Cardiovascular Engineering and Technology

, Volume 2, Issue 3, pp 137–148

Tissue Engineering of Blood Vessels: Functional Requirements, Progress, and Future Challenges

  • Vivek A. Kumar
  • Luke P. Brewster
  • Jeffrey M. Caves
  • Elliot L. Chaikof
Article

Abstract

Vascular disease results in the decreased utility and decreased availability of autologus vascular tissue for small diameter (<6 mm) vessel replacements. While synthetic polymer alternatives to date have failed to meet the performance of autogenous conduits, tissue-engineered replacement vessels represent an ideal solution to this clinical problem. Ongoing progress requires combined approaches from biomaterials science, cell biology, and translational medicine to develop feasible solutions with the requisite mechanical support, a non-fouling surface for blood flow, and tissue regeneration. Over the past two decades interest in blood vessel tissue engineering has soared on a global scale, resulting in the first clinical implants of multiple technologies, steady progress with several other systems, and critical lessons-learned. This review will highlight the current inadequacies of autologus and synthetic grafts, the engineering requirements for implantation of tissue-engineered grafts, and the current status of tissue-engineered blood vessel research.

Keywords

Vascular tissue engineering Mechanical requirements of blood vessels Biological requirements of blood vessels Stems cells Blood vessels Cardiovascular disease 

References

  1. 1.
    Allen, J., et al. Characterization of porcine circulating progenitor cells: toward a functional endothelium. Tissue Eng. Part A 14(1):183–194, 2008.CrossRefGoogle Scholar
  2. 2.
    Allen, J. B., et al. Toward engineering a human neoendothelium with circulating progenitor cells. Stem Cells 28(2):318–328, 2010.Google Scholar
  3. 3.
    Amarnath, L. P., A. Srinivas, and A. Ramamurthi. In vitro hemocompatibility testing of UV-modified hyaluronan hydrogels. Biomaterials 27(8):1416–1424, 2006.CrossRefGoogle Scholar
  4. 4.
    ANSI/AAMI/ISO. Cardiovascular Implants—Tubular Vascular Prostheses, 2001.Google Scholar
  5. 5.
    Ariganello, M. B., R. S. Labow, and J. M. Lee. In vitro response of monocyte-derived macrophages to a decellularized pericardial biomaterial. J. Biomed. Mater. Res. A 93(1):280–288, 2010.Google Scholar
  6. 6.
    Ariganello, M. B., et al. Macrophage differentiation and polarization on a decellularized pericardial biomaterial. Biomaterials 32(2):439–449, 2011.CrossRefGoogle Scholar
  7. 7.
    Arrigoni, C., D. Camozzi, and A. Remuzzi. Vascular tissue engineering. Cell Transplant. 15(Suppl. 1):S119–S125, 2006.CrossRefGoogle Scholar
  8. 8.
    ASTM Committee F-4 on Medical Surgical, M.D. Vascular Graft Update: Safety and Performance. Philadelphia, PA: ASTM, 1986.Google Scholar
  9. 9.
    Badylak, S. F., et al. Comparison of the resistance to infection of intestinal submucosa arterial autografts versus polytetrafluoroethylene arterial prostheses in a dog model. J. Vasc. Surg. 19(3):465–472, 1994.Google Scholar
  10. 10.
    Ball, S. G., C. A. Shuttleworth, and C. M. Kielty. Mesenchymal stem cells and neovascularization: role of platelet-derived growth factor receptors. J. Cell. Mol. Med. 11(5):1012–1030, 2007.CrossRefGoogle Scholar
  11. 11.
    Bowlin, G. L., et al. The persistence of electrostatically seeded endothelial cells lining a small diameter expanded polytetrafluoroethylene vascular graft. J. Biomater. Appl. 16(2):157–173, 2001.CrossRefGoogle Scholar
  12. 12.
    Byrne, J., P. Feustel, and R. C. Darling, III. Primary closure, routine patching, and eversion endarterectomy: what is the current state of the literature supporting use of these techniques? Semin. Vasc. Surg. 20(4):226–235, 2007.CrossRefGoogle Scholar
  13. 13.
    Campbell, G. R., and J. H. Campbell. Development of tissue engineered vascular grafts. Curr. Pharm. Biotechnol. 8(1):43–50, 2007.CrossRefGoogle Scholar
  14. 14.
    Campbell, J. H., J. L. Efendy, and G. R. Campbell. Novel vascular graft grown within recipient’s own peritoneal cavity. Circ. Res. 85(12):1173–1178, 1999.Google Scholar
  15. 15.
    Campbell, G. R., et al. The peritoneal cavity as a bioreactor for tissue engineering visceral organs: bladder, uterus and vas deferens. J. Tissue Eng. Regen. Med. 2(1):50–60, 2008.CrossRefGoogle Scholar
  16. 16.
    Campoccia, D., et al. Human neutrophil chemokinesis and polarization induced by hyaluronic acid derivatives. Biomaterials 14(15):1135–1139, 1993.CrossRefGoogle Scholar
  17. 17.
    Caves, J. M., et al. The use of microfiber composites of elastin-like protein matrix reinforced with synthetic collagen in the design of vascular grafts. Biomaterials 31(27):7175–7182, 2010.CrossRefGoogle Scholar
  18. 18.
    Chan-Park, M. B., et al. Biomimetic control of vascular smooth muscle cell morphology and phenotype for functional tissue-engineered small-diameter blood vessels. J. Biomed. Mater. Res. A 88(4):1104–1121, 2009.Google Scholar
  19. 19.
    Chaouat, M., et al. The evaluation of a small-diameter polysaccharide-based arterial graft in rats. Biomaterials 27(32):5546–5553, 2006.CrossRefGoogle Scholar
  20. 20.
    Chemla, E. S., and M. Morsy. Randomized clinical trial comparing decellularized bovine ureter with expanded polytetrafluoroethylene for vascular access. Br. J. Surg. 96(1):34–39, 2009.CrossRefGoogle Scholar
  21. 21.
    Cho, S. W., et al. Small-diameter blood vessels engineered with bone marrow-derived cells. Ann. Surg. 241(3):506–515, 2005.CrossRefGoogle Scholar
  22. 22.
    Chuang, T. W., and K. S. Masters. Regulation of polyurethane hemocompatibility and endothelialization by tethered hyaluronic acid oligosaccharides. Biomaterials 30(29):5341–5351, 2009.CrossRefGoogle Scholar
  23. 23.
    Clarke, D. R., et al. Transformation of nonvascular acellular tissue matrices into durable vascular conduits. Ann. Thorac. Surg. 71(5 Suppl.):S433–S436, 2001.CrossRefGoogle Scholar
  24. 24.
    Cummings, C. L., et al. Properties of engineered vascular constructs made from collagen, fibrin, and collagen–fibrin mixtures. Biomaterials 25(17):3699–3706, 2004.CrossRefGoogle Scholar
  25. 25.
    Dahl, S. L., M. E. Vaughn, and L. E. Niklason. An ultrastructural analysis of collagen in tissue engineered arteries. Ann. Biomed. Eng. 35(10):1749–1755, 2007.CrossRefGoogle Scholar
  26. 26.
    Dahl, S. L., et al. Mechanical properties and compositions of tissue engineered and native arteries. Ann. Biomed. Eng. 35(3):348–355, 2007.MathSciNetCrossRefGoogle Scholar
  27. 27.
    Dahl, S. L., et al. Readily available tissue-engineered vascular grafts. Sci. Transl. Med. 3(68):68ra9, 2011.Google Scholar
  28. 28.
    Daniel, J. M., and D. G. Sedding. Circulating smooth muscle progenitor cells in arterial remodeling. J. Mol. Cell. Cardiol. 50(2):273–279, 2011.CrossRefGoogle Scholar
  29. 29.
    Das, N., et al. Results of a seven-year, single-centre experience of the long-term outcomes of bovine ureter grafts used as novel conduits for haemodialysis fistulas. Cardiovasc. Intervent. Radiol. 1–6, 2011.Google Scholar
  30. 30.
    Davis, N. P., et al. Sustained axial loading lengthens arteries in organ culture. Ann. Biomed. Eng. 33(7):867–877, 2005.CrossRefGoogle Scholar
  31. 31.
    Derham, C., et al. Tissue engineering small-diameter vascular grafts: preparation of a biocompatible porcine ureteric scaffold. Tissue Eng. Part A 14(11):1871–1882, 2008.CrossRefGoogle Scholar
  32. 32.
    Deutsch, M., et al. Long-term experience in autologous in vitro endothelialization of infrainguinal ePTFE grafts. J. Vasc. Surg. 49(2):352–362, 2009; discussion 362.CrossRefGoogle Scholar
  33. 33.
    Dorafshar, A. H., et al. Interposition grafts for difficult carotid artery reconstruction: a 17-year experience. Ann. Vasc. Surg. 22(1):63–69, 2008.CrossRefGoogle Scholar
  34. 34.
    Drilling, S., J. Gaumer, and J. Lannutti. Fabrication of burst pressure competent vascular grafts via electrospinning: effects of microstructure. J. Biomed. Mater. Res. A 88(4):923–934, 2009.Google Scholar
  35. 35.
    Ehrbar, M., et al. Cell-demanded liberation of VEGF121 from fibrin implants induces local and controlled blood vessel growth. Circ. Res. 94(8):1124–1132, 2004.CrossRefGoogle Scholar
  36. 36.
    Fernandez, P., and A. R. Bausch. The compaction of gels by cells: a case of collective mechanical activity. Integr. Biol. (Camb.) 1(3):252–259, 2009.CrossRefGoogle Scholar
  37. 37.
    Fidkowski, C., et al. Endothelialized microvasculature based on a biodegradable elastomer. Tissue Eng. 11(1–2):302–309, 2005.CrossRefGoogle Scholar
  38. 38.
    Fitzpatrick, J. C., P. M. Clark, and F. M. Capaldi. Effect of decellularization protocol on the mechanical behavior of porcine descending aorta. Int. J. Biomater. 2010:620503 (11 pp), 2010.Google Scholar
  39. 39.
    Gan, Q., et al. Smooth muscle cells and myofibroblasts use distinct transcriptional mechanisms for smooth muscle alpha-actin expression. Circ. Res. 101(9):883–892, 2007.CrossRefGoogle Scholar
  40. 40.
    Gauvin, R., et al. A novel single-step self-assembly approach for the fabrication of tissue-engineered vascular constructs. Tissue Eng. Part A 16(5):1737–1747, 2010.CrossRefGoogle Scholar
  41. 41.
    Goldstein, L. J., et al. Carotid artery stenting is safe and associated with comparable outcomes in men and women. J. Vasc. Surg. 49(2):315–323, 2009; discussion 323–4.CrossRefGoogle Scholar
  42. 42.
    Gong, Z., and L. E. Niklason. Small-diameter human vessel wall engineered from bone marrow-derived mesenchymal stem cells (hMSCs). FASEB J. 22(6):1635–1648, 2008.CrossRefGoogle Scholar
  43. 43.
    Gong, Z., et al. Influence of culture medium on smooth muscle cell differentiation from human bone marrow-derived mesenchymal stem cells. Tissue Eng. Part A 15(2):319–330, 2009.CrossRefGoogle Scholar
  44. 44.
    Goodman, S. L. Sheep, pig, and human platelet–material interactions with model cardiovascular biomaterials. J. Biomed. Mater. Res. 45(3):240–250, 1999.CrossRefGoogle Scholar
  45. 45.
    Gotherstrom, C. Immunomodulation by multipotent mesenchymal stromal cells. Transplantation 84(1 Suppl.):S35–S37, 2007.CrossRefGoogle Scholar
  46. 46.
    Grassl, E. D., T. R. Oegema, and R. T. Tranquillo. Fibrin as an alternative biopolymer to type-I collagen for the fabrication of a media equivalent. J. Biomed. Mater. Res. 60(4):607–612, 2002.CrossRefGoogle Scholar
  47. 47.
    Greenwald, S. E., and C. L. Berry. Improving vascular grafts: the importance of mechanical and haemodynamic properties. J. Pathol. 190(3):292–299, 2000.CrossRefGoogle Scholar
  48. 48.
    Gui, L., et al. Development of decellularized human umbilical arteries as small-diameter vascular grafts. Tissue Eng. Part A 15(9):2665–2676, 2009.CrossRefGoogle Scholar
  49. 49.
    Han, H. C., D. N. Ku, and R. P. Vito. Arterial wall adaptation under elevated longitudinal stretch in organ culture. Ann. Biomed. Eng. 31(4):403–411, 2003.CrossRefGoogle Scholar
  50. 50.
    Hancock, W. W. Delayed xenograft rejection. World J. Surg. 21(9):917–923, 1997.CrossRefGoogle Scholar
  51. 51.
    Hashi, C. K., et al. Antithrombogenic property of bone marrow mesenchymal stem cells in nanofibrous vascular grafts. Proc. Natl Acad. Sci. USA 104(29):11915–11920, 2007.CrossRefGoogle Scholar
  52. 52.
    He, W., et al. Tubular nanofiber scaffolds for tissue engineered small-diameter vascular grafts. J. Biomed. Mater. Res. A 90(1):205–216, 2009.Google Scholar
  53. 53.
    Heidenhain, C., et al. Polymer coating of porcine decellularized and cross-linked aortic grafts. J. Biomed. Mater. Res. B Appl. Biomater. 94(1):256–263, 2010.Google Scholar
  54. 54.
    Hjortnaes, J., et al. Intravital molecular imaging of small-diameter tissue-engineered vascular grafts in mice: a feasibility study. Tissue Eng. Part C Methods 16(4):597–607, 2010.CrossRefGoogle Scholar
  55. 55.
    Hong, Y., et al. A small diameter, fibrous vascular conduit generated from a poly(ester urethane)urea and phospholipid polymer blend. Biomaterials 30(13):2457–2467, 2009.CrossRefGoogle Scholar
  56. 56.
    Isaka, M., et al. Experimental study on stability of a high-porosity expanded polytetrafluoroethylene graft in dogs. Ann. Thorac. Cardiovasc. Surg. 12(1):37–41, 2006.Google Scholar
  57. 57.
    Isenberg, B. C., and R. T. Tranquillo. Long-term cyclic distention enhances the mechanical properties of collagen-based media-equivalents. Ann. Biomed. Eng. 31(8):937–949, 2003.CrossRefGoogle Scholar
  58. 58.
    Iwakura, A., et al. Estrogen-mediated, endothelial nitric oxide synthase-dependent mobilization of bone marrow-derived endothelial progenitor cells contributes to reendothelialization after arterial injury. Circulation 108(25):3115–3121, 2003.CrossRefGoogle Scholar
  59. 59.
    Iwasaki, K., et al. Bioengineered three-layered robust and elastic artery using hemodynamically-equivalent pulsatile bioreactor. Circulation 118(14 Suppl.):S52–S57, 2008.CrossRefGoogle Scholar
  60. 60.
    Jiang, Z., et al. Established neointimal hyperplasia in vein grafts expands via TGF-beta-mediated progressive fibrosis. Am. J. Physiol. Heart Circ. Physiol. 297(4):H1200–H1207, 2009.CrossRefGoogle Scholar
  61. 61.
    Jorgensen, C. Mesenchymal stem cells immunosuppressive properties: is it specific to bone marrow-derived cells? Stem Cell Res. Ther. 1(2):15, 2010.CrossRefGoogle Scholar
  62. 62.
    Kaushiva, A., et al. A biodegradable vascularizing membrane: a feasibility study. Acta Biomater. 3(5):631–642, 2007.CrossRefGoogle Scholar
  63. 63.
    Kibbe, M. R., et al. Citric acid-based elastomers provide a biocompatible interface for vascular grafts. J. Biomed. Mater. Res. A 93(1):314–324, 2010.Google Scholar
  64. 64.
    Kielty, C. M., et al. Applying elastic fibre biology in vascular tissue engineering. Philos. Trans. R. Soc. Lond. B Biol. Sci. 362(1484):1293–1312, 2007.CrossRefGoogle Scholar
  65. 65.
    Klinger, R. Y., et al. Relevance and safety of telomerase for human tissue engineering. Proc. Natl Acad. Sci. USA 103(8):2500–2505, 2006.CrossRefGoogle Scholar
  66. 66.
    Konig, G., et al. Mechanical properties of completely autologous human tissue engineered blood vessels compared to human saphenous vein and mammary artery. Biomaterials 30(8):1542–1550, 2009.CrossRefGoogle Scholar
  67. 67.
    Ku, D. N., and D. P. Giddens. Pulsatile flow in a model carotid bifurcation. Arteriosclerosis 3(1):31–39, 1983.CrossRefGoogle Scholar
  68. 68.
    Ku, D. N., et al. Hemodynamics of the normal human carotid bifurcation: in vitro and in vivo studies. Ultrasound Med. Biol. 11(1):13–26, 1985.CrossRefGoogle Scholar
  69. 69.
    Ku, D. N., et al. Pulsatile flow and atherosclerosis in the human carotid bifurcation. Positive correlation between plaque location and low oscillating shear stress. Arteriosclerosis 5(3):293–302, 1985.CrossRefGoogle Scholar
  70. 70.
    Laurent, S., et al. Carotid artery distensibility and distending pressure in hypertensive humans. Hypertension 23(6 Pt 2):878–883, 1994.Google Scholar
  71. 71.
    Lee, M. H., et al. Considerations for tissue-engineered and regenerative medicine product development prior to clinical trials in the United States. Tissue Eng. Part B Rev. 16(1):41–54, 2010.CrossRefGoogle Scholar
  72. 72.
    L’Heureux, N., T. N. McAllister, and L. M. de la Fuente. Tissue-engineered blood vessel for adult arterial revascularization. N. Engl. J. Med. 357(14):1451–1453, 2007.CrossRefGoogle Scholar
  73. 73.
    L’Heureux, N., et al. A completely biological tissue-engineered human blood vessel. FASEB J. 12(1):47–56, 1998.Google Scholar
  74. 74.
    L’Heureux, N., et al. Human tissue-engineered blood vessels for adult arterial revascularization. Nat. Med. 12(3):361–365, 2006.CrossRefGoogle Scholar
  75. 75.
    L’Heureux, N., et al. Technology insight: the evolution of tissue-engineered vascular grafts—from research to clinical practice. Nat. Clin. Pract. Cardiovasc. Med. 4(7):389–395, 2007.CrossRefGoogle Scholar
  76. 76.
    Li, C., A. Hill, and M. Imran. In vitro and in vivo studies of ePTFE vascular grafts treated with P15 peptide. J. Biomater. Sci. Polym. Ed. 16(7):875–891, 2005.CrossRefGoogle Scholar
  77. 77.
    Liu, J. Y., et al. Functional tissue-engineered blood vessels from bone marrow progenitor cells. Cardiovasc. Res. 75(3):618–628, 2007.CrossRefGoogle Scholar
  78. 78.
    Liu, G. F., et al. Decellularized aorta of fetal pigs as a potential scaffold for small diameter tissue engineered vascular graft (Engl). Chin. Med. J. 121(15):1398–1406, 2008.Google Scholar
  79. 79.
    Lloyd-Jones, D., et al. Heart disease and stroke statistics—2010 update: a report from the American Heart Association. Circulation 121(7):e46–e215, 2010.CrossRefGoogle Scholar
  80. 80.
    Long, J. L., and R. T. Tranquillo. Elastic fiber production in cardiovascular tissue-equivalents. Matrix Biol. 22(4):339–350, 2003.CrossRefGoogle Scholar
  81. 81.
    Lopez-Soler, R. I., et al. Development of a mouse model for evaluation of small diameter vascular grafts. J. Surg. Res. 139(1):1–6, 2007.CrossRefGoogle Scholar
  82. 82.
    Lund, A. W., J. P. Stegemann, and G. E. Plopper. Inhibition of ERK promotes collagen gel compaction and fibrillogenesis to amplify the osteogenesis of human mesenchymal stem cells in three-dimensional collagen I culture. Stem Cells Dev. 18(2):331–341, 2009.CrossRefGoogle Scholar
  83. 83.
    Matsumura, G., et al. First evidence that bone marrow cells contribute to the construction of tissue-engineered vascular autografts in vivo. Circulation 108(14):1729–1734, 2003.CrossRefGoogle Scholar
  84. 84.
    McAllister, T. N., et al. Cell-based therapeutics from an economic perspective: primed for a commercial success or a research sinkhole? Regen. Med. 3(6):925–937, 2008.CrossRefGoogle Scholar
  85. 85.
    McAllister, T. N., et al. Effectiveness of haemodialysis access with an autologous tissue-engineered vascular graft: a multicentre cohort study. Lancet 373(9673):1440–1446, 2009.CrossRefGoogle Scholar
  86. 86.
    McKee, J. A., et al. Human arteries engineered in vitro. EMBO Rep. 4(6):633–638, 2003.CrossRefGoogle Scholar
  87. 87.
    Meinhart, J., M. Deutsch, and P. Zilla. Eight years of clinical endothelial cell transplantation. Closing the gap between prosthetic grafts and vein grafts. ASAIO J. 43(5):M515–M521, 1997.CrossRefGoogle Scholar
  88. 88.
    Mine, Y., et al. Suture retention strength of expanded polytetrafluoroethylene (ePTFE) graft. Acta Med. Okayama 64(2):121–128, 2010.Google Scholar
  89. 89.
    Mirensky, T. L., et al. Tissue-engineered arterial grafts: long-term results after implantation in a small animal model. J. Pediatr. Surg. 44(6):1127–1132, 2009; discussion 1132–3.CrossRefGoogle Scholar
  90. 90.
    Mitchell, S. L., and L. E. Niklason. Requirements for growing tissue-engineered vascular grafts. Cardiovasc. Pathol. 12(2):59–64, 2003.CrossRefGoogle Scholar
  91. 91.
    Motlagh, D., et al. Hemocompatibility evaluation of poly(glycerol-sebacate) in vitro for vascular tissue engineering. Biomaterials 27(24):4315–4324, 2006.CrossRefGoogle Scholar
  92. 92.
    Motlagh, D., et al. Hemocompatibility evaluation of poly(diol citrate) in vitro for vascular tissue engineering. J. Biomed. Mater. Res. A 82(4):907–916, 2007.Google Scholar
  93. 93.
    Narita, Y., et al. Decellularized ureter for tissue-engineered small-caliber vascular graft. J. Artif. Organs 11(2):91–99, 2008.MathSciNetCrossRefGoogle Scholar
  94. 94.
    Neff, L. P., et al. Vascular smooth muscle enhances functionality of tissue-engineered blood vessels in vivo. J. Vasc. Surg. 53(2):426–434, 2011.CrossRefGoogle Scholar
  95. 95.
    Nieponice, A., et al. Development of a tissue-engineered vascular graft combining a biodegradable scaffold, muscle-derived stem cells and a rotational vacuum seeding technique. Biomaterials 29(7):825–833, 2008.CrossRefGoogle Scholar
  96. 96.
    Niklason, L. E. Techview: medical technology. Replacement arteries made to order. Science 286(5444):1493–1494, 1999.CrossRefGoogle Scholar
  97. 97.
    Niklason, L. E., et al. Functional arteries grown in vitro. Science 284(5413):489–493, 1999.CrossRefGoogle Scholar
  98. 98.
    Noel, D., et al. Multipotent mesenchymal stromal cells and immune tolerance. Leuk. Lymphoma 48(7):1283–1289, 2007.CrossRefGoogle Scholar
  99. 99.
    Opitz, F., et al. Tissue engineering of aortic tissue: dire consequence of suboptimal elastic fiber synthesis in vivo. Cardiovasc. Res. 63(4):719–730, 2004.CrossRefGoogle Scholar
  100. 100.
    Owens, G. K. Regulation of differentiation of vascular smooth muscle cells. Physiol. Rev. 75(3):487–517, 1995.Google Scholar
  101. 101.
    Owens, G. K. Role of mechanical strain in regulation of differentiation of vascular smooth muscle cells. Circ. Res. 79(5):1054–1055, 1996.Google Scholar
  102. 102.
    Owens, G. K. Molecular control of vascular smooth muscle cell differentiation and phenotypic plasticity. Novartis Found Symp. 283:174–191, 2007; discussion 191–3, 238–41.CrossRefGoogle Scholar
  103. 103.
    Pektok, E., et al. Degradation and healing characteristics of small-diameter poly(epsilon-caprolactone) vascular grafts in the rat systemic arterial circulation. Circulation 118(24):2563–2570, 2008.CrossRefGoogle Scholar
  104. 104.
    Petersen, T. H., et al. Utility of telomerase-pot1 fusion protein in vascular tissue engineering. Cell Transplant. 19(1):79–87, 2010.CrossRefGoogle Scholar
  105. 105.
    Poh, M., et al. Blood vessels engineered from human cells. Lancet 365(9477):2122–2124, 2005.CrossRefGoogle Scholar
  106. 106.
    Qi, J., et al. Modulation of collagen gel compaction by extracellular ATP is MAPK and NF-kappaB pathways dependent. Exp. Cell Res. 315(11):1990–2000, 2009.CrossRefGoogle Scholar
  107. 107.
    Quillard, T., et al. Impaired Notch4 activity elicits endothelial cell activation and apoptosis: implication for transplant arteriosclerosis. Arterioscler. Thromb. Vasc. Biol. 28(12):2258–2265, 2008.CrossRefGoogle Scholar
  108. 108.
    Rachev, A., Z. Dominguez, and R. Vito. System and method for investigating arterial remodeling. J. Biomech. Eng. 131:104501, 2009.CrossRefGoogle Scholar
  109. 109.
    Ravi, S., Z. Qu, and E. L. Chaikof. Polymeric materials for tissue engineering of arterial substitutes. Vascular 17(Suppl. 1):S45–S54, 2009.CrossRefGoogle Scholar
  110. 110.
    Roeder, R., et al. Compliance, elastic modulus, and burst pressure of small-intestine submucosa (SIS), small-diameter vascular grafts. J. Biomed. Mater. Res. 47(1):65–70, 1999.CrossRefGoogle Scholar
  111. 111.
    Roh, J. D., et al. Tissue-engineered vascular grafts transform into mature blood vessels via an inflammation-mediated process of vascular remodeling. Proc. Natl Acad. Sci. USA 107(10):4669–4674, 2010.CrossRefGoogle Scholar
  112. 112.
    Salem, H. K., and C. Thiemermann. Mesenchymal stromal cells: current understanding and clinical status. Stem Cells 28(3):585–596, 2010.Google Scholar
  113. 113.
    Salom, R. N., J. A. Maguire, and W. W. Hancock. Endothelial activation and cytokine expression in human acute cardiac allograft rejection. Pathology 30(1):24–29, 1998.CrossRefGoogle Scholar
  114. 114.
    Sandusky, G. E., G. C. Lantz, and S. F. Badylak. Healing comparison of small intestine submucosa and ePTFE grafts in the canine carotid artery. J. Surg. Res. 58(4):415–420, 1995.CrossRefGoogle Scholar
  115. 115.
    Sarkar, S., et al. Critical parameter of burst pressure measurement in development of bypass grafts is highly dependent on methodology used. J. Vasc. Surg. 44(4):846–852, 2006.CrossRefGoogle Scholar
  116. 116.
    Sarkar, S., et al. The mechanical properties of infrainguinal vascular bypass grafts: their role in influencing patency. Eur. J. Vasc. Endovasc. Surg. 31(6):627–636, 2006.CrossRefGoogle Scholar
  117. 117.
    Sarkar, S., et al. Addressing thrombogenicity in vascular graft construction. J. Biomed. Mater. Res. B Appl. Biomater. 82(1):100–108, 2007.Google Scholar
  118. 118.
    Schaner, P. J., et al. Decellularized vein as a potential scaffold for vascular tissue engineering. J. Vasc. Surg. 40(1):146–153, 2004.CrossRefGoogle Scholar
  119. 119.
    Seliktar, D., et al. Dynamic mechanical conditioning of collagen–gel blood vessel constructs induces remodeling in vitro. Ann. Biomed. Eng. 28(4):351–362, 2000.CrossRefGoogle Scholar
  120. 120.
    Sell, S. A., et al. Electrospun polydioxanone-elastin blends: potential for bioresorbable vascular grafts. Biomed. Mater. 1(2):72–80, 2006.MathSciNetCrossRefGoogle Scholar
  121. 121.
    Sell, S. A., et al. Electrospinning of collagen/biopolymers for regenerative medicine and cardiovascular tissue engineering. Adv. Drug Deliv. Rev. 61(12):1007–1019, 2009.CrossRefGoogle Scholar
  122. 122.
    Shaikh, F. M., et al. Fibrin: a natural biodegradable scaffold in vascular tissue engineering. Cells Tissues Organs 188(4):333–346, 2008.CrossRefGoogle Scholar
  123. 123.
    Sharp, M. A., et al. A cautionary case: the SynerGraft vascular prosthesis. Eur. J. Vasc. Endovasc. Surg. 27(1):42–44, 2004.CrossRefGoogle Scholar
  124. 124.
    Shaw, J. A., et al. Determinants of coronary artery compliance in subjects with and without angiographic coronary artery disease. J. Am. Coll. Cardiol. 39(10):1637–1643, 2002.CrossRefGoogle Scholar
  125. 125.
    Shi, Y., et al. Mesenchymal stem cells: a new strategy for immunosuppression and tissue repair. Cell Res. 20(5):510–518, 2010.CrossRefGoogle Scholar
  126. 126.
    Shin’oka, T., Y. Imai, and Y. Ikada. Transplantation of a tissue-engineered pulmonary artery. N. Engl. J. Med. 344(7):532–533, 2001.CrossRefGoogle Scholar
  127. 127.
    Shin’oka, T., et al. Midterm clinical result of tissue-engineered vascular autografts seeded with autologous bone marrow cells. J. Thorac. Cardiovasc. Surg. 129(6):1330–1338, 2005.CrossRefGoogle Scholar
  128. 128.
    Solan, A., S. L. Dahl, and L. E. Niklason. Effects of mechanical stretch on collagen and cross-linking in engineered blood vessels. Cell Transplant. 18(8):915–921, 2009.CrossRefGoogle Scholar
  129. 129.
    Soletti, L., et al. A bilayered elastomeric scaffold for tissue engineering of small diameter vascular grafts. Acta Biomater. 6(1):110–122, 2010.CrossRefGoogle Scholar
  130. 130.
    Soletti, L., et al. A bilayered elastomeric scaffold for tissue engineering of small diameter vascular grafts. Acta Biomater. 6(1):110–122, 2010.CrossRefGoogle Scholar
  131. 131.
    Spark, J. I., et al. Incomplete cellular depopulation may explain the high failure rate of bovine ureteric grafts. Br. J. Surg. 95(5):582–585, 2008.CrossRefGoogle Scholar
  132. 132.
    Stekelenburg, M., et al. Dynamic straining combined with fibrin gel cell seeding improves strength of tissue-engineered small-diameter vascular grafts. Tissue Eng. Part A 15(5):1081–1089, 2009.CrossRefGoogle Scholar
  133. 133.
    Sussman, M. A. Showing up isn’t enough for vascularization: persistence is essential. Circ. Res. 103(11):1200–1201, 2008.CrossRefGoogle Scholar
  134. 134.
    Sutherland, K., et al. Degradation of biomaterials by phagocyte-derived oxidants. J. Clin. Invest. 92(5):2360–2367, 1993.CrossRefGoogle Scholar
  135. 135.
    Swartz, D. D., J. A. Russell, and S. T. Andreadis. Engineering of fibrin-based functional and implantable small-diameter blood vessels. Am. J. Physiol. Heart Circ. Physiol. 288(3):H1451–H1460, 2005.CrossRefGoogle Scholar
  136. 136.
    Syedain, Z. H., et al. Implantable arterial grafts from human fibroblasts and fibrin using a multi-graft pulsed flow-stretch bioreactor with noninvasive strength monitoring. Biomaterials 32(3):714–722, 2010.CrossRefGoogle Scholar
  137. 137.
    Tai, N. R., et al. In vivo femoropopliteal arterial wall compliance in subjects with and without lower limb vascular disease. J. Vasc. Surg. 30(5):936–945, 1999.MathSciNetCrossRefGoogle Scholar
  138. 138.
    Tai, N. R., et al. Compliance properties of conduits used in vascular reconstruction. Br. J. Surg. 87(11):1516–1524, 2000.CrossRefGoogle Scholar
  139. 139.
    Timaran, C. H., et al. Trends and outcomes of concurrent carotid revascularization and coronary bypass. J. Vasc. Surg. 48(2):355–360, 2008; discussion 360–1.CrossRefGoogle Scholar
  140. 140.
    Torikai, K., et al. A self-renewing, tissue-engineered vascular graft for arterial reconstruction. J. Thorac. Cardiovasc. Surg. 136(1):37–45, 45 e1 2008.CrossRefGoogle Scholar
  141. 141.
    Uccelli, A., V. Pistoia, and L. Moretta. Mesenchymal stem cells: a new strategy for immunosuppression? Trends Immunol. 28(5):219–226, 2007.CrossRefGoogle Scholar
  142. 142.
    Urbich, C., and S. Dimmeler. Endothelial progenitor cells: characterization and role in vascular biology. Circ. Res. 95(4):343–353, 2004.CrossRefGoogle Scholar
  143. 143.
    van Andel, C. J., P. V. Pistecky, and C. Borst. Mechanical properties of porcine and human arteries: implications for coronary anastomotic connectors. Ann. Thorac. Surg. 76(1):58–64, 2003; discussion 64–5.CrossRefGoogle Scholar
  144. 144.
    Villalona, G. A., et al. Cell-seeding techniques in vascular tissue engineering. Tissue Eng. Part B Rev. 16(3):341–350, 2010.CrossRefGoogle Scholar
  145. 145.
    Wagenseil, J. E., and R. P. Mecham. Vascular extracellular matrix and arterial mechanics. Physiol. Rev. 89(3):957–989, 2009.CrossRefGoogle Scholar
  146. 146.
    Walter, D. H., et al. Statin therapy accelerates reendothelialization: a novel effect involving mobilization and incorporation of bone marrow-derived endothelial progenitor cells. Circulation 105(25):3017–3024, 2002.CrossRefGoogle Scholar
  147. 147.
    Wang, C., et al. A new vascular prosthesis coated with polyamino-acid urethane copolymer (PAU) to enhance endothelialization. J. Biomed. Mater. Res. 62(3):315–322, 2002.CrossRefGoogle Scholar
  148. 148.
    Wang, S., et al. Fabrication and properties of the electrospun polylactide/silk fibroin–gelatin composite tubular scaffold. Biomacromolecules 10(8):2240–2244, 2009.CrossRefGoogle Scholar
  149. 149.
    Wayman, B. H., et al. Arteries respond to independent control of circumferential and shear stress in organ culture. Ann. Biomed. Eng. 36(5):673–684, 2008.CrossRefGoogle Scholar
  150. 150.
    Webb, A. R., et al. In vitro characterization of a compliant biodegradable scaffold with a novel bioreactor system. Ann. Biomed. Eng. 35(8):1357–1367, 2007.CrossRefGoogle Scholar
  151. 151.
    Weinberg, C. B., and E. Bell. A blood vessel model constructed from collagen and cultured vascular cells. Science 231(4736):397–400, 1986.CrossRefGoogle Scholar
  152. 152.
    Werner, N., et al. Intravenous transfusion of endothelial progenitor cells reduces neointima formation after vascular injury. Circ. Res. 93(2):e17–e24, 2003.CrossRefGoogle Scholar
  153. 153.
    Wise, S. G., et al. A multilayered synthetic human elastin/polycaprolactone hybrid vascular graft with tailored mechanical properties. Acta Biomater. 7(1):295–303, 2011.CrossRefGoogle Scholar
  154. 154.
    Wolfe, P. S., et al. Evaluation of thrombogenic potential of electrospun bioresorbable vascular graft materials: acute monocyte tissue factor expression. J. Biomed. Mater. Res. A 92(4):1321–1328, 2010.MathSciNetGoogle Scholar
  155. 155.
    Wootton, D. M., and D. N. Ku. Fluid mechanics of vascular systems, diseases, and thrombosis. Annu. Rev. Biomed. Eng. 1:299–329, 1999.CrossRefGoogle Scholar
  156. 156.
    Yazdani, S. K., et al. Smooth muscle cell seeding of decellularized scaffolds: the importance of bioreactor preconditioning to development of a more native architecture for tissue-engineered blood vessels. Tissue Eng. Part A 15(4):827–840, 2009.CrossRefGoogle Scholar
  157. 157.
    Yow, K. H., et al. Tissue engineering of vascular conduits. Br. J. Surg. 93(6):652–661, 2006.CrossRefGoogle Scholar
  158. 158.
    Yu, X. X., C. X. Wan, and H. Q. Chen. Preparation and endothelialization of decellularised vascular scaffold for tissue-engineered blood vessel. J. Mater. Sci. Mater. Med. 19(1):319–326, 2008.CrossRefGoogle Scholar
  159. 159.
    Zaucha, M. T., et al. A novel cylindrical biaxial computer-controlled bioreactor and biomechanical testing device for vascular tissue engineering. Tissue Eng. Part A 15(11):3331–3340, 2009.CrossRefGoogle Scholar
  160. 160.
    Zetrenne, E., et al. Prosthetic vascular graft infection: a multi-center review of surgical management. Yale J. Biol. Med. 80(3):113–121, 2007.Google Scholar
  161. 161.
    Zhang, X., V. Thomas, and Y. K. Vohra. In vitro biodegradation of designed tubular scaffolds of electrospun protein/polyglyconate blend fibers. J. Biomed. Mater. Res. B Appl. Biomater. 89(1):135–147, 2009.Google Scholar
  162. 162.
    Zhang, W. J., et al. Tissue engineering of blood vessel. J. Cell. Mol. Med. 11(5):945–957, 2007.CrossRefGoogle Scholar
  163. 163.
    Zhang, L., et al. A novel small-diameter vascular graft: in vivo behavior of biodegradable three-layered tubular scaffolds. Biotechnol. Bioeng. 99(4):1007–1015, 2008.CrossRefGoogle Scholar
  164. 164.
    Zhou, M., et al. Constructing a small-diameter decellularized vascular graft pre-loaded with bFGF. Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi 22(3):370–375, 2008.Google Scholar
  165. 165.
    Zhou, M., et al. Development and validation of small-diameter vascular tissue from a decellularized scaffold coated with heparin and vascular endothelial growth factor. Artif. Organs 33(3):230–239, 2009.CrossRefGoogle Scholar
  166. 166.
    Zhou, M., et al. Beneficial effects of granulocyte-colony stimulating factor on small-diameter heparin immobilized decellularized vascular graft. J. Biomed. Mater. Res. A 95(2):600–610, 2010.Google Scholar
  167. 167.
    Ziegler, T., and R. M. Nerem. Tissue engineering a blood vessel: regulation of vascular biology by mechanical stresses. J. Cell. Biochem. 56(2):204–209, 1994.CrossRefGoogle Scholar
  168. 168.
    Zilla, P., D. Bezuidenhout, and P. Human. Prosthetic vascular grafts: wrong models: wrong questions and no healing. Biomaterials 28(34):5009–5027, 2007.CrossRefGoogle Scholar
  169. 169.
    Zilla, P., M. Deutsch, and J. Meinhart. Endothelial cell transplantation. Semin. Vasc. Surg. 12(1):52–63, 1999.Google Scholar
  170. 170.
    Zorlutuna, P., A. Elsheikh, and V. Hasirci. Nanopatterning of collagen scaffolds improve the mechanical properties of tissue engineered vascular grafts. Biomacromolecules 10(4):814–821, 2009.CrossRefGoogle Scholar

Copyright information

© Biomedical Engineering Society 2011

Authors and Affiliations

  • Vivek A. Kumar
    • 1
  • Luke P. Brewster
    • 2
  • Jeffrey M. Caves
    • 3
  • Elliot L. Chaikof
    • 1
    • 2
    • 3
    • 4
  1. 1.Department of Biomedical EngineeringGeorgia Institute of Technology/Emory UniversityAtlantaUSA
  2. 2.Department of SurgeryEmory UniversityAtlantaUSA
  3. 3.Department of SurgeryHarvard Medical School, Beth Israel Deaconess Medical CenterBostonUSA
  4. 4.Wyss Institute of Biologically Inspired EngineeringHarvard UniversityBostonUSA

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