright: N. R. Kübler, American and ScientificH. P. Publishers Wiesmann; Fast element mapping of titanium wear around U. Meyer; Osseointegration of zirconia implants: An SEMDelivered obser- by Ingentaimplants of different surface structures; Clin. Oral Implants Res. vation of the bone-implant interface. Head Face Med. 4, 25 (2008). 17, 206 (2006). 13. R. Depprich, H. Zipprich, M. Ommerborn, C. Naujoks, H.-P. 33. H. J. Wenz, J. Bartsch, S. Wolfart, and M. Kern; Osseointegra- Wiesmann, S. Kiattavorncharoen, H.-C. Lauer, U. Meyer, N. R. tion and clinical success of zirconia dental implants: A systematic

Review Kübler, and J. Handschel; Osseointegration of zirconia implants review; Int. J. Prosthodont. 21, 27 (2008). compared with titanium: an in vivo study; Head Face Med. 4, 30 34. M. Hisbergues, S. Vendeville, and P. Vendeville; Zirconia: Estab- (2008). lished facts and perspectives for a biomaterial in dental implantol- 14. O. Hoffmann, N. Angelov, F. Gallez, R. E. Jung, and F. E. Weber; ogy; J. Biomed. Mater. Res. B Appl. Biomater. 88, 519 (2009). The zirconia implant-bone interface: A preliminary histologic eval- 35. S. D. Heintze and V. Rousson; Survival of zirconia-and metal- uation in rabbits; Int. J. Oral Maxillofac. Implants 23, 691 (2008). supported fixed dental prostheses: A systematic review; Int. 15. M. Gahlert, S. Röhling, M. Wieland, C. M. Sprecher, H. Kniha, and J. Prosthodont. 23, 493 (2010). S. Milz; Osseointegration of zirconia and titanium dental implants: 36. K. Nakamura, T. Kanno, P. Milleding, and U. Ortengren; Zirconia A histological and histomorphometrical study in the maxilla of as a abutment material: A systematic review; Int. pigs; Clin. Oral Implants Res. 20, 1247 (2009). J. Prosthodont. 23, 299 (2010). 16. O. Hoffmann, N. Angelov, G.-G. Zafiropoulos, and S. Andreana; 37. J.-S. Schley, N. Heussen, S. Reich, J. Fischer, K. Haselhuhn, and Osseointegration of zirconia implants with different surface charac- S. Wolfart; Survival probability of zirconia-based fixed dental pros- teristics: an evaluation in rabbits; Int. J. Oral Maxillofac. Implants theses up to 5 yr: A systematic review of the literature; Eur.J.Oral 27, 352 (2012). Sci. 118, 443 (2010). 17. F. Martinez-Rus, A. M. Garcia, A. H. de Aza, and G. Pradies; 38. A.-L. Gomes and J. Montero; Zirconia implant abutments: Radiopacity of zirconia-based all-ceramic crown systems; Int. A review; Med Oral Patol Oral Cir Bucal 16, e50 (2011). J. Prosthodont. 24, 144 (2010). 39. A. J. Raigrodski, M. B. Hillstead, G. K. Meng, and K.-H. Chung; 18. J. Aberg, H. B. Henriksson, H. Engqvist, A. Palmquist, Survival and complications of zirconia-based fixed dental prosthe- C. Brantsing, A. Lindahl, P. Thomsen, and H. Brisby; Biocompat- ses: A systematic review; J. Prosthet. Dent. 107, 170 (2012). ibility and resorption of a radiopaque premixed calcium phosphate 40. P. Triwatana, N. Nagaviroj, and C. Tulapornchai; Clinical per- cement; J. Biomed. Mater. Res. A 100, 1269 (2012). formance and failures of zirconia-based fixed partial dentures: 19. C. Chen, S.-C. Hsieh, N.-C. Teng, C.-K. Kao, S.-Y. Lee, C.-K. Lin, A review literature; J. Adv. Prosthodont. 4, 76 (2012). and J.-C. Yang; Radiopacity and cytotoxicity of portland cement 41. E. D. Roumanas; The clinical reliability of zirconia-based fixed containing zirconia doped bismuth oxide radiopacifiers. J. Endod. dental prostheses appears acceptable but further research is neces- doi:10.1016/j. joen.2013.07.006 (2013). sary; J. Evid. Based Dent. Pr. 13, 14 (2013). 20. R. C. Garvie, R. H. Hannink, and R. T. Pascoe; Ceramic steel? 42. R. D. L. Mattiello, T. M. K. Coelho, E. Insaurralde, A. A. 258, 703 (1975). K. Coelho, G. P. Terra, A. V. B. Kasuya, I. N. Favarão, L. de 21. D. L. Porter, A. G. Evans, and A. H. Heuer; Transformation- S. Gonccalves, and R. B. Fonseca; A review of surface treatment toughening in partially-stabilized zirconia (PSZ); Acta Met. methods to improve the adhesive cementation of zirconia-based 27, 1649 (1979). ceramics; ISRN Biomater. 2013 (2013).

8 Mater. Express, Vol. 4, 2014 Implantable zirconia bioceramics for bone repair and replacement Materials Express Afzal

43. R. L. Hentrich, G. A. Graves, H. G. Stein, and P. K. Bajpai; 65. A. K. Pandey and K. Biswas; Influence of sintering parameters An evaluation of inert and resorbale ceramics for future clinical on tribological properties of ceria stabilized zirconia bio-ceramics; orthopedic applications; J. Biomed. Mater. Res. 5, 25 (1971). Ceram. Int. 37, 257 (2011). 44. P. Christel, A. Meunier, J.-M. Dorlot, J.-M. Crolet, J. Witvoet, 66. L. Hallmann, P. Ulmer, E. Reusser, M. Louvel, and C. H. L. Sedel, and P. Boutin; Biomechanical compatibility and design Hämmerle; Effect of dopants and sintering temperature on of ceramic implants for orthopedic surgery; Ann. N. Y. Acad. Sci. microstructure and low temperature degradation of dental Y-TZP- 523, 234 (1988). zirconia; J. Eur. Ceram. Soc. 32, 4091 (2012). 45. B. Cales, Y. Stefani, and E. Lilley; Long-term in vivo and in vivo 67. J. Li, J. Peng, S. Guo, and L. Zhang; Application of response sur- aging of a zirconia ceramic used in orthopaedy; J. Biomed. Mater. face methodology (RSM) for optimization of sintering process for Res. 28, 619 (1994). the preparation of magnesia partially stabilized zirconia (Mg-PSZ) 46. B. Derbyshire, J. Fisher, D. Dowson, C. Hardaker, and using natural baddeleyite as starting material; Ceram. Int. 39, 197 K. Brummitt; Comparative study of the wear of UHMWPE with (2013). zirconia ceramic and stainless steel femoral heads in artificial hip 68. M. Guazzato, M. Albakry, S. P. Ringer, and M. V. Swain; Strength, joints; Med. Eng. Phys. 16, 229 (1994). fracture toughness and microstructure of a selection of all-ceramic 47. V. Saikko; Wear of polyethylene acetabular cups against zirconia materials, Part II, Zirconia-based dental ceramics; Dent. Mater. femoral heads studied with a hip joint simulator; Wear 176, 207 20, 449 (2004). (1994). 69. K. Nakamura, E. Adolfsson, P. Milleding, T. Kanno, and 48. J. M. Cuckler, J. Bearcroft, and C. M. Asgian; Femoral head tech- U. Örtengren; Influence of grain size and veneer firing process on nologies to reduce polyethylene wear in total hip arthroplasty; Clin. the flexural strength of zirconia ceramics; Eur. J. Oral Sci. 120, 249 Orthop. 317, 57 (1995). (2012). 49. V. Good, M. Ries, R. L. Barrack, K. Widding, G. Hunter, and 70. R. Benzaid, J. Chevalier, M. Saâdaoui, G. Fantozzi, M. Nawa, L. A. D. Heuer; Reduced wear with oxidized zirconium femoral heads; Diaz, and R. Torrecillas; Fracture toughness, strength and slow J. Bone Jt. Surg. 85, 105 (2003). crack growth in a ceria stabilized zirconia–alumina nanocomposite 50. W. R. Moore, S. E. Graves, and G. I. Bain; Synthetic bone graft for medical applications; Biomaterials 29, 3636 (2008). substitutes; ANZ J. Surg. 71, 354 (2001). 71. Y. Akagawa, R. Hosokawa, Y. Sato, and K. Kamayama; Compar- 51. R. Murugan and S. Ramakrishna; Development of nanocomposites ison between freestanding and tooth-connected partially stabilized for bone grafting; Compos. Sci. Technol. 65, 2385 (2005). zirconia implants after two years’ function in monkeys: A clinical and histologic study; J. Prosthet. Dent. 80, 551 (1998). 52. P. V. Giannoudis, H. Dinopoulos, and E. Tsiridis; Bone substitutes: 72. A. Scarano, F. Di Carlo, M. Quaranta, and A. Piattelli; Bone Review An update; Injury 36, S20 (2005). response to zirconia ceramic implants: An experimental study in 53. K. A. Hing; Bioceramic bone graft substitutes: Influence of porosity rabbits; J. Oral Implantol. 29, 8 (2003). and chemistry; Int. J. Appl. Ceram. Technol. 2, 184 (2005). IP: 192.168.39.211 On: Thu, 73.23 L.Sep Hao, 2021 J. Lawrence, 18:24:00 K. S. Chian, D. K. Y. Low, G. C. Lim, and 54. A. Sahafi, A. Peutzfeldt, E. Asmussen, and K. Gotfredsen; Bond Copyright: American ScientificH. Y. Publishers Zheng; The formation of a hydroxyl bond and the effects strength of resin cement to dentin and to surface-treated posts of Delivered by Ingentathereof on bone-like apatite formation on a magnesia partially sta- titanium alloy, glass fiber, and zirconia; J. Adhes. Dent. 5, 153 bilized zirconia (MgO–PSZ) bioceramic following CO laser irra- (2002). 2 diation; J. Mater. Sci. Mater. Med. 15, 967 (2004). 55. L. F. Valandro, M. Ozcan, M. C. Bottino, M. A. Bottino, R. Scotti, 74. L. Sennerby, A. Dasmah, B. Larsson, and M. Iverhed; Bone tissue and A. D. Bona; Bond strength of a resin cement to high-alumina responses to surface-modified zirconia implants: A histomorpho- and zirconia-reinforced ceramics: the effect of surface conditioning; metric and removal torque study in the rabbit; Clin. Implant Dent. J. Adhes. Dent. 8, 175 (2006). Relat. Res. 7, s13 (2005). 56. R. Amaral, M. Özcan, M. A. Bottino, and L. F. Valandro; Microten- 75. F. Adilstam and M. Iverhed; Förfarande och anordning vid dental sile bond strength of a resin cement to glass infiltrated zirconia- installation. (2005). reinforced ceramic: The effect of surface conditioning; Dent. Mater. 76. J.-T. Lee, S.-J. Heo, J.-Y. Koak, S.-K. Kim, S.-Y. Lee, H.-E. Kim, 22, 283 (2006). and C.-H. Han; A histomophometric Analysis of Bone Healing 57. X. Niu, Y. Yang, and W. Soboyejo; Contact deformation and crack- around Zirconia Implant; Key Eng. Mater. 342–343, 593 (2007). ing of zirconia/cement/foundation dental multilayers; Mater. Sci. 77. W. Att, M. Takeuchi, T. Suzuki, K. Kubo, M. Anpo, and T. Ogawa; Eng. 485, 517 (2008). Enhanced osteoblast function on ultraviolet light-treated zirconia; 58. C. Piconi and G. Maccauro; Zirconia as a ceramic biomaterial; Biomaterials 30, 1273 (2009). Biomaterials 20, 1 (1999). 78. S.-H. Han, K.-H. Kim, J.-S. Han, K.-T. Koo, T.-I. Kim, Y.-J. Seol, 59. J. Y. Thompson, B. R. Stoner, J. R. Piascik, and R. Smith; Adhe- Y.-M. Lee, Y. Ku, and I.-C. Rhyu; Response of osteoblast-like cells sion/cementation to zirconia and other non-silicate ceramics: Where cultured on zirconia to bone morphogenetic protein-2; J. Periodon- are we now? Dent. Mater. 27, 71 (2011). tal Implant Sci. 41, 227 (2011). 60. Q. Mahmood, A. Afzal, H. M. Siddiqi, and A. Habib; Sol–gel syn- 79. B.-C. Lee, I.-S. Yeo, D.-J. Kim, J.-B. Lee, S.-H. Kim, and J.-S. thesis of tetragonal ZrO2 nanoparticles stabilized by crystallite size Han; Bone formation around zirconia implants combined with and oxygen vacancies; J. Sol-Gel Sci. Technol. 67, 670 (2013). rhBMP-2 gel in the canine mandible; Clin. Oral Implants Res. 61. A. C. Subbarao; Sci. Technol. Zirconia, The American Chemical doi:10.1111/clr.12004 (2012). Society (1981) pp. 1–24. 80. R. J. Kohal, M. Bächle, W. Att, S. Chaar, B. Altmann, A. Renz, 62. G. Wang, X. Liu, and C. Ding; Phase composition and in-vitro and F. Butz; Osteoblast and bone tissue response to surface modi- bioactivity of plasma sprayed calcia stabilized zirconia coatings; fied zirconia and titanium implant materials; Dent. Mater. 29, 763 Surf. Coatings Technol. 202, 5824 (2008). (2013). 63. J. R. Kelly and I. Denry; Stabilized zirconia as a structural ceramic: 81. B. Setzer, M. Bächle, M. C. Metzger, and R. J. Kohal; The gene- An overview. Dent. Mater. 24, 289 (2008). expression and phenotypic response of hFOB 1.19 osteoblasts 64. Y.-W. Hsu, K.-H. Yang, K.-M. Chang, S.-W. Yeh, and M.-C. Wang; to surface-modified titanium and zirconia; Biomaterials 30, 979 Synthesis and crystallization behavior of 3 mol% yttria stabilized (2009). tetragonal zirconia polycrystals (3Y-TZP) nanosized powders pre- 82. H. Schliephake, T. Hefti, F. Schlottig, P. Gédet, and H. Staedt; pared using a simple co-precipitation process; J. Alloys Compd. Mechanical anchorage and peri-implant bone formation of surface- 509, 6864 (2011). modified zirconia in minipigs; J. Clin. Periodontol. 37, 818 (2010).

Mater. Express, Vol. 4, 2014 9 Materials Express Implantable zirconia bioceramics for bone repair and replacement Afzal

83. J. D. Langhoff, K. Voelter, D. Scharnweber, M. Schnabelrauch, 101. E. Sachlos and J. T. Czernuszka; Making tissue engineering scaf- F. Schlottig, T. Hefti, K. Kalchofner, K. Nuss, and B. von folds work. Review: the application of solid freeform fabrication Rechenberg; Comparison of chemically and pharmaceutically mod- technology to the production of tissue engineering scaffolds; Eur ified titanium and zirconia implant surfaces in dentistry: A study in Cell Mater 5, 39 (2003). sheep; Int. J. Oral Maxillofac. Surg. 37, 1125 (2008). 102. X. Liu and P. X. Ma; Polymeric scaffolds for bone tissue engineer- 84. S. H. Chung, H.-K. Kim, W.-J. Shon, and Y.-S. Park; Peri-implant ing; Ann. Biomed. Eng. 32, 477 (2004).

bone formations around (Ti,Zr)O2-coated zirconia implants with 103. S. J. Hollister; Porous scaffold design for tissue engineering; Nat. different surface roughness; J. Clin. Periodontol. 40, 404 (2013). Mater. 4, 518 (2005). 85. B. Bacchelli, G. Giavaresi, M. Franchi, D. Martini, V. De Pasquale, 104. V. Karageorgiou and D. Kaplan; Porosity of 3D biomaterial scaf- A. Trirè, M. Fini, R. Giardino, and A. Ruggeri; Influence of a folds and osteogenesis; Biomaterials 26, 5474 (2005). zirconia sandblasting treated surface on peri-implant bone healing: 105. D. W. Hutmacher, J. T. Schantz, C. X. F. Lam, K. C. Tan, and T. C. An experimental study in sheep; Acta Biomater. 5, 2246 (2009). Lim; State of the art and future directions of scaffold-based bone 86. C.-F. Wang, H.-L. Huang, D.-J. Lin, Y.-W. Shen, L.-J. Fuh, and engineering from a biomaterials perspective; J. Tissue Eng. Regen. J.-T. Hsu; Comparisons of maximum deformation and failure forces Med. 1, 245 (2007). at the implant–abutment interface of titanium implants between 106. T. A. Holland and A. G. Mikos; Tissue Eng. Springer (2006) pp. titanium-alloy and zirconia abutments with two levels of marginal 161–185. bone loss; Biomed. Eng. Online 12, 45 (2013). 107. K. Rezwan, Q. Z. Chen, J. J. Blaker, and A. R. Boccaccini; 87. Y.-S. Park, S.-H. Chung, and W.-J. Shon; Peri-implant bone forma- Biodegradable and bioactive porous polymer/inorganic composite tion and surface characteristics of rough surface zirconia implants scaffolds for bone tissue engineering; Biomaterials 27, 3413 (2006). manufactured by powder injection molding technique in rabbit tib- 108. H.-Y. Cheung, K.-T. Lau, T.-P. Lu, and D. Hui; A critical review on iae; Clin. Oral Implants Res. 24, 586 (2013). polymer-based bio-engineered materials for scaffold development; 88. X. Liu, A. Huang, C. Ding, and P. K. Chu; Bioactivity and cyto- Compos. Part B Eng. 38, 291 (2007).

compatibility of zirconia (ZrO2) films fabricated by cathodic arc 109. D. M. Yunos, O. Bretcanu, and A. R. Boccaccini; Polymer- deposition; Biomaterials 27, 3904 (2006). bioceramic composites for tissue engineering scaffolds; J. Mater. 89. V. Sollazzo, F. Pezzetti, A. Scarano, A. Piattelli, C. Bignozzi, Sci. 43, 4433 (2008). L. Massari, G. Brunelli, and F. Carinci; Zirconium oxide coating 110. X. He, Y. Z. Zhang, J. P. Mansell, and B. Su; Zirconia toughened improves implant osseointegration in vivo; Dent. Mater. 24, 357 alumina ceramic foams for potential bone graft applications: fabri- (2008). cation, bioactivation, and cellular responses; J. Mater. Sci. Mater.

90. Y. Han, Y. Yan, and C. Lu; Ultraviolet-enhanced bioactivity of ZrO2 Med. 19, 2743 (2008). films prepared by micro-arc oxidation; Thin Solid Films 517, 1577 111. L.-C. Gerhardt and A. R. Boccaccini; Bioactive glass and glass- (2009). IP: 192.168.39.211 On: Thu, 23 ceramicSep 2021 scaffolds 18:24:00 for bone tissue engineering; Materials 3, 3867 91. G. Wang, F. Meng, C. Ding, P. K. Chu, andCopyright: X. Liu; Microstructure, American Scientific(2010) Publishers. bioactivity and osteoblast behavior of monoclinic zirconia coating 112. H. Tiainen, G. Eder, O. Nilsen, and H. J. Haugen; Effect of ZrO Delivered by Ingenta 2 with nanostructured surface; Acta Biomater. 6, 990 (2010). addition on the mechanical properties of porous TiO2 bone scaf- 92. Y. W. Gu, K. A. Khor, D. Pan, and P. Cheang; Activity of plasma folds; Mater. Sci. Eng. C 32, 1386 (2012). sprayed yttria stabilized zirconia reinforced hydroxyapatite/Ti– 113. Q. Z. Chen, A. R. Boccaccini, H. B. Zhang, D. Z. Wang, and

Review 6Al–4V composite coatings in simulated body fluid; Biomaterials M. J. Edirisinghe; Improved mechanical reliability of bone tissue 25, 3177 (2004). engineering (zirconia) scaffolds by electrospraying; J. Am. Ceram. 93. A. Balamurugan, G. Balossier, S. Kannan, J. Michel, J. Faure, Soc. 89, 1534 (2006). and S. Rajeswari; Electrochemical and structural characterisation 114. C. Mansur, M. Pope, M. R. Pascucci, and S. Shivkumar; Zirconia- of zirconia reinforced hydroxyapatite bioceramic sol–gel coatings calcium phosphate composites for bone replacement; Ceram. Int. on surgical grade 316L SS for biomedical applications; Ceram. Int. 24, 77 (1998). 33, 605 (2007). 115. L. Fu, K. A. Khor, and J. P. Lim; Yttria stabilized zirconia rein- 94. M. Jelínek, T. Dostálová, Z. Teuberová, M. Seydlová, P. Mašínová, forced hydroxyapatite coatings; Surf. Coatings Technol. 127, 66 T. Kocourek, W. Mróz, A. Prokopiuk, and K. Smetana; Study of (2000).

laser created ZrO2 and hydroxyapatite/ZrO2 films for implantology; 116. V. V. Silva, R. Z. Domingues, and F. S. Lameiras; Microstruc- Biomol. Eng. 24, 103 (2007). tural and mechanical study of zirconia-hydroxyapatite (ZH) com- 95. Y. Huang, Y. Yan, and X. Pang; Electrolytic deposition of fluorine- posite ceramics for biomedical applications; Compos. Sci. Technol.

doped hydroxyapatite/ZrO2 films on titanium for biomedical appli- 61, 301 (2001). cations; Ceram. Int. 39, 245 (2013). 117. A. Rapacz-Kmita, A. Slósarczyk,´ and Z. Paszkiewicz; Mechanical

96. J. Wang, C. Huang, Q. Wan, Y. Chen, and Y. Chao; Characteriza- properties of HAp–ZrO2 composites; J. Eur. Ceram. Soc. 26, 1481 tion of fluoridated hydroxyapatite/zirconia nano-composite coating (2006). deposited by a modified electrocodeposition technique; Surf. Coat- 118. G. Levita, B. Cioni, G. Gallone, and A. Lazzeri; Synthesis of ings Technol. 204, 2576 (2010). bioactive hydroxyapatite-zirconia toughened composites for bone 97. F. Yang, Y. Xie, H. Li, T. Tang, X. Zhang, Y. Gan, X. Zheng, and replacement; Adv. Sci. Technol. 57, 31 (2009). K. Dai; Human bone marrow-derived stromal cells cultured with a 119. I. Ozden, M. Ipekoglu, N. Mahmutyazicioglu, and S. Altıntaº;

plasma sprayed CaO-ZrO2-SiO2 coating; J. Biomed. Mater. Res. B Effect of addition on the mechanical properties and the microstruc- Appl. Biomater. 95B, 192 (2010). ture of natural hydroxyapatite obtained from calf femoral bone; Key 98. D. W. Hutmacher; Scaffolds in tissue engineering bone and carti- Eng. Mater. 493–494, 199 (2011). lage; Biomaterials 21, 2529 (2000). 120. H.-W. Kim, S.-Y. Lee, C.-J. Bae, Y.-J. Noh, H.-E. Kim, H.-M. Kim,

99. S. Yang, K.-F. Leong, Z. Du, and C.-K. Chua; The design of scaf- and J. S. Ko; Porous ZrO2 bone scaffold coated with hydroxyapatite folds for use in tissue engineering. Part I. Traditional factors; Tissue with fluorapatite intermediate layer; Biomaterials 24, 3277 (2003). Eng. 7, 679 (2001). 121. T. Matsuno, M. Morita, K. Watanabe, K. Ono, and M. Koishi; 100. S. Yang, K.-F. Leong, Z. Du, and C.-K. Chua; The design of scaf- Strength of bond to bone and cytotoxicity of sintered bodies of folds for use in tissue engineering, Part II, Rapid prototyping tech- hydroxyapatite/zirconia composite particles; J. Mater. Sci. Mater. niques; Tissue Eng. 8, 1 (2002). Med. 14, 547 (2003).

10 Mater. Express, Vol. 4, 2014 Implantable zirconia bioceramics for bone repair and replacement Materials Express Afzal

122. H.-W. Kim, G. Georgiou, J. C. Knowles, Y.-H. Koh, and H.-E. Kim; 140. F. Lin, C. Yan, W. Zheng, W. Fan, C. Adam, and A. Oloyede; Calcium phosphates and glass composite coatings on zirconia for Preparation of Mesoporous Bioglass Coated Zirconia Scaffold for enhanced biocompatibility; Biomaterials 25, 4203 (2004). Bone Tissue Engineering; Adv. Mater. Res. 365, 209 (2011). 123. H.-W. Kim, S.-Y. Shin, H.-E. Kim, Y.-M. Lee, C.-P. Chung, H.-H. 141. A. Sabokbar, Y. Fujikawa, D. W. Murray, and N. A. Athanasou; Lee, and I.-C. Rhyu; Bone formation on the apatite-coated zirconia Radio-Opaque Agents in Bone Cement Increase Bone Resorption; porous scaffolds within a rabbit calvarial defect; J. Biomater. Appl. J. Bone Joint Surg. Br. 79-B, 129 (1997). 22, 485 (2008). 142. R. Gillani, B. Ercan, A. Qiao, and T. J. Webster; Nanofunctional- 124. J. Li, H. Liao, and L. Hermansson; Sintering of partially-stabilized ized zirconia and barium sulfate particles as bone cement additives; zirconia and partially-stabilized zirconia-hydroxyapatite composites Int. J. Nanomedicine 5, 1 (2010). by hot isostatic pressing and pressureless sintering; Biomaterials 143. D. E. Baciu, J. Simitzis, and D. Giannakopoulos; synthesis 17, 1787 (1996). and characterization of acrylic bone cement reinforced with 125. V. J. Lim, K. Khor, L. Fu, and P. Cheang; Hydroxyapatite–zirconia zirconia-bioceramic; Dig. J. Nanomater. Biostructures 7, 1779 composite coatings via the plasma spraying process; J. Mater. Pro- (2012). cess. Technol. 89–90, 491 (1999). 144. M. Arora; Polymethylmethacrylate bone cements and additives: 126. V. V. Silva, F. S. Lameiras, and R. Z. Domingues; Synthe- A review of the literature; World J. Orthop. 4, 67 (2013). sis and characterization of calcia partially stabilized zirconia- 145. S. Kitayama, T. Nikaido, R. Takahashi, L. Zhu, M. Ikeda, R. M. hydroxyapatite powders prepared by co-precipitation method; Foxton, A. Sadr, and J. Tagami; Effect of primer treatment on bond- Ceram. Int. 27, 615 (2001). ing of resin cements to zirconia ceramic; Dent. Mater. 26, 426 127. L. Fu, K. A. Khor, and J. P. Lim; The evaluation of powder pro- (2010). cessing on microstructure and mechanical properties of hydroxyap- 146. S. Kotha, C. Li, S. Schmid, and J. Mason; Reinforcement of bone atite (HA)/yttria stabilized zirconia (YSZ) composite coatings; Surf. cement using zirconia fibers with and without acrylic coating; Coatings Technol. 140, 263 (2001). J. Biomed. Mater. Res. A 88A, 898 (2009). ´ 128. A. Rapacz-Kmita, A. Slósarczyk, Z. Paszkiewicz, and 147. R. Gillani, A. Qiao, and T. Webster; ZrO2 nano-additives to C. Paluszkiewicz; Phase stability of hydroxyapatite–zirconia bone cement increase osteoblast adhesion and proliferation; Bio-

(HAp–ZrO2) composites for bone replacement; J. Mol. Struct. eng. Conf. 2009 IEEE 35th Annu. Northeast, Boston, MA (2009), 704, 333 (2004). pp. 1–2. 129. D. Singh, M. de la Cinta Lorenzo-Martin, F. Gutiérrez-Mora, J. L. 148. R. J. Kane, W. Yue, J. J. Mason, and R. K. Roeder; Improved Routbort, and E. D. Case; Self-joining of zirconia/hydroxyapatite fatigue life of acrylic bone cements reinforced with zirconia fibers;

composites using plastic deformation process; Acta Biomater. J. Mech. Behav. Biomed. Mater. 3, 504 (2010). Review 2, 669 (2006). 149. C. D. Hummer III, R. H. Rothman, and W. J. Hozack; Catastrophic 130. Z. Evis, M. Usta, and I. Kutbay; Improvement in sinterability and failure of modular zirconia-ceramic femoral head components after phase stability of hydroxyapatite andIP: partially192.168.39.211 stabilized zirconia On: Thu, 23 totalSep hip 2021 arthroplasty; 18:24:00J. Arthroplasty 10, 848 (1995). composites; J. Eur. Ceram. Soc. 29, 621 (2009)Copyright:. American Scientific150. S. A. Publishers Catledge, M. Cook, Y. K. Vohra, E. M. Santos, M. D. 131. J. Malmström, E. Adolfsson, L. Emanuelsson, and P.Delivered Thomsen; by IngentaMcClenny, and K. D. Moore; Surface crystalline phases and Bone ingrowth in zirconia and hydroxyapatite scaffolds with iden- nanoindentation hardness of explanted zirconia femoral heads; tical macroporosity; J. Mater. Sci. Mater. Med. 19, 2983 (2007). J. Mater. Sci. Mater. Med. 14, 863 (2003). 132. J. Malmström, C. Slotte, E. Adolfsson, O. Norderyd, and 151. E. M. Santos, S. Vohra, S. A. Catledge, M. D. McClenny, P. Thomsen; Bone response to free form-fabricated hydroxyapatite J. Lemons, and K. D. Moore; Examination of surface and mate- and zirconia scaffolds: A histological study in the human maxilla; rial properties of explanted zirconia femoral heads; J. Arthroplasty Clin. Oral Implants Res. 20, 379 (2009). 19, 30 (2004). 133. K. Grandfield, A. Palmquist, F. Ericson, J. Malmström, 152. J. L. Masonis, R. B. Bourne, M. D. Ries, R. W. McCalden, L. Emanuelsson, C. Slotte, E. Adolfsson, G. A. Botton, P. Thomsen, A. Salehi, and D. C. Kelman; Zirconia femoral head fractures: a and H. Engqvist; Bone response to free-form fabricated hydroxya- clinical and retrieval analysis; J. Arthroplasty 19, 898 (2004). patite and zirconia scaffolds: A transmission electron microscopy 153. J. Chevalier; What future for zirconia as a biomaterial? Biomateri-

study in the human maxilla: Bone response to HA and ZrO2 scaf- als 27, 535 (2006). folds; Clin. Implant Dent. Relat. Res. 14, 461 (2012). 154. A. H. De Aza, J. Chevalier, G. Fantozzi, M. Schehl, and 134. J.-Z. Yang, R. Sultana, X.-Z. Hu, and P. Ichim; Novel layered R. Torrecillas; Crack growth resistance of alumina, zirconia and hydroxyapatite/tri-calcium phosphate-zirconia scaffold composite zirconia toughened alumina ceramics for joint prostheses; Bioma- with high bending strength for load-bearing bone implant applica- terials 23, 937 (2002). tion; Int. J. Appl. Ceram. Technol. doi:10.1111/ijac.12024 (2013). 155. Y.-M. Kong, C.-J. Bae, S.-H. Lee, H.-W. Kim, and H.-E. Kim;

135. T. J. Matsumoto, S.-H. An, T. Ishimoto, T. Nakano, T. Matsumoto, Improvement in biocompatibility of ZrO2–Al2O3 nano-composite and S. Imazato; Zirconia–hydroxyapatite composite material with by addition of HA; Biomaterials 26, 509 (2005). micro porous structure; Dent. Mater. 27, e205 (2011). 156. O. Roualdes, M.-E. Duclos, D. Gutknecht, L. Frappart, J. Chevalier, 136. S.-H. An, T. Matsumoto, H. Miyajima, A. Nakahira, K.-H. Kim, and D. J. Hartmann; In vitro and in vivo evaluation of an and S. Imazato; Porous zirconia/hydroxyapatite scaffolds for bone alumina–zirconia composite for arthroplasty applications; Biomate- reconstruction; Dent. Mater. 28, 1221 (2012). rials 31, 2043 (2010). 137. D.-W. Jang, Y.-H. Kim, and B.-T. Lee; Microstructure control of 157. M. Takemoto, S. Fujibayashi, M. Neo, J. Suzuki, T. Kokubo,

TCP/TCP-(t-ZrO2/t-ZrO2 composites for artificial cortical bone; and T. Nakamura; Bone-bonding ability of a hydroxyapatite Mater. Sci. Eng. C 31, 1660 (2011). coated zirconia–alumina nanocomposite with a microporous sur- 138. D. Mondal, S. So-Ra, S. K. Sarkar, Y. K. Min, H. M. Yang, face; J. Biomed. Mater. Res. A 78A, 693 (2006).

and B. T. Lee; Fabrication of multilayer ZrO2-biphasic calcium 158. I. Mobasherpour, M. Solati Hashjin, S. S. Razavi Toosi, and phosphate-poly-caprolactone unidirectional channeled scaffold for R. Darvishi Kamachali; Effect of the addition ZrO2–Al2O3 on bone tissue formation; J. Biomater. Appl. 28, 462 (2012). nanocrystalline hydroxyapatite bending strength and fracture tough- 139. S. Pattnaik, S. Nethala, A. Tripathi, S. Saravanan, A. Moorthi, and ness; Ceram. Int. 35, 1569 (2009). N. Selvamurugan; Chitosan scaffolds containing silicon dioxide and 159. M. Ferraris, E. Verne, P. Appendino, C. Moisescu, A. Krajewski, zirconia nano particles for bone tissue engineering; Int. J. Biol. A. Ravaglioli, and A. Piancastelli; Coatings on zirconia for medical Macromol. 49, 1167 (2011). applications; Biomaterials 21, 765 (2000).

Mater. Express, Vol. 4, 2014 11 Materials Express Implantable zirconia bioceramics for bone repair and replacement Afzal

160. M. Bosetti, E. Vernè, M. Ferraris, A. Ravaglioli, and M. Cannas; glass coating: An in vitro and in vivo investigation; J. Biomed. In vitro characterisation of zirconia coated by bioactive glass; Bio- Mater. Res. 61, 282 (2002). materials 22, 987 (2001). 163. E. Verne, R. Defilippi, G. Carl, C. Vitale Brovarone, and 161. V. Stanic, N. N. Aldini, M. Fini, G. Giavaresi, R. Gia- P. Appendino; Viscous flow sintering of bioactive glass-ceramic rdino, A. Krajewski, A. Ravaglioli, M. Mazzocchi, B. Dubini, composites toughened by zirconia particles; J. Eur. Ceram. Soc. M. G. P. Bossi, and F. Rustichelli; Osteointegration of bioactive 23, 675 (2003). glass-coated zirconia in healthy bone: an in vivo evaluation; Bio- 164. N. N. Aldini, M. Fini, G. Giavaresi, L. Martini, B. Dubini, M. G. materials 23, 3833 (2002). P. Bossi, F. Rustichelli, A. Krajewski, A. Ravaglioli, M. Mazzoc- 162. N. N. Aldini, M. Fini, G. Giavaresi, P. Torricelli, L. Martini, R. Gia- chi, and R. Giardino; Osteointegration of bioactive glass-coated rdino, A. Ravaglioli, A. Krajewski, M. Mazzocchi, and B. Dubini; and uncoated zirconia in osteopenic bone: An in vivo experimental Improvement in zirconia osseointegration by means of a biological study; J. Biomed. Mater. Res. A 68A, 264 (2004).

Received: 22 October 2013. Accepted: 4 December 2013.

IP: 192.168.39.211 On: Thu, 23 Sep 2021 18:24:00 Copyright: American Scientific Publishers Delivered by Ingenta Review

12 Mater. Express, Vol. 4, 2014