Macroporous bioceramics: A remarkable material for bone regeneration

Journal of Biomaterials Applications

Volumn 27, Issue 3, 2012, Pages 345-358

  Lew, Kien Seng ^a   Othman, Radzali ^a   Ishikawa, Kunio ^b   Yeoh, Fei Yee ^a  

^a SCHOOL OF MATERIALS AND MINERAL RESOURCES ENGINEERING   (Malaysia)

^b KYUSHU UNIVERSITY   (Japan)

Author keywords

alumina; bone repair; hydroxyapatite; Macroporous bioceramics; tricalcium phosphate; zirconia

Indexed keywords

ALUMINA COATING; BIOACTIVE MATERIAL; BIOINERT; BIOINERTNESS; BONE DEFECT; BONE GROWTH; BONE REGENERATION; BONE REPAIR; BONE TISSUE; COATED SYSTEMS; GROWTH FACTOR; HOST TISSUES; INITIAL STAGES; MACROPOROUS; PORE FORMATION; POROUS BIOCERAMIC; POROUS HYDROXYAPATITE; POROUS ZIRCONIA; RIGID BONDS; SURFACE AREA; TISSUE IN-GROWTH; TRI-CALCIUM PHOSPHATES;

ALUMINA; BIOCERAMICS; BIOMECHANICS; BONE; COATED MATERIALS; HISTOLOGY; HYDROXYAPATITE; IMPREGNATION; MECHANICAL PROPERTIES; PORE SIZE; TISSUE; ZIRCONIA;

SCAFFOLDS (BIOLOGY);

TISSUE SCAFFOLD;

ARTICLE; BONE REGENERATION; CERAMICS;

BONE REGENERATION; CERAMICS; TISSUE SCAFFOLDS;

EID: 84865510523     PISSN: 08853282     EISSN: 15308022     Source Type: Journal    
DOI: 10.1177/0885328211406459     Document Type: Article

References (96)

1. Hench LL. Bioceramics. J Am Ceram Soc. 1998 ; 81: 1705-1728
2. Albee FH, Morrison HR. Studies in bone growth triple calcium phosphate as a stimulus to osteogenesis. Ann Surg. 1920 ; 71: 32-39
3. Boutin P. Arthroplastie totale de la hanche par prothese en alumina fritte: etude experimentale et premieres applications cliniques. Rev Chir Orthop. 1972 ; 58: 229-246
4. Hulbert SF, Morrison SJ, Klawitter JJ. Tissue reaction to three ceramics of porous and non-porous structures. J Biomed Mater Res. 1972 ; 6: 347-374
5. Hulbert SF, Young FA, Mathews RS, Klawitter JJ, Talbert CD, Stelling FH. Potential of ceramic materials as permanently implantable skeletal prostheses. J Biomed Mater Res. 1970 ; 4: 433-456
6. Williams DF The Williams dictionary of Biomaterials. Liverpool: Liverpool University Press ; 1999:
7. Tanaka Y, Yamashita K Bioceramics and their clinical applications. Kokubo T, ed. Cambridge: Woodhead Publishing Limited ; 2008: 28-52.
8. Shackelford JF Advanced ceramics, volume 1: bioceramics. Singapore: Gordon and Breach Science Publishers ; 2005:
9. Tamai N, Myoui A, Tomita T, Nakase T, Tanaka J, Ochi T, et al. Novel hydroxyapatite ceramics with an interconnective porous structure exhibit superior osteoconduction in vivo. J Biomed Mater Res. 2002 ; 59: 110-117
10. Gauthier O, Bouler JM, Aguado E, Pilet P, Daculsi G. Macroporous biphasic calcium phosphate ceramics influence of macropore diameter and macroporosity percentage on bone ingrowth. Biomaterials. 1998 ; 19: 133-139
11. Yamasaki H, Sakai H. Osteogenic response to porous hydroxyapatite ceramics under the skin of dogs. Biomaterials. 1992 ; 13: 308-312
12. Yunoki S, Ikoma T, Tsuchiya A, Monkawa A, Ohta K, Sotome S, et al. Fabrication and mechanical and tissue ingrowth properties of unidirectionally porous hydroxyapatite/collagen composite. J Biomed Mater Res. 2007 ; 80B: 166-173
13. Yuan H, De Groot K. Calcium phosphate biomaterials an overview. Learning from nature how to design new implantable biomaterials. 2004 ;: 37-57
14. Dorozhkin SV. Bioceramics of calcium orthophosphates. Biomaterials. 2010 ; 31: 1465-1485
15. Sing KSW, Everett DH, Haul RAW, Moscou L, Pierotti RA, Rouquerol J, et al. Reporting physisorption data for gas/solid systems with special reference to the determination of surface area and porosity. Pure Appl Chem. 1985 ; 57: 603-619
16. Holmes RE, Bucholz RW, Mooney V. Porous hydroxyapatite as a bone graft substitute in diaphyseal defects a histometric study. J Orthop Res. 1987 ; 5: 114-121
17. Holmes RE, Bucholz RW, Mooney V. Porous hydroxyapatite as a bone graft substitute in metaphyseal defects a histometric study. J Bone Joint Surg Am. 1986 ; 68: 904-911
18. Shimazaki K, Mooney V. Comparative study of porous hydroxyapatite and tricalcium phosphate as bone substitute. J Orthop Res. 1985 ; 3: 301-310
19. Albrektsson T, Johansson C. Osteoinduction, ssteoconduction and ssseointegration. Eur Spine J. 2001 ; 10: S96 - S101
20. Uchida A, Shinto Y, Araki N, Ono K. Slow release of anticancer drugs from porous calcium hydroxyapatite ceramic. J Orthop Res. 1992 ; 10: 440-445
21. Ma MY, Zhu YJ, Li L, Cao SW. Nanostructured porous hollow ellipsoidal capsules of hydroxyapatite and calcium silicate: preparation and application in drug delivery. J Mater Chem. 2008 ; 18: 2722-2727
22. Galbusera F, Bertolazzi L, Balossino R, Dubini G. Combined computational study of mechanical behaviour and drug delivery from a porous, hydroxyaptite-based bone graft. Biomech Model Mechanobiol. 2009 ; 8: 209-216
23. Silverman LD, Lukashova L, Herman OT, Lane JM, Boskey AL. Release of gentamicin from a tricalcium phosphate bone implant. J Orthop Res. 2007 ; 25: 23-29
24. Slowing II, Escoto JLV, Wu CW, Lin VSY. Mesoporous silica nanoparticles as controlled release drug delivery and gene transfection carriers. Adv Drug Del Rev. 2008 ; 60: 1278-1288
25. Zhao L, Yan X, Zhou X, Zhou L, Wang H, Tang J, et al. Mesoporous bioactive glasses for controlled drug release. Microporous Mesoporous Mater. 2008 ; 109: 210-215
26. Zhu Y, Kaskel S. Comparison of the in vitro bioactivity and drug release property of mesoporous bioactive glasses (MBGs) and bioactive glasses (BGs) scaffolds. Microporous Mesoporous Mater. 2009 ; 118: 176-182
27. Hench LL, Wilson J An introduction to bioceramics. Singapore: World Scientific ; 1993:
28. Den Boer FC, Wippermann BW, Blokhuis TJ, Patka P, Bakker FC, Haarman HJTM. Healing of segmental bone defects with granular porous hydroxyapatite augmented with recombinant human osteogenic protein-1 or autologous bone marrow. J Orthop Res. 2003 ; 21: 521-528
29. Yuan H, Kurashina K, De Bruijn JD, Li Y, De Groot K, Zhang X. A preliminary study on osteoinduction of two kinds of calcium phosphate ceramics. Biomaterials. 1999 ; 20: 1799-1806
30. Bodde EWH, Wolke JGC, Rick SZK, Jansen JA. Bone regeneration of porous β-tricalcium phosphate (Conduit™ TCP) and of biphasic calcium phosphate ceramic (Biosel) in trabecular defects in sheep. JBiomed Mater Res. 2007 ; 82A: 711-722
31. Shi D, Wen X Introduction to biomaterials. Shi D, ed. China: Tsinghua University Press, Singapore: World Scientific Publishing ; 2006: 25-25.
32. Rey C, Combes C, Drouet C, Somrani S. Tricalcium phosphate-based ceramics. Bioceramics and their clinical applications. 2008 ;: 326-355
33. Dos Santos LA, Carrodeguas RG, Rogero SO, Higa OZ, Boschi AO, De Arruda ACF. α-tricalcium phosphate cement "in vitro" cytotoxicity. Biomaterials. 2002 ; 23: 2035-2042
34. Wakae H, Takeuchi A, Udoh K, Matsuya S, Munar ML, LeGeros RZ, et al. Fabrication of macroporous carbonate apatite foam by hydrothermal conversion of α-tricalcium phosphate in carbonate solutions. J Biomed Mater Res. 2008 ; 87A: 957-963
35. Park J Bioceramics properties, characterization, and applications. New York: Springer Science+Business Media ; 2008:
36. Asazuma T, Masuoka K, Motosuneya T, Tsuji T, Yasuoka H, Fujikawa K. Posterior lumbar interbody fusion using dense hydroxyapatite blocks and autogenous iliac bone. J Spinal Disord Tech. 2005 ; 18: 41-47
37. Mangano C, Piattelli A, Perrotti V, Iezzi G. Dense hydroxyapatite inserted into postextraction sockets a histologic and histomorphometric 20-year case report. JPeriodontol. 2008 ; 79: 929-933
38. Layman DL, Ardoin RC. An in vitro system for studying osteointegration of dental implants utilizing cells grown on dense hydroxyapatite disks. J Biomed Mater Res. 1998 ; 40: 282-290
39. Chen QZ, Bretcanu O, Boccaccini AR Biomaterials fabrication and processing handbook. Chu PK Liu X, ed. Boca Raton: CRC Press ; 2008: 3-43.
40. Chang BS, Lee CK, Hong KS, Youn HJ, Ryu HS, Chung SS, et al. Osteoconduction at porous hydroxyapatite with various pore configurations. Biomaterials. 2000 ; 21: 1291-1298
41. Vuola J, Taurio R, Goransson H, Seljavaara SA. Compressive strength of calcium carbonate and hydroxyapatite implants after bone-marrow-induced osteogenesis. Biomaterials. 1998 ; 19: 223-227
42. Hench LL. Bioceramics from concept to clinic. J Am Ceram Soc. 1991 ; 74: 1487-1510
43. Omae H, Mochizuki Y, Yokoya S, Adachi N, Ochi M. Effects of interconnecting porous structure of hydroxyapatite ceramics on interface between grafted tendon and ceramics. J Biomed Mater Res. 2006 ; 79A: 329-337
44. Andrade JCT, Camilli JA, Kawachi EY, Bertran CA. Behavior of dense and porous hydroxyapatite implants and tissue response in rat femoral defects. J Biomed Mater Res. 2002 ; 62A: 30-36
45. Kuhne JH, Bartl R, Frisch B, Hammer C, Jansson V, Zimmer M. Bone formation in coralline hydroxyapatite effects of pore size studied in rabbits. Acta Orthop Scand. 1994 ; 65: 246-252
46. Hing KA, Best SM, Tanner KE, Bonfield W, Revell PA. Mediation of bone ingrowth in porous hydroxyapatite bone graft substitutes. J Biomed Mater Res. 2004 ; 68A: 187-200
47. Ayers RA, Wolford LM, Bateman TA, Ferguson VL, Simske SJ. Quantification of bone ingrowth into porous block hydroxyapatite in humans. J Biomed Mater Res. 1999 ; 47: 54-59
48. Ryu HS, Kim SJ, Kim JH, Kim H, Hong KS, Chang BS, et al. Fabrication of 1-dimensional porous hydroxyapatite and evaluation of its osteoconductivity. J Mater Sci Mater Med. 2004 ; 15: 267-273
49. Lu XJ, Flautre B, AnselmeK, Hardouin P, Gallur A, Descamps M, Thierry B. Role of interconnections in porous bioceramics on bone recolonization in vitro and in vivo. J Mater Sci Mater Med. 1999 ; 10: 111-120
50. Hutmacher DW. Scaffolds in tissue engineering bone and cartilage. Biomaterials. 2000 ; 21: 2529-2543
51. Hing KA, Best SM, Tanner KE, Bonfield W, Revell PA. Quantification of bone ingrowth within bone-derived porous hydroxyapatite implants of varying density. J Mater Sci Mater Med. 1999 ; 10: 663-670
52. Kokubun S, Kashimoto O, Tanaka Y. Histological verification of bone bonding and ingrowth into porous hydroxyapatite spinous process spacer for cervical laminoplasty. Tohoku J Exp Med. 1994 ; 173: 337-344
53. Flautre B, Descamps M, Delecourt C, Blary MC, Hardouin P. Porous hydroxyapatite ceramic for bone replacement: role of the pores and interconnections-experimental study in the rabbit. J Mater Sci Mater Med. 2001 ; 12: 679-682
54. Ripamonti U. Osteoinduction in porous hydroxyapatite implanted in heterotopic sites of different animal models. Biomaterials. 1996 ; 17: 31-35
55. Urist MR, Huo YK, Brownell AG, Hohl WM, Buyske J, Lietze A, et al. Purification of bovine bone morphogenetic protein by hydroxyapatite chromatography. Proc Natl Acad Sci. 1984 ; 81: 371-375
56. Guo X, Lee KM, Law LP, Chow HKD, Rosier R, Cheng CYJ. Recombinant human bone morphogenetic protein-4 (rhBMP-4) enhanced posterior spinal fusion without decortication. J Orthop Res. 2002 ; 20: 740-746
57. Wang EA, Rosen V, D'Alessandro JS, Bauduy M, Cordes P, Harada T, et al. Recombinant human bone morphogenetic protein induces bone formation. Proc Natl Acad Sci. 1990 ; 87: 2220-2224
58. Ito Y, Tanaka N, Fujimoto Y, Yasunaga Y, Ishida O, Agung M, et al. Bone formation using novel interconnected porous calcium hydroxyapatite ceramic hybridized with cultured marrow stromal stem cells derived from green rat. J Biomed Mater Res. 2004 ; 69A: 454-461
59. Nakasa T, Ishida O, Sunagawa T, Nakamae A, Yasunaga Y, Agung M, et al. Prefabrication of vascularized bone graft using a combination of fibroblast growth factor-2 and vascular bundle implantation into a novel interconnected porous calcium hydroxyapatite ceramic. J Biomed Mater Res. 2005 ; 75A: 350-355
60. Knabe C, Koch C, Rack A, Stiller M. Effect of β-tricalcium phosphate particles with varying porosity on osteogenesis after sinus floor augmentation in humans. Biomaterials. 2008 ; 29: 2249-2258
61. Zheng QX, Zhu TB, Du JY, Hong GX, Li SP, Yan YH, et al. Artificial bone of porous tricalcium phosphate ceramics and its preliminary clinical application. J Tongji Med Univ. 1992 ; 12: 173-178
62. Ogose A, Hotta T, Hatano H, Kawashima H, Tokunaga K, Endo N, et al. Histological examination of β-tricalcium phosphate graft in human femur. J Biomed Mater Res. 2002 ; 63B: 601-604
63. Zerbo IR, Bronckers ALJJ, De Lange G, Van Beek GJ, Burger EH. Histology of human alveolar bone regeneration with a porous tricalcium phosphate. Clin Oral Impl Res. 2001 ; 12: 379-384
64. Zerbo IR, Bronckers ALJJ, De Lange G, Burger EH. Localisation of osteogenic and osteoclastic cells in porous β-tricalcium phosphate particles used for human maxilarry sinus floor elevation. Biomaterials. 2005 ; 26: 1445-1451
65. Zerbo IR, Zijderveld SA, De Boer A, Bronckers ALJJ, De Lange G, Ten Bruggenkate CM, et al. Histomorephometry of human sinus floor augmentation using a porous β-tricalcium phosphate a prospective study. Clin Oral Impl Res. 2004 ; 15: 724-732
66. Laffargue PH, Hildebrand HF, Rtaimate M, Frayssinet P, Amoureux JP, Marchandise X. Evaluation of human recombinant bone morphogenetic protein-2-loaded tricalcium phosphate implants in rabbits' bone defects. Bone. 1999 ; 25: 55S - 58S
67. Matsushita N, Terai H, Okada T, Nozaki K, Inoue H, Miyamoto S, et al. A new bone-inducing biodegradable porous β-tricalcium phosphate. J Biomed Mater Res. 2004 ; 70A: 450-458
68. Liang G, Yang Y, Oh S, Ong JL, Zheng C, Ran J, et al. Ectopic osteoinduction and early degradation of recombinant human bone morphogenetic protein-2-loaded porous β-tricalcium phosphate in mice. Biomaterials. 2005 ; 26: 4265-4271
69. Hoshino M, Egi T, Terai H, Namikawa T, Takaoka K. Repair of long intercalated rib defects using porous beta-tricalcium phosphate cylinders containing recombinant human bone morphogenetic protein-2 in dogs. Biomaterials. 2006 ; 27: 4934-4940
70. Laffargue P, Fialdes P, Frayssinet P, Rtaimate M, Hildebrand HF, Marchandise X. Adsorption and release of insulin-like growth factor-I on porous tricalcium phosphate implant. J Biomed Mater Res. 2000 ; 49: 415-421
71. Steffen T, Stoll T, Arvinte T, Schenk RK. Porous tricalcium phosphate and transforming growth factor used for anterior spine surgery. Eur Spine J. 2001 ; 10: S132 - S140
72. Yuan J, Cui L, Zhang WJ, Liu W, Cao Y. Repair of canine mandibular bone defects with bone marrow stromal cells and porous β-tricalcium phosphate. Biomaterials. 2007 ; 28: 1005-1013
73. Gan Y, Dai K, Zhang P, Tang T, Zhu Z, Lu J. The clinical use of enriched bone marrow stem cells combined with porous beta-tricalcium phosphate in posterior spinal fusion. Biomaterials. 2008 ; 29: 3973-3982
74. Sohier J, Daculsi G, Sourice S, De Groot K, Layrolle P. Porous beta tricalcium phosphate scaffolds used as a BMP-2 delivery system for bone tissue engineering. J Biomed Mater Res. 2009 ; 92A: 1105-1114
75. Tamura K, Sato S, Kishida M, Asano S, Murai M, Ito K. The use of porous β-tricalcium phosphate blocks with platelet-rich plasma as an onlay bone graft biomaterial. J Periodontol. 2007 ; 78: 315-321
76. Ohgushi H, Okumura M, Tamai S, Shors EC, Caplan AI. Marrow cell induced osteogenesis in porous hydroxyapatite and tricalcium phosphate: a comparative histomorphometric study of ectopic bone formation. J Biomed Mater Res. 1990 ; 24: 1563-1570
77. De Aza AH, Chevalier J, Fantozzi G, Schehl M, Torrecillas R. Crack growth resistance of alumina, zirconia and zirconia toughened alumina ceramics for joint prostheses. Biomaterials. 2002 ; 23: 937-945
78. Hatton A, Nevelos JE, Nevelos AA, Banks RE, Fisher J, Ingham E. Alumina-alumina artificial hip joints Part I: a histological analysis and characterization of wear debris by laser capture microdissection of tissues retrieved at revision. Biomaterials. 2002 ; 23: 3429-3440
79. Willmann G, Fruh HJ, Pfaff HG. Wear characteristics of sliding pairs of zirconia (Y-TZP) for hip endoprostheses. Biomaterials. 1996 ; 17: 2157-2162
80. Eckert KL, Mathey M, Mayer J, Homberger FR, Thomann PE, Groscurth P, et al. Preparation and in vivo testing of porous alumina ceramics for cell carrier applications. Biomaterials. 2000 ; 21: 63-69
81. Padera RF, Colton CK. Time course of membrane microarchitecture-driven neovasvularization. Biomaterials. 1996 ; 17: 277-284
82. Bose S, Darsell J, Hosick HL, Yang L, Sarka DK, Bandyopadhyay A. Processing and characterization of porous alumina scaffolds. J Mater Sci Mater Med. 2002 ; 13: 23-28
83. Karlsson M, Palsgard E, Wilshaw PR, Di Silvio L. Initial in vitro interaction of osteoblasts with nano-porous alumina. Biomaterials. 2003 ; 24: 3039-3046
84. Walpole AR, Xia Z, Wilson CW, Triffitt JT, Wilshaw PR. A novel bano-porous alumina biomaterial with potential for loading with bioactive materials. J Biomed Mater Res. 2009 ; 90A: 46-54
85. Drouin JM, Cales B, Chevalier J, Fantozzi G. Fatigue behavior of zirconia hip joint heads experimental results and finite element analysis. J Biomed Mater Res. 1997 ; 34: 149-155
86. Helmer JD, Driskell TD Symposium on Use of Ceramics as Surgical Implants. South Carolina: Clemson University ; 1969:
87. Christel P, Meunier A, Dorlot JM, Crolet JM, Witvoet J, Sedel L, et al. Biomechanical compatibility and design of ceramic implants for orthopedic Surgery. Ann N. Y. Acad Sci. 1988 ; 523: 234-256
88. Chevalier J. What future for zirconia as a biomaterial?. Biomaterials. 2006 ; 27: 535-543
89. Kim HW, Lee SY, Bae CJ, Noh YJ, Kim HE, Kim HM, et al. Porous ZrO2 bone scaffold coated with hydroxyapatite with fluoroapatite intermediate layer. Biomaterials. 2003 ; 24: 3277-3284
90. Kim HW, Kim HE, Salih V, Knowles JC. Dissolution control and cellular responses of calcium phosphate coatings on zirconia porous scaffold. J Biomed Mater Res. 2004 ; 68A: 522-530
91. Kim HW, Kim HE, Knowles JC. Hard-tissue-engineered zirconia porous scaffolds with hydroxyapatite sol-gel and slurry coatings. J Biomed Mater Res. 2004 ; 70B: 270-277
92. Kim HW, Shin SY, Kim HE, Lee YM, Chung CP, Lee HH, et al. Bone formation on the apatite-coated zirconia porous scaffolds within a rabbit calvarial defect. J Biomater Appl. 2008 ; 22: 485-504
93. Lew KS, Othman R, Yeoh FY. Synthesis and characterization of mesoporous hydroxyapatite. Adv Sci Tech. 2010 ; 63: 152-157
94. Xia Z, Liao L, Zhao S. Synthesis of mesoporous hydroxyapatite using a modified hard-templating route. Mater Res Bull. 2009 ; 44: 1626-1629
95. Zhao YF, Ma J. Triblock polymer templating synthesis of mesostructured hydroxyapatite. Microporous Mesoporous Mater. 2005 ; 87: 110-117
96. Yao J, Tjandra W, Chen YZ, Tam KC, Ma J, Soh B. Hydroxyapatite nanostructure material derived using cationic surfactant as a template. J Mater Chem. 2003 ; 13: 3053-3057