Skip to main content
Log in

Three-Dimensional Printing of Tissue/Organ Analogues Containing Living Cells

  • Additive Manufacturing of Biomaterials, Tissues, and Organs
  • Published:
Annals of Biomedical Engineering Aims and scope Submit manuscript

Abstract

The technical advances of three-dimensional (3D) printing in the field of tissue engineering have enabled the creation of 3D living tissue/organ analogues. Diverse 3D tissue/organ printing techniques with computer-aided systems have been developed and used to dispose living cells together with biomaterials and supporting biochemicals as pre-designed 3D tissue/organ models. Furthermore, recent advances in bio-inks, which are printable hydrogels with living cell encapsulation, have greatly enhanced the versatility of 3D tissue/organ printing. Here, we introduce 3D tissue/organ printing techniques and biomaterials that have been developed and widely used thus far. We also review a variety of applications in an attempt to repair or replace the damaged or defective tissue/organ, and develop the in vitro tissue/organ models. The potential challenges are finally discussed from the technical perspective of 3D tissue/organ printing.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5

Similar content being viewed by others

References

  1. Arcaute, K., B. K. Mann, and R. B. Wicker. Stereolithography of three-dimensional bioactive poly(ethylene glycol) constructs with encapsulated cells. Ann. Biomed. Eng. 34:1429–1441, 2006.

    Article  PubMed  Google Scholar 

  2. Barry, R. A., R. F. Shepherd, J. N. Hanson, R. G. Nuzzo, P. Wiltzius, and J. A. Lewis. Direct-write assembly of 3D hydrogel scaffolds for guided cell growth. Adv. Mater. 21:2407–2410, 2009.

    Article  CAS  Google Scholar 

  3. Benam, K. H., S. Dauth, B. Hassell, A. Herland, A. Jain, K.-J. Jang, K. Karalis, H. J. Kim, L. MacQueen, and R. Mahmoodian. Engineered in vitro disease models. Annu. Rev. Pathol. Mech. Dis. 10:195–262, 2015.

    Article  CAS  Google Scholar 

  4. Billiet, T., M. Vandenhaute, J. Schelfhout, S. V. Vlierberghe, and P. Dubruel. A review of trends and limitations in hydrogel-rapid prototyping for tissue engineering. Biomaterials 33:6020–6041, 2012.

    Article  CAS  PubMed  Google Scholar 

  5. Boland, T., X. Xu, B. Damon, and X. Cui. Application of inkjet printing to tissue engineering. Biotechnol. J. 1:910–917, 2006.

    Article  CAS  PubMed  Google Scholar 

  6. Breitenkamp, M. G., M. Finn, and D. D. Lotz. D’Lima. Direct human cartilage repair using three-dimensional bioprinting technology. Tissue Eng. Part A 18:1304–1312, 2012.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Chang, C. C., E. D. Boland, S. K. Williams, and J. B. Hoying. Direct-write bioprinting three-dimensional biohybrid systems for future regenerative therapies. J. Biomed. Mater. Res. B. Appl. Biomater. 98:160–170, 2011.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Chang, R., J. Nam, and W. Sun. Effects of dispensing pressure and nozzle diameter on cell survival from solid freeform fabrication-based direct cell writing. Tissue Eng. A. 14:41–48, 2008.

    Article  CAS  Google Scholar 

  9. De Gans, B. J., and U. S. Schubert. Inkjet printing of well-defined polymer dots and arrays. Langmuir 20:7789–7793, 2004.

    Article  PubMed  Google Scholar 

  10. Derby, B. Printing and prototyping of tissues and scaffolds. Science 338:921–926, 2012.

    Article  CAS  PubMed  Google Scholar 

  11. Dhariwala, B., E. Hunt, and T. Boland. Rapid prototyping of tissue-engineering constructs, using photopolymerizable hydrogels and stereolithography. Tissue Eng. 10:1316–1322, 2004.

    Article  CAS  PubMed  Google Scholar 

  12. Do, A. V., B. Khorsand, S. N. Geary, and A. K. Salem. 3D printing of scaffolds for tissue regeneration applications. Adv. Healthc. Mater. 4(12):1742–1762, 2015.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Duan, B., L. A. Hockaday, K. H. Kang, and J. T. Butcher. 3D bioprinting of heterogeneous aortic valve conduits with alginate/gelatin hydrogels. J. Biomed. Mater. Res. A. 101:1255–1264, 2013.

    Article  PubMed  Google Scholar 

  14. Fedorovich, N. E., J. Alblas, J. R. de Wijn, W. E. Hennink, A. J. Verbout, and W. J. Dhert. Hydrogels as extracellular matrices for skeletal tissue engineering: state-of-the-art and novel application in organ printing. Tissue Eng. 13:1905–1925, 2007.

    Article  CAS  PubMed  Google Scholar 

  15. Fedorovich, N. E., W. Schuurman, H. M. Wijnberg, H. J. Prins, P. R. Weeren, J. Malda, J. Alblas, and W. J. Dhert. Biofabrication of osteochondral tissue equivalents by printing topologically defined, cell-laden hydrogel scaffolds. Tissue Eng. C. 18:33–44, 2011.

    Article  Google Scholar 

  16. Fujisato, T., T. Sajiki, Q. Liu, and Y. Ikada. Effect of basic fibroblast growth factor on cartilage regeneration in chondrocyte-seeded collagen sponge scaffold. Biomaterials. 17:155–162, 1996.

    Article  CAS  PubMed  Google Scholar 

  17. Gaetani, R., P. A. Doevendans, C. H. Metz, J. Alblas, E. Messina, A. Giacomello, and J. P. Sluijter. Cardiac tissue engineering using tissue printing technology and human cardiac progenitor cells. Biomaterials. 33:1782–1790, 2012.

    Article  CAS  PubMed  Google Scholar 

  18. Gaetani, R., D. A. Feyen, V. Verhage, R. Slaats, E. Messina, K. L. Christman, A. Giacomello, P. A. Doevendans, and J. P. Sluijter. Epicardial application of cardiac progenitor cells in a 3D-printed gelatin/hyaluronic acid patch preserves cardiac function after myocardial infarction. Biomaterials. 61:339–348, 2015.

    Article  CAS  PubMed  Google Scholar 

  19. Gerecht, S., J. A. Burdick, L. S. Ferreira, S. A. Townsend, R. Langer, and G. Vunjak-Novakovic. Hyaluronic acid hydrogel for controlled self-renewal and differentiation of human embryonic stem cells. Proc. Natl. Acad. Sci. USA 104:11298–11303, 2007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Guillotin, B., and F. Guillemot. Cell patterning technologies for organotypic tissue fabrication. Trends Biotechnol. 29:183–190, 2011.

    Article  CAS  PubMed  Google Scholar 

  21. Guillotin, B., A. Souquet, S. Catros, M. Duocastella, B. Pippenger, S. Bellance, R. Bareille, M. Rémy, L. Bordenave, J. Amédée, and F. Guillemot. Laser assisted bioprinting of engineered tissue with high cell density and microscale organization. Biomaterials 21:7250–7256, 2010.

    Article  Google Scholar 

  22. Hashimdeen, S. H., M. Miodownik, and M. J. Edirisinghe. The Design and construction of an electrohydrodynamic cartesian robot for the preparation of tissue engineering constructs. PLOS One 9:e1121166, 2014.

    Article  Google Scholar 

  23. Hockaday, L., K. Kang, N. Colangelo, P. Cheung, B. Duan, E. Malone, J. Wu, L. Girardi, L. Bonassar, and H. Lipson. Rapid 3D printing of anatomically accurate and mechanically heterogeneous aortic valve hydrogel scaffolds. Biofabrication 4:035005, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Hutmacher, D. W., M. Sittinger, and M. V. Risbud. Scaffold-based tissue engineering: rationale for computer-aided design and solid free-form fabrication systems. Trends Biotechnol. 22:354–362, 2004.

    Article  CAS  PubMed  Google Scholar 

  25. Jang, J., T. G. Kim, B. S. Kim, S.-W. Kim, S.-M. Kwon, and D. W. Cho. Tailoring mechanical properties of decellularized extracellular matrix bioink by vitamin B2-induced photo-crosslinking. Acta Biomater. 33:88–95, 2016.

    Article  CAS  PubMed  Google Scholar 

  26. Jung, J. W., H. Lee, J. M. Hong, J. H. Park, J. H. Shim, T. H. Choi, and D.-W. Cho. A new method of fabricating a blend scaffold using an indirect three-dimensional printing technique. Biofabrication 7:045003, 2015.

    Article  PubMed  Google Scholar 

  27. Jung, J. W., J. H. Park, J. M. Hong, H. Y. Kang, and D. W. Cho. Octahedron pore architecture to enhance flexibility of nasal implant-shaped scaffold for rhinoplasty. Int. J. Precis. Eng. Manuf. 15:2611–2616, 2014.

    Article  Google Scholar 

  28. Kang, H. Y., and D. W. Cho. Development of an indirect stereolithography technology for scaffold fabrication with a wide range of biomaterial selectivity. Tissue Eng. 18:719–729, 2012.

    Article  CAS  Google Scholar 

  29. Kang, H. Y., J. H. Park, T. Y. Kang, Y. J. Seol, and D. W. Cho. Unit cell-based computer-aided manufacturing system for tissue engineering. Biofabrication 4:015005, 2012.

    Article  PubMed  Google Scholar 

  30. Khalil, S., J. Nam, and W. Sun. Multi-nozzle deposition for construction of 3D biopolymer tissue scaffolds. Rapid Prototyp. J. 11:9–17, 2005.

    Article  Google Scholar 

  31. Kim, S., and B.-S. Kim. Control of adult stem cell behavior with biomaterials. Tissue Eng. Regen. Med. 11:423–430, 2014.

    Article  CAS  Google Scholar 

  32. Kim, D. H., J. T. Martin, D. M. Elliott, L. J. Smith, and R. L. Mauck. Phenotypic stability, matrix elaboration and functional maturation of nucleus pulposus cells encapsulated in photocrosslinkable hyaluronic acid hydrogels. Acta Biomater. 12:21–29, 2015.

    Article  CAS  PubMed  Google Scholar 

  33. Kim, J. Y., E. K. Park, S. Y. Kim, J. W. Shin, and D. W. Cho. Fabrication of a SFF-based three-dimensional scaffold using a precision deposition system in tissue engineering. J. Micromech. Microeng. 18:055027, 2008.

    Article  Google Scholar 

  34. King, S. M., S. C. Presnell, and D. G. Nguyen. Development of 3D bioprinted human breast cancer for in vitro drug screening. Cancer Res. 74:2034, 2014.

    Article  Google Scholar 

  35. Knowlton, S., S. Onal, C. H. Yu, J. J. Zhao, and S. Tasoglu. Bioprinting for cancer research. Trends Biotechnol. 33:504–513, 2015.

    Article  CAS  PubMed  Google Scholar 

  36. Kolesky, D. B., R. L. Truby, A. Gladman, T. A. Busbee, K. A. Homan, and J. A. Lewis. 3D bioprinting of vascularized, heterogeneous cell-laden tissue constructs. Adv. Mater. 26:3124–3130, 2014.

    Article  CAS  PubMed  Google Scholar 

  37. Kundu, J., J. H. Shim, J. Jang, S. W. Kim, and D. W. Cho. An additive manufacturing-based PCL–alginate–chondrocyte bioprinted scaffold for cartilage tissue engineering. J. Tissue Eng. Regen. Med. 9:1286–1297, 2013.

    Article  PubMed  Google Scholar 

  38. Labbaf, S., H. Ghanbar, E. Stride, and M. Edirisinghe. Preparation of multilayered polymeric structures using a novel four-needle coaxial electrohydrodynamic device. Macromol. Rapid Commun. 35:618–623, 2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Lee, J. W. 3D nanoprinting technologies for tissue engineering applications. J. Nanomater. 2015:213521, 2015.

    Google Scholar 

  40. Lee, J. S., H. D. Cha, J. H. Shim, J. W. Jung, J. Y. Kim, and D. W. Cho. Effect of pore architecture and stacking direction on mechanical properties of solid freeform fabrication based scaffold for bone tissue engineering. J. Biomed. Mater. Res. A 100A:1846–1853, 2012.

    Article  CAS  Google Scholar 

  41. Lee, I. H., and D. W. Cho. An investigation on photopolymer solidification considering laser irradiation energy in micro-stereolithography. Microsyst. Technol. 10:592–598, 2004.

    Article  Google Scholar 

  42. Lee, W., J. C. Debasitis, V. K. Lee, J. H. Lee, K. Fischer, K. Edminster, J. K. Park, and S. S. Yoo. Multi-layered culture of human skin fibroblasts and keratinocytes through three-dimensional freeform fabrication. Biomaterials 30:1587–1595, 2009.

    Article  CAS  PubMed  Google Scholar 

  43. Lee, J. S., J. M. Hong, J. W. Jung, J. H. Shim, J. H. Oh, and D. W. Cho. 3D printing of composite tissue with complex shape applied to ear regeneration. Biofabrication 6:024103, 2014.

    Article  PubMed  Google Scholar 

  44. Lee, S.-H., A. R. Jo, G. P. Choi, C. H. Woo, S. J. Lee, B.-S. Kim, H.-K. You, and Y.-S. Cho. Fabrication of 3D alginate scaffold with interconnected pores using wire-network molding technique. Tissue Eng. Regen. Med. 10:53–59, 2013.

    Article  CAS  Google Scholar 

  45. Lee, J. W., K. S. Kang, S. H. Lee, J. Y. Kim, B. K. Lee, and D. W. Cho. Bone regeneration using a microstereolithography-produced customized poly(propylene fumarate)/diethyl fumarate photopolymer 3D scaffold incorporating BMP-2 loaded PLGA microspheres. Biomaterials 32:744–752, 2011.

    Article  CAS  PubMed  Google Scholar 

  46. Lee, K. Y., and D. J. Mooney. Hydrogels for tissue engineering. Chem. Rev. 101:1869–1880, 2001.

    Article  CAS  PubMed  Google Scholar 

  47. Lu, Y., G. Mapili, G. Suhali, S. C. Chen, and K. Roy. A digital micro-mirror device-based system for the microfabrication of complex, spatially patterned tissue engineering scaffolds. J. Biomed. Mater. Res. A 77:396–405, 2006.

    Article  PubMed  Google Scholar 

  48. Madden, L. R., D. J. Mortisen, E. M. Sussman, S. K. Dupras, J. A. Fugate, J. L. Cuy, K. D. Hauch, M. A. Laflamme, C. E. Murry, and B. D. Ratner. Proangiogenic scaffolds as functional templates for cardiac tissue engineering. Proc. Natl. Acad. Sci. USA 107:15211–15216, 2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Madry, H., A. Rey-Rico, J. K. Venkatesan, B. Johnstone, and M. Cucchiarini. Transforming growth factor beta-releasing scaffolds for cartilage tissue engineering. Tissue Eng. Part B: Rev. 20:106–125, 2013.

    Article  Google Scholar 

  50. Malda, J., J. Visser, F. P. Melchels, T. Jüngst, W. E. Hennink, W. J. Dhert, J. Groll, and D. W. Hutmacher. 25th anniversary article: engineering hydrogels for biofabrication. Adv. Mater. 25:5011–5028, 2013.

    Article  CAS  PubMed  Google Scholar 

  51. Markstedt, K., A. Mantas, I. Tournier, H. Martínez Ávila, D. Hägg, and P. Gatenholm. 3D bioprinting human chondrocytes with nanocellulose–alginate bioink for cartilage tissue engineering applications. Biomacromolecules. 16:1489–1496, 2015.

    Article  CAS  PubMed  Google Scholar 

  52. Matsuura, K., R. Utoh, K. Nagase, and T. Okano. Cell sheet approach for tissue engineering and regenerative medicine. J. Control Release 190:228–239, 2014.

    Article  CAS  PubMed  Google Scholar 

  53. Melchels, F. P., M. A. Domingos, T. J. Klein, J. Malda, P. J. Bartolo, and D. W. Hutmacher. Additive manufacturing of tissues and organs. Prog. Polymer Sci. 37:1079–1104, 2012.

    Article  CAS  Google Scholar 

  54. Melchels, F. P., J. Feijen, and D. W. Grijpma. A review on stereolithography and its applications in biomedical engineering. Biomaterials 31:6121–6130, 2010.

    Article  CAS  PubMed  Google Scholar 

  55. Miller, J. S., K. R. Stevens, M. T. Yang, B. M. Baker, D.-H. T. Nguyen, D. M. Cohen, E. Toro, A. A. Chen, P. A. Galie, and X. Yu. Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues. Nat. Mater. 11:768–774, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Mironov, V., T. Boland, T. Trusk, G. Forgacs, and R. R. Markwald. Organ printing: computer-aided jet-based 3D tissue engineering. Trends Biotechnol. 21:157–161, 2003.

    Article  CAS  PubMed  Google Scholar 

  57. Mironov, V., N. Reis, and B. Derby. Review: bioprinting: a beginning. Tissue Eng. 12:631–634, 2006.

    Article  PubMed  Google Scholar 

  58. Mironov, V., R. P. Visconti, V. Kasyanov, G. Forgacs, C. J. Drake, and R. R. Markwald. Organ printing: tissue spheroids as building blocks. Biomaterials 30:2164–2174, 2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Mozaffarian, D., E. J. Benjamin, A. S. Go, D. K. Arnett, M. J. Blaha, M. Cushman, S. de Ferranti, J.-P. Despres, H. J. Fullerton, and V. J. Howard. Heart disease and stroke statistics-2015 update: a report from the american heart association. Circulation 131:e29, 2015.

    Article  PubMed  Google Scholar 

  60. Murphy, S. V., and A. Atala. 3D bioprinting of tissues and organs. Nat. Biotechnol. 32:773–785, 2014.

    Article  CAS  PubMed  Google Scholar 

  61. Nahmias, Y., R. E. Schwartz, C. M. Verfaillie, and D. J. Odde. Laser-guided direct writing for three-dimensional tissue engineering. Biotechnol. Bioeng. 92:129–136, 2005.

    Article  CAS  PubMed  Google Scholar 

  62. Nakamura, M., S. Iwanaga, C. Henmi, K. Arai, and Y. Nishiyama. Biomatrices and biomaterials for future developments of bioprinting and biofabrication. Biofabrication. 2:014110, 2010.

    Article  CAS  PubMed  Google Scholar 

  63. Nakamura, M., A. K. Kobawashi, F. Takagi, A. Watanabe, Y. Hiruma, K. Ohuchi, Y. Iwasaki, M. Horie, I. Morita, and S. Takatani. Biocompatible inkjet printing technique for designed seeding of individual living cells. Tissue Eng. 11:1658–1666, 2005.

    Article  CAS  PubMed  Google Scholar 

  64. Norotte, C., F. S. Marga, L. E. Niklason, and G. Forgacs. Scaffold-free vascular tissue engineering using bioprinting. Biomaterials 30:5910–5917, 2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Odde, D. J., and M. J. Renn. Laser-guided direct writing for applications in biotechnology. Trends Biotechnol. 17:385–389, 1999.

    Article  CAS  PubMed  Google Scholar 

  66. Park, J. H., J. M. Hong, Y. M. Ju, J. W. Jung, H. Y. Kang, S. J. Lee, J. J. Yoo, S. W. Kim, S. H. Kim, and D. W. Cho. A novel tissue-engineered trachea with a mechanical behavior similar to native trachea. Biomaterials 62:106–115, 2015.

    Article  CAS  PubMed  Google Scholar 

  67. Park, J. H., J. Jang, and D. W. Cho. Three-dimensional printed 3D structure for tissue engineering. Trans. Korean. Soc. Mech. Eng. 38:817–829, 2014.

    Article  Google Scholar 

  68. Park, J. H., J. W. Jung, H. Y. Kang, Y. H. Joo, J. S. Lee, and D. W. Cho. Development of a 3D bellows tracheal graft: mechanical behavior analysis, fabrication and an in vivo feasibility study. Biofabrication 4:035004, 2012.

    Article  PubMed  Google Scholar 

  69. Park, J. K., J. H. Shim, K. S. Kang, J. Yeom, H. S. Jung, J. Y. Kim, K. H. Lee, T. H. Kim, S. Y. Kim, and D. W. Cho. Solid free-form fabrication of tissue-engineering scaffolds with a poly (lactic-co-glycolic acid) grafted hyaluronic acid conjugate encapsulating an intact bone morphogenetic protein-2/poly (ethylene glycol) complex. Adv. Funct. Mater. c21:2906–2912, 2011.

    Article  Google Scholar 

  70. Park, H., J. S. Temenoff, Y. Tabata, A. I. Caplan, and A. G. Mikos. Injectable biodegradable hydrogel composites for rabbit marrow mesenchymal stem cell and growth factor delivery for cartilage tissue engineering. Biomaterials 28:3217–3227, 2007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Pati, F., D. H. Ha, J. Jang, H. H. Han, J. W. Rhie, and D. W. Cho. Biomimetic 3D tissue printing for soft tissue regeneration. Biomaterials 62:164–175, 2015.

    Article  CAS  PubMed  Google Scholar 

  72. Pati, F., J. Jang, D. H. Ha, S. W. Kim, J. W. Rhie, J. H. Shim, D. H. Kim, and D. W. Cho. Printing three dimensional tissue analogues with decellularized extracellular matrix bioink. Nat. Commun. 5:3935, 2014. doi:10.1038/ncomms4935

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Pati, F., T.-H. Song, G. Rijal, J. Jang, S. W. Kim, and D.-W. Cho. Ornamenting 3D printed scaffolds with cell-laid extracellular matrix for bone tissue regeneration. Biomaterials. 37:230–241, 2015.

    Article  CAS  PubMed  Google Scholar 

  74. Ringeisen, B. R., H. Kim, J. A. Barron, D. B. Krizman, D. B. Chrisey, S. Jackman, R. Auyeung, and B. J. Spargo. Laser printing of pluripotent embryonal carcinoma cells. Tissue Eng. 10:483–491, 2004.

    Article  CAS  PubMed  Google Scholar 

  75. Seok, J., H. S. Warren, A. G. Cuenca, M. N. Mindrinos, H. V. Baker, W. Xu, D. R. Richards, G. P. McDonald-Smith, H. Gao, and L. Hennessy. Genomic responses in mouse models poorly mimic human inflammatory diseases. Proc. Natl. Acad. Sci. USA 110:3507–3512, 2013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Seol, Y. J., T. Y. Kang, and D. W. Cho. Solid freeform fabrication technology applied to tissue engineering with various biomaterials. Soft Matter 8:1730–1735, 2012.

    Article  CAS  Google Scholar 

  77. Seol, Y. J., H. Y. Kang, S. J. Lee, A. Atala, and J. J. Yoo. Bioprinting technology and its applications. Eur. J. Cardiothorac. Surg. 46(3):342–348, 2014.

    Article  PubMed  Google Scholar 

  78. Shanjani, Y., C. C. Pan, L. Elomaa, and Y. Yang. A novel bioprinting method and system for forming hybrid tissue engineering constructs. Biofabrication 7:045008, 2015.

    Article  CAS  PubMed  Google Scholar 

  79. Shim, J.-H., J.-B. Huh, J. Y. Park, Y.-C. Jeon, S. S. Kang, J. Y. Kim, J.-W. Rhie, and D.-W. Cho. Fabrication of blended polycaprolactone/poly (lactic-co-glycolic acid)/β-tricalcium phosphate thin membrane using solid freeform fabrication technology for guided bone regeneration. Tissue Eng. Part A. 19:317–328, 2012.

    Article  PubMed  PubMed Central  Google Scholar 

  80. Shim, J. H., J. Y. Kim, M. Park, J. Park, and D. W. Cho. Development of a hybrid scaffold with synthetic biomaterials and hydrogel using solid freeform fabrication technology. Biofabrication 3:034102, 2011.

    Article  PubMed  Google Scholar 

  81. Shim, J. H., J. S. Lee, J. Y. Kim, and D. W. Cho. Bioprinting of a mechanically enhanced three-dimensional dual cell-laden construct for osteochondral tissue engineering using a multi-head tissue/organ building system. J. Micromech. Microeng. 22:085014, 2012.

    Article  Google Scholar 

  82. Singh, S., I. O. Afara, A. H. Tehrani, and A. Oloyede. Effect of decellularization on the load-bearing characteristics of articular cartilage matrix. Tissue Eng. Regen. Med. 12:294–305, 2015.

    Article  CAS  Google Scholar 

  83. Smith, C. M., A. L. Stone, R. L. Parkhill, R. L. Stewart, M. W. Simpkins, A. M. Kachurin, W. L. Warren, and S. K. Williams. Three-dimensional bioassembly tool for generating viable tissue-engineered constructs. Tissue Eng. 10:1566–1576, 2004.

    Article  CAS  PubMed  Google Scholar 

  84. Sohn, Y. S., J. W. Jung, J. Y. Kim, and D. W. Cho. Investigation of bi-pore scaffold based on the cell behaviors on 3D scaffold patterns. Tissue Eng. Regen. Med. 8:66–72, 2011.

    Google Scholar 

  85. Song, B. R., S. S. Yang, H. Jin, S. H. Lee, D. Y. Park, J. H. Lee, S. R. Park, S.-H. Park and B.-H. Min. Three dimensional plotted extracellular matrix scaffolds using a rapid prototyping for tissue engineering applications. Tissue Eng. Regen. Med. 12:172–180, 2015.

    Article  CAS  Google Scholar 

  86. Spiller, K. L., Y. Liu, J. L. Holloway, S. A. Maher, Y. Cao, W. Liu, G. Zhou, and A. M. Lowman. A novel method for the direct fabrication of growth factor-loaded microspheres within porous nondegradable hydrogels: controlled release for cartilage tissue engineering. J. Control Release 157:39–45, 2012.

    Article  CAS  PubMed  Google Scholar 

  87. Spotnitz, W. D. Commercial fibrin sealants in surgical care. Am. J. Surg. 182:S8–S14, 2001.

    Article  Google Scholar 

  88. Tabata, Y., and Y. Ikada. Protein release from gelatin matrices. Adv. Drug Deliv. Rev. 31:287–301, 1998.

    Article  CAS  PubMed  Google Scholar 

  89. Visser, J., B. Peters, T. J. Burger, J. Boomstra, W. J. Dhert, F. P. Melchels, and J. Malda. Biofabrication of multi-material anatomically shaped tissue constructs. Biofabrication 5:035007, 2013.

    Article  PubMed  Google Scholar 

  90. Wang, Z., R. Abdulla, B. Parker, R. Samanipour, S. Ghosh, and K. Kim. A simple and high-resolution stereolithography-based 3D bioprinting system using visible light crosslinkable bioinks. Biofabrication 7:045009, 2015.

    Article  PubMed  Google Scholar 

  91. Wei, C., and J. Dong. Direct fabrication of high-resolution three-dimensional polymeric scaffolds using electrohydrodynamic hot jet plotting. J. Micromech. Microeng. 23:025017, 2013.

    Article  Google Scholar 

  92. Wu, W., A. DeConinck, and J. A. Lewis. Omnidirectional printing of 3D microvascular networks. Adv. Mater. 23:H178–H183, 2011.

    Article  CAS  PubMed  Google Scholar 

  93. Xiong, Q., K. L. Hill, Q. Li, P. Suntharalingam, A. Mansoor, X. Wang, M. N. Jameel, P. Zhang, C. Swingen, and D. S. Kaufman. A fibrin patch-based enhanced delivery of human embryonic stem cell-derived vascular cell transplantation in a porcine model of postinfarction left ventricular remodeling. Stem Cells. 29:367–375, 2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Ye, L., W.-H. Zimmermann, D. J. Garry, and J. Zhang. Patching the heart cardiac repair from within and outside. Circ. Res. 113:922–932, 2013.

    Article  CAS  PubMed  Google Scholar 

  95. Yeong, W. Y., C. K. Chua, K. F. Leong, and M. Chandrasekaran. Rapid prototyping in tissue engineering: challenges and potential. Trends Biotechnol. 22:354–362, 2004.

    Article  Google Scholar 

  96. Zhang, Y., Y. Yu, and I. T. Ozbolat. Direct bioprinting of vessel-like tubular microfluidic channels. J. Nanotechnol. Eng. Med. 4:020902, 2013.

    Article  Google Scholar 

  97. Zhao, Y., R. Yao, L. Ouyang, H. Ding, T. Zhang, K. Zhang, S. Cheng, and W. Sun. Three-dimensional printing of Hela cells for cervical tumor model in vitro. Biofabrication. 6:035001, 2014.

    Article  PubMed  Google Scholar 

  98. Zimmermann, W.-H., I. Melnychenko, G. Wasmeier, M. Didié, H. Naito, U. Nixdorff, A. Hess, L. Budinsky, K. Brune, and B. Michaelis. Engineered heart tissue grafts improve systolic and diastolic function in infarcted rat hearts. Nat. Med. 12:452–458, 2006.

    Article  CAS  PubMed  Google Scholar 

  99. Zorlutuna, P., J. H. Jeong, H. Kong, and R. Bashir. Tissue engineering: stereolithography-based hydrogel microenvironments to examine cellular interactions. Adv. Funct. Mater. 21:3597, 2011.

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIP) (No. 2010-0018294).

Conflict of interest

The authors have no financial conflicts of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dong-Woo Cho.

Additional information

Associate Editor Amir Abbas Zadpoor oversaw the review of this article.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Park, J.H., Jang, J., Lee, JS. et al. Three-Dimensional Printing of Tissue/Organ Analogues Containing Living Cells. Ann Biomed Eng 45, 180–194 (2017). https://doi.org/10.1007/s10439-016-1611-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10439-016-1611-9

Keywords

Navigation