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Annual Review of Biomedical Engineering

Volume 21, 2019

The Biocompatibility Challenges in the Total Artificial Heart Evolution

Abstract

There are limited therapeutic options for final treatment of end-stage heart failure. Among them, implantation of a total artificial heart (TAH) is an acceptable strategy when suitable donors are not available. TAH development began in the 1930s, followed by a dramatic evolution of the actuation mechanisms operating the mechanical pumps. Nevertheless, the performance of TAHs has not yet been optimized, mainly because of the low biocompatibility of the blood-contacting surfaces. Low hemocompatibility, calcification, and sensitivity to infections seriously affect the success of TAHs. These unsolved issues have led to the withdrawal of many prototypes during preclinical phases of testing. This review offers a comprehensive analysis of the pathophysiological events that may occur in the materials that compose TAHs developed to date. In addition, this review illustrates bioengineering strategies to prevent these events and describes the most significant steps toward the achievement of a fully biocompatible TAH.

Keyword(s): calcification, hemocompatibility, materials, microorganism contamination, total artificial hearts
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/content/journals/10.1146/annurev-bioeng-060418-052432
2019-06-04
2024-04-25
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Literature Cited

  1. 1.
    Benjamin EJ, Virani SS, Callaway CW, Chang AR, Cheng S et al. 2018. Heart disease and stroke statistics—2018 update: a report from the American Heart Association. Circ. J. 137:e67–492
     [Google Scholar]
  2. 2.
    Ho KK, Pinsky JL, Kannel WB, Levy D 1993. The epidemiology of heart failure: the Framingham study. J. Am. Coll. Cardiol. 22:4 Suppl. A6–13
     [Google Scholar]
  3. 3.
    Cowie MR, Wood DA, Coats AJ, Thompson SG, Suresh V et al. 2000. Survival of patients with a new diagnosis of heart failure: a population based study. Heart 83:505–10
     [Google Scholar]
  4. 4.
    Braunschweig F, Cowie MR, Auricchio A 2011. What are the costs of heart failure?. Europace 13:Suppl. 213–17
     [Google Scholar]
  5. 5.
    Gerosa G, Scuri S, Iop L, Torregrossa G 2014. Present and future perspectives on total artificial hearts. Ann. Cardiothorac. Surg. 3:595–602
     [Google Scholar]
  6. 6.
    Demikhov VP. 1951. Experimental basis for replacement of the heart with a mechanical device in acute experiments. Bull. Exp. Biol. Med. 32:22–24
     [Google Scholar]
  7. 7.
    Cooley DA, Liotta D, Hallman GL, Bloodwell RD, Leachman RD, Milam JD 1969. Orthotopic cardiac prosthesis for two-staged cardiac replacement. Am. J. Cardiol. 24:723–30
     [Google Scholar]
  8. 8.
    INTERMACS 2018. Quarterly Statistical Report 2016 Q1 Interagency Registry for Mechanically Assisted Circulatory Support (INTERMACS), Univ Ala., Birmingham: https://www.uab.edu/medicine/intermacs/reports/quarterly-site-reports
  9. 9.
    Gorbet MB, Sefton MV. 2004. Biomaterial-associated thrombosis: roles of coagulation factors, complement, platelets and leukocytes. Biomaterials 25:5681–703
     [Google Scholar]
  10. 10.
    Schoen FJ, Clagett GP, Hill JD, Chenoweth DE, Anderson JM, Eberhart RC 1987. The biocompatibility of artificial organs. ASAIO Trans 33:824–33
     [Google Scholar]
  11. 11.
    Sefton MV, Gemmell CH, Gorbet MB 2000. What really is blood compatibility?. J. Biomater. Sci. Polym. Ed. 11:1165–82
     [Google Scholar]
  12. 12.
    Nilsson B, Ekdahl KN, Mollnes TE, Lambris JD 2007. The role of complement in biomaterial-induced inflammation. Mol. Immunol. 44:82–94
     [Google Scholar]
  13. 13.
    Sevastianov VI, Tseytlina EA, Volkov AV, Shumakov VI 1984. Importance of absorption desorption processes of plasma proteins in biomaterials hemocompatibility. Trans. Am. Soc. Artif. Intern. Organs 30:137–42
     [Google Scholar]
  14. 14.
    Cumming RD, Phillips PA, Singh PI 1983. Surface chemistry and blood material interactions. Trans. Am. Soc. Artif. Intern. Organs 29:163–68
     [Google Scholar]
  15. 15.
    Sevastianov VI, Drushlyak IV, Eberhart RC, Kim SW 1996. Blood compatible biomaterials: hydrophilicity versus hydrophobicity. Macromol. Symp. 103:1–4
     [Google Scholar]
  16. 16.
    Grasel TG, Wilson RS, Lelah MD, Bielich HW, Cooper SL 1986. Blood flow and surface-induced thrombosis. ASAIO Trans 32:515–20
     [Google Scholar]
  17. 17.
    Vroman L, Adams AL. 1969. Findings with the recording ellipsometer suggesting rapid exchange of specific plasma proteins at liquid/solid interfaces. Surf. Sci. 16:438–46
     [Google Scholar]
  18. 18.
    Horbett TA. 1993. Principles underlying the role of adsorbed plasma proteins in blood interactions with foreign materials. Cardiovasc. Pathol. 2:Suppl. 3137–48
     [Google Scholar]
  19. 19.
    Gimbrone MA Jr 1987. Vascular endothelium: nature's blood-compatible container. Ann. N. Y. Acad. Sci. 516:5–11
     [Google Scholar]
  20. 20.
    Rajendran P, Rengarajan T, Thangavel J, Nishigaki Y, Sakthisekaran D et al. 2013. The vascular endothelium and human diseases. Int. J. Biol. Sci. 9:1057–69
     [Google Scholar]
  21. 21.
    Andrade JD, Coleman DL, Didisheim P, Hanson SR, Mason R, Merrill E 1981. Panel conference: blood-materials interactions—20 years of frustration. Trans. Am. Soc. Artif. Intern. Organs 27:659–62
     [Google Scholar]
  22. 22.
    Ratner BD. 1993. The blood compatibility catastrophe. J. Biomed. Mater. Res. 27:283–87
     [Google Scholar]
  23. 23.
    Liotta D, Hall CW, Akers WW, Villanueva A, O’ Neal RM, DeBakey ME 1966. A pseudo endocardium for implantable blood pumps. Trans. Am. Soc. Artif. Intern. Organs 12:129–38
     [Google Scholar]
  24. 24.
    Harasaki H, Kiraly R, Nosé Y 1978. Endothelialization in blood pumps. Trans. Am. Soc. Artif. Intern. Organs 24:415–25
     [Google Scholar]
  25. 25.
    Szycher M, Poirier V, Bernhard WF, Franzblau C, Haudenschild CC, Toselli P 1980. Integrally textured polymeric surfaces for permanently implantable cardiac assist devices. Trans. Am. Soc. Artif. Intern. Organs 26:493–97
     [Google Scholar]
  26. 26.
    Fasol R, Zilla P, Deutsch M, Fischlein T, Kadletz M et al. 1987. Endothelialization of artificial surfaces: does surface tension determine in vitro growth of human saphenous vein endothelial cells?. Tex. Heart Inst. J. 14:119–26
     [Google Scholar]
  27. 27.
    Jantzen AE, Lane WO, Gage SM, Jamiolkowski RM, Haseltine JM et al. 2011. Use of autologous blood-derived endothelial progenitor cells at point-of-care to protect against implant thrombosis in a large animal model. Biomaterials 32:8356–63
     [Google Scholar]
  28. 28.
    Noviani M, Jamiolkowski RM, Grenet JE, Lin Q, Carlon TA et al. 2016. Point-of-care rapid-seeding ventricular assist device with blood-derived endothelial cells to create a living antithrombotic coating. ASAIO J 62:447–53
     [Google Scholar]
  29. 29.
    Sharma CP. 2005. Biomaterials and artificial organs: few challenging areas. Trends Biomater. Artif. Organs 18:148–56
     [Google Scholar]
  30. 30.
    Sevastianov VI. 2002. Biocompatible materials: current status and future perspectives. Trends Biomater. Artif. Organs 15:20–30
     [Google Scholar]
  31. 31.
    Biran R, Pond D. 2016. Heparin coatings for improving blood compatibility of medical devices. Adv. Drug Deliv. Rev. 112:12–23
     [Google Scholar]
  32. 32.
    Dion I, Baquey C, Candelon B, Monties JR 1992. Hemocompatibility of titanium nitride. Int. J. Artif. Organs 15:617–21
     [Google Scholar]
  33. 33.
    Dion I, Roques X, Baquey C, Baudet E, Basse Cathalinat B, More N 1993. Hemocompatibility of diamond-like carbon coating. Biomed. Mater. Eng. 3:51–55
     [Google Scholar]
  34. 34.
    Jones MI, McColl IR, Grant DM, Parker KG, Parker TL 1999. Haemocompatibility of DLC and TiC–TiN interlayers on titanium. Diam. Relat. Mater. 8:457–62
     [Google Scholar]
  35. 35.
    Nakabayashi N, Williams DF. 2003. Preparation of non-thrombogenic materials using 2-methacryloyloxyethyl phosphorylcholine. Biomaterials 24:2431–35
     [Google Scholar]
  36. 36.
    Koster A, Loebe M, Sodian R, Potapov EV, Hansen R et al. 2001. Heparin antibodies and thromboembolism in heparin-coated and noncoated ventricular assist devices. J. Thorac. Cardiovasc. Surg 121:331–35
     [Google Scholar]
  37. 37.
    Hetzer R, Loebe M, Potapov EV, Weng Y, Stiller B et al. 1998. Circulatory support with pneumatic paracorporeal ventricular assist device in infants and children. Ann. Thorac. Surg. 66:1498–506
     [Google Scholar]
  38. 38.
    Hetzer R, Weng Y, Potapov EV, Pasic M, Drews T et al. 2004. First experiences with a novel magnetically suspended axial flow left ventricular assist device. Eur. J. Cardiothorac. Surg. 25:964–70
     [Google Scholar]
  39. 39.
    Yamazaki K, Litwak P, Tagusari O, Mori T, Kono K et al. 1998. An implantable centrifugal blood pump with a recirculating purge system (Cool-Seal system). Artif. Organs 22:466–74
     [Google Scholar]
  40. 40.
    Esmore D, Spratt P, Larbalestier R, Tsui S, Fiane A et al. 2007. VentrAssist left ventricular assist device: clinical trial results and Clinical Development Plan update. Eur. J. Cardiothorac. Surg 32:735–44
     [Google Scholar]
  41. 41.
    Snyder TA, Tsukui H, Kihara S, Akimoto T, Litwak KN et al. 2007. Preclinical biocompatibility assessment of the EVAHEART ventricular assist device: coating comparison and platelet activation. J. Biomed. Mater. Res. A 81:85–92
     [Google Scholar]
  42. 42.
    Yamazaki K, Kihara S, Akimoto T, Tagusari O, Kawai A et al. 2002. EVAHEART: an implantable centrifugal blood pump for long-term circulatory support. Jpn. J. Thorac. Cardiovasc. Surg. 50:461–65
     [Google Scholar]
  43. 43.
    Coleman D, Lawson J, Kolff WJ 1978. Scanning electron microscopic evaluation of the surfaces of artificial hearts. Artif. Organs 2:166–72
     [Google Scholar]
  44. 44.
    Christie AM, Donachy JH, Rosenberg G, Pierce WS 1985. Scanning electron microscopic evaluation of polyurethanes used for biomedical applications. Trans. Am. Soc. Artif. Intern. Organs 31:512–16
     [Google Scholar]
  45. 45.
    Zdrahala RJ, Zdrahala IJ. 1999. Biomedical applications of polyurethanes: a review of past promises, present realities, and a vibrant future. J. Biomater. Appl. 14:67–90
     [Google Scholar]
  46. 46.
    Kumbar S, Laurencin C, Deng M 2014. Natural and Synthetic Biomedical Polymers Amsterdam: Elsevier
  47. 47.
    Zartnack F, Dunkel W, Affeld K, Bucherl ES 1978. Fatigue problems in artificial blood pumps. Trans. Am. Soc. Artif. Intern. Organs 24:600–5
     [Google Scholar]
  48. 48.
    Nichols WK, Gospodarowicz D, Kessler TR, Olsen DB 1981. Increased adherence of vascular endothelial cells to Biomer precoated with extracellular matrix. Trans. Am. Soc. Artif. Intern. Organs 27:208–12
     [Google Scholar]
  49. 49.
    Belanger MC, Marois Y, Roy R, Mehri Y, Wagner E et al. 2000. Selection of a polyurethane membrane for the manufacture of ventricles for a totally implantable artificial heart: blood compatibility and biocompatibility studies. Artif. Organs 24:879–88
     [Google Scholar]
  50. 50.
    Zapanta CM, Griffith JW, Hess GD, Doxtater BJ, Khalapyan T et al. 2006. Microtextured materials for circulatory support devices: preliminary studies. ASAIO J 52:17–23
     [Google Scholar]
  51. 51.
    Nosé Y, Harasaki H, Murray J 1981. Mineralization of artificial surfaces that contact blood. Trans. Am. Soc. Artif. Intern. Organs 27:714–19
     [Google Scholar]
  52. 52.
    Harasaki H, Kambic H, Whalen R, Murray J, Snow J et al. 1980. Comparative study of flocked versus biolized surface for long-term assist pumps. Trans. Am. Soc. Artif. Intern. Organs 26:470–74
     [Google Scholar]
  53. 53.
    Harasaki H, Field A, Sato N, Snow J, Kiraly R, Nosé Y 1983. Polyester fibril flocked surface for blood pumps. Trans. Am. Soc. Artif. Intern. Organs 29:563–68
     [Google Scholar]
  54. 54.
    Metman LV, De Paulis R, Mohammad SF, Kolff WJ 1987. Evaluation of thrombogenesis on smooth and rough intima in artificial ventricles. ASAIO Trans 33:732–37
     [Google Scholar]
  55. 55.
    Dasse KA, Chipman SD, Sherman CN, Levine AH, Frazier OH 1987. Clinical experience with textured blood contacting surfaces in ventricular assist devices. ASAIO Trans 33:418–25
     [Google Scholar]
  56. 56.
    Graham TR, Dasse KA, Coumbe A, Salih V, Marrinan MT et al. 1990. Neo-intimal development on textured biomaterial surfaces during clinical use of an implantable ventricular assist device. Eur. J. Cardiothorac. Surg. 4:182–90
     [Google Scholar]
  57. 57.
    Whalen RL, Snow JL, Harasaki H, Nosé Y 1980. Mechanical strain and calcification in blood pumps. Trans. Am. Soc. Artif. Intern. Organs 26:487–92
     [Google Scholar]
  58. 58.
    Kiraly RJ, Nosé Y. 1974. Natural tissue as a biomaterial. Biomater. Med. Devices Artif. Organs 2:207–24
     [Google Scholar]
  59. 59.
    Imai Y, Tajima K, Nosé Y 1971. Biolized materials for cardiovascular prosthesis. Trans. Am. Soc. Artif. Intern. Organs 17:6–9
     [Google Scholar]
  60. 60.
    Nosé Y, Tajima K, Imai Y, Klain M, Mrava G et al. 1971. Artificial heart constructed with biological material. Trans. Am. Soc. Artif. Intern. Organs 17:482–89
     [Google Scholar]
  61. 61.
    Imai Y, Von Bally K, Nosé Y 1970. New elastic materials for the artificial heart. Trans. Am. Soc. Artif. Intern. Organs 16:17–25
     [Google Scholar]
  62. 62.
    Nosé Y, Imai Y, Tajima K, Ogawa H, Klain M, von Bally K 1971. Cardiac prosthesis utilizing biological material. J. Thorac. Cardiovasc. Surg. 62:714–24
     [Google Scholar]
  63. 63.
    Kambic H, Picha G, Kiraly R, Koshino I, Nosé Y 1976. Application of aldehyde treatments to cardiovascular devices. Trans. Am. Soc. Artif. Intern. Organs 22:664–72
     [Google Scholar]
  64. 64.
    Picha G, Helmus M, Barenberg S, Gibbons D, Martin R, Nosé Y 1976. The characterization of intima development in left ventricular assist device (LVAD) and total artificial heart (TAH). Trans. Am. Soc. Artif. Intern. Organs 22:554–69
     [Google Scholar]
  65. 65.
    Hayashi K, Snow J, Washizu T, Jacobs GB, Kiraly RJ, Nosé Y 1977. Biolized intrathoracic left ventricular assist device (LVAD). Med. Instrum. 11:202–7
     [Google Scholar]
  66. 66.
    Chatel D. 1996. Concept of totally biological internal coating for newly shaped artificial ventricles. Artif. Organs 20:814–17
     [Google Scholar]
  67. 67.
    Chatel D, Delamare L, Dang P, Lebouvier D, Trocherie F 1997. A biomechanical double sac (pericardium–Pebax) for specially shaped artificial ventricles: a computerized study to evaluate its mechanical and volumetric properties. Artif. Organs 21:1098–104
     [Google Scholar]
  68. 68.
    Olsen DB, Unger F, Oster H, Lawson J, Kessler T et al. 1975. Thrombus generation within the artificial heart. J. Thorac. Cardiovasc. Surg. 70:248–55
     [Google Scholar]
  69. 69.
    Rennekamp F, Affeld K, Clevert HD, Frank J, Gerlach K et al. 1979. Long term results with seamless blood pumps out of polyurethanes for the replacement of the heart. Proc. Eur. Soc. Artif. Organs 6:94–98
     [Google Scholar]
  70. 70.
    Vaškù J, Urbánek P. 1995. Electron microscopic study of driving diaphragms in long-term survival with a total artificial heart. Artif. Organs 19:344–54
     [Google Scholar]
  71. 71.
    Harasaki H, Gerrity R, Kiraly R, Jacobs G, Nosé Y 1979. Calcification in blood pumps. Trans. Am. Soc. Artif. Intern. Organs 25:305–10
     [Google Scholar]
  72. 72.
    Turner SA, Bossart MI, Milam JD, Fuqua JM Jr, Igo SR et al. 1982. Calcification in chronically-implanted blood pumps: experimental results and review of the literature. Tex. Heart Inst. J. 9:195–205
     [Google Scholar]
  73. 73.
    Coleman DL, Lim D, Kessler T, Andrade JD 1981. Calcification of nontextured implantable blood pumps. ASAIO J 27:97–104
     [Google Scholar]
  74. 74.
    Valente M, Bortolotti U, Thiene G 1985. Ultrastructural substrates of dystrophic calcification in porcine bioprosthetic valve failure. Am. J. Pathol. 119:12–21
     [Google Scholar]
  75. 75.
    Schoen FJ, Tsao JW, Levy RJ 1986. Calcification of bovine pericardium used in cardiac valve bioprostheses. Implications for the mechanisms of bioprosthetic tissue mineralization. Am. J. Pathol. 123:134–45
     [Google Scholar]
  76. 76.
    Schoen FJ, Levy RJ. 2005. Calcification of tissue heart valve substitutes: progress toward understanding and prevention. Ann. Thorac. Surg. 79:1072–80
     [Google Scholar]
  77. 77.
    Vasin SL, Rosanova IB, Sevastianov VI 1998. The role of proteins in the nucleation and formation of calcium-containing deposits on biomaterial surfaces. J. Biomed. Mater. Res. 39:491–97
     [Google Scholar]
  78. 78.
    Shumakov VI, Rosanova IB, Vasin SL, Salomatina LA, Sevastianov VI 1990. Biomaterial calcification without direct material–cell interaction. ASAIO Trans 36:M181–84
     [Google Scholar]
  79. 79.
    Schoen FJ. 1987. Biomaterial-associated infection, neoplasia, and calcification: clinicopathologic features and pathophysiologic concepts. ASAIO Trans 33:8–18
     [Google Scholar]
  80. 80.
    Anderson HC. 1981. Normal and abnormal mineralization in mammals. Trans. Am. Soc. Artif. Intern. Organs 27:702–8
     [Google Scholar]
  81. 81.
    Harasaki H, McMahon J, Richards T, Goldcamp J, Kiraly R, Nosé Y 1985. Calcification in cardiovascular implants: degraded cell related phenomena. Trans. Am. Soc. Artif. Intern. Organs 31:489–94
     [Google Scholar]
  82. 82.
    Hughes SD, Coleman DL, Dew PA, Burns GL, Olsen DB, Kolff WJ 1984. Effects of coumadin on thrombus and mineralization in total artificial hearts. Trans. Am. Soc. Artif. Intern. Organs 30:75–80
     [Google Scholar]
  83. 83.
    Pierce WS, Donachy JH, Rosenberg G, Baier RE 1980. Calcification inside artificial hearts: inhibition by warfarin-sodium. Science 208:601–3
     [Google Scholar]
  84. 84.
    Coleman DL. 1981. Mineralization of blood pump bladders. Trans. Am. Soc. Artif. Intern. Organs 27:708–13
     [Google Scholar]
  85. 85.
    Harasaki H, Moritz A, Uchida N, Chen JF, McMahon JT et al. 1987. Initiation and growth of calcification in a polyurethane-coated blood pump. ASAIO Trans 33:643–49
     [Google Scholar]
  86. 86.
    Owen DR, Zone RM. 1981. Analysis of a possible mechanism of surface calcification on a biomedical elastomer. Trans. Am. Soc. Artif. Intern. Organs 27:528–31
     [Google Scholar]
  87. 87.
    Yang M, Zhang Z, Hahn C, King MW, Guidoin R 1999. Assessing the resistance to calcification of polyurethane membranes used in the manufacture of ventricles for a totally implantable artificial heart. J. Biomed. Mater. Res. 48:648–59
     [Google Scholar]
  88. 88.
    Imachi K, Chinzei T, Abe Y, Mabuchi K, Matsuura H et al. 2001. A new hypothesis on the mechanism of calcification formed on a blood-contacted polymer surface. J. Artif. Organs 4:74–82
     [Google Scholar]
  89. 89.
    Mason RG, Lian JB, Levy RJ, Bernhard W, Szycher M 1981. LVAD mineralization and γ-carboxyglutamic acid containing proteins in normal and pathologically mineralized tissues. Trans. Am. Soc. Artif. Intern. Organs 27:683–89
     [Google Scholar]
  90. 90.
    Dostal M, Vasku J, Vasku J, Sotolova O, Vasku A et al. 1990. Mineralization of polyurethane membranes in the total artificial heart (TAH): a retrospective study from long-term animal experiments. Int. J. Artif. Organs 13:498–502
     [Google Scholar]
  91. 91.
    Santos LL, Cavalcanti TB, Bandeira FA 2012. Vascular effects of bisphosphonates—a systematic review. Clin. Med. Insights Endocrinol. Diabetes 5:47–54
     [Google Scholar]
  92. 92.
    Joshi RR, Frautschi JR, Phillips RE Jr, Levy RJ 1994. Phosphonated polyurethanes that resist calcification. J. Appl. Biomater. 5:65–77
     [Google Scholar]
  93. 93.
    Alferiev I, Vyavahare N, Song C, Connolly J, Hinson JT et al. 2001. Bisphosphonate derivatized polyurethanes resist calcification. Biomaterials 22:2683–93
     [Google Scholar]
  94. 94.
    Khardori N, Yassien M. 1995. Biofilms in device-related infections. J. Ind. Microbiol. 15:141–47
     [Google Scholar]
  95. 95.
    Costerton JW, Montanaro L, Arciola CR 2005. Biofilm in implant infections: its production and regulation. Int. J. Artif. Organs 28:1062–68
     [Google Scholar]
  96. 96.
    Costerton JW, Irvin RT, Cheng KJ 1981. The role of bacterial surface structures in pathogenesis. Crit. Rev. Microbiol. 8:303–38
     [Google Scholar]
  97. 97.
    Costerton JW, Geesey GG, Cheng KJ 1978. How bacteria stick. Sci. Am. 238:86–95
     [Google Scholar]
  98. 98.
    Marrie TJ, Nelligan J, Costerton JW 1982. A scanning and transmission electron microscopic study of an infected endocardial pacemaker lead. Circulation 66:1339–41
     [Google Scholar]
  99. 99.
    Conley J, Olson ME, Cook LS, Ceri H, Phan V, Davies HD 2003. Biofilm formation by group A streptococci: Is there a relationship with treatment failure?. J. Clin. Microbiol. 41:4043–48
     [Google Scholar]
  100. 100.
    Hoffman LR, D'Argenio DA, MacCoss MJ, Zhang Z, Jones RA, Miller SI 2005. Aminoglycoside antibiotics induce bacterial biofilm formation. Nature 436:1171–75
     [Google Scholar]
  101. 101.
    Fields A, Harasaki H, Sands D, Nosé Y 1983. Infection in artificial blood pump implantation. Trans. Am. Soc. Artif. Intern. Organs 29:532–38
     [Google Scholar]
  102. 102.
    Murray KD, Hughes S, Bearnson D, Olsen DB 1983. Infection in total artificial heart recipients. Trans. Am. Soc. Artif. Intern. Organs 29:539–45
     [Google Scholar]
  103. 103.
    Didisheim P, Olsen DB, Farrar DJ, Portner PM, Griffith BP et al. 1989. Infections and thromboembolism with implantable cardiovascular devices. ASAIO Trans 35:54–70
     [Google Scholar]
  104. 104.
    McBride LR, Ruzevich SA, Pennington DG, Kennedy DJ, Kanter KR et al. 1987. Infectious complications associated with ventricular assist device support. ASAIO Trans 33:201–2
     [Google Scholar]
  105. 105.
    Sivaratnam K, Duggan JM. 2002. Left ventricular assist device infections: three case reports and a review of the literature. ASAIO J 48:2–7
     [Google Scholar]
  106. 106.
    Goldberg SP, Baddley JW, Aaron MF, Pappas PG, Holman WL 2000. Fungal infections in ventricular assist devices. ASAIO J 46:S37–40
     [Google Scholar]
  107. 107.
    Firstenberg MS, Louis LB, Vesco P, Sai-Sudhakar CB, Mangino J et al. 2008. Fungemia in patients with long-term left ventricular assist devices: a chronic problem, but not the kiss of death. J. Heart Lung Transplant. 27:S157
     [Google Scholar]
  108. 108.
    Bagdasarian NG, Malani AN, Pagani FD, Malani PN 2009. Fungemia associated with left ventricular assist device support. J. Card. Surg. 24:763–65
     [Google Scholar]
  109. 109.
    Hastings WL, Aaron JL, Deneris J, Kessler TR, Pons AB et al. 1981. A retrospective study of nine calves surviving five months on the pneumatic total artificial heart. Trans. Am. Soc. Artif. Intern. Organs 27:71–76
     [Google Scholar]
  110. 110.
    Asai T, Lee MH, Arrecubieta C, von Bayern MP, Cespedes CA et al. 2007. Cellular coating of the left ventricular assist device textured polyurethane membrane reduces adhesion of Staphylococcus aureus. J. Thorac. Cardiovasc. Surg 133:1147–53
     [Google Scholar]
  111. 111.
    Cohn WE, Timms DL, Frazier OH 2015. Total artificial hearts: past, present, and future. Nat. Rev. Cardiol. 12:609–17
     [Google Scholar]
  112. 112.
    Fox CS, McKenna KL, Allaire PE, Mentzer RM Jr, Throckmorton AL 2015. Total artificial hearts—past, current, and future. J. Card. Surg. 30:856–64
     [Google Scholar]
  113. 113.
    Ratner BD, Hoffman AS, Schoen FJ, Lemons JE 2004. Biomaterials Science: An Introduction to Materials in Medicine Amsterdam: Elsevier 2nd ed .
  114. 114.
    Akutsu T, Kantrowitz A. 1967. Problems of materials in mechanical heart systems. J. Biomed. Mater. Res. 1:33–54
     [Google Scholar]
  115. 115.
    Nosé Y, Phillips P, Kolff WJ 1968. Problems with materials used in the intrathoracic artificial heart. Ann. N. Y. Acad. Sci 146:271–88
     [Google Scholar]
  116. 116.
    Cooley DA, Liotta D, Hallam GL, Bloodwell RD, Leachman RD, Milam JD 1969. First human implantation of cardiac prosthesis for staged total replacement of the heart. Trans. Am. Soc. Artif. Intern. Organs 15:252–66
     [Google Scholar]
  117. 117.
    Akutsu T, Mirkovitch V, Topaz SR, Kolff WJ 1964. A sac type of artificial heart inside the chest of dogs. J. Thorac. Cardiovasc. Surg. 47:512–27
     [Google Scholar]
  118. 118.
    Cheng K, Meador JW, Serrato MA, Akutsu T 1977. The design and fabrication of a new total artificial heart. Cardiovasc. Dis. 4:7–17
     [Google Scholar]
  119. 119.
    Nyilas E, Ward RS Jr 1977. Development of blood-compatible elastomers. V. Surface structure and blood compatibility of avcothane elastomers. J. Biomed. Mater. Res. 11:69–84
     [Google Scholar]
  120. 120.
    Cooley DA, Akutsu T, Norman JC, Serrato MA, Frazier OH 1981. Total artificial heart in two-staged cardiac transplantation. Cardiovasc. Dis. 8:305–19
     [Google Scholar]
  121. 121.
    Kwan-Gett C, Zwart HH, Kralios AC, Kessler T, Backman K, Kolff WJ 1970. A prosthetic heart with hemispherical ventricles designed for low hemolytic action. Trans. Am. Soc. Artif. Intern. Organs 16:409–15
     [Google Scholar]
  122. 122.
    Jarvik R, Volder J, Olsen D, Moulopoulos S, Kolff WJ 1974. Venous return of an artificial heart designed to prevent right heart syndrome. Ann. Biomed. Eng. 2:335–42
     [Google Scholar]
  123. 123.
    Kessler TR, Pons AB, Jarvik RK, Lawson JH, Razzeca KJ, Kolff WJ 1978. Elimination of predilection sites for thrombus formation in the total artificial heart—before and after. Trans. Am. Soc. Artif. Intern. Organs 24:532–36
     [Google Scholar]
  124. 124.
    Olsen DB, Fukumasu H, Kolff J, Nakagaki M, Finch LR, Kolff WJ 1977. Implantation of the total artificial heart by lateral thoracotomy. Artif. Organs 1:92–98
     [Google Scholar]
  125. 125.
    DeVries WC, Anderson JL, Joyce LD, Anderson FL, Hammond EH et al. 1984. Clinical use of the total artificial heart. N. Engl. J. Med. 310:273–78
     [Google Scholar]
  126. 126.
    Joyce LD, DeVries WC, Hastings WL, Olsen DB, Jarvik RK, Kolff WJ 1983. Response of the human body to the first permanent implant of the Jarvik-7 Total Artificial Heart. Trans. Am. Soc. Artif. Intern. Organs 29:81–87
     [Google Scholar]
  127. 127.
    Copeland JG, Smith RG, Arabia FA, Nolan PE, McClellan D et al. 2004. Total artificial heart bridge to transplantation: a 9-year experience with 62 patients. J. Heart Lung Transplant. 23:823–31
     [Google Scholar]
  128. 128.
    Torregrossa G, Morshuis M, Varghese R, Hosseinian L, Vida V et al. 2014. Results with SynCardia total artificial heart beyond 1 year. ASAIO J 60:626–34
     [Google Scholar]
  129. 129.
    Slepian MJ, Alemu Y, Girdhar G, Soares JS, Smith RG et al. 2013. The Syncardia™ total artificial heart: in vivo, in vitro, and computational modeling studies. J. Biomech. 46:266–75
     [Google Scholar]
  130. 130.
    Yu LS, Finnegan M, Vaughan S, Ochs B, Parnis S et al. 1993. A compact and noise free electrohydraulic total artificial heart. ASAIO J 39:M386–91
     [Google Scholar]
  131. 131.
    Parnis S, Yu LS, Ochs B, Macris MP, Frazier OH, Kung RT 1994. Chronic in vivo evaluation of an electrohydraulic total artificial heart. ASAIO J 40:M489–93
     [Google Scholar]
  132. 132.
    Kung RT, Yu LS, Ochs BD, Parnis SM, Macris MP, Frazier OH 1995. Progress in the development of the ABIOMED total artificial heart. ASAIO J 41:M245–48
     [Google Scholar]
  133. 133.
    Dowling RD, Etoch SW, Stevens KA, Johnson AC, Gray LA Jr 2001. Current status of the AbioCor implantable replacement heart. Ann. Thorac. Surg. 71:Suppl. 3147–49
     [Google Scholar]
  134. 134.
    Dowling RD, Gray LA Jr, Etoch SW, Laks H, Marelli D et al. 2004. Initial experience with the AbioCor implantable replacement heart system. J. Thorac. Cardiovasc. Surg. 127:131–41
     [Google Scholar]
  135. 135.
    Dowling RD, Gray LA Jr, Etoch SW, Laks H, Marelli D et al. 2003. The AbioCor implantable replacement heart. Ann. Thorac. Surg. 75:Suppl. 693–99
     [Google Scholar]
  136. 136.
    Dowling RD, Etoch SW, Stevens KA, Butterfield A, Koenig SE et al. 2000. Initial experience with the AbioCor implantable replacement heart at the University of Louisville. ASAIO J 46:579–81
     [Google Scholar]
  137. 137.
    Nosé Y. 2007. FDA approval of totally implantable permanent total artificial heart for humanitarian use. Artif. Organs 31:1–3
     [Google Scholar]
  138. 138.
    Mohacsi P, Leprince P. 2014. The CARMAT total artificial heart. Eur. J. Cardiothorac. Surg. 46:933–34
     [Google Scholar]
  139. 139.
    Poirer NC, Pelletier LC, Pellerin M, Carrier M 1998. 15-year experience with the Carpentier–Edwards pericardial bioprosthesis. Ann. Thorac. Surg. 66:Suppl. 657–61
     [Google Scholar]
  140. 140.
    Marchand MA, Aupart MR, Norton R, Goldsmith IR, Pelletier LC et al. 2001. Fifteen-year experience with the mitral Carpentier–Edwards PERIMOUNT pericardial bioprosthesis. Ann. Thorac. Surg. 71:Suppl. 5236–39
     [Google Scholar]
  141. 141.
    Jansen P, van Oeveren W, Capel A, Carpentier A 2012. In vitro haemocompatibility of a novel bioprosthetic total artificial heart. Eur. J. Cardiothorac. Surg. 41:e166–72
     [Google Scholar]
  142. 142.
    Carpentier A, Latrémouille C, Cholley B, Smadja DM, Roussel JC et al. 2015. First clinical use of a bioprosthetic total artificial heart: report of two cases. Lancet 386:1556–63
     [Google Scholar]
  143. 143.
    Latrémouille C, Duveau D, Cholley B, Zilberstein L, Belbis G et al. 2015. Animal studies with the Carmat bioprosthetic total artificial heart. Eur. J. Cardiothorac. Surg. 47:e172–78
     [Google Scholar]
  144. 144.
    Smadja DM, Susen S, Rauch A, Cholley B, Latrémouille C et al. 2017. The CARMAT bioprosthetic total artificial heart is associated with early hemostatic recovery and no acquired von Willebrand syndrome in calves. J. Cardiothorac. Vasc. Anesth. 31:1595–602
     [Google Scholar]
  145. 145.
    Latrémouille C, Carpentier A, Leprince P, Roussel J-CC, Cholley B et al. 2017. A bioprosthetic total artificial heart for end-stage heart failure: results from a pilot study. J. Heart Lung Transplant. 37:33–37
     [Google Scholar]
  146. 146.
    CARMAT. 2018. CARMAT completes patient enrollment in the first part of the PIVOTAL study in line with the objective of obtaining CE marking in 2019 Press release, July 11. https://www.carmatsa.com/en/news/carmat-completes-patient-enrollment-first-part-pivotal-study-line-objective-obtaining-ce-marking-2019/
  147. 147.
    Iop L, Renier V, Naso F, Piccoli M, Bonetti A et al. 2009. The influence of heart valve leaflet matrix characteristics on the interaction between human mesenchymal stem cells and decellularized scaffolds. Biomaterials 30:4104–16
     [Google Scholar]
  148. 148.
    Naso F, Iop L, Spina M, Gerosa G 2014. Are FDA and CE sacrificing safety for a faster commercialization of xenogeneic tissue devices? Unavoidable need for legislation in decellularized tissue manufacturing. Tissue Antigens 83:193–94
     [Google Scholar]
  149. 149.
    Aguiari P, Iop L, Favaretto F, Fidalgo CML, Naso F et al. 2017. In vitro comparative assessment of decellularized bovine pericardial patches and commercial bioprosthetic heart valves. Biomed. Mater. 12:015021
     [Google Scholar]
  150. 150.
    US Food Drug. Admin. 2016. Use of International Standard ISO 10993–1, “Biological evaluation of medical devices—part 1: Evaluation and testing within a risk management process. .” 81 Fed. Reg. 39269 (June 16)
  151. 151.
    Gerosa G, Gallo M, Bottio T, Tarzia V 2016. Successful heart transplant after 1374 days living with a total artificial heart. Eur. J. Cardiothorac. Surg. 49:e88–89
     [Google Scholar]
  152. 152.
    Monteagudo Vela M, García Sáez D, Simon AR 2018. Current approaches in retrieval and heart preservation. Ann. Cardiothorac. Surg. 7:67–74
     [Google Scholar]
  153. 153.
    Iop L, Palmosi T, Dal Sasso E, Gerosa G 2018. Bioengineered tissue solutions for repair, correction and reconstruction in cardiovascular surgery. J. Thorac. Dis. 8:E503–10
     [Google Scholar]
  154. 154.
    Iop L, Dal Sasso E, Menabò R, Di Lisa F, Gerosa G 2017. The rapidly evolving concept of whole heart engineering. Stem Cells Int 2017:8920940
     [Google Scholar]
/content/journals/10.1146/annurev-bioeng-060418-052432
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The Biocompatibility Challenges in the Total Artificial Heart Evolution
Annual Review of Biomedical Engineering 21, 85 (2019); https://doi.org/10.1146/annurev-bioeng-060418-052432
/content/journals/10.1146/annurev-bioeng-060418-052432
/content/journals/10.1146/annurev-bioeng-060418-052432
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