Advertisement

Bioprosthetic Heart Valves: From a Biomaterials Perspective

  • Naren VyavahareEmail author
  • Hobey Tam
Chapter

Abstract

For the past 50+ years, the heart valve replacement (HVR) industry has gone through multiple growth phases in terms of innovation and market growth, and is now a formidable submarket of the cardiovascular medical device space. HVRs started off as small, compact simplistic devices made from synthetic parts. Now, these archaic prototypes have evolved into a diverse product offering from a multitude of small to large healthcare firms that range from completely synthetic materials to crosslinked tissue-based HVRs to new research being performed to investigate engineered tissue valves. These innovative leaps in technology and growth in commerce would not have been possible without the collaboration of multidisciplinary investigators unified through their passion in pursuing one goal—a superior healthcare option that resulted in a better quality of life for individuals throughout the world needing a new heart valve. Everything from biomaterial design to micro/macro-biomechanics to build computational modeling to optimize valve design has been utilized to create the current product line and are currently still in use as our metrics and methods get more advanced to innovate the future of heart valves as well as cardiovascular device technology. The future of HVRs rests on academia and industry coming together to move technology forward to provide patients in dire need of a more durable HVR device. Therefore, the rest of the content covered in this book is a comprehensive review of current art and models in existence to design an effective HVR in the efforts of empowering individuals wishing to bring healthcare options to a patient segment in dire need of change. The following chapter will cover past and current approaches in designing and fabricating HVR materials, current performance of HVRs, material design considerations of next generation materials, and major research interests in the next generation of HVR materials. The rest of this publication will cover approaches in properly leveraging this base biomaterial in valve-specific design to innovate a more effective HVR.

Key words

Xenografts Heart valve replacement Tissue-based materials Tissue crosslinking Heart valve design 

References

  1. 1.
    Research and markets adds report: US implantable medical devices market report 2013–2018—reconstructive joint replacement, spinal implants, cardiovascular implants, dental implants, intraocular lens and breast implants, professional services close-up. 2013.Google Scholar
  2. 2.
    Manji RA, Menkis AH, Ekser B, Cooper DK. Porcine bioprosthetic heart valves: the next generation. Am Heart J. 2012;164(2):177–85.PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Schoen FJ. Cardiac valves and valvular pathology: update on function, disease, repair, and replacement. Cardiovasc Pathol. 2005;14(4):189–94.PubMedCrossRefGoogle Scholar
  4. 4.
    Yacoub MH. Establishing pediatric cardiovascular services in the developing world: a wake-up call. Circulation. 2007;116(17):1876–8.PubMedCrossRefGoogle Scholar
  5. 5.
    Zilla P, Brink J, Human P, Bezuidenhout D. Prosthetic heart valves: catering for the few. Biomaterials. 2008;29(4):385–406.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Kidane AG, Burriesci G, Cornejo P, Dooley A, Sarkar S, Bonhoeffer P, Edirisinghe M, Seifalian AM. Current developments and future prospects for heart valve replacement therapy. J Biomed Mater Res B Appl Biomater. 2009;88(1):290–303.PubMedCrossRefGoogle Scholar
  7. 7.
    Schoen FJ. Evolving concepts of cardiac valve dynamics: the continuum of development, functional structure, pathobiology, and tissue engineering. Circulation. 2008;118(18):1864–80.PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Siddiqui RF, Abraham JR, Butany J. Bioprosthetic heart valves: modes of failure. Histopathology. 2009;55(2):135–44.PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Writing Group Members, Lloyd-Jones D, Adams RJ, Brown TM, Carnethon M, Dai S, De Simone G, Ferguson TB, Ford E, Furie K, Gillespie C, Go A, Greenlund K, Haase N, Hailpern S, Ho PM, Howard V, Kissela B, Kittner S, Lackland D, Lisabeth L, Marelli A, McDermott MM, Meigs J, Mozaffarian D, Mussolino M, Nichol G, Roger VL, Rosamond W, Sacco R, Sorlie P, Roger VL, Thom T, Wasserthiel-Smoller S, Wong ND, Wylie-Rosett J, American Heart Association Statistics Committee, Stroke Statistics Subcommittee. Heart disease and stroke statistics—2010 update: a report from the American Heart Association. Circulation. 2010;121(7):e46–e215.Google Scholar
  10. 10.
    Cotran RS, Kumar V, Collins T. Robbins pathologic basis of disease. 6th ed. Philadelphia, PA: W.B. Saunders; 1999.Google Scholar
  11. 11.
    Akat K, Borggrefe M, Kaden JJ. Aortic valve calcification: basic science to clinical practice. Heart. 2009;95(8):616–23.PubMedCrossRefPubMedCentralGoogle Scholar
  12. 12.
    Weska RF, Aimoli CG, Nogueira GM, Leirner AA, Maizato MJ, Higa OZ, Polakievicz B, Pitombo RN, Beppu MM. Natural and prosthetic heart valve calcification: morphology and chemical composition characterization. Artif Organs. 2010;34(4):311–8.PubMedCrossRefPubMedCentralGoogle Scholar
  13. 13.
    Lee WJ, Son CW, Yoon JC, Jo HS, Son JW, Park KH, Lee SH, Shin DG, Hong GR, Park JS, Kim YJ. Massive left atrial calcification associated with mitral valve replacement. J Cardiovasc Ultrasound. 2010;18(4):151–3.PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    O’Brien KD. Pathogenesis of calcific aortic valve disease: a disease process comes of age (and a good deal more). Arterioscler Thromb Vasc Biol. 2006;26(8):1721–8.PubMedCrossRefPubMedCentralGoogle Scholar
  15. 15.
    Freeman RV, Otto CM. Spectrum of calcific aortic valve disease: pathogenesis, disease progression, and treatment strategies. Circulation. 2005;111(24):3316–26.CrossRefGoogle Scholar
  16. 16.
    Piazza N, Lange R, Martucci G, Serruys PW. Patient selection for transcatheter aortic valve implantation: patient risk profile and anatomical selection criteria. Arch Cardiovasc Dis. 2012;105(3):165–73.PubMedCrossRefPubMedCentralGoogle Scholar
  17. 17.
    Li C, Xu S, Gotlieb AI. The response to valve injury. A paradigm to understand the pathogenesis of heart valve disease. Cardiovasc Pathol. 2011;20(3):183–90.PubMedCrossRefPubMedCentralGoogle Scholar
  18. 18.
    Siu SC, Silversides CK. Bicuspid aortic valve disease. J Am Coll Cardiol. 2010;55(25):2789–800.PubMedCrossRefPubMedCentralGoogle Scholar
  19. 19.
    Que YA, Moreillon P. Infective endocarditis. Nat Rev Cardiol. 2011;8(6):322–36.PubMedCrossRefGoogle Scholar
  20. 20.
    El-Ahdab F, Benjamin DK Jr, Wang A, Cabell CH, Chu VH, Stryjewski ME, Corey GR, Sexton DJ, Reller LB, Fowler VG Jr. Risk of endocarditis among patients with prosthetic valves and Staphylococcus aureus bacteremia. Am J Med. 2005;118(3):225–9.PubMedCrossRefPubMedCentralGoogle Scholar
  21. 21.
    Giessel BE, Koenig CJ, Blake RL Jr. Management of bacterial endocarditis. Am Fam Physician. 2000;61(6):1725–32, 1739.PubMedPubMedCentralGoogle Scholar
  22. 22.
    Griffin FM Jr, Jones G, Cobbs CC. Aortic insufficiency in bacterial endocarditis. Ann Intern Med. 1972;76(1):23–8.PubMedCrossRefPubMedCentralGoogle Scholar
  23. 23.
    Jegatheeswaran A, Butany J. Pathology of infectious and inflammatory diseases in prosthetic heart valves. Cardiovasc Pathol. 2006;15(5):252–5.PubMedCrossRefPubMedCentralGoogle Scholar
  24. 24.
    Guilherme L, Kalil J. Rheumatic fever: from innate to acquired immune response. Ann N Y Acad Sci. 2007;1107:426–33.PubMedCrossRefPubMedCentralGoogle Scholar
  25. 25.
    Guilherme L, Kalil J. Rheumatic fever and rheumatic heart disease: cellular mechanisms leading autoimmune reactivity and disease. J Clin Immunol. 2010;30(1):17–23.PubMedCrossRefPubMedCentralGoogle Scholar
  26. 26.
    Guilherme L, Ramasawmy R, Kalil J. Rheumatic fever and rheumatic heart disease: genetics and pathogenesis. Scand J Immunol. 2007;66(2–3):199–207.PubMedCrossRefPubMedCentralGoogle Scholar
  27. 27.
    Baasanjav S, Al-Gazali L, Hashiguchi T, Mizumoto S, Fischer B, Horn D, Seelow D, Ali BR, Aziz SA, Langer R, Saleh AA, Becker C, Nurnberg G, Cantagrel V, Gleeson JG, Gomez D, Michel JB, Stricker S, Lindner TH, Nurnberg P, Sugahara K, Mundlos S, Hoffmann K. Faulty initiation of proteoglycan synthesis causes cardiac and joint defects. Am J Hum Genet. 2011;89(1):15–27.PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Olivier C. Rheumatic fever—is it still a problem? J Antimicrob Chemother. 2000;45(Suppl):13–21.PubMedCrossRefPubMedCentralGoogle Scholar
  29. 29.
    Becker AE. Acquired heart valve pathology. An update for the millennium. Herz. 1998;23(7):415–9.PubMedCrossRefPubMedCentralGoogle Scholar
  30. 30.
    Maganti K, Rigolin VH, Sarano ME, Bonow RO. Valvular heart disease: diagnosis and management. Mayo Clin Proc. 2010;85(5):483–500.PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Simionescu A, Simionescu DT, Vyavahare NR. Osteogenic responses in fibroblasts activated by elastin degradation products and transforming growth factor-beta1: role of myofibroblasts in vascular calcification. Am J Pathol. 2007;171(1):116–23.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Liu AC, Joag VR, Gotlieb AI. The emerging role of valve interstitial cell phenotypes in regulating heart valve pathobiology. Am J Pathol. 2007;171(5):1407–18.PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Gott VL, Alejo DE, Cameron DE. Mechanical heart valves: 50 years of evolution. Ann Thorac Surg. 2003;76(6):S2230–9.PubMedCrossRefGoogle Scholar
  34. 34.
    Bahnson HT, Spencer FC, Busse EF, Davis FW. Cusp replacement and coronary artery perfusion in open operations on the aortic valve. Ann Surg. 1960;152(3):494–503.PubMedPubMedCentralGoogle Scholar
  35. 35.
    Chiam PT, Ruiz CE. Percutaneous transcatheter aortic valve implantation: evolution of the technology. Am Heart J. 2009;157(2):229–42.PubMedCrossRefGoogle Scholar
  36. 36.
    Fann JI, Chronos N, Rowe SJ, Michiels R, Lyons BE, Leon MB, Kaplan AV. Evolving strategies for the treatment of valvular heart disease: preclinical and clinical pathways for percutaneous aortic valve replacement. Catheter Cardiovasc Interv. 2008;71(3):434–40.PubMedCrossRefGoogle Scholar
  37. 37.
    Ghanbari H, Viatge H, Kidane AG, Burriesci G, Tavakoli M, Seifalian AM. Polymeric heart valves: new materials, emerging hopes. Trends Biotechnol. 2009;27(6):359–67.PubMedCrossRefGoogle Scholar
  38. 38.
    Zeltinger J, Landeen LK, Alexander HG, Kidd ID, Sibanda B. Development and characterization of tissue-engineered aortic valves. Tissue Eng. 2001;7(1):9–22.PubMedCrossRefGoogle Scholar
  39. 39.
    Pibarot P, Dumesnil JG. Prosthetic heart valves: selection of the optimal prosthesis and long-term management. Circulation. 2009;119(7):1034–48.PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Bachraoui K, Darghouth B, Haddad W, Saaidi I, Ben Halima A, Sdiri W, Selmi K, Makni H, Mokaddem A, Boujnah MR. [Pregnancy in patients with prosthetic heart valves]. Tunis Med. 2003;81(Suppl 8):613–6.Google Scholar
  41. 41.
    Khamooshi AJ, Kashfi F, Hoseini S, Tabatabaei MB, Javadpour H, Noohi F. Anticoagulation for prosthetic heart valves in pregnancy. Is there an answer? Asian Cardiovasc Thorac Ann. 2007;15(6):493–6.PubMedCrossRefGoogle Scholar
  42. 42.
    Sillesen M, Hjortdal V, Vejlstrup N, Sorensen K. Pregnancy with prosthetic heart valves—30 years’ nationwide experience in Denmark. Eur J Cardiothorac Surg. 2011;40(2):448–54.PubMedGoogle Scholar
  43. 43.
    Jonkaitiene R, Benetis R, Eidukaityte R. [Management of patients with prosthetic heart valves]. Medicina (Kaunas). 2005;41(7):553–60.Google Scholar
  44. 44.
    Vink R, Van Den Brink RB, Levi M. Management of anticoagulant therapy for patients with prosthetic heart valves or atrial fibrillation. Hematology. 2004;9(1):1–9.PubMedCrossRefGoogle Scholar
  45. 45.
    Simionescu D. Artificial heart valves. Hoboken, NJ: Wiley; 2006.CrossRefGoogle Scholar
  46. 46.
    Alsoufi B, Manlhiot C, McCrindle BW, Canver CC, Sallehuddin A, Al-Oufi S, Joufan M, Al-Halees Z. Aortic and mitral valve replacement in children: is there any role for biologic and bioprosthetic substitutes? Eur J Cardiothorac Surg. 2009;36(1):84–90; discussion 90.PubMedCrossRefGoogle Scholar
  47. 47.
    Sako EY. Newer concepts in the surgical treatment of valvular heart disease. Curr Cardiol Rep. 2004;6(2):100–5.PubMedCrossRefGoogle Scholar
  48. 48.
    Harken DE, Taylor WJ, Lefemine AA, Lunzer S, Low HB, Cohen ML, Jacobey JA. Aortic valve replacement with a caged ball valve. Am J Cardiol. 1962;9:292–9.PubMedCrossRefGoogle Scholar
  49. 49.
    Schoen FJ, Levy RJ. Calcification of tissue heart valve substitutes: progress toward understanding and prevention. Ann Thorac Surg. 2005;79(3):1072–80.PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Calisi P, Griffo R. [Anticoagulation in patients with heart valve prosthesis]. Monaldi Arch Chest Dis. 2002;58(2):121–7.Google Scholar
  51. 51.
    Frater RW. The development of the Starr-Edwards heart valve. Tex Heart Inst J. 1999;26(1):99.PubMedPubMedCentralGoogle Scholar
  52. 52.
    Blot WJ, Ibrahim MA, Ivey TD, Acheson DE, Brookmeyer R, Weyman A, Defauw J, Smith JK, Harrison D. Twenty-five-year experience with the Bjork-Shiley convexoconcave heart valve: a continuing clinical concern. Circulation. 2005;111(21):2850–7.PubMedCrossRefGoogle Scholar
  53. 53.
    Butany J, Collins MJ. Analysis of prosthetic cardiac devices: a guide for the practising pathologist. J Clin Pathol. 2005;58(2):113–24.PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Bourguignon T, Bouquiaux-Stablo AL, Candolfi P, Mirza A, Loardi C, May MA, El-Khoury R, Marchand M, Aupart M. Very long-term outcomes of the Carpentier-Edwards Perimount valve in aortic position. Ann Thorac Surg. 2015;99(3):831–7.PubMedCrossRefGoogle Scholar
  55. 55.
    Takkenberg JJ, van Herwerden LA, Eijkemans MJ, Bekkers JA, Bogers AJ. Evolution of allograft aortic valve replacement over 13 years: results of 275 procedures. Eur J Cardiothorac Surg. 2002;21(4):683–91; discussion 691.PubMedCrossRefGoogle Scholar
  56. 56.
    Isaacs AJ, Shuhaiber J, Salemi A, Isom OW, Sedrakyan A. National trends in utilization and in-hospital outcomes of mechanical versus bioprosthetic aortic valve replacements. J Thorac Cardiovasc Surg. 2015;149(5):1262–9, e3.PubMedCrossRefGoogle Scholar
  57. 57.
    Bourguignon T, El Khoury R, Candolfi P, Loardi C, Mirza A, Boulanger-Lothion J, Bouquiaux-Stablo-Duncan AL, Espitalier F, Marchand M, Aupart M. Very long-term outcomes of the Carpentier-Edwards Perimount aortic valve in patients aged 60 or younger. Ann Thorac Surg. 2015;100(3):853–9.PubMedCrossRefGoogle Scholar
  58. 58.
    Johansen P. Mechanical heart valve cavitation. Expert Rev Med Devices. 2004;1(1):95–104.PubMedCrossRefGoogle Scholar
  59. 59.
    Vesely I. The evolution of bioprosthetic heart valve design and its impact on durability. Cardiovasc Pathol. 2003;12(5):277–86.PubMedCrossRefGoogle Scholar
  60. 60.
    Munnelly AE, Cochrane L, Leong J, Vyavahare NR. Porcine vena cava as an alternative to bovine pericardium in bioprosthetic percutaneous heart valves. Biomaterials. 2012;33(1):1–8.PubMedCrossRefGoogle Scholar
  61. 61.
    Lovekamp JJ, Simionescu DT, Mercuri JJ, Zubiate B, Sacks MS, Vyavahare NR. Stability and function of glycosaminoglycans in porcine bioprosthetic heart valves. Biomaterials. 2006;27(8):1507–18.PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Simionescu DT, Lovekamp JJ, Vyavahare NR. Glycosaminoglycan-degrading enzymes in porcine aortic heart valves: implications for bioprosthetic heart valve degeneration. J Heart Valve Dis. 2003;12(2):217–25.PubMedPubMedCentralGoogle Scholar
  63. 63.
    Simionescu DT, Lovekamp JJ, Vyavahare NR. Extracellular matrix degrading enzymes are active in porcine stentless aortic bioprosthetic heart valves. J Biomed Mater Res A. 2003;66(4):755–63.PubMedCrossRefGoogle Scholar
  64. 64.
    Vyavahare N, Ogle M, Schoen FJ, Zand R, Gloeckner DC, Sacks M, Levy RJ. Mechanisms of bioprosthetic heart valve failure: fatigue causes collagen denaturation and glycosaminoglycan loss. J Biomed Mater Res. 1999;46(1):44–50.PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Simionescu DT, Lovekamp JJ, Vyavahare NR. Degeneration of bioprosthetic heart valve cusp and wall tissues is initiated during tissue preparation: an ultrastructural study. J Heart Valve Dis. 2003;12(2):226–34.PubMedGoogle Scholar
  66. 66.
    Isenburg JC, Simionescu DT, Vyavahare NR. Elastin stabilization in cardiovascular implants: improved resistance to enzymatic degradation by treatment with tannic acid. Biomaterials. 2004;25(16):3293–302.PubMedCrossRefGoogle Scholar
  67. 67.
    Chiang YP, Chikwe J, Moskowitz AJ, Itagaki S, Adams DH, Egorova NN. Survival and long-term outcomes following bioprosthetic vs mechanical aortic valve replacement in patients aged 50 to 69 years. JAMA. 2014;312(13):1323–9.PubMedCrossRefGoogle Scholar
  68. 68.
    Dasi LP, Simon HA, Sucosky P, Yoganathan AP. Fluid mechanics of artificial heart valves. Clin Exp Pharmacol Physiol. 2009;36(2):225–37.PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Butany J, Fayet C, Ahluwalia MS, Blit P, Ahn C, Munroe C, Israel N, Cusimano RJ, Leask RL. Biological replacement heart valves. Identification and evaluation. Cardiovasc Pathol. 2003;12(3):119–39.PubMedCrossRefGoogle Scholar
  70. 70.
    Crick SJ, Sheppard MN, Ho SY, Gebstein L, Anderson RH. Anatomy of the pig heart: comparisons with normal human cardiac structure. J Anat. 1998;193(Pt 1):105–19.PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Hoffmann G, Lutter G, Cremer J. Durability of bioprosthetic cardiac valves. Dtsch Arztebl Int. 2008;105(8):143–8.PubMedPubMedCentralGoogle Scholar
  72. 72.
    Wells SM, Sellaro T, Sacks MS. Cyclic loading response of bioprosthetic heart valves: effects of fixation stress state on the collagen fiber architecture. Biomaterials. 2005;26(15):2611–9.PubMedCrossRefGoogle Scholar
  73. 73.
    Sun W, Sacks M, Fulchiero G, Lovekamp J, Vyavahare N, Scott M. Response of heterograft heart valve biomaterials to moderate cyclic loading. J Biomed Mater Res A. 2004;69(4):658–69.PubMedCrossRefGoogle Scholar
  74. 74.
    Martin C, Sun W. Modeling of long-term fatigue damage of soft tissue with stress softening and permanent set effects. Biomech Model Mechanobiol. 2013;12(4):645–55.PubMedCrossRefGoogle Scholar
  75. 75.
    Smith DB, Sacks MS, Pattany PM, Schroeder R. High-resolution magnetic resonance imaging to characterize the geometry of fatigued porcine bioprosthetic heart valves. J Heart Valve Dis. 1997;6(4):424–32.PubMedGoogle Scholar
  76. 76.
    Sacks MS, Schoen FJ. Collagen fiber disruption occurs independent of calcification in clinically explanted bioprosthetic heart valves. J Biomed Mater Res. 2002;62(3):359–71.PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Sacks MS. The biomechanical effects of fatigue on the porcine bioprosthetic heart valve. J Long-Term Eff Med Implants. 2001;11(3–4):231–47.PubMedGoogle Scholar
  78. 78.
    Billiar KL, Sacks MS. Biaxial mechanical properties of the natural and glutaraldehyde treated aortic valve cusp—part I: experimental results. J Biomech Eng. 2000;122(1):23–30.PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    Sacks MS, David Merryman W, Schmidt DE. On the biomechanics of heart valve function. J Biomech. 2009;42(12):1804–24.PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Stella JA, Sacks MS. On the biaxial mechanical properties of the layers of the aortic valve leaflet. J Biomech Eng. 2007;129(5):757–66.CrossRefGoogle Scholar
  81. 81.
    Lee TC, Midura RJ, Hascall VC, Vesely I. The effect of elastin damage on the mechanics of the aortic valve. J Biomech. 2001;34(2):203–10.PubMedCrossRefGoogle Scholar
  82. 82.
    Vesely I. The role of elastin in aortic valve mechanics. J Biomech. 1998;31(2):115–23.PubMedCrossRefGoogle Scholar
  83. 83.
    Eckert CE, Fan R, Mikulis B, Barron M, Carruthers CA, Friebe VM, Vyavahare NR, Sacks MS. On the biomechanical role of glycosaminoglycans in the aortic heart valve leaflet. Acta Biomater. 2013;9(1):4653–60.PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Sierad LN, Simionescu A, Albers C, Chen J, Maivelett J, Tedder ME, Liao J, Simionescu DT. Design and testing of a pulsatile conditioning system for dynamic endothelialization of polyphenol-stabilized tissue engineered heart valves. Cardiovasc Eng Technol. 2010;1(2):138–53.PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Scott M, Vesely I. Aortic valve cusp microstructure: the role of elastin. Ann Thorac Surg. 1995;60(2 Suppl):S391–4.PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Grande-Allen KJ, Mako WJ, Calabro A, Shi Y, Ratliff NB, Vesely I. Loss of chondroitin 6-sulfate and hyaluronan from failed porcine bioprosthetic valves. J Biomed Mater Res A. 2003;65(2):251–9.PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Butany J, Feng T, Luk A, Law K, Suri R, Nair V. Modes of failure in explanted mitroflow pericardial valves. Ann Thorac Surg. 2011;92(5):1621–7.PubMedCrossRefGoogle Scholar
  88. 88.
    Vongpatanasin W, Hillis LD, Lange RA. Prosthetic heart valves. N Engl J Med. 1996;335(6):407–16.PubMedCrossRefGoogle Scholar
  89. 89.
    Farhat F, Durand M, Delahaye F, Jegaden O. Prosthetic valve sewing-ring sealing with antibiotic and fibrin glue in infective endocarditis. A prospective clinical study. Interact Cardiovasc Thorac Surg. 2007;6(1):16–20.PubMedCrossRefGoogle Scholar
  90. 90.
    Lepidi H, Casalta JP, Fournier PE, Habib G, Collart F, Raoult D. Quantitative histological examination of bioprosthetic heart valves. Clin Infect Dis. 2006;42(5):590–6.PubMedCrossRefPubMedCentralGoogle Scholar
  91. 91.
    Irving CA, Kelly D, Gould FK, O’Sullivan JJ. Successful medical treatment of bioprosthetic pulmonary valve endocarditis caused by methicillin-resistant Staphylococcus aureus. Pediatr Cardiol. 2010;31(4):553–5.PubMedCrossRefPubMedCentralGoogle Scholar
  92. 92.
    McAllister RG Jr, Samet J, Mazzoleni A, Dillon ML. Endocarditis on prosthetic mitral valves. Fatal obstruction to left ventricular inflow. Chest. 1974;66(6):682–6.PubMedCrossRefPubMedCentralGoogle Scholar
  93. 93.
    Zilla P, Human P, Bezuidenhout D. Bioprosthetic heart valves: the need for a quantum leap. Biotechnol Appl Biochem. 2004;40(Pt 1):57–66.PubMedPubMedCentralGoogle Scholar
  94. 94.
    Beauchesne LM, Veinot JP, Higginson LA, Mesana T. Severe aortic insufficiency secondary to an aortic bioprosthesis tear. Cardiovasc Pathol. 2004;13(3):165–7.PubMedCrossRefPubMedCentralGoogle Scholar
  95. 95.
    Raghavan D, Simionescu DT, Vyavahare NR. Neomycin prevents enzyme-mediated glycosaminoglycan degradation in bioprosthetic heart valves. Biomaterials. 2007;28(18):2861–8.PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Mercuri JJ, Lovekamp JJ, Simionescu DT, Vyavahare NR. Glycosaminoglycan-targeted fixation for improved bioprosthetic heart valve stabilization. Biomaterials. 2007;28(3):496–503.PubMedCrossRefPubMedCentralGoogle Scholar
  97. 97.
    Leong J, Munnelly A, Liberio B, Cochrane L, Vyavahare N. Neomycin and carbodiimide crosslinking as an alternative to glutaraldehyde for enhanced durability of bioprosthetic heart valves. J Biomater Appl. 2013;27(8):948–60.PubMedCrossRefPubMedCentralGoogle Scholar
  98. 98.
    Raghavan D, Shah SR, Vyavahare NR. Neomycin fixation followed by ethanol pretreatment leads to reduced buckling and inhibition of calcification in bioprosthetic valves. J Biomed Mater Res B Appl Biomater. 2010;92(1):168–77.PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    Friebe VM, Mikulis B, Kole S, Ruffing CS, Sacks MS, Vyavahare NR. Neomycin enhances extracellular matrix stability of glutaraldehyde crosslinked bioprosthetic heart valves. J Biomed Mater Res B Appl Biomater. 2011;99(2):217–29.PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Purinya B, Kasyanov V, Volkolakov J, Latsis R, Tetere G. Biomechanical and structural properties of the explanted bioprosthetic valve leaflets. J Biomech. 1994;27(1):1–11.PubMedCrossRefPubMedCentralGoogle Scholar
  101. 101.
    Broom N, Christie GW. The structure/function relationship of fresh and glutaraldehyde-fixed aortic valve leaflets. 1st ed. New York: Yorke Medical Books; 1982.Google Scholar
  102. 102.
    Schoen FJ. Aortic valve structure-function correlations: role of elastic fibers no longer a stretch of the imagination. J Heart Valve Dis. 1997;6(1):1–6.PubMedPubMedCentralGoogle Scholar
  103. 103.
    Strates B, Lian JB, Nimni ME. Calcification in cardiovascular tissues and bioprostheses. In: Nimni ME, editor. Biotechnology. Boca Raton, FL: CRC Press; 1989.Google Scholar
  104. 104.
    Shah SR, Vyavahare NR. The effect of glycosaminoglycan stabilization on tissue buckling in bioprosthetic heart valves. Biomaterials. 2008;29(11):1645–53.PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Mirnajafi A, Raymer JM, McClure LR, Sacks MS. The flexural rigidity of the aortic valve leaflet in the commissural region. J Biomech. 2006;39(16):2966–73.CrossRefGoogle Scholar
  106. 106.
    Erdmann E, Schwinger RH, Beuckelmann D, Bohm M. [Altered calcium homeostasis in chronic heart failure]. Z Kardiol. 1996;85(Suppl 6):123–8.Google Scholar
  107. 107.
    Li L, van Breemen C. Na(+)-Ca2+ exchange in intact endothelium of rabbit cardiac valve. Circ Res. 1995;76(3):396–404.PubMedCrossRefPubMedCentralGoogle Scholar
  108. 108.
    Levy RJ, Schoen FJ, Flowers WB, Staelin ST. Initiation of mineralization in bioprosthetic heart valves: studies of alkaline phosphatase activity and its inhibition by AlCl3 or FeCl3 preincubations. J Biomed Mater Res. 1991;25(8):905–35.PubMedCrossRefPubMedCentralGoogle Scholar
  109. 109.
    Lovekamp J, Vyavahare N. Periodate-mediated glycosaminoglycan stabilization in bioprosthetic heart valves. J Biomed Mater Res. 2001;56(4):478–86.PubMedCrossRefPubMedCentralGoogle Scholar
  110. 110.
    Jorge-Herrero E, Fernandez P, Gutierrez M, Castillo-Olivares JL. Study of the calcification of bovine pericardium: analysis of the implication of lipids and proteoglycans. Biomaterials. 1991;12(7):683–9.PubMedCrossRefGoogle Scholar
  111. 111.
    Khor E. Methods for the treatment of collagenous tissues for bioprostheses. Biomaterials. 1997;18(2):95–105.PubMedCrossRefGoogle Scholar
  112. 112.
    Chanda J, Kuribayashi R, Abe T. Prevention of calcification in glutaraldehyde-treated porcine aortic and pulmonary valves. Ann Thorac Surg. 1997;64(4):1063–6.PubMedCrossRefGoogle Scholar
  113. 113.
    Vyavahare N, Hirsch D, Lerner E, Baskin JZ, Schoen FJ, Bianco R, Kruth HS, Zand R, Levy RJ. Prevention of bioprosthetic heart valve calcification by ethanol preincubation. Efficacy and mechanisms. Circulation. 1997;95(2):479–88.PubMedCrossRefGoogle Scholar
  114. 114.
    Bianco RW, Phillips R, Mrachek J, Witson J. Feasibility evaluation of a new pericardial bioprosthesis with dye mediated photo-oxidized bovine pericardial tissue. J Heart Valve Dis. 1996;5(3):317–22.PubMedGoogle Scholar
  115. 115.
    Connolly JM, Alferiev I, Clark-Gruel JN, Eidelman N, Sacks M, Palmatory E, Kronsteiner A, Defelice S, Xu J, Ohri R, Narula N, Vyavahare N, Levy RJ. Triglycidylamine crosslinking of porcine aortic valve cusps or bovine pericardium results in improved biocompatibility, biomechanics, and calcification resistance: chemical and biological mechanisms. Am J Pathol. 2005;166(1):1–13.PubMedPubMedCentralCrossRefGoogle Scholar
  116. 116.
    Vasudev SC, Chandy T, Umasankar MM, Sharma CP. Inhibition of bioprosthesis calcification due to synergistic effect of Fe/Mg ions to polyethylene glycol grafted bovine pericardium. J Biomater Appl. 2001;16(2):93–107.PubMedCrossRefGoogle Scholar
  117. 117.
    Vasudev SC, Chandy T. Polyethylene glycol-grafted bovine pericardium: a novel hybrid tissue resistant to calcification. J Mater Sci Mater Med. 1999;10(2):121–8.PubMedCrossRefGoogle Scholar
  118. 118.
    Zhai W, Lu X, Chang J, Zhou Y, Zhang H. Quercetin-crosslinked porcine heart valve matrix: mechanical properties, stability, anticalcification and cytocompatibility. Acta Biomater. 2010;6(2):389–95.PubMedCrossRefGoogle Scholar
  119. 119.
    Raghavan D, Starcher BC, Vyavahare NR. Neomycin binding preserves extracellular matrix in bioprosthetic heart valves during in vitro cyclic fatigue and storage. Acta Biomater. 2009;5(4):983–92.PubMedCrossRefGoogle Scholar
  120. 120.
    Everaerts F, Torrianni M, van Luyn M, van Wachem P, Feijen J, Hendriks M. Reduced calcification of bioprostheses, cross-linked via an improved carbodiimide based method. Biomaterials. 2004;25(24):5523–30.PubMedCrossRefGoogle Scholar
  121. 121.
    Everaerts F, Gillissen M, Torrianni M, Zilla P, Human P, Hendriks M, Feijen J. Reduction of calcification of carbodiimide-processed heart valve tissue by prior blocking of amine groups with monoaldehydes. J Heart Valve Dis. 2006;15(2):269–77.PubMedGoogle Scholar
  122. 122.
    Meuris B, Phillips R, Moore MA, Flameng W. Porcine stentless bioprostheses: prevention of aortic wall calcification by dye-mediated photo-oxidation. Artif Organs. 2003;27(6):537–43.PubMedCrossRefGoogle Scholar
  123. 123.
    Schoen FJ, Tsao JW, Levy RJ. Calcification of bovine pericardium used in cardiac valve bioprostheses. Implications for the mechanisms of bioprosthetic tissue mineralization. Am J Pathol. 1986;123(1):134–45.PubMedPubMedCentralGoogle Scholar
  124. 124.
    Schoen FJ, Levy RJ, Nelson AC, Bernhard WF, Nashef A, Hawley M. Onset and progression of experimental bioprosthetic heart valve calcification. Lab Invest. 1985;52(5):523–32.PubMedGoogle Scholar
  125. 125.
    Levy RJ, Schoen FJ, Sherman FS, Nichols J, Hawley MA, Lund SA. Calcification of subcutaneously implanted type I collagen sponges. Effects of formaldehyde and glutaraldehyde pretreatments. Am J Pathol. 1986;122(1):71–82.PubMedPubMedCentralGoogle Scholar
  126. 126.
    Golomb G, Schoen F, Smith M, Linden J, Dixon M, Levy R. The role of glutaraldehyde-induced cross-links in calcification of bovine pericardium used in cardiac valve bioprostheses. Am J Pathol. 1987;127(1):122–30.PubMedPubMedCentralGoogle Scholar
  127. 127.
    Rucker RB. Calcium binding to elastin. Adv Exp Med Biol. 1974;48(0):185–209.PubMedCrossRefGoogle Scholar
  128. 128.
    Levy RJ, Vyavahare N, Ogle M, Ashworth P, Bianco R, Schoen FJ. Inhibition of cusp and aortic wall calcification in ethanol- and aluminum-treated bioprosthetic heart valves in sheep: background, mechanisms, and synergism. J Heart Valve Dis. 2003;12(2):209–16; discussion 216.PubMedGoogle Scholar
  129. 129.
    Isenburg JC, Karamchandani NV, Simionescu DT, Vyavahare NR. Structural requirements for stabilization of vascular elastin by polyphenolic tannins. Biomaterials. 2006;27(19):3645–51.PubMedGoogle Scholar
  130. 130.
    Basalyga DM, Simionescu DT, Xiong W, Baxter BT, Starcher BC, Vyavahare NR. Elastin degradation and calcification in an abdominal aorta injury model: role of matrix metalloproteinases. Circulation. 2004;110(22):3480–7.PubMedPubMedCentralCrossRefGoogle Scholar
  131. 131.
    Dahm M, Lyman WD, Schwell AB, Factor SM, Frater RW. Immunogenicity of glutaraldehyde-tanned bovine pericardium. J Thorac Cardiovasc Surg. 1990;99(6):1082–90.PubMedGoogle Scholar
  132. 132.
    Dahm M, Husmann M, Eckhard M, Prufer D, Groh E, Oelert H. Relevance of immunologic reactions for tissue failure of bioprosthetic heart valves. Ann Thorac Surg. 1995;60(2 Suppl):S348–52.PubMedCrossRefGoogle Scholar
  133. 133.
    Christian AJ, Lin H, Alferiev IS, Connolly JM, Ferrari G, Hazen SL, Ischiropoulos H, Levy RJ. The susceptibility of bioprosthetic heart valve leaflets to oxidation. Biomaterials. 2014;35(7):2097–102.PubMedCrossRefGoogle Scholar
  134. 134.
    Everts V, van der Zee E, Creemers L, Beertsen W. Phagocytosis and intracellular digestion of collagen, its role in turnover and remodelling. Histochem J. 1996;28(4):229–45.PubMedCrossRefGoogle Scholar
  135. 135.
    Human P, Zilla P. The possible role of immune responses in bioprosthetic heart valve failure. J Heart Valve Dis. 2001;10(4):460–6.PubMedGoogle Scholar
  136. 136.
    Levy RJ, Schoen FJ, Howard SL. Mechanism of calcification of porcine bioprosthetic aortic valve cusps: role of T-lymphocytes. Am J Cardiol. 1983;52(5):629–31.PubMedCrossRefGoogle Scholar
  137. 137.
    Sellaro TL, Hildebrand D, Lu Q, Vyavahare N, Scott M, Sacks MS. Effects of collagen fiber orientation on the response of biologically derived soft tissue biomaterials to cyclic loading. J Biomed Mater Res A. 2007;80(1):194–205.PubMedCrossRefGoogle Scholar
  138. 138.
    Billiar KL, Sacks MS. Biaxial mechanical properties of the native and glutaraldehyde-treated aortic valve cusp: part II—a structural constitutive model. J Biomech Eng. 2000;122(4):327–35.PubMedPubMedCentralCrossRefGoogle Scholar
  139. 139.
    Zilla P, Weissenstein C, Bracher M, Human P. The anticalcific effect of glutaraldehyde detoxification on bioprosthetic aortic wall tissue in the sheep model. J Card Surg. 2001;16(6):467–72.PubMedCrossRefGoogle Scholar
  140. 140.
    Zilla P, Bezuidenhout D, Weissenstein C, van der Walt A, Human P. Diamine extension of glutaraldehyde crosslinks mitigates bioprosthetic aortic wall calcification in the sheep model. J Biomed Mater Res. 2001;56(1):56–64.PubMedCrossRefGoogle Scholar
  141. 141.
    Mendoza-Novelo B, Cauich-Rodríguez JV. Decellularization stabilization and functionalization of collagenous tissues used as cardiovascular biomaterials. In: Biomaterials—Physics and Chemistry; 2011. p. 159–82.Google Scholar
  142. 142.
    Bezuidenhout D, Oosthuysen A, Human P, Weissenstein C, Zilla P. The effects of cross-link density and chemistry on the calcification potential of diamine-extended glutaraldehyde-fixed bioprosthetic heart-valve materials. Biotechnol Appl Biochem. 2009;54(3):133–40.PubMedCrossRefGoogle Scholar
  143. 143.
    Deshmukh A, Deshmukh K, Nimni ME. Synthesis of aldehydes and their interactions during the in vitro aging of collagen. Biochemistry. 1971;10(12):2337–42.PubMedCrossRefGoogle Scholar
  144. 144.
    Connolly J, Alferiev I, Kronsteiner A, Lu Z, Levy R. Ethanol inhibition of porcine bioprosthetic heart valve cusp calcification is enhanced by reduction with sodium borohydride. J Heart Valve Dis. 2004;13:487–93.PubMedGoogle Scholar
  145. 145.
  146. 146.
  147. 147.
  148. 148.
    Oosthuysen A, Zilla PP, Human PA, Schmidt CA, Bezuidenhout D. Bioprosthetic tissue preservation by filling with a poly(acrylamide) hydrogel. Biomaterials. 2006;27(9):2123–30.PubMedCrossRefGoogle Scholar
  149. 149.
    Tam H, Zhang W, Feaver KR, Parchment N, Sacks MS, Vyavahare N. A novel crosslinking method for improved tear resistance and biocompatibility of tissue based biomaterials. Biomaterials. 2015;66:83–91.PubMedPubMedCentralCrossRefGoogle Scholar
  150. 150.
    Bourguignon T, Lhommet P, El Khoury R, Candolfi P, Loardi C, Mirza A, Boulanger-Lothion J, Bouquiaux-Stablo-Duncan AL, Marchand M, Aupart M. Very long-term outcomes of the Carpentier-Edwards Perimount aortic valve in patients aged 50–65 years. Eur J Cardiothorac Surg. 2016;49(5):1462–8.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Clemson UniversityClemsonUSA

Personalised recommendations