A review of 3D bio-printing for bone and skin tissue engineering: a commercial approach

  • Nima Beheshtizadeh
  • Nasrin LotfibakhshaieshEmail author
  • Zahra Pazhouhnia
  • Mahdieh Hoseinpour
  • Masoud Nafari


The ultimate prospect of tissue engineering is to create autologous tissue grafts for future replacement therapies through utilization of cells and biomaterials simultaneously. Bio-printing is a novel technique, a growing field that is leading to the global revolution in medical sciences that has gained significant attention. Bio-printing has the potential to be used in producing human engineered tissues like bone and skin which then ultimately can be used in the clinics. In this paper, the 3D bio-printing applications of the engineered human tissues that are available (skin and bone) are reviewed. It is evident that various tissue engineering techniques have been applied in the fabrication of skin tissue; therefore, it leads to introduce tissue substitutes such as complementary, split-thickness skin graft, allografts, acellular dermal substitutes and cellularized graft-like commercial products, i.e., Dermagraft and Apligraf. Also, some bone scaffolds based on hydroxyapatite and biphasic calcium phosphate are available in the market. The technology of bio-printing has got validated for bone and skin tissue fabrication, and it is hoped that other tissues could be produced by this technique.



A word of appreciation must be given to Aron Munggela Foma for his invaluable assistance and comments on the first phase of paper editing. Also, we are extremely grateful to Mariam Sharifi Sistani for her precision and insightful comments on the second draft edition.


This study was not funded by any institute.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. 1.
    Mason C, Dunnill P (2008) A brief definition of regenerative medicine. Regen Med 3(1):1–5. CrossRefGoogle Scholar
  2. 2.
    Abouna GM (2008) Organ shortage crisis: problems and possible solutions. Transpl Proc 40(1):34–38. CrossRefGoogle Scholar
  3. 3.
    Bajaj P, Schweller RM, Khademhosseini A, West JL, Bashir R (2014) 3D biofabrication strategies for tissue engineering and regenerative medicine. Annu Rev Biomed Eng 16:247–276. CrossRefGoogle Scholar
  4. 4.
    Mao AS, Mooney DJ (2015) Regenerative medicine: current therapies and future directions. Proc Natl Acad Sci USA 112(47):14452–14459. CrossRefGoogle Scholar
  5. 5.
    Orlando G, Booth C, Wang Z, Totonelli G, Ross CL, Moran E, Salvatori M, Maghsoudlou P, Turmaine M, Delario G, Al-Shraideh Y, Farooq U, Farney AC, Rogers J, Iskandar SS, Burns A, Marini FC, De Coppi P, Stratta RJ, Soker S (2013) Discarded human kidneys as a source of ECM scaffold for kidney regeneration technologies. Biomaterials 34(24):5915–5925. CrossRefGoogle Scholar
  6. 6.
    Peloso A, Petrosyan A, Da Sacco S, Booth C, Zambon JP, O’Brien T, Aardema C, Robertson J, De Filippo RE, Soker S, Stratta RJ, Perin L, Orlando G (2015) Renal extracellular matrix scaffolds from discarded kidneys maintain glomerular morphometry and vascular resilience and retains critical growth factors. Transplantation 99(9):1807–1816. CrossRefGoogle Scholar
  7. 7.
    Yu YL, Shao YK, Ding YQ, Lin KZ, Chen B, Zhang HZ, Zhao LN, Wang ZB, Zhang JS, Tang ML, Mei J (2014) Decellularized kidney scaffold-mediated renal regeneration. Biomaterials 35(25):6822–6828. CrossRefGoogle Scholar
  8. 8.
    Balestrini JL, Gard AL, Liu A, Leiby KL, Schwan J, Kunkemoeller B, Calle EA, Sivarapatna A, Lin T, Dimitrievska S, Cambpell SG, Niklason LE (2015) Production of decellularized porcine lung scaffolds for use in tissue engineering. Integr Biol 7(12):1598–1610. CrossRefGoogle Scholar
  9. 9.
    Gilpin SE, Guyette JP, Gonzalez G, Ren X, Asara JM, Mathisen DJ, Vacanti JP, Ott HC (2014) Perfusion decellularization of human and porcine lungs: bringing the matrix to clinical scale. J Heart Lung Transpl 33(3):298–308. CrossRefGoogle Scholar
  10. 10.
    Stabler CT, Lecht S, Mondrinos MJ, Goulart E, Lazarovici P, Lelkes PI (2015) Revascularization of decellularized lung scaffolds: principles and progress. Am J Physiol Lung Cell Mol Physiol 309(11):L1273–L1285. CrossRefGoogle Scholar
  11. 11.
    Kim TH, Jung Y, Kim SH (2018) Nanofibrous electrospun heart decellularized extracellular matrix-based hybrid scaffold as wound dressing for reducing scarring in wound healing. Tissue Eng Part A 24(9–10):830–848. CrossRefGoogle Scholar
  12. 12.
    Sánchez PL, Fernández-Santos ME, Costanza S, Climent AM, Moscoso I, Gonzalez-Nicolas MA, Sanz-Ruiz R, Rodríguez H, Kren SM, Garrido G, Escalante JL, Bermejo J, Elizaga J, Menarguez J, Yotti R, Pérez del Villar C, Espinosa MA, Guillem MS, Willerson JT, Bernad A, Matesanz R, Taylor DA, Fernández-Avilés F (2015) Acellular human heart matrix: a critical step toward whole heart grafts. Biomaterials 61:279–289. CrossRefGoogle Scholar
  13. 13.
    Seo Y, Jung Y, Kim SH (2018) Decellularized heart ECM hydrogel using supercritical carbon dioxide for improved angiogenesis. Acta Biomater 67:270–281. CrossRefGoogle Scholar
  14. 14.
    Lee H, Han W, Kim H, Ha DH, Jang J, Kim BS, Cho DW (2017) Development of liver decellularized extracellular matrix bioink for three-dimensional cell printing-based liver tissue engineering. Biomacromolecules 18(4):1229–1237. CrossRefGoogle Scholar
  15. 15.
    Mattei G, Magliaro C, Pirone A, Ahluwalia A (2017) Decellularized human liver is too heterogeneous for designing a generic extracellular matrix mimic hepatic scaffold. Artif Organs 41(12):E347–E355. CrossRefGoogle Scholar
  16. 16.
    Mazza G, Rombouts K, Rennie Hall A, Urbani L, Vinh Luong T, Al-Akkad W, Longato L, Brown D, Maghsoudlou P, Dhillon AP, Fuller B, Davidson B, Moore K, Dhar D, De Coppi P, Malago M, Pinzani M (2015) Decellularized human liver as a natural 3D-scaffold for liver bioengineering and transplantation. Sci Rep 5:13079. CrossRefGoogle Scholar
  17. 17.
    Garreta E, Oria R, Tarantino C, Pla-Roca M, Prado P, Fernández-Avilés F, Campistol JM, Samitier J, Montserrat N (2017) Tissue engineering by decellularization and 3D bioprinting. Mater Today 20(4):166–178. CrossRefGoogle Scholar
  18. 18.
    Moser PT, Ott HC (2014) Recellularization of organs: what is the future for solid organ transplantation? Curr Opin Organ Transpl 19(6):603–609. CrossRefGoogle Scholar
  19. 19.
    Cheung DYC, Duan B, Butcher JT (2015) Chapter 21—Bioprinting of cardiac tissues. In: Atala A, Yoo JJ (eds) Essentials of 3D biofabrication and translation. Academic Press, Boston, pp 351–370. CrossRefGoogle Scholar
  20. 20.
    Groll J, Boland T, Blunk T, Burdick JA, Cho D-W, Dalton PD, Derby B, Forgacs G, Li Q, Mironov VA, Moroni L, Nakamura M, Shu W, Takeuchi S, Vozzi G, Woodfield TBF, Xu T, Yoo JJ, Malda J (2016) Biofabrication: reappraising the definition of an evolving field. Biofabrication 8(1):013001. CrossRefGoogle Scholar
  21. 21.
    Mandrycky C, Wang Z, Kim K, Kim D-H (2016) 3D bioprinting for engineering complex tissues. Biotechnol Adv 34(4):422–434. CrossRefGoogle Scholar
  22. 22.
    Murphy SV, Atala A (2014) 3D bioprinting of tissues and organs. Nat Biotechnol 32(8):773–785. CrossRefGoogle Scholar
  23. 23.
    Ozbolat IT (2015) Bioprinting scale-up tissue and organ constructs for transplantation. Trends Biotechnol 33(7):395–400. CrossRefGoogle Scholar
  24. 24.
    Derakhshanfar S, Mbeleck R, Xu K, Zhang X, Zhong W, Xing M (2018) 3D bioprinting for biomedical devices and tissue engineering: a review of recent trends and advances. Bioact Mater 3(2):144–156. CrossRefGoogle Scholar
  25. 25.
    Jakab K, Norotte C, Marga F, Murphy K, Vunjak-Novakovic G, Forgacs G (2010) Tissue engineering by self-assembly and bio-printing of living cells. Biofabrication 2(2):022001. CrossRefGoogle Scholar
  26. 26.
    Moroni L, de Wijn JR, van Blitterswijk CA (2006) 3D fiber-deposited scaffolds for tissue engineering: influence of pores geometry and architecture on dynamic mechanical properties. Biomaterials 27(7):974–985. CrossRefGoogle Scholar
  27. 27.
    Zhu W, Ock J, Ma X, Li W, Chen S (2015) “Chapter 2—3D printing and nanomanufacturing. In: Zhang LG, Fisher JP, Leong KW (eds) 3D bioprinting and nanotechnology in tissue engineering and regenerative medicine. Academic Press, New York, pp 25–55. CrossRefGoogle Scholar
  28. 28.
    Shanjani Y, Pan CC, Elomaa L, Yang Y (2015) A novel bioprinting method and system for forming hybrid tissue engineering constructs. Biofabrication 7(4):045008. CrossRefGoogle Scholar
  29. 29.
    Lim G, Choi D, Richardson EB (2014) 3-D printing in organ transplantation. Hanyang Med Rev 34(4):158–164. CrossRefGoogle Scholar
  30. 30.
    Snyder JE, Hamid Q, Wang C, Chang R, Emami K, Wu H, Sun W (2011) Bioprinting cell-laden matrigel for radioprotection study of liver by pro-drug conversion in a dual-tissue microfluidic chip. Biofabrication 3(3):034112. CrossRefGoogle Scholar
  31. 31.
    Perkins JD (2007) Are we reporting the same thing? Liver Transpl: Off Publ Am Assoc Study Liver Dis Int Liver Transpl Soc 13(3):465–466CrossRefGoogle Scholar
  32. 32.
    Midha S, Dalela M, Sybil D, Patra P, Mohanty S (2019) Advances in three-dimensional bioprinting of bone: progress and challenges. J Tissue Eng Regen Med 13(6):925–945. CrossRefGoogle Scholar
  33. 33.
    Moreno Madrid AP, Vrech SM, Sanchez MA, Rodriguez AP (2019) Advances in additive manufacturing for bone tissue engineering scaffolds. Mater Sci Eng, C 100:631–644. CrossRefGoogle Scholar
  34. 34.
    Ashammakhi N, Hasan A, Kaarela O, Byambaa B, Sheikhi A, Gaharwar AK, Khademhosseini A (2019) Advancing frontiers in bone bioprinting. Adv Healthc Mater 8(7):1801048. CrossRefGoogle Scholar
  35. 35.
    Atala A, Forgacs G (2019) Three-dimensional bioprinting in regenerative medicine: reality, hype, and future. Stem Cells Transl Med 8(8):744–745. CrossRefGoogle Scholar
  36. 36.
    Dasgupta Q, Black LD (2019) A fresh slate for 3D bioprinting. Science 365(6452):446. CrossRefGoogle Scholar
  37. 37.
    Kuss M, Duan B (2019) Chapter 2—Extrusion-based bioprinting. In: Cho D-W (ed) Biofabrication and 3D tissue modeling. The Royal Society of Chemistry, London, pp 22–48. CrossRefGoogle Scholar
  38. 38.
    Matai I, Kaur G, Seyedsalehi A, McClinton A, Laurencin CT (2019) Progress in 3D bioprinting technology for tissue/organ regenerative engineering. Biomaterials 226:119536. CrossRefGoogle Scholar
  39. 39.
    Miri AK, Khalilpour A, Cecen B, Maharjan S, Shin SR, Khademhosseini A (2019) Multiscale bioprinting of vascularized models. Biomaterials 198:204–216. CrossRefGoogle Scholar
  40. 40.
    Moldovan F (2019) Recent trends in bioprinting. Procedia Manuf 32:95–101. CrossRefGoogle Scholar
  41. 41.
    Shafiee A, Ghadiri E, Ramesh H, Kengla C, Kassis J, Calvert P, Williams D, Khademhosseini A, Narayan R, Forgacs G, Atala A (2019) Physics of bioprinting. Appl Phys Rev 6(2):021315. CrossRefGoogle Scholar
  42. 42.
    Zhang B, Gao L, Ma L, Luo Y, Yang H, Cui Z (2019) 3D bioprinting: a novel avenue for manufacturing tissues and organs. Engineering 5(4):777–794. CrossRefGoogle Scholar
  43. 43.
    Zhou D, Chen J, Liu B, Zhang X, Li X, Xu T (2019) Bioinks for jet-based bioprinting. Bioprinting 16:e00060. CrossRefGoogle Scholar
  44. 44.
    Unagolla JM, Jayasuriya AC (2019) Hydrogel-based 3D bioprinting: a comprehensive review on cell-laden hydrogels, bioink formulations, and future perspectives. Appl Mater Today. CrossRefGoogle Scholar
  45. 45.
    Liu P, Shen H, Zhi Y, Si J, Shi J, Guo L, Shen SG (2019) 3D bioprinting and in vitro study of bilayered membranous construct with human cells-laden alginate/gelatin composite hydrogels. Colloids Surf, B 181:1026–1034. CrossRefGoogle Scholar
  46. 46.
    Cheng L, Yao B, Hu T, Cui X, Shu X, Tang S, Wang R, Wang Y, Liu Y, Song W, Fu X, Li H, Huang S (2019) Properties of an alginate-gelatin-based bioink and its potential impact on cell migration, proliferation, and differentiation. Int J Biol Macromol 135:1107–1113. CrossRefGoogle Scholar
  47. 47.
    Gonzalez-Fernandez T, Rathan S, Hobbs C, Pitacco P, Freeman FE, Cunniffe GM, Dunne NJ, McCarthy HO, Nicolosi V, O’Brien FJ, Kelly DJ (2019) Pore-forming bioinks to enable spatio-temporally defined gene delivery in bioprinted tissues. J Control Release 301:13–27. CrossRefGoogle Scholar
  48. 48.
    Kim W, Kim G (2019) A functional bioink and its application in myoblast alignment and differentiation. Chem Eng J 366:150–162. CrossRefGoogle Scholar
  49. 49.
    Oliveira EP, Malysz-Cymborska I, Golubczyk D, Kalkowski L, Kwiatkowska J, Reis RL, Oliveira JM, Walczak P (2019) Advances in bioinks and in vivo imaging of biomaterials for CNS applications. Acta Biomater 95:60–72. CrossRefGoogle Scholar
  50. 50.
    Kajave NS, Schmitt T, Nguyen T-U, Kishore V (2019) Dual crosslinking strategy to generate mechanically viable cell-laden printable constructs using methacrylated collagen bioinks. Materials Science and Engineering: C 107:110290. CrossRefGoogle Scholar
  51. 51.
    Zhu K, Shin SR, van Kempen T, Li Y-C, Ponraj V, Nasajpour A, Mandla S, Hu N, Liu X, Leijten J, Lin Y-D, Hussain MA, Zhang YS, Tamayol A, Khademhosseini A (2017) Gold nanocomposite bioink for printing 3D cardiac constructs. Adv Func Mater 27(12):1605352. CrossRefGoogle Scholar
  52. 52.
    Johnson BN, Lancaster KZ, Zhen G, He J, Gupta MK, Kong YL, Engel EA, Krick KD, Ju A, Meng F, Enquist LW, Jia X, McAlpine MC (2015) 3D printed anatomical nerve regeneration pathways. Adv Funct Mater 25(39):6205–6217. CrossRefGoogle Scholar
  53. 53.
    Homan KA, Kolesky DB, Skylar-Scott MA, Herrmann J, Obuobi H, Moisan A, Lewis JA (2016) Bioprinting of 3D convoluted renal proximal tubules on perfusable chips. Sci Rep 6:34845.
  54. 54.
    Kesti M, Eberhardt C, Pagliccia G, Kenkel D, Grande D, Boss A, Zenobi-Wong M (2015) Bioprinting complex cartilaginous structures with clinically compliant biomaterials. Adv Funct Mater 25(48):7406–7417. CrossRefGoogle Scholar
  55. 55.
    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(6):2634–2639. CrossRefGoogle Scholar
  56. 56.
    Khan Y, Pavinatto FJ, Lin MC, Liao A, Swisher SL, Mann K, Subramanian V, Maharbiz MM, Arias AC (2016) Inkjet-printed flexible gold electrode arrays for bioelectronic interfaces. Adv Funct Mater 26(7):1004–1013. CrossRefGoogle Scholar
  57. 57.
    Shin SR, Farzad R, Tamayol A, Manoharan V, Mostafalu P, Zhang YS, Akbari M, Jung SM, Kim D, Comotto M, Annabi N, Al-Hazmi FE, Dokmeci MR, Khademhosseini A (2016) A bioactive carbon nanotube-based ink for printing 2D and 3D flexible electronics. Adv Mater 28(17):3280–3289. CrossRefGoogle Scholar
  58. 58.
    Coruh A, Yontar Y (2012) Application of split-thickness dermal grafts in deep partial- and full-thickness burns: a new source of auto-skin grafting. J Burn Care Res: Off Publ Am Burn Assoc 33(3):e94–e100. CrossRefGoogle Scholar
  59. 59.
    Leon-Villapalos J, Eldardiri M, Dziewulski P (2010) The use of human deceased donor skin allograft in burn care. Cell Tissue Bank 11(1):99–104. CrossRefGoogle Scholar
  60. 60.
    Metcalfe AD, Ferguson MWJ (2007) Tissue engineering of replacement skin: the crossroads of biomaterials, wound healing, embryonic development, stem cells and regeneration. J R Soc Interface 4(14):413–437. CrossRefGoogle Scholar
  61. 61.
    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. CrossRefGoogle Scholar
  62. 62.
    Cubo N, Garcia M, del Cañizo JF, Velasco D, Jorcano JL (2016) 3D bioprinting of functional human skin: production andin vivoanalysis. Biofabrication 9(1):015006. CrossRefGoogle Scholar
  63. 63.
    Zhao X, Lang Q, Yildirimer L, Lin ZY, Cui W, Annabi N, Ng KW, Dokmeci MR, Ghaemmaghami AM, Khademhosseini A (2016) photocrosslinkable gelatin hydrogel for epidermal tissue engineering. Adv Healthc Mater 5(1):108–118. CrossRefGoogle Scholar
  64. 64.
    Lee V, Singh G, Trasatti JP, Bjornsson C, Xu X, Tran TN, Yoo S-S, Dai G, Karande P (2014) Design and fabrication of human skin by three-dimensional bioprinting. Tissue Eng Part C, Methods 20(6):473–484. CrossRefGoogle Scholar
  65. 65.
    Xiong S, Zhang X, Lu P, Wu Y, Wang Q, Sun H, Heng BC, Bunpetch V, Zhang S, Ouyang H (2017) A gelatin-sulfonated silk composite scaffold based on 3D printing technology enhances skin regeneration by stimulating epidermal growth and dermal neovascularization. Sci Rep 7(1):4288. CrossRefGoogle Scholar
  66. 66.
    Rutz AL, Hyland KE, Jakus AE, Burghardt WR, Shah RN (2015) A multimaterial bioink method for 3D printing tunable, cell-compatible hydrogels. Adv Mater 27(9):1607–1614. CrossRefGoogle Scholar
  67. 67.
    Ng WL, Yeong WY, Naing MW (2016) Polyelectrolyte gelatin-chitosan hydrogel optimized for 3D bioprinting in skin tissue engineering. Int J Biopr 2(1):10. CrossRefGoogle Scholar
  68. 68.
    Min D, Lee W, Bae IH, Lee TR, Croce P, Yoo SS (2018) Bioprinting of biomimetic skin containing melanocytes. Exp Dermatol 27(5):453–459. CrossRefGoogle Scholar
  69. 69.
    Li J, Chi J, Liu J, Gao C, Wang K, Shan T, Li Y, Shang W, Gu F (2017) 3D printed gelatin-alginate bioactive scaffolds combined with mice bone marrow mesenchymal stem cells: a biocompatibility study. Int J Clin Exp Pathol 10(6):6299–6307Google Scholar
  70. 70.
    Huang S, Yao B, Xie J, Fu X (2016) 3D bioprinted extracellular matrix mimics facilitate directed differentiation of epithelial progenitors for sweat gland regeneration. Acta Biomater 32:170–177. CrossRefGoogle Scholar
  71. 71.
    Ng WL, Yeong WY, Win Naing M (2014) Potential of bioprinted films for skin tissue engineering. In: Paper presented at the 1st international conference on progress in additive manufacturingGoogle Scholar
  72. 72.
    Rimann M, Bono E, Annaheim H, Bleisch M, Graf-Hausner U (2016) Standardized 3D bioprinting of soft tissue models with human primary cells. J Lab Autom 21(4):496–509. CrossRefGoogle Scholar
  73. 73.
    Skardal A, Mack D, Kapetanovic E, Atala A, Jackson JD, Yoo J, Soker S (2012) Bioprinted amniotic fluid-derived stem cells accelerate healing of large skin wounds. Stem cells Transl Med 1(11):792–802. CrossRefGoogle Scholar
  74. 74.
    Kim BS, Lee J-S, Gao G, Cho D-W (2017) Direct 3D cell-printing of human skin with functional transwell system. Biofabrication 9(2):025034. CrossRefGoogle Scholar
  75. 75.
    Michael S, Sorg H, Peck C-T, 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(3):e57741CrossRefGoogle Scholar
  76. 76.
    Binder KW (2011) In situ bioprinting of the skin. Wake Forest University, Winston-SalemGoogle Scholar
  77. 77.
    Thayer PS, Orrhult LS, Martínez H (2018) Bioprinting of cartilage and skin tissue analogs utilizing a novel passive mixing unit technique for bioink precellularization. J Vis Exp JoVE 3(131):56372. CrossRefGoogle Scholar
  78. 78.
    Albanna M, Binder KW, Murphy SV, Kim J, Qasem SA, Zhao W, Tan J, El-Amin IB, Dice DD, Marco J, Green J, Xu T, Skardal A, Holmes JH, Jackson JD, Atala A, Yoo JJ (2019) In situ bioprinting of autologous skin cells accelerates wound healing of extensive excisional full-thickness wounds. Sci Rep 9(1):1856. CrossRefGoogle Scholar
  79. 79.
    Admane P, Gupta AC, Jois P, Roy S, Chandrasekharan Lakshmanan C, Kalsi G, Bandyopadhyay B, Ghosh S (2019) Direct 3D bioprinted full-thickness skin constructs recapitulate regulatory signaling pathways and physiology of human skin. Bioprinting 15:e00051. CrossRefGoogle Scholar
  80. 80.
    Mao JS, Zhao LG, Yin YJ, Yao KD (2003) Structure and properties of bilayer chitosan-gelatin scaffolds. Biomaterials 24(6):1067–1074CrossRefGoogle Scholar
  81. 81.
    Leukers B, Gülkan H, Irsen SH, Milz S, Tille C, Schieker M, Seitz H (2005) Hydroxyapatite scaffolds for bone tissue engineering made by 3D printing. J Mater Sci Mater Med 16(12):1121–1124. CrossRefGoogle Scholar
  82. 82.
    Cox SC, Thornby JA, Gibbons GJ, Williams MA, Mallick KK (2015) 3D printing of porous hydroxyapatite scaffolds intended for use in bone tissue engineering applications. Mater Sci Eng, C 47:237–247. CrossRefGoogle Scholar
  83. 83.
    Brunello G, Sivolella S, Meneghello R, Ferroni L, Gardin C, Piattelli A, Zavan B, Bressan E (2016) Powder-based 3D printing for bone tissue engineering. Biotechnol Adv 34(5):740–753. CrossRefGoogle Scholar
  84. 84.
    Murphy C, Kolan K, Li W, Semon J, Day D, Leu M (2017) 3D bioprinting of stem cells and polymer/bioactive glass composite scaffolds for bone tissue engineering. Int J Biopr 3(1):11. CrossRefGoogle Scholar
  85. 85.
    Byambaa B, Annabi N, Yue K, Trujillo-de Santiago G, Alvarez MM, Jia W, Kazemzadeh-Narbat M, Shin SR, Tamayol A, Khademhosseini A (2017) Bioprinted osteogenic and vasculogenic patterns for engineering 3D bone tissue. Adv Healthc Mater. CrossRefGoogle Scholar
  86. 86.
    Kim MS, Kim G (2014) Three-dimensional electrospun polycaprolactone (PCL)/alginate hybrid composite scaffolds. Carbohydr Polym 114:213–221. CrossRefGoogle Scholar
  87. 87.
    Holmes B, Bulusu K, Plesniak M, Zhang LG (2016) A synergistic approach to the design, fabrication and evaluation of 3D printed micro and nano featured scaffolds for vascularized bone tissue repair. Nanotechnology 27(6):064001. CrossRefGoogle Scholar
  88. 88.
    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(10):1304–1311. CrossRefGoogle Scholar
  89. 89.
    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(3):312–319. CrossRefGoogle Scholar
  90. 90.
    Wang J, Yang M, Zhu Y, Wang L, Tomsia AP, Mao C (2014) Phage nanofibers induce vascularized osteogenesis in 3D printed bone scaffolds. Adv Mater 26(29):4961–4966. CrossRefGoogle Scholar
  91. 91.
    Costantini M, Idaszek J, Szoke K, Jaroszewicz J, Dentini M, Barbetta A, Brinchmann JE, Swieszkowski W (2016) 3D bioprinting of BM-MSCs-loaded ECM biomimetic hydrogels for in vitro neocartilage formation. Biofabrication 8(3):035002. CrossRefGoogle Scholar
  92. 92.
    Kim HH, Park JB, Kang MJ, Park YH (2014) Surface-modified silk hydrogel containing hydroxyapatite nanoparticle with hyaluronic acid-dopamine conjugate. Int J Biol Macromol 70:516–522. CrossRefGoogle Scholar
  93. 93.
    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(5):1457–1468. CrossRefGoogle Scholar
  94. 94.
    Nyberg E, Rindone A, Dorafshar A, Grayson WL (2017) Comparison of 3D-printed poly-varepsilon-caprolactone scaffolds functionalized with tricalcium phosphate, hydroxyapatite, bio-oss, or decellularized bone matrix. Tissue Eng Part A 23(11–12):503–514. CrossRefGoogle Scholar
  95. 95.
    Buyuksungur S, Endogan Tanir T, Buyuksungur A, Bektas EI, Torun Kose G, Yucel D, Beyzadeoglu T, Cetinkaya E, Yenigun C, Tonuk E, Hasirci V, Hasirci N (2017) 3D printed poly(epsilon-caprolactone) scaffolds modified with hydroxyapatite and poly(propylene fumarate) and their effects on the healing of rabbit femur defects. Biomater Sci 5(10):2144–2158. CrossRefGoogle Scholar
  96. 96.
    Bose S, Vahabzadeh S, Bandyopadhyay A (2013) Bone tissue engineering using 3D printing. Mater Today 16(12):496–504. CrossRefGoogle Scholar
  97. 97.
    Daly AC, Pitacco P, Nulty J, Cunniffe GM, Kelly DJ (2018) 3D printed microchannel networks to direct vascularisation during endochondral bone repair. Biomaterials 162:34–46. CrossRefGoogle Scholar
  98. 98.
    Fedorovich NE, Schuurman W, Wijnberg HM, Prins HJ, van Weeren PR, Malda J, Alblas J, Dhert WJ (2012) Biofabrication of osteochondral tissue equivalents by printing topologically defined, cell-laden hydrogel scaffolds. Tissue Eng Part C, Methods 18(1):33–44. CrossRefGoogle Scholar
  99. 99.
    Huang B, Bártolo PJ (2018) Rheological characterization of polymer/ceramic blends for 3D printing of bone scaffolds. Polym Test 68:365–378. CrossRefGoogle Scholar
  100. 100.
    Hung BP, Naved BA, Nyberg EL, Dias M, Holmes CA, Elisseeff JH, Dorafshar AH, Grayson WL (2016) Three-dimensional printing of bone extracellular matrix for craniofacial regeneration. ACS Biomater Sci Eng 2(10):1806–1816. CrossRefGoogle Scholar
  101. 101.
    Kebede MA, Asiku KS, Imae T, Kawakami M, Furukawa H, Wu CM (2018) Stereolithographic and molding fabrications of hydroxyapatite-polymer gels applicable to bone regeneration materials. J Taiwan Inst Chem Eng 92:91–96. CrossRefGoogle Scholar
  102. 102.
    Khanarian NT, Jiang J, Wan LQ, Mow VC, Lu HH (2012) A hydrogel-mineral composite scaffold for osteochondral interface tissue engineering. Tissue Eng Part A 18(5–6):533–545. CrossRefGoogle Scholar
  103. 103.
    Kim YC, Min KH, Choi JW, Koh KS, Oh TS, Jeong WS (2018) Patient-specific puzzle implant preformed with 3D-printed rapid prototype model for combined orbital floor and medial wall fracture. J Plast Reconstr Aesthet Surg: JPRAS 71(4):496–503. CrossRefGoogle Scholar
  104. 104.
    Lee H, Yang GH, Kim M, Lee J, Huh J, Kim G (2018) Fabrication of micro/nanoporous collagen/dECM/silk-fibroin biocomposite scaffolds using a low temperature 3D printing process for bone tissue regeneration. Mater Sci Eng, C 84:140–147. CrossRefGoogle Scholar
  105. 105.
    Luo Y, Lode A, Wu C, Chang J, Gelinsky M (2015) Alginate/nanohydroxyapatite scaffolds with designed core/shell structures fabricated by 3D plotting and in situ mineralization for bone tissue engineering. ACS Appl Mater Interfaces 7(12):6541–6549. CrossRefGoogle Scholar
  106. 106.
    Müller M, Becher J, Schnabelrauch M, Zenobi-Wong M (2013) Printing thermoresponsive reverse molds for the creation of patterned two-component hydrogels for 3D cell culture. JoVE 77:e50632. CrossRefGoogle Scholar
  107. 107.
    Ni J, Li D, Mao M, Dang X, Wang K, He J, Shi Z (2018) A method of accurate bone tunnel placement for anterior cruciate ligament reconstruction based on 3-dimensional printing technology: a cadaveric study. Arthroscopy 34(2):546–556. CrossRefGoogle Scholar
  108. 108.
    Park J, Lee SJ, Lee H, Park SA, Lee JY (2018) Three dimensional cell printing with sulfated alginate for improved bone morphogenetic protein-2 delivery and osteogenesis in bone tissue engineering. Carbohydr Polym 196:217–224. CrossRefGoogle Scholar
  109. 109.
    Spalazzi JP, Dagher E, Doty SB, Guo XE, Rodeo SA, Lu HH (2008) In vivo evaluation of a multiphased scaffold designed for orthopaedic interface tissue engineering and soft tissue-to-bone integration. J Biomed Mater Res, Part A 86(1):1–12. CrossRefGoogle Scholar
  110. 110.
    Tayebi L, Rasoulianboroujeni M, Moharamzadeh K, Almela TKD, Cui Z, Ye H (2018) 3D-printed membrane for guided tissue regeneration. Mater Sci Eng, C 84:148–158. CrossRefGoogle Scholar
  111. 111.
    Trauner KB (2018) The emerging role of 3D printing in arthroplasty and orthopedics. J Arthroplasty 33(8):2352–2354. CrossRefGoogle Scholar
  112. 112.
    Zhang B, Pei X, Zhou C, Fan Y, Jiang Q, Ronca A, D’Amora U, Chen Y, Li H, Sun Y, Zhang X (2018) The biomimetic design and 3D printing of customized mechanical properties porous Ti6Al4 V scaffold for load-bearing bone reconstruction. Mater Des 152:30–39. CrossRefGoogle Scholar
  113. 113.
    Hernández-González AC, Téllez-Jurado L, Rodríguez-Lorenzo LM (2019) Alginate hydrogels for bone tissue engineering, from injectables to bioprinting: a review. Carbohydr Polym. CrossRefGoogle Scholar
  114. 114.
    Oladapo BI, Zahedi SA, Adeoye AOM (2019) 3D printing of bone scaffolds with hybrid biomaterials. Compos B Eng 158:428–436. CrossRefGoogle Scholar
  115. 115.
    Zhao L, Pei X, Jiang L, Hu C, Sun J, Xing F, Zhou C, Fan Y, Zhang X (2019) Bionic design and 3D printing of porous titanium alloy scaffolds for bone tissue repair. Compos B Eng 162:154–161. CrossRefGoogle Scholar
  116. 116.
    Lai Y, Li Y, Cao H, Long J, Wang X, Li L, Li C, Jia Q, Teng B, Tang T, Peng J, Eglin D, Alini M, Grijpma DW, Richards G, Qin L (2019) Osteogenic magnesium incorporated into PLGA/TCP porous scaffold by 3D printing for repairing challenging bone defect. Biomaterials 197:207–219. CrossRefGoogle Scholar
  117. 117.
    Roopavath UK, Malferrari S, Van Haver A, Verstreken F, Rath SN, Kalaskar DM (2019) Optimization of extrusion based ceramic 3D printing process for complex bony designs. Mater Des 162:263–270. CrossRefGoogle Scholar
  118. 118.
    Rupnick MA, Panigrahy D, Zhang C-Y, Dallabrida SM, Lowell BB, Langer R, Folkman MJ (2002) Adipose tissue mass can be regulated through the vasculature. Proc Natl Acad Sci USA 99(16):10730–10735. CrossRefGoogle Scholar
  119. 119.
    Kaully T, Kaufman-Francis K, Lesman A, Levenberg S (2009) Vascularization–the conduit to viable engineered tissues. Tissue Eng Part B, Rev 15(2):159–169. CrossRefGoogle Scholar
  120. 120.
    Hutmacher DW, Schantz T, Zein I, Ng KW, Teoh SH, Tan KC (2001) Mechanical properties and cell cultural response of polycaprolactone scaffolds designed and fabricated via fused deposition modeling. J Biomed Mater Res 55(2):203–216CrossRefGoogle Scholar
  121. 121.
    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(11–12):1304–1312. CrossRefGoogle Scholar
  122. 122.
    Dolati F, Yu Y, Zhang Y, De Jesus AM, Sander EA, Ozbolat IT (2014) In vitro evaluation of carbon-nanotube-reinforced bioprintable vascular conduits. Nanotechnology 25(14):145101. CrossRefGoogle Scholar
  123. 123.
    Duan B, Hockaday LA, Kang KH, Butcher JT (2013) 3D bioprinting of heterogeneous aortic valve conduits with alginate/gelatin hydrogels. J Biomed Mater Res, Part A 101(5):1255–1264. CrossRefGoogle Scholar
  124. 124.
    Keriquel V, Guillemot F, Arnault I, Guillotin B, Miraux S, Amedee J, Fricain JC, Catros S (2010) In vivo bioprinting for computer- and robotic-assisted medical intervention: preliminary study in mice. Biofabrication 2(1):014101. CrossRefGoogle Scholar
  125. 125.
    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(1):015001. CrossRefGoogle Scholar
  126. 126.
    Zhang T, Yan KC, Ouyang L, Sun W (2013) Mechanical characterization of bioprinted in vitro soft tissue models. Biofabrication 5(4):045010. CrossRefGoogle Scholar
  127. 127.
    Duarte Campos DF, Blaeser A, Weber M, Jakel J, Neuss S, Jahnen-Dechent W, Fischer H (2013) Three-dimensional printing of stem cell-laden hydrogels submerged in a hydrophobic high-density fluid. Biofabrication 5(1):015003. CrossRefGoogle Scholar
  128. 128.
    Gruene M, Pflaum M, Deiwick A, Koch L, Schlie S, Unger C, Wilhelmi M, Haverich A, Chichkov BN (2011) Adipogenic differentiation of laser-printed 3D tissue grafts consisting of human adipose-derived stem cells. Biofabrication 3(1):015005. CrossRefGoogle Scholar
  129. 129.
    Hong S, Song SJ, Lee JY, Jang H, Choi J, Sun K, Park Y (2013) Cellular behavior in micropatterned hydrogels by bioprinting system depended on the cell types and cellular interaction. J Biosci Bioeng 116(2):224–230. CrossRefGoogle Scholar
  130. 130.
    Owens CM, Marga F, Forgacs G, Heesch CM (2013) Biofabrication and testing of a fully cellular nerve graft. Biofabrication 5(4):045007. CrossRefGoogle Scholar
  131. 131.
    Visser J, Peters B, Burger TJ, Boomstra J, Dhert WJ, Melchels FP, Malda J (2013) Biofabrication of multi-material anatomically shaped tissue constructs. Biofabrication 5(3):035007. CrossRefGoogle Scholar
  132. 132.
    Xu F, Sridharan B, Wang S, Gurkan UA, Syverud B, Demirci U (2011) Embryonic stem cell bioprinting for uniform and controlled size embryoid body formation. Biomicrofluidics 5(2):22207. CrossRefGoogle Scholar
  133. 133.
    Kannan S (2014) The 3D bio printing revolution. Harv Sci Rev.
  134. 134.
    Arslan-Yildiz A, El Assal R, Chen P, Guven S, Inci F, Demirci U (2016) Towards artificial tissue models: past, present, and future of 3D bioprinting. Biofabrication 8(1):014103. CrossRefGoogle Scholar
  135. 135.
    Vaidya M (2015) Startups tout commercially 3D-printed tissue for drug screening. Nat Med 21(1):2. CrossRefGoogle Scholar
  136. 136.
    Wang CC, Yang KC, Lin KH, Liu HC, Lin FH (2011) A highly organized three-dimensional alginate scaffold for cartilage tissue engineering prepared by microfluidic technology. Biomaterials 32(29):7118–7126. CrossRefGoogle Scholar
  137. 137.
    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):045004. CrossRefGoogle Scholar
  138. 138.
    Singh S, Choudhury D, Yu F, Mironov V, Naing MW (2019) In situ bioprinting–bioprinting from benchside to bedside? Acta Biomater. CrossRefGoogle Scholar
  139. 139.
    Murr LE (2015) Bioprinting and biofabrication of organs. In: Handbook of materials structures, properties, processing and performance. Springer, Cham, pp 629–638. Google Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Department of Tissue Engineering and Applied Cell Sciences, School of Advanced Technologies in MedicineTehran University of Medical SciencesTehranIran
  2. 2.Department of Stem Cells and Developmental Biology, Cell Science Research CenterRoyan Institute for Stem Cell Biology and Technology, ACECRTehranIran

Personalised recommendations