A review of materials, fabrication methods, and strategies used to enhance bone regeneration in engineered bone tissues

Journal of Biomedical Materials Research - Part B Applied Biomaterials

Volumn 85, Issue 2, 2008, Pages 573-582

  Stevens, Brian ^a   Yang, Yanzhe ^a   Mohandas, Arunesh ^b,c   Stucker, Brent ^a   Nguyen, Kytai Truong ^a,b,c  

^a Utah State University   (United States)

^b The University of Texas at Arlington   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Bone; Bone graft; Bone ingrowth; Scaffolds; Tissue engineering

Indexed keywords

BIOMIMETIC MATERIALS; BIOMOLECULES; BONE; RAPID PROTOTYPING; SCAFFOLDS; TISSUE ENGINEERING;

ALLOGRAFTS; BONE GRAFTS; BONE INGROWTH; NANOTOPOGRAPHY;

GRAFTS;

BIOREACTOR; BONE GRAFT; BONE GROWTH; BONE REGENERATION; BONE TISSUE; PRINTING; REVIEW; TISSUE ENGINEERING;

ANIMALS; BIOCOMPATIBLE MATERIALS; BIOMIMETIC MATERIALS; BIOPROSTHESIS; BONE AND BONES; BONE REGENERATION; BONE SUBSTITUTES; HUMANS; TISSUE ENGINEERING;

EID: 42649095181     PISSN: 15524973     EISSN: 15524981     Source Type: Journal    
DOI: 10.1002/jbm.b.30962     Document Type: Review

References (115)

1. Laurencin C, Khan Y, El-Amin SF. Bone graft substitutes. Expert Rev Med Devices 2006;3:49-57.
2. Greenwald AS, Boden SD, Goldberg VM, Khan Y, Laurencin CT, Rosier RN. Bone-graft substitutes: Facts, fictions, and applications. J Bone Joint Surg Am 2001;83:98-103.
3. Karageorgiou V, Kaplan D. Porosity of 3D biomaterial scaffolds and osteogenesis. Biomaterials 2005;26:5474-5491.
4. Zeltinger J, Sherwood JK, Graham DA, Mèueller R, Griffith LG. Effect of pore size and void fraction on cellular adhesion, proliferation, and matrix deposition. Tissue Eng 2001;7:557-572.
5. Mastrogiacomo M, Scaglione S, Martinetti R, Dolcini L, Beltrame F, Cancedda R, Quarto R. Role of scaffold internal structure on in vivo bone formation in macroporous calcium phosphate bioceramics. Biomaterials 2006;27:3230-3237.
6. Smith IO, Baumann MJ, McCabe LR. Electrostatic interactions as a predictor for osteoblast attachment to biomaterials. J Biomed Mater Res A 2004;70:436-441.
7. Ducheyne P, Qiu Q. Bioactive ceramics: The effect of surface reactivity on bone formation and bone cell function. Biomaterials 1999;20:2287-2303.
8. Dieudonnâe SC, van den Dolder J, de Ruijter JE, Paldan H, Peltola T, van't Hof MA, Happonen RP, Jansen JA. Osteoblast differentiation of bone marrow stromal cells cultured on silica gel and sol-gel-derived titania. Biomaterials 2002;23:3041-3051.
9. Ishaug SL, Yaszemski MJ, Bizios R, Mikos AG. Osteoblast function on synthetic biodegradable polymers. J Biomed Mater Res 1994;28:1445-1453.
10. Athanasiou KA, Agrawal CM, Barber FA, Burkhart SS. Orthopaedic applications for PLA-PGA biodegradable polymers. Arthroscopy 1998;14:726-737.
11. Wang M. Developing bioactive composite materials for tissue replacement. Biomaterials 2003;24:2133-2151.
12. Vermes C, Glant TT, Hallab NJ, Fritz EA, Roebuck KA, Jacobs JJ. The potential role of the osteoblast in the development of periprosthetic osteolysis: Review of in vitro osteoblast responses to wear debris, corrosion products, and cytokines and growth factors. J Arthroplasty 2001;16:95-100.
13. Goodman SB, Ma T, Chiu R, Ramachandran R, Smith RL. Effects of orthopaedic wear particles on osteoprogenitor cells. Biomaterials 2006;27:6096-6101.
14. Vermes C, Chandrasekaran R, Jacobs JJ, Galante JO, Roebuck KA, Glant TT. The effects of particulate wear debris, cytokines, and growth factors on the functions of MG-63 osteoblasts. J Bone Joint Surg Am A 2001;83:201-211.
15. Takei H, Pioletti DP, Kwon SY, Sung KL. Combined effect of titanium particles and TNF-α on the production of IL-6 by osteoblast-like cells. J Biomed Mater Res 2000;52:382-387.
16. Christenson EM, Anseth KS, van den Beucken JJ, Chan CK, Ercan B, Jansen JA, Laurencin CT, Li WJ, Murugan R, Nair LS, Ramakrishna S, Tuan RS, Webster TJ, Mikos AG. Nanobiomaterial applications in orthopedics. J Orthop Res 2007;25:11-22.
17. Laurencin CT, Attawia MA, Elgendy HE, Herbert KM. Tissue engineered bone-regeneration using degradable polymers: The formation of mineralized matrices. Bone 1996;19:93S-99S.
18. Wang M, Joseph R, Bonfield W. Hydroxyapatite-polyethylene composites for bone substitution: Effects of ceramic particle size and morphology. Biomaterials 1998;19:2357-2366.
19. Zhang Y, Tanner KE. Impact behavior of hydroxyapatite reinforced polyethylene composites. J Mater Sci: Mater Med 2003;14:63-68.
20. Sato M, Slamovich EB, Webster TJ. Enhanced osteoblast adhesion on hydrothermally treated hydroxyapatite/titania/poly(lactide-co-glycolide) sol-gel titanium coatings. Biomaterials 2005;26:1349-1357.
21. Arinzeh TL. Mesenchymal stem cells for bone repair: Preclinical studies and potential orthopedic applications. Foot Ankle Clin 2005;10:651-665, viii.
22. Caplan AI. Review: Mesenchymal stem cells: Cell-based reconstructive therapy in orthopedics. Tissue Eng 2005;11:1198-1211.
23. Humes HD. Stem cells: The next therapeutic frontier. Trans Am Clin Climatol Assoc 2005;116:167-183; discussion 183-184.
24. El-Amin SF, Botchwey E, Tuli R, Kofron MD, Mesfin A, Sethuraman S, Tuan RS, Laurencin CT. Human osteoblast cells: Isolation, characterization, and growth on polymers for musculoskeletal tissue engineering. J Biomed Mater Res A 2006;76:439-449.
25. Voegele TJ, Voegele-Kadletz M, Esposito V, Macfelda K, Oberndorfer U, Vecsei V, Schabus R. The effect of different isolation techniques on human osteoblast-like cell growth. Anticancer Res 2000;20:3575-3581.
26. Mehlhorn AT, Niemeyer P, Kaiser S, Finkenzeller G, Stark GB, Sèudkamp NP, Schmal H. Differential expression pattern of extracellular matrix molecules during chondrogenesis of mesenchymal stem cells from bone marrow and adipose tissue. Tissue Eng 2006;12:2853-2862.
27. Shahdadfar A, Frønsdal K, Haug T, Reinholt FP, Brinchmann JE. In vitro expansion of human mesenchymal stem cells: Choice of serum is a determinant of cell proliferation, differentiation, gene expression, and transcriptome stability. Stem Cells (Dayton, Ohio) 2005;23:1357-1366.
28. Stoltz JF, Bensoussan D, Decot V, Ciree A, Netter P, Gillet P. Cell and tissue engineering and clinical applications: An overview. Biomed Mater Eng 2006;16:S3-S18.
29. Peter SJ, Liang CR, Kim DJ, Widmer MS, Mikos AG. Osteoblastic phenotype of rat marrow stromal cells cultured in the presence of dexamethasone, β-glycerolphosphate, and L-ascorbic acid. J Cell Biochem 1998;71:55-62.
30. Morris DC, Masuhara K, Takaoka K, Ono K, Anderson HC. Immunolocalization of alkaline phosphatase in osteoblasts and matrix vesicles of human fetal bone. Bone Miner 1992;19:287-298.
31. Mendes SC, Tibbe JM, Veenhof M, Both S, Oner FC, van Blitterswijk CA, de Bruijn JD. Relation between in vitro and in vivo osteogenic potential of cultured human bone marrow stromal cells. J Mater Sci: Mater Med 2004;15:1123-1128.
32. Mendes SC, Tibbe JM, Veenhof M, Bakker K, Both S, Platenburg PP, Oner FC, de Bruijn JD, van Blitterswijk CA. Bone tissue-engineered implants using human bone marrow stromal cells: Effect of culture conditions and donor age. Tissue Eng 2002;8:911-920.
33. Ramoshebi LN, Matsaba TN, Teare J, Renton L, Patton J, Ripamonti U. Tissue engineering: TGF-β superfamily members and delivery systems in bone regeneration. Expert Rev Mol Med 2002;2002:1-11.
34. Schlegel KA, Donath K, Rupprecht S, Falk S, Zimmermann R, Felszeghy E, Wiltfang J. De novo bone formation using bovine collagen and platelet-rich plasma. Biomaterials 2004;25:5387-5393.
35. Rose FR, Hou Q, Oreffo RO. Delivery systems for bone growth factors - The new players in skeletal regeneration. J Pharm Pharmacol 2004;56:415-427.
36. Chen D, Zhao M, Mundy GR. Bone morphogenetic proteins. Growth Factors (Chur, Switzerland) 2004;22:233-241.
37. Wozney JM, Rosen V. Bone morphogenetic protein and bone morphogenetic protein gene family in bone formation and repair. Clin Orthop Relat Res 1998:26-37.
38. Zou X, Li H, Chen L, Baatrup A, Bèunger C, Lind M. Stimulation of porcine bone marrow stromal cells by hyaluronan, dexamethasone and rhBMP-2. Biomaterials 2004;25:5375-5385.
39. Tan KH, Chua CK, Leong KF, Cheah CM, Gui WS, Tan WS, Wiria FE. Selective laser sintering of biocompatible polymers for applications in tissue engineering. Biomed Mater Eng 2005;15:113-124.
40. Tan KH, Chua CK, Leong KF, Naing MW, Cheah CM. Fabrication and characterization of three-dimensional poly (ether-ether-ketone)/-hydroxyapatite biocomposite scaffolds using laser sintering. Proc Inst Mech Eng Part H: J Eng Med 2005;219:183-194.
41. Temenoff JS, Mikos AG. Injectable biodegradable materials for orthopedic tissue engineering. Biomaterials 2000;21:2405-2412.
42. Shin H, Quinten Ruhâe P, Mikos AG, Jansen JA. In vivo bone and soft tissue response to injectable, biodegradable oligo(poly(ethylene glycol) fumarate) hydrogels. Biomaterials 2003;24:3201-3211.
43. Payne RG, McGonigle JS, Yaszemski MJ, Yasko AW, Mikos AG. Development of an injectable, in situ crosslinkable, degradable polymeric carrier for osteogenic cell populations, Part 2: Viability of encapsulated marrow stromal osteoblasts cultured on crosslinking poly(propylene fumarate). Biomaterials 2002;23:4373-4380.
44. Gutowska A, Jeong B, Jasionowski M. Injectable gels for tissue engineering. Anat Rec 2001;263:342-349.
45. Radomsky ML, Thompson AY, Spiro RC, Poser JW. Potential role of fibroblast growth factor in enhancement of fracture healing. Clin Orthop Relat Res 1998 (355 Suppl):S283-S293.
46. Lanza RP, Robert L, Vacanti J. Principles of tissue engineering.
47. Taqvi S, Roy K. Influence of scaffold physical properties and stromal cell coculture on hematopoietic differentiation of mouse embryonic stem cells. Biomaterials 2006;27:6024-6031.
48. Lu L, Peter SJ, Lyman MD, Lai HL, Leite SM, Tamada JA, Uyama S, Vacanti JP, Langer R, Mikos AG. In vitro and in vivo degradation of porous poly(DL-lactic-co-glycolic acid) foams. Biomaterials 2000;21:1837-1845.
49. Lu L, Peter SJ, Lyman MD, Lai HL, Leite SM, Tamada JA, Vacanti JP, Langer R, Mikos AG. In vitro degradation of porous poly(L-lactic acid) foams. Biomaterials 2000;21:1595-1605.
50. Leong KF, Cheah CM, Chua CK. Solid freeform fabrication of three-dimensional scaffolds for engineering replacement tissues and organs. Biomaterials 2003;24:2363-2378.
51. Yang S, Leong KF, Du Z, Chua CK. The design of scaffolds for use in tissue engineering, Part 2: Rapid prototyping techniques. Tissue Eng 2002;8:1-11.
52. Liao CJ, Chen CF, Chen JH, Chiang SF, Lin YJ, Chang KY. Fabrication of porous biodegradable polymer scaffolds using a solvent merging/particulate leaching method. J Biomed Mater Res 2002;59:676-681.
53. Mikos AG, Sarakinos G, Leite SM, Vacanti JP, Langer R. Laminated three-dimensional biodegradable foams for use in tissue engineering. Biomaterials 1993;14:323-330.
54. Gibson I. Rapid prototyping: A review. In: Bartolo P, editor. Virtual Modeling and Rapid Manufacturing. Leiria, Portugal: CRC; 2005. pp 7-17.
55. Chua CK, Leong KF, Lim CS. Rapid Prototyping: Principles and Applications, 2nd ed. Singapore: World Scientific; 2003.
56. Berry E, Brown JM, Connell M, Craven CM, Efford ND, Radjenovic A, Smith MA. Preliminary experience with medical applications of rapid prototyping by selective laser sintering. Med Eng Phys 1997;19:90-96.
57. Cheah CM, Leong KF, Chua CK, Low KH, Quek HS. Characterization of microfeatures in selective laser sintered drug delivery devices. Proc Inst Mech Eng Part H: J Eng Med 2002;216:369-383.
58. Lu Y, Chen SC. Micro and nano-fabrication of biodegradable polymers for drug delivery. Adv Drug Deliv Rev 2004;56:1621-1633.
59. Razzacki SZ, Thwar PK, Yang M, Ugaz VM, Burns MA. Integrated microsystems for controlled drug delivery. Adv Drug Deliv Rev 2004;56:185-198.
60. Smith AR, Stucker BE. Laser deposition of pure titanium powder onto a cast CoCrMo substrate using laser engineering net shaping (LENS). In: Second International Conference on Advanced Research in Virtual and Rapid Prototyping (VRAP 2005), Leira, Portugal, 2005.
61. Sachlos E, Czernuszka JT. Making tissue engineering scaffolds work. Review: The application of solid freeform fabrication technology to the production of tissue engineering scaffolds. Eur Cell Mater 2003;5:29-39; discussion 39-40.
62. Sachlos E, Reis N, Ainsley C, Derby B, Czernuszka JT. Novel collagen scaffolds with predefined internal morphology made by solid freeform fabrication. Biomaterials 2003;24:1487-1497.
63. Yan Y, Wang X, Pan Y, Liu H, Cheng J, Xiong Z, Lin F, Wu R, Zhang R, Lu Q. Fabrication of viable tissue-engineered constructs with 3D cell-assembly technique. Biomaterials 2005;26:5864-5871.
64. Zein I, Hutmacher DW, Tan KC, Teoh SH. Fused deposition modeling of novel scaffold architectures for tissue engineering applications. Biomaterials 2002;23:1169-1185.
65. Seitz H, Rieder W, Irsen S, Leukers B, Tille C. Three-dimensional printing of porous ceramic scaffolds for bone tissue engineering. J Biomed Mater Res B Appl Biomater 2005;74:782-788.
66. Clinkenbeard RE, Johnson DL, Parthasarathy R, Altan MC, Tan KH, Park SM, Crawford RH. Replication of human tracheobronchial hollow airway models using a selective laser sintering rapid prototyping technique. AIHA J 2002;63:141-150.
67. Landers R, Hèubner U, Schmelzeisen R, Mèulhaupt R. Rapid prototyping of scaffolds derived from thermoreversible hydrogels and tailored for applications in tissue engineering. Biomaterials 2002;23:4437-4447.
68. Cooke MN, Fisher JP, Dean D, Rimnac C, Mikos AG. Use of stereolithography to manufacture critical-sized 3D biodegradable scaffolds for bone ingrowth. J Biomed Mater Res B Appl Biomater 2003;64:65-69.
69. th Annual Solid Freeform Fabrication Symposium, Austin, TX; 2005. pp 434-445.
70. Porter NL, Pilliar RM, Grynpas MD. Fabrication of porous calcium polyphosphate implants by solid freeform fabrication: A study of processing parameters and in vitro degradation characteristics. J Biomed Mater Res 2001;56:504-515.
71. Tan KH, Chua CK, Leong KF, Cheah CM, Cheang P, Abu Bakar MS, Cha SW. Scaffold development using selective laser sintering of polyetheretherketone- hydroxyapatite biocomposite blends. Biomaterials 2003;24:3115-3123.
72. Cruz F, Simoes J, Coole T, Bocking C. Direct manufacturing of hydroxyapatite based bone implants by selective laser sintering. In: Bartolo P, editor. Virtual Modeling and Rapid Manufacturing. Leiria, Portugal: CRC Press; 2005. pp 119-125.
73. Hao L, Savalani MM, Harris RA. Layer manufacturing of polymer/bioceramic implants for bone replacement and tissue growth. In: Bartolo P, editor. Virtual Modeling and Rapid Manufacturing. Leiria, Portugal: CRC Press; 2005. pp 127-134.
74. Coole T, Cruz F, Simoes J, Bocking C. Customization of bioceramic implants using SLS. In: Bartolo P, editor. Virtual Modeling and Rapid Manufacturing. Leiria, Portugal: CRC Press; 2005. p 147-151.
75. Curodeau A, Sachs E, Caldarise S. Design and fabrication of cast orthopedic implants with freeform surface textures from 3D printed ceramic shell. J Biomed Mater Res 2000;53:525-535.
76. Leukers B, Gèulkan H, Irsen SH, Milz S, Tille C, Schieker M, Seitz H. Hydroxyapatite scaffolds for bone tissue engineering made by 3D printing. J Mater Sci: Mater Med 2005;16:1121-1124.
77. Lee M, Dunn JC, Wu BM. Scaffold fabrication by indirect three-dimensional printing. Biomaterials 2005;26:4281-4289.
78. Hutmacher DW, Schantz T, Zein I, Ng KW, Teoh SH, Tan KC. Mechanical properties and cell cultural response of polycaprolactone scaffolds designed and fabricated via fused deposition modeling. J Biomed Mater Res 2001;55:203-216.
79. De Silva MN, Paulsen J, Renn MJ, Odde DJ. Two-step cell patterning on planar and complex curved surfaces by precision spraying of polymers. Biotechnol Bioeng 2006;93:919-927.
80. Ang TH, Sultana FSA, Hutmacher DW, Wong YS, Fuh JYH, Mo XM, Loh HT, Burdet E, Teoh SH. Fabrication of 3D chitosan-hydroxyapatite scaffolds using a robotic dispensing system. Mater Sci Eng C 2002;20:35-42.
81. Landers R, Hubner U, Schmelzeisen R, Mèulhaupt R. Rapid prototyping of hydrogel structures - Scaffolds for artificial organs. Int J Artif Organs 2002;25:622-623.
82. Das S, Hollister SJ, Flanagan CL, Adewunmi A, Bark K, Chen C, Ramaswamy K, Rose D, Widjaja E. Freeform fabrication of nylon-6 tissue engineering scaffolds. Rapid Prototyping J 2003;9:43-49.
83. Cesarano JI, Dellinger JG, Saavedra MP. Customization of load-bearing hydroxyapatite lattice scaffolds. Int J Appl Ceram Technol 2005;2:212-220.
84. Marquez GJ, Renn MJ, Miller WD. Aerosol-Based Direct-Write of Biological Materials for Biomedical Applications. In: Materials Research Society Symposium Proceedings, Boston, MA; 2001;698:343-349.
85. Sears JW, Colvin J. Applying Nanoparticles via Direct-Write Technology for Industry Applications. In: Proceedings of the 2005 Conference on Powder Metallurgy and Particulate Materials, PM2TEC 2005. Montreal, Canada; 2005. pp 17-31.
86. Cesarano JI. A review of robocasting technology. In: Solid Freeform and Additive Fabrication, Materials Research Society Symposium, Boston, MA, 1998.
87. Kriparamanan R, Aswath P, Zhou A, Tang L, Nguyen KT. Nanotopography: Cellular responses to nanostructured materials. J Nanosci Nanotechnol 2006;6:1905-1919.
88. de Oliveira PT, Zalzal SF, Beloti MM, Rosa AL, Nanci A. Enhancement of in vitro osteogenesis on titanium by chemically produced nanotopography. J Biomed Mater Res A 2007;80:554-564.
89. Vaahtio M, Peltola T, Hentunen T, Ylèanen H, Areva S, Wolke J, Salonen JI. The properties of biomimetically processed calcium phosphate on bioactive ceramics and their response on bone cells. J Mater Sci: Mater Med 2006;17:1113-1125.
90. Areva S, Paldan H, Peltola T, Nèarhi T, Jokinen M, Lindâen M. Use of sol-gel-derived titania coating for direct soft tissue attachment. J Biomed Mater Res A 2004;70:169-178.
91. Ward BC, Webster TJ. The effect of nanotopography on calcium and phosphorus deposition on metallic materials in vitro. Biomaterials 2006;27:3064-3074.
92. Lim JY, Hansen JC, Siedlecki CA, Runt J, Donahue HJ. Human foetal osteoblastic cell response to polymer-demixed nanotopographic interfaces. J R Soc Interface 2005;2:97-108.
93. Dalby MJ, McCloy D, Robertson M, Wilkinson CD, Oreffo RO. Osteoprogenitor response to defined topographies with nanoscale depths. Biomaterials 2006;27:1306-1315.
94. LeBaron RG, Athanasiou KA. Extracellular matrix cell adhesion peptides: Functional applications in orthopedic materials. Tissue Eng 2000;6:85-103.
95. Siebers MC, ter Brugge PJ, Walboomers XF, Jansen JA. Integrins as linker proteins between osteoblasts and bone replacing materials. A critical review. Biomaterials 2005;26:137-146.
96. Shin H, Jo S, Mikos AG. Biomimetic materials for tissue engineering. Biomaterials 2003;24:4353-4364.
97. Southwood LL, Frisbie DD, Kawcak CE, Ghivizzani SC, Evans CH, McIlwraith CW. Evaluation of Ad-BMP-2 for enhancing fracture healing in an infected defect fracture rabbit model. J Orthop Res 2004;22:66-72.
98. Southwood LL, Frisbie DD, Kawcak CE, McIlwraith CW. Delivery of growth factors using gene therapy to enhance bone healing. Vet Surg 2004;33:565-578.
99. Leach JK, Mooney DJ. Bone engineering by controlled delivery of osteoinductive molecules and cells. Expert Opin Biol Ther 2004;4:1015-1027.
100. Saito N, Takaoka K. New synthetic biodegradable polymers as BMP carriers for bone tissue engineering. Biomaterials 2003;24:2287-2293.
101. Orban JM, Marra KG, Hollinger JO. Composition options for tissue-engineered bone. Tissue Eng 2002;8:529-539.
102. Loty C, Sautier JM, Loty S, Hattar S, Asselin A, Oboeuf M, Kokubo T, Kim HM, Boulekbache H, Berdal A. The biomimetics of bone: Engineered glass-ceramics a paradigm for in vitro biomineralization studies. Connect Tissue Res 2002;43:524-528.
103. Kim HM, Uenoyama M, Kokubo T, Minoda M, Miyamoto T, Nakamura T. Biomimetic apatite formation on polyethylene photografted with vinyltrimethoxysilane and hydrolyzed. Biomaterials 2001;22:2489-2494.
104. Kokubo T, Kim HM, Kawashita M. Novel bioactive materials with different mechanical properties. Biomaterials 2003;24:2161-2175.
105. Miyazaki T, Ohtsuki C, Tanihara M. Synthesis of bioactive organic-inorganic nanohybrid for bone repair through sol-gel processing. J Nanosci Nanotechnol 2003;3:511-515.
106. Yu X, Botchwey EA, Levine EM, Pollack SR, Laurencin CT. Bioreactor-based bone tissue engineering: The influence of dynamic flow on osteoblast phenotypic expression and matrix mineralization. Proc Natl Acad Sci USA 2004;101:11203-11208.
107. Botchwey EA, Pollack SR, Levine EM, Johnston ED, Laurencin CT. Quantitative analysis of three-dimensional fluid flow in rotating bioreactors for tissue engineering. J Biomed Mater Res A 2004;69:205-215.
108. Botchwey EA, Pollack SR, Levine EM, Laurencin CT. Bone tissue engineering in a rotating bioreactor using a microcarrier matrix system. J Biomed Mater Res 2001;55:242-253.
109. Sikavitsas VI, Temenoff JS, Mikos AG. Biomaterials and bone mechanotransduction. Biomaterials 2001;22:2581-2593.
110. Meinel L, Karageorgiou V, Fajardo R, Snyder B, Shinde-Patil V, Zichner L, Kaplan D, Langer R, Vunjak-Novakovic G. Bone tissue engineering using human mesenchymal stem cells: Effects of scaffold material and medium flow. Ann Biomed Eng 2004;32:112-122.
111. Alvarez-Barreto JF, Linehan SM, Shambaugh RL, Sikavitsas VI. Flow perfusion improves seeding of tissue engineering scaffolds with different architectures. Ann Biomed Eng 2007;35:429-442.
112. Sikavitsas VI, Bancroft GN, Holtorf HL, Jansen JA, Mikos AG. Mineralized matrix deposition by marrow stromal osteoblasts in 3D perfusion culture increases with increasing fluid shear forces. Proc Natl Acad Sci USA 2003;100:14683-14688.
113. Datta N, Pham QP, Sharma U, Sikavitsas VI, Jansen JA, Mikos AG. In vitro generated extracellular matrix and fluid shear stress synergistically enhance 3D osteoblastic differentiation. Proc Natl Acad Sci USA 2006;103:2488-2493.
114. Holtorf HL, Jansen JA, Mikos AG. Flow perfusion culture induces the osteoblastic differentiation of marrow stroma cell-scaffold constructs in the absence of dexamethasone. J Biomed Mater Res A 2005;72:326-334.
115. Gomes ME, Sikavitsas VI, Behravesh E, Reis RL, Mikos AG. Effect of flow perfusion on the osteogenic differentiation of bone marrow stromal cells cultured on starch-based three-dimensional scaffolds. J Biomed Mater Res A 2003;67:87-95.