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Biomimetic Orthopedic Materials

  • R. Portillo-Lara
  • E. Shirzaei Sani
  • N. Annabi
Chapter

Abstract

Biomimetics refers to the design and engineering of artificial materials, structures, and systems that emulate those naturally occurring in biological entities. In recent years, interdisciplinary approaches based on biomimicry, materials sciences, and tissue engineering have enabled the development of biomimetic materials with defined chemical composition, physical structure, and biological function for a wide range of biomedical applications. These types of materials mimic the biochemical properties of native tissues, while also possessing the physical properties of core materials. Hence, they can be used to deliver different types of physiological stimuli that can modulate cell behavior. Significant efforts have been made to engineer biomimetic materials that can recapitulate specific features of the native ECM to act as bioactive templates to promote the repair and functional reconstruction of various types of tissues. In this chapter, we will provide an overview of current trends in the design of biomimetic orthopedic materials, which feature structural and functional properties inspired from biological entities.

Keywords

Biomimetic biomaterial Biologically inspired biomaterial Orthopedic biomaterial Bone tissue engineering Cartilage tissue engineering Musculoskeletal tissue Engineering Regenerative medicine Nanofibrous scaffold Biofabrication 3D bioprinting 

Notes

Acknowledgements

N.A. acknowledges the support from the National Institutes of Health (NIH, R01EB023052-01A1, R01HL140618-01), the American Heart Association (AHA, 16SDG31280010), The Center for Dental, Oral & Craniofacial Tissue & Organ Regeneration (C-DOCTOR) Interdisciplinary Project Team award, FY17 TIER 1 Interdisciplinary Research Seed Grants from Northeastern University, and the startup fund provided by the Department of Chemical Engineering, College of Engineering at Northeastern University. R.P.L. acknowledges institutional funding received from the Escuela de Ingeniería y Ciencias at Tecnológico de Monterrey, México (L03022214).

References

  1. 1.
    Kushner AM, Guan Z. Modular design in natural and biomimetic soft materials. Angew Chem Int Ed Engl. 2011;50(39):9026–57.PubMedCrossRefGoogle Scholar
  2. 2.
    Chen C, et al. Research trends in biomimetic medical materials for tissue engineering: 3D bioprinting, surface modification, nano/micro-technology and clinical aspects in tissue engineering of cartilage and bone. Biomater Res. 2016;20:10.PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Green JJ, Elisseeff JH. Mimicking biological functionality with polymers for biomedical applications. Nature. 2016;540(7633):386–94.PubMedCrossRefGoogle Scholar
  4. 4.
    Yi S, et al. Extracellular matrix scaffolds for tissue engineering and regenerative medicine. Curr Stem Cell Res Ther. 2017;12(3):233–46.PubMedCrossRefGoogle Scholar
  5. 5.
    Maradit Kremers H, et al. Prevalence of total hip and knee replacement in the United States. J Bone Joint Surg Am. 2015;97(17):1386–97.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Laurencin CT, et al. Tissue engineering: orthopedic applications. Annu Rev Biomed Eng. 1999;1:19–46.PubMedCrossRefGoogle Scholar
  7. 7.
    Yannas IV. Tissue and organ regeneration in adults: extension of the paradigm to several organs. 2nd ed. New York: Springer; 2015. p. xxiii. 332 pagesGoogle Scholar
  8. 8.
    Sprio S, et al. Biomimesis and biomorphic transformations: new concepts applied to bone regeneration. J Biotechnol. 2011;156(4):347–55.PubMedCrossRefGoogle Scholar
  9. 9.
    Balasundaram G, Webster TJ. Nanotechnology and biomaterials for orthopedic medical applications. Nanomedicine (Lond). 2006;1(2):169–76.CrossRefGoogle Scholar
  10. 10.
    Raphel J, et al. Multifunctional coatings to simultaneously promote osseointegration and prevent infection of orthopaedic implants. Biomaterials. 2016;84:301–14.PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Mouthuy PA, et al. Biocompatibility of implantable materials: an oxidative stress viewpoint. Biomaterials. 2016;109:55–68.PubMedCrossRefGoogle Scholar
  12. 12.
    Ruys A. Biomimetic biomaterials: structure and applications, vol. 57. Sawston: Woodhead Publishing; 2013. p. 3.CrossRefGoogle Scholar
  13. 13.
    Zhang X, et al. Biomimetic scaffold design for functional and integrative tendon repair. J Shoulder Elb Surg. 2012;21(2):266–77.CrossRefGoogle Scholar
  14. 14.
    Holzapfel BM, et al. How smart do biomaterials need to be? A translational science and clinical point of view. Adv Drug Deliv Rev. 2013;65(4):581–603.PubMedCrossRefGoogle Scholar
  15. 15.
    O'Brien FJ. Biomaterials & scaffolds for tissue engineering. Mater Today. 2011;14(3):88–95.CrossRefGoogle Scholar
  16. 16.
    Ma PX. Biomimetic materials for tissue engineering. Adv Drug Deliv Rev. 2008;60(2):184–98.PubMedCrossRefGoogle Scholar
  17. 17.
    Anderson JM. Future challenges in the in vitro and in vivo evaluation of biomaterial biocompatibility. Regen Biomater. 2016;3(2):73–7.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Sridhar R, et al. Medical devices regulatory aspects: a special focus on polymeric material based devices. Curr Pharm Des. 2015;21(42):6246–59.PubMedCrossRefGoogle Scholar
  19. 19.
    Harvey AG, Hill EW, Bayat A. Designing implant surface topography for improved biocompatibility. Expert Rev Med Devices. 2013;10(2):257–67.PubMedCrossRefGoogle Scholar
  20. 20.
    Wang G, et al. Enhancing orthopedic implant bioactivity: refining the nanotopography. Nanomedicine (Lond). 2015;10(8):1327–41.CrossRefGoogle Scholar
  21. 21.
    Lahner M, et al. Biomimetic structured surfaces increase primary adhesion capacity of cartilage implants. Technol Health Care. 2015;23(2):205–13.PubMedGoogle Scholar
  22. 22.
    Zhao JM, et al. Biomimetic deposition of hydroxyapatite by mixed acid treatment of titanium surfaces. J Nanosci Nanotechnol. 2015;15(3):2552–5.PubMedCrossRefGoogle Scholar
  23. 23.
    Tibbitt MW, et al. Progress in material design for biomedical applications. Proc Natl Acad Sci U S A. 2015;112(47):14444–51.PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Pillai CK, Sharma CP. Review paper: absorbable polymeric surgical sutures: chemistry, production, properties, biodegradability, and performance. J Biomater Appl. 2010;25(4):291–366.PubMedCrossRefGoogle Scholar
  25. 25.
    Ulery BD, Nair LS, Laurencin CT. Biomedical applications of biodegradable polymers. J Polym Sci B Polym Phys. 2011;49(12):832–64.PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Sotomi Y, et al. Bioresorbable scaffold: the emerging reality and future directions. Circ Res. 2017;120(8):1341–52.PubMedCrossRefGoogle Scholar
  27. 27.
    Guan X, et al. Development of hydrogels for regenerative engineering. Biotechnol J. 2017;12(5). https://doi.org/10.1002/biot.201600394.Google Scholar
  28. 28.
    Yang J, et al. Cell-laden hydrogels for osteochondral and cartilage tissue engineering. Acta Biomater. 2017;57:1–25.PubMedCrossRefGoogle Scholar
  29. 29.
    Ma PX, Langer R. Degradation, structure and properties of fibrous nonwoven poly(glycolic acid) scaffolds for tissue engineering. Polymers Medicine Pharmacy. 1995;394:99–104.Google Scholar
  30. 30.
    Chen VJ, Ma PX. The effect of surface area on the degradation rate of nano-fibrous poly(L-lactic acid) foams. Biomaterials. 2006;27(20):3708–15.PubMedCrossRefGoogle Scholar
  31. 31.
    Klotz BJ, et al. Gelatin-methacryloyl hydrogels: towards biofabrication-based tissue repair. Trends Biotechnol. 2016;34(5):394–407.PubMedCrossRefGoogle Scholar
  32. 32.
    Sahoo S, et al. Hydrolytically degradable hyaluronic acid hydrogels with controlled temporal structures. Biomacromolecules. 2008;9(4):1088–92.PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Wassenaar JW, et al. Modulating in vivo degradation rate of injectable extracellular matrix hydrogels. J Mater Chem B Mater Biol Med. 2016;4(16):2794–802.PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Coletta DJ, et al. Bone regeneration mediated by a bioactive and biodegradable ECM-like hydrogel based on elastin-like recombinamers. Tissue Eng Part A. 2017;23(23–24):1361–71.PubMedCrossRefGoogle Scholar
  35. 35.
    Peeters M, et al. BMP-2 and BMP-2/7 heterodimers conjugated to a fibrin/hyaluronic acid hydrogel in a large animal model of mild intervertebral disc degeneration. Biores Open Access. 2015;4(1):398–406.PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Bryant SJ, Anseth KS. Controlling the spatial distribution of ECM components in degradable PEG hydrogels for tissue engineering cartilage. J Biomed Mater Res A. 2003;64((1):70–9.CrossRefGoogle Scholar
  37. 37.
    Sheikhpour M, Barani L, Kasaeian A. Biomimetics in drug delivery systems: a critical review. J Control Release. 2017;253:97–109.PubMedCrossRefGoogle Scholar
  38. 38.
    Alford AI, Kozloff KM, Hankenson KD. Extracellular matrix networks in bone remodeling. Int J Biochem Cell Biol. 2015;65:20–31.PubMedCrossRefGoogle Scholar
  39. 39.
    Paiva KB, Granjeiro JM. Bone tissue remodeling and development: focus on matrix metalloproteinase functions. Arch Biochem Biophys. 2014;561:74–87.PubMedCrossRefGoogle Scholar
  40. 40.
    Kondiah PJ, et al. A review of injectable polymeric hydrogel systems for application in bone tissue engineering. Molecules. 2016;21(11):pii: E1580.CrossRefGoogle Scholar
  41. 41.
    Gibbs DM, et al. A review of hydrogel use in fracture healing and bone regeneration. J Tissue Eng Regen Med. 2016;10(3):187–98.PubMedCrossRefGoogle Scholar
  42. 42.
    Hutmacher DW. Scaffolds in tissue engineering bone and cartilage. Biomaterials. 2000;21(24):2529–43.PubMedCrossRefGoogle Scholar
  43. 43.
    Pal S. Design of artificial human joints & organs. New York: Springer; 2013.Google Scholar
  44. 44.
    Rho JY, Kuhn-Spearing L, Zioupos P. Mechanical properties and the hierarchical structure of bone. Med Eng Phys. 1998;20(2):92–102.PubMedCrossRefGoogle Scholar
  45. 45.
    Velasco MA, Narvaez-Tovar CA, Garzon-Alvarado DA. Design, materials, and mechanobiology of biodegradable scaffolds for bone tissue engineering. Biomed Res Int. 2015;2015:729076.PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Pearle AD, Warren RF, Rodeo SA. Basic science of articular cartilage and osteoarthritis. Clin Sports Med. 2005;24(1):1–12.PubMedCrossRefGoogle Scholar
  47. 47.
    Treppo S, et al. Comparison of biomechanical and biochemical properties of cartilage from human knee and ankle pairs. J Orthop Res. 2000;18(5):739–48.PubMedCrossRefGoogle Scholar
  48. 48.
    Moutos FT, Estes BT, Guilak F. Multifunctional hybrid three-dimensionally woven scaffolds for cartilage tissue engineering. Macromol Biosci. 2010;10(11):1355–64.PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Hendrikson WJ, et al. The use of finite element analyses to design and fabricate three-dimensional scaffolds for skeletal tissue engineering. Front Bioeng Biotechnol. 2017;5:30.PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Maganaris CN, et al. Quantification of internal stress-strain fields in human tendon: unraveling the mechanisms that underlie regional tendon adaptations and mal-adaptations to mechanical loading and the effectiveness of therapeutic eccentric exercise. Front Physiol. 2017;8:91.PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Youngstrom DW, Barrett JG. Engineering tendon: scaffolds, bioreactors, and models of regeneration. Stem Cells Int. 2016;2016:3919030.PubMedCrossRefGoogle Scholar
  52. 52.
    Fernandez-Yague MA, et al. Biomimetic approaches in bone tissue engineering: Integrating biological and physicomechanical strategies. Adv Drug Deliv Rev. 2015;84:1–29.PubMedCrossRefGoogle Scholar
  53. 53.
    Markides H, McLaren JS, El Haj AJ. Overcoming translational challenges—the delivery of mechanical stimuli in vivo. Int J Biochem Cell Biol. 2015;69:162–72.PubMedCrossRefGoogle Scholar
  54. 54.
    Sailaja GS, et al. Biomimetic approaches with smart interfaces for bone regeneration. J Biomed Sci. 2016;23(1):77.PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Madurantakam PA, et al. Science of nanofibrous scaffold fabrication: strategies for next generation tissue-engineering scaffolds. Nanomedicine (Lond). 2009;4(2):193–206.CrossRefGoogle Scholar
  56. 56.
    Hogrebe NJ, Reinhardt JW, Gooch KJ. Biomaterial microarchitecture: a potent regulator of individual cell behavior and multicellular organization. J Biomed Mater Res A. 2017;105(2):640–61.PubMedCrossRefGoogle Scholar
  57. 57.
    Akhmanova M, et al. Physical, spatial, and molecular aspects of extracellular matrix of in vivo niches and artificial scaffolds relevant to stem cells research. Stem Cells Int. 2015;2015:167025.PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Maheshwari G, et al. Cell adhesion and motility depend on nanoscale RGD clustering. J Cell Sci. 2000;113(Pt 10):1677–86.PubMedGoogle Scholar
  59. 59.
    Curry AS, et al. Taking cues from the extracellular matrix to design bone-mimetic regenerative scaffolds. Matrix Biol. 2016;52-54:397–412.PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Tatman PD, et al. Multiscale biofabrication of articular cartilage: bioinspired and biomimetic approaches. Tissue Eng Part B Rev. 2015;21(6):543–59.PubMedCrossRefGoogle Scholar
  61. 61.
    Ban E, et al. Collagen organization in facet capsular ligaments varies with spinal region and with ligament deformation. J Biomech Eng. 2017;139(7). https://doi.org/10.1115/1.4036019.Google Scholar
  62. 62.
    Wade RJ, Burdick JA. Engineering ECM signals into biomaterials. Mater Today. 2012;15(10):454–9.CrossRefGoogle Scholar
  63. 63.
    Smith LA, Liu X, Ma PX. Tissue engineering with nano-fibrous scaffolds. Soft Matter. 2008;4(11):2144–9.PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Chen R, Hunt JA. Biomimetic materials processing for tissue-engineering processes. J Mater Chem. 2007;17(38):3974–9.CrossRefGoogle Scholar
  65. 65.
    Hartgerink JD, Beniash E, Stupp SI. Self-assembly and mineralization of peptide-amphiphile nanofibers. Science. 2001;294(5547):1684–8.PubMedCrossRefGoogle Scholar
  66. 66.
    Mata A, et al. Bone regeneration mediated by biomimetic mineralization of a nanofiber matrix. Biomaterials. 2010;31(23):6004–12.PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Horii A, et al. Biological designer self-assembling peptide nanofiber scaffolds significantly enhance osteoblast proliferation, differentiation and 3-D migration. PLoS One. 2007;2(2):e190.PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Galler KM, et al. Self-assembling peptide amphiphile nanofibers as a scaffold for dental stem cells. Tissue Eng A. 2008;14(12):2051–8.CrossRefGoogle Scholar
  69. 69.
    Kirkham J, et al. Self-assembling peptide scaffolds promote enamel remineralization. J Dent Res. 2007;86(5):426–30.PubMedCrossRefGoogle Scholar
  70. 70.
    Shah RN, et al. Supramolecular design of self-assembling nanofibers for cartilage regeneration. Proc Natl Acad Sci U S A. 2010;107(8):3293–8.PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Sargeant TD, et al. Hybrid bone implants: self-assembly of peptide amphiphile nanofibers within porous titanium. Biomaterials. 2008;29(2):161–71.PubMedCrossRefGoogle Scholar
  72. 72.
    Hosseinkhani H, et al. Ectopic bone formation in collagen sponge self-assembled peptide-amphiphile nanofibers hybrid scaffold in a perfusion culture bioreactor. Biomaterials. 2006;27(29):5089–98.PubMedCrossRefGoogle Scholar
  73. 73.
    Pina S, Oliveira JM, Reis RL. Natural-based nanocomposites for bone tissue engineering and regenerative medicine: a review. Adv Mater. 2015;27(7):1143–69.PubMedCrossRefGoogle Scholar
  74. 74.
    Buttafoco L, et al. Electrospinning of collagen and elastin for tissue engineering applications. Biomaterials. 2006;27(5):724–34.PubMedCrossRefGoogle Scholar
  75. 75.
    Asran AS, Henning S, Michler GH. Polyvinyl alcohol–collagen–hydroxyapatite biocomposite nanofibrous scaffold: mimicking the key features of natural bone at the nanoscale level. Polymer. 2010;51(4):868–76.CrossRefGoogle Scholar
  76. 76.
    Zhang Y, et al. Electrospinning of gelatin fibers and gelatin/PCL composite fibrous scaffolds. J Biomed Mater Res B Appl Biomater. 2005;72((1):156–65.CrossRefGoogle Scholar
  77. 77.
    Kim HW, Song JH, Kim HE. Nanofiber generation of gelatin–hydroxyapatite biomimetics for guided tissue regeneration. Adv Funct Mater. 2005;15(12):1988–94.CrossRefGoogle Scholar
  78. 78.
    Park YJ, et al. Immobilization of bone morphogenetic protein-2 on a nanofibrous chitosan membrane for enhanced guided bone regeneration. Biotechnol Appl Biochem. 2006;43(Pt 1):17–24.PubMedGoogle Scholar
  79. 79.
    Shalumon KT, et al. Effect of incorporation of nanoscale bioactive glass and hydroxyapatite in PCL/chitosan nanofibers for bone and periodontal tissue engineering. J Biomed Nanotechnol. 2013;9(3):430–40.PubMedCrossRefGoogle Scholar
  80. 80.
    Li C, et al. Electrospun silk-BMP-2 scaffolds for bone tissue engineering. Biomaterials. 2006;27(16):3115–24.PubMedCrossRefGoogle Scholar
  81. 81.
    Jin HJ, et al. Human bone marrow stromal cell responses on electrospun silk fibroin mats. Biomaterials. 2004;25(6):1039–47.PubMedCrossRefGoogle Scholar
  82. 82.
    Prabhakaran MP, Venugopal J, Ramakrishna S. Electrospun nanostructured scaffolds for bone tissue engineering. Acta Biomater. 2009;5(8):2884–93.PubMedCrossRefGoogle Scholar
  83. 83.
    Shin YC, et al. Stimulated myoblast differentiation on graphene oxide-impregnated PLGA-collagen hybrid fibre matrices. J Nanobiotechnol. 2015;13(1):21.CrossRefGoogle Scholar
  84. 84.
    Zamanlui S, et al. Enhanced chondrogenic differentiation of human bone marrow mesenchymal stem cells on PCL/PLGA electrospun with different alignment and composition. Int J Polym Mater Polym Biomater. 2018;67:50–60.CrossRefGoogle Scholar
  85. 85.
    Yoshimoto H, et al. A biodegradable nanofiber scaffold by electrospinning and its potential for bone tissue engineering. Biomaterials. 2003;24(12):2077–82.PubMedCrossRefGoogle Scholar
  86. 86.
    Phipps MC, et al. Increasing the pore sizes of bone-mimetic electrospun scaffolds comprised of polycaprolactone, collagen I and hydroxyapatite to enhance cell infiltration. Biomaterials. 2012;33(2):524–34.PubMedCrossRefGoogle Scholar
  87. 87.
    Brun P, et al. Electrospun scaffolds of self-assembling peptides with poly(ethylene oxide) for bone tissue engineering. Acta Biomater. 2011;7(6):2526–32.PubMedCrossRefGoogle Scholar
  88. 88.
    Ma PX, Zhang R. Synthetic nano-scale fibrous extracellular matrix. J Biomed Mater Res. 1999;46(1):60–72.PubMedCrossRefGoogle Scholar
  89. 89.
    Vasita R, Katti DS. Nanofibers and their applications in tissue engineering. Int J Nanomedicine. 2006;1(1):15.PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Hu Y, et al. Development of a porous poly (L-lactic acid)/hydroxyapatite/collagen scaffold as a BMP delivery system and its use in healing canine segmental bone defect. J Biomed Mater Res A. 2003;67(2):591–8.PubMedCrossRefGoogle Scholar
  91. 91.
    Liu X, et al. Biomimetic nanofibrous gelatin/apatite composite scaffolds for bone tissue engineering. Biomaterials. 2009;30(12):2252–8.PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Liu X, Ma PX. Phase separation, pore structure, and properties of nanofibrous gelatin scaffolds. Biomaterials. 2009;30(25):4094–103.PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Toskas G, et al. Chitosan (PEO)/silica hybrid nanofibers as a potential biomaterial for bone regeneration. Carbohydr Polym. 2013;94(2):713–22.PubMedCrossRefGoogle Scholar
  94. 94.
    Chen VJ, Smith LA, Ma PX. Bone regeneration on computer-designed nano-fibrous scaffolds. Biomaterials. 2006;27(21):3973–9.PubMedCrossRefGoogle Scholar
  95. 95.
    Wei G, Ma PX. Macroporous and nanofibrous polymer scaffolds and polymer/bone-like apatite composite scaffolds generated by sugar spheres. J Biomed Mater Res A. 2006;78((2):306–15.CrossRefGoogle Scholar
  96. 96.
    Zhang R, Ma PX. Synthetic nano-fibrillar extracellular matrices with predesigned macroporous architectures. J Biomed Mater Res. 2000;52(2):430–8.PubMedCrossRefGoogle Scholar
  97. 97.
    Holzwarth JM, Ma PX. Biomimetic nanofibrous scaffolds for bone tissue engineering. Biomaterials. 2011;32(36):9622–9.PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Villa MM, et al. Bone tissue engineering with a collagen-hydroxyapatite scaffold and culture expanded bone marrow stromal cells. J Biomed Mater Res B Appl Biomater. 2015;103(2):243–53.PubMedCrossRefGoogle Scholar
  99. 99.
    Calabrese G, et al. Collagen-hydroxyapatite scaffolds induce human adipose derived stem cells osteogenic differentiation in vitro. PLoS One. 2016;11(3):e0151181.PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Kim HW, Kim HE, Salih V. Stimulation of osteoblast responses to biomimetic nanocomposites of gelatin-hydroxyapatite for tissue engineering scaffolds. Biomaterials. 2005;26(25):5221–30.PubMedCrossRefGoogle Scholar
  101. 101.
    Ravichandran R, et al. Bioinspired hybrid mesoporous silica–gelatin sandwich construct for bone tissue engineering. Microporous Mesoporous Mater. 2014;187:53–62.CrossRefGoogle Scholar
  102. 102.
    Cheng H, et al. Mussel-inspired multifunctional hydrogel coating for prevention of infections and enhanced osteogenesis. ACS Appl Mater Interfaces. 2017;9(13):11428–39.PubMedCrossRefGoogle Scholar
  103. 103.
    Xu C, et al. Biocompatibility and osteogenesis of biomimetic bioglass-collagen-phosphatidylserine composite scaffolds for bone tissue engineering. Biomaterials. 2011;32(4):1051–8.PubMedCrossRefGoogle Scholar
  104. 104.
    Bhumiratana S, et al. Nucleation and growth of mineralized bone matrix on silk-hydroxyapatite composite scaffolds. Biomaterials. 2011;32(11):2812–20.PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Zhang Y, et al. The osteogenic properties of CaP/silk composite scaffolds. Biomaterials. 2010;31(10):2848–56.PubMedCrossRefGoogle Scholar
  106. 106.
    Isikli C, Hasirci V, Hasirci N. Development of porous chitosan-gelatin/hydroxyapatite composite scaffolds for hard tissue-engineering applications. J Tissue Eng Regen Med. 2012;6(2):135–43.PubMedCrossRefGoogle Scholar
  107. 107.
    Deepthi S, et al. An overview of chitin or chitosan/nano ceramic composite scaffolds for bone tissue engineering. Int J Biol Macromol. 2016;93(Pt B):1338–53.PubMedCrossRefGoogle Scholar
  108. 108.
    Thein-Han WW, Misra RD. Biomimetic chitosan-nanohydroxyapatite composite scaffolds for bone tissue engineering. Acta Biomater. 2009;5(4):1182–97.PubMedCrossRefGoogle Scholar
  109. 109.
    Lin HR, Yeh YJ. Porous alginate/hydroxyapatite composite scaffolds for bone tissue engineering: preparation, characterization, and in vitro studies. J Biomed Mater Res B Appl Biomater. 2004;71(1):52–65.PubMedCrossRefGoogle Scholar
  110. 110.
    Luo Y, et al. Hierarchical mesoporous bioactive glass/alginate composite scaffolds fabricated by three-dimensional plotting for bone tissue engineering. Biofabrication. 2012;5(1):015005.PubMedCrossRefGoogle Scholar
  111. 111.
    Silva-Correia J, et al. Gellan gum-based hydrogels for intervertebral disc tissue-engineering applications. J Tissue Eng Regen Med. 2011;5(6):e97–107.PubMedCrossRefGoogle Scholar
  112. 112.
    Manda-Guiba G, et al. Gellan gum: hydroxyapatite composite hydrogels for bone tissue engineering. J Tissue Eng Regen Med. 2012;6(Suppl. 2):15.Google Scholar
  113. 113.
    Tan H, et al. Injectable in situ forming biodegradable chitosan-hyaluronic acid based hydrogels for cartilage tissue engineering. Biomaterials. 2009;30(13):2499–506.PubMedPubMedCentralCrossRefGoogle Scholar
  114. 114.
    Tang S, et al. Fabrication and characterization of porous hyaluronic acid-collagen composite scaffolds. J Biomed Mater Res A. 2007;82(2):323–35.PubMedCrossRefGoogle Scholar
  115. 115.
    Middleton JC, Tipton AJ. Synthetic biodegradable polymers as orthopedic devices. Biomaterials. 2000;21(23):2335–46.PubMedCrossRefGoogle Scholar
  116. 116.
    Gunatillake P, Mayadunne R, Adhikari R. Recent developments in biodegradable synthetic polymers. Biotechnol Annu Rev. 2006;12:301–47.PubMedCrossRefGoogle Scholar
  117. 117.
    Lee CR, et al. Fibrin-polyurethane composites for articular cartilage tissue engineering: a preliminary analysis. Tissue Eng. 2005;11(9–10):1562–73.PubMedCrossRefGoogle Scholar
  118. 118.
    McKeon-Fischer KD, Freeman JW. Characterization of electrospun poly(L-lactide) and gold nanoparticle composite scaffolds for skeletal muscle tissue engineering. J Tissue Eng Regen Med. 2011;5(7):560–8.PubMedCrossRefGoogle Scholar
  119. 119.
    Dong Z, Li Y, Zou Q. Degradation and biocompatibility of porous nano-hydroxyapatite/polyurethane composite scaffold for bone tissue engineering. Appl Surf Sci. 2009;255(12):6087–91.CrossRefGoogle Scholar
  120. 120.
    Liao SS, et al. Hierarchically biomimetic bone scaffold materials: nano-HA/collagen/PLA composite. J Biomed Mater Res B Appl Biomater. 2004;69((2):158–65.CrossRefGoogle Scholar
  121. 121.
    Chu CR, et al. Articular cartilage repair using allogeneic perichondrocyteseeded biodegradable porous polylactic acid (PLA): a tissue-engineering study. J Biomed Mater Res. 1995;29(9):1147–54.PubMedCrossRefGoogle Scholar
  122. 122.
    Liao IC, et al. Composite three-dimensional woven scaffolds with interpenetrating network hydrogels to create functional synthetic articular cartilage. Adv Funct Mater. 2013;23(47):5833–9.PubMedPubMedCentralCrossRefGoogle Scholar
  123. 123.
    Zhao J, et al. Preparation of bioactive porous HA/PCL composite scaffolds. Appl Surf Sci. 2008;255(5):2942–6.CrossRefGoogle Scholar
  124. 124.
    Kim HW, Knowles JC, Kim HE. Hydroxyapatite/poly(epsilon-caprolactone) composite coatings on hydroxyapatite porous bone scaffold for drug delivery. Biomaterials. 2004;25(7–8):1279–87.PubMedCrossRefGoogle Scholar
  125. 125.
    Shin H, Jo S, Mikos AG. Biomimetic materials for tissue engineering. Biomaterials. 2003;24(24):4353–64.PubMedCrossRefGoogle Scholar
  126. 126.
    Humphries MJ, et al. Identification of an alternatively spliced site in human plasma fibronectin that mediates cell type-specific adhesion. J Cell Biol. 1986;103(6):2637–47.PubMedCrossRefGoogle Scholar
  127. 127.
    Bougas K, et al. In vivo evaluation of a novel implant coating agent: laminin-1. Clin Implant Dent Relat Res. 2014;16(5):728–35.PubMedCrossRefGoogle Scholar
  128. 128.
    Javed F, et al. Laminin coatings on implant surfaces promote osseointegration: fact or fiction? Arch Oral Biol. 2016;68:153–61.PubMedCrossRefGoogle Scholar
  129. 129.
    Munisamy S, Vaidyanathan TK, Vaidyanathan J. A bone-like precoating strategy for implants: collagen immobilization and mineralization on pure titanium implant surface. J Oral Implantol. 2008;34(2):67–75.PubMedCrossRefGoogle Scholar
  130. 130.
    Nagai M, et al. In vitro study of collagen coating of titanium implants for initial cell attachment. Dent Mater J. 2002;21(3):250–60.PubMedCrossRefGoogle Scholar
  131. 131.
    Rammelt S, et al. Coating of titanium implants with type-I collagen. J Orthop Res. 2004;22(5):1025–34.PubMedCrossRefGoogle Scholar
  132. 132.
    Schmidmaier G, et al. Bone morphogenetic protein-2 coating of titanium implants increases biomechanical strength and accelerates bone remodeling in fracture treatment: a biomechanical and histological study in rats. Bone. 2002;30(6):816–22.PubMedCrossRefGoogle Scholar
  133. 133.
    Wang J, et al. BMP-functionalised coatings to promote osteogenesis for orthopaedic implants. Int J Mol Sci. 2014;15(6):10150–68.PubMedPubMedCentralCrossRefGoogle Scholar
  134. 134.
    Goodman SB, et al. The future of biologic coatings for orthopaedic implants. Biomaterials. 2013;34(13):3174–83.PubMedPubMedCentralCrossRefGoogle Scholar
  135. 135.
    Ferris DM, et al. RGD-coated titanium implants stimulate increased bone formation in vivo. Biomaterials. 1999;20(23–24):2323–31.PubMedCrossRefGoogle Scholar
  136. 136.
    Elmengaard B, Bechtold JE, Søballe K. In vivo study of the effect of RGD treatment on bone ongrowth on press-fit titanium alloy implants. Biomaterials. 2005;26(17):3521–6.PubMedCrossRefGoogle Scholar
  137. 137.
    Agarwal R, García AJ. Biomaterial strategies for engineering implants for enhanced osseointegration and bone repair. Adv Drug Deliv Rev. 2015;94:53–62.PubMedPubMedCentralCrossRefGoogle Scholar
  138. 138.
    Reyes CD, et al. Biomolecular surface coating to enhance orthopaedic tissue healing and integration. Biomaterials. 2007;28(21):3228–35.PubMedPubMedCentralCrossRefGoogle Scholar
  139. 139.
    Dee KC, Andersen TT, Bizios R. Design and function of novel osteoblast-adhesive peptides for chemical modification of biomaterials. J Biomed Mater Res A. 1998;40(3):371–7.CrossRefGoogle Scholar
  140. 140.
    Rezania A, Healy KE. Biomimetic peptide surfaces that regulate adhesion, spreading, cytoskeletal organization, and mineralization of the matrix deposited by osteoblast-like cells. Biotechnol Prog. 1999;15(1):19–32.PubMedCrossRefGoogle Scholar
  141. 141.
    Suzuki Y, et al. Alginate hydrogel linked with synthetic oligopeptide derived from BMP-2 allows ectopic osteoinduction in vivo. J Biomed Mater Res. 2000;50(3):405–9.PubMedCrossRefGoogle Scholar
  142. 142.
    Ramaraju H, Miller SJ, Kohn DH. Dual-functioning phage-derived peptides encourage human bone marrow cell-specific attachment to mineralized biomaterials. Connect Tissue Res. 2014;55(Suppl 1):160–3.PubMedPubMedCentralCrossRefGoogle Scholar
  143. 143.
    West JL, Hubbell JA. Polymeric biomaterials with degradation sites for proteases involved in cell migration. Macromolecules. 1999;32(1):241–4.CrossRefGoogle Scholar
  144. 144.
    Samorezov JE, Alsberg E. Spatial regulation of controlled bioactive factor delivery for bone tissue engineering. Adv Drug Deliv Rev. 2015;84:45–67.PubMedCrossRefGoogle Scholar
  145. 145.
    Seeherman H, Wozney JM. Delivery of bone morphogenetic proteins for orthopedic tissue regeneration. Cytokine Growth Factor Rev. 2005;16(3):329–45.PubMedCrossRefGoogle Scholar
  146. 146.
    Blackwood KA, et al. Scaffolds for growth factor delivery as applied to bone tissue engineering. Int J Polym Sci. 2012;2012:25.CrossRefGoogle Scholar
  147. 147.
    Chen FM, Zhang M, Wu ZF. Toward delivery of multiple growth factors in tissue engineering. Biomaterials. 2010;31(24):6279–308.PubMedCrossRefGoogle Scholar
  148. 148.
    Chen RR, Mooney DJ. Polymeric growth factor delivery strategies for tissue engineering. Pharm Res. 2003;20(8):1103–12.PubMedCrossRefGoogle Scholar
  149. 149.
    Borselli C, et al. Functional muscle regeneration with combined delivery of angiogenesis and myogenesis factors. Proc Natl Acad Sci U S A. 2010;107(8):3287–92.PubMedPubMedCentralCrossRefGoogle Scholar
  150. 150.
    Doukas J, et al. Delivery of FGF genes to wound repair cells enhances arteriogenesis and myogenesis in skeletal muscle. Mol Ther. 2002;5(5 Pt 1):517–27.PubMedCrossRefGoogle Scholar
  151. 151.
    Whitehead KA, Langer R, Anderson DG. Knocking down barriers: advances in siRNA delivery. Nat Rev Drug Discov. 2009;8(2):129–38.PubMedCrossRefGoogle Scholar
  152. 152.
    Stallmann HP, et al. Antimicrobial peptides: review of their application in musculoskeletal infections. Injury. 2006;37(2):S34–40.PubMedCrossRefGoogle Scholar
  153. 153.
    Liu Y, et al. Biofabrication to build the biology-device interface. Biofabrication. 2010;2(2):022002.PubMedCrossRefGoogle Scholar
  154. 154.
    Patra S, Young V. A review of 3D printing techniques and the future in biofabrication of bioprinted tissue. Cell Biochem Biophys. 2016;74(2):93–8.PubMedCrossRefGoogle Scholar
  155. 155.
    Pedde RD, et al. Emerging biofabrication strategies for engineering complex tissue constructs. Adv Mater. 2017;29(19). https://doi.org/10.1002/adma.201606061.Google Scholar
  156. 156.
    Groll J, et al. Biofabrication: reappraising the definition of an evolving field. Biofabrication. 2016;8(1):013001.PubMedCrossRefGoogle Scholar
  157. 157.
    Orciani M, et al. Biofabrication and bone tissue regeneration: cell source, approaches, and challenges. Front Bioeng Biotechnol. 2017;5:17.PubMedPubMedCentralCrossRefGoogle Scholar
  158. 158.
    Skardal A, Atala A. Biomaterials for integration with 3-D bioprinting. Ann Biomed Eng. 2015;43(3):730–46.PubMedCrossRefGoogle Scholar
  159. 159.
    Derby B. Printing and prototyping of tissues and scaffolds. Science. 2012;338(6109):921–6.PubMedCrossRefGoogle Scholar
  160. 160.
    Datta P, Ayan B, Ozbolat IT. Bioprinting for vascular and vascularized tissue biofabrication. Acta Biomater. 2017;51:1–20.PubMedCrossRefGoogle Scholar
  161. 161.
    Imade S, et al. Effectiveness and limitations of autologous osteochondral grafting for the treatment of articular cartilage defects in the knee. Knee Surg Sports Traumatol Arthrosc. 2012;20(1):160–5.PubMedCrossRefGoogle Scholar
  162. 162.
    Camp CL, Stuart MJ, Krych AJ. Current concepts of articular cartilage restoration techniques in the knee. Sports Health. 2014;6(3):265–73.PubMedPubMedCentralCrossRefGoogle Scholar
  163. 163.
    Charalambous CP, Kwaees TA. Anatomical considerations in hamstring tendon harvesting for anterior cruciate ligament reconstruction. Muscles Ligaments Tendons J. 2012;2(4):253–7.PubMedGoogle Scholar
  164. 164.
    Macaulay AA, Perfetti DC, Levine WN. Anterior cruciate ligament graft choices. Sports Health. 2012;4(1):63–8.PubMedPubMedCentralCrossRefGoogle Scholar
  165. 165.
    Koh HS, et al. Factors affecting patients’ graft choice in anterior cruciate ligament reconstruction. Clin Orthop Surg. 2010;2(2):69–75.PubMedPubMedCentralCrossRefGoogle Scholar
  166. 166.
    Shaunak S, Dhinsa BS, Khan WS. The role of 3D modelling and printing in orthopaedic tissue engineering: a review of the current literature. Curr Stem Cell Res Ther. 2017;12(3):225–32.PubMedCrossRefGoogle Scholar
  167. 167.
    Will J, et al. Porous ceramic bone scaffolds for vascularized bone tissue regeneration. J Mater Sci Mater Med. 2008;19(8):2781–90.PubMedCrossRefGoogle Scholar
  168. 168.
    Saijo H, et al. Maxillofacial reconstruction using custom-made artificial bones fabricated by inkjet printing technology. J Artif Organs. 2009;12(3):200–5.PubMedCrossRefGoogle Scholar
  169. 169.
    Inzana JA, et al. 3D printing of composite calcium phosphate and collagen scaffolds for bone regeneration. Biomaterials. 2014;35(13):4026–34.PubMedPubMedCentralCrossRefGoogle Scholar
  170. 170.
    Wang Y, et al. 3D fabrication and characterization of phosphoric acid scaffold with a HA/beta-TCP weight ratio of 60:40 for bone tissue engineering applications. PLoS One. 2017;12(4):e0174870.PubMedPubMedCentralCrossRefGoogle Scholar
  171. 171.
    Nganga S, et al. Inkjet printing of Chitlac-nanosilver--a method to create functional coatings for non-metallic bone implants. Biofabrication. 2014;6(4):041001.PubMedCrossRefGoogle Scholar
  172. 172.
    Barui S, et al. Microstructure and compression properties of 3D powder printed Ti-6Al-4V scaffolds with designed porosity: experimental and computational analysis. Mater Sci Eng C Mater Biol Appl. 2017;70(Pt 1):812–23.PubMedCrossRefGoogle Scholar
  173. 173.
    Lauria I, et al. Inkjet printed periodical micropatterns made of inert alumina ceramics induce contact guidance and stimulate osteogenic differentiation of mesenchymal stromal cells. Acta Biomater. 2016;44:85–96.PubMedCrossRefGoogle Scholar
  174. 174.
    Cui X, et al. Direct human cartilage repair using three-dimensional bioprinting technology. Tissue Eng A. 2012;18(11–12):1304–12.CrossRefGoogle Scholar
  175. 175.
    Cui X, et al. Human cartilage tissue fabrication using three-dimensional inkjet printing technology. J Vis Exp. 2014(88). https://doi.org/10.3791/51294.Google Scholar
  176. 176.
    Xu T, et al. Hybrid printing of mechanically and biologically improved constructs for cartilage tissue engineering applications. Biofabrication. 2013;5(1):015001.PubMedCrossRefGoogle Scholar
  177. 177.
    Gao G, et al. Bioactive nanoparticles stimulate bone tissue formation in bioprinted three-dimensional scaffold and human mesenchymal stem cells. Biotechnol J. 2014;9(10):1304–11.PubMedCrossRefGoogle Scholar
  178. 178.
    Gao G, et al. 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
  179. 179.
    Gao G, et al. Inkjet-bioprinted acrylated peptides and PEG hydrogel with human mesenchymal stem cells promote robust bone and cartilage formation with minimal printhead clogging. Biotechnol J. 2015;10(10):1568–77.PubMedCrossRefGoogle Scholar
  180. 180.
    Mozetic P, et al. Engineering muscle cell alignment through 3D bioprinting. J Biomed Mater Res A. 2017;105(9):2582–8.PubMedCrossRefGoogle Scholar
  181. 181.
    Costantini M, et al. Microfluidic-enhanced 3D bioprinting of aligned myoblast-laden hydrogels leads to functionally organized myofibers in vitro and in vivo. Biomaterials. 2017;131:98–110.PubMedCrossRefGoogle Scholar
  182. 182.
    Kang HW, et al. A 3D bioprinting system to produce human-scale tissue constructs with structural integrity. Nat Biotechnol. 2016;34(3):312–9.PubMedCrossRefGoogle Scholar
  183. 183.
    Merceron TK, et al. A 3D bioprinted complex structure for engineering the muscle-tendon unit. Biofabrication. 2015;7(3):035003.PubMedCrossRefGoogle Scholar
  184. 184.
    Xu N, et al. 3D artificial bones for bone repair prepared by computed tomography-guided fused deposition modeling for bone repair. ACS Appl Mater Interfaces. 2014;6(17):14952–63.PubMedCrossRefGoogle Scholar
  185. 185.
    Byambaa B, et al. Bioprinted osteogenic and vasculogenic patterns for engineering 3D bone tissue. Adv Healthc Mater. 2017;6(16). https://doi.org/10.1002/adhm.201700015.Google Scholar
  186. 186.
    McBeth C, et al. 3D bioprinting of GelMA scaffolds triggers mineral deposition by primary human osteoblasts. Biofabrication. 2017;9(1):015009.PubMedCrossRefGoogle Scholar
  187. 187.
    O’Connell CD, et al. Development of the Biopen: a handheld device for surgical printing of adipose stem cells at a chondral wound site. Biofabrication. 2016;8(1):015019.PubMedCrossRefGoogle Scholar
  188. 188.
    Di Bella C, et al. In-situ handheld 3D bioprinting for cartilage regeneration. J Tissue Eng Regen Med. 2017. https://doi.org/10.1002/term.2476.Google Scholar
  189. 189.
    Muller M, et al. Alginate sulfate-nanocellulose bioinks for cartilage bioprinting applications. Ann Biomed Eng. 2017;45(1):210–23.PubMedCrossRefGoogle Scholar
  190. 190.
    Skoog SA, Goering PL, Narayan RJ. Stereolithography in tissue engineering. J Mater Sci Mater Med. 2014;25(3):845–56.PubMedCrossRefGoogle Scholar
  191. 191.
    Thavornyutikarn B, et al. Porous 45S5 Bioglass(R)-based scaffolds using stereolithography: effect of partial pre-sintering on structural and mechanical properties of scaffolds. Mater Sci Eng C Mater Biol Appl. 2017;75:1281–8.PubMedCrossRefGoogle Scholar
  192. 192.
    Guillaume O, et al. Surface-enrichment with hydroxyapatite nanoparticles in stereolithography-fabricated composite polymer scaffolds promotes bone repair. Acta Biomater. 2017;54:386–98.PubMedCrossRefGoogle Scholar
  193. 193.
    Zhou X, et al. Improved human bone marrow mesenchymal stem cell osteogenesis in 3D bioprinted tissue scaffolds with low intensity pulsed ultrasound stimulation. Sci Rep. 2016;6:32876.PubMedPubMedCentralCrossRefGoogle Scholar
  194. 194.
    Bian W, et al. Morphological characteristics of cartilage-bone transitional structures in the human knee joint and CAD design of an osteochondral scaffold. Biomed Eng Online. 2016;15(1):82.PubMedPubMedCentralCrossRefGoogle Scholar
  195. 195.
    Sun AX, et al. Projection stereolithographic fabrication of human adipose stem cell-incorporated biodegradable scaffolds for cartilage tissue engineering. Front Bioeng Biotechnol. 2015;3:115.PubMedPubMedCentralGoogle Scholar
  196. 196.
    Melchels FP, Feijen J, Grijpma DW. A review on stereolithography and its applications in biomedical engineering. Biomaterials. 2010;31(24):6121–30.PubMedCrossRefGoogle Scholar
  197. 197.
    Catros S, et al. Laser-assisted bioprinting for creating on-demand patterns of human osteoprogenitor cells and nano-hydroxyapatite. Biofabrication. 2011;3(2):025001.PubMedCrossRefGoogle Scholar
  198. 198.
    Keriquel V, et al. In situ printing of mesenchymal stromal cells, by laser-assisted bioprinting, for in vivo bone regeneration applications. Sci Rep. 2017;7(1):1778.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2017

Authors and Affiliations

  • R. Portillo-Lara
    • 1
    • 2
  • E. Shirzaei Sani
    • 1
  • N. Annabi
    • 1
    • 3
    • 4
  1. 1.Department of Chemical EngineeringNortheastern UniversityBostonUSA
  2. 2.Tecnologico de MonterreyEscuela de Ingeniería y CienciasZapopanMexico
  3. 3.Harvard-MIT Division of Health Sciences and TechnologyMassachusetts Institute of TechnologyCambridgeUSA
  4. 4.Biomaterials Innovation Research Center, Brigham and Women’s HospitalHarvard Medical SchoolBostonUSA

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