Tissue engineering of heart valves: Advances and current challenges

Expert Review of Medical Devices

Volumn 6, Issue 3, 2009, Pages 259-275

  Mol, Anita ^a   Smith, Anthal I P M ^a   Bouten, Carlijn V C ^a   Baaijens, Frank P T ^a  

^a EINDHOVEN UNIVERSITY OF TECHNOLOGY   (Netherlands)

Author keywords

Cardiovascular; Cells; Extracellular; Heart valve; In vitro; In vivo; Matrix; Scaffold; Tissue engineering

Indexed keywords

DEOXYCHOLATE SODIUM; ELASTIN; OCTOXINOL; POLITEF; POLY(3 HYDROXYBUTYRIC ACID); POLYCAPROLACTONE; POLYGLYCOLIC ACID;

ALLOGRAFT; ANTICOAGULANT THERAPY; BIOCOMPATIBILITY; BIODEGRADATION; BIOMECHANICS; BIOREACTOR; CELL POPULATION; HEART VALVE PROSTHESIS; HEART VALVE REPLACEMENT; HOST CELL; HUMAN; MINIMALLY INVASIVE PROCEDURE; NONHUMAN; QUALITY OF LIFE; REVIEW; SURVIVAL TIME; TISSUE ENGINEERING; VALVULAR HEART DISEASE; XENOGRAFT; ANIMAL; BIOPROSTHESIS; METHODOLOGY; TRICUSPID VALVE;

ANIMALS; BIOPROSTHESIS; HEART VALVE DISEASES; HEART VALVE PROSTHESIS; HEART VALVE PROSTHESIS IMPLANTATION; HUMANS; TISSUE ENGINEERING; TRICUSPID VALVE;

EID: 67651028269     PISSN: 17434440     EISSN: 17452422     Source Type: Journal    
DOI: 10.1586/erd.09.12     Document Type: Review

References (171)

1. Nkomo VT, Gardin JM, Skelton TN, Gottdiener JS, Scott CG, Enriquez-Sarano M. Burden of valvular heart diseases: a population-based study. Lancet 368, 1005-1011 (2006).
2. Rosamond W, Flegal K, Furie K et al.. Heart disease and stroke statistics - 2008 update: a report from the American Heart Association statistics committee and stroke statistics subcommittee. Circulation 117, E25-E146 (2008).
3. Nkomo VT. Epidemiology and prevention of valvular heart diseases and infective endocarditis in Africa. Heart 93, 1510-1019 (2007).
4. Zilla P, Brink J, Human P, Bezuidenhout D. Prosthetic heart valves: catering for the few. Biomaterials 29, 385-406 (2008).
5. Iung B, Baron G, Butchart EG et al.. A prospective survey of patients with valvular heart disease in Europe: the Euro Heart Survey on valvular heart disease. Eur. Heart J. 24, 1231-1243 (2003).
6. Goldbarg SH, Elmariah S, Miller MA, Fuster V. Insights into degenerative aortic valve disease. J. Am. Coll. Cardiol. 50, 1205-1213 (2007).
7. Yacoub MH, Cohn LH. Novel approaches to cardiac valve repair: from structure to function: part I. Circulation 109, 942-950 (2004).
8. Yacoub MH, Cohn LH. Novel approaches to cardiac valve repair: from structure to function: part II. Circulation 109, 1064-1072 (2004).
9. Friedewald VE, Bonow RO, Borer JS et al.. The editor's roundtable: cardiac valve surgery. Am. J. Cardiol. 99, 1269-1278 (2007).
10. Yacoub MH, Takkenberg JJM. Will heart valve tissue engineering change the world? Nat. Clin. Pract. Cardiovasc. Med. 2, 60-61 (2005).
11. Mikos AG, Herring SW, Ochareon P et al.. Engineering complex tissues. Tissue Eng. 12, 3307-3339 (2006).
12. Bonow RO, Carabello BA, Chatterjee K et al.. ACC/AHA 2006 guidelines for the management of patients with valvular heart disease: a report of the American College of Cardiology/American Heart Association task force on practice guidelines (writing committee to revise the 1998 guidelines for the management of patients with valvular heart disease): developed in collaboration with the Society of Cardiovascular Anesthesiologists: endorsed by the Society for Cardiovascular Angiography and Interventions and the Society of Thoracic Surgeons. Circulation 114, E84-E231 (2006).
13. 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. 36, 1152-1158 (2000).
14. Oxenham H, Bloom?eld P, Wheatley DJ et al.. Twenty year comparison of a Bjork-Shiley mechanical heart valve with porcine bioprostheses. Heart 89, 715-721 (2003).
15. Jamieson WRE, Von Lipinski O, Miyagishima RT et al.. Performance of bioprostheses and mechanical prostheses assessed by composites of valve-related complications to 15 years after mitral valve replacement. J. Thorac. Cardiovasc. Surg. 129, 1301-1308 (2005).
16. Chan V, Jamieson WRE, Germann E et al.. Performance of bioprostheses and mechanical prostheses assessed by composites of valve-related complications to 15 years after aortic valve replacement. J. Thorac. Cardiovasc. Surg. 131, 1267-1273 (2006).
17. Eichinger WB, Hettich IM, Ruzicka DJ et al.. Twenty-year experience with the St. Jude Medical Biocor bioprosthesis in the aortic position. Ann. Thorac. Surg. 86, 1204-1211 (2008).
18. Lund O, Bland M. Risk-corrected impact of mechanical versus bioprosthetic valves on long-term mortality after aortic valve replacement. J. Thorac. Cardiovasc. Surg. 132, 20-26 (2006).
19. Brown ML, Schaff HV, Lahr BD et al.. Aortic valve replacement in patients aged 50 to 70 years: improved outcome with mechanical versus biologic prostheses. J. Thorac. Cardiovasc. Surg. 135, 878-884 (2008).
20. Koertke H, Minami K, Boethig D et al.. INR self-management permits lower anticoagulation levels after mechanical heart valve replacement. Circulation 108(Suppl. II), II75-II78 (2003).
21. Koertke H, Zittermann A, Tenderich G et al.. Low-dose oral anticoagulation in patients with mechanical heart valve prostheses: final report from the Self-Management Anticoagulation trial II. Eur. Heart J. 28, 2479-2484 (2007).
22. Koolbergen DR, Hazekamp MG, de Heer E et al.. Structural degeneration of pulmonary homografts used as aortic valve substitute underlines early graft failure. Eur. J. Cardiothorac. Surg. 22, 802-807 (2002).
23. Jennings LM, Butterfield M, Booth C, Watterson KG, Fisher J. The pulmonary bioprosthetic heart valve: its unsuitability as an aortic valve replacement. J. Heart Valve Dis. 11, 668-678 (2002).
24. Schoof PH, Takkenberg JJM, van Suylen R et al.. Degeneration of the pulmonary autograft: an explant study. J. Thorac. Cardiovasc. Surg. 132, 1426-1432 (2006).
25. Klieverik LMA, Takkenberg JJM, Bekkers JA, Roos-Hesselink JW, Witsenburg M, Bogers AJJC. The Ross operation: a Trojan horse? Eur. Heart J. 28, 1993-2000 (2007).
26. El Oakley R, Kleine P, Bach DS. Choice of prosthetic heart valve in today's practice. Circulation 117, 253-256 (2008).
27. Puvimanasinghe JP, Steyerberg EW, Takkenberg JJ et al.. Prognosis after aortic valve replacement with a bioprosthesis: predictions based on meta-analysis and microsimulation. Circulation 103, 1535-1541 (2001).
28. Wheatley DJ, Raco L, Bernacca GM, Sim I, Belcher PR, Boyd JS. Polyurethane: material for the next generation of heart valve prostheses? Eur. J. Cardiothorac. Surg. 17, 440-448 (2000).
29. Daebritz SH, Sachweh JS, Hermanns B et al.. Introduction of a flexible polymeric heart valve prosthesis with special design for mitral position. Circulation 108(Suppl. II), II134-II139 (2003).
30. Daebritz SH, Fausten B, Hermanns B et al.. Introduction of a flexible polymeric heart valve prosthesis with special design for aortic position. Eur. J. Cardiothorac. Surg. 25, 946-952 (2004).
31. Gallocher SL, Aguirre AF, Kasyanov V, Pinchuk L, Schoephoerster RT. A novel polymer for potential use in a trileaflet heart valve. J. Biomed. Mater. Res. Part B Appl. Biomaterials 79(2), 325-334 (2006).
32. Schoen FJ. Evolving concepts of cardiac valve dynamics. The continuum of development, functional structure, pathobiology, and tissue engineering. Circulation 118, 1864-1880 (2008).
33. Adachi M, Suzuki M, Kennedy JH. Neointimas cultured for circulatory assist devices: comparison of cultured cells derived from autologous tissues of various organs. J. Surg. Res. 11, 483-491 (1971).
34. Mansfield PB, Wechezak AR, Sauvage LR. Preventing thrombus on artificial vascular surfaces: true endothelial cell linings. Trans. Am. Soc. Artif. Intern. Organs 21, 264-272 (1975).
35. Eberl T, Siedler S, Schumacher B, Zilla P, Schlaudraff K, Fasol R. Experimental in vitro endothelialization of cardiac valve leaflets. Ann. Thorac. Surg. 53, 487-492 (1992).
36. Langer R, Vacanti JP. Tissue engineering. Science 260, 920-926 (1993).
37. Kasimir MT, Rieder E, Seebacher G et al.. Comparison of different decellularization procedures of porcine heart valves. Int. J. Artif. Organs 26, 421-427 (2003).
38. Tudorache I, Cebotari S, Sturz G et al.. Tissue engineering of heart valves: biomechanical and morphological properties of decellularized heart valves. J. Heart Valve Dis. 16, 567-573 (2007).
39. Liao J, Joyce EM, Sacks MS. Effects of decellularization on the mechanical and structural properties of the porcine aortic valve leaflet. Biomaterials 29, 1065-1074 (2008).
40. Curtil A, Pegg DE, Wilson A. Repopulation of freeze-dried porcine valves with human fibroblasts and endothelial cells. J. Heart Valve Dis. 6, 296-306 (1997).
41. Schenke-Layland K, Opitz F, Gross M et al.. Complete dynamic repopulation of decellularized heart valves by application of defined physical signals - an in vitro study. Cardiovasc. Res. 60, 497-509 (2003).
42. Cushing MC, Jaeggli MP, Masters KS, Leinwand LA, Anseth KS. Serum deprivation improves seeding and repopulation of acellular matriced with valvular interstitial cells. J. Biomed. Mater. Res. A 75, 232-241 (2005).
43. 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. 14, 806-813 (2005).
44. Steinhoff G, Stock U, Karim N et al.. Tissue engineering of pulmonary heart valves on allogenic acellular matrix conduits. Circulation 102(Suppl. 3), III150-III155 (2000).
45. Kim S, Lim S, Hong Y et al.. Tissue engineering of heart valves in vivo using bone-marrow derived cells. Artif. Organs 30, 554-567 (2006).
46. Walles T, Lichtenberg A, Puschmann C et al.. in vivo model for cross-species porcine endogenous retrovirus transmission using tissue engineered pulmonary arteries. Eur. J. Cardiothorac. Surg. 24, 358-363 (2003).
47. Shinoka T, Breuer CK, Tanel RE et al.. Tissue engineering of heart valves: valve replacement study in a lamb model. Ann. Thorac. Surg. 60, S513-S516 (1995).
48. Shinoka T, Ma PX, Shum-Tim D et al.. Tissue engineered heart valves: autologous valve replacement study in a lamb model. Circulation 94(Suppl. 3), III64-III68 (1996).
49. Kim WG, Cho SK, Kang MC, Lee TY, Park JK. Tissue-engineered heart valve leaflets: an animal study. Int. J. Artif. Organs 24, 642-648 (2001).
50. Sodian R, Hoerstrup SP, Sperling et al.. Early in vivo experience with tissue-engineered trileaflet heart valves. Circulation 102(Suppl. 3), III22-III29 (2000).
51. Stock UA, Nagashima M, Khalil PN et al.. Tissue-engineered valved conduits in the pulmonary circulation. J. Thorac. Cardiovasc. Surg. 119, 732-740 (2000).
52. Sutherland FWH, Perry TE, Yu Y et al.. From stem cells to viable semilunar autologous heart valve. Circulation 111, 2783-2791 (2005).
53. Hoerstrup SP, Sodian R, Sperling JS, Vacanti JP, Mayer JE. New pulsatile bioreactor for in vitro formation of tissue engineered valves. Tissue Eng. 6, 75-79 (2000).
54. Hoerstrup SP, Sodian R, Daebritz S et al.. Functional living trileaflet heart valves grown in vitro. Circulation 102(Suppl. 3), III44-III49 (2000).
55. Hoerstrup SP, Cummings I, Lachat M et al.. Functional growth in tissue-engineered vascular grafts: follow-up at 100 weeks in a large animal model. Circulation 114(Suppl.), I159-I166 (2006).
56. Shinoka T, Imai Y. Transplantation of a tissue-engineered pulmonary artery. N. Engl. J. Med. 344, 532-533 (2001).
57. Matsumura G, Hibino N, Ikada Y, Kurosawa H, Shinoka T. Successful application of tissue engineered vascular autografts: clinical experience. Biomaterials 24, 2303-2308 (2003).
58. Schmidt D, Mol A, Breymann C et al.. Living autologous heart valves engineered from human prenatally harvested progenitors. Circulation 114(Suppl.), I125-I131 (2006).
59. Schmidt D, Mol A, Odermatt B et al.. Engineering of biologically active living heart valve leaflets using umbilical cord-derived progenitor cells. Tissue Eng. 12, 3223-3232 (2006).
60. Sodian R, Lueders C, Kraemer L et al.. Tissue engineering of autologous human heart valves using cryopreserved vascular umbilical cord cells. Ann. Thorac. Surg. 81, 2207-2216 (2006).
61. Schmidt D, Achermann J, Odermatt B et al.. Prenatally fabricated autologous human living heart valves based on amniotic fluid derived progenitor cells as a single cell source. Circulation 116(Suppl.), I64-I70 (2007).
62. Schmidt D, Achermann J, Odermatt B, Genoni M, Zund G, Hoerstrup SP. Cryopreserved amniotic fluid-derived cells: a lifelong autologous fetal stem cell source for heart valve tissue engineering. J. Heart Valve Dis. 17, 446-455 (2008).
63. Hoerstrup SP, Kadner A, Melnitchouk S et al.. Tissue engineering of functional trileaflet heart valves from human marrow stromal cells. Circulation 106(Suppl.), I143-I150 (2002).
64. Mol A, Driessen NJB, Rutten MCM, Hoerstrup SP, Bouten CVC, Baaijens FPT. Tissue engineering of human heart valve leaflets: a novel bioreactor for a strain-based conditioning approach. Ann. Biomed. Eng. 33, 1778-1788 (2005).
65. Dumont K, Yperman J, Verbeken E et al.. Design of a new pulsatile bioreactor for tissue engineered aortic heart valve formation. Artif. Organs 26, 710-714 (2002).
66. Hildebrand DK, Wu ZJ, Mayer JE, Sacks MS. Design and hydrodynamic evaluation of a novel pulsatile bioreactor for biologically active heart valves. Ann. Biomed. Eng. 32, 1039-1049 (2004).
67. Morsi YS, Yang WW, Owida A, Wong CS. Development of a novel pulsatile bioreactor for tissue culture. J. Artif. Organs 10, 109-114 (2007).
68. Mol A, Rutten MCM, Driessen NJB, Bouten CVC, Baaijens FPT, Hoerstrup SP. Autologous human tissue-engineered heart valves: prospects for systemic application. Circulation 114(Suppl.), I152-I158 (2006).
69. Sodian R, Loebe M, Hein A et al.. Application of stereolithography for scaffold fabrication for tissue engineered heart valves. ASAIO J. 48, 12-16 (2002).
70. van Lieshout MI, Vaz CM, Rutten MCM, Peters GW, Baaijens FPT. Electrospinning versus knitting: two scaffolds for tissue engineering of the aortic valve. J. Biomaterials Sci. Polym. Ed. 17, 77-89 (2006).
71. Morsi YS, Wong CS. Current developments and future challenges for the creation of aortic heart valve. J. Mech. Med. Biol. 8, 1-15 (2008).
72. Jockenhoevel S, Chalabi K, Sachweh JS et al.. Tissue engineering: complete autologous valve conduit - a new moulding technique. Thorac. Cardiovasc. Surg. 49, 287-290 (2001).
73. Flanagan TC, Cornelissen C, Koch S et al.. The in vitro development of autologous fibrin-based tissue-engineered heart valves through optimised dynamic conditioning. Biomaterials 28, 3388-3397 (2007).
74. Jockenhoevel S, Zund G, Hoerstrup SP et al.. Fibrin gel-advantages of a new scaffold in cardiovascular tissue engineering. Eur. J. Cardiothorac. Surg. 19, 424-430 (2001).
75. Neidert MR, Tranquillo RT. Tissue-engineered valves with commissural alignment. Tissue Eng. 12, 891-903 (2006).
76. Mol A, Lieshout van MI, Dam-de Veen CG et al.. Fibrin as a cell carrier in cardiovascular tissue engineering aaplications. Biomaterials 26, 3113-3121 (2005).
77. Scott M, Vesely I. Aortic valve cusp microstructure: the role of elastin. Ann. Thorac. Surg. 60, S391-S394 (1995).
78. Vesely I. The role of elastin in aortic valve mechanics. J. Biomech. 31, 115-123 (1998).
79. Lee TC, Midura RJ, Hascall VC, Vesely I. The effect of elastin damage on the mechanics of the aortic valve. J. Biomech. 34, 203-210 (2001).
80. Anidjar S, Salzmann JL, Gentric D, Lagneau P, Camilleri JP, Michel JB. Elastase-induced experimental aneurysms in rats. Circulation 82, 973-981 (1990).
81. Patel A, Fine B, Sandig M, Mequanint K. Elastin biosynthesis: the missing link in tissue-engineered blood vessels. Cardiovasc. Res. 71, 40-49 (2006).
82. Long JL, Tranquillo RT. Elastic fiber production in cardiovascular tissue-equivalents. Matrix Biol. 22, 339-350 (2003).
83. Williams C, Johnson SL, Robinson PS, Tranquillo RT. Cell sourcing and culture conditions for fibrin-based valve constructs. Tissue Eng. 12, 1489-1502 (2006).
84. Yang C, Sodian R, Fu P et al. in vitro fabrication of a tissue engineered human cardiovascular patch for future use in cardiovascular surgery. Ann. Thorac. Surg. 81, 57-64 (2006).
85. Ogle BM, Mooradian DL. Manipulation of remodelling pathways to enhance the mechanical properties of a tissue engineered blood vessel. J. Biomech. Eng. 124, 724-733 (2002).
86. Luo Y, Kobler JB, Zeitels SM, Langer R. Effects of growth factors on extracellular matrix production by vocal cord fibroblasts in 3-dimensional culture. Tissue Eng. 12, 3365-3374 (2006).
87. Gupta V, Grande-Allen J. Effects of static and cyclic loading in regulating extracellular matrix synthesis by cardiovascular cells. Cardiovasc. Res. 72, 375-383 (2006).
88. Rosenbloom J, Abrams WR, Mecham R. Extracellular matrix 4: the elastic fiber. FASEB J. 7, 1208-1218 (1993).
89. Balguid A, Rubbens MP, Mol A et al.. The role of collagen cross-links in biomechanical behavior of human aortic heart valve leaflets - relevance for tissue engineering. Tissue Eng. 13, 1501-1511 (2007).
90. Huang SD, Liu XH, Bai CG et al.. Synergistic effect of fibronectin and hepatocyte growth factor on stable cell-matrix adhesion, re-endothelialization, and reconstitution in developing tissue-engineered heart valves. Heart Vessels 22, 116-122 (2007).
91. Robinson PS, Johnson SL, Evans MC, Barocas VH, Tranquillo RT. Functional tissue-engineered valves from cell-remodeled fibrin with commissural alignment of cell-produced collagen. Tissue Eng. Part A 14, 83-95 (2008).
92. Mol A, Bouten CV, Zund G et al.. The relevance of large strains in functional tissue engineering of heart valves. Thorac. Cardiovasc. Surg. 51, 78-83 (2003).
93. Isenberg BC, Tranquillo RT. Long-term cyclic distention enhances the mechanical properties of collagen based media-equivalents. Ann. Biomed. Eng. 31, 937-949 (2003).
94. Seliktar D, Nerem RM, Galis ZS. Mechanical strain stimulated remodeling of tissue-engineered blood vessel constructs. Tissue Eng. 9, 657-666 (2003).
95. Hinz B, Gabbiani G. Mechanisms of force generation and transmission by myofibroblasts. Curr. Opinion. Biotechnol. 14, 538-546 (2003).
96. Grenier G, Rémy-Zolghadri M, Larouche D et al.. Tissue reorganization in response to mechanical load increases functionality. Tissue Eng. 11, 90-100 (2005).
97. Boerboom RA, Rubbens MP, Driessen NJB, Bouten CVC, Baaijens FPT. Effect of strain magnitude on the tissue properties of engineered cardiovascular constructs. Ann. Biomed. Eng. 36, 244-253 (2008).
98. Rubbens MP, Mol A, Marion van MH et al.. Straining-mode dependent collagen remodeling in engineered cardiovascular tissues. Tissue Eng. DOI: 10.1089/ten.tea.2008.0185 (2008) (Epub ahead of print).
99. Rubbens MP, Mol A, Boerboom RA, Bank RA, Baaijens FPT, Bouten CVC. Intermittent straining accelerates the development of tissue properties in engineered heart valve tissue. Tissue Eng. DOI: 10.1089/ ten.tea.2007.0396 (2008) (Epub ahead of print).
100. Balguid A, Mol A, Vlimmeren MA, Baaijens FPT, Bouten CVC. Hypoxia induces near-native mechanical properties in engineered heart valve tissue. Circulation 119, 290-297 (2009).
101. Kortsmit J, Driessen NJB, Rutten MCM, Baaijens FPT. Real-time non-invasive assessment of leaflet deformation in heart valve tissue engineering. Ann. Biomed. Eng. 37(3), 532-541 (2009).
102. Kortsmit J, Driessen NJB, Rutten MCM, Baaijens FPT. Nondestructive and noninvasive assessment of mechanical properties in heart valve tissue engineering. Tissue Eng. Part A DOI: 10.1089/ten.tea.2008.0197 (2009) (Epub ahead of print).
103. Yacoub M. Viewpoint: heart valve engineering. Interview by James Butcher. Circulation 116, F44-F46 (2007).
104. Driessen NJB, Mol A, Bouten CVC, Baaijens FPT. Modeling the mechanics of tissue-engineered human heart valve leaflets. J. Biomech. 40, 325-334 (2007).
105. Stute N, Holtz K, Bubenheim A, Lange C, Blake F, Zander AR. Autologous serum for isolation and expansion of human mesenchymal stem cells for clinical use. Exp. Hematol. 32, 1212-1225 (2004).
106. Bernardo ME, Avanzini MA, Perotti C et al.. Optimization of in vitro expansion of human multipotent mesenchymal stromal cells for cell-therapy approaches: further insights into the search for a fetal calf serum substitute. J. Cell. Physiol. 211, 121-130 (2007).
107. Kocaoemer A, Kern S, Kluter H, Bieback K. Human AB serum and thrombin-activated platelet-rich plasma are suitable alternatives to fetal calf serum for the expansion of mesenchymal stem cells from adipose tissue. Stem Cells 25, 1270-1278 (2007).
108. Lutter G, Ardehali R, Cremer J, Bonhoeffer P. Percutaneous valve replacement: current state and future prospects. Ann. Thorac. Surg. 78, 2199-2206 (2004).
109. Lichtenstein SV, Cheung A, Ye J et al.. Transapical transcatheter aortic valve implantation in humans. Initial clinical experience. Circulation 114, 591-596 (2006).
110. Walther T, Simon P, Dewey T et al.. Transapical minimally invasive aortic valve implantation: multicenter experience. Circulation 116(Suppl.), I240-I245 (2007).
111. Stock UA, Degenkolbe I, Atmann T, Schenke-Layland K, Freitag S, Lutter G. Prevention of device-related tissue damage during percutaneous deployement of tissue-engineered heart valves. J. Thorac. Cardiovasc. Surg. 131, 1323-1330 (2006).
112. Goldstein S, Clarke DR, Walsh SP, Black KS, O'Brien MF. Transpecies heart valve transplant: advanced studies of a bioengineered xeno-autograft. Ann. Thorac. Surg. 70, 1962-1969 (2000).
113. Elkins RC, Goldstein S, Hewitt CW et al.. Recellularization of heart valve grafts by a process of adaptive remodeling. Semin. Thorac. Cardiovasc. Surg. 13(Suppl. 1), I87-I92 (2001).
114. Leyh RG, Wilhelmi M, Rebe P et al.. in vivo repopulation of xenogeneic and allogeneic acellular valvular matrix conduits in the pulmonary circulation. Ann. Thorac. Surg. 75, 1457-1463 (2003).
115. Takagi K, Fukunaga S, Nishi A et al.. in vivo recellularization of plain decellularized xenografts with specific cell characterization in the systemic circulation: histological and immunohistochemical study. Artif. Organs 30, 233-241 (2006).
116. Kim WG, Huh JH. Time related histopathological changes of acellularized xenogeneic pulmonary valved conduits. ASAIO J. 50, 601-605.
117. Iwai S, Torikai K, Coppin CM, Sawa Y. Minimally immunogenic decellularized porcine valve provides in situ recellularization as a stentless bioprosthetic valve. J. Artif. Organs 10, 29-35 (2007).
118. Erdbrugger W, Konertz W, Dohmen PM et al.. Decellularized xenogenic heart valves reveal remodeling and growth potential in vivo. Tissue Eng. 12, 2059-2068 (2006).
119. Dohmen PM, da Costa F, Holonski S et al.. Is there a possibility for a glutaraldehyde-free porcine heart valve to grow? Eur. Surg. Res. 38, 54-61 (2006).
120. Simon P, Kasimir MT, Seebacher G et al.. Early failure of the tissue engineered porcine heart valve SYNERGRAFT in pediatric patients. Eur. J. Cardiothorac. Surg. 23, 1002-1006 (2003).
121. Kasimir MT, Rieder E, Seebacher G et al.. Decellularization does not eliminate thrombogenicity and inflammatory stimulation in tissue-engineered porcine heart valves. J. Heart Valve Dis. 15, 278-286 (2006).
122. Rieder E, Nigisch A, Dekan B et al.. Granulocyte-based immune response against decellularized or glutaraldehyde cross-linked vascular tissue. Biomaterials 27, 5634-5642 (2006).
123. Bastian F, Stelzmüller ME, Kratochwill K, Kasimir MT, Simon P, Weigel G. IgG deposition and activation of the classical complement pathway involved in the activation of human granulocytes by decellularized porcine heart valve tissue. Biomaterials 29, 1824-1832 (2008).
124. Rieder E, Kasimir MT, Silberhumer G et al.. Decellularization protocols of porcine heart valves differ importantly in efficiency of cell removal and susceptibility of the matrix to recellularization with human vascular cells. J. Thorac. Cardiovasc. Surg. 127, 399-405 (2004).
125. Dohmen PM, Konertz W. Results with decellularized xenografts. Circ. Res. 99, E10 (2006).
126. Dohmen PM, Hauptmann S, Terytze A, Konertz W. in vivo repopulation of a tissue-engineered heart valve in a human subject. J. Heart Valve Dis. 16, 447-449 (2007).
127. Stamm C, Khosravi A, Grabow N et al.. Biomatrix/polymer composite material for heart valve tissue engineering. Ann. Thorac Surg. 78, 2084-2092 (2004).
128. Stamm C, Steinhoff G. When less is more: go slowly when repopulating a valve in vivo. J. Thorac. Cardiovasc. Surg. 132, 735-737 (2007).
129. Lichtenberg A, Cebotari S, Tudorache I et al.. Flow-dependent re-endothelialization of tissue-engineered heart valves. J. Heart Valve Dis. 15, 287-293 (2006).
130. Lichtenberg A, Tudorache I, Cebotari et al. in vitro re-endothelialization of detergent decellularized heart valves under simulated physiological dynamic conditions. Biomaterials 27, 4221-4229 (2006).
131. Stock UA, Schenke-Layland K. Performance of decellularized xenogeneic tissue in heart valve replacement. Biomaterials 27, 1-2 (2006).
132. Rieder E, Seebacher G, Kasimir MT et al.. Tissue engineering of heart valves: decellularized porcine and human valve scaffolds differ importantly in residual potential to attract monocytic cells. Circulation 111, 2792-2797 (2005).
133. Sayk F, Bos I, Schubert U, Wedel T, Sievers HH. Histopathologic findings in a novel decellularized pulmonary homograft: an autopsy study. Ann. Thorac. Surg. 79, 1755-1758 (2005).
134. Miller DV, Edwards WD, Zehr KJ. Endothelial and smooth muscle cell populations in a decellularized cryopreserved aortic homograft (SynerGraft) 2 years after implantation. J. Thorac. Cardiovasc. Surg. 132, 175-176 (2006).
135. Elkins RC, Dawson PE, Goldstein S, Walsh SP, Black SP. Decellularized human valve allografts. Ann. Thorac. Surg. 71, S428-S432.
136. Zehr KJ, Yagubyan M, Connolly HM, Nelson, Schaff HV. Aortic root replacement with a novel decellularized cryopreserved aortic homograft: postoperative immunoreactivity and early results. J. Thorac. Cardiovasc. Surg. 130, 1010-1015 (2005).
137. Bechtel JF, Müller-Steinhardt M, Schmidtke C, Brunswik A, Stierle U, Sievers HH. Evaluation of the decellularized valve homograft (SynerGraft®). J. Heart Valve Dis. 12, 734-739 (2003).
138. Bechtel JF, Stierle U, Sievers HH. Fifty-two months' mean follow up of decellularized SynerGraft-treated pulmonary valve allografts. J. Heart Valve Dis. 17, 98-104 (2008).
139. Shinoka T, Shum-Tim D, Ma PX et al.. Creation of viable pulmonary autografts through tissue engineering. J. Thorac. Cardiovasc. Surg. 115, 536-545 (1998).
140. Iwai S, Sawa Y, Ichikawa H et al.. Biodegradable polymer with collagen microsponge serves as new bioengineered cardiovascular prosthesis. J. Thorac. Cardiovasc. Surg. 128, 472-479 (2004).
141. Iwai S, Sawa Y, Taketani S, Torikai K, Hirakawa K, Matsuda H. Novel tissue-engineered biodegradable material for reconstruction of vascular wall. Ann. Thorac. Surg. 80, 1821-1827 (2005).
142. Torikai K, Ichikawa H, Hirakawa K et al.. A self-renewing, tissue-engineered vascular graft for arterial reconstruction. J. Thorac. Cardiovasc. Surg. 136, 37-45 (2008).
143. Yokota T, Ichikawa H, Matsumiya G et al.. in situ tissue regeneration using a novel tissue-engineered, small-caliber vascular graft without cell seeding. J. Thorac. Cardiovasc. Surg. 136, 900-907 (2008).
144. Hibino N, Shinoka T, Matsumura G, Ikada Y, Kurosawa H. The tissue-engineered vascular graft using bone marrow without culture. J. Thorac. Cardiovasc. Surg. 129, 1064-1070 (2005).
145. Shinoka T, Matsumura G, Hibino N et al.. Midterm clinical result of tissue-engineered vascular autografts seeded with autologous bone marrow cells. J. Thorac. Cardiovasc. Surg. 129, 1330-1338 (2005).
146. Matsumura G, Ishihara Y, Miyagawa-Tomita S et al.. Evaluation of tissue-engineered vascular autografts. Tissue Eng. 12, 3075-3083 (2006).
147. Brennan MP, Dardik A, Hibino N et al.. Tissue-engineered vascular grafts demonstrate evidence of growth and development when implanted in a juvenile animal model. Ann. Surg. 248, 370-377 (2008).
148. De Visscher G, Vranken I, Lebacq A et al. in vivo cellularization of a cross-linked matrix by intraperitoneal implantation: a new tool in heart valve tissue engineering. Eur. Heart J. 28, 1389-1396 (2007).
149. De Visscher G, Blockx H, Meuris B et al.. Functional and biomechanical evaluation of a completely recellularized stentless pulmonary bioprostheses in sheep. J. Thorac. Cardiovasc. Surg. 135, 395-404 (2008).
150. Sievers HH. in vivo tissue engineering an autologous semilunar biovalve: can we get what we want? J. Thorac. Cardiovasc. Surg. 134, 20-22 (2007).
151. Vranken I, De Visscher G, Lebacq A, Verbeken E, Flameng W. The recruitment of primitive Lin(-), Sca-1(+), CD34(+), c-kit(+) and CD271(+) cells during the early intraperitoneal foreign body reaction. Biomaterials 29, 797-808 (2008).
152. Shi Q, Rafii S, Wu MH et al.. Evidence for circulating bone marrow-derived endothelial cells. Blood 92, 362-367 (1998).
153. Asahara T, Masuda H, Takahashi T et al.. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ. Res. 85, 221-228 (1999).
154. Shimizu K, Sugiyma S, Aikawa M et al.. Host bone-marrow cell are a source of donor intimal smooth-muscle-like cells in murine aortic transplant arteriopathy. Nat. Med. 7, 738-741 (2001).
155. Zilla P, Bezuidenhout D, Human P. Prosthetic vascular grafts: wrong models, wrong questions and no healing. Biomaterials 28, 5009-5027 (2007).
156. Deb A, Wang SH, Skelding K, Miller D, Simper D, Caplice N. Bone marrow-derived myofibroblasts are present in adult human heart valves. J. Heart Valve Dis. 14, 674-678 (2005).
157. Lee SJ, Van Dyke M, Atala A, Yoo JJ. Host cell mobilization for in situ tissue regeneration. Rejuvenation Res. 11, 747-756 (2008).
158. Schutte RJ, Xie L, Klitzman B, Reichert WM. in vivo cytokine-associated responses to biomaterials. Biomaterials 30, 160-168 (2009).
159. Aoki J, Serruys PW, Van Beusekom H et al.. Endothelial progenitor cell capture by stents coated with antibody against CD34: the HEALING-FIM (Healthy Endothelial Accelerated Lining Inhibits Neointimal Growth-First In Man) Registry. J. Am. Coll. Cardiol. 45, 1574-1579 (2005).
160. Avci-Adali M, Paul A, Ziemer G, Wendel HP. New strategies for in vivo tissue engineering by mimicry of homing factors for self-endothelialisation of blood contacting materials. Biomaterials 29, 3936-3945 (2008).
161. Ota T, Sawa Y, Iwai S et al.. Fibronectin-hepatocyte growth factor enhances reendothelialization in tissue-engineered heart valve. Ann. Thorac. Surg. 80, 1801-1802 (2005).
162. Stephan S, Ball SG, Williamson M et al.. Cell-matrix biology in vascular tissue engineering. J. Anat. 209, 495-502 (2006).
163. Williamson MR, Shuttleworth A, Canfield AE, Black RA, Kielty CM. The role of endothelial cell attachment to elastic fibre molecules in the enhancement of monolayer formation and retention, and the inhibition of smooth muscle cell recruitment. Biomaterials 28, 5307-5318 (2007).
164. Damsky CH, Ilic D. Integrin signaling: it's where the action is. Curr. Opin. Cell Biol. 14, 594-602 (2002).
165. Meyers SR, Khoo X, Huang X, Walsh EB, Grinstaff MW, Kenan DJ. The development of peptide-based interfacial biomaterials for generating biological functionality on the surface of bioinert materials. Biomaterials 30, 277-286 (2009).
166. Kim TG, Park TG. Biomimicking extracellular matrix: cell adhesive RGD peptide modified electrospun poly(d,l-lactic-co-glycolic acid) nanofiber mesh. Tissue Eng. 15, 221-233 (2006).
167. Sales VL, Engelmayr GC Jr, Johnson JA Jr et al.. Protein precoating of elastomeric tissue-engineering scaffolds increased cellularity, enhanced extracellular matrix protein production, and differentially regulated the phenotypes of circulating endothelial progenitor cells. Circulation 116(Suppl.), I55-I63 (2007).
168. Schmidt-Lucke C, Rossig L, Fichtlscherer S et al.. Reduced number of circulating endothelial progenitor cells predicts future cardiovascular events: proof of concept for the clinical importance of endogenous vascular repair. Circulation 111, 2981-2987 (2005).
169. Tillman BW, Yazdani SK, Lee SJ, Geary RL, Atala A, Yoo JJ. The in vivo stability of electrospun polycaprolactone-collagen scaffolds in vascular reconstruction. Biomaterials 30, 583-588 (2009).
170. Wisse E, Govaert LE, Meijer HEH, Meijer EW. Unusual tuning of mechanical properties of thermoplastic elastomers using supramolecular fillers. Macromolecules 39, 7425-7432 (2006).
171. Pektok E, Nottelet B, Tille J et al.. Degradation and healing characteristics of small-diameter poly(e-caprolactone) vascular grafts in the rat systemic arterial circulation. Circulation 118, 2563-2570 (2008).