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Autologous Mandril-Based Vascular Grafts

  • Wouter J. GeelhoedEmail author
  • Lorenzo Moroni
  • Joris I. Rotmans
Living reference work entry
Part of the Reference Series in Biomedical Engineering book series (RSBE)

Abstract

It is well-known that the number of patients requiring a vascular graft for use as arterial bypass or as vascular access site for hemodialysis is ever increasing. The development of tissue-engineered vascular grafts (TEVGs) is a promising method to meet this increasing demand, without having to rely synthetic grafts such as polytetrafluoroethylene (PTFE) or Dacron, that have limited long-term durability. The generation of in vivo TEVGs involves utilizing the host reaction to an implanted biomaterial for the generation of completely autologous tissues. Essentially this approach to the development of TEVGs makes use of the foreign body response to biomaterials for the construction of the entire vascular replacement tissue within the patient’s own body. In this review we will discuss the method of developing in vivo TEVGs and debate the approaches of several research groups that have implemented this method.

This review is partly based on a previous publication in the Journal of Cardiovascular Translational Research (2017, 10(2):167–179) and includes an update with recent literature.

Notes

Conflicts of Interest

The authors have no conflicts of interest to disclose.

Ethical Approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Abbott WM, Megerman J, Hasson JE, L'Italien G, Warnock DF (1987) Effect of compliance mismatch on vascular graft patency. J Vasc Surg 5:376–382CrossRefGoogle Scholar
  2. Anderson JM, Rodriguez A, Chang DT (2008) Foreign body reaction to biomaterials. Semin Immunol 20:86–100.  https://doi.org/10.1016/j.smim.2007.11.004CrossRefGoogle Scholar
  3. Aslam S, Vaida F, Ritter M, Mehta RL (2014) Systematic review and meta-analysis on management of hemodialysis catheter-related bacteremia. J Am Soc Nephrol 25:2927–2941.  https://doi.org/10.1681/asn.2013091009CrossRefGoogle Scholar
  4. Bambrah RK, Pham DC, Rana F (2013) Argatroban in heparin-induced thrombocytopenia: rationale for use and place in therapy. Therapeutic Adv Chronic Disease 4:302–304.  https://doi.org/10.1177/2040622313494987CrossRefGoogle Scholar
  5. Bezhaeva T et al (2018) Contribution of bone marrow-derived cells to in situ engineered tissue capsules in a rat model of chronic kidney disease. Biomaterials 194:47–56.  https://doi.org/10.1016/j.biomaterials.2018.12.014CrossRefGoogle Scholar
  6. Bootle-Wilbraham CA, Tazzyman S, Thompson WD, Stirk CM, Lewis CE (2001) Fibrin fragment E stimulates the proliferation, migration and differentiation of human microvascular endothelial cells in vitro. Angiogenesis 4:269–275CrossRefGoogle Scholar
  7. Brem H, Tomic-Canic M (2007) Cellular and molecular basis of wound healing in diabetes. J Clin Investig 117:1219–1222.  https://doi.org/10.1172/JCI32169CrossRefGoogle Scholar
  8. Brouty-Boye D, Pottin-Clemenceau C, Doucet C, Jasmin C, Azzarone B (2000) Chemokines and CD40 expression in human fibroblasts. Eur J Immunol 30:914–919.  https://doi.org/10.1002/1521-4141(200003)30:3<914::aid-immu914>3.0.co;2-dCrossRefGoogle Scholar
  9. Byrom MJ, Bannon PG, White GH, Ng MK (2010) Animal models for the assessment of novel vascular conduits. J Vasc Surg 52:176–195.  https://doi.org/10.1016/j.jvs.2009.10.080CrossRefGoogle Scholar
  10. Campbell GR, Campbell JH (2007) Development of tissue engineered vascular grafts. Curr Pharm Biotechnol 8:43–50CrossRefGoogle Scholar
  11. Campbell JH, Efendy JL, Campbell GR (1999) Novel vascular graft grown within recipient’s own peritoneal cavity. Circ Res 85:1173–1178CrossRefGoogle Scholar
  12. Chue WL et al (2004) Dog peritoneal and pleural cavities as bioreactors to grow autologous vascular grafts. J Vasc Surg 39:859–867.  https://doi.org/10.1016/j.jvs.2003.03.003CrossRefGoogle Scholar
  13. Cummings I et al (2012) Tissue-engineered vascular graft remodeling in a growing lamb model: expression of matrix metalloproteinases. Eur J Cardiothorac Surg 41:167–172.  https://doi.org/10.1016/j.ejcts.2011.02.077CrossRefGoogle Scholar
  14. Damanik FF, Rothuizen TC, van Blitterswijk C, Rotmans JI, Moroni L (2014) Towards an in vitro model mimicking the foreign body response: tailoring the surface properties of biomaterials to modulate extracellular matrix. Sci Rep 4:6325.  https://doi.org/10.1038/srep06325CrossRefGoogle Scholar
  15. Dao H Jr, Kazin RA (2007) Gender differences in skin: a review of the literature. Gend Med 4:308–328CrossRefGoogle Scholar
  16. Duffield JS, Lupher M, Thannickal VJ, Wynn TA (2013) Host responses in tissue repair and fibrosis. Annu Rev Pathol Mech Dis 8:241–276.  https://doi.org/10.1146/annurev-pathol-020712-163930CrossRefGoogle Scholar
  17. Farndale RW, Sixma JJ, Barnes MJ, de Groot PG (2004) The role of collagen in thrombosis and hemostasis. J Thromb Haemost 2:561–573.  https://doi.org/10.1111/j.1538-7836.2004.00665.xCrossRefGoogle Scholar
  18. Furukoshi M, Moriwaki T, Nakayama Y (2016) Development of an in vivo tissue-engineered vascular graft with designed wall thickness (biotube type C) based on a novel caged mold. J Artif Organs 19:54–61.  https://doi.org/10.1007/s10047-015-0859-4CrossRefGoogle Scholar
  19. Geelhoed WJ, Moroni L, Rotmans JI (2017) Utilizing the foreign body response to grow tissue engineered blood vessels in vivo. J Cardiovasc Transl Res 10(2):167–179.  https://doi.org/10.1007/s12265-017-9731-7CrossRefGoogle Scholar
  20. Gemmiti CV, Guldberg RE (2009) Shear stress magnitude and duration modulates matrix composition and tensile mechanical properties in engineered cartilaginous tissue. Biotechnol Bioeng 104:809–820.  https://doi.org/10.1002/bit.22440CrossRefGoogle Scholar
  21. Ghosh AK, Hirasawa N, Ohtsu H, Watanabe T, Ohuchi K (2002) Defective angiogenesis in the inflammatory granulation tissue in histidine decarboxylase–deficient mice but not in mast cell–deficient mice. J Exp Med 195:973–982.  https://doi.org/10.1084/jem.20011782CrossRefGoogle Scholar
  22. Gorbet MB, Sefton MV (2004) Biomaterial-associated thrombosis: roles of coagulation factors, complement, platelets and leukocytes. Biomaterials 25:5681–5703.  https://doi.org/10.1016/j.biomaterials.2004.01.023CrossRefGoogle Scholar
  23. Guidoin R et al (1984) The Sparks-Mandril arterial prosthesis. An ingenious concept, a total failure. What can we learn from it? J Mal Vasc 9:277–283Google Scholar
  24. Hackam DG, Redelmeier DA (2006) Translation of research evidence from animals to humans. JAMA 296:1731–1732.  https://doi.org/10.1001/jama.296.14.1731CrossRefGoogle Scholar
  25. Hallin RW (1975) Complications with the mandril-grown (Sparks) dacron arterial graft. Am Surg 41:550–554Google Scholar
  26. Hallin RW, Sweetman WR (1976) The Sparks’ mandril graft. A seven year follow-up of mandril grafts placed by Charles H. Sparks and his associates. Am J Surg 132:221–223CrossRefGoogle Scholar
  27. Hirsh SL et al (2013) The Vroman effect: competitive protein exchange with dynamic multilayer protein aggregates. Colloids Surf B Biointerfaces 103:395–404.  https://doi.org/10.1016/j.colsurfb.2012.10.039CrossRefGoogle Scholar
  28. Hiwatashi S et al (2019) Tracheal replacement using an in-body tissue-engineered collagenous tube “BIOTUBE” with a biodegradable stent in a beagle model: a preliminary report on a new technique. Eur J Pediatr Surg 29:90–96.  https://doi.org/10.1055/s-0038-1673709CrossRefGoogle Scholar
  29. Hu WJ, Eaton JW, Ugarova TP, Tang L (2001) Molecular basis of biomaterial-mediated foreign body reactions. Blood 98:1231–1238CrossRefGoogle Scholar
  30. Hynes RO (2009) The extracellular matrix: not just pretty fibrils. Science 326:1216–1219.  https://doi.org/10.1126/science.1176009CrossRefGoogle Scholar
  31. Jadlowiec CC, Lavallee M, Mannion EM, Brown MG (2015) An outcomes comparison of native arteriovenous fistulae, polytetrafluorethylene grafts, and cryopreserved vein allografts. Ann Vasc Surg 29:1642–1647.  https://doi.org/10.1016/j.avsg.2015.07.009CrossRefGoogle Scholar
  32. Jie KE et al (2010) Progenitor cells and vascular function are impaired in patients with chronic kidney disease. Nephrol Dial Transplant 25:1875–1882.  https://doi.org/10.1093/ndt/gfp749CrossRefGoogle Scholar
  33. Johnston B, Butcher EC (2002) Chemokines in rapid leukocyte adhesion triggering and migration. Semin Immunol 14:83–92.  https://doi.org/10.1006/smim.2001.0345CrossRefGoogle Scholar
  34. Jones JA et al (2007) Proteomic analysis and quantification of cytokines and chemokines from biomaterial surface-adherent macrophages and foreign body giant cells. J Biomed Mater Res A 83:585–596.  https://doi.org/10.1002/jbm.a.31221CrossRefGoogle Scholar
  35. Kainz A et al (2015) Prediction of prevalence of chronic kidney disease in diabetic patients in countries of the European Union up to 2025. Nephrol Dial Transplant 30(Suppl 4):iv113-118.  https://doi.org/10.1093/ndt/gfv073CrossRefGoogle Scholar
  36. Kato N et al (2016) First successful clinical application of the in vivo tissue-engineered autologous vascular graft. Ann Thorac Surg 102:1387–1390.  https://doi.org/10.1016/j.athoracsur.2016.06.095CrossRefGoogle Scholar
  37. Kenneth Ward W (2008) A review of the foreign-body response to subcutaneously-implanted devices: the role of macrophages and cytokines in biofouling and fibrosis. J Diabetes Sci Technol 2:768–777CrossRefGoogle Scholar
  38. Kim DJ, Mustoe T, Clark RA (2015) Cutaneous wound healing in aging small mammals: a systematic review. Wound Repair Regen 23:318–339.  https://doi.org/10.1111/wrr.12290CrossRefGoogle Scholar
  39. Knapp J, Rizzo A, Maxwell M, Duran C, Cheung D (2016) Evaluation of a bovine vascular graft in sheep. Mil Med 181:240–246.  https://doi.org/10.7205/milmed-d-15-00154CrossRefGoogle Scholar
  40. Kourtzelis I et al (2013) Inhibition of biomaterial-induced complement activation attenuates the inflammatory host response to implantation. FASEB J 27:2768–2776.  https://doi.org/10.1096/fj.12-225888CrossRefGoogle Scholar
  41. Kumar G, Waters MS, Farooque TM, Young MF, Simon CG Jr (2012) Freeform fabricated scaffolds with roughened struts that enhance both stem cell proliferation and differentiation by controlling cell shape. Biomaterials 33:4022–4030.  https://doi.org/10.1016/j.biomaterials.2012.02.048CrossRefGoogle Scholar
  42. Lawson JH et al (2016) Bioengineered human acellular vessels for dialysis access in patients with end-stage renal disease: two phase 2 single-arm trials. Lancet (London, England) 387:2026–2034.  https://doi.org/10.1016/s0140-6736(16)00557-2CrossRefGoogle Scholar
  43. Lindblad WJ (2008) Considerations for selecting the correct animal model for dermal wound-healing studies. J Biomater Sci Polym Ed 19:1087–1096.  https://doi.org/10.1163/156856208784909390CrossRefGoogle Scholar
  44. Lindner D et al (2012) Differential expression of matrix metalloproteases in human fibroblasts with different origins. Biochem Res Int 2012:875742.  https://doi.org/10.1155/2012/875742CrossRefGoogle Scholar
  45. Long JL, Tranquillo RT (2003) Elastic fiber production in cardiovascular tissue-equivalents. Matrix Biol 22:339–350CrossRefGoogle Scholar
  46. Lu P, Takai K, Weaver VM, Werb Z (2011) Extracellular matrix degradation and remodeling in development and disease. Cold Spring Harb Perspect Biol 3.  https://doi.org/10.1101/cshperspect.a005058CrossRefGoogle Scholar
  47. Luster AD (1998) Chemokines–chemotactic cytokines that mediate inflammation. N Engl J Med 338:436–445.  https://doi.org/10.1056/nejm199802123380706CrossRefGoogle Scholar
  48. Luttikhuizen DT, Harmsen MC, Van Luyn MJ (2006) Cellular and molecular dynamics in the foreign body reaction. Tissue Eng 12:1955–1970.  https://doi.org/10.1089/ten.2006.12.1955CrossRefGoogle Scholar
  49. Maroz N, Simman R (2013) Wound healing in patients with impaired kidney function. J Am Coll Clin Wound Specialists 5:2–7.  https://doi.org/10.1016/j.jccw.2014.05.002CrossRefGoogle Scholar
  50. McGuigan AP, Sefton MV (2007) The influence of biomaterials on endothelial cell thrombogenicity. Biomaterials 28:2547–2571.  https://doi.org/10.1016/j.biomaterials.2007.01.039CrossRefGoogle Scholar
  51. McNally AK, Jones JA, Macewan SR, Colton E, Anderson JM (2008) Vitronectin is a critical protein adhesion substrate for IL-4-induced foreign body giant cell formation. J Biomed Mater Res A 86:535–543.  https://doi.org/10.1002/jbm.a.31658CrossRefGoogle Scholar
  52. Morais JM, Papadimitrakopoulos F, Burgess DJ (2010) Biomaterials/tissue interactions: possible solutions to overcome foreign body response. AAPS J 12:188–196.  https://doi.org/10.1208/s12248-010-9175-3CrossRefGoogle Scholar
  53. Mozaffarian D et al (2016) Heart disease and stroke Statistics-2016 update: a report from the American Heart Association. Circulation 133:e38-360.  https://doi.org/10.1161/cir.0000000000000350CrossRefGoogle Scholar
  54. Nakayama Y, Tsujinaka T (2014) Acceleration of robust “biotube” vascular graft fabrication by in-body tissue architecture technology using a novel eosin Y-releasing mold. J Biomed Mater Res B Appl Biomater 102:231–238.  https://doi.org/10.1002/jbm.b.32999CrossRefGoogle Scholar
  55. Nakayama Y, Ishibashi-Ueda H, Takamizawa K (2004) In vivo tissue-engineered small-caliber arterial graft prosthesis consisting of autologous tissue (biotube). Cell Transplant 13:439–449CrossRefGoogle Scholar
  56. Nakayama Y, Furukoshi M, Terazawa T, Iwai R (2018) Development of long in vivo tissue-engineered “biotube” vascular grafts. Biomaterials 185:232–239.  https://doi.org/10.1016/j.biomaterials.2018.09.032CrossRefGoogle Scholar
  57. Nemeno-Guanzon JG et al (2012) Trends in tissue engineering for blood vessels. J Biomed Biotechnol 2012:956345.  https://doi.org/10.1155/2012/956345CrossRefGoogle Scholar
  58. Oie T et al (2010) In-body optical stimulation formed connective tissue vascular grafts, “biotubes,” with many capillaries and elastic fibers. J Artif Organs 13:235–240.  https://doi.org/10.1007/s10047-010-0517-9CrossRefGoogle Scholar
  59. Papenburg BJ, Rodrigues ED, Wessling M, Stamatialis D (2010) Insights into the role of material surface topography and wettability on cell-material interactions. Soft Matter 6:4377–4388.  https://doi.org/10.1039/B927207KCrossRefGoogle Scholar
  60. Pashneh-Tala S, MacNeil S, Claeyssens F (2015) The tissue-engineered vascular graft-past, present, and future. Tissue Eng Part B Rev.  https://doi.org/10.1089/ten.teb.2015.0100CrossRefGoogle Scholar
  61. Patel A, Fine B, Sandig M, Mequanint K (2006) Elastin biosynthesis: the missing link in tissue-engineered blood vessels. Cardiovasc Res 71:40–49.  https://doi.org/10.1016/j.cardiores.2006.02.021CrossRefGoogle Scholar
  62. Pawlowski KJ, Rittgers SE, Schmidt SP, Bowlin GL (2004) Endothelial cell seeding of polymeric vascular grafts. Front Biosci 9:1412–1421CrossRefGoogle Scholar
  63. Peck M, Gebhart D, Dusserre N, McAllister TN, L'Heureux N (2012) The evolution of vascular tissue engineering and current state of the art. Cells Tissues Organs 195:144–158.  https://doi.org/10.1159/000331406CrossRefGoogle Scholar
  64. Peirce EC 2nd (1953) Autologous tissue tubes for aortic grafts in dogs. Surgery 33:648–657Google Scholar
  65. Petersen E, Wagberg F, Angquist KA (2002) Serum concentrations of elastin-derived peptides in patients with specific manifestations of atherosclerotic disease. Eur J Vasc Endovasc Surg 24:440–444CrossRefGoogle Scholar
  66. Rajendran P et al (2013) The vascular endothelium and human diseases. Int J Biol Sci 9:1057–1069.  https://doi.org/10.7150/ijbs.7502CrossRefGoogle Scholar
  67. Ratner BD (2002) Reducing capsular thickness and enhancing angiogenesis around implant drug release systems. J Control Release 78:211–218.  https://doi.org/10.1016/S0168-3659(01)00502-8CrossRefGoogle Scholar
  68. Rhodes NP, Hunt JA, Williams DF (1997) Macrophage subpopulation differentiation by stimulation with biomaterials. J Biomed Mater Res 37:481–488CrossRefGoogle Scholar
  69. Roberts PN, Hopkinson BR (1977) The Sparks mandril in femoropopliteal bypass. Br Med J 2:1190–1191CrossRefGoogle Scholar
  70. Rosenbloom J, Abrams WR, Mecham R (1993) Extracellular matrix 4: the elastic fiber. FASEB J 7:1208–1218CrossRefGoogle Scholar
  71. Rothuizen TC et al (2015) Tailoring the foreign body response for in situ vascular tissue engineering. Tissue Eng Part C Methods 21:436–446.  https://doi.org/10.1089/ten.TEC.2014.0264CrossRefGoogle Scholar
  72. Rothuizen TC et al (2016a) Development and evaluation of in vivo tissue engineered blood vessels in a porcine model. Biomaterials 75:82–90.  https://doi.org/10.1016/j.biomaterials.2015.10.023CrossRefGoogle Scholar
  73. Rothuizen TC et al (2016b) Promoting Tropoelastin expression in arterial and venous vascular smooth muscle cells and fibroblasts for vascular tissue engineering. Tissue Eng Part C Methods 22(10):923–931.  https://doi.org/10.1089/ten.TEC.2016.0173CrossRefGoogle Scholar
  74. Rotmans JI (2014) Animal models for studying pathophysiology of hemodialysis access. Open Urol Nephrol J 7:14–21CrossRefGoogle Scholar
  75. Rotmans JI et al (2005) Hemodialysis access graft failure: time to revisit an unmet clinical need? J Nephrol 18:9–20Google Scholar
  76. Rotmans JI, Heyligers JMM, Stroes ESG, Pasterkamp G (2006) Endothelial progenitor cell-seeded grafts: rash and risky. Can J Cardiol 22:1113–1116CrossRefGoogle Scholar
  77. Roy-Chaudhury P et al (2001) Venous neointimal hyperplasia in polytetrafluoroethylene dialysis grafts. Kidney Int 59:2325–2334.  https://doi.org/10.1046/j.1523-1755.2001.00750.xCrossRefGoogle Scholar
  78. Sakai O et al (2009) Faster and stronger vascular “biotube” graft fabrication in vivo using a novel nicotine-containing mold. J Biomed Mater Res B Appl Biomater 90:412–420.  https://doi.org/10.1002/jbm.b.31300CrossRefGoogle Scholar
  79. Sayers RD, Raptis S, Berce M, Miller JH (1998) Long-term results of femorotibial bypass with vein or polytetrafluoroethylene. Br J Surg 85:934–938.  https://doi.org/10.1046/j.1365-2168.1998.00765.xCrossRefGoogle Scholar
  80. Shah A, Shah S, Mani G, Wenke J, Agrawal M (2011) Endothelial cell behaviour on gas-plasma-treated PLA surfaces: the roles of surface chemistry and roughness. J Tissue Eng Regen Med 5:301–312.  https://doi.org/10.1002/term.316CrossRefGoogle Scholar
  81. Shen M, Garcia I, Maier RV, Horbett TA (2004) Effects of adsorbed proteins and surface chemistry on foreign body giant cell formation, tumor necrosis factor alpha release and procoagulant activity of monocytes. J Biomed Mater Res A 70:533–541.  https://doi.org/10.1002/jbm.a.30069CrossRefGoogle Scholar
  82. Sica A, Mantovani A (2012) Macrophage plasticity and polarization: in vivo veritas. J Clin Invest 122:787–795.  https://doi.org/10.1172/jci59643CrossRefGoogle Scholar
  83. Sparks CH (1969) Autogenous grafts made to order. Ann Thorac Surg 8:104–113CrossRefGoogle Scholar
  84. Sparks CH (1973) Silicone mandril method for growing reinforced autogenous femoro-popliteal artery grafts in situ. Ann Surg 177:293–300CrossRefGoogle Scholar
  85. Stickler P et al (2010) Cyclically stretching developing tissue in vivo enhances mechanical strength and organization of vascular grafts. Acta Biomater 6:2448–2456.  https://doi.org/10.1016/j.actbio.2010.01.041CrossRefGoogle Scholar
  86. Strang AC et al (2014) Superior in vivo compatibility of hydrophilic polymer coated prosthetic vascular grafts. J Vasc Access 15:95–101.  https://doi.org/10.5301/jva.5000166CrossRefGoogle Scholar
  87. Sullivan TP, Eaglstein WH, Davis SC, Mertz P (2001) The pig as a model for human wound healing. Wound Repair Regen 9:66–76CrossRefGoogle Scholar
  88. Sullivan DE, Ferris M, Nguyen H, Abboud E, Brody AR (2009) TNF-alpha induces TGF-beta1 expression in lung fibroblasts at the transcriptional level via AP-1 activation. J Cell Mol Med 13:1866–1876.  https://doi.org/10.1111/j.1582-4934.2009.00647.xCrossRefGoogle Scholar
  89. Summerfield A, Meurens F, Ricklin ME (2015) The immunology of the porcine skin and its value as a model for human skin. Mol Immunol 66:14–21.  https://doi.org/10.1016/j.molimm.2014.10.023CrossRefGoogle Scholar
  90. Szaba FM, Smiley ST (2002) Roles for thrombin and fibrin(ogen) in cytokine/chemokine production and macrophage adhesion in vivo. Blood 99:1053–1059CrossRefGoogle Scholar
  91. Tang L, Eaton JW (1993) Fibrin(ogen) mediates acute inflammatory responses to biomaterials. J Exp Med 178:2147–2156CrossRefGoogle Scholar
  92. Tang L, Liu L, Elwing HB (1998a) Complement activation and inflammation triggered by model biomaterial surfaces. J Biomed Mater Res 41:333–340CrossRefGoogle Scholar
  93. Tang L, Jennings TA, Eaton JW (1998b) Mast cells mediate acute inflammatory responses to implanted biomaterials. Proc Natl Acad Sci U S A 95:8841–8846CrossRefGoogle Scholar
  94. Tatsumi E, Nakayama Y, Okumura N, Kaneko Y (2018) P2664Long-term follow up of first-in-human study in bypass of stenosis av shunt by an autologous in-body-tissue-engineered (biotube) vascular graft. Eur Heart J 39.  https://doi.org/10.1093/eurheartj/ehy565.P2664
  95. Teirstein PS et al (2000) Three-year clinical and angiographic follow-up after intracoronary radiation: results of a randomized clinical trial. Circulation 101:360–365CrossRefGoogle Scholar
  96. Tsukagoshi T, Yenidunya MO, Sasaki E, Suse T, Hosaka Y (1999) Experimental vascular graft using small-caliber fascia-wrapped fibrocollagenous tube: short-term evaluation. J Reconstr Microsurg 15:127–131.  https://doi.org/10.1055/s-2007-1000083CrossRefGoogle Scholar
  97. Tzoulaki I, Elliott P, Kontis V, Ezzati M (2016) Worldwide exposures to cardiovascular risk factors and associated health effects: current knowledge and data gaps. Circulation 133:2314–2333.  https://doi.org/10.1161/circulationaha.115.008718CrossRefGoogle Scholar
  98. Verhagen HJ et al (1996) Thrombomodulin activity on mesothelial cells: perspectives for mesothelial cells as an alternative for endothelial cells for cell seeding on vascular grafts. Br J Haematol 95:542–549CrossRefGoogle Scholar
  99. Vouyouka AG et al (2001) The role of type I collagen in aortic wall strength with a homotrimeric [α1(I)]3 collagen mouse model. J Vasc Surg 33:1263–1270.  https://doi.org/10.1067/mva.2001.113579CrossRefGoogle Scholar
  100. Wallace DG, Rosenblatt J, Ksander GA (1992) Tissue compatibility of collagen-silicone composites in a rat subcutaneous model. J Biomed Mater Res 26:1517–1534.  https://doi.org/10.1002/jbm.820261110CrossRefGoogle Scholar
  101. Watanabe T et al (2011) Long-term animal implantation study of biotube-autologous small-caliber vascular graft fabricated by in-body tissue architecture. J Biomed Mater Res B Appl Biomater 98:120–126.  https://doi.org/10.1002/jbm.b.31841CrossRefGoogle Scholar
  102. Watanabe T, Kanda K, Ishibashi-Ueda H, Yaku H, Nakayama Y (2010) Autologous small-caliber “biotube” vascular grafts with argatroban loading: a histomorphological examination after implantation to rabbits. J Biomed Mater Res B Appl Biomater 92:236–242.  https://doi.org/10.1002/jbm.b.31510CrossRefGoogle Scholar
  103. Weigand A et al (2013) New aspects on efficient anticoagulation and antiplatelet strategies in sheep. BMC Vet Res 9:192.  https://doi.org/10.1186/1746-6148-9-192CrossRefGoogle Scholar
  104. Wilson CJ, Clegg RE, Leavesley DI, Pearcy MJ (2005) Mediation of biomaterial-cell interactions by adsorbed proteins: a review. Tissue Eng 11:1–18.  https://doi.org/10.1089/ten.2005.11.1CrossRefGoogle Scholar
  105. Wise SG, Weiss AS (2009) Tropoelastin. Int J Biochem Cell Biol 41:494–497.  https://doi.org/10.1016/j.biocel.2008.03.017CrossRefGoogle Scholar
  106. Wise SG, Mithieux SM, Weiss AS (2009) Engineered tropoelastin and elastin-based biomaterials. Adv Protein Chem Struct Biol 78:1–24.  https://doi.org/10.1016/s1876-1623(08)78001-5CrossRefGoogle Scholar
  107. Yamanami M et al (2013) Implantation study of small-caliber “biotube” vascular grafts in a rat model. J Artif Organs 16:59–65.  https://doi.org/10.1007/s10047-012-0676-yCrossRefGoogle Scholar
  108. Yates CC, Hebda P, Wells A (2012) Skin wound healing and scarring: fetal wounds and regenerative restitution. Birth Defects Res C Embryo Today 96:325–333.  https://doi.org/10.1002/bdrc.21024CrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Wouter J. Geelhoed
    • 1
    • 2
    Email author
  • Lorenzo Moroni
    • 3
  • Joris I. Rotmans
    • 1
    • 2
  1. 1.Department of Internal MedicineLeiden University Medical CenterLeidenThe Netherlands
  2. 2.Eindhoven Laboratory of Experimental Vascular MedicineLeiden University Medical CenterLeidenThe Netherlands
  3. 3.MERLN Institute for Technology Inspired Regenerative Medicine, Complex Tissue RegenerationMaastricht UniversityMaastrichtThe Netherlands

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