Advertisement

Biofabrication for osteochondral tissue regeneration: bioink printability requirements

  • Saba AbdulghaniEmail author
  • Pedro G. Morouço
S.I.: Biofabrication and Bioinks for Tissue Engineering
Part of the following topical collections:
  1. S.I.: Biofabrication and Bioinks for Tissue Engineering

Abstract

Biofabrication allows the formation of 3D scaffolds through a precise spatial control. This is of foremost importance when aiming to mimic heterogeneous and anisotropic architecture, such as that of the osteochondral tissue. Osteochondral defects are a supreme challenge for tissue engineering due to the compositional and structural complexity of stratified architecture and contrasting biomechanical properties of the cartilage-bone interface. This review highlights the advancements and retreats witnessed by using developed bioinks for tissue regeneration, taking osteochondral tissue as a challenging example. Methods, materials and requirements for bioprinting were discussed, highlighting the pre and post-processing factors that researchers should consider towards the development of a clinical treatment.

Notes

Acknowledgements

This work was funded by PAMI (ROTEIRO/0328/2013; Nº 022158), a Research Infrastructure of the National Roadmap of Research Infrastructures of Strategic Relevance for 2014–2020, co-funded by the FCT and European Union through the Centro2020.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Easley ME, Cushner FD, Scott WN. Insall & Scott surgery of the knee. Surgery of the Knee. New York, Churchill Livingstone. 2001;1:480.Google Scholar
  2. 2.
    Prakash D, Learmonth D. Natural progression of osteo-chondral defect in the femoral condyle. Knee. 2002;9:7–10.CrossRefGoogle Scholar
  3. 3.
    Solomon L, Warwick DJ, Nayagam S. Apley’s system of orthopaedics and fractures, Ninth Edition. Malaysian Orthop. 2010;875.Google Scholar
  4. 4.
    Marcacci M, Kon E, Delcogliano M, Filardo G, Busacca M, Zaffagnini S. Arthroscopic autologous osteochondral grafting for cartilage defects of the knee: prospective study results at a minimum 7-year follow-up. Am J Sports Med. 2007;35(12):2014–21.CrossRefGoogle Scholar
  5. 5.
    Hangody L, Vásárhelyi G, Hangody LR, Sükösd Z, Tibay G, Bartha L, et al. Autologous osteochondral grafting-technique and long-term results. Injury. 2008;39(1 SUPPL.):32–9.CrossRefGoogle Scholar
  6. 6.
    Kon E, Gobbi A, Filardo G, Delcogliano M, Zaffagnini S, Marcacci M. Arthroscopic second-generation autologous chondrocyte implantation compared with microfracture for chondral lesions of the knee: Prospective nonrandomized study at 5 years. Am J Sports Med. 2009;37(1):33–41.CrossRefGoogle Scholar
  7. 7.
    Lane JG, Healey RM, Chen AC, Sah RL, Amiel D. Can osteochondral grafting be augmented with microfracture in an extended-size lesion of articular cartilage? Am J Sports Med. 2010;38(7):1316–23.CrossRefGoogle Scholar
  8. 8.
    Martin I, Miot S, Barbero A, Jakob M, Wendt D. Osteochondral tissue engineering. J Biomech. 2007;40:750–65.CrossRefGoogle Scholar
  9. 9.
    Schaefer D, Martin I, Shastri P, Padera RF, Langer R, Freed LE, et al. In vitro generation of osteochondral composites. Biomaterials. 2000;21(24):2599–606.CrossRefGoogle Scholar
  10. 10.
    Castro NJ, Hacking SA, Zhang LG. Recent progress in interfacial tissue engineering approaches for osteochondral defects. Ann Biomed Eng. 2012;40:1628–40.CrossRefGoogle Scholar
  11. 11.
    Zhang L, Hu J, Athanasiou KA. The role of tissue engineering in articular cartilage repair and regeneration. Crit Rev Biomed Eng. 2009;37(1–2):1–57.CrossRefGoogle Scholar
  12. 12.
    Zhang L, Webster TJ. Nanotechnology and nanomaterials: promises for improved tissue regeneration. Nano Today. 2009;4:66–80.CrossRefGoogle Scholar
  13. 13.
    Yang PJ, Temenoff JS. Engineering orthopedic tissue interfaces. Tissue Eng Part B Rev. 2009;15(2):127–41.CrossRefGoogle Scholar
  14. 14.
    Keeney M, Pandit A. The osteochondral junction and its repair via bi-phasic tissue engineering scaffolds. Tissue Eng Part B Rev. 2009;15(1):55–73.CrossRefGoogle Scholar
  15. 15.
    Schinagl RM, Gurskis D, Chen AC, Sah RL. Depth-dependent confined compression modulus of full-thickness bovine articular cartilage. J Orthop Res. 1997;15(4):499–506.CrossRefGoogle Scholar
  16. 16.
    Mente PL, Lewis JL. Elastic modulus of calcified cartilage is an order of magnitude less than that of subchondral bone. J Orthop Res. 1994;12(5):637–47.CrossRefGoogle Scholar
  17. 17.
    Arvidson K, Abdallah BM, Applegate LA, Baldini N, Cenni E, Gomez-Barrena E, et al. Bone regeneration and stem cells. J Cell Mol Med. 2011;15:718–46.CrossRefGoogle Scholar
  18. 18.
    Mouser VHM, Levato R, Bonassar LJ, D’Lima DD, Grande DA, Klein TJ, et al. Three-dimensional bioprinting and its potential in the field of articular cartilage regeneration. Cartilage. 2017;8:327–40.CrossRefGoogle Scholar
  19. 19.
    Kelly DJ, Prendergast PJ. Prediction of the optimal mechanical properties for a scaffold used in osteochondral defect repair. Tissue Eng. 2006;12(9):2509–19.CrossRefGoogle Scholar
  20. 20.
    Stoop R. Smart biomaterials for tissue engineering of cartilage. Injury. 2008;39(1 SUPPL.):77–87.CrossRefGoogle Scholar
  21. 21.
    Nukavarapu SP, Dorcemus DL. Osteochondral tissue engineering: current strategies and challenges. Biotechnol Adv. 2013;31:706–21.CrossRefGoogle Scholar
  22. 22.
    Bhosale AM, Richardson JB. Articular cartilage: structure, injuries and review of management. Br Med Bull. 2008;87:77–95.Google Scholar
  23. 23.
    Toh WS, Spector M, Lee EH, Cao T. Biomaterial-mediated delivery of microenvironmental cues for repair and regeneration of articular cartilage. Mol Pharm. 2011;8:994–1001.CrossRefGoogle Scholar
  24. 24.
    Aspberg A. Cartilage proteoglycans. In: Cartilage: Volume 1: physiology and development. 2016. p. 1–22.Google Scholar
  25. 25.
    Poole AR, Kojima T, Yasuda T, Mwale F, Kobayashi M, Laverty S. Composition and structure of articular cartilage: a template for tissue repair. Clin Orthop Relat Res. 2001;1(391 Suppl):S26–33.CrossRefGoogle Scholar
  26. 26.
    Goldring MB, Marcu KB. Cartilage homeostasis in health and rheumatic diseases. Arthritis Res Ther. 2009;11(3):224.CrossRefGoogle Scholar
  27. 27.
    Holland TA, Tabata Y, Mikos AG. Dual growth factor delivery from degradable oligo(poly(ethylene glycol) fumarate) hydrogel scaffolds for cartilage tissue engineering. J Control Release. 2005;101:111–25.CrossRefGoogle Scholar
  28. 28.
    Harley BA, Lynn AK, Wissner-Gross Z, Bonfield W, Yannas IV, Gibson LJ. Design of a multiphase osteochondral scaffold III: fabrication of layered scaffolds with continuous interfaces. J Biomed Mater Res - Part A. 2010;92(3):1078–93.Google Scholar
  29. 29.
    Almarza AJ, Athanasiou KA. Design characteristics for the tissue engineering of cartilaginous tissues. Ann Biomed Eng. 2004;32(1):2–17.CrossRefGoogle Scholar
  30. 30.
    Ozbolat IT. Bioprinting of osteochondral tissues: A perspective on current gaps and future trends. Int J Bioprinting. 2017;3(2):1–12.CrossRefGoogle Scholar
  31. 31.
    Clark JM, Huber JD. The structure of the human subchondral plate. J Bone Jt Surg Br. 1990;72:866–73.CrossRefGoogle Scholar
  32. 32.
    Moroni L, Burdick JA, Highley C, Lee SJ, Morimoto Y, Takeuchi S. et al. Biofabrication strategies for 3D in vitro models and regenerative medicine. Nature Reviews Materials. 2018;3:21–37.CrossRefGoogle Scholar
  33. 33.
    Groll J, Boland T, Blunk T, Burdick JA, Cho DW, Dalton PD, et al. Biofabrication: reappraising the definition of an evolving field. Biofabrication. 2016;8:013001.CrossRefGoogle Scholar
  34. 34.
    Moroni L, Boland T, Burdick JA, De Maria C, Derby B, Forgacs G, et al. Biofabrication: a guide to technology and terminology. Trends Biotechnol. 2018;36(4):384–402.CrossRefGoogle Scholar
  35. 35.
    Liu X, Wu S, Yeung KWK, Chan YL, Hu T, Xu Z, et al. Relationship between osseointegration and superelastic biomechanics in porous NiTi scaffolds. Biomaterials. 2011;32(2):330–8.CrossRefGoogle Scholar
  36. 36.
    Malda J, Woodfield TBF, Van Der Vloodt F, Wilson C, Martens DE, Tramper J, et al. The effect of PEGT/PBT scaffold architecture on the composition of tissue engineered cartilage. Biomaterials. 2005;26(1):63–72.CrossRefGoogle Scholar
  37. 37.
    Hedayati R, Ahmadi SM, Lietaert K, Pouran B, Li Y, Weinans H, et al. Isolated and modulated effects of topology and material type on the mechanical properties of additively manufactured porous biomaterials. J Mech Behav Biomed Mater. 2018;79:254–63.CrossRefGoogle Scholar
  38. 38.
    Fu CY, Tseng SY, Yang SM, Hsu L, Liu CH, Chang HY. A microfluidic chip with a U-shaped microstructure array for multicellular spheroid formation, culturing and analysis. Biofabrication. 2014;6(1):5009.CrossRefGoogle Scholar
  39. 39.
    Young C, Rozario K, Serra C, Poole-Warren L, Martens P. Poly(vinyl alcohol)-heparin biosynthetic microspheres produced by microfluidics and ultraviolet photopolymerisation. Biomicrofluidics. 2013;7(4):44109.CrossRefGoogle Scholar
  40. 40.
    Schon BS, Hooper GJ, Woodfield TBF. Modular tissue assembly strategies for biofabrication of engineered cartilage. Ann Biomed Eng. 2017;45:100–14.CrossRefGoogle Scholar
  41. 41.
    Murphy SV, Atala A. 3D bioprinting of tissues and organs. Nat Biotechnol. 2014;32:773–85.CrossRefGoogle Scholar
  42. 42.
    Ozbolat IT, Hospodiuk M. Current advances and future perspectives in extrusion-based bioprinting. Biomaterials. 2016;76:321–43.CrossRefGoogle Scholar
  43. 43.
    Visser J, Peters B, Burger TJ, Boomstra J, Dhert WJA, Melchels FPW. et al. Biofabrication of multi-material anatomically shaped tissue constructs. Biofabrication. 2013;5(3):5007.CrossRefGoogle Scholar
  44. 44.
    Schuurman W, Levett PA, Pot MW, van Weeren PR, Dhert WJA, Hutmacher DW, et al. Gelatin-methacrylamide hydrogels as potential biomaterials for fabrication of tissue-engineered cartilage constructs. Macromol Biosci. 2013;13(5):551–61.CrossRefGoogle Scholar
  45. 45.
    Cui X, Breitenkamp K, Lotz M, D’Lima D. Synergistic action of fibroblast growth factor-2 and transforming growth factor-beta1 enhances bioprinted human neocartilage formation. Biotechnol Bioeng. 2012;109(9):2357–68.CrossRefGoogle Scholar
  46. 46.
    Kim JE, Kim SH, Jung Y. Current status of three-dimensional printing inks for soft tissue regeneration. Tissue Eng Regen Med. 2016;13:636–46.CrossRefGoogle Scholar
  47. 47.
    Tan H, Marra KG. Injectable, biodegradable hydrogels for tissue engineering applications. Mater (Basel). 2010;3(3):1746–67.CrossRefGoogle Scholar
  48. 48.
    Billiet T, Vandenhaute M, Schelfhout J, Van Vlierberghe S, Dubruel P. A review of trends and limitations in hydrogel-rapid prototyping for tissue engineering. Biomaterials. 2012;33:6020–41.CrossRefGoogle Scholar
  49. 49.
    Malda J, Visser J, Melchels FP, Jüngst T, Hennink WE, Dhert WJA, et al. 25th anniversary article: Engineering hydrogels for biofabrication. Adv Mater. 2013;25:5011–28.CrossRefGoogle Scholar
  50. 50.
    Ott HC, Matthiesen TS, Goh SK, Black LD, Kren SM, Netoff TI, et al. Perfusion-decellularized matrix: Using nature’s platform to engineer a bioartificial heart. Nat Med. 2008;14(2):213–21.CrossRefGoogle Scholar
  51. 51.
    Malda J, Frondoza CG. Microcarriers in the engineering of cartilage and bone. Trends Biotechnol. 2006;24:299–304.CrossRefGoogle Scholar
  52. 52.
    Greenwald AS. Biological performance of materials. Fundamentals of Biocompatibility. J Bone Jt Surg. 2001;83(6):970.Google Scholar
  53. 53.
    Williams DF. On the mechanisms of biocompatibility. Biomaterials. 2008;29(20):2941–53.CrossRefGoogle Scholar
  54. 54.
    Gaharwar AK, Sant S, Hancock MJ, Hacking SA. Nanomaterials in tissue engineering: fabrication and applications. Nanomaterials in Tissue Engineering: Fabrication and Applications. 2013.Google Scholar
  55. 55.
    Vyas C, Poologasundarampillai G, Hoyland J, Bartolo P. 3D printing of biocomposites for osteochondral tissue engineering. In: Biomedical Composites (Second Edition). Woodhead Publishing Series in Biomaterials. 2017, p. 261–302.Google Scholar
  56. 56.
    Stevens MM, George JH. Exploring and engineering the cell surface interface. Science. 2005;310(5751):1135–8.CrossRefGoogle Scholar
  57. 57.
    Place ES, Evans ND, Stevens MM. Complexity in biomaterials for tissue engineering. Nat Mater. 2009;8(6):457–70.CrossRefGoogle Scholar
  58. 58.
    Crowder SW, Leonardo V, Whittaker T, Papathanasiou P, Stevens MM. Material cues as potent regulators of epigenetics and stem cell function. Cell Stem Cell. 2016;18(1):39–52.CrossRefGoogle Scholar
  59. 59.
    Morouço P, Lattanzi W, Alves N. Four-dimensional bioprinting as a new era for tissue engineering and regenerative medicine. Front Bioeng Biotechnol. 2017;5:61.CrossRefGoogle Scholar
  60. 60.
    Gaharwar AK, Peppas NA, Khademhosseini A. Nanocomposite hydrogels for biomedical applications. Biotechnol Bioeng. 2014;111(3):441–53.CrossRefGoogle Scholar
  61. 61.
    Xu K, Wang J, Chen Q, Yue Y, Zhang W, Wang P. Spontaneous volume transition of polyampholyte nanocomposite hydrogels based on pure electrostatic interaction. J Colloid Interface Sci. 2008;321(2):272–8.CrossRefGoogle Scholar
  62. 62.
    Utech S, Boccaccini AR. A review of hydrogel-based composites for biomedical applications: enhancement of hydrogel properties by addition of rigid inorganic fillers. J Mater Sci. 2016;51:271–310.CrossRefGoogle Scholar
  63. 63.
    Ribeiro A, Blokzijl MM, Levato R, Visser CW, Castilho M, Hennink WE. et al. Assessing bioink shape fidelity to aid material development in 3D bioprinting. Biofabrication. 2017;10(1):4102.CrossRefGoogle Scholar
  64. 64.
    Nicodemus GD, Bryant SJ. Cell encapsulation in biodegradable hydrogels for tissue engineering applications. Tissue Eng Part B Rev. 2008;14(2):149–65.CrossRefGoogle Scholar
  65. 65.
    Aguado BA, Mulyasasmita W, Su J, Lampe KJ, Heilshorn SC. Improving viability of stem cells during syringe needle flow through the design of hydrogel cell carriers. Tissue Eng Part A. 2012;18(7–8):806–15.CrossRefGoogle Scholar
  66. 66.
    Blaeser A, Duarte Campos DF, Puster U, Richtering W, Stevens MM, Fischer H. Controlling shear stress in 3D bioprinting is a key factor to balance printing resolution and stem cell integrity. Adv Healthc Mater. 2016;5(3):326–33.CrossRefGoogle Scholar
  67. 67.
    Nair K, Gandhi M, Khalil S, Yan KC, Marcolongo M, Barbee K, et al. Characterization of cell viability during bioprinting processes. Biotechnol J. 2009;4(8):1168–77.CrossRefGoogle Scholar
  68. 68.
    Bencherif SA, Srinivasan A, Horkay F, Hollinger JO, Matyjaszewski K, Washburn NR. Influence of the degree of methacrylation on hyaluronic acid hydrogels properties. Biomaterials. 2008;29(12):1739–49.CrossRefGoogle Scholar
  69. 69.
    Jungst T, Smolan W, Schacht K, Scheibel T, Groll J. Strategies and molecular design criteria for 3D printable hydrogels. Chem Rev. 2016;116:1496–539.CrossRefGoogle Scholar
  70. 70.
    Gulrez SK, Al-Assaf S, Phillips GO. Hydrogels: Methods of preparation, characterisation and applications in molecular and environmental bioengineering. Prog Mol Environ Bioeng - From Anal Moddelling to Technol Appl. 2011;646.Google Scholar
  71. 71.
    Dragan ES. Design and applications of interpenetrating polymer network hydrogels. A review. Chem Eng J. 2014;243:572–90.CrossRefGoogle Scholar
  72. 72.
    Wang Z, Abdulla R, Parker B, Samanipour R, Ghosh S, Kim K. A simple and high-resolution stereolithography-based 3D bioprinting system using visible light crosslinkable bioinks. Biofabrication 2015;7(4):045009.CrossRefGoogle Scholar
  73. 73.
    Hennink WE, van Nostrum CF. Novel crosslinking methods to design hydrogels. Adv Drug Deliv Rev. 2012;64:223–36.CrossRefGoogle Scholar
  74. 74.
    Duarte Campos DF, Blaeser A, Weber M, Jäkel J, Neuss S, Jahnen-Dechent W, et al. Three-dimensional printing of stem cell-laden hydrogels submerged in a hydrophobic high-density fluid. Biofabrication. 2013;5(1):5003–13.Google Scholar
  75. 75.
    Nikkhah M, Eshak N, Zorlutuna P, Annabi N, Castello M, Kim K, et al. Directed endothelial cell morphogenesis in micropatterned gelatin methacrylate hydrogels. Biomaterials. 2012;33(35):9009–18.CrossRefGoogle Scholar
  76. 76.
    You F, Wu X, Zhu N, Lei M, Eames BF, Chen X. 3D Printing of porous cell-laden hydrogel constructs for potential applications in cartilage tissue engineering. ACS Biomater Sci Eng. 2016;2(7):1200–10.CrossRefGoogle Scholar
  77. 77.
    Li X, Ding J, Wang J, Zhuang X, Chen X. Biomimetic biphasic scaffolds for osteochondral defect repair. Regen Biomater. 2015;2(3):221–8.CrossRefGoogle Scholar
  78. 78.
    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.Google Scholar
  79. 79.
    Holmes B, Zhu W, Li J, Lee JD, Zhang LG. Development of novel three-dimensional printed scaffolds for osteochondral regeneration. Tissue Eng Part A. 2015;21(1–2):403–15.Google Scholar
  80. 80.
    Gao J, Dennis JE, Solchaga LA, Awadallah AS, Goldberg VM, Caplan AI. Tissue-engineered fabrication of an osteochondral composite graft using rat bone marrow-derived mesenchymal stem cells. Tissue Eng. 2001;7(4):363–71.Google Scholar
  81. 81.
    Theodoropoulos JS, De Croos JNA, Park SS, Pilliar R, Kandel RA. Integration of tissue-engineered cartilage with host cartilage: An in vitro model. Clin Orthop Relat Res. 2011;469:2785–95.CrossRefGoogle Scholar
  82. 82.
    Rodrigues MT, Lee SJ, Gomes ME, Reis RL, Atala A, Yoo JJ. Bilayered constructs aimed at osteochondral strategies: the influence of medium supplements in the osteogenic and chondrogenic differentiation of amniotic fluid-derived stem cells. Acta Biomater. 2012;8(7):2795–806.CrossRefGoogle Scholar
  83. 83.
    Miot S, Brehm W, Dickinson S, Sims T, Wixmerten A, Longinotti C, et al. Influence of in vitro maturation of engineered cartilage on the outcome of osteochondral repair in a goat model. Eur Cells Mater. 2012;23:222–36.CrossRefGoogle Scholar
  84. 84.
    Newitt DC, Majumdar S, Van Rietbergen B, Von Ingersleben G, Harris ST, Genant HK, et al. In vivo assessment of architecture and micro-finite element analysis derived indices of mechanical properties of trabecular bone in the radius. Osteoporos Int. 2002;13(1):6–17.CrossRefGoogle Scholar
  85. 85.
    Fedorovich NE, Schuurman W, Wijnberg HM, Prins HJ, van Weeren PR, Malda J, et al. Biofabrication of osteochondral tissue equivalents by printing topologically defined, cell-laden hydrogel scaffolds. Tissue Eng Part C Methods. 2012;18(1):33–44.CrossRefGoogle Scholar
  86. 86.
    Nowicki MA, Castro NJ, Plesniak MW, Zhang LG. 3D printing of novel osteochondral scaffolds with graded microstructure. Nanotechnology 2016;27(41):4001–10.Google Scholar
  87. 87.
    Markstedt K, Mantas A, Tournier I, Martínez Ávila H, Hägg D, Gatenholm P. 3D bioprinting human chondrocytes with nanocellulose-alginate bioink for cartilage tissue engineering applications. Biomacromolecules. 2015;16(5):1489–96.CrossRefGoogle Scholar
  88. 88.
    Rhee S, Puetzer JL, Mason BN, Reinhart-King CA, Bonassar LJ. 3D Bioprinting of spatially heterogeneous collagen constructs for cartilage tissue engineering. ACS Biomater Sci Eng. 2016;2(10):1800–5.CrossRefGoogle Scholar
  89. 89.
    Das S, Pati F, Choi YJ, Rijal G, Shim JH, Kim SW, et al. Bioprintable, cell-laden silk fibroin-gelatin hydrogel supporting multilineage differentiation of stem cells for fabrication of three-dimensional tissue constructs. Acta Biomater. 2015;11(1):233–46.CrossRefGoogle Scholar
  90. 90.
    Chung JHY, Naficy S, Yue Z, Kapsa R, Quigley A, Moulton SE. et al. Bio-ink properties and printability for extrusion printing living cells. Biomater Sci. 2013;1(7):763.Google Scholar
  91. 91.
    Ouyang L, Highley CB, Rodell CB, Sun W, Burdick JA. 3D Printing of shear-thinning hyaluronic acid hydrogels with secondary cross-linking. ACS Biomater Sci Eng. 2016;2(10):1743–51.CrossRefGoogle Scholar
  92. 92.
    Hong S, Sycks D, Chan HFA, Lin S, Lopez GP, Guilak F, et al. 3D Printing: 3D printing of highly stretchable and tough hydrogels into complex, cellularized structures. Adv Mater. 2015;27(27):4034.CrossRefGoogle Scholar
  93. 93.
    Zhu F, Cheng L, Wang ZJ, Hong W, Wu ZL, Yin J, et al. 3D-Printed ultratough hydrogel structures with titin-like domains. ACS Appl Mater Interfaces. 2017;9(13):11363–7.CrossRefGoogle Scholar
  94. 94.
    Yang F, Tadepalli V, Wiley BJ. 3D Printing of a double network hydrogel with a compression strength and elastic modulus greater than those of cartilage. ACS Biomater Sci Eng. 2017;3(5):863–9.CrossRefGoogle Scholar
  95. 95.
    Gao F, Xu Z, Liang Q, Liu B, Li H, Wu Y, et al. Direct 3D printing of high strength biohybrid gradient hydrogel scaffolds for efficient repair of osteochondral defect. Adv Funct Mater. 2018;28:1706644–56.Google Scholar
  96. 96.
    Du Y, Liu H, Yang Q, Wang S, Wang J, Ma J, et al. Selective laser sintering scaffold with hierarchical architecture and gradient composition for osteochondral repair in rabbits. Biomaterials. 2017;137:37–48.CrossRefGoogle Scholar
  97. 97.
    3D printing of a lithium-calcium-silicate crystal bioscaffold with dual bioactivities for osteochondral interface reconstruction. Biomaterials. 2018.Google Scholar
  98. 98.
    Doulabi AH, Mequanint K, Mohammadi H. Blends and nanocomposite biomaterials for articular cartilage tissue engineering. Mater (Basel). 2014;7(7):5327–55.CrossRefGoogle Scholar
  99. 99.
    Tiruvannamalai-Annamalai R, Armant DR, Matthew HWT. A glycosaminoglycan based, modular tissue scaffold system for rapid assembly of perfusable, high cell density, engineered tissues. PLoS One. 2014;9(1):e84287.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Centre for Rapid and Sustainable Product DevelopmentPolytechnic Institute of LeiriaMarinha GrandePortugal

Personalised recommendations