Microporous calcium phosphate ceramics driving osteogenesis through surface architecture

Journal of Biomedical Materials Research - Part A

Volumn 103, Issue 3, 2015, Pages 1188-1199

  Zhang, Jingwei ^a,b   Barbieri, Davide ^c   Ten Hoopen, Hetty ^a   De Bruijn, Joost D ^a,c,d   Van Blitterswijk, Clemens A ^a   Yuan, Huipin ^a,c,e  

^a UNIVERSITY OF TWENTE   (Netherlands)

^b SOUTHWEST JIAOTONG UNIVERSITY   (China)

^c XPand Biotechnology BV   (Netherlands)

^d QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^e SICHUAN UNIVERSITY   (China)

Author keywords

Bone grafting; Calcium phosphate ceramics; Microstructure; Osteogenesis; Surface architecture

Indexed keywords

ARCHITECTURE; BONE; CALCIUM; CERAMIC MATERIALS; ION EXCHANGE; MICROPOROSITY; MICROSTRUCTURE; SURFACE ROUGHNESS;

BONE GRAFTING; CALCIUM PHOSPHATE CERAMICS; CHEMICAL COMPOSITIONS; EQUIVALENT SURFACE AREAS; OSTEOGENESIS; SURFACE ARCHITECTURES; SURFACE MINERALIZATION; SURFACE ROUGHNESS (RA);

CALCIUM PHOSPHATE;

PROTEIN; BONE PROSTHESIS; CALCIUM PHOSPHATE; CERAMICS;

ADSORPTION; ADULT; ANIMAL EXPERIMENT; ARTICLE; BONE DEVELOPMENT; BONE MASS; CALCIUM PHOSPHATE CERAMIC; CERAMIC PROSTHESIS; CHEMICAL COMPOSITION; CONTROLLED STUDY; DENSITY; MALE; MINERALIZATION; NONHUMAN; OSSIFICATION; PARASPINAL MUSCLE; PHYSICAL CHEMISTRY; SURFACE PROPERTY; ANIMAL; BONE PROSTHESIS; CERAMICS; CHEMISTRY; DOG; DRUG EFFECTS; HUMAN; MATERIALS TESTING; PHARMACOLOGY; POROSITY;

ANIMALS; BONE SUBSTITUTES; CALCIUM PHOSPHATES; CERAMICS; DOGS; HUMANS; MALE; MATERIALS TESTING; OSTEOGENESIS; POROSITY;

EID: 84922988635     PISSN: 15493296     EISSN: 15524965     Source Type: Journal    
DOI: 10.1002/jbm.a.35272     Document Type: Article

References (58)

1. Kanzler B, Kuschert SJ, Liu Y.H., Mallo M. Hoxa-2 restricts the chondrogenic domain and inhibits bone formation during development of the branchial area. Development 1998; 125:2587-2597.
2. Gorski J. Is all bone the same? Distinctive distributions and properties of non-collagenous matrix proteins in lamellar vs. woven bone imply the existence of different underlying osteogenic mechanisms. Crit Rev Oral Biol Med 1998; 9:201-223.
3. Van der Stok J, van Lieshout EM, El-Massoudi Y, van Kralingen GH, Patka P. Bone substitutes in the Netherlands-A systematic literature review. Acta Biomater 2011; 7:739-750.
4. Ripamonti U. Osteoinduction in porous hydroxyapatite implanted in heterotopic sites of different animal models. Biomaterials 1998; 17:31-35.
5. Yang Z, Yuan H, Tong W., Zou P, Chen W, Zhang X. Osteogenesis in extraskeletally implanted porous calcium phosphate ceramics: Variability among different kinds of animals. Biomaterials 1996; 17:2131-2137.
6. 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.
7. Siddappa R, Martens A, Doorn J., Leusink A, Olivo C, Licht R., van Rijn L, Gaspar C, Fodde R, Janssen F, van Blitterswijk CA, de Boer J. cAMP/PKA pathway activation in human mesenchymal stem cells in vitro results in robust bone formation in vivo. Proc Natl Acad Sci U S A 2008; 105:7281-7286.
8. Yamasaki H, Sakai H. Osteogenic response to porous hydroxyapa-tite ceramics under the skin of dogs. Biomaterials 1992; 13:308-312.
9. Klein C, de Groot K, Chen W, Li Y., Zhang X. Osseous substance formation induced in porous calcium phosphate ceramics in soft tissues. Biomaterials 1994; 15:31-34.
10. Ripamonti U. The morphogenesis of bone in replicas of porous hydroxyapatite obtained from conversion of calcium carbonate exoskeletons of coral. J Bone Joint Surg Am 1991; 73:692-703.
11. Ripamonti U, Richter PW, Thomas ME. Self-inducing shape memory geometric cues embedded within smart hydroxyapatite-based biomimetic matrices. Plast Reconstr Surg 2007; 120:1796-1807.
12. Ripamonti U, Crooks J, Khoali L., Roden L. The induction of bone formation by coral-derived calcium carbonate/hydroxyapatite constructs. Biomaterials 2009; 30:1428-1439.
13. Yuan H, van Blitterswijk CA, de Groot K, de Bruijn JD. Cross-species comparison of ectopic bone formation in biphasic calcium phosphate (BCP) and hydroxyapatite (HA) scaffolds. Tissue Eng 2006; 12:1607-1615.
14. Gosain AK, Song L, Riordan P., Amarante MT, Nagy PG, Wilson CR, Toth J.M., Ricci JL. A 1-year study of osteoinduction in hydroxyapatite-derived biomaterials in an adult sheep model. I. Plast Reconstr Surg 2002; 109:619-630.
15. Habibovic P, Yuan H, van der Valk CM, Meijer G, van Blitterswijk CA, de Groot K. 3D microenvironment as essential element for osteoinduction by biomaterials. Biomaterials 2005; 26:3565-3575.
16. Habibovic P, Sees TM, van den Doel MA, van Blitterswijk CA, de Groot K. Osteoinduction by biomaterials-Physicochemical and structural influences. J Biomed Mater Res A 2006; 77:747-762.
17. Yuan H, Yang Z, Li Y., Zhang X, de Bruijn JD, de Groot K. Osteoinduction by calcium phosphate biomaterials. J Mater Sci Mater Med 1998; 9:723-726.
18. Yuan H, Yang Z, de Bruijn JD, de Groot K, Zhang X. Material-dependent bone induction by calcium phosphate ceramics: A 2.5-year study in dog. Biomaterials 2001; 22:2617-2623.
19. Yuan H, de Bruijn JD, Li Y, Feng J, Yang Z., de Groot K, Zhang X. Bone formation induced by calcium phosphate ceramics in soft tissue of dogs: A comparative study between porous α-TCP and β-TCP. J Mater Sci Mater Med 2001; 12:7-13.
20. Kondo N, Ogose A, Tokunaga K., Umezu H, Arai K, Kudo N., Hoshino M, Inoue H, Irie H, Kuroda K, Mera H, Endo N. Osteoin-duction with highly purified β-tricalcium phosphate in dog dorsal muscles and the proliferation of osteoclasts before heterotopic bone formation. Biomaterials 2006; 27:4419-4427.
21. Yuan H, Fernandes H, Habibovic P., de Boer J, Barradas A, de Ruiter A, Walsh WR, van Blitterswijk CA, de Bruijn JD. Osteoin-ductive ceramics as a synthetic alternative to autologous bone grafting. Proc Natl Acad Sci U S A 2010; 107:13614-13619.
22. Yuan H, van Blitterswijk CA, de Groot K, de Bruijn JD. A comparison of bone formation in biphasic calcium phosphate (BCP) and hydroxyapatite (HA) implanted in muscle and bone of dogs at different time periods. J Biomed Mater Res A 2006; 78:139-147.
23. le Nihouannen D, Saffarzadeh A, Gauthier O., Moreau F, Pilet P, Spaethe R., Layrolle P, Daculsi G. Bone tissue formation in sheep muscles induced by a biphasic calcium phosphate ceramic and fibrin glue composite. J Mater Sci Mater Med 2008; 19:667-675.
24. Yuan H, van den Doel M, Li S, van Blitterswijk CA, de Groot K, de Bruijn JD. A comparison of the osteoinductive potential of two calcium phosphate ceramics implanted intramuscularly in goats. J Mater Sci Mater Med 2002; 13:1271-1275.
25. Habibovic P, van der Valk C, van Blitterswijk CA, de Groot K, Meijer G. Influence of octacalcium phosphate coating on osteoin-ductive properties of biomaterials. J Mater Sci Mater Med 2004; 15:373-380.
26. Li JP, Habibovic P, Yuan H., van den Doel M, Wilson CE, de Wijn JR, van Blitterswijk CA, de Groot K. Biological performance in goats of a porous titanium alloy-biphasic calcium phosphate composite. Biomaterials 2007; 28:4209-4218.
27. Habibovic P, Kruyt MC, Juhl M.V., Clyens S., Martinetti R, Dolcini L, Theilgaard N., van Blitterswijk CA. Comparative in vivo study of six hydroxyapatite-based bone graft substitutes. J Orth Res 2008; 26:1363-1370.
28. Kurashina K, Kurita H, Wu Q., Ohtsuka A, Kobayashi H. Ectopic osteogenesis with biphasic ceramics of hydroxyapatite and trical-cium phosphate in rabbits. Biomaterials 2002; 23:407-412.
29. Habibovic P, Yuan H, van den Doel M, Sees TM, van Blitterswijk CA, de Groot K. Relevance of osteoinductive biomaterials in critical-sized orthotopic defect. J Orth Res 2006; 24:867-876.
30. Ripamonti U, Crooks J, Tucker M., Sampath T, Rueger D, Reddi A. Long-term evaluation of bone formation by osteogenic protein 1 in the baboon and relative efficacy of bone-derived bone morpho-genetic proteins delivered by irradiated xenogeneic collagenous matrices. J Bone Min Res 2000; 15:1798-1809.
31. Duneas N, Crooks J, Ripamonti U. Transforming growth factor-b 1: Induction of bone morphogenetic protein genes expression during endochondral bone formation in the baboon, and syner-gistic interaction with osteogenic protein-1 (BMP-7). Growth Factors 1998; 15:259-277.
32. Ripamonti U, Heliotis M, Rueger D., Sampath T. Induction of cementogenesis by recombinant human osteogenic protein-1 (hOP-1/BMP-7) in the baboon (Papio ursinus). Arch Oral Biol 1996; 41:121-126.
33. Barradas A, Fernandes HA, Groen N, Chai Y.C., Schrooten J., van de Peppel J, van Leeuwen JP, van Blitterswijk CA, de Boer J. A calcium-induced signaling cascade leading to osteogenic differentiation of human bone marrow-derived mesenchymal stromal cells. Biomaterials 2012; 33:3205-3215.
34. Geesink R, de Groot K, Klein C. Bonding of bone to apatite-coated implants. J Bone Joint Surg Br 1988; 70:17-22.
35. Fujibayashi S, Neo M, Kim H.M., Kokubo T., Nakamura T. Osteoinduction of porous bioactive titanium metal. Biomaterials 2004; 25: 443-450.
36. Hu X, Park SH, Gil E.S., Xia XX, Weiss AS, Kaplan DL. The influence of elasticity and surface roughness on myogenic and osteogenic-differentiation of cells on silk-elastin biomaterials. Biomaterials 2011; 32:8979-8989.
37. Anselme K, Bigerelle M. Topography effects of pure titanium substrates on human osteoblast long-term adhesion. Acta Biomater 2005; 1:211-222.
38. Bowers KT, Keller JC, Randolph B.A., Wick DG, Michaels CM. Optimization of surface micromorphology for enhanced osteoblast responses in vitro. Int J Oral Maxillofac Implants 1992; 7:302-310.
39. 2 nanoparticle thin films. Biomaterials 2006; 27:4296-4303.
40. Zhao G, Raines A, Wieland M., Schwartz Z, Boyan B. Requirement for both micron-and submicron scale structure for synergistic responses of osteoblasts to substrate surface energy and topography. Biomaterials 2007; 28:2821-2829.
41. Mendonca G, Mendonca D, Simoes LGP, Araujo AL, Leite E.R., Duarte WR, Aragao FJ, Cooper LF. The effects of implant surface nanoscale features on osteoblast-specific gene expression. Biomaterials 2009; 30:4053-4062.
42. Oh S, Brammer KS, Li Y, Teng D., Engler AJ, Chien S, Jin S. Stem cell fate dictated solely by altered nanotube dimension. Proc Natl Acad Sci U S A 2009; 106:2130-2135.
43. Dalby MJ, McCloy D, Robertson M., Agheli H, Sutherland D, Affrossman S., Oreffo RO. Osteoprogenitor response to semi-ordered and random nanotopographies. Biomaterials 2006; 27: 2980-2987.
44. Kilian KA, Bugarija B, Lahn B.T., Mrksich M. Geometric cues for directing the differentiation of mesenchymal stem cells. Proc Natl Acad Sci U S A 2010; 107:4872-4877.
45. Dalby MJ, Gadegaard N, Tare R., Andar A, Riehle MO, Herzyk P, Wilkinson C.D., Oreffo RO. The control of human mesenchymal cell differentiation using nanoscale symmetry and disorder. Nature Mater 2007; 6:997-1003.
46. Fu J, Wang YK, Yang M.T., Desai RA, Yu X, Liu Z, Chen CS. Mechanical regulation of cell function with geometrically modulated elastomeric substrates. Nat Methods 2010; 7:733-736.
47. Kokubo T, Takadama H. How useful is SBF in predicting in vivo bone bioactivity? Biomaterials 2006; 27:2907-2915.
48. Barradas AMC, Yuan H, van Blitterswijk CA, Habibovic P. Osteoinductive biomaterials: Current knowledge of properties, experimental models and biological mechanisms. Eur Cell Mater 2011; 21:407-429.
49. Curtis A, Wilkinson C. Nantotechniques and approaches in biotechnology. Trends Biotechnol 2001; 19:97-101.
50. Galli C, Piemontese M, Lumetti S., Manfredi E, Macaluso G, Passeri G. The importance of WNT pathways for bone metabolism and their regulation by implant topography. Eur Cells Mater 2012; 24:46-59.
51. Chai YC, Truscello S, van Bael S, Luyten FP, Vleugels J, Schrooten J. Perfusion electrodeposition of calcium phosphate on additive manufactured titanium scaffolds for bone engineering. Acta Biomater 2011; 7: 2310-2319.
52. Winter GD, Simpson BJ. Heterotopic bone formation in a synthetic sponge in the skin of young pigs. Nature 1969; 223:88-90.
53. Barbieri D, Renard AJS, de Bruijn JD, Yuan H. Heterotopic bone formation by nano-apatite containing poly(D, L-lactide) composites. Eur Cells Mater 2010; 19:252-261.
54. Arafat MT, Lam CXF, Ekaputra AK, Wong S.Y., Li X., Gibson I. Bio-mimetic composite coating on rapid prototyped scaffolds for bone tissue engineering. Acta Biomater 2011; 7:809-820.
55. Vaquette C, Ivanovski S, Hamlet S.M., Hutmacher DW. Effect of culture conditions and calcium phosphate coating on ectopic bone formation. Biomaterials 2013; 34:5538-5551.
56. Anderson JM, Rodriguez A, Chang DT. Foreign body reaction to biomaterials. Semin Immunol 2008; 20:86-100.
57. Davies JE. Understanding peri-implant endosseous healing. J Dent Ed 2003; 67:932-949.
58. Holzapfel BM, Wagner F, Loessner D., Holzapfel NP, Thibaudeau L, Crawford R, Ling M.T., Clements JA, Russell PJ, Hutmacher DW. Species-specific homing mechanisms of human prostate cancer metastasis in tissue engineered bone. Biomaterials 2014; 35:4108-4115.