SiO2 and ZnO dopants in three-dimensionally printed tricalcium phosphate bone tissue engineering scaffolds enhance osteogenesis and angiogenesis in vivo

Acta Biomaterialia

Volumn 9, Issue 11, 2013, Pages 9137-9148

  Fielding, Gary ^a   Bose, Susmita ^a  

^a Washington State University   (United States)

Author keywords

3 D printing; Bone tissue engineering; Calcium phosphate; Dopants; Scaffold

Indexed keywords

3D PRINTERS; BONE; CALCIUM PHOSPHATE; II-VI SEMICONDUCTORS; SCAFFOLDS (BIOLOGY); SILICON OXIDES; TRACE ELEMENTS; TRANSMISSION CONTROL PROTOCOL; ZINC OXIDE;

3-D PRINTING; ANGIOGENESIS; BONE GROWTH; BONE TISSUE ENGINEERING; CALCIUM PHOSPHATE MATERIALS; IN-VIVO; OSTEOGENESIS; OXIDE DOPANTS; TISSUE ENGINEERING SCAFFOLD; TRI-CALCIUM PHOSPHATES;

SILICA;

ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME; CALCIUM PHOSPHATE; COLLAGEN TYPE 1; OSTEOCALCIN; SILICON DIOXIDE; TISSUE SCAFFOLD; ZINC OXIDE; ACID PHOSPHATASE; ION; ISOENZYME; TARTRATE-RESISTANT ACID PHOSPHATASE;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; BONE GROWTH; BONE REGENERATION; BONE TISSUE; ENZYME ACTIVITY; FIELD EMISSION SCANNING ELECTRON MICROSCOPY; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MORPHOMETRICS; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; OSTEOCLAST ACTIVITY; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RAT; TISSUE ENGINEERING; ANIMAL; BLOOD VESSEL; BONE; CHEMISTRY; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; IMPLANT; METABOLISM; MOUSE; OSTEOCLAST; PHYSIOLOGY; PRINTING; PROCEDURES; SPRAGUE DAWLEY RAT; TISSUE SCAFFOLD; ULTRASTRUCTURE; URINE; 3-D PRINTING; BONE TISSUE ENGINEERING; DOPANTS; DRUG EFFECT; METHODOLOGY; SCAFFOLD;

MURINAE;

ACID PHOSPHATASE; ANIMALS; BLOOD VESSELS; BONE AND BONES; CALCIUM PHOSPHATES; COLLAGEN TYPE I; IMPLANTS, EXPERIMENTAL; IONS; ISOENZYMES; MICE; NEOVASCULARIZATION, PHYSIOLOGIC; OSTEOCALCIN; OSTEOCLASTS; OSTEOGENESIS; PRINTING; RATS; RATS, SPRAGUE-DAWLEY; SILICON DIOXIDE; TISSUE ENGINEERING; TISSUE SCAFFOLDS; ZINC OXIDE;

3-D PRINTING; BONE TISSUE ENGINEERING; CALCIUM PHOSPHATE; DOPANTS; SCAFFOLD;

EID: 84885077192     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2013.07.009     Document Type: Article

References (57)

1. P.W. Brown Calcium phosphates in biomedical engineering 2nd ed. Encyclopedia of materials: science and technology 2001 Elsevier Oxford 893 897
2. S. Bose, and S. Tarafder Calcium phosphate ceramic systems in growth factor and drug delivery for bone tissue engineering - a review Acta Biomater 8 2012 1401 1421
3. M. Yamada, M. Shiota, and Y. Yamashita Histological and histomorphometrical comparative study of the degradation and osteoconductive characteristics of α- and β-tricalcium phosphate in block grafts J Biomed Mater Res B Appl Biomater 82B 2007 139 148 (Pubitemid 47015363)
4. J.E. Davies Mechanisms of endosseous integration Int J Prosthodont 11 1998 391 401 (Pubitemid 128513397)
5. S.J. Hollister Porous scaffold design for tissue engineering Nat Mater 4 2005 518 524 (Pubitemid 40952745)
6. J. Franco, A.P. Launey, and E.S. Tomsia Direct write assembly of calcium phosphate scaffolds using a water-based hydrogel Acta 6 2010 218 228
7. E. Vorndran, M. Klarner, and U. Klammert 3D powder printing of β-tricalcium phosphate ceramics using different strategies Adv Eng Mater 10 2008 B67 B71
8. A. Khalyfa, S. Vogt, and J. Weisser Development of a new calcium phosphate powder-binder system for the 3D printing of patient specific implants J Mater Sci Mater Med 18 2007 909 916 (Pubitemid 46764024)
9. G.A. Fielding, A. Bandyopadhyay, and S. Bose Effects of SiO2 and ZnO doping on mechanical and biological properties of 3D printed TCP scaffolds Dent Mater 28 2012 113 122
10. T. Albrektsson, and C. Johansson Osteoinduction, osteoconduction and osseointegration Eur Spine J 10 Suppl. 2 2001 S96 S101
11. P. Habibovic, H. Yuan, and C.M. van der Valk 3D microenvironment as essential element for osteoinduction by biomaterials Biomaterials 26 2005 3565 3575 (Pubitemid 40038151)
12. O. Chan, M.J. Coathup, and A. Nesbitt The effects of microporosity on osteoinduction of calcium phosphate bone graft substitute biomaterials Acta Biomater 8 2012 2788 2794
13. B. Otsuki, M. Takemoto, and S. Fujibayashi Pore throat size and connectivity determine bone and tissue ingrowth into porous implants: three-dimensional micro-CT based structural analyses of porous bioactive titanium implants Biomaterials 27 2006 5892 5900 (Pubitemid 44332516)
14. B. Li, X. Liao, and L. Zheng Effect of nanostructure on osteoinduction of porous biphasic calcium phosphate ceramics Acta Biomater 8 2012 3794 3804
15. T. Matsumoto, M. Okazaki, and A. Nakahira Modification of apatite materials for bone tissue engineering and drug delivery carriers Curr Med Chem 14 2007 2726 2733 (Pubitemid 350048326)
16. M. Yoshinari, Y. Oda, and T. Inoue Bone response to calcium phosphate-coated and bisphosphonate-immobilized titanium implants Biomaterials 23 2002 2879 2885 (Pubitemid 34497078)
17. I. Martin, A. Muraglia, and G. Campanile Fibroblast growth factor-2 supports ex vivo expansion and maintenance of osteogenic precursors from human bone marrow Endocrinology 138 1997 4456 4462 (Pubitemid 27408494)
18. S.K. Lan Levengood, S.J. Polak, and M.J. Poellmann The effect of BMP-2 on micro- and macroscale osteointegration of biphasic calcium phosphate scaffolds with multiscale porosity Acta Biomater 6 2010 3283 3291
19. M. Bohner Silicon-substituted calcium phosphates-a critical view Biomaterials 30 2009 6403 6406
20. S. Tarafder 3D printed tricalcium phosphate bone tissue engineering scaffolds: effect of SrO and MgO doping on in vivo osteogenesis in a rat distal femoral defect model Biomater Sci 2013 10.1039/c3bm60132c
21. 2 dopants J Am Ceram Soc 89 2006 2675 2688 (Pubitemid 44266407)
22. 2 doped β-TCP Bone 48 2011 1282 1290
23. S.S. Banerjee, S. Tarafder, and N.M. Davies Understanding the influence of MgO and SrO binary doping on the mechanical and biological properties of [beta]-TCP ceramics Acta Biomater 6 2010 4167 4174
24. A. Obata, S. Tokuda, and T. Kasuga Enhanced in vitro cell activity on silicon-doped vaterite/poly (lactic acid) composites Acta Biomater 5 2009 57 62
25. M. Mastrogiacomo, A. Papadimitropoulos, and A. Cedola Engineering of bone using bone marrow stromal cells and a silicon-stabilized tricalcium phosphate bioceramic: evidence for a coupling between bone formation and scaffold resorption Biomaterials 28 2007 1376 1384 (Pubitemid 46016949)
26. A.M. Pietak, J.W. Reid, and M.J. Stott Silicon substitution in the calcium phosphate bioceramics Biomaterials 28 2007 4023 4032 (Pubitemid 47048372)
27. J.C.D. Eisinger Effects of silicon, fluoride, etidronate and magnesium on bone mineral density: a retrospective study Magnesium Res 6 1993 247 249
28. C.M. Botelho, R.A. Brooks, and S.M. Best Human osteoblast response to silicon-substituted hydroxyapatite J Biomed Mater Res A 79 2006 723 730 (Pubitemid 44845188)
29. M. Yamaguchi Role of nutritional zinc in the prevention of osteoporosis Mol Cell Biochem 338 2009 241 254
30. M. Yamaguchi, and M.N. Weitzmann Zinc stimulates osteoblastogenesis and suppresses osteoclastogenesis by antagonizing NF-κB activation Mol Cell Biochem 355 2011 179 186
31. I.S. Kwun, Y.E. Cho, and R.A.R. Lomeda Zinc deficiency suppresses matrix mineralization and retards osteogenesis transiently with catch-up possibly through Runx 2 modulation Bone 46 2010 732 741
32. M. Yamaguchi, M. Goto, and S. Uchiyama Effect of zinc on gene expression in osteoblastic MC3T3-E1 cells: enhancement of Runx2, OPG, and regucalcin mRNA expressions Mol Cell Biochem 312 2008 157 166
33. J. Reginster, O. Saltman, and P. Franchimont Trace elements and postmenopausal osteoporosis: a preliminary study of decreased serum manganese J Nutr 111 1981 1641 1647
34. W. Xue, K. Dahlquist, and A. Banerjee Synthesis and characterization of tricalcium phosphate with Zn and Mg based dopants J Mater Sci Mater Med 19 2008 2669 2677
35. K.P. Egan, T.A. Brennan, and R.J. Pignolo Bone histomorphometry using free and commonly available software Histopathology 61 2012 1168 1173
36. Q. Wang, Q. Chen, and J. Zhu Effects of pore shape and porosity on the properties of porous LNKN ceramics as bone substitute Mater Chem Phys 109 2008 488 491 (Pubitemid 351446069)
37. S. Van Bael, Y.C. Chai, and S. Truscello The effect of pore geometry on the in vitro biological behavior of human periosteum-derived cells seeded on selective laser-melted Ti6Al4V bone scaffolds Acta Biomater 8 2012 2824 2834
38. M. Bohner, G.H. van Lenthe, and S. Grünenfelder Synthesis and characterization of porous beta-tricalcium phosphate blocks Biomaterials 26 2005 6099 6105 (Pubitemid 40834284)
39. S. Tarafder, V.K. Balla, and N.M. Davies Microwave-sintered 3D printed tricalcium phosphate scaffolds for bone tissue engineering J Tissue Eng Regener Med 2012 10.1002/term.555
40. S.J. Polak, S.K.L. Levengood, and M.B. Wheeler Analysis of the roles of microporosity and BMP-2 on multiple measures of bone regeneration and healing in calcium phosphate scaffolds Acta Biomater 7 2011 1760 1771
41. K.B. Hadley, S.M. Newman, and J.R. Hunt Dietary zinc reduces osteoclast resorption activities and increases markers of osteoblast differentiation, matrix maturation, and mineralization in the long bones of growing rats J Nutr Biochem 21 2010 297 303
42. M. Hie, N. Iitsuka, and T. Otsuka Zinc deficiency decreases osteoblasts and osteoclasts associated with the reduced expression of Runx2 and RANK Bone 49 2011 1152 1159
43. N.B. Matsko, N. Žnidaršič, and I. Letofsky-Papst Silicon: the key element in early stages of biocalcification J Struct Biol 174 2011 180 186
44. K.A. Hing, P.A. Revell, and N. Smith Effect of silicon level on rate, quality and progression of bone healing within silicate-substituted porous hydroxyapatite scaffolds Biomaterials 27 2006 5014 5026 (Pubitemid 44202357)
45. L. Bjerre, C.E. Bünger, and M. Kassem Flow perfusion culture of human mesenchymal stem cells on silicate-substituted tricalcium phosphate scaffolds Biomaterials 29 2008 2616 2627
46. G. Gupta, S. Kirakodu, and A. El-Ghannam Effects of exogenous phosphorus and silicon on osteoblast differentiation at the interface with bioactive ceramics J Biomed Mater Res Part A 95A 2010 882 890
47. H.P. Wiesmann, U. Meyer, and U. Plate Aspects of collagen mineralization in hard tissue formation International review of cytology 2004 Elsevier Oxford 121 156 (Pubitemid 39642962)
48. M. Hie, and I. Tsukamoto Administration of zinc inhibits osteoclastogenesis through the suppression of RANK expression in bone Eur J Pharmacol 668 2011 140 146
49. C.D. Seaborn, and F.H. Nielsen Silicon deprivation decreases collagen formation in wounds and bone, and ornithine transaminase enzyme activity in liver Biol Trace Elem Res 89 2002 251 261 (Pubitemid 35335240)
50. B. Sommer, M. Bickel, and W. Hofstetter Expression of matrix proteins during the development of mineralized tissues Bone 19 1996 371 380 (Pubitemid 26370839)
51. M. Yamaguchi, and M. Hashizume Effect of β-alanyl-L-histidinato zinc on protein components in osteoblastic MC3T3-El cells: increase in osteocalcin, insulin-like growth factor-I and transforming growth factor-β Mol Cell Biochem 136 1994 163 169
52. 2O system) ions Acta Biomater 5 2009 3536 3547
53. A.M.C. Barradas, H.A.M. Fernandes, and N. Groen A calcium-induced signaling cascade leading to osteogenic differentiation of human bone marrow-derived mesenchymal stromal cells Biomaterials 33 2012 3205 3215
54. W. Zhai, H. Lu, and L. Chen Silicate bioceramics induce angiogenesis during bone regeneration Acta Biomater 8 2012 341 349
55. Y. Hanai, H. Tokuda, and E. Yasuda Up-regulation by zinc of FGF-2-induced VEGF release throughenhancing p44/p42 MAP kinase activation in osteoblasts Life Sci 80 2006 230 234 (Pubitemid 44853990)
56. W.R. Holloway, F.M. Collier, and R.E. Herbst Osteoblast-mediated effects of zinc on isolated rat osteoclasts: inhibition of bone resorption and enhancement of osteoclast number Bone 19 1996 137 142 (Pubitemid 26283227)
57. G.R. Beck, S.-W. Ha, and C.E. Camalier Bioactive silica-based nanoparticles stimulate bone-forming osteoblasts, suppress bone-resorbing osteoclasts, and enhance bone mineral density in vivo Nanomed Nanotechnol Biol Med 8 2012 793 803