Cited by 117Tissue Engineering and Regenerative Medicine3D Printing in Biomedical ResearchCardiac Valve Diseases and Treatments

Recellularization of decellularized heart valves: Progress toward the tissue-engineered heart valve

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VeDepo, Mitchell C, Detamore, Michael S, Hopkins, Richard A, Converse, Gabriel L·2017·Journal of Tissue Engineering

Abstract

The tissue-engineered heart valve portends a new era in the field of valve replacement. Decellularized heart valves are of great interest as a scaffold for the tissue-engineered heart valve due to their naturally bioactive composition, clinical relevance as a stand-alone implant, and partial recellularization in vivo. However, a significant challenge remains in realizing the tissue-engineered heart valve: assuring consistent recellularization of the entire valve leaflets by phenotypically appropriate cells. Many creative strategies have pursued complete biological valve recellularization; however, identifying the optimal recellularization method, including in situ or in vitro recellularization and chemical and/or mechanical conditioning, has proven difficult. Furthermore, while many studies have focused on individual parameters for increasing valve interstitial recellularization, a general understanding of the interacting dynamics is likely necessary to achieve success. Therefore, the purpose of this review is to explore and compare the various processing strategies used for the decellularization and subsequent recellularization of tissue-engineered heart valves.

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  • Hypoxic bioreactor conditioning increases cellular infiltration in decellularized heart valve leaflets.

    “Initiatives to develop decellularized heart valves with anti‐calcification properties have been undertaken, with hypoxic bioreactor conditioning demonstrating increased cellular infiltration in valve leaflets.[ 169 , 170 ]”

    From Bioactive scaffolds for tissue engineering: A review of decellularized extracellular matrix applications and innovations (2025) · cites this paper as [170]

    The In vitro recellularization section (page unavailable) reports greater leaflet cell infiltration after cyclic pressure conditioning in a bioreactor than after static culture. It describes mechanical pressure conditioning, not hypoxic conditioning; the claimed role of hypoxia is unsupported. (LLM, conf=0.87)

    Experimental — accuracy not yet measured

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References 144 · Cited by 117

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  1. [1]D’Arcy JL Prendergast BD Chambers JB et al Valvular heart disease: the next cardiac epidemic. Heart 2011; 97: 91– 93. 21149862
  2. [2]Go AS Mozaffarian D Roger VL et al Heart disease and stroke statistics—2014 update: a report from the American Heart Association. Circulation 2014; 129: e28– e292. 24352519 PMC5408159
  3. [3]Nkomo VT Gardin JM Skelton TN et al Burden of valvular heart diseases: a population-based study. Lancet 2006; 368: 1005– 1011. 16980116
  4. [4]Yacoub MH Takkenberg JJ. Will heart valve tissue engineering change the world? Nat Clin Pract Cardiovasc Med 2005; 2: 60– 61. 16265355
  5. [5]Bourguignon T Bergoend E Mirza A et al Risk factors for valve-related complications after mechanical heart valve replacement in 505 patients with long-term follow up. J Heart Valve Dis 2011; 20: 673– 680. 22655498
  6. [6]Hopkins RA Jones AL Wolfinbarger L et al Decellularization reduces calcification while improving both durability and 1-year functional results of pulmonary homograft valves in juvenile sheep. J Thorac Cardiovasc Surg 2009; 137: 907– 913. 19327516
  7. [7]Siddiqui RF Abraham JR Butany J. Bioprosthetic heart valves: modes of failure. Histopathology 2009; 55: 135– 144. 19694820
  8. [8]Hopkins R. From cadaver harvested homograft valves to tissue-engineered valve conduits. Prog Pediatr Cardiol 2006; 21: 137– 152.
  9. [9]Brody S Pandit A. Approaches to heart valve tissue engineering scaffold design. J Biomed Mater Res B Appl Biomater 2007; 83: 16– 43. 17318822
  10. [10]Li F Li W Johnson S et al Low-molecular-weight peptides derived from extracellular matrix as chemoattractants for primary endothelial cells. Endothelium 2004; 11: 199– 206. 15370297
  11. [11]Iop L Renier V Naso F et al The influence of heart valve leaflet matrix characteristics on the interaction between human mesenchymal stem cells and decellularized scaffolds. Biomaterials 2009; 30: 4104– 4116. 19481252
  12. [12]Converse GL Armstrong M Quinn RW et al Effects of cryopreservation, decellularization and novel extracellular matrix conditioning on the quasi-static and time-dependent properties of the pulmonary valve leaflet. Acta Biomater 2012; 8: 2722– 2729. 22484150
  13. [13]Korossis SA Booth C Wilcox HE et al Tissue engineering of cardiac valve prostheses II: biomechanical characterization of decellularized porcine aortic heart valves. J Heart Valve Dis 2002; 11: 463– 471. 12150291
  14. [14]Liao J Joyce EM Sacks MS. Effects of decellularization on the mechanical and structural properties of the porcine aortic valve leaflet. Biomaterials 2008; 29: 1065– 1074. 18096223 PMC2253688
  15. [15]VeDepo MC Buse EE Quinn RW et al Species-specific effects of aortic valve decellularization. Acta Biomater 2017; 50: 249– 258. 28069510
  16. [16]Argento G Simonet M Oomens CW et al Multi-scale mechanical characterization of scaffolds for heart valve tissue engineering. J Biomech 2012; 45: 2893– 2898. 22999107
  17. [17]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 2003; 23: 1002– 1006; discussion 1006. 12829079
  18. [18]Dohmen PM Hauptmann S Terytze A et al In-vivo repopularization of a tissue-engineered heart valve in a human subject. J Heart Valve Dis 2007; 16: 447– 449. 17702372
  19. [19]Dohmen PM Lembcke A Holinski S et al Mid-term clinical results using a tissue-engineered pulmonary valve to reconstruct the right ventricular outflow tract during the Ross procedure. Ann Thorac Surg 2007; 84: 729– 736. 17720368
  20. [20]Dohmen PM Lembcke A Holinski S et al Ten years of clinical results with a tissue-engineered pulmonary valve. Ann Thorac Surg 2011; 92: 1308– 1314. 21958777
  21. [21]Dohmen PM Lembcke A Hotz H et al Ross operation with a tissue-engineered heart valve. Ann Thorac Surg 2002; 74: 1438– 1442. 12440590
  22. [22]Dohmen PM. Clinical results of implanted tissue engineered heart valves. HSR Proc Intensive Care Cardiovasc Anesth 2012; 4: 225– 231. 23439388 PMC3563556
  23. [23]Quinn R Hilbert S Converse G et al Enhanced autologous re-endothelialization of decellularized and extracellular matrix conditioned allografts implanted into the right ventricular outflow tracts of juvenile sheep. Cardiovasc Eng Techn 2012; 3: 217– 227.
  24. [24]Quinn RW Hilbert SL Bert AA et al Performance and morphology of decellularized pulmonary valves implanted in juvenile sheep. The Ann Thorac Surg 2011; 92: 131– 137. 21718838
  25. [25]Wang S Goecke T Meixner C et al Freeze-died heart valve scaffolds. Tissue Eng Part C Methods 2012; 18: 517– 525. 22224705
  26. [26]Kluin J Talacua H Smits AI et al In situ heart valve tissue engineering using a bioresorbable elastomeric implant—from material design to 12 months follow-up in sheep. Biomaterials 2017; 125: 101– 117. 28253994
  27. [27]Xue Y Sant V Phillippi J et al Biodegradable and biomimetic elastomeric scaffolds for tissue-engineered heart valves. Acta Biomater 2017; 48: 2– 19. 27780764
  28. [28]Cheung DY Duan B Butcher JT. Current progress in tissue engineering of heart valves: multiscale problems, multiscale solutions. Expert Opin Biol Ther 2015; 15: 1155– 1172. 26027436 PMC4883659
  29. [29]Mol A Smits AI Bouten CV et al Tissue engineering of heart valves: advances and current challenges. Expert Rev Med Devices 2009; 6: 259– 275. 19419284
  30. [30]Crapo PM Gilbert TW Badylak SF. An overview of tissue and whole organ decellularization processes. Biomaterials 2011; 32: 3233– 3243. 21296410 PMC3084613
  31. [31]Gilbert TW. Strategies for tissue and organ decellularization. J Cell Biochem 2012; 113: 2217– 2222. 22415903
  32. [32]Keane TJ Londono R Turner NJ et al Consequences of ineffective decellularization of biologic scaffolds on the host response. Biomaterials 2012; 33: 1771– 1781. 22137126
  33. [33]Badylak SF. Decellularized allogeneic and xenogeneic tissue as a bioscaffold for regenerative medicine: factors that influence the host response. Ann Biomed Eng 2014; 42: 1517– 1527. 24402648
  34. [34]Badylak SF Gilbert TW. Immune response to biologic scaffold materials. Semin Immunol 2008; 20: 109– 116. 18083531 PMC2605275
  35. [35]Wong ML Griffiths LG. Immunogenicity in xenogeneic scaffold generation: antigen removal vs. decellularization. Acta Biomater 2014; 10: 1806– 1816. 24486910 PMC3976714
  36. [36]Bloch O Erdbrugger W Volker W et al Extracellular matrix in deoxycholic acid decellularized aortic heart valves. Med Sci Monit 2012; 18: BR487– BR492. 23207452 PMC3560792
  37. [37]Erdbrugger W Konertz W Dohmen PM et al Decellularized xenogenic heart valves reveal remodeling and growth potential in vivo. Tissue Eng 2006; 12: 2059– 2068. 16968148
  38. [38]Friedrich LH Jungebluth P Sjoqvist S et al Preservation of aortic root architecture and properties using a detergent-enzymatic perfusion protocol. Biomaterials 2014; 35: 1907– 1913. 24321707
  39. [39]Kasimir MT Rieder E Seebacher G et al Comparison of different decellularization procedures of porcine heart valves. Int J Artif Organs 2003; 26: 421– 427. 12828309
  40. [40]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 2007; 16: 567– 573; discussion 574. 17944130
  41. [41]Zhou J Fritze O Schleicher M et al Impact of heart valve decellularization on 3-D ultrastructure, immunogenicity and thrombogenicity. Biomaterials 2010; 31: 2549– 2554. 20061016
  42. [42]Cebotari S Tudorache I Jaekel T et al Detergent decellularization of heart valves for tissue engineering: toxicological effects of residual detergents on human endothelial cells. Artif Organs 2010; 34: 206– 210. 20447045
  43. [43]Grauss RW Hazekamp MG Oppenhuizen F et al Histological evaluation of decellularised porcine aortic valves: matrix changes due to different decellularisation methods. Eur J Cardiothorac Surg 2005; 27: 566– 571. 15784352
  44. [44]Meyer SR Chiu B Churchill TA et al Comparison of aortic valve allograft decellularization techniques in the rat. J Biomed Mater Res A 2006; 79: 254– 262. 16817222
  45. [45]Somers P De Somer F Cornelissen M et al Decellularization of heart valve matrices: search for the ideal balance. Artif Cells Blood Substit Immobil Biotechnol 2012; 40: 151– 162. 22192069
  46. [46]Naso F Gandaglia A Formato M et al Differential distribution of structural components and hydration in aortic and pulmonary heart valve conduits: impact of detergent-based cell removal. Acta Biomater 2010; 6: 4675– 4688. 20620247
  47. [47]Spina M Ortolani F El Messlemani A et al Isolation of intact aortic valve scaffolds for heart-valve bioprostheses: extracellular matrix structure, prevention from calcification, and cell repopulation features. J Biomed Mater Res A 2003; 67: 1338– 1350. 14624521
  48. [48]Yu BT Li WT Song BQ et al Comparative study of the Triton X-100-sodium deoxycholate method and detergent-enzymatic digestion method for decellularization of porcine aortic valves. Eur Rev Med Pharmacol Sci 2013; 17: 2179– 2184. 23893184
  49. [50]Schenke-Layland K Vasilevski O Opitz F et al Impact of decellularization of xenogeneic tissue on extracellular matrix integrity for tissue engineering of heart valves. J Struct Biol 2003; 143: 201– 208. 14572475
  50. [51]Luo J Korossis SA Wilshaw SP et al Development and characterization of acellular porcine pulmonary valve scaffolds for tissue engineering. Tissue Eng Part A 2014; 20: 2963– 2974. 24786313 PMC4229718
  51. [52]Jing H Wang Z Chang Q. De-endothelialized aortic homografts: a promising scaffold material for tissue-engineered heart valves. Cells Tissues Organs 2014; 200: 195– 203. 26138278
  52. [53]Ota T Taketani S Iwai S et al Novel method of decellularization of porcine valves using polyethylene glycol and gamma irradiation. Ann Thorac Surg 2007; 83: 1501– 1507. 17383366
  53. [54]Wong ML Leach JK Athanasiou KA et al The role of protein solubilization in antigen removal from xenogeneic tissue for heart valve tissue engineering. Biomaterials 2011; 32: 8129– 8138. 21810537
  54. [56]Qiao WH Liu P Hu D et al Sequential hydrophile and lipophile solubilization as an efficient method for decellularization of porcine aortic valve leaflets: structure, mechanical property and biocompatibility study. J Tissue Eng Regen Med. Epub ahead of print 13 12 2016 DOI: 10.1002/term.2388. 27957807 · DOI
  55. [57]Sawada K Terada D Yamaoka T et al Cell removal with supercritical carbon dioxide for acellular artificial tissue. J Chem Technol Biot 2008; 83: 943– 949.
  56. [58]Sierad LN Shaw EL Bina A et al Functional heart valve scaffolds obtained by complete decellularization of porcine aortic roots in a novel differential pressure gradient perfusion system. Tissue Eng Part C Methods 2015; 21: 1284– 1296. 26467108 PMC4663650
  57. [59]Dohmen PM da Costa F Holinski S et al Is there a possibility for a glutaraldehyde-free porcine heart valve to grow? Eur Surg Res 2006; 38: 54– 61. 16490995
  58. [60]Baraki H Tudorache I Braun M et al Orthotopic replacement of the aortic valve with decellularized allograft in a sheep model. Biomaterials 2009; 30: 6240– 6246. 19703713
  59. [61]Goldstein S Clarke DR Walsh SP et al Transpecies heart valve transplant: advanced studies of a bioengineered xeno-autograft. Ann Thorac Surg 2000; 70: 1962– 1969. 11156103
  60. [62]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 2006; 15: 278– 286; discussion 286. 16607912
  61. [63]Konertz W Angeli E Tarusinov G et al Right ventricular outflow tract reconstruction with decellularized porcine xenografts in patients with congenital heart disease. J Heart Valve Dis 2011; 20: 341– 347. 21714427
  62. [64]Voges I Brasen JH Entenmann A et al Adverse results of a decellularized tissue-engineered pulmonary valve in humans assessed with magnetic resonance imaging. Eur J Cardiothorac Surg 2013; 44: e272– e279. 23818571
  63. [65]Bechtel JF Stierle U Sievers HH. Fifty-two months’ mean follow up of decellularized SynerGraft-treated pulmonary valve allografts. J Heart Valve Dis 2008; 17: 98– 104; discussion 104. 18365576
  64. [66]Brown JW Ruzmetov M Eltayeb O et al Performance of SynerGraft decellularized pulmonary homograft in patients undergoing a Ross procedure. Ann Thorac Surg 2011; 91: 416– 422; discussion 422–423. 21256282
  65. [67]Konuma T Devaney EJ Bove EL et al Performance of CryoValve SG decellularized pulmonary allografts compared with standard cryopreserved allografts. Ann Thorac Surg 2009; 88: 849– 854; discussion 554–555. 19699910
  66. [68]Ruzmetov M Shah JJ Geiss DM et al Decellularized versus standard cryopreserved valve allografts for right ventricular outflow tract reconstruction: a single-institution comparison. J Thorac Cardiovasc Surg 2012; 143: 543– 549. 22340029
  67. [69]Sievers HH Stierle U Schmidtke C et al Decellularized pulmonary homograft (SynerGraft) for reconstruction of the right ventricular outflow tract: first clinical experience. Z Kardiol 2003; 92: 53– 59. 12545302
  68. [70]Tavakkol Z Gelehrter S Goldberg CS et al Superior durability of SynerGraft pulmonary allografts compared with standard cryopreserved allografts. Ann Thorac Surg 2005; 80: 1610– 1614. 16242425
  69. [72]Bibevski S Ruzmetov M Fortuna RS et al Performance of SynerGraft decellularized pulmonary allografts compared with standard cryopreserved allografts: results from multiinstitutional data. Ann Thorac Surg 2017; 103: 869– 874. 27788940
  70. [73]Cebotari S Tudorache I Ciubotaru A et al Use of fresh decellularized allografts for pulmonary valve replacement may reduce the reoperation rate in children and young adults: early report. Circulation 2011; 124: S115– S123. 21911800
  71. [74]Sarikouch S Horke A Tudorache I et al Decellularized fresh homografts for pulmonary valve replacement: a decade of clinical experience. Eur J Cardiothorac Surg 2016; 50: 281– 290. 27013071 PMC4951634
  72. [75]Da Costa FD Costa AC Prestes R et al The early and midterm function of decellularized aortic valve allografts. Ann Thorac Surg 2010; 90: 1854– 1860. 21095325
  73. [76]Della Rocca F Sartore S Guidolin D et al Cell composition of the human pulmonary valve: a comparative study with the aortic valve—the VESALIO Project. Vitalitate Exornatum Succedaneum Aorticum labore Ingegnoso Obtinebitur. Ann Thorac Surg 2000; 70: 1594– 1600. 11093493
  74. [77]Butcher JT Nerem RM. Valvular endothelial cells regulate the phenotype of interstitial cells in co-culture: effects of steady shear stress. Tissue Eng 2006; 12: 905– 915. 16674302
  75. [78]Liu AC Joag VR Gotlieb AI. The emerging role of valve interstitial cell phenotypes in regulating heart valve pathobiology. Am J Pathol 2007; 171: 1407– 1418. 17823281 PMC2043503
  76. [79]Iop L Bonetti A Naso F et al Decellularized allogeneic heart valves demonstrate self-regeneration potential after a long-term preclinical evaluation. PLoS ONE 2014; 9: e99593. 24940754 PMC4062459
  77. [80]Iop L Gerosa G. Guided tissue regeneration in heart valve replacement: from preclinical research to first-in-human trials. Biomed Res Int 2015; 2015: 432901 (13 pp.). 26495295 PMC4606187
  78. [81]James I Yi T Tara S et al Hemodynamic characterization of a mouse model for investigating the cellular and molecular mechanisms of neotissue formation in tissue engineered heart valves. Tissue Eng Part C Methods 2015; 21: 987– 994. 25915105 PMC4553370
  79. [82]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 2006; 30: 233– 241. 16643381
  80. [83]Iwai S Torikai K Coppin CM et al Minimally immunogenic decellularized porcine valve provides in situ recellularization as a stentless bioprosthetic valve. J Artif Organs 2007; 10: 29– 35. 17380294
  81. [84]Juthier F Vincentelli A Gaudric J et al Decellularized heart valve as a scaffold for in vivo recellularization: deleterious effects of granulocyte colony-stimulating factor. J Thorac Cardiovasc Surg 2006; 131: 843– 852. 16580443
  82. [85]Paniagua Gutierrez JR Berry H Korossis S et al Regenerative potential of low-concentration SDS-decellularized porcine aortic valved conduits in vivo. Tissue Eng Part A 2015; 21: 332– 342. 25156153 PMC4293138
  83. [86]Leyh RG Wilhelmi M Rebe P et al In vivo repopulation of xenogeneic and allogeneic acellular valve matrix conduits in the pulmonary circulation. Ann Thorac Surg 2003; 75: 1457– 1463; discussion 1463. 12735562
  84. [87]Honge JL Funder J Hansen E et al Recellularization of aortic valves in pigs. Eur J Cardiothorac Surg 2011; 39: 829– 834. 21055964
  85. [88]Cebotari S Lichtenberg A Tudorache I et al Clinical application of tissue engineered human heart valves using autologous progenitor cells. Circulation 2006; 114: I132– I137. 16820562
  86. [89]Neumann A Sarikouch S Breymann T et al Early systemic cellular immune response in children and young adults receiving decellularized fresh allografts for pulmonary valve replacement. Tissue Eng Part A 2014; 20: 1003– 1011. 24138470 PMC3938920
  87. [90]Perri G Polito A Esposito C et al Early and late failure of tissue-engineered pulmonary valve conduits used for right ventricular outflow tract reconstruction in patients with congenital heart disease. Eur J Cardiothorac Surg 2012; 41: 1320– 1325. 22219487
  88. [91]Ruffer A Purbojo A Cicha I et al Early failure of xenogenous de-cellularised pulmonary valve conduits—a word of caution! Eur J Cardiothorac Surg 2010; 38: 78– 85. 20219384
  89. [92]Assmann A Delfs C Munakata H et al Acceleration of autologous in vivo recellularization of decellularized aortic conduits by fibronectin surface coating. Biomaterials 2013; 34: 6015– 6026. 23683757
  90. [93]Flameng W De Visscher G Mesure L et al Coating with fibronectin and stromal cell-derived factor-1alpha of decellularized homografts used for right ventricular outflow tract reconstruction eliminates immune response-related degeneration. J Thorac Cardiovasc Surg 2014; 147: 1398– 1404.e2. 23896322
  91. [94]Ota T Sawa Y Iwai S et al Fibronectin-hepatocyte growth factor enhances reendothelialization in tissue-engineered heart valve. Ann Thorac Surg 2005; 80: 1794– 1801. 16242457
  92. [95]Jordan JE Williams JK Lee SJ et al Bioengineered self-seeding heart valves. J Thorac Cardiovasc Surg 2012; 143: 201– 208. 22047685
  93. [96]Williams JK Miller ES Lane MR et al Characterization of CD133 antibody-directed recellularized heart valves. J Cardiovasc Transl Res 2015; 8: 411– 420. 26341225
  94. [97]Hopkins RA Bert AA Hilbert SL et al Bioengineered human and allogeneic pulmonary valve conduits chronically implanted orthotopically in baboons: hemodynamic performance and immunologic consequences. J Thorac Cardiovasc Surg 2013; 145: 1098– 1107. 22841171 PMC3530005
  95. [98]Quinn RW Bert AA Converse GL et al Performance of allogeneic bioengineered replacement pulmonary valves in rapidly growing young lambs. J Thorac Cardiovasc Surg 2016; 152: 1156– 1165.e4. 27641300
  96. [99]Jana S Tranquillo RT Lerman A. Cells for tissue engineering of cardiac valves. J Tissue Eng Regen Med 2016; 10: 804– 824. 25712485
  97. [100]Bin F Yinglong L Nin X et al Construction of tissue-engineered homograft bioprosthetic heart valves in vitro. ASAIO J 2006; 52: 303– 309. 16760720
  98. [102]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 2005; 111: 2792– 2797. 15911701
  99. [103]Dainese L Guarino A Burba I et al Heart valve engineering: decellularized aortic homograft seeded with human cardiac stromal cells. J Heart Valve Dis 2012; 21: 125– 134. 22474754
  100. [104]Knight RL Booth C Wilcox HE et al Tissue engineering of cardiac valves: re-seeding of acellular porcine aortic valve matrices with human mesenchymal progenitor cells. J Heart Valve Dis 2005; 14: 806– 813. 16359063
  101. [105]Zeltinger J Landeen LK Alexander HG et al Development and characterization of tissue-engineered aortic valves. Tissue Eng 2001; 7: 9– 22. 11224920
  102. [106]Kim SS Lim SH Hong YS et al Tissue engineering of heart valves in vivo using bone marrow-derived cells. Artif Organs 2006; 30: 554– 557. 16836737
  103. [107]Steinhoff G Stock U Karim N et al Tissue engineering of pulmonary heart valves on allogenic acellular matrix conduits: in vivo restoration of valve tissue. Circulation 2000; 102: III50– III55. 11082362
  104. [108]Vincentelli A Wautot F Juthier F et al In vivo autologous recellularization of a tissue-engineered heart valve: are bone marrow mesenchymal stem cells the best candidates? J Thorac Cardiovasc Surg 2007; 134: 424– 432. 17662783
  105. [109]Emmert MY Weber B Wolint P et al Stem cell-based transcatheter aortic valve implantation: first experiences in a pre-clinical model. JACC Cardiovasc Interv 2012; 5: 874– 883. 22917460
  106. [110]Weber B Scherman J Emmert MY et al Injectable living marrow stromal cell-based autologous tissue engineered heart valves: first experiences with a one-step intervention in primates. Eur Heart J 2011; 32: 2830– 2840. 21415068
  107. [111]Thayer P Balachandran K Rathan S et al The effects of combined cyclic stretch and pressure on the aortic valve interstitial cell phenotype. Ann Biomed Eng 2011; 39: 1654– 1667. 21347552 PMC5467644
  108. [112]Yamamoto K Takahashi T Asahara T et al Proliferation, differentiation, and tube formation by endothelial progenitor cells in response to shear stress. J Appl Physiol 2003; 95: 2081– 2088. 12857765
  109. [113]Ahsan T Nerem RM. Fluid shear stress promotes an endothelial-like phenotype during the early differentiation of embryonic stem cells. Tissue Eng Part A 2010; 16: 3547– 3553. 20666609 PMC2992398
  110. [114]Merryman WD Lukoff HD Long RA et al Synergistic effects of cyclic tension and transforming growth factor-beta1 on the aortic valve myofibroblast. Cardiovasc Pathol 2007; 16: 268– 276. 17868877 PMC2094120
  111. [115]Merryman WD Youn I Lukoff HD et al Correlation between heart valve interstitial cell stiffness and transvalvular pressure: implications for collagen biosynthesis. Am J Physiol Heart Circ Physiol 2006; 290: H224– H231. 16126816
  112. [116]Rath S Salinas M Villegas AG et al Differentiation and distribution of marrow stem cells in flex-flow environments demonstrate support of the valvular phenotype. PLoS ONE 2015; 10: e0141802. 26536240 PMC4633293
  113. [117]Balachandran K Konduri S Sucosky P et al An ex vivo study of the biological properties of porcine aortic valves in response to circumferential cyclic stretch. Ann Biomed Eng 2006; 34: 1655– 1665. PMC1705516 17031600
  114. [118]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 2003; 60: 497– 509. 14659795
  115. [119]Lichtenberg A Cebotari S Tudorache I et al Flow-dependent re-endothelialization of tissue-engineered heart valves. J Heart Valve Dis 2006; 15: 287– 293; discussion 293–294. 16607913
  116. [120]Lichtenberg A Tudorache I Cebotari S et al In vitro re-endothelialization of detergent decellularized heart valves under simulated physiological dynamic conditions. Biomaterials 2006; 27: 4221– 4229. 16620956
  117. [121]Converse GL Buse EE Neill KR et al Design and efficacy of a single-use bioreactor for heart valve tissue engineering. J Biomed Mater Res B Appl Biomater 2017; 105: 249– 259. 26469196
  118. [122]Kajbafzadeh AM Ahmadi Tafti SH Mokhber-Dezfooli MR et al Aortic valve conduit implantation in the descending thoracic aorta in a sheep model: the outcomes of pre-seeded scaffold. Int J Surg 2016; 28: 97– 105. 26923632
  119. [123]Tudorache I Calistru A Baraki H et al Orthotopic replacement of aortic heart valves with tissue-engineered grafts. Tissue Eng Part A 2013; 19: 1686– 1694. 23488793 PMC3699955
  120. [124]Hong H Dong N Shi J et al Fabrication of a novel hybrid scaffold for tissue engineered heart valve. J Huazhong Univ Sci Technolog Med Sci 2009; 29: 599– 603. 19821093
  121. [125]Stamm C Khosravi A Grabow N et al Biomatrix/polymer composite material for heart valve tissue engineering. Ann Thorac Surg 2004; 78: 2084– 2092; discussion 92–93. 15561041
  122. [126]Deng C Dong N Shi J et al Application of decellularized scaffold combined with loaded nanoparticles for heart valve tissue engineering in vitro. J Huazhong Univ Sci Technolog Med Sci 2011; 31: 88– 93. 21336730
  123. [127]Zhou J Hu S Ding J et al Tissue engineering of heart valves: PEGylation of decellularized porcine aortic valve as a scaffold for in vitro recellularization. Biomed Eng Online 2013; 12: 87. 24006837 PMC3774219
  124. [128]Zhou J Nie B Zhu Z et al Promoting endothelialization on decellularized porcine aortic valve by immobilizing branched polyethylene glycolmodified with cyclic-RGD peptide: an in vitro study. Biomed Mater 2015; 10: 065014. 26584634
  125. [129]Hu XJ Dong NG Shi JW et al Evaluation of a novel tetra-functional branched poly(ethylene glycol) crosslinker for manufacture of crosslinked, decellularized, porcine aortic valve leaflets. J Biomed Mater Res B Appl Biomater 2014; 102: 322– 336. 24115395
  126. [130]Ouyang H Zhang JB Liu Y et al Research on application of modified polyethylene glycol hydrogels in the construction of tissue engineered heart valve. Zhonghua Wai Ke Za Zhi 2008; 46: 1723– 1726. 19094734
  127. [131]Zhou J Ye X Wang Z et al Development of decellularized aortic valvular conduit coated by heparin-SDF-1alpha multilayer. Ann Thorac Surg 2015; 99: 612– 618. 25499473
  128. [132]Ye X Hu X Wang H et al Polyelectrolyte multilayer film on decellularized porcine aortic valve can reduce the adhesion of blood cells without affecting the growth of human circulating progenitor cells. Acta Biomater 2012; 8: 1057– 1067. 22122977
  129. [133]Ye X Wang H Zhou J et al The effect of heparin-VEGF multilayer on the biocompatibility of decellularized aortic valve with platelet and endothelial progenitor cells. PLoS ONE 2013; 8: e54622. 23359625 PMC3554718
  130. [134]Theodoridis K Tudorache I Calistru A et al Successful matrix guided tissue regeneration of decellularized pulmonary heart valve allografts in elderly sheep. Biomaterials 2015; 52: 221– 228. 25818428
  131. [135]Ye X Zhao Q Sun X et al Enhancement of mesenchymal stem cell attachment to decellularized porcine aortic valve scaffold by in vitro coating with antibody against CD90: a preliminary study on antibody-modified tissue-engineered heart valve. Tissue Eng Part A 2009; 15: 1– 11. 18759669
  132. [136]Bertipaglia B Ortolani F Petrelli L et al Cell characterization of porcine aortic valve and decellularized leaflets repopulated with aortic valve interstitial cells: the VESALIO Project (Vitalitate Exornatum Succedaneum Aorticum Labore Ingenioso Obtenibitur). Ann Thorac Surg 2003; 75: 1274– 1282. 12683575
  133. [137]Dohmen PM da Costa F Yoshi S et al Histological evaluation of tissue-engineered heart valves implanted in the juvenile sheep model: is there a need for in-vitro seeding? J Heart Valve Dis 2006; 15: 823– 829. 17152791
  134. [138]Lu X Zhai W Zhou Y et al Crosslinking effect of Nordihydroguaiaretic acid (NDGA) on decellularized heart valve scaffold for tissue engineering. J Mater Sci Mater Med 2010; 21: 473– 480. 19936890
  135. [139]Zhai W Chang J Lin K et al Crosslinking of decellularized porcine heart valve matrix by procyanidins. Biomaterials 2006; 27: 3684– 3690. 16513164
  136. [140]Zhai W Lu X Chang J et al Quercetin-crosslinked porcine heart valve matrix: mechanical properties, stability, anticalcification and cytocompatibility. Acta Biomater 2010; 6: 389– 395. 19651252
  137. [141]Huang W Xiao DZ Wang Y et al Fn14 promotes differentiation of human mesenchymal stem cells into heart valvular interstitial cells by phenotypic characterization. J Cell Physiol 2014; 229: 580– 587. 24122208
  138. [142]Gwanmesia P Ziegler H Eurich R et al Opposite effects of transforming growth factor-beta1 and vascular endothelial growth factor on the degeneration of aortic valvular interstitial cell are modified by the extracellular matrix protein fibronectin: implications for heart valve engineering. Tissue Eng Part A 2010; 16: 3737– 3746. 20673026
  139. [143]Roh JD Sawh-Martinez R Brennan MP et al Tissue-engineered vascular grafts transform into mature blood vessels via an inflammation-mediated process of vascular remodeling. Proc Natl Acad Sci U S A 2010; 107: 4669– 4674. 20207947 PMC2842056
  140. [144]Weber B Scherman J Emmert MY et al Injectable living marrow stromal cell-based autologous tissue engineered heart valves: first experiences with a one-step intervention in primates. Eur Heart J 2011; 32: 2830– 2840. 21415068
  141. [147]Syedain Z Reimer J Schmidt J et al 6-month aortic valve implantation of an off-the-shelf tissue-engineered valve in sheep. Biomaterials 2015; 73: 175– 184. 26409002 PMC5520964
  142. [148]Syedain ZH Bradee AR Kren S et al Decellularized tissue-engineered heart valve leaflets with recellularization potential. Tissue Eng Part A 2013; 19: 759– 769. 23088577 PMC3566676
  143. [149]Syedain ZH Meier LA Reimer JM et al Tubular heart valves from decellularized engineered tissue. Ann Biomed Eng 2013; 41: 2645– 2654. 23897047 PMC3847912

Authors
VeDepo, M. C., Detamore, M. S., Hopkins, R. A., & Converse, G. L.
Affiliations
  • Children's Mercy Hospital (US)
  • University of Oklahoma (US)
Corresponding author
Converse, Gabriel L
Venue
Journal of Tissue Engineering
Published
2017-01-01
Volume
8
Pages
2041731417726327-2041731417726327
ISSN
2041-7314 (ISSN-L)
OpenAlex
W2748725547
Cited by
117
References
144
Citations by year
2026: 4 · 2025: 8 · 2024: 17 · 2023: 11 · 2022: 10 · 2021: 19 · 2020: 24 · 2019: 12 · 2018: 11 · 2017: 1
FWCI
2.78
Type
journal article
Language
en
Open access
Locations
  • Journal of Tissue Engineering (publishedVersion, cc-by-nc)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Topics
  • Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
  • Physical Sciences › Engineering › Biomedical Engineering › 3D Printing in Biomedical Research
  • Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac Valve Diseases and Treatments
Keywords
tissue-engineered heart valves, decellularized heart valves, recellularization, valve leaflets, valvular interstitial cells, mechanical conditioning, chemical conditioning, heart valve replacement

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