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Tissue Engineered Heart Valves

  • Jay M. Reimer
  • Robert T. TranquilloEmail author
Chapter

Abstract

Tissue engineered heart valves are being developed in order to provide an alternative prosthetic valve to patients suffering from valvular heart disease. They aim to address the limitations of currently existing bioprosthetic and mechanical heart valves, which have a limited functional life or require lifelong anticoagulation, respectively. Tissue engineered valves generally consist of three parts: a biodegradable polymeric scaffold for initial structural integrity and cell attachment sites, entrapped or seeded cells that remodel that biodegradable scaffold, and stimulation paradigms to direct cellular activity (especially production of a functional extracellular matrix). In vitro functional testing is useful to assess valve designs based on their hydrodynamic performance under physiologic pressure and flow conditions. However, in vivo testing is crucial since tissue engineered heart valves aim to provide a living valve capable of cell-mediated repair, remodeling, and growth. The aforementioned considerations comprise the focus of this chapter.

Keywords

Heart valve engineering Tissue engineered heart valves Biopolymer scaffold Synthetic polymer scaffold Animal model Pulse duplicator 

References

  1. 1.
    Mozaffarian D, Benjamin EJ, Go AS, Arnett DK, Blaha MJ, Cushman M, et al. Heart disease and stroke statistics—2015 update: a report from the American Heart Association. Circulation. 2015;131(4):e29–322.  https://doi.org/10.1161/CIR.0000000000000152.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Moller J. Prevalence and incidence of cardiac malformations. In: Moller J, editor. Surgery of congenital heart disease: pediatric care consortium 1984–1995. Armonk, NY: Futura Publishing Company Inc.; 1998. p. 19–26.Google Scholar
  3. 3.
    Minnesota Department of Health. Diseases and conditions identified in children. [Webpage] 2015. Available from: http://www.health.state.mn.us/divs/cfh/topic/diseasesconds/. Cited 24 Aug 2015.
  4. 4.
    Centers for Disease Control and Prevention. Data & statistics for congenital defects in the US. 2015. Available from: http://www.cdc.gov/ncbddd/birthdefects/data.html. Cited 24 Aug 2015.
  5. 5.
    Liao K, John R. Handbook of cardiac anatomy, physiology, and devices. 2nd ed. Minneapolis, MN: Spring Science & Business Media; 2009.Google Scholar
  6. 6.
    Waterbolk TW, Hoendermis ES, den Hamer IJ, Ebels T. Pulmonary valve replacement with a mechanical prosthesis. Promising results of 28 procedures in patients with congenital heart disease. Eur J Cardiothorac Surg. 2006;30(1):28–32.  https://doi.org/10.1016/j.ejcts.2006.02.069.CrossRefPubMedGoogle Scholar
  7. 7.
    Bouzas B, Kilner PJ, Gatzoulis MA. Pulmonary regurgitation: not a benign lesion. Eur Heart J. 2005;26(5):433–9.  https://doi.org/10.1093/eurheartj/ehi091.CrossRefPubMedGoogle Scholar
  8. 8.
    Yemets IM, Williams WG, Webb GD, Harrison DA, McLaughlin PR, Trusler GA, et al. Pulmonary valve replacement late after repair of tetralogy of Fallot. Ann Thorac Surg. 1997;64(2):526–30.  https://doi.org/10.1016/S0003-4975(97)00577-8.CrossRefPubMedGoogle Scholar
  9. 9.
    Tweddell JS, Simpson P, Li SH, Dunham-Ingle J, Bartz PJ, Earing MG, et al. Timing and technique of pulmonary valve replacement in the patient with tetralogy of Fallot. Semin Thorac Cardiovasc Surg Pediatr Card Surg Annu. 2012;15(1):27–33.  https://doi.org/10.1053/j.pcsu.2012.01.007.CrossRefPubMedGoogle Scholar
  10. 10.
    Kheradvar A, Groves EM, Goergen CJ, Alavi SH, Tranquillo R, Simmons CA, et al. Emerging trends in heart valve engineering: part II. Novel and standard technologies for aortic valve replacement. Ann Biomed Eng. 2015;43(4):844–57.  https://doi.org/10.1007/s10439-014-1191-5.CrossRefPubMedGoogle Scholar
  11. 11.
    Kheradvar A, Groves EM, Simmons CA, Griffith B, Alavi SH, Tranquillo R, et al. Emerging trends in heart valve engineering: part III. Novel technologies for mitral valve repair and replacement. Ann Biomed Eng. 2015;43(4):858–70.  https://doi.org/10.1007/s10439-014-1129-y.CrossRefPubMedGoogle Scholar
  12. 12.
    Rahimtoola SH. Choice of prosthetic heart valve for adult patients. J Am Coll Cardiol. 2003;41(6):893–904.  https://doi.org/10.1016/S0735-1097(02)02965-0.CrossRefPubMedGoogle Scholar
  13. 13.
    Rahimtoola SH. Choice of prosthetic heart valve in adults an update. J Am Coll Cardiol. 2010;55(22):2413–26.  https://doi.org/10.1016/j.jacc.2009.10.085.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Birkmeyer NJ, Birkmeyer JD, Tosteson AN, Grunkemeier GL, Marrin CA, O’Connor GT. Prosthetic valve type for patients undergoing aortic valve replacement: a decision analysis. Ann Thorac Surg. 2000;70(6):1946–52.CrossRefGoogle Scholar
  15. 15.
    El Oakley R, Kleine P, Bach DS. Choice of prosthetic heart valve in today’s practice. Circulation. 2008;117(2):253–6.  https://doi.org/10.1161/CIRCULATIONAHA.107.736819.CrossRefPubMedGoogle Scholar
  16. 16.
    Kaneko T, Cohn LH, Aranki SF. Tissue valve is the preferred option for patients aged 60 and older. Circulation. 2013;128:1365–71.  https://doi.org/10.1161/CIRCULATIONAHA.113.002584.CrossRefPubMedGoogle Scholar
  17. 17.
    van Geldorp MWA, Eric Jamieson WR, Kappetein AP, Ye J, Fradet GJ, Eijkemans MJC, et al. Patient outcome after aortic valve replacement with a mechanical or biological prosthesis: weighing lifetime anticoagulant-related event risk against reoperation risk. J Thorac Cardiovasc Surg. 2009;137(4):881–6, 886e1–5.  https://doi.org/10.1016/j.jtcvs.2008.09.028.CrossRefPubMedGoogle Scholar
  18. 18.
    Mankad S. Management of prosthetic heart valve complications. Curr Treat Options Cardiovasc Med. 2012;14(6):608–21.  https://doi.org/10.1007/s11936-012-0212-7.CrossRefPubMedGoogle Scholar
  19. 19.
    Tillquist MN, Maddox TM. Cardiac crossroads: deciding between mechanical or bioprosthetic heart valve replacement. Patient Prefer Adherence. 2011;5:91–9.  https://doi.org/10.2147/PPA.S16420.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Oterhals K, Fridlund B, Nordrehaug JE, Haaverstad R, Norekvål TM. Adapting to living with a mechanical aortic heart valve: a phenomenographic study. J Adv Nurs. 2013;69(9):2088–98.  https://doi.org/10.1111/jan.12076.CrossRefPubMedGoogle Scholar
  21. 21.
    Hammermeister K, Sethi GK, Henderson WG, Grover FL, Oprian C, Rahimtoola SH. Outcomes 15 years after valve replacement with a mechanical versus a bioprosthetic valve: final report of the Veterans Affairs randomized trial. J Am Coll Cardiol. 2000;36:1152–8.CrossRefGoogle Scholar
  22. 22.
    Delmo Walter EM, de By TMMH, Meyer R, Hetzer R. The future of heart valve banking and of homografts: perspective from the Deutsches Herzzentrum Berlin. HSR Proc Intensive Care Cardiovasc Anesth. 2012;4(2):97–108.PubMedPubMedCentralGoogle Scholar
  23. 23.
    Elkins RC, Goldstein S, Hewitt CW, Walsh SP, Dawson PE, Ollerenshaw JD, et al. Recellularization of heart valve grafts by a process of adaptive remodeling. Semin Thorac Cardiovasc Surg. 2001;13(4 Suppl 1):87–92.PubMedGoogle Scholar
  24. 24.
    Neumann A, Cebotari S, Tudorache I, Haverich A, Sarikouch S. Heart valve engineering: decellularized allograft matrices in clinical practice. Biomed Tech (Berl). 2013;58(5):453–6.  https://doi.org/10.1515/bmt-2012-0115.CrossRefGoogle Scholar
  25. 25.
    Elkins R, Dawson P, Goldstein S, Walsh S, Black K. Decellularized human valve allografts. Ann Thorac Surg. 2001;71(5):S428–32.  https://doi.org/10.1016/S0003-4975(01)02503-6.CrossRefPubMedGoogle Scholar
  26. 26.
    Jones JM, O’kane H, Gladstone DJ, Sarsam MA, Campalani G, MacGowan SW, et al. Repeat heart valve surgery: risk factors for operative mortality. J Thorac Cardiovasc Surg. 2001;122(5):913–8.  https://doi.org/10.1067/mtc.2001.116470.CrossRefPubMedGoogle Scholar
  27. 27.
    Gurvitch R, Cheung A, Ye J, Wood DA, Willson AB, Toggweiler S, et al. Transcatheter valve-in-valve implantation for failed surgical bioprosthetic valves. J Am Coll Cardiol. 2011;58(21):2196–209.  https://doi.org/10.1016/j.jacc.2011.09.009.CrossRefPubMedGoogle Scholar
  28. 28.
    Gurvitch R, Cheung A, Bedogni F, Webb JG. Coronary obstruction following transcatheter aortic valve-in-valve implantation for failed surgical bioprostheses. Catheter Cardiovasc Interv. 2011;77(3):439–44.  https://doi.org/10.1002/ccd.22861.CrossRefPubMedGoogle Scholar
  29. 29.
    Dvir D, Webb J, Brecker S, Bleiziffer S, Hildick-Smith D, Colombo A, et al. Transcatheter aortic valve replacement for degenerative bioprosthetic surgical valves: results from the global valve-in-valve registry. Circulation. 2012;126(19):2335–44.  https://doi.org/10.1161/CIRCULATIONAHA.112.104505.CrossRefPubMedGoogle Scholar
  30. 30.
    Cebotari S, Tudorache I, Ciubotaru A, Boethig D, Sarikouch S, Goerler A, et al. Use of fresh decellularized allografts for pulmonary valve replacement may reduce the reoperation rate in children and young adults early report. Circulation. 2011;124(11):S115–23.  https://doi.org/10.1161/Circulationaha.110.012161.CrossRefPubMedGoogle Scholar
  31. 31.
    Erdbrügger W, Konertz W, Dohmen PM, Posner S, Ellerbrok H, Brodde O-EE, et al. Decellularized xenogenic heart valves reveal remodeling and growth potential in vivo. Tissue Eng. 2006;12(8):2059–68.  https://doi.org/10.1089/ten.2006.12.2059.CrossRefPubMedGoogle Scholar
  32. 32.
    Dohmen PM, Lembcke A, Holinski S, Pruss A, Konertz W. Ten years of clinical results with a tissue-engineered pulmonary valve. Ann Thorac Surg. 2011;92(4):1308–14.  https://doi.org/10.1016/j.athoracsur.2011.06.009.CrossRefPubMedGoogle Scholar
  33. 33.
    Konertz W, Angeli E, Tarusinov G, Christ T, Kroll J, Dohmen PM, et al. Right ventricular outflow tract reconstruction with decellularized porcine xenografts in patients with congenital heart disease. J Heart Valve Dis. 2011;20(3):341–7.PubMedGoogle Scholar
  34. 34.
    Ruzmetov M, Shah JJ, Geiss DM, Fortuna RS. Decellularized versus standard cryopreserved valve allografts for right ventricular outflow tract reconstruction: a single-institution comparison. J Thorac Cardiovasc Surg. 2012;143(3):543–9.  https://doi.org/10.1016/j.jtcvs.2011.12.032.CrossRefPubMedGoogle Scholar
  35. 35.
    Brown JW, Elkins RC, Clarke DR, Tweddell JS, Huddleston CB, Doty JR, et al. Performance of the CryoValve SG human decellularized pulmonary valve in 342 patients relative to the conventional CryoValve at a mean follow-up of four years. J Thorac Cardiovasc Surg. 2010;139:339–48.  https://doi.org/10.1016/j.jtcvs.2009.04.065.CrossRefPubMedGoogle Scholar
  36. 36.
    Tudorache I, Theodoridis K, Baraki H, Sarikouch S, Bara C, Meyer T, et al. Decellularized aortic allografts versus pulmonary autografts for aortic valve replacement in the growing sheep model: haemodynamic and morphological results at 20 months after implantation. Eur J Cardiothorac Surg. 2015;49:1228–38.  https://doi.org/10.1093/ejcts/ezv362.CrossRefPubMedGoogle Scholar
  37. 37.
    Baraki H, Tudorache I, Braun M, Hoffler K, Gorler A, Lichtenberg A, et al. Orthotopic replacement of the aortic valve with decellularized allograft in a sheep model. Biomaterials. 2009;30(31):6240–6.  https://doi.org/10.1016/j.biomaterials.2009.07.068.CrossRefPubMedGoogle Scholar
  38. 38.
    Bibevski S, Wilkinson D, Ruzmetov M, Fortuna R, Turrentine M, Brown JW, et al., cartographers. Performance of synergraft decellularized pulmonary allografts compared with standard cryopreserved allografts: results from multi-institutional data [Abstract]. Circulation. 2012;126 (supplement 21).Google Scholar
  39. 39.
    Tudorache I, Calistru A, Baraki H, Meyer T, Hoffler K, Sarikouch S, et al. Orthotopic replacement of aortic heart valves with tissue-engineered grafts. Tissue Eng Part A. 2013;19(15–16):1686–94.  https://doi.org/10.1089/ten.TEA.2012.0074.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Perri G, Polito A, Esposito C, Albanese SB, Francalanci P, Pongiglione G, et al. Early and late failure of tissue-engineered pulmonary valve conduits used for right ventricular outflow tract reconstruction in patients with congenital heart disease. Eur J Cardiothorac Surg. 2012;41(6):1320–5.  https://doi.org/10.1093/ejcts/ezr221.CrossRefPubMedGoogle Scholar
  41. 41.
    Kheradvar A, Groves EM, Dasi LP, Alavi SH, Tranquillo R, Grande-Allen KJ, et al. Emerging trends in heart valve engineering: part I. Solutions for future. Ann Biomed Eng. 2015;43(4):833–43.  https://doi.org/10.1007/s10439-014-1209-z.CrossRefPubMedGoogle Scholar
  42. 42.
    Chester A, Yacoub MH, Taylor PM. Heart valve tissue engineering. In: Boccaccini AR, Harding SE, editors. Myocardial tissue engineering. Berlin: Springer; 2011. p. 243–66.Google Scholar
  43. 43.
    Schmidt JB, Tranquillo RT. Tissue-engineered heart valves. In: Iaizzo PA, Bianco R, Hill AJ, St. Louis JD, editors. Heart valves: from design to clinical implantation. Springer: New York; 2013. p. 261–80.CrossRefGoogle Scholar
  44. 44.
    van Loon SLM, Smits AIPM, Driessen-Mol A, Baaijens F, Bouten CV. The immune response in in situ tissue engineering of aortic heart valves. In: Aikawa E, editor. Calcific aortic valve disease. Rijeka: InTech; 2013. p. 207–45.Google Scholar
  45. 45.
    Bouten CV, Driessen-Mol A, Baaijens FP. In situ heart valve tissue engineering: simple devices, smart materials, complex knowledge. Expert Rev Med Devices. 2012;9(5):453–5.  https://doi.org/10.1586/erd.12.43.CrossRefPubMedGoogle Scholar
  46. 46.
    Hayashida K, Kanda K, Yaku H, Ando J, Nakayama Y. Development of an in vivo tissue-engineered, autologous heart valve (the biovalve): preparation of a prototype model. J Thorac Cardiovasc Surg. 2007;134(1):152–9.  https://doi.org/10.1016/j.jtcvs.2007.01.087.CrossRefPubMedGoogle Scholar
  47. 47.
    Bouten CV, Smits AI, Talacua H, Muylaert DE, Janssen HM, Bosman A, et al., editors. Biomaterial-based in situ tissue engineering of heart valves. 2015 4th TERMIS world congress, Sept 2015, Boston, MA, Tissue Engineering Part A.Google Scholar
  48. 48.
    Ott HC, Matthiesen TS, Goh SK, Black LD, Kren SM, Netoff TI, et al. Perfusion-decellularized matrix: using nature’s platform to engineer a bioartificial heart. Nat Med. 2008;14(2):213–21.  https://doi.org/10.1038/nm1684.CrossRefPubMedGoogle Scholar
  49. 49.
    Gilbert TW, Sellaro TL, Badylak SF. Decellularization of tissues and organs. Biomaterials. 2006;27(19):3675–83.  https://doi.org/10.1016/j.biomaterials.2006.02.014.CrossRefPubMedGoogle Scholar
  50. 50.
    Taylor PM. Biological matrices and bionanotechnology. Philos Trans R Soc Lond Ser B Biol Sci. 2007;362(1484):1313–20.  https://doi.org/10.1098/rstb.2007.2117.CrossRefGoogle Scholar
  51. 51.
    Sung HJ, Meredith C, Johnson C, Galis ZS. The effect of scaffold degradation rate on three-dimensional cell growth and angiogenesis. Biomaterials. 2004;25(26):5735–42.  https://doi.org/10.1016/j.biomaterials.2004.01.066.CrossRefPubMedGoogle Scholar
  52. 52.
    Zund G, Breuer CK, Shinoka T, Ma PX, Langer R, Mayer JE, et al. The in vitro construction of a tissue engineered bioprosthetic heart valve. Eur J Cardiothorac Surg. 1997;11(3):493–7.  https://doi.org/10.1016/S1010-7940(96)01005-6.CrossRefPubMedGoogle Scholar
  53. 53.
    Stock UA, Nagashima M, Khalil PN, Nollert GD, Herden T, Sperling JS, et al. Tissue-engineered valved conduits in the pulmonary circulation. J Thorac Cardiovasc Surg. 2000;119(4 Pt 1):732–40.  https://doi.org/10.1067/mtc.2000.104584.CrossRefPubMedGoogle Scholar
  54. 54.
    Knight R, Wilcox HE, Korossis SA, Ingham E. The use of acellular matrices for tissue engineering of cardiac valves. Proc Inst Mech Eng H. 2008;222(1):129–43.  https://doi.org/10.1243/09544119JEIM230.CrossRefPubMedGoogle Scholar
  55. 55.
    Hoerstrup SP, Sodian R, Daebritz S, Wang J, Bacha EA, Martin DP, et al. Functional living trileaflet heart valves grown in vitro. Circulation. 2000;102(19 Suppl 3):III44–9.  https://doi.org/10.1161/01.CIR.102.suppl_3.III-44.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Knight RL, Booth C, Wilcox HE, Fisher J, Ingham E. Tissue engineering of cardiac valves: re-seeding of acellular porcine aortic valve matrices with human mesenchymal progenitor cells. J Heart Valve Dis. 2005;14(6):806–13.PubMedGoogle Scholar
  57. 57.
    Rippel RA, Ghanbari H, Seifalian AM. Tissue-engineered heart valve: future of cardiac surgery. World J Surg. 2012;36(7):1581–91.  https://doi.org/10.1007/s00268-012-1535-y.CrossRefPubMedGoogle Scholar
  58. 58.
    Glowacki J, Mizuno S. Collagen scaffolds for tissue engineering. Biopolymers. 2008;89(5):338–44.  https://doi.org/10.1002/bip.20871.CrossRefPubMedGoogle Scholar
  59. 59.
    Chevallay B, Herbage D. Collagen-based biomaterials as 3D scaffold for cell cultures: applications for tissue engineering and gene therapy. Med Biol Eng Comput. 2000;38(2):211–8.  https://doi.org/10.1007/BF02344779.CrossRefPubMedGoogle Scholar
  60. 60.
    Thie M, Schlumberger W, Semich R, Rauterberg J, Robenek H. Aortic smooth muscle cells in collagen lattice culture: effects on ultrastructure, proliferation and collagen synthesis. Eur J Cell Biol. 1991;55(2):295–304.PubMedGoogle Scholar
  61. 61.
    Clark RA, Nielsen LD, Welch MP, McPherson JM. Collagen matrices attenuate the collagen-synthetic response of cultured fibroblasts to TGF-beta. J Cell Sci. 1995;108(Pt 3):1251–61.PubMedGoogle Scholar
  62. 62.
    Ma P. Biomaterials and regenerative medicine. Cambridge: Cambridge University Press; 2012.Google Scholar
  63. 63.
    Coustry F, Gillery P, Maquart FX, Borel JP. Effect of transforming growth factor beta on fibroblasts in three-dimensional lattice cultures. FEBS Lett. 1990;262(2):339–41.CrossRefGoogle Scholar
  64. 64.
    Grassl ED, Oegema TR, Tranquillo RT. Fibrin as an alternative biopolymer to type-I collagen for the fabrication of a media equivalent. J Biomed Mater Res. 2002;60(4):607–12.  https://doi.org/10.1002/jbm.10107.CrossRefPubMedGoogle Scholar
  65. 65.
    Alavi SH, Kheradvar A. Metal mesh scaffold for tissue engineering of membranes. Tissue Eng Part C Methods. 2012;18(4):293–301.  https://doi.org/10.1089/ten.TEC.2011.0531.CrossRefPubMedGoogle Scholar
  66. 66.
    Loger K, Engel A, Haupt J, Li Q, Lima de Miranda R, Quandt E, et al. Cell adhesion on NiTi thin film sputter-deposited meshes. Mater Sci Eng C. 2016;59:611–6.  https://doi.org/10.1016/j.msec.2015.10.008.CrossRefGoogle Scholar
  67. 67.
    Loger K, de Miranda RL, Engel A, Marczynski-Bühlow M, Lutter G, Quandt E. Fabrication and evaluation of nitinol thin film heart valves. Cardiovasc Eng Technol. 2014;5(4):308–16.  https://doi.org/10.1007/s13239-014-0194-6.CrossRefGoogle Scholar
  68. 68.
    Stepan LL, Levi DS, Carman GP. A thin film nitinol heart valve. J Biomech Eng. 2005;127(6):915–8.CrossRefGoogle Scholar
  69. 69.
    Alavi SH, Kheradvar A. A hybrid tissue-engineered heart valve. Ann Thorac Surg. 2015;99(6):2183–7.  https://doi.org/10.1016/j.athoracsur.2015.02.058.CrossRefPubMedGoogle Scholar
  70. 70.
    Alavi SH, Liu WF, Kheradvar A. Inflammatory response assessment of a hybrid tissue-engineered heart valve leaflet. Ann Biomed Eng. 2013;41(2):316–26.  https://doi.org/10.1007/s10439-012-0664-7.CrossRefPubMedGoogle Scholar
  71. 71.
    Neidert MR, Lee ES, Oegema TR, Tranquillo RT. Enhanced fibrin remodeling in vitro with TGF-beta1, insulin and plasmin for improved tissue-equivalents. Biomaterials. 2002;23(17):3717–31.CrossRefGoogle Scholar
  72. 72.
    Ramaswamy S, Gottlieb D, Engelmayr GC, Aikawa E, Schmidt DE, Gaitan-Leon DM, et al. The role of organ level conditioning on the promotion of engineered heart valve tissue development in-vitro using mesenchymal stem cells. Biomaterials. 2010;31(6):1114–25.  https://doi.org/10.1016/j.biomaterials.2009.10.019.CrossRefPubMedGoogle Scholar
  73. 73.
    Robinson P, Johnson S, Evans M, Barocas V, Tranquillo R. Functional tissue-engineered valves from cell-remodeled fibrin with commissural alignment of cell-produced collagen. Tissue Eng Part A. 2008;14(1):83–95.  https://doi.org/10.1089/ten.a.2007.0148.CrossRefPubMedGoogle Scholar
  74. 74.
    Alenghat FJ, Ingber DE. Mechanotransduction: all signals point to cytoskeleton, matrix, and integrins. Sci STKE. 2002;2002(119):pe6.  https://doi.org/10.1126/stke.2002.119.pe6.CrossRefPubMedGoogle Scholar
  75. 75.
    Chiquet M, Renedo AS, Huber F, Fluck M. How do fibroblasts translate mechanical signals into changes in extracellular matrix production? Matrix Biol. 2003;22(1):73–80.  https://doi.org/10.1016/S0945-053X(03)00004-0.CrossRefPubMedGoogle Scholar
  76. 76.
    Syedain ZH, Weinberg JS, Tranquillo RT. Cyclic distension of fibrin-based tissue constructs: evidence of adaptation during growth of engineered connective tissue. Proc Natl Acad Sci U S A. 2008;105(18):6537–42.  https://doi.org/10.1073/pnas.0711217105.CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Syedain ZH, Tranquillo RT. Controlled cyclic stretch bioreactor for tissue-engineered heart valves. Biomaterials. 2009;30(25):4078–84.  https://doi.org/10.1016/j.biomaterials.2009.04.027.CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Schmidt JB, Tranquillo RT. Cyclic stretch and perfusion bioreactor for conditioning large diameter engineered tissue tubes. Ann Biomed Eng. 2015;44:1785.  https://doi.org/10.1007/s10439-015-1437-x.CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Dumont K, Yperman J, Verbeken E, Segers P, Meuris B, Vandenberghe S, et al. Design of a new pulsatile bioreactor for tissue engineered aortic heart valve formation. Artif Organs. 2002;26(8):710–4.  https://doi.org/10.1046/j.1525-1594.2002.06931_3.x.CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Hildebrand DK, Wu ZJ, Mayer JE Jr, Sacks MS. Design and hydrodynamic evaluation of a novel pulsatile bioreactor for biologically active heart valves. Ann Biomed Eng. 2004;32(8):1039–49.  https://doi.org/10.1114/B:ABME.0000036640.11387.4b.CrossRefPubMedGoogle Scholar
  81. 81.
    Mol A, Driessen NJ, Rutten MC, Hoerstrup SP, Bouten CV, Baaijens FP. Tissue engineering of human heart valve leaflets: a novel bioreactor for a strain-based conditioning approach. Ann Biomed Eng. 2005;33(12):1778–88.  https://doi.org/10.1007/s10439-005-8025-4.CrossRefPubMedGoogle Scholar
  82. 82.
    Ruel J, Lachance G. A new bioreactor for the development of tissue-engineered heart valves. Ann Biomed Eng. 2009;37(4):674–81.  https://doi.org/10.1007/s10439-009-9646-9.CrossRefPubMedGoogle Scholar
  83. 83.
    Flanagan T, Cornelissen C, Koch S, Tschoeke B, Sachweh J, Schmitz-Rode T, et al. The in vitro development of autologous fibrin-based tissue-engineered heart valves through optimized dynamic conditioning. Biomaterials. 2007;28(23):3388–97.  https://doi.org/10.1016/j.biomaterials.2007.04.012.CrossRefPubMedGoogle Scholar
  84. 84.
    Hoerstrup SP, Sodian R, Sperling JS, Vacanti JP, Mayer JE Jr. New pulsatile bioreactor for in vitro formation of tissue engineered heart valves. Tissue Eng. 2000;6(1):75–9.  https://doi.org/10.1089/107632700320919.CrossRefPubMedGoogle Scholar
  85. 85.
    Berry JL, Steen JA, Koudy Williams J, Jordan JE, Atala A, Yoo JJ. Bioreactors for development of tissue engineered heart valves. Ann Biomed Eng. 2010;38(11):3272–9.  https://doi.org/10.1007/s10439-010-0148-6.CrossRefGoogle Scholar
  86. 86.
    Engelmayr GC Jr, Soletti L, Vigmostad SC, Budilarto SG, Federspiel WJ, Chandran KB, et al. A novel flex-stretch-flow bioreactor for the study of engineered heart valve tissue mechanobiology. Ann Biomed Eng. 2008;36(5):700–12.  https://doi.org/10.1007/s10439-008-9447-6.CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Ramaswamy S, Boronyak SM, Le T, Holmes A, Sotiropoulos F, Sacks MS. A novel bioreactor for mechanobiological studies of engineered heart valve tissue formation under pulmonary arterial physiological flow conditions. J Biomech Eng. 2014;136(12):1210091–12100914.  https://doi.org/10.1115/1.4028815.CrossRefPubMedCentralGoogle Scholar
  88. 88.
    Weber M, Heta E, Moreira R, Gesche VN, Schermer T, Frese J, et al. Tissue-engineered fibrin-based heart valve with a tubular leaflet design. Tissue Eng Part C Methods. 2014;20(4):265–75.  https://doi.org/10.1089/ten.TEC.2013.0258.CrossRefPubMedGoogle Scholar
  89. 89.
    Cox JL, Ad N, Myers K, Gharib M, Quijano RC. Tubular heart valves: a new tissue prosthesis design—preclinical evaluation of the 3F aortic bioprosthesis. J Thorac Cardiovasc Surg. 2005;130(2):520–7.  https://doi.org/10.1016/j.jtcvs.2004.12.054.CrossRefPubMedGoogle Scholar
  90. 90.
    Syedain ZH, Meier LA, Reimer JM, Tranquillo RT. Tubular heart valves from decellularized engineered tissue. Ann Biomed Eng. 2013;41(12):2645–54.  https://doi.org/10.1007/s10439-013-0872-9.CrossRefPubMedGoogle Scholar
  91. 91.
    Driessen-Mol A, Emmert MY, Dijkman PE, Frese L, Sanders B, Weber B, et al. Transcatheter implantation of homologous “off-the-shelf” tissue-engineered heart valves with self-repair capacity: long-term functionality and rapid in vivo remodeling in sheep. J Am Coll Cardiol. 2014;63(13):1320–9.  https://doi.org/10.1016/j.jacc.2013.09.082.CrossRefPubMedGoogle Scholar
  92. 92.
    Moreira R, Velz T, Alves N, Gesche VN, Malischewski A, Schmitz-Rode T, et al. Tissue-engineered heart valve with a tubular leaflet design for minimally invasive transcatheter implantation. Tissue Eng Part C Methods. 2015;21(6):530–40.  https://doi.org/10.1089/ten.TEC.2014.0214.CrossRefPubMedPubMedCentralGoogle Scholar
  93. 93.
    Reimer JM, Syedain ZH, Haynie BH, Tranquillo RT. Pediatric tubular pulmonary heart valve from decellularized engineered tissue tubes. Biomaterials. 2015;62:88–94.  https://doi.org/10.1016/j.biomaterials.2015.05.009.CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Dijkman PE, Driessen-Mol A, Frese L, Hoerstrup SP, Baaijens FP. Decellularized homologous tissue-engineered heart valves as off-the-shelf alternatives to xeno- and homografts. Biomaterials. 2012;33(18):4545–54.  https://doi.org/10.1016/j.biomaterials.2012.03.015.CrossRefPubMedGoogle Scholar
  95. 95.
    Sodian R, Lueders C, Kraemer L, Kuebler W, Shakibaei M, Reichart B, et al. Tissue engineering of autologous human heart valves using cryopreserved vascular umbilical cord cells. Ann Thorac Surg. 2006;81(6):2207–16.  https://doi.org/10.1016/j.athoracsur.2005.12.073.CrossRefPubMedGoogle Scholar
  96. 96.
    Robinson PS, Tranquillo RT. Planar biaxial behavior of fibrin-based tissue-engineered heart valve leaflets. Tissue Eng Part A. 2009;15(10):2763–72.  https://doi.org/10.1089/ten.tea.2008.0426.CrossRefPubMedPubMedCentralGoogle Scholar
  97. 97.
    Kelley TA, Marquez S, Popelar CF. In vitro testing of heart valve substitutes. In: Iaizzo PA, Bianco R, Hill AJ, St. Louis JD, editors. Heart valves: from design to clinical implantation. New York: Springer; 2013. p. 283–320.CrossRefGoogle Scholar
  98. 98.
    Ahlberg SE, Bateman MG, Eggen MD, Quill JL, Richardson ES, Iaizzo PA. Animal models for cardiac valve research. In: Iaizzo PA, Bianco R, Hill AJ, St. Louis JD, editors. Heart valves: from design to clinical implantation. New York: Springer; 2013. p. 343–57.CrossRefGoogle Scholar
  99. 99.
    Weber B, Dijkman PE, Scherman J, Sanders B, Emmert MY, Grunenfelder J, et al. Off-the-shelf human decellularized tissue-engineered heart valves in a non-human primate model. Biomaterials. 2013;34(30):7269–80.  https://doi.org/10.1016/j.biomaterials.2013.04.059.CrossRefPubMedGoogle Scholar
  100. 100.
    Roosens B, Bala G, Droogmans S, Van Camp G, Breyne J, Cosyns B. Animal models of organic heart valve disease. Int J Cardiol. 2013;165(3):398–409.  https://doi.org/10.1016/j.ijcard.2012.03.065.CrossRefPubMedGoogle Scholar
  101. 101.
    Gottlieb D, Fata B, Powell AJ, Cois CA, Annese D, Tandon K, et al. Pulmonary artery conduit in vivo dimensional requirements in a growing ovine model: comparisons with the ascending aorta. J Heart Valve Dis. 2013;22(2):195–203.PubMedGoogle Scholar
  102. 102.
    Molina JE, Edwards JE, Bianco RW, Clack RW, Lang G, Molina JR. Composite and plain tubular synthetic graft conduits in right ventricle-pulmonary artery position: fate in growing lambs. J Thorac Cardiovasc Surg. 1995;110(2):427–35.CrossRefGoogle Scholar
  103. 103.
    Akay HO, Ozmen CA, Bayrak AH, Senturk S, Katar S, Nazaroglu H, et al. Diameters of normal thoracic vascular structures in pediatric patients. Surg Radiol Anat. 2009;31(10):801–7.  https://doi.org/10.1007/s00276-009-0525-8.CrossRefPubMedGoogle Scholar
  104. 104.
    Shinoka T, Breuer CK, Tanel RE, Zund G, Miura T, Ma PX, et al. Tissue engineering heart valves: valve leaflet replacement study in a lamb model. Ann Thorac Surg. 1995;60(6 Suppl):S513–6.CrossRefGoogle Scholar
  105. 105.
    Schmidt D, Dijkman PE, Driessen-Mol A, Stenger R, Mariani C, Puolakka A, et al. Minimally-invasive implantation of living tissue engineered heart valves. J Am Coll Cardiol. 2010;56(6):510–20.  https://doi.org/10.1016/j.jacc.2010.04.024.CrossRefPubMedGoogle Scholar
  106. 106.
    Weber B, Scherman J, Emmert MY, Gruenenfelder J, Verbeek R, Bracher M, et al. Injectable living marrow stromal cell-based autologous tissue engineered heart valves: first experiences with a one-step intervention in primates. Eur Heart J. 2011;32(22):2830–40.  https://doi.org/10.1093/eurheartj/ehr059.CrossRefPubMedPubMedCentralGoogle Scholar
  107. 107.
    Nakayama Y, Takewa Y, Sumikura H, Yamanami M, Matsui Y, Oie T, et al. In-body tissue-engineered aortic valve (Biovalve type VII) architecture based on 3D printer molding. J Biomed Mater Res B Appl Biomater. 2015;103(1):1–11.  https://doi.org/10.1002/jbm.b.33186.CrossRefPubMedGoogle Scholar
  108. 108.
    Yamanami M, Yahata Y, Uechi M, Fujiwara M, Ishibashi-Ueda H, Kanda K, et al. Development of a completely autologous valved conduit with the sinus of Valsalva using in-body tissue architecture technology: a pilot study in pulmonary valve replacement in a beagle model. Circulation. 2010;122(11 Suppl):S100–6.  https://doi.org/10.1161/CIRCULATIONAHA.109.922211.CrossRefPubMedGoogle Scholar
  109. 109.
    Flanagan TC, Sachweh JS, Frese J, Schnoring H, Gronloh N, Koch S, et al. In vivo remodeling and structural characterization of fibrin-based tissue-engineered heart valves in the adult sheep model. Tissue Eng Part A. 2009;15(10):2965–76.  https://doi.org/10.1089/ten.TEA.2009.0018.CrossRefGoogle Scholar
  110. 110.
    Syedain ZH, Lahti MT, Johnson SL, Robinson PS, Ruth GR, Bianco RW, et al. Implantation of a tissue-engineered heart valve from human fibroblasts exhibiting short term function in the sheep pulmonary artery. Cardiovasc Eng Technol. 2011;2(2):101–12.  https://doi.org/10.1007/s13239-011-0039-5.CrossRefGoogle Scholar
  111. 111.
    Syedain Z, Reimer J, Schmidt J, Lahti M, Berry J, Bianco R, et al. 6-Month aortic valve implantation of an off-the-shelf tissue-engineered valve in sheep. Biomaterials. 2015;73:175–84.  https://doi.org/10.1016/j.biomaterials.2015.09.016.CrossRefPubMedPubMedCentralGoogle Scholar
  112. 112.
    Emmert MY, Weber B, Behr L, Sammut S, Frauenfelder T, Wolint P, et al. Transcatheter aortic valve implantation using anatomically oriented, marrow stromal cell-based, stented, tissue-engineered heart valves: technical considerations and implications for translational cell-based heart valve concepts. Eur J Cardiothorac Surg. 2014;45(1):61–8.  https://doi.org/10.1093/ejcts/ezt243.CrossRefPubMedGoogle Scholar
  113. 113.
    Reimer J, Syedain Z, Haynie B, Lahti M, Berry J, Tranquillo R. Implantation of a tissue-engineered tubular heart valve in growing lambs. Ann Biomed Eng. 2017;45(2):439–451.CrossRefGoogle Scholar
  114. 114.
    Schoen FJ. Heart valve tissue engineering: quo vadis? Curr Opin Biotechnol. 2011;22(5):698–705.  https://doi.org/10.1016/j.copbio.2011.01.004.CrossRefPubMedGoogle Scholar

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© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Department of Biomedical EngineeringUniversity of MinnesotaMinneapolisUSA

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