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Clinical Reviews in Bone and Mineral Metabolism

, Volume 13, Issue 4, pp 245–255 | Cite as

Cell-Laden 3D Printed Scaffolds for Bone Tissue Engineering

  • Charlotte M. Piard
  • Yu Chen
  • John P. Fisher
Fracture healing and bone regeneration
Part of the following topical collections:
  1. Fracture healing and bone regeneration

Abstract

Tissue engineering, relying on a combination of biomaterial scaffolds, cells, and bioactive molecules, has emerged as a promising strategy for the treatment of bone defects. The presence of viable cells inside the engineered tissue has been shown to be crucial for bone formation in vivo. However, cells require mechanical support and a physical template, or scaffold, to facilitate their attachment and to stimulate neotissue formation. The advent of additive manufacturing technologies, and most critically three-dimensional (3D) printing, has allowed the development of a new generation of scaffolds. Cells used alongside 3D bioprinting in bone tissue engineering are typically utilized in two different strategies. The first strategy, 3D bioprinting, involves the layer-by-layer deposition of a bioink, made of a scaffold material and cells. The second strategy focuses on the fabrication of a scaffold by printing an acellular material, followed by seeding living cells. Here we review these two approaches, discussing printing techniques, their inconveniences and advantages, hydrogels for 3D printing, and how to overcome obstacles. Finally, we consider the resulting engineered tissues from these two approaches, specifically their mechanical properties, matrix production, and tissue mineralization.

Keywords

Bone tissue engineering 3D printing Bioprinting Biomaterials 

Notes

Acknowledgments

This work was supported by the National Institutes of Health (R01 EB014946). The authors would wish to thank Dr. Hannah Baker and Ms. Jordan Trachtenberg for this assistance in constructing this work.

Compliance with Ethical Standards

Conflict of interest

Charlotte M. Piard, Yu Chen, and John P. Fisher declare that they have no conflict of interest.

Animal/Human Studies

This article does not include any studies with human or animal subjects performed by the author.

References

  1. 1.
    Giannoudis PV, Dinopoulos H, Tsiridis E. Bone substitutes: an update. Injury. 2005;36(3):S20–7.PubMedCrossRefGoogle Scholar
  2. 2.
    Rubin J, Rubin C, Jacobs CR. Molecular pathways mediating mechanical signaling in bone. Gene. 2006;367:1–16.PubMedCentralPubMedCrossRefGoogle Scholar
  3. 3.
    Weiner S, Wagner HD. The material bone: structure-mechanical function relations. Annu Rev Mater Sci. 1998;28(1):271–98.CrossRefGoogle Scholar
  4. 4.
    Pittenger MF. Multilineage potential of adult human mesenchymal stem cells. Science (80-.). 1999;284(5411):143–7.CrossRefGoogle Scholar
  5. 5.
    Damien CJ, Parsons JR. Bone graft and bone graft substitutes: a review of current technology and applications. J Appl Biomater. 1991;2(3):187–208.PubMedCrossRefGoogle Scholar
  6. 6.
    Yaszemski MJ, Payne RG, Hayes WC, Langer R, Mikos AG. Evolution of bone transplantation: molecular, cellular and tissue strategies to engineer human bone. Biomaterials. 1996;17(2):175–85.PubMedCrossRefGoogle Scholar
  7. 7.
    Arrington ED, Smith WJ, Chambers HG, Bucknell AL, Davino NA. Complications of iliac crest bone graft harvesting. Clin Orthop Relat Res. 1996;329:300–9.PubMedCrossRefGoogle Scholar
  8. 8.
    Langer R, Vacanti JP. Tissue engineering. Science. 1993;260(5110):920–6.PubMedCrossRefGoogle Scholar
  9. 9.
    Cancedda R, Giannoni P, Mastrogiacomo M. A tissue engineering approach to bone repair in large animal models and in clinical practice. Biomaterials. 2007;28(29):4240–50.PubMedCrossRefGoogle Scholar
  10. 10.
    Santos MI, Reis RL. Vascularization in bone tissue engineering: physiology, current strategies, major hurdles and future challenges. Macromol Biosci. 2010;10(1):12–27.PubMedCrossRefGoogle Scholar
  11. 11.
    Quarto R, Mastrogiacomo M, Cancedda R, Kutepov SM, Mukhachev V, Lavroukov A, Kon E, Marcacci M. Repair of large bone defects with the use of autologous bone marrow stromal cells. N Engl J Med. 2001;344(5):385–6.PubMedCrossRefGoogle Scholar
  12. 12.
    Schimming R, Schmelzeisen R. Tissue-engineered bone for maxillary sinus augmentation. J Oral Maxillofac Surg. 2004;62(6):724–9.PubMedCrossRefGoogle Scholar
  13. 13.
    Bruder SP, Kraus KH, Goldberg VM, Kadiyala S. The effect of implants loaded with autologous mesenchymal stem cells on the healing of canine segmental bone defects. J Bone Joint Surg Am. 1998;80(7):985–96.PubMedGoogle Scholar
  14. 14.
    Puelacher WC, Vacanti JP, Ferraro NF, Schloo B, Vacanti CA. Femoral shaft reconstruction using tissue-engineered growth of bone. Int J Oral Maxillofac Surg. 1996;25(3):223–8.PubMedCrossRefGoogle Scholar
  15. 15.
    Shang Q, Wang Z, Liu W, Shi Y, Cui L, Cao Y. Tissue-engineered bone repair of sheep cranial defects with autologous bone marrow stromal cells. J Craniofac Surg. 2001;12(6):586–93 (discussions 594–5).PubMedCrossRefGoogle Scholar
  16. 16.
    Schliephake H, Knebel JW, Aufderheide M, Tauscher M. Use of cultivated osteoprogenitor cells to increase bone formation in segmental mandibular defects: an experimental pilot study in sheep. Int J Oral Maxillofac Surg. 2001;30(6):531–7.PubMedCrossRefGoogle Scholar
  17. 17.
    Karageorgiou V, Kaplan D. Porosity of 3D biomaterial scaffolds and osteogenesis. Biomaterials. 2005;26(27):5474–91.PubMedCrossRefGoogle Scholar
  18. 18.
    Jones AC, Arns CH, Sheppard AP, Hutmacher DW, Milthorpe BK, Knackstedt MA. Assessment of bone ingrowth into porous biomaterials using MICRO-CT. Biomaterials. 2007;28(15):2491–504.PubMedCrossRefGoogle Scholar
  19. 19.
    Otsuki B, Takemoto M, Fujibayashi S, Neo M, Kokubo T, Nakamura T. 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. 2006;27(35):5892–900.PubMedCrossRefGoogle Scholar
  20. 20.
    Cao H, Kuboyama N. A biodegradable porous composite scaffold of PGA/beta-TCP for bone tissue engineering. Bone. 2010;46(2):386–95.PubMedCrossRefGoogle Scholar
  21. 21.
    Kucharska M, Butruk B, Walenko K, Brynk T, Ciach T. Fabrication of in situ foamed chitosan/β-TCP scaffolds for bone tissue engineering application. Mater Lett. 2012;85:124–7.CrossRefGoogle Scholar
  22. 22.
    Sultana N, Wang M. Fabrication of HA/PHBV composite scaffolds through the emulsion freezing/freeze-drying process and characterisation of the scaffolds. J Mater Sci Mater Med. 2007;19(7):2555–61.PubMedCrossRefGoogle Scholar
  23. 23.
    Hutmacher DW. Scaffolds in tissue engineering bone and cartilage. Biomaterials. 2000;21(24):2529–43.PubMedCrossRefGoogle Scholar
  24. 24.
    Bose S, Vahabzadeh S, Bandyopadhyay A. Bone tissue engineering using 3D printing. Mater Today. 2013;16(12):496–504.CrossRefGoogle Scholar
  25. 25.
    Murphy SV, Atala A. 3D bioprinting of tissues and organs. Nat Biotechnol. 2014;32(8):773–85.PubMedCrossRefGoogle Scholar
  26. 26.
    Gao G, Schilling AF, Hubbell K, Yonezawa T, Truong D, Hong Y, Dai G, Cui X. Improved properties of bone and cartilage tissue from 3D inkjet-bioprinted human mesenchymal stem cells by simultaneous deposition and photocrosslinking in PEG-GelMA. Biotechnol Lett. 2015;37(11):2349-55.PubMedCrossRefGoogle Scholar
  27. 27.
    Poldervaart MT, Wang H, van der Stok J, Weinans H, Leeuwenburgh SCG, Öner FC, Dhert WJA, Alblas J. Sustained release of BMP-2 in bioprinted alginate for osteogenicity in mice and rats. PLoS One. 2013;8(8):e72610.PubMedCentralPubMedCrossRefGoogle Scholar
  28. 28.
    Fedorovich NE, Kuipers E, Gawlitta D, Dhert WJA, Alblas J. Scaffold porosity and oxygenation of printed hydrogel constructs affect functionality of embedded osteogenic progenitors. Tissue Eng Part A. 2011;17(19–20):2473–86.PubMedCrossRefGoogle Scholar
  29. 29.
    Wang X, Tolba E, Schröder HC, Neufurth M, Feng Q, Diehl-Seifert B, Müller WEG. Effect of bioglass on growth and biomineralization of SaOS-2 cells in hydrogel after 3D cell bioprinting. PLoS One. 2014;9(11):e112497.PubMedCentralPubMedCrossRefGoogle Scholar
  30. 30.
    Levato R, Visser J, Planell JA, Engel E, Malda J, Mateos-Timoneda MA. Biofabrication of tissue constructs by 3D bioprinting of cell-laden microcarriers. Biofabrication. 2014;6(3):035020.PubMedCrossRefGoogle Scholar
  31. 31.
    Schütz K, Placht AM, Paul B, Brüggemeier S, Gelinsky M, Lode A. Three-dimensional plotting of a cell-laden alginate/methylcellulose blend: towards biofabrication of tissue engineering constructs with clinically relevant dimensions. J Tissue Eng Regen Med. 2015. doi: 10.1002/term.2058.PubMedGoogle Scholar
  32. 32.
    Wüst S, Godla ME, Müller R, Hofmann S. Tunable hydrogel composite with two-step processing in combination with innovative hardware upgrade for cell-based three-dimensional bioprinting. Acta Biomater. 2014;10(2):630–40.PubMedCrossRefGoogle Scholar
  33. 33.
    Sawkins MJ, Mistry P, Brown BN, Shakesheff KM, Bonassar LJ, Yang J. Cell and protein compatible 3D bioprinting of mechanically strong constructs for bone repair. Biofabrication. 2015;7(3):035004.PubMedCrossRefGoogle Scholar
  34. 34.
    Martínez-Vázquez FJ, Cabañas MV, Paris JL, Lozano D, Vallet-Regí M. Fabrication of novel Si-doped hydroxyapatite/gelatine scaffolds by rapid prototyping for drug delivery and bone regeneration. Acta Biomater. 2015;15:200–9.PubMedCrossRefGoogle Scholar
  35. 35.
    Gonçalves EM, Oliveira FJ, Silva RF, Neto MA, Fernandes MH, Amaral M, Vallet-Regí M, Vila M. Three-dimensional printed PCL-hydroxyapatite scaffolds filled with CNTs for bone cell growth stimulation. J Biomed Mater Res B. 2015. doi: 10.1002/jbm.b.33432.Google Scholar
  36. 36.
    Ge Z, Wang L, Heng BC, Tian X-F, Lu K, Fan VTW, Yeo JF, Cao T, Tan E. Proliferation and differentiation of human osteoblasts within 3D printed poly-lactic-co-glycolic acid scaffolds. J Biomater Appl. 2009;23(6):533–47.CrossRefGoogle Scholar
  37. 37.
    Kruyt M, De Bruijn J, Rouwkema J, Van Bliterswijk C, Oner C, Verbout A, Dhert W. Analysis of the dynamics of bone formation, effect of cell seeding density, and potential of allogeneic cells in cell-based bone tissue engineering in goats. Tissue Eng Part A. 2008;14(6):1081–8.PubMedCrossRefGoogle Scholar
  38. 38.
    Kruyt MC, de Bruijn JD, Wilson CE, Oner FC, van Blitterswijk CA, Verbout AJ, Dhert WJA. Viable osteogenic cells are obligatory for tissue-engineered ectopic bone formation in goats. Tissue Eng. 2003;9(2):327–36.PubMedCrossRefGoogle Scholar
  39. 39.
    Nair K, Gandhi M, Khalil S, Yan KC, Marcolongo M, Barbee K, Sun W. Characterization of cell viability during bioprinting processes. Biotechnol J. 2009;4(8):1168–77.PubMedCrossRefGoogle Scholar
  40. 40.
    Chang R, Nam J, Sun W. Effects of dispensing pressure and nozzle diameter on cell survival from solid freeform fabrication-based direct cell writing. Tissue Eng Part A. 2008;14(1):41–8.PubMedCrossRefGoogle Scholar
  41. 41.
    Lutolf MP, Hubbell JA. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat Biotechnol. 2005;23(1):47–55.PubMedCrossRefGoogle Scholar
  42. 42.
    Drury JL, Mooney DJ. Hydrogels for tissue engineering: scaffold design variables and applications. Biomaterials. 2003;24(24):4337–51.PubMedCrossRefGoogle Scholar
  43. 43.
    Slaughter BV, Khurshid SS, Fisher OZ, Khademhosseini A, Peppas NA. Hydrogels in regenerative medicine. Adv Mater. 2009;21(32–33):3307–29.PubMedCentralPubMedCrossRefGoogle Scholar
  44. 44.
    Bokhari MA, Akay G, Zhang S, Birch MA. The enhancement of osteoblast growth and differentiation in vitro on a peptide hydrogel-polyHIPE polymer hybrid material. Biomaterials. 2005;26(25):5198–208.PubMedCrossRefGoogle Scholar
  45. 45.
    Abbott A. Cell culture: biology’s new dimension. Nature. 2003;424(6951):870–2.PubMedCrossRefGoogle Scholar
  46. 46.
    Fedorovich NE, Schuurman W, Wijnberg HM, Prins H-J, van Weeren PR, Malda J, Alblas J, Dhert WJA. Biofabrication of osteochondral tissue equivalents by printing topologically defined, cell-laden hydrogel scaffolds. Tissue Eng Part C Methods. 2012;18(1):33–44.PubMedCentralPubMedCrossRefGoogle Scholar
  47. 47.
    Ahn S, Lee H, Bonassar LJ, Kim G. Cells (MC3T3-E1)-laden alginate scaffolds fabricated by a modified solid-freeform fabrication process supplemented with an aerosol spraying. Biomacromolecules. 2012;13(9):2997–3003.PubMedCrossRefGoogle Scholar
  48. 48.
    Cohen DL, Malone E, Lipson H, Bonassar LJ. Direct freeform fabrication of seeded hydrogels in arbitrary geometries. Tissue Eng. 2006;12(5):1325–35.PubMedCrossRefGoogle Scholar
  49. 49.
    Gasperini L, Mano JF, Reis RL. Natural polymers for the microencapsulation of cells. J R Soc Interface. 2014;11(100):20140817.PubMedCentralPubMedCrossRefGoogle Scholar
  50. 50.
    Fedorovich NE, Alblas J, de Wijn JR, Hennink WE, Verbout AJ, Dhert WJA. Hydrogels as extracellular matrices for skeletal tissue engineering: state-of-the-art and novel application in organ printing. Tissue Eng. 2007;13(8):1905–25.PubMedCrossRefGoogle Scholar
  51. 51.
    Stevens MM, Marini RP, Schaefer D, Aronson J, Langer R, Shastri VP. In vivo engineering of organs: the bone bioreactor. Proc Natl Acad Sci USA. 2005;102(32):11450–5.PubMedCentralPubMedCrossRefGoogle Scholar
  52. 52.
    Augst AD, Kong HJ, Mooney DJ. Alginate hydrogels as biomaterials. Macromol Biosci. 2006;6(8):623–33.PubMedCrossRefGoogle Scholar
  53. 53.
    Wang L, Shelton RM, Cooper PR, Lawson M, Triffitt JT, Barralet JE. Evaluation of sodium alginate for bone marrow cell tissue engineering. Biomaterials. 2003;24(20):3475–81.PubMedCrossRefGoogle Scholar
  54. 54.
    Atala A, Yoo JJ. Essentials of 3D biofabrication and translation. Amsterdam: Elsevier Science; 2015.Google Scholar
  55. 55.
    Malda J, Visser J, Melchels FP, Jüngst T, Hennink WE, Dhert WJA, Groll J, Hutmacher DW. 25th anniversary article: engineering hydrogels for biofabrication. Adv Mater. 2013;25(36):5011–28.PubMedCrossRefGoogle Scholar
  56. 56.
    Sisson K, Zhang C, Farach-Carson MC, Chase DB, Rabolt JF. Evaluation of cross-linking methods for electrospun gelatin on cell growth and viability. Biomacromolecules. 2009;10(7):1675–80.PubMedCrossRefGoogle Scholar
  57. 57.
    Young S, Wong M, Tabata Y, Mikos AG. Gelatin as a delivery vehicle for the controlled release of bioactive molecules. J Control Release. 2005;109(1–3):256–74.PubMedCrossRefGoogle Scholar
  58. 58.
    Hoch E, Hirth T, Tovar GEM, Borchers K. Chemical tailoring of gelatin to adjust its chemical and physical properties for functional bioprinting. J Mater Chem B. 2013;1(41):5675.CrossRefGoogle Scholar
  59. 59.
    Schiele NR, Chrisey DB, Corr DT. Gelatin-based laser direct-write technique for the precise spatial patterning of cells. Tissue Eng Part C Methods. 2011;17(3):289–98.PubMedCentralPubMedCrossRefGoogle Scholar
  60. 60.
    Zhang T, Yan KC, Ouyang L, Sun W. Mechanical characterization of bioprinted in vitro soft tissue models. Biofabrication. 2013;5(4):045010.PubMedCrossRefGoogle Scholar
  61. 61.
    Xu T, Binder KW, Albanna MZ, Dice D, Zhao W, Yoo JJ, Atala A. Hybrid printing of mechanically and biologically improved constructs for cartilage tissue engineering applications. Biofabrication. 2013;5(1):015001.PubMedCrossRefGoogle Scholar
  62. 62.
    Luo Y, Wu C, Lode A, Gelinsky M. Hierarchical mesoporous bioactive glass/alginate composite scaffolds fabricated by three-dimensional plotting for bone tissue engineering. Biofabrication. 2013;5(1):015005.PubMedCrossRefGoogle Scholar
  63. 63.
    Jones JR. Review of bioactive glass: from hench to hybrids. Acta Biomater. 2013;9(1):4457–86.PubMedCrossRefGoogle Scholar
  64. 64.
    Sart S, Agathos SN, Li Y. Engineering stem cell fate with biochemical and biomechanical properties of microcarriers. Biotechnol Prog. 2013;29(6):1354–66.PubMedCrossRefGoogle Scholar
  65. 65.
    Martin Y, Eldardiri M, Lawrence-Watt DJ, Sharpe JR. Microcarriers and their potential in tissue regeneration. Tissue Eng Part B Rev. 2011;17(1):71–80.PubMedCrossRefGoogle Scholar
  66. 66.
    Malda J, Frondoza CG. Microcarriers in the engineering of cartilage and bone. Trends Biotechnol. 2006;24(7):299–304.PubMedCrossRefGoogle Scholar
  67. 67.
    Tadic D, Epple M. A thorough physicochemical characterisation of 14 calcium phosphate-based bone substitution materials in comparison to natural bone. Biomaterials. 2004;25(6):987–94.PubMedCrossRefGoogle Scholar
  68. 68.
    Obregon F, Vaquette C, Ivanovski S, Hutmacher DW, Bertassoni LE. Three-dimensional bioprinting for regenerative dentistry and craniofacial tissue engineering. J Dent Res. 2015;94(9 Suppl):143S–52S.PubMedCrossRefGoogle Scholar
  69. 69.
    Hutmacher DW, Sittinger M, Risbud MV. Scaffold-based tissue engineering: rationale for computer-aided design and solid free-form fabrication systems. Trends Biotechnol. 2004;22(7):354–62.PubMedCrossRefGoogle Scholar
  70. 70.
    Melchels FPW, Feijen J, Grijpma DW. A review on stereolithography and its applications in biomedical engineering. Biomaterials. 2010;31(24):6121–30.PubMedCrossRefGoogle Scholar
  71. 71.
    Seyednejad H, Gawlitta D, Dhert WJA, Van Nostrum CF, Vermonden T, Hennink WE. Preparation and characterization of a three-dimensional printed scaffold based on a functionalized polyester for bone tissue engineering applications. Acta Biomater. 2011;7(5):1999–2006.PubMedCrossRefGoogle Scholar
  72. 72.
    Eosoly S, Brabazon D, Lohfeld S, Looney L. Selective laser sintering of hydroxyapatite/poly-epsilon-caprolactone scaffolds. Acta Biomater. 2010;6(7):2511–7.PubMedCrossRefGoogle Scholar
  73. 73.
    Schantz J-T, Brandwood A, Hutmacher DW, Khor HL, Bittner K. Osteogenic differentiation of mesenchymal progenitor cells in computer designed fibrin-polymer-ceramic scaffolds manufactured by fused deposition modeling. J Mater Sci Mater Med. 2005;16(9):807–19.PubMedCrossRefGoogle Scholar
  74. 74.
    Gratson GM, Xu M, Lewis JA. Microperiodic structures: direct writing of three-dimensional webs. Nature. 2004;428(6981):386.PubMedCrossRefGoogle Scholar
  75. 75.
    Detsch R, Uhl F, Deisinger U, Ziegler G. 3D-Cultivation of bone marrow stromal cells on hydroxyapatite scaffolds fabricated by dispense-plotting and negative mould technique. J Mater Sci Mater Med. 2008;19(4):1491–6.PubMedCrossRefGoogle Scholar
  76. 76.
    Lode A, Bernhardt A, Gelinsky M. Cultivation of human bone marrow stromal cells on three-dimensional scaffolds of mineralized collagen: influence of seeding density on colonization, proliferation and osteogenic differentiation. J Tissue Eng Regen Med. 2008;2(7):400–7.PubMedCrossRefGoogle Scholar
  77. 77.
    Wu C, Luo Y, Cuniberti G, Xiao Y, Gelinsky M. Three-dimensional printing of hierarchical and tough mesoporous bioactive glass scaffolds with a controllable pore architecture, excellent mechanical strength and mineralization ability. Acta Biomater. 2011;7(6):2644–50.PubMedCrossRefGoogle Scholar
  78. 78.
    Sobral JM, Caridade SG, Sousa RA, Mano JF, Reis RL. Three-dimensional plotted scaffolds with controlled pore size gradients: effect of scaffold geometry on mechanical performance and cell seeding efficiency. Acta Biomater. 2011;7(3):1009–18.PubMedCrossRefGoogle Scholar
  79. 79.
    Shor L, Güçeri S, Wen X, Gandhi M, Sun W. Fabrication of three-dimensional polycaprolactone/hydroxyapatite tissue scaffolds and osteoblast-scaffold interactions in vitro. Biomaterials. 2007;28(35):5291–7.PubMedCrossRefGoogle Scholar
  80. 80.
    Mondrinos MJ, Dembzynski R, Lu L, Byrapogu VKC, Wootton DM, Lelkes PI, Zhou J. Porogen-based solid freeform fabrication of polycaprolactone-calcium phosphate scaffolds for tissue engineering. Biomaterials. 2006;27(25):4399–408.PubMedCrossRefGoogle Scholar
  81. 81.
    Heo S-J, Kim S-E, Wei J, Hyun Y-T, Yun H-S, Kim D-H, Shin JW, Shin J-W. Fabrication and characterization of novel nano- and micro-HA/PCL composite scaffolds using a modified rapid prototyping process. J Biomed Mater Res A. 2009;89(1):108–16.PubMedGoogle Scholar
  82. 82.
    Hollinger JO, Battistone GC. Biodegradable bone repair materials. Synthetic polymers and ceramics. Clin Orthop Relat Res. 1986;207:290–305.PubMedGoogle Scholar
  83. 83.
    Rezwan K, Chen QZ, Blaker JJ, Boccaccini AR. Biodegradable and bioactive porous polymer/inorganic composite scaffolds for bone tissue engineering. Biomaterials. 2006;27(18):3413–31.PubMedCrossRefGoogle Scholar
  84. 84.
    Sousa FCG, Evans JRG. Sintered hydroxyapatite latticework for bone substitute. J Am Ceram Soc. 2003;86(3):517–9.CrossRefGoogle Scholar
  85. 85.
    Tarafder S, Balla VK, Davies NM, Bandyopadhyay A, Bose S. Microwave-sintered 3D printed tricalcium phosphate scaffolds for bone tissue engineering. J Tissue Eng Regen Med. 2013;7(8):631–41.PubMedCentralPubMedCrossRefGoogle Scholar
  86. 86.
    Kalita SJ, Bose S, Hosick HL, Bandyopadhyay A. Development of controlled porosity polymer-ceramic composite scaffolds via fused deposition modeling. Mater Sci Eng C. 2003;23(5):611–20.CrossRefGoogle Scholar
  87. 87.
    Liu X, Ma PX. Polymeric scaffolds for bone tissue engineering. Ann Biomed Eng. 2004;32(3):477–86.PubMedCrossRefGoogle Scholar
  88. 88.
    Giordano RA, Wu BM, Borland SW, Cima LG, Sachs EM, Cima MJ. Mechanical properties of dense polylactic acid structures fabricated by three dimensional printing. J Biomater Sci Polym Ed. 1996;8(1):63–75.PubMedCrossRefGoogle Scholar
  89. 89.
    Suwanprateeb J, Thammarakcharoen F, Wongsuvan V, Chokevivat W. Development of porous powder printed high density polyethylene for personalized bone implants. J Porous Mater. 2011;19(5):623–32.CrossRefGoogle Scholar
  90. 90.
    Wang MO, Vorwald CE, Dreher ML, Mott EJ, Cheng M-H, Cinar A, Mehdizadeh H, Somo S, Dean D, Brey EM, Fisher JP. Evaluating 3D-printed biomaterials as scaffolds for vascularized bone tissue engineering. Adv Mater. 2015;27(1):138–44.PubMedCrossRefPubMedCentralGoogle Scholar
  91. 91.
    Goh BT, Teh LY, Tan DBP, Zhang Z, Teoh SH. Novel 3D polycaprolactone scaffold for ridge preservation—a pilot randomised controlled clinical trial. Clin Oral Implants Res. 2015;26(3):271–7.PubMedCrossRefGoogle Scholar
  92. 92.
    Reichert JC, Wullschleger ME, Cipitria A, Lienau J, Cheng TK, Schütz MA, Duda GN, Nöth U, Eulert J, Hutmacher DW. Custom-made composite scaffolds for segmental defect repair in long bones. Int Orthop. 2011;35(8):1229–36.PubMedCentralPubMedCrossRefGoogle Scholar
  93. 93.
    Wang MO, Piard CM, Melchiorri A, Dreher ML, Fisher JP. Evaluating changes in structure and cytotoxicity during in vitro degradation of three-dimensional printed scaffolds. Tissue Eng Part A. 2015;21(9–10):1642–53.PubMedCrossRefGoogle Scholar
  94. 94.
    Ghasemi-Mobarakeh L, Prabhakaran MP, Tian L, Shamirzaei-Jeshvaghani E, Dehghani L, Ramakrishna S. Structural properties of scaffolds: crucial parameters towards stem cells differentiation. World J Stem Cells. 2015;7(4):728–44.PubMedCentralPubMedCrossRefGoogle Scholar
  95. 95.
    Lee JW, Kang KS, Lee SH, Kim J-Y, Lee B-K, Cho D-W. Bone regeneration using a microstereolithography-produced customized poly(propylene fumarate)/diethyl fumarate photopolymer 3D scaffold incorporating BMP-2 loaded PLGA microspheres. Biomaterials. 2011;32(3):744–52.PubMedCrossRefGoogle Scholar
  96. 96.
    Vila M, Cicuéndez M, Sánchez-Marcos J, Fal-Miyar V, Manzano M, Prieto C, Vallet-Regi M. Electrical stimuli to increase cell proliferation on carbon nanotubes/mesoporous silica composites for drug delivery. J Biomed Mater Res A. 2013;101(1):213–21.PubMedCrossRefGoogle Scholar
  97. 97.
    Wang M, Cheng X, Zhu W, Holmes B, Keidar M, Zhang LG. Design of biomimetic and bioactive cold plasma-modified nanostructured scaffolds for enhanced osteogenic differentiation of bone marrow-derived mesenchymal stem cells. Tissue Eng Part A. 2014;20(5–6):1060–71.PubMedCrossRefGoogle Scholar
  98. 98.
    Liu X, Feng Q, Bachhuka A, Vasilev K. Surface modification by allylamine plasma polymerization promotes osteogenic differentiation of human adipose-derived stem cells. ACS Appl Mater Interfaces. 2014;6(12):9733–41.PubMedCrossRefGoogle Scholar
  99. 99.
    Chen G, Zhou P, Mei N, Chen X, Shao Z, Pan L, Wu C. Silk fibroin modified porous poly(epsilon-caprolactone) scaffold for human fibroblast culture in vitro. J Mater Sci Mater Med. 2004;15(6):671–7.PubMedCrossRefGoogle Scholar
  100. 100.
    Kao C-T, Lin C-C, Chen Y-W, Yeh C-H, Fang H-Y, Shie M-Y. Poly(dopamine) coating of 3D printed poly(lactic acid) scaffolds for bone tissue engineering. Mater Sci Eng C. 2015;56:165–73.CrossRefGoogle Scholar
  101. 101.
    Kuo Y-C, Yeh C-F. Effect of surface-modified collagen on the adhesion, biocompatibility and differentiation of bone marrow stromal cells in poly(lactide-co-glycolide)/chitosan scaffolds. Colloids Surf B Biointerfaces. 2011;82(2):624–31.PubMedCrossRefGoogle Scholar
  102. 102.
    Volkmer E, Drosse I, Otto S, Stangelmayer A, Stengele M, Kallukalam BC, Mutschler W, Schieker M. Hypoxia in static and dynamic 3D culture systems for tissue engineering of bone. Tissue Eng Part A. 2008;14(8):1331–40.PubMedCrossRefGoogle Scholar
  103. 103.
    Yeatts AB, Fisher JP. Bone tissue engineering bioreactors: dynamic culture and the influence of shear stress. Bone. 2011;48(2):171–81.PubMedCrossRefGoogle Scholar
  104. 104.
    Yeatts AB, Fisher JP. Tubular perfusion system for the long-term dynamic culture of human mesenchymal stem cells. Tissue Eng Part C Methods. 2011;17(3):337–48.PubMedCrossRefGoogle Scholar
  105. 105.
    Rowley JA, Madlambayan G, Mooney DJ. Alginate hydrogels as synthetic extracellular matrix materials. Biomaterials. 1999;20(1):45–53.PubMedCrossRefGoogle Scholar
  106. 106.
    Grieb TA, Forng R-Y, Stafford RE, Lin J, Almeida J, Bogdansky S, Ronholdt C, Drohan WN, Burgess WH. Effective use of optimized, high-dose (50 kGy) gamma irradiation for pathogen inactivation of human bone allografts. Biomaterials. 2005;26(14):2033–42.PubMedCrossRefGoogle Scholar
  107. 107.
    Reilly DT, Burstein AH. The elastic and ultimate properties of compact bone tissue. J Biomech. 1975;8(6):393–405.PubMedCrossRefGoogle Scholar
  108. 108.
    Trachtenberg JE, Mountziaris PM, Miller JS, Wettergreen M, Kasper FK, Mikos AG. Open-source three-dimensional printing of biodegradable polymer scaffolds for tissue engineering. J Biomed Mater Res A. 2014;102(12):4326–35.PubMedPubMedCentralGoogle Scholar
  109. 109.
    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(17):3565–75.PubMedCrossRefGoogle Scholar
  110. 110.
    Phillippi JA, Miller E, Weiss L, Huard J, Waggoner A, Campbell P. Microenvironments engineered by inkjet bioprinting spatially direct adult stem cells toward muscle- and bone-like subpopulations. Stem Cells. 2008;26(1):127–34.PubMedCrossRefGoogle Scholar
  111. 111.
    Fedorovich NE, Wijnberg HM, Dhert WJA, Alblas J. Distinct tissue formation by heterogeneous printing of osteo- and endothelial progenitor cells. Tissue Eng Part A. 2011;17(15–16):2113–21.PubMedCrossRefGoogle Scholar
  112. 112.
    Annabi N, Tamayol A, Uquillas JA, Akbari M, Bertassoni LE, Cha C, Camci-Unal G, Dokmeci MR, Peppas NA, Khademhosseini A. 25th anniversary article: rational design and applications of hydrogels in regenerative medicine. Adv Mater. 2014;26(1):85–123.PubMedCentralPubMedCrossRefGoogle Scholar
  113. 113.
    Lutolf MP, Hubbell JA. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat Biotechnol. 2005;23(1):47–55.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  1. 1.Fischell Department of BioengineeringUniversity of MarylandCollege ParkUSA

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