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Annals of Biomedical Engineering

, Volume 45, Issue 1, pp 195–209 | Cite as

State-of-the-Art Review of 3D Bioprinting for Cardiovascular Tissue Engineering

  • Bin DuanEmail author
Additive Manufacturing of Biomaterials, Tissues, and Organs

Abstract

3D bioprinting is a group of rapidly growing techniques that allows building engineered tissue constructs with complex and hierarchical structures, mechanical and biological heterogeneity. It enables implementation of various bioinks through different printing mechanisms and precise deposition of cell and/or biomolecule laden biomaterials in predefined locations. This review briefly summarizes applicable bioink materials and various bioprinting techniques, and presents the recent advances in bioprinting of cardiovascular tissues, with focusing on vascularized constructs, myocardium and heart valve conduits. Current challenges and further perspectives are also discussed to help guide the bioink and bioprinter development, improve bioprinting strategies and direct future organ bioprinting and translational applications.

Keywords

Bioink Hydrogel Vascularization Heart valve Organ Bioprinting 

Notes

Acknowledgments

This work has been supported by Mary & Dick Holland Regenerative Medicine Program start-up grant and Nebraska Research Initiative funding. The author has no financial disclosures.

References

  1. 1.
    Ali, M., E. Pages, A. Ducom, A. Fontaine, and F. Guillemot. Controlling laser-induced jet formation for bioprinting mesenchymal stem cells with high viability and high resolution. Biofabrication 6:045001, 2014.PubMedCrossRefGoogle Scholar
  2. 2.
    Barannyk, O., and P. Oshkai. The influence of the aortic root geometry on flow characteristics of a prosthetic heart valve. J. Biomech. Eng. 137:051005, 2015.PubMedCrossRefGoogle Scholar
  3. 3.
    Bertassoni, L. E., J. C. Cardoso, V. Manoharan, A. L. Cristino, N. S. Bhise, W. A. Araujo, P. Zorlutuna, N. E. Vrana, A. M. Ghaemmaghami, M. R. Dokmeci, and A. Khademhosseini. Direct-write bioprinting of cell-laden methacrylated gelatin hydrogels. Biofabrication 6:024105, 2014.PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Bertassoni, L. E., M. Cecconi, V. Manoharan, M. Nikkhah, J. Hjortnaes, A. L. Cristino, G. Barabaschi, D. Demarchi, M. R. Dokmeci, Y. Z. Yang, and A. Khademhosseini. Hydrogel bioprinted microchannel networks for vascularization of tissue engineering constructs. Lab Chip 14:2202–2211, 2014.PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Billiet, T., E. Gevaert, T. De Schryver, M. Cornelissen, and P. Dubruel. The 3d printing of gelatin methacrylamide cell-laden tissue-engineered constructs with high cell viability. Biomaterials 35:49–62, 2014.PubMedCrossRefGoogle Scholar
  6. 6.
    Billiet, T., M. Vandenhaute, J. Schelfhout, S. Van Vlierberghe, and P. Dubruel. A review of trends and limitations in hydrogel-rapid prototyping for tissue engineering. Biomaterials 33:6020–6041, 2012.PubMedCrossRefGoogle Scholar
  7. 7.
    Bouten, C. V. C., P. Y. W. Dankers, A. Driessen-Mol, S. Pedron, A. M. A. Brizard, and F. P. T. Baaijens. Substrates for cardiovascular tissue engineering. Adv. Drug Deliv. Rev. 63:221–241, 2011.PubMedCrossRefGoogle Scholar
  8. 8.
    Butcher, J. T., G. J. Mahler, and L. A. Hockaday. Aortic valve disease and treatment: The need for naturally engineered solutions. Adv. Drug Deliv. Rev. 63:242–268, 2011.PubMedCrossRefGoogle Scholar
  9. 9.
    Catros, S., F. Guillemot, A. Nandakumar, S. Ziane, L. Moroni, P. Habibovic, C. van Blitterswijk, B. Rousseau, O. Chassande, J. Amedee, and J. C. Fricain. Layer-by-layer tissue microfabrication supports cell proliferation in vitro and in vivo. Tissue Eng. C 18:62–70, 2012.CrossRefGoogle Scholar
  10. 10.
    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 98B:160–170, 2011.CrossRefGoogle Scholar
  11. 11.
    Chen, J. H., and C. A. Simmons. Cell-matrix interactions in the pathobiology of calcific aortic valve disease critical roles for matricellular, matricrine, and matrix mechanics cues. Circ. Res. 108:1510–1524, 2011.PubMedCrossRefGoogle Scholar
  12. 12.
    Cui, X. F., and T. Boland. Human microvasculature fabrication using thermal inkjet printing technology. Biomaterials 30:6221–6227, 2009.PubMedCrossRefGoogle Scholar
  13. 13.
    Cui, X. F., T. Boland, D. D. D’Lima, and M. K. Lotz. Thermal inkjet printing in tissue engineering and regenerative medicine. Recent Pat. Drug Deliv. Formul. 6:149–155, 2012.PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Derby, B. Printing and prototyping of tissues and scaffolds. Science 338:921–926, 2012.PubMedCrossRefGoogle Scholar
  15. 15.
    Duan, B., L. A. Hockaday, S. Das, C. Y. Xu, and J. T. Butcher. Comparison of mesenchymal stem cell source differentiation towards human pediatric aortic valve interstitial cells within 3d engineered matrices. Tissue Eng. C 21:795–807, 2015.CrossRefGoogle Scholar
  16. 16.
    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., Part A 101A:1255–1264, 2013.CrossRefGoogle Scholar
  17. 17.
    Duan, B., L. A. Hockaday, E. Kapetanovic, K. H. Kang, and J. T. Butcher. Stiffness and adhesivity control aortic valve interstitial cell behavior within hyaluronic acid based hydrogels. Acta Biomater. 9:7640–7650, 2013.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Duan, B., E. Kapetanovic, L. A. Hockaday, and J. T. Butcher. Three-dimensional printed trileaflet valve conduits using biological hydrogels and human valve interstitial cells. Acta Biomater. 10:1836–1846, 2014.PubMedCrossRefGoogle Scholar
  19. 19.
    Duan, B., and M. Wang. Customized ca-p/phbv nanocomposite scaffolds for bone tissue engineering: design, fabrication, surface modification and sustained release of growth factor. J. R. Soc. Interface 7:S615–S629, 2010.PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Duan, B., and M. Wang. Selective laser sintering and its application in biomedical engineering. MRS Bull. 36:998–1005, 2011.CrossRefGoogle Scholar
  21. 21.
    Duan, B., M. Wang, W. Y. Zhou, W. L. Cheung, Z. Y. Li, and W. W. Lu. Three-dimensional nanocomposite scaffolds fabricated via selective laser sintering for bone tissue engineering. Acta Biomater. 6:4495–4505, 2010.PubMedCrossRefGoogle Scholar
  22. 22.
    Gaebel, R., N. Ma, J. Liu, J. J. Guan, L. Koch, C. Klopsch, M. Gruene, A. Toelk, W. W. Wang, and P. Mark. Patterning human stem cells and endothelial cells with laser printing for cardiac regeneration. Biomaterials 32:9218–9230, 2011.PubMedCrossRefGoogle Scholar
  23. 23.
    Gaetani, R., P. A. Doevendans, C. H. G. Metz, J. Alblas, E. Messina, A. Giacomello, and J. P. G. Sluijtera. Cardiac tissue engineering using tissue printing technology and human cardiac progenitor cells. Biomaterials 33:1782–1790, 2012.PubMedCrossRefGoogle Scholar
  24. 24.
    Gaetani, R., D. A. M. Feyen, V. Verhage, R. Slaats, E. Messina, K. L. Christman, A. Giacomello, P. A. F. M. Doevendans, and J. P. G. 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.PubMedCrossRefGoogle Scholar
  25. 25.
    Gao, Q., Y. He, J. Z. Fu, A. Liu, and L. Ma. Coaxial nozzle-assisted 3d bioprinting with built-in microchannels for nutrients delivery. Biomaterials 61:203–215, 2015.PubMedCrossRefGoogle Scholar
  26. 26.
    Gao, G. F., A. F. Schilling, K. Hubbell, T. Yonezawa, D. Truong, Y. Hong, G. H. Dai, and X. F. Cui. 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. 37:2349–2355, 2015.PubMedCrossRefGoogle Scholar
  27. 27.
    Gerstle, T. L., A. M. S. Ibrahim, P. S. Kim, B. T. Lee, and S. J. Lin. A plastic surgery application in evolution: Three-dimensional printing. Plast. Reconstr. Surg. 133:446–451, 2014.PubMedCrossRefGoogle Scholar
  28. 28.
    Go, A. S., D. Mozaffarian, V. L. Roger, E. J. Benjamin, J. D. Berry, M. J. Blaha, S. F. Dai, E. S. Ford, C. S. Fox, S. Franco, H. J. Fullerton, C. Gillespie, S. M. Hailpern, J. A. Heit, V. J. Howard, M. D. Huffman, S. E. Judd, B. M. Kissela, S. J. Kittner, D. T. Lackland, J. H. Lichtman, L. D. Lisabeth, R. H. Mackey, D. J. Magid, G. M. Marcus, A. Marelli, D. B. Matchar, D. K. McGuire, E. R. Mohler, C. S. Moy, M. E. Mussolino, R. W. Neumar, G. Nichol, D. K. Pandey, N. P. Paynter, M. J. Reeves, P. D. Sorlie, J. Stein, A. Towfighi, T. N. Turan, S. S. Virani, N. D. Wong, D. Woo, M. B. Turner, A. H. A. S. Comm, and S. S. Subcomm. Heart disease and stroke statistics-2014 update a report from the American heart association. Circulation 129:E28–E292, 2014.PubMedCrossRefGoogle Scholar
  29. 29.
    Gou, M. L., X. Qu, W. Zhu, M. L. Xiang, J. Yang, K. Zhang, Y. Q. Wei, and S. C. Chen. Bio-inspired detoxification using 3d-printed hydrogel nanocomposites. Nat. Commun. 5:3774, 2014.PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Guillemot, F., V. Mironov, and M. Nakamura. Bioprinting is coming of age: Report from the international conference on bioprinting and biofabrication in bordeaux (3b’09). Biofabrication 2:010201, 2010.PubMedCrossRefGoogle Scholar
  31. 31.
    Guillotin, B., A. Souquet, S. Catros, M. Duocastella, B. Pippenger, S. Bellance, R. Bareille, M. Remy, L. Bordenave, J. Amedee, and F. Guillemot. Laser assisted bioprinting of engineered tissue with high cell density and microscale organization. Biomaterials 31:7250–7256, 2010.PubMedCrossRefGoogle Scholar
  32. 32.
    Haraguchi, Y., T. Shimizu, M. Yamato, and T. Okano. Concise review: cell therapy and tissue engineering for cardiovascular disease. Stem Cells and Translational Medicine. 1:136–141, 2012.CrossRefGoogle Scholar
  33. 33.
    Hasan, A., K. Ragaert, W. Swieszkowski, S. Selimovic, A. Paul, G. Camci-Unal, M. R. K. Mofrad, and A. Khademhosseini. Biomechanical properties of native and tissue engineered heart valve constructs. J. Biomech. 47:1949–1963, 2014.PubMedCrossRefGoogle Scholar
  34. 34.
    Hinton, T. J., Q. Jallerat, R. N. Palchesko, J. H. Park, M. S. Grodzicki, H. J. Shue, M. H. Ramadan, A. R. Hudson, and A. W. Feinberg. Three-dimensional printing of complex biological structures by freeform reversible embedding of suspended hydrogels. Sci. Adv. 1:e1500758, 2015.PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Hirt, M. N., A. Hansen, and T. Eschenhagen. Cardiac tissue engineering state of the art. Circ. Res. 114:354–367, 2014.PubMedCrossRefGoogle Scholar
  36. 36.
    Hockaday, L. A., B. Duan, K. H. Kang, and J. T. Butcher. 3D printed hydrogel technologies for tissue engineered heart valves. 3D Print. Addit. Manuf. 1:122–136, 2014.CrossRefGoogle Scholar
  37. 37.
    Hockaday, L. A., K. H. Kang, N. W. Colangelo, P. Y. C. Cheung, B. Duan, E. Malone, J. Wu, L. N. Girardi, L. J. Bonassar, H. Lipson, C. C. Chu, and J. T. Butcher. Rapid 3D printing of anatomically accurate and mechanically heterogeneous aortic valve hydrogel scaffolds. Biofabrication 4:035005, 2012.PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Horch, R. E., U. Kneser, E. Polykandriotis, V. J. Schmidt, J. M. Sun, and A. Arkudas. Tissue engineering and regenerative medicine—where do we stand? J. Cell Mol. Med. 16:1157–1165, 2012.PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Horvath, L., Y. Umehara, C. Jud, F. Blank, A. Petri-Fink, and B. Rothen-Rutishauser. Engineering an in vitro air-blood barrier by 3D bioprinting. Sci. Rep. 5:7974, 2015.PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Hribar, K. C., P. Soman, J. Warner, P. Chung, and S. C. Chen. Light-assisted direct-write of 3D functional biomaterials. Lab Chip 14:268–275, 2014.PubMedCrossRefGoogle Scholar
  41. 41.
    Jakab, K., C. Norotte, F. Marga, K. Murphy, G. Vunjak-Novakovic, and G. Forgacs. Tissue engineering by self-assembly and bio-printing of living cells. Biofabrication 2:022001, 2010.PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Jana, S., and A. Lerman. Bioprinting a cardiac valve. Biotechnol. Adv. 33:1503–1521, 2015.PubMedCrossRefGoogle Scholar
  43. 43.
    Jana, S., B. J. Tefft, D. B. Spoon, and R. D. Simari. Scaffolds for tissue engineering of cardiac valves. Acta Biomater. 10:2877–2893, 2014.PubMedCrossRefGoogle Scholar
  44. 44.
    Jia, J., D. J. Richards, S. Pollard, Y. Tan, J. Rodriguez, R. P. Visconti, T. C. Trusk, M. J. Yost, H. Yao, R. R. Markwald, and Y. Mei. Engineering alginate as bioink for bioprinting. Acta Biomater. 10:4323–4331, 2014.PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Kang, K. H., L. A. Hockaday, and J. T. Butcher. Quantitative optimization of solid freeform deposition of aqueous hydrogels. Biofabrication 5:035001, 2013.PubMedCrossRefGoogle Scholar
  46. 46.
    Kirchmajer, D. M., R. Gorkin, and M. I. H. Panhuis. An overview of the suitability of hydrogel-forming polymers for extrusion-based 3d-printing. J. Mater. Chem. B 3:4105–4117, 2015.CrossRefGoogle Scholar
  47. 47.
    Kolesky, D. B., R. L. Truby, A. S. 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.PubMedCrossRefGoogle Scholar
  48. 48.
    Kucukgul, C., S. B. Ozler, I. Inci, E. Karakas, S. Irmak, D. Gozuacik, A. Taralp, and B. Koc. 3d bioprinting of biomimetic aortic vascular constructs with self-supporting cells. Biotechnol. Bioeng. 112:811–821, 2015.PubMedCrossRefGoogle Scholar
  49. 49.
    Lantada, A. D., and P. L. Morgado. Rapid prototyping for biomedical engineering: current capabilities and challenges. Annu. Rev. Biomed. Eng. 14:73–96, 2012.PubMedCrossRefGoogle Scholar
  50. 50.
    Lee, V. K., D. Y. Kim, H. G. Ngo, Y. Lee, L. Seo, S. S. Yoo, P. A. Vincent, and G. H. Dai. Creating perfused functional vascular channels using 3d bio-printing technology. Biomaterials 35:8092–8102, 2014.PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Lee, V. K., A. M. Lanzi, H. Ngo, S. S. Yoo, P. A. Vincent, and G. H. Dai. Generation of multi-scale vascular network system within 3d hydrogel using 3d bio-printing technology. Cell. Mol. Bioeng. 7:460–472, 2014.PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Levato, R., J. Visser, J. A. Planell, E. Engel, J. Malda, and M. A. Mateos-Timoneda. Biofabrication of tissue constructs by 3d bioprinting of cell-laden microcarriers. Biofabrication 6:035020, 2014.PubMedCrossRefGoogle Scholar
  53. 53.
    Li, C., A. Faulkner-Jones, A. R. Dun, J. Jin, P. Chen, Y. Z. Xing, Z. Q. Yang, Z. B. Li, W. M. Shu, D. S. Liu, and R. R. Duncan. Rapid formation of a supramolecular polypeptide-DNA hydrogel for in situ three-dimensional multilayer bioprinting. Angew. Chem. Int. Ed. 54:3957–3961, 2015.CrossRefGoogle Scholar
  54. 54.
    Loerakker, S., G. Argento, C. W. J. Oomens, and F. P. T. Baaijens. Effects of valve geometry and tissue anisotropy on the radial stretch and coaptation area of tissue-engineered heart valves. J. Biomech. 46:1792–1800, 2013.PubMedCrossRefGoogle Scholar
  55. 55.
    Loo, Y. H., A. Lakshmanan, M. Ni, L. L. Toh, S. Wang, and C. A. E. Hauser. Peptide bioink: self-assembling nanofibrous scaffolds for three-dimensional organotypic cultures. Nano Lett. 15:6919–6925, 2015.PubMedCrossRefGoogle Scholar
  56. 56.
    Lundberg, M. S. Cardiovascular tissue engineering research support at the national heart, lung, and blood institute. Circ. Res. 112:1097–1103, 2013.PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Markstedt, K., A. Mantas, I. Tournier, H. M. Avila, D. Hagg, and P. Gatenholm. 3D bioprinting human chondrocytes with nanocellulose-alginate bioink for cartilage tissue engineering applications. Biomacromolecules 16:1489–1496, 2015.PubMedCrossRefGoogle Scholar
  58. 58.
    Mehesz, A. N., J. Brown, Z. Hajdu, W. Beaver, J. V. L. da Silva, R. P. Visconti, R. R. Markwald, and V. Mironov. Scalable robotic biofabrication of tissue spheroids. Biofabrication 3:025002, 2011.PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Melchels, F. P. W., M. A. N. Domingos, T. J. Klein, J. Malda, P. J. Bartolo, and D. W. Hutmacher. Additive manufacturing of tissues and organs. Prog. Polym. Sci. 37:1079–1104, 2012.CrossRefGoogle Scholar
  60. 60.
    Melchels, F. P. W., J. Feijen, and D. W. Grijpma. A review on stereolithography and its applications in biomedical engineering. Biomaterials 31:6121–6130, 2010.PubMedCrossRefGoogle Scholar
  61. 61.
    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, X. Yu, R. Chaturvedi, S. N. Bhatia, and C. S. Chen. Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues. Nat. Mater. 11:768–774, 2012.PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Mironov, V., N. Reis, and B. Derby. Bioprinting: a beginning. Tissue Eng. 12:631–634, 2006.PubMedCrossRefGoogle Scholar
  63. 63.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Mosadegh, B., G. L. Xiong, S. Dunham, and J. K. Min. Current progress in 3d printing for cardiovascular tissue engineering. Biomed. Mater. 10:034002, 2015.PubMedCrossRefGoogle Scholar
  65. 65.
    Murphy, S. V., and A. Atala. 3d bioprinting of tissues and organs. Nat. Biotechnol. 32:773–785, 2014.PubMedCrossRefGoogle Scholar
  66. 66.
    Murry, C. E., R. W. Wiseman, S. M. Schwartz, and S. D. Hauschka. Skeletal myoblast transplantation for repair of myocardial necrosis. J. Clin. Invest. 98:2512–2523, 1996.PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Norotte, C., F. S. Marga, L. E. Niklason, and G. Forgacs. Scaffold-free vascular tissue engineering using bioprinting. Biomaterials 30:5910–5917, 2009.PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Novosel, E. C., C. Kleinhans, and P. J. Kluger. Vascularization is the key challenge in tissue engineering. Adv. Drug Deliv. Rev. 63:300–311, 2011.PubMedCrossRefGoogle Scholar
  69. 69.
    Ozbolat, I. T. Bioprinting scale-up tissue and organ constructs for transplantation. Trends Biotechnol. 33:395–400, 2015.PubMedCrossRefGoogle Scholar
  70. 70.
    Ozbolat, I. T., and M. Hospodiuk. Current advances and future perspectives in extrusion-based bioprinting. Biomaterials 76:321–343, 2016.PubMedCrossRefGoogle Scholar
  71. 71.
    Ozbolat, I. T., and Y. Yu. Bioprinting toward organ fabrication: challenges and future trends. IEEE Trans. Biomed. Eng. 60:691–699, 2013.PubMedCrossRefGoogle Scholar
  72. 72.
    Park, J. Y., J. H. Shim, S. A. Choi, J. Jang, M. Kim, S. H. Lee, and D. W. Cho. 3d printing technology to control bmp-2 and vegf delivery spatially and temporally to promote large-volume bone regeneration. J. Mater. Chem. B 3:5415–5425, 2015.CrossRefGoogle Scholar
  73. 73.
    Parvin, N. S., M. C. Blaser, J. P. Santerre, C. A. Caldarone, and C. A. Simmons. Biomechanical conditioning of tissue engineered heart valves: too much of a good thing? Adv. Drug Deliv. Rev. 96:161–175, 2016.CrossRefGoogle Scholar
  74. 74.
    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.PubMedCrossRefGoogle Scholar
  75. 75.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Paulsen, S. J., and J. S. Miller. Tissue vascularization through 3D printing: will technology bring us flow? Dev. Dyn. 244:629–640, 2015.PubMedCrossRefGoogle Scholar
  77. 77.
    Peltola, S. M., F. P. W. Melchels, D. W. Grijpma, and M. Kellomaki. A review of rapid prototyping techniques for tissue engineering purposes. Ann. Med. 40:268–280, 2008.PubMedCrossRefGoogle Scholar
  78. 78.
    Poldervaart, M. T., H. Gremmels, K. van Deventer, J. O. Fledderus, F. C. Oner, M. C. Verhaar, W. J. A. Dhert, and J. Alblas. Prolonged presence of vegf promotes vascularization in 3d bioprinted scaffolds with defined architecture. J. Controlled Release 184:58–66, 2014.CrossRefGoogle Scholar
  79. 79.
    Reffelmann, T., and R. A. Kloner. Cellular cardiomyoplasty—cardiomyocytes, skeletal myoblasts, or stem cells for regenerating myocardium and treatment of heart failure? Cardiovasc. Res. 58:358–368, 2003.PubMedCrossRefGoogle Scholar
  80. 80.
    Rouwkema, J., N. C. Rivron, and C. A. van Blitterswijk. Vascularization in tissue engineering. Trends Biotechnol. 26:434–441, 2008.PubMedCrossRefGoogle Scholar
  81. 81.
    Rutz, A. L., K. E. Hyland, A. E. Jakus, W. R. Burghardt, and R. N. Shah. A multimaterial bioink method for 3D printing tunable, cell-compatible hydrogels. Adv. Mater. 27:1607–1614, 2015.PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Sanders, B., S. Loerakker, E. S. Fioretta, D. J. P. Bax, A. Driessen-Mol, S. P. Hoerstrup, and F. P. T. Baaijens. Improved geometry of decellularized tissue engineered heart valves to prevent leaflet retraction. Ann. Biomed. Eng. 2015. doi: 10.1007/s10439-10015-11386-10434.PubMedPubMedCentralGoogle Scholar
  83. 83.
    Saunders, R. E., and B. Derby. Inkjet printing biomaterials for tissue engineering: bioprinting. Int. Mater. Rev. 59:430–448, 2014.CrossRefGoogle Scholar
  84. 84.
    Schiele, N. R., D. T. Corr, Y. Huang, N. A. Raof, Y. B. Xie, and D. B. Chrisey. Laser-based direct-write techniques for cell printing. Biofabrication 2:032001, 2010.PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Schmidt, C. E., and J. M. Baier. Acellular vascular tissues: Natural biomaterials for tissue repair and tissue engineering. Biomaterials 21:2215–2231, 2000.PubMedCrossRefGoogle Scholar
  86. 86.
    Seol, Y. J., H. W. Kang, S. J. Lee, A. Atala, and J. J. Yoo. Bioprinting technology and its applications. Eur. J. Cardiothorac. Surg. 46:342–348, 2014.PubMedCrossRefGoogle Scholar
  87. 87.
    Sodian, R., D. Schmauss, M. Markert, S. Weber, K. Nikolaou, S. Haeberle, F. Vogt, C. Vicol, T. Lueth, B. Reichart, and C. Schmitz. Three-dimensional printing creates models for surgical planning of aortic valve replacement after previous coronary bypass grafting. Ann. Thorac. Surg. 85:2105–2109, 2008.PubMedCrossRefGoogle Scholar
  88. 88.
    Spadaccio, C., M. Chello, M. Trombetta, A. Rainer, Y. Toyoda, and J. A. Genovese. Drug releasing systems in cardiovascular tissue engineering. J. Cell Mol. Med. 13:422–439, 2009.PubMedCrossRefGoogle Scholar
  89. 89.
    Sui, R. Q., X. B. Liao, X. M. Zhou, and Q. Tan. The current status of engineering myocardial tissue. Stem Cell Rev. Rep. 7:172–180, 2011.CrossRefGoogle Scholar
  90. 90.
    Sun, X., W. Altalhi, and S. S. Nunes. Vascularization strategies of engineered tissues and their application in cardiac regeneration. Adv. Drug Deliv. Rev. 2015. doi: 10.1016/j.addr.2015.1006.1001.Google Scholar
  91. 91.
    Visser, J., F. P. W. Melchels, J. E. Jeon, E. M. van Bussel, L. S. Kimpton, H. M. Byrne, W. J. A. Dhert, P. D. Dalton, D. W. Hutmacher, and J. Malda. Reinforcement of hydrogels using three-dimensionally printed microfibres. Nat. Commun. 6:6933, 2015.PubMedCrossRefGoogle Scholar
  92. 92.
    Wang, F., and J. J. Guan. Cellular cardiomyoplasty and cardiac tissue engineering for myocardial therapy. Adv. Drug Deliv. Rev. 62:784–797, 2010.PubMedCrossRefGoogle Scholar
  93. 93.
    Williams, J. M., A. Adewunmi, R. M. Schek, C. L. Flanagan, P. H. Krebsbach, S. E. Feinberg, S. J. Hollister, and S. Das. Bone tissue engineering using polycaprolactone scaffolds fabricated via selective laser sintering. Biomaterials 26:4817–4827, 2005.PubMedCrossRefGoogle Scholar
  94. 94.
    Williams, S. K., J. S. Touroo, K. H. Church, and J. B. Hoying. Encapsulation of adipose stromal vascular fraction cells in alginate hydrogel spheroids using a direct-write three-dimensional printing system. Biores. Open Access. 2:448–454, 2013.PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Wong, N. D. Epidemiological studies of chd and the evolution of preventive cardiology. Nat. Rev. Cardiol. 11:276–289, 2014.PubMedCrossRefGoogle Scholar
  96. 96.
    Woodfield, T. B. F., J. Malda, J. de Wijn, F. Peters, J. Riesle, and C. A. van Blitterswijk. Design of porous scaffolds for cartilage tissue engineering using a three-dimensional fiber-deposition technique. Biomaterials 25:4149–4161, 2004.PubMedCrossRefGoogle Scholar
  97. 97.
    Xu, T., K. W. Binder, M. Z. Albanna, D. Dice, W. X. Zhao, J. J. Yoo, and A. Atala. Hybrid printing of mechanically and biologically improved constructs for cartilage tissue engineering applications. Biofabrication. 5:015001, 2013.PubMedCrossRefGoogle Scholar
  98. 98.
    Xu, Y. F., and X. H. Wang. Application of 3d biomimetic models in drug delivery and regenerative medicine. Curr. Pharm. Des. 21:1618–1626, 2015.PubMedCrossRefGoogle Scholar
  99. 99.
    Yang, S. F., K. F. Leong, Z. H. Du, and C. K. Chua. The design of scaffolds for use in tissue engineering. Part II. Rapid prototyping techniques. Tissue Eng. 8:1–11, 2002.PubMedCrossRefGoogle Scholar
  100. 100.
    Yeh, R. W., S. Sidney, M. Chandra, M. Sorel, J. V. Selby, and A. S. Go. Population trends in the incidence and outcomes of acute myocardial infarction. N. Engl. J. Med. 362:2155–2165, 2010.PubMedCrossRefGoogle Scholar
  101. 101.
    Yeong, W. Y., C. K. Chua, K. F. Leong, and M. Chandrasekaran. Rapid prototyping in tissue engineering: challenges and potential. Trends Biotechnol. 22:643–652, 2004.PubMedCrossRefGoogle Scholar
  102. 102.
    Yu, Y., Y. H. Zhang, and I. T. Ozbolat. A hybrid bioprinting approach for scale-up tissue fabrication. J. Manuf. Sci. Eng. Trans. ASME. 136:61013, 2014.CrossRefGoogle Scholar
  103. 103.
    Zein, I., D. W. Hutmacher, K. C. Tan, and S. H. Teoh. Fused deposition modeling of novel scaffold architectures for tissue engineering applications. Biomaterials 23:1169–1185, 2002.PubMedCrossRefGoogle Scholar
  104. 104.
    Zhang, A. P., X. Qu, P. Soman, K. C. Hribar, J. W. Lee, S. C. Chen, and S. L. He. Rapid fabrication of complex 3D extracellular microenvironments by dynamic optical projection stereolithography. Advanced Materials. 24:4266–4270, 2012.PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Zheng, Y., J. M. Chen, M. Craven, N. W. Choi, S. Totorica, A. Diaz-Santana, P. Kermani, B. Hempstead, C. Fischbach-Teschl, J. A. Lopez, and A. D. Stroock. In vitro microvessels for the study of angiogenesis and thrombosis. Proc. Natl Acad. Sci. USA 109:9342–9347, 2012.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Biomedical Engineering Society 2016

Authors and Affiliations

  1. 1.Division of Cardiology, Department of Internal MedicineUniversity of Nebraska Medical CenterOmahaUSA
  2. 2.Mary & Dick Holland Regenerative Medicine ProgramUniversity of Nebraska Medical CenterOmahaUSA

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