Bioprinting of artificial blood vessels: Current approaches towards a demanding goal

European Journal of Cardio-thoracic Surgery

Volumn 46, Issue 5, 2014, Pages 767-778

  Hoch, Eva ^a   Tovar, Günter E M ^a,b   Borchers, Kirsten ^b  

^a UNIVERSITY OF STUTTGART   (Germany)

^b FRAUNHOFER INSTITUTE FOR INTERFACIAL ENGINEERING AND BIOTECHNOLOGY IGB   (Germany)

Author keywords

Artificial blood vessels; Bioprinting; Tissue engineering

Indexed keywords

POLYMER;

ARTIFICIAL BLOOD VESSEL; BIOLOGICAL FUNCTIONS; BIOPRINTING; BLOOD VESSEL; CARDIOVASCULAR EQUIPMENT; CELL ENCAPSULATION; EXTRACELLULAR MATRIX; HUMAN; HYDROGEL; IN VITRO STUDY; PRIORITY JOURNAL; REVIEW; SURFACE PROPERTY; UMBILICAL VEIN ENDOTHELIAL CELL; ANIMAL; BIOLOGICAL MODEL; BLOOD VESSEL PROSTHESIS; CELL LINE; CYTOLOGY; PHYSIOLOGY; TISSUE ENGINEERING;

ANIMALS; BIOPRINTING; BLOOD VESSEL PROSTHESIS; BLOOD VESSELS; CELL LINE; HUMANS; MODELS, BIOLOGICAL; TISSUE ENGINEERING;

EID: 84907332980     PISSN: 10107940     EISSN: 1873734X     Source Type: Journal    
DOI: 10.1093/ejcts/ezu242     Document Type: Review

References (78)

1. Langer R, Vacanti J. Tissue engineering. Science 1993;260:920-6.
2. De Kanter R, Olinga P, De Jager MH, Merema MT, Meijer DKF, Groothius GMM. Organ slices as an in vitro test system for drug metabolism in human liver, lung and kidney. Toxicol In Vitro 1999;13:737-44.
3. Henmi C, Nakamura M, Nishiyama Y, Yamaguchi K, Mochizuki S, Takiura K et al. Development of an effective three dimensional fabrication technique using inkjet technology for tissue model samples. In: AATEX 14 Proceedings of 6th World Congress on Alternatives & Animal Use in Life Sciences. Tokyo: Japanese Society for Alternatives to Animal Experiments, 2007;689-92.
4. Risbud MV, Sittinger M. Tissue engineering: advances in in vitro cartilage generation. Trends Biotechnol 2002;20:351-6.
5. Hou N. Tissue-engineered trachea using perfusion-decellularized technique and mesenchymal stem cells in a rabbit model. J Neurol Surg B 2012;73:438-43.
6. Ott HC, Matthiesen TS, Goh S-K, Black LD, Kren SM, Netoff TI et al. Perfusion-decellularized matrix: using nature's platform to engineer a bioartificial heart. Nat Med 2008;14:213-21.
7. Uygun BE, Soto-Gutierrez A, Yagi H, Izamis M-L, Guzzardi MA, Shulman C et al. Organ reengineering through development of a transplantable recellularized liver graft using decellularized liver matrix. Nat Med 2010;16: 814-20.
8. Price AP, England KA, Matson AM, Blazar BR, Panoskaltsis-Mortari A. Development of a decellularized lung bioreactor system for bioengineering the lung: the matrix reloaded. Tissue Eng Part A 2010;16:2581-91.
9. Freyman TM, Yannas IV, Gibson LJ. Cellular materials as porous scaffolds for tissue engineering. Prog Mater Sci 2001;46:273-82.
10. Mikos AG, Temenoff JS. Formation of highly porous biodegradable scaffolds for tissue engineering. Electron J Biotechnol 2000;3:1-6.
11. Lannutti J, Reneker D, Ma T, Tomasko D, Farson D. Electrospinning for tissue engineering scaffolds. Mater Sci Eng C 2007;27:504-9.
12. Sachlos E, Czernuszka JT. Making tissue engineering scaffolds work. Review: the application of solid freeform fabrication technology to the production of tissue engineering scaffolds. Eur Cell Mater 2003;5:29-39.
13. Hoffman AS. Hydrogels for biomedical applications. Adv Drug Deliv Rev 2012;64:18-23.
14. Hunt N, Grover L. Cell encapsulation using biopolymer gels for regenerative medicine. Biotechnol Lett 2010;32:733-42.
15. Nicodemus GD, Bryant SJ. Cell encapsulation in biodegradable hydrogels for tissue engineering applications. Tissue Eng 2008;14:149-65.
16. Lee W, Debasitis JC, Lee VK, Lee J-H, Fischer K, Edminster K et al. Multi-layered culture of human skin fibroblasts and keratinocytes through three-dimensional freeform fabrication. Biomaterials 2009;30:1587-95.
17. Yang EK, Seo YK, Youn HH, Lee DH, Park SN, Park JK. Tissue engineered artificial skin composed of dermis and epidermis. Artif Organs 2000;24:7-17.
18. Benders KEM, Weeren PRv, Badylak SF, Saris DBF, Dhert WJA, Malda J. Extracellular matrix scaffolds for cartilage and bone regeneration. Trends Biotechnol 2013;31:169-76.
19. Temenoff JS, Mikos AG. Review: tissue engineering for regeneration of articular cartilage. Biomaterials 2000;21:431-40.
20. Sabater AL, Guarnieri A, Espana EM, Li W, Prosper F, Moreno-Montanes J. Strategies of human corneal endothelial tissue regeneration. Regen Med 2013;8:183-95.
21. Kuo CK, Li W-J, Mauck RL, Tuan RS. Cartilage tissue engineering: its potential and uses. Curr Opin Rheumatol 2006;18:64-73.
22. Schulz RM, Bader A. Cartilage tissue engineering and bioreactor systems for the cultivation and stimulation of chondrocytes. Eur Biophys J 2007;36: 539-68.
23. Novosel EC, Kleinhans C, Kluger PJ. Vascularization is the key challenge in tissue engineering. Adv Drug Deliv Rev 2011;63:300-11.
24. Tortorra GJD. Anatomie und Physiologie. Weinheim: Wiley-VHC, 2006.
25. Kamiya A, Togawa T. Optimal branching structure of the vascular tree. Bull Math Biophys 1972;34:431-8.
26. Moya ML, Hsu Y-H, Lee AP, Hughes CCW, George SC. In vitro perfused human capillary networks. Tissue Eng Part C Methods 2013;19:730-7.
27. Tremblay PL, Hudon V, Berthod F, Germain L, Auger FA. Inosculation of tissue-engineered capillaries with the host's vasculature in a reconstructed skin transplanted on mice. Am J Transplant 2005;5:1002.
28. Nunes SS, Krishnan L, Gerard CS, Dale JR, Maddie MA, Benton RL et al. Angiogenic potential of microvessel fragments is independent of the tissue of origin and can be influenced by the cellular composition of the implants. Microcirculation 2010;17:557-67.
29. Kannan RY, Salacinski HJ, Sales K, Butler P, Seifalian AM. The roles of tissue engineering and vascularisation in the development of micro-vascular networks: a review. Biomaterials 2005;26:1857-75.
30. Scheller K. Upcyte(R) microvascular endothelial cells repopulate decellularized scaffold. Tissue Eng Part C Methods 2013;19:57-67.
31. Novosel EC, Meyer W, Klechowitz N, Krüger H, Wegener M, Walles H et al. Evaluation of cell-material interactions on newly designed, printable polymers for tissue engineering applications. Adv Eng Mater 2011;13: B467-75.
32. Tsang VL, Bhatia SN. Three-dimensional tissue fabrication. Adv Drug Deliv Rev 2004;56:1635-47.
33. Guillemot F, Mironov V, Nakamura M. Bioprinting is coming of age: report from International Conference on Bioprinting and Biofabrication in Bordeaux (3B'09). Biofabrication 2010;2:1-7.
34. Melchels FPW, Domingos MAN, Klein TJ, Malda J, Bartolo PJ, Hutmacher DW. Additive manufacturing of tissues and organs. Prog Polym Sci 2012; 37:1079-104.
35. Wüst S, Müller R, Hofmann S. Controlled positioning of cells in biomaterials-approaches towards 3D tissue printing. J Funct Biomater 2011;2:119-54.
36. Chang CC, Boland ED, Williams SK, Hoying JB. Direct-write bioprinting three-dimensional biohybrid systems for future regenerative therapies. J Biomed Mater Res B Appl Biomater 2011;98B:160-70.
37. Hoch E, Hirth T, Tovar GEM, Borchers K. Chemical tailoring of gelatin to adjust its chemical and physical properties for functional bioprinting. J Mater Chem B 2013;1:5675-85.
38. Baudis S, Nehl F, Ligon SC, Nigisch A, Bergmeister H, Bernhard D et al. Elastomeric degradable biomaterials by photopolymerization-based CAD-CAM for vascular tissue engineering. Biomed Mater 2011;6:055003.
39. Engelhardt S, Hoch E, Borchers K, Meyer W, Krüger H, Tovar G et al. Fabrication of 2D protein microstructures and 3D polymer-protein hybrid microstructures by two-photon polymerization. Biofabrication 2011;3:025003.
40. Bellan LM, Pearsall M, Cropek DM, Langer R. A 3D interconnected microchannel network formed in gelatin by sacrificial shellac microfibers. Adv Mater 2012;24:5187-91.
41. Miller JS, Stevens KR, Yang MT, Baker BM, Nguyen D-HT, Cohen DM et al. Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues. Nat Mater 2012;11:768-74.
42. Wu W, DeConinck A, Lewis JA. Omnidirectional printing of 3D microvascular networks. Adv Mater 2011;23:H178-83.
43. Lee W, Lee V, Polio S, Keegan P, Lee JH, Fischer K et al. On-demand threedimensional freeform fabrication of multi-layered hydrogel scaffold with fluidic channels. Biotechnol Bioeng 2010;105:1178-86.
44. Li S, Xiong Z, Wang X, Yan Y, Liu H, Zhang J. Direct fabrication of a hybrid cell/hydrogel construct by a double-nozzle assembling technology. J Bioact Compat Polym 2009;24:249-65.
45. Wu PK, Ringeisen BR. Development of human umbilical vein endothelial cell (HUVEC) and human umbilical vein smooth muscle cell (HUVSMC) branch/stem structures on hydrogel layers via biological laser printing (BioLP). Biofabrication 2010;2:014111-119.
46. Guillotin B, Souquet A, Catros S, Duocastella M, Pippenger B, Bellance S et al. Laser assisted bioprinting of engineered tissue with high cell density and microscale organization. Biomaterials 2010;31:7250-6.
47. Cui X, Boland T. Human microvasculature fabrication using thermal inkjet printing technology. Biomaterials 2009;30:6221-7.
48. Chang CC, Krishnan L, Nunes SS, Church KH, Edgar LT, Boland ED et al. Determinants of microvascular network topologies in implanted neovasculatures. Arterioscler Thromb Vasc Biol 2012;32:5-14.
49. Meyer W, Engelhardt S, Novosel E, Elling B, Wegener M, Krüger H. Soft Polymers for building up small and smallest blood supplying systems by stereolithography. J Funct Biomater 2012;3:257-68.
50. Nakamura M, Nishiyama Y, Henmi C. 3D micro-fabrication by inkjet 3D biofabrication for 3D tissue engineering. In: Proceedings of the International Symposium on Micro-NanoMechatronics and Human Science. New York, USA: Institute of Electrical and Electronics Engineers IEEE, 2008;451-6.
51. Nakamura M, Nishiyama Y, Henmi C, Iwanaga S, Nakagawa H. Ink jet three-dimensional digital fabrication for biological tissue manufacturing: analysis of alginate microgel beads produced by ink jet droplets for three dimensional tissue fabrication. J Imaging Sci Technol 2008;52:1-16.
52. Nishiyama Y, Nakamura M, Henmi C, Yamaguchi K, Mochizuki S, Nakagawa H et al. Development of a three-dimensional bioprinter: construction of cell supporting structures using hydrogel and state-of-the-art inkjet technology. J Biomech Eng 2009;131:1-6.
53. Kesari P, Xu T, Boland T. Layer-by-layer printing of cells and its application to tissue engineering. Nanoscale Mater Sci Biol Med 2005;845:111-7.
54. Xu C, Chai W, Huang Y, Markwald RR. Scaffold-free inkjet printing of three-dimensional zigzag cellular tubes. Biotechnol Bioeng 2012;109: 3152-60.
55. Duarte Campos DF, Blaeser A,Weber M, Jäkel J, Neuss S, Jahnen-DechentW et al. Three-dimensional printing of stem cell-laden hydrogels submerged in a hydrophobic high-density fluid. Biofabrication 2013;5:015003-014.
56. Kucukgul C, Ozler B, Karakas HE, Gozuacik D, Koc B. 3D Hybrid bioprinting of macrovascular structures. Proc Eng 2013;59:183-92.
57. Skardal A, Zhang J, McCoard L, Oottamasathien S, Prestwich GD. Dynamically crosslinked gold nanoparticle-hyaluronan hydrogels. Adv Mater 2010;22:4736-40.
58. Skardal A, Zhang J, McCoard L, Xu X, Oottamasathien S, Prestwich GD. Photocrosslinkable hyaluronan-gelatin hydrogels for two-step bioprinting. Tissue Eng Part A 2010;16:2675-85.
59. Skardal A, Zhang J, Prestwich GD. Bioprinting vessel-like constructs using hyaluronan hydrogels crosslinked with tetrahedral polyethylene glycol tetracrylates. Biomaterials 2010;31:6173-81.
60. Visser J, Peters B, Burger TJ, Boomstra J, Dhert WJ, Melchels FP et al. Biofabrication of multi-material anatomically shaped tissue constructs. Biofabrication 2013;5:1-9.
61. Norotte C, Marga FS, Niklason LE, Forgacs G. Scaffold-free vascular tissue engineering using bioprinting. Biomaterials 2009;30:5910-7.
62. Yu Y, Zhang Y, Martin JA, Ozbolat IT. Evaluation of cell viability and functionality in vessel-like bioprintable cell-laden tubular channels. J Biomech Eng 2013;135:91011.
63. Zhang Y, Yu Y, Chen H, Ozbolat IT. Characterization of printable cellular micro-fluidic channels for tissue engineering. Biofabrication 2013;5:025004.
64. Zhang Y, Yu Y, Ozbolat IT. Direct bioprinting of vessel-like tubular microfluidic channels. J Nanotechnol Eng Med 2013;4:021001-1-021001-7.
65. Golden AP, Tien J. Fabrication of microfluidic hydrogels using molded gelatin as a sacrificial element. Lab Chip 2007;7:720-5.
66. Choi NW, Cabodi M, Held B, Gleghorn JP, Bonassar LJ, Stroock AD. Microfluidic scaffolds for tissue engineering. Nat Mater 2007;6:908-15.
67. Ling Y, Rubin J, Deng Y, Huang C, Demirci U, Karp JM et al. A cell-laden microfluidic hydrogel. Lab Chip 2007;7:756-62.
68. Abdi S, Choi J, Lee J, Lim H, Lee C, Kim J et al. In vivo study of a blended hydrogel composed of pluronic F-127-alginate-hyaluronic acid for its cell injection application. Tissue Eng Regen Med 2012;9:1-9.
69. Khattak SF, Bhatia SR, Roberts SC. Pluronic F127 as a cell encapsulation material: utilization of membrane-stabilizing agents. Tissue Eng 2005;11:974-83.
70. Thonhoff JR, Lou DI, Jordan PM, Zhao X, Wu P. Compatibility of human fetal neural stem cells with hydrogel biomaterials in vitro. Brain Res 2008; 1187:42-51.
71. Jakab K, Norotte C, Marga F, Murphy K, Vunjak-Novakovic G, Forgacs G. Tissue engineering by self-assembly and bio-printing of living cells. Biofabrication 2010;2:022001.
72. Cascone I, Giraudo E, Caccavari F, Napione L, Bertotti E, Collard JG et al. Temporal and spatial modulation of Rho GTPases during in vitro formation of capillary vascular network: adherens junctions and myosin light chain as targets of Rac1 and RhoA. J Biol Chem 2003;278:50702-13.
73. Korff T, Kimmina S, Martiny-Baron G, Augustin HG. Blood vessel maturation in a 3-dimensional spheroidal coculture model: direct contact with smooth muscle cells regulates endothelial cell quiescence and abrogates VEGF responsiveness. FASEB J 2001;15:447-57.
74. Darland DC, Massingham LJ, Smith SR, Piek E, Saint-Geniez M, D'Amore PA. Pericyte production of cell-associated VEGF is differentiation-dependent and is associated with endothelial survival. Dev Biol 2003;264:275-88.
75. Schuster M, Turecek C, Kaiser B, Stampfl J, Liska R, Varga F. Evaluation of biocompatible photopolymers I: photoreactivity and mechanical properties of reactive diluents. J Macromol Sci Part A 2007;44:547-57.
76. Nakamura M, Iwanaga S, Henmi C, Arai K, Nishiyama Y. Biomatrices and biomaterials for future developments of bioprinting and biofabrication. Biofabrication 2010;2:014110-116.
77. Kucukgul C, Ozler B, Karakas HE, Gozuacik D, Koc B. 3D hybrid bioprinting of macrovascular structures. Procedia Engineering 2013;59:183-92.
78. Luo Y, Lode A, Gelinsky M. Direct plotting of three-dimensional hollow fiber scaffolds based on concentrated alginate pastes for tissue engineering. Adv Healthcare Mater 2013;2:777-83.