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Potential Clinical Applications of Three-Dimensional Bioprinting

  • Ippokratis PountosEmail author
  • Nazzar Tellisi
  • Nureddin Ashammakhi
Chapter

Abstract

Three-dimensional (3D) bioprinting aims to construct complex personalized living tissues mimicking the native tissues. This chapter presents the current advances in 3D bioprinting. Available evidence revealed promising results in potential applications for the regeneration of musculoskeletal, cardiovascular, dermal, and neural tissues. These applications comprise a developing field. However, there are still barriers that hamper further expansion of this technology. Such challenges involve the reliable mechanical properties, size limitations, integration of transplanted grafts, and safeguarding of safety throughout the process of 3D printing and resulting constructs.

Keywords

3D bioprinting Bone Mesenchymal stem cells Cartilage Blood vessels Cardiovascular tissue 

Notes

Acknowledgements

Conflict of Interest: No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this chapter.

References

  1. 1.
    Ashammakhi N, Kaarela O, Hasan A, Byambaa B, Sheikhi A, Gaharwar AK, Khademhosseini A (2019) Advancing frontiers in bone bioprinting. Adv Healthc Mater 8:e1801048CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Tellisi N, Ashammakhi NA, Billi F, Kaarela O (2018) Three dimensional printed bone implants in the clinic. J Craniofac Surg 29:2363–2367PubMedPubMedCentralGoogle Scholar
  3. 3.
    Skardal A, Atala A (2015) Biomaterials for integration with 3-D bioprinting. Ann Biomed Eng 43:730–746CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Lei M, Wang X (2018) Biodegradable polymers and stem cells for bioprinting. Molecules 21(5):pii: E539CrossRefGoogle Scholar
  5. 5.
    Malda J, Visser J, Melchels FP, Jüngst T, Hennink WE, Dhert WJ, Groll J, Hutmacher DW (2013) 25th anniversary article: engineering hydrogels for biofabrication. Adv Mater 25:5011–5028CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Jessop ZM, Al-Sabah A, Gardiner MD, Combellack E, Hawkins K, Whitaker IS (2007) 3D bioprinting for reconstructive surgery: principles, applications and challenges. J Plast Reconstr Aesthet Surg 70(9):1155–1170CrossRefGoogle Scholar
  7. 7.
    Ashammakhi N, Ahadian S, Pountos I, Hu S-K, Tellisi N, Bandaru P, Ostrovidov S, Dokmeci M, Khademhosseini A (2019) In situ three-dimensional printing for reparative and regenerative therapy. Biomed Microdevices 21(2):42CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Hong N, Yang GH, Lee J, Kim G (2018) 3D bioprinting and its in vivo applications. J Biomed Mater Res B Appl Biomater 106:444–459CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Luo Y, Lin X, Huang P (2018) 3D Bioprinting of artificial tissues: construction of biomimetic microstructures. Macromol Biosci 18:e1800034CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Pountos I, Giannoudis PV (2016) Is there a role of coral bone substitutes in bone repair? Injury 47:2606–2613CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Panteli M, Pountos I, Jones E, Giannoudis PV (2015) Biological and molecular profile of fracture non-union tissue: current insights. J Cell Mol Med 19:685–713CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Pountos I, Panteli M, Panagiotopoulos E, Jones E, Giannoudis PV (2014) Can we enhance fracture vascularity: what is the evidence? Injury 45(Suppl 2):S49–S57CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Pountos I, Georgouli T, Pneumaticos S, Giannoudis PV (2013) Fracture non-union: can biomarkers predict outcome? Injury 44:1725–1732CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Bajada S, Harrison PE, Ashton BA, Cassar-Pullicino VN, Ashammakhi N, Richardson JB (2007) Successful treatment of refractory tibial nonunion using calcium sulphate and bone marrow stromal cell implantation. J Bone Joint Surg Br 89:1382–1386CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Poldervaart MT, Goversen B, de Ruijter M, Abbadessa A, Melchels FPW, Öner FC, Dhert WJA, Vermonden T, Alblas J (2017) 3D bioprinting of methacrylated hyaluronic acid (MeHA) hydrogel with intrinsic osteogenicity. PLoS One 12:e0177628CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Wang XF, Song Y, Liu YS, Sun YC, Wang YG, Wang Y, Lyu PJ (2016) Osteogenic differentiation of three-dimensional bioprinted constructs consisting of human adipose-derived stem cells in vitro and in vivo. PLoS One 11:e0157214CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Poldervaart MT, Wang H, van der Stok J, Weinans H, Leeuwenburgh SC, Öner FC, Dhert WJ, Alblas J (2013) Sustained release of BMP-2 in bioprinted alginate for osteogenicity in mice and rats. PLoS One 8(8):e72610CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Duarte Campos DF, Blaeser A, Buellesbach K, Sen KS, Xun W, Tillmann W, Fischer H (2016) Bioprinting organotypic hydrogels with improved mesenchymal stem cell remodeling and mineralization properties for bone tissue engineering. Adv Healthc Mater 5:1336–1345CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Seyednejad H, Gawlitta D, Kuiper RV, de Brui A, van Nostrum CF, Vermonden T, Dhert WJA, Hennink WE (2012) In vivo biocompatibility and biodegradation of 3D-printed porous scaffolds based on a hydroxyl-functionalized poly(ε-caprolactone). Biomaterials 33:4309CrossRefGoogle Scholar
  20. 20.
    Park SH, Park DS, Shin JW, Kang YG, Kim HK, Yoon TR, Shin JW (2012) Scaffolds for bone tissue engineering fabricated from two different materials by the rapid prototyping technique: PCL versus PLGA. J Mater Sci Mater Med 23:2671CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Heo SJ, Kim SE, Wei J, Kim DH, Hyun YT, Yun HS, Kim HK, Yoon TR, Kim SH, Park SA, Shin JW, Shin JW (2009) In vitro and animal study of novel nano-hydroxyapatite/poly(epsilon-caprolactone) composite scaffolds fabricated by layer manufacturing process. Tissue Eng Part A 15:977–989CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Kim J, McBride S, Brandi T, Alvarez-Urena P, Song YH, Dean DD, Sylvia VL, Elgendy H, Ong J, Hollinger JO (2012) Rapid-prototyped PLGA/β-TCP/hydroxyapatite nanocomposite scaffolds in a rabbit femoral defect model. Biofabrication 4(2):025003CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Gao G, Schilling AF, Yonezawa T, Wang J, Dai G, Cui X (2014) Bioactive nanoparticles stimulate bone tissue formation in bioprinted three-dimensional scaffold and human mesenchymal stem cells. Biotechnol J 9:1304–1311CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Martin Y, Eldardiri M, Lawrence-Watt DJ, Sharpe JR (2011) Microcarriers and their potential in tissue regeneration. Tissue Eng Part B Rev 17:71–80CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Sart S, Agathos SN, Li Y (2013) Engineering stem cell fate with biochemical and biomechanical properties of microcarriers. Biotechnol Prog 29:1354–1366CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Luo Y, Wu C, Lode A, Gelinsky M (2013) Hierarchical mesoporous bioactive glass/alginate composite scaffolds fabricated by three-dimensional plotting for bone tissue engineering. Biofabrication 5:15005CrossRefGoogle Scholar
  27. 27.
    Reichert JC, Wullschleger ME, Cipitria A, Lienau J, Cheng TK, Schütz MA, Duda GN, Nöth U, Eulert J, Hutmacher DW (2011) Custom-made composite scaffolds for segmental defect repair in long bones. Int Orthop 35:1229–1236CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Keriquel V, Guillemot F, Arnault I, Guillotin B, Miraux S, Amédée J, Fricain JC, Catros S (2010) In vivo bioprinting for computer- and robotic-assisted medical intervention: preliminary study in mice. Biofabrication 2:014101CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Keriquel V, Oliveira H, Rémy M, Ziane S, Delmond S, Rousseau B, Rey S, Catros S, Amédée J, Guillemot F, Fricain JC (2017) In situ printing of mesenchymal stromal cells, by laser-assisted bioprinting, for in vivo bone regeneration applications. Sci Rep 7:1778CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Bendtsen ST, Quinnell SP, Wei M (2017) Development of a novel alginate-polyvinyl alcohol-hydroxyapatite hydrogel for 3D bioprinting bone tissue engineered scaffolds. J Biomed Mater Res A 105:1457–1468CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Demirtaş TT, Irmak G, Gümüşderelioğlu M (2017) A bioprintable form of chitosan hydrogel for bone tissue engineering. Biofabrication 9:035003CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Neufurth M, Wang X, Wang S, Steffen R, Ackermann M, Haep ND, Schröder HC, Müller WEG (2017) 3D printing of hybrid biomaterials for bone tissue engineering: calcium-polyphosphate microparticles encapsulated by polycaprolactone. Acta Biomater 64:377–388CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Zhang Y, Zhai D, Xu M, Yao Q, Zhu H, Chang J, Wu C (2017) 3D-printed bioceramic scaffolds with antibacterial and osteogenic activity. Biofabrication 9:025037CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Du M, Chen B, Meng Q, Liu S, Zheng X, Zhang C, Wang H, Li H, Wang N, Dai J (2015) 3D bioprinting of BMSC-laden methacrylamide gelatin scaffolds with CBD-BMP2-collagen microfibers. Biofabrication 7:044104CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Buckwalter JA, Saltzman C, Brown T (2004) The impact of osteoarthritis: implications for research. Clin Orthop Relat Res (427 Suppl):S6–S15Google Scholar
  36. 36.
    Ashammakhi N, Ahadian S, Darabi MA, Tahchi ME, Lee J, Suthiwanich K, Sheikhi A, Dokmeci MR, Oklu R, Khademhosseini A (2018) Minimally invasive and regenerative therapeutics. Adv Mater 22:e1804041Google Scholar
  37. 37.
    Shi W, Sun M, Hu X, Ren B, Cheng J, Li C, Duan X, Fu X, Zhang J, Chen H, Ao Y (2017) Structurally and functionally optimized silk-fibroin-gelatin scaffold using 3D printing to repair cartilage injury in vitro and in vivo. Adv Mater 29(29)Google Scholar
  38. 38.
    Cui X, Breitenkamp K, Finn MG, Lotz M, D’Lima DD (2012) Direct human cartilage repair using three-dimensional bioprinting technology. Tissue Eng Part A 18:1304–1312CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Kundu J, Shim JH, Jang J, Kim SW, Cho DW (2015) An additive manufacturing-based PCL-alginate-chondrocyte bioprinted scaffold for cartilage tissue engineering. J Tissue Eng Regen Med 9:1286–1297CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Xu T, Binder KW, Albanna MZ, Dice D, Zhao W, Yoo JJ, Atala A (2013) Hybrid printing of mechanically and biologically improved constructs for cartilage tissue engineering applications. Biofabrication 5:015001CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Di Bella C, Duchi S, O'Connell CD, Blanchard R, Augustine C, Yue Z, Thompson F, Richards C, Beirne S, Onofrillo C, Bauquier SH, Ryan SD, Pivonka P, Wallace GG, Choong PF (2018) In situ handheld three-dimensional bioprinting for cartilage regeneration. J Tissue Eng Regen Med 12(3):611–621CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Daly AC, Critchley SE, Rencsok EM, Kelly DJ (2016) A comparison of different bioinks for 3D bioprinting of fibrocartilage and hyaline cartilage. Biofabrication 8:045002CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Pountos I, Giannoudis PV (2017) Modulation of cartilage’s response to injury: can chondrocyte apoptosis be reversed? Injury 48:2657–2669CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Shim JH, Jang KM, Hahn SK, Park JY, Jung H, Oh K, Park KM, Yeom J, Park SH, Kim SW, Wang JH, Kim K, Cho DW (2017) Three-dimensional bioprinting of multilayered constructs containing human mesenchymal stromal cells for osteochondral tissue regeneration in the rabbit knee joint. Biofabrication 8(1):014102CrossRefGoogle Scholar
  45. 45.
    Woodfield TB, Guggenheim M, von Rechenberg B, Riesle J, van Blitterswijk CA, Wedler V (2009) Rapid prototyping of anatomically shaped, tissue-engineered implants for restoring congruent articulating surfaces in small joints. Cell Prolif 42:485–497CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Lee CH, Cook JL, Mendelson A, Moioli EK, Yao H, Mao JJ (2010) Regeneration of the articular surface of the rabbit synovial joint by cell homing: a proof of concept study. Lancet 376:440–448CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Tarafder S, Koch A, Jun Y, Chou C, Awadallah MR, Lee CH (2016) Micro-precise spatiotemporal delivery system embedded in 3D printing for complex tissue regeneration. Biofabrication 8:025003CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Ding C, Qiao Z, Jiang W, Li H, Wei J, Zhou G, Dai K (2013) Regeneration of a goat femoral head using a tissue-specific, biphasic scaffold fabricated with CAD/CAM technology. Biomaterials 34:6706–6716CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Schuurman W, Levett PA, Pot MW, van Weeren PR, Dhert WJ, Hutmacher DW, Melchels FP, Klein TJ, Malda J (2013) Gelatin-methacrylamide hydrogels as potential biomaterials for fabrication of tissue-engineered cartilage constructs. Macromol Biosci 13:551–561CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Markstedt K, Mantas A, Tournier I, Martínez Ávila H, Hägg D, Gatenholm P (2015) 3D bioprinting human chondrocytes with nanocellulose-alginate bioink for cartilage tissue engineering applications. Biomacromolecules 16(5):1489–1496CrossRefGoogle Scholar
  51. 51.
    Costantini M, Idaszek J, Szöke K, Jaroszewicz J, Dentini M, Barbetta A, Brinchmann JE, Święszkowski W (2016) 3D bioprinting of BM-MSCs-loaded ECM biomimetic hydrogels for in vitro neocartilage formation. Biofabrication 8(3):035002CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Ren X, Wang F, Chen C, Gong X, Yin L, Yang L (2016) Engineering zonal cartilage through bioprinting collagen type II hydrogel constructs with biomimetic chondrocyte density gradient. BMC Musculoskelet Disord 17:301CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Nguyen D, Hägg DA, Forsman A, Ekholm J, Nimkingratana P, Brantsing C, Kalogeropoulos T, Zaunz S, Concaro S, Brittberg M, Lindahl A, Gatenholm P, Enejder A, Simonsson S (2017) Cartilage tissue engineering by the 3D bioprinting of iPS cells in a nanocellulose/alginate bioink. Sci Rep 7:658CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Apelgren P, Amoroso M, Lindahl A, Brantsing C, Rotter N, Gatenholm P, Kölby L (2017) Chondrocytes and stem cells in 3D-bioprinted structures create human cartilage in vivo. PLoS One 12:e0189428CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Lee V, Singh G, Trasatti JP, Bjornsson C, Xu X, Tran TN, Yoo SS, Dai G, Karande P (2014) Design and fabrication of human skin by three-dimensional bioprinting. Tissue Eng Part C Methods 20:473–484CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Cubo N, Garcia M, Del Cañizo JF, Velasco D, Jorcano JL (2016) 3D bioprinting of functional human skin: production and in vivo analysis. Biofabrication 9:015006CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Pourchet LJ, Thepot A, Albouy M, Courtial EJ, Boher A, Blum LJ, Marquette CA (2017) Human skin 3D bioprinting using scaffold-free approach. Adv Healthc Mater 6(4):1601101CrossRefGoogle Scholar
  58. 58.
    Lee W, Debasitis JC, Lee VK, Lee JH, Fischer K, Edminster K, Park JK, Yoo SS (2009) Multi-layered culture of human skin fibroblasts and keratinocytes through three-dimensional free form fabrication. Biomaterials 30:1587–1595CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Koch L, Deiwick A, Schlie S, Michael S, Gruene M, Coger V, Zychlinski D, Schambach A, Reimers K, Vogt PM, Chichkov B (2012) Skin tissue generation by laser cell printing. Biotechnol Bioeng 109:1855–1863CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Koch L, Kuhn S, Sorg H, Gruene M, Schlie S, Gaebel R, Polchow B, Reimers K, Stoelting S, Ma N, Vogt PM, Steinhoff G, Chichkov B (2010) Laser printing of skin cells and human stem cells. Tissue Eng Part C Methods 16:847–854CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Michael S, Sorg H, Peck CT, Koch L, Deiwick A, Chichkov B, Vogt PM, Reimers K (2013) Tissue engineered skin substitutes created by laser-assisted bioprinting form skin-like structures in the dorsal skin fold chamber in mice. PLoS One 8:e57741CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Kim BS, Lee JS, Gao G, Cho DW (2017) Direct 3D cell-printing of human skin with functional transwell system. Biofabrication 9(2):025034CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Min D, Lee W, Bae IH, Lee TR, Croce P, Yoo SS (2018) Bioprinting of biomimetic skin containing melanocytes. Exp Dermatol 27:453–459CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Liu J, Chi J, Wang K, Liu X, Liu J, Gu F (2016) Full-thickness wound healing using 3D bioprinted gelatin-alginate scaffolds in mice: a histopathological study. Int J Clin Exp Pathol 9(11):11197–11205Google Scholar
  65. 65.
    Binder KW, Zhao W, Aboushwareb T, Dice D, Atala A, Yoo JJ (2010) In situ bioprinting of the skin for burns. J Am Coll Surg 211:S76CrossRefGoogle Scholar
  66. 66.
    Skardal A, Zhang J, McCoard L, Xu X, Oottamasathien S, Prestwich GD (2010) Photocrosslinkable hyaluronan-gelatin hydrogels for two-step bioprinting. Tissue Eng Part A 16:2675–2685CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Albanna M, Murphy S, Zhao W, El-Amin I, Josh Tan J, Dennis Dice D, Kang HW, Jackson J, Atala A, Yoo J (2012) In situ bioprinting of skin for reconstruction. J Urol 187:e8CrossRefGoogle Scholar
  68. 68.
    Pfister BJ, Gordon T, Loverde JR, Kochar AS, Mackinnon SE, Cullen DK (2011) Biomedical engineering strategies for peripheral nerve repair: surgical applications, state of the art, and future challenges. Crit Rev Biomed Eng 39:81–124CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    England S, Rajaram A, Schreyer DJ, Chen X (2017) Bioprinted fibrin-factor XIII-hyaluronate hydrogel scaffolds with encapsulated Schwann cells and their in vitro characterization for use in nerve regeneration. Bioprinting 5:1–9CrossRefGoogle Scholar
  70. 70.
    Evans GR, Brandt K, Widmer MS, Lu L, Meszlenyi RK, Gupta PK, Mikos AG, Hodges J, Williams J, Gürlek A, Nabawi A, Lohman R, Patrick CW Jr (1999) In vivo evaluation of poly(L-lactic acid) porous conduits for peripheral nerve regeneration. Biomaterials 20:1109–1115CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Radulescu D, Dhar S, Young CM, Taylor DM, Trost HJ, Hayes DJ, Evans GR (2007) Tissue engineering scaffolds for nerve regeneration manufactured by ink-jet technology. Mater Sci Eng C 23:534–539CrossRefGoogle Scholar
  72. 72.
    Lee SJ, Zhu W, Heyburn L, Nowicki M, Harris B, Zhang LG (2017) Development of novel 3-D printed scaffolds with core-shell nanoparticles for nerve regeneration. IEEE Trans Biomed Eng 64:408–418CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Hu Y, Wu Y, Gou Z, Tao J, Zhang J, Liu Q, Kang T, Jiang S, Huang S, He J, Chen S, Du Y, Gou M (2016) 3D-engineering of cellularized conduits for peripheral nerve regeneration. Sci Rep 6:32184CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Yurie H, Ikeguchi R, Aoyama T, Kaizawa Y, Tajino J, Ito A, Ohta S, Oda H, Takeuchi H, Akieda S, Tsuji M, Nakayama K, Matsuda S (2017) The efficacy of a scaffold-free Bio 3D conduit developed from human fibroblasts on peripheral nerve regeneration in a rat sciatic nerve model. PLoS One 12:e0171448CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Adams AM, VanDusen KW, Kostrominova TY, Mertens JP, Larkin LM (2017) Scaffoldless tissue-engineered nerve conduit promotes peripheral nerve regeneration and functional recovery after tibial nerve injury in rats. Neural Regen Res 12:1529–1537CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Atala A, Kasper FK, Mikos AG (2012) Engineering complex tissues. Sci Transl Med 4:160rv12CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Penttilä H, Tulamo R-M, Waris T, Ellä V, Kellomäki M, Törmälä P, Ashammakhi N (2004) Combining prefabricated microvascularied perichondrial flaps and bioabsorbable polylactide nonwoven scaffolds to tissue engineered cartilage. In: Joint Meeting of the Tissue Engineering Society International (TESI) and the European Tissue Engineering Society (ETES), Lausanne, Switzerland, 10–13.10.2004, P020Google Scholar
  78. 78.
    Zhao L, Lee VK, Yoo SS, Dai G, Intes X (2012) The integration of 3-D cell printing and mesoscopic fluorescence molecular tomography of vascular constructs within thick hydrogel scaffolds. Biomaterials 33:5325–5332CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Wu W, DeConinck A, Lewis JA (2011) Omnidirectional printing of 3D microvascular networks. Adv Mater 23(24):H178–H183CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Lee VK, Lanzi AM, Haygan N, Yoo SS, Vincent PA, Dai G (2014) Generation of multi-scale vascular network system within 3D hydrogel using 3D bio-printing technology. Cell Mol Bioeng 7(3):460–472CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Kucukgul C, Ozler SB, Inci I, Karakas E, Irmak S, Gozuacik D, Taralp A, Koc B (2015) 3D bioprinting of biomimetic aortic vascular constructs with self-supporting cells. Biotechnol Bioeng 112(4):811–821CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Kolesky DB, Homan KA, Skylar-Scott MA, Lewis JA (2016) Three-dimensional bioprinting of thick vascularized tissues. Proc Natl Acad Sci U S A 113(12):3179–3184CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Huber B, Engelhardt S, Meyer W, Krüger H, Wenz A, Schönhaar V, Tovat GEM, Kluger PJ, Borchers K (2016) Blood-vessel mimicking structures by stereolithographic fabrication of small porous tubes using cytocompatible polyacrylate elastomers, biofunctionalization and endothelialization. J Funct Biomater 7(2):11CrossRefGoogle Scholar
  84. 84.
    Kolesky DB, Truby RL, Gladman A, Busbee TA, Homan KA, Lewis JA (2014) 3D bioprinting of vascularized, heterogeneous cell-laden tissue constructs. Adv Mater 26(19):3124–3130CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Meyer EP, Ulmann-Schuler A, Staufenbiel M, Krucker T (2008) Altered morphology and 3D architecture of brain vasculature in a mouse model for Alzheimer’s disease. Proc Natl Acad Sci U S A 105(9):3587–3592CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    Xu Y, Hu Y, Liu C, Yao H, Liu B, Mi S (2018) A novel strategy for creating tissue-engineered biomimetic blood vessels using 3D bioprinting technology. Materials (Basel) 11(9):E1581CrossRefGoogle Scholar
  87. 87.
    Kang HW, Lee SJ, Ko IK, Kengla C, Yoo JJ, Atala A (2016) A 3D bioprinting system to produce human-scale tissue constructs with structural integrity. Nat Biotechnol 34:312–319CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Merceron TK, Burt M, Seol YJ, Kang HW, Lee SJ, Yoo JJ, Atala A (2015) A 3D bioprinted complex structure for engineering the muscle-tendon unit. Biofabrication 7:035003CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Cui X, Gao G, Qiu Y (2013) Accelerated myotube formation using bioprinting technology for biosensor applications. Biotechnol Lett 35:315–321CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Altomare L, Riehle M, Gadegaard N, Tanzi MC, Farè S (2010) Microcontact printing of fibronectin on a biodegradable polymeric surface for skeletal muscle cell orientation. Int J Artif Organs 33:535–543CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Peele BN, Wallin TJ, Zhao H, Shepherd RF (2015) 3D printing antagonistic systems of artificial muscle using projection stereolithography. Bioinspir Biomim 10:055003CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    McAloon CJ, Boylan LM, Hamborg T, Stallard N, Osman F, Lim PB, Hayat SA (2016) The changing face of cardiovascular disease 2000-2012: an analysis of the world health organisation global health estimates data. Int J Cardiol 224:256–264CrossRefPubMedPubMedCentralGoogle Scholar
  93. 93.
    Smit FE, Dohmen PM (2015) Cardiovascular tissue engineering: where we come from and where are we now? Med Sci Monit Basic Res 21:1–3PubMedPubMedCentralGoogle Scholar
  94. 94.
    Weinberger F, Mannhardt I, Eschenhagen T (2017) Engineering cardiac muscle tissue: a maturating field of research. Circ Res 120:1487–1500CrossRefPubMedPubMedCentralGoogle Scholar
  95. 95.
    Izadifar M, Chapman D, Babyn P, Chen X, Kelly ME (2018) UV-assisted 3D bioprinting of nanoreinforced hybrid cardiac patch for myocardial tissue engineering. Tissue Eng Part C Methods 24:74–88CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    Gaetani R, Feyen DA, Verhage V, Slaats R, Messina E, Christman KL, Giacomello A, Doevendans PA, Sluijter JP (2015) Epicardial application of cardiac progenitor cells in a 3D-printed gelatin/hyaluronic acid patch preserves cardiac function after myocardial infarction. Biomaterials 61:339–348CrossRefPubMedPubMedCentralGoogle Scholar
  97. 97.
    Wang Z, Lee SJ, Cheng HJ, Yoo JJ, Atala A (2018) 3D bioprinted functional and contractile cardiac tissue constructs. Acta Biomater 70:48–56CrossRefPubMedPubMedCentralGoogle Scholar
  98. 98.
    Hockaday LA, Kang KH, Colangelo NW, Cheung PY, Duan B, Malone E, Wu J, Girardi LN, Bonassar LJ, Lipson H, Chu CC, Butcher JT (2012) Rapid 3D printing of anatomically accurate and mechanically heterogeneous aortic valve hydrogelscaffolds. Biofabrication 4:035005CrossRefPubMedPubMedCentralGoogle Scholar
  99. 99.
    Duan B, Hockaday LA, Kang KH, Butcher JT (2013) 3D bioprinting of heterogeneous aortic valve conduits with alginate/gelatin hydrogels. J Biomed Mater Res A 101:1255–1264CrossRefPubMedPubMedCentralGoogle Scholar
  100. 100.
    Kang LH, Armstrong PA, Lee LJ, Duan B, Kang KH, Butcher JT (2017) Optimizing photo-encapsulation viability of heart valve cell types in 3D printable composite hydrogels. Ann Biomed Eng 45:360–377CrossRefPubMedPubMedCentralGoogle Scholar
  101. 101.
    Lee JW, Choi YJ, Yong WJ, Pati F, Shim JH, Kang KS, Kang IH, Park J, Cho DW (2016) Development of a 3D cell printed construct considering angiogenesis for liver tissue engineering. Biofabrication 8:015007CrossRefPubMedPubMedCentralGoogle Scholar
  102. 102.
    Chang R, Emami K, Wu H, Sun W (2010) Biofabrication of a three-dimensional liver micro-organ as an in vitro drug metabolism model. Biofabrication 2(4):045004CrossRefPubMedPubMedCentralGoogle Scholar
  103. 103.
    Park HS, Lee JS, Jung H, Kim DY, Kim SW, Sultan MT, Park CH (2018) An omentum-cultured 3D-printed artificial trachea: in vivo bioreactor. Artif Cells Nanomed Biotechnol 19:1–10Google Scholar
  104. 104.
    Ávila HM, Schwarz S, Rotter N, Gatenholm P (2016) 3D bioprinting of human chondrocyte-laden nanocellulose hydrogels for patient-specific auricular cartilage regeneration. Bioprinting 1–2:22–35CrossRefGoogle Scholar
  105. 105.
    Lee JS, Hong JM, Jung JW, Shim JH, Oh JH, Cho DW (2014) 3D printing of composite tissue with complex shape applied to ear regeneration. Biofabrication 6(2):024103CrossRefPubMedPubMedCentralGoogle Scholar
  106. 106.
    Reiffel AJ, Kafka C, Hernandez KA, Popa S, Perez JL, Zhou S, Pramanik S, Brown BN, Ryu WS, Bonassar LJ, Spector JA (2013) High-fidelity tissue engineering of patient-specific auricles for reconstruction of pediatric microtia and other auricular deformities. PLoS One 8(2):e56506CrossRefPubMedPubMedCentralGoogle Scholar
  107. 107.
    Mannoor MS, Jiang Z, James T, Kong YL, Malatesta KA, Soboyejo WO, Verma N, Gracias DH, McAlpine MC (2013) 3D printed bionic ears. Nano Lett 13:2634–2639CrossRefPubMedPubMedCentralGoogle Scholar
  108. 108.
    Lorber B, Hsiao WK, Hutchings IM, Martin KR (2014) Adult rat retinal ganglion cells and glia can be printed by piezoelectric inkjet printing. Biofabrication 6:015001CrossRefPubMedPubMedCentralGoogle Scholar
  109. 109.
    Hunt NC, Hallam D, Karimi A, Mellough CM, Chen J, Steel DM, La M (2016) 3D culture of human pluripotent stem cells in alginate hydrogel improves retinal tissue development. Acta Biomater 49:329–343.  https://doi.org/10.1017/CBO9781107415324.004CrossRefPubMedPubMedCentralGoogle Scholar
  110. 110.
    Wang P, Li X, Zhu W, Zhong Z, Moran A, Wang W, Zhang K, Chen S (2018) 3D bioprinting of hydrogels for retina cell culturing. Bioprinting 12:e00029CrossRefGoogle Scholar
  111. 111.
    Shi P, Tan YSE, Yeong WY, Li HY, Laude A (2018) A bilayer photoreceptor-retinal tissue model with gradient cell density design: a study of microvalve-based bioprinting. J Tissue Eng Regen Med 12:1297–1306CrossRefPubMedPubMedCentralGoogle Scholar
  112. 112.
    Mitrousis N, Tam RY, Baker AEG, Van Der Kooy D, Shoichet MS (2016) Hyaluronic acid-based hydrogels enable rod photoreceptor survival and maturation in vitro through activation of the mTOR pathway. Adv Funct Mater 26:1975–1985CrossRefGoogle Scholar
  113. 113.
    Zhao Y, Yao R, Ouyang L, Ding H, Zhang T, Zhang K, Cheng S, Sun W (2014) Three-dimensional printing of Hela cells for cervical tumor model in vitro. Biofabrication 6:035001CrossRefPubMedPubMedCentralGoogle Scholar
  114. 114.
    Zhou X, Zhu W, Nowicki M, Miao S, Cui H, Holmes B, Glazer RI, Zhang LG (2016) 3D bioprinting a cell-laden bone matrix for breast cancer metastasis study. ACS Appl Mater Interfaces 8:30017–30026CrossRefPubMedPubMedCentralGoogle Scholar
  115. 115.
    Massa S, Sakr MA, Seo J, Bandaru P, Arneri A, Bersini S, Zare-Eelanjegh E, Jalilian E, Cha BH, Antona S, Enrico A, Gao Y, Hassan S, Acevedo JP, Dokmeci MR, Zhang YS, Khademhosseini A, Shin SR (2017) Bioprinted 3D vascularized tissue model for drug toxicity analysis. Biomicrofluidics 11:044109CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Ippokratis Pountos
    • 1
    • 2
    Email author
  • Nazzar Tellisi
    • 1
    • 2
  • Nureddin Ashammakhi
    • 3
    • 4
    • 5
    • 6
  1. 1.Academic Department of Trauma and OrthopaedicsLeeds Teaching Hospitals, University of LeedsLeedsUK
  2. 2.Chapel Allerton HospitalLeeds Teaching HospitalsLeedsUK
  3. 3.Center for Minimally Invasive Therapeutics (C-MIT)University of California Los AngelesLos AngelesUSA
  4. 4.California NanoSystems Institute (CNSI)University of California Los AngelesLos AngelesUSA
  5. 5.Department of Radiological Sciences, David Geffen School of MedicineUniversity of California Los AngelesLos AngelesUSA
  6. 6.Biotechnology Research CenterLibyan Authority for Research, Science and TechnologyTripoliLibya

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