Cited by 45Tissue Engineering and Regenerative MedicineCardiac Valve Diseases and TreatmentsHydrogels: synthesis, properties, applications

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A method for simultaneously crosslinking and functionalizing extracellular matrix-based biomaterials as bioprosthetic heart valves with enhanced endothelialization and reduced inflammation

Abstract

With the coming of an aging society and the emergence of transcatheter valve technology, the implantation of bioprosthetic heart valves (BHVs) in patients with valvular disease has significantly increased worldwide. Currently, most clinically available BHVs are crosslinked with glutaraldehyde (GLUT). However, the GLUT treated BHV is less durable due to the combined effect of multiple factors such as cytotoxicity, immune responses, and calcification. In this study, the in-situ polymerization of sulfonic monomers with a decellularized extracellular matrix (ECM) was performed to simultaneously achieve the crosslinking and functionalization of ECM. Subsequently, the feasibility of the hybrid ECM used as leaflet material of BHV was evaluated. In in-vitro tests, the results indicated that the hybrid ECM fixed collagen efficiently and the introduction of sulfonic polymer promoted the proliferation and migration of human umbilical vein endothelial cells (HUVECs). In in-vivo tests, after being implanted in SD rats and mice, the hybrid ECM significantly inhibited immune response and calcification compared with the non-hybrid counterpart and GLUT crosslinked tissue. These results indicated that the hybrid ECM exhibited more competitive stability and better biocompatibility compared to these features in GLUT-crosslinked valve. Therefore, the sulfonic polymer hybrid ECM provides a potential material for more durable BHV and the in-situ polymerization strategy can serve as a general treatment method for tissue crosslinking as well as tailoring the biophysical properties of ECM.

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Research works printed but not linked: 75

  1. Zilla, 2008, Prosthetic heart valves: catering for the few, Biomaterials, 29, 385, 10.1016/j.biomaterials.2007.09.033 · DOI
  2. Walther, 2012, Contemporary management of aortic stenosis: surgical aortic valve replacement remains the gold standard, Heart, 98, iv23, 10.1136/heartjnl-2012-302399 · DOI
  3. Tam, 2015, A novel crosslinking method for improved tear resistance and biocompatibility of tissue based biomaterials, Biomaterials, 66, 83, 10.1016/j.biomaterials.2015.07.011 · DOI
  4. Yacoub, 2007, Establishing pediatric cardiovascular services in the developing world: a wake-up call, Circulation, 116, 1876, 10.1161/CIRCULATIONAHA.107.726265 · DOI
  5. D'Amore, 2018, Heart valve scaffold fabrication: Bioinspired control of macro-scale morphology, mechanics and micro-structure, Biomaterials, 150, 25, 10.1016/j.biomaterials.2017.10.011 · DOI
  6. Chakos, 2017, Long term outcomes of transcatheter aortic valve implantation (TAVI): a systematic review of 5-year survival and beyond, Ann Cardiothorac Surg, 6, 432, 10.21037/acs.2017.09.10 · DOI
  7. Terre, 2017, Pros and cons of transcatheter aortic valve implantation (TAVI), Ann Cardiothorac Surg, 6, 444, 10.21037/acs.2017.09.15 · DOI
  8. Zhao, 2003, Blood compatible aspects of DNA-modified polysulfone membrane—protein adsorption and platelet adhesion, Biomaterials, 24, 3747, 10.1016/S0142-9612(03)00250-3 · DOI
  9. GI, 1983, Calcification of Glutaraldehyde-Preserved Porcine and Bovine Xenograft Valves in Young-Children, Ann. Thorac. Surg., 35, 5
  10. Lopez-Moya, 2018, Optimizing glutaraldehyde-fixed tissue heart valves with chondroitin sulfate hydrogel for endothelialization and shielding against deterioration, Biomacromolecules, 19, 1234, 10.1021/acs.biomac.8b00077 · DOI
  11. Schmidt, 2000, Acellular vascular tissues: natural biomaterials for tissue repair and tissue engineering, Biomaterials, 21, 2215, 10.1016/S0142-9612(00)00148-4 · DOI · Paper page
  12. Zhang, 2018, Reducing immunoreactivity of porcine bioprosthetic heart valves by genetically-deleting three major glycan antigens, GGTA1/β4GalNT2/CMAH, Acta Biomater, 72, 196, 10.1016/j.actbio.2018.03.055 · DOI
  13. Stein, 1988, Leukocytes, platelets, and surface microstructure of spontaneously degenerated porcine bioprosthetic valves, J, Card. Surg., 3, 253, 10.1111/j.1540-8191.1988.tb00246.x · DOI
  14. Manji, 2014, Bioprosthetic heart valves of the future, Xenotransplantation, 21, 1, 10.1111/xen.12080 · DOI
  15. Schoen, 2005, Calcification of tissue heart valve substitutes: progress toward understanding and prevention, Ann Thorac Surg, 79, 1072, 10.1016/j.athoracsur.2004.06.033 · DOI
  16. Zhai, 2010, Quercetin-crosslinked porcine heart valve matrix: mechanical properties, stability, anticalcification and cytocompatibility, Acta Biomater, 6, 389, 10.1016/j.actbio.2009.07.035 · DOI
  17. Simionescu, 2004, Prevention of calcification in bioprosthetic heart valves: challenges and perspectives, Expert opinion on biological therapy, 4, 1971, 10.1517/14712598.4.12.1971 · DOI
  18. Cao, 2008, EDC/NHS-crosslinked type II collagen-chondroitin sulfate scaffold: characterization and in vitro evaluation, J, Mater. Sci. Mater. Med., 19, 567, 10.1007/s10856-007-3281-5 · DOI
  19. Zeeman, 1999, Successive epoxy and carbodiimide cross-linking of dermal sheep collagen, Biomaterials, 20, 921, 10.1016/S0142-9612(98)00242-7 · DOI
  20. Everaerts, 2004, Reduced calcification of bioprostheses, cross-linked via an improved carbodiimide based method, Biomaterials, 25, 5523, 10.1016/j.biomaterials.2003.12.054 · DOI
  21. TOUYAMA, 1994, Studies on the blue pigments produced from genipin and methylamine. I. Structures of the brownish-red pigments, intermediates leading to the blue pigments, Chem. Pharm. Bull., 42, 668, 10.1248/cpb.42.668 · DOI
  22. Sung, 1999, Crosslinking characteristics and mechanical properties of a bovine pericardium fixed with a naturally occurring crosslinking agent, J, Biomed. Mater. Res., 47, 116, 10.1002/(SICI)1097-4636(199911)47:2<116::AID-JBM2>3.0.CO;2-J · DOI
  23. Ju, 2008, A novel porous collagen scaffold around an implantable biosensor for improving biocompatibility. I. In vitro/in vivo stability of the scaffold and in vitro sensitivity of the glucose sensor with scaffold, Journal Of Biomedical Materials Research Part A, 87A, 136, 10.1002/jbm.a.31756 · DOI
  24. Kristensen, 2006, Heparin coating durability on artificial heart valves studied by XPS and antithrombin binding capacity, Colloids and Surfaces B: Biointerfaces, 49, 1, 10.1016/j.colsurfb.2006.02.007 · DOI
  25. Levy, 2009, Evaluation of drug‐eluting stents' coating durability—Clinical and regulatory implications, Journal of Biomedical Materials Research Part B: Applied Biomaterials, 91, 441, 10.1002/jbm.b.31420 · DOI
  26. Ayyaru, 2017, Application of sulfonic acid group functionalized graphene oxide to improve hydrophilicity, permeability, and antifouling of PVDF nanocomposite ultrafiltration membranes, J, Membr. Sci., 525, 210, 10.1016/j.memsci.2016.10.048 · DOI
  27. Shi, 2016, Hydrophilic sulfonic acid-functionalized micro-bead silica for dehydration of sorbitol to isosorbide, RSC advances, 6, 13514, 10.1039/C5RA27510E · DOI
  28. Hoshi, 2013, The blood and vascular cell compatibility of heparin-modified ePTFE vascular grafts, Biomaterials, 34, 30, 10.1016/j.biomaterials.2012.09.046 · DOI
  29. Boström, 2011, The regulation of valvular and vascular sclerosis by osteogenic morphogens, Circulation research, 109, 564, 10.1161/CIRCRESAHA.110.234278 · DOI
  30. Kim, 2011, The effect of immobilization of heparin and bone morphogenic protein-2 (BMP-2) to titanium surfaces on inflammation and osteoblast function, Biomaterials, 32, 366, 10.1016/j.biomaterials.2010.09.008 · DOI
  31. Gong, 2010, Heparin-immobilized polymers as non-inflammatory and non-thrombogenic coating materials for arsenic trioxide eluting stents, Acta biomaterialia, 6, 534, 10.1016/j.actbio.2009.07.013 · DOI
  32. Guo, 2018, Radical polymerization-crosslinking method for improving extracellular matrix stability in bioprosthetic heart valves with reduced potential for calcification and inflammatory response, Acta Biomater, 82, 44, 10.1016/j.actbio.2018.10.017 · DOI
  33. Liao, 2008, Effects of decellularization on the mechanical and structural properties of the porcine aortic valve leaflet, Biomaterials, 29, 1065, 10.1016/j.biomaterials.2007.11.007 · DOI
  34. Guo, 2018, Radical polymerization-crosslinking method for improving extracellular matrix stability in bioprosthetic heart valves with reduced potential for calcification and inflammatory response, Acta Biomater, 37
  35. Lien, 2009, Effect of pore size on ECM secretion and cell growth in gelatin scaffold for articular cartilage tissue engineering, Acta Biomater, 5, 670, 10.1016/j.actbio.2008.09.020 · DOI
  36. Lopez-Moya, 2018, Optimizing Glutaraldehyde-Fixed Tissue Heart Valves with Chondroitin Sulfate Hydrogel for Endothelialization and Shielding against Deterioration, Biomacromolecules, 19, 1234, 10.1021/acs.biomac.8b00077 · DOI
  37. Waterston, 2002, Initial sequencing and comparative analysis of the mouse genome, Nature, 420, 520, 10.1038/nature01262 · DOI · Paper page
  38. Zelenay, 1984, Adsorption of trifluoromethane sulfonic acid on Pt by FTIR and radiotracer methods, J, Electrochem. Soc., 131, 2464, 10.1149/1.2115323 · DOI
  39. Belfer, 1998, Surface modification of commercial polyamide reverse osmosis membranes by radical grafting: An ATR‐FTIR study, Acta Polym, 49, 574, 10.1002/(SICI)1521-4044(199810)49:10/11<574::AID-APOL574>3.0.CO;2-0 · DOI
  40. Dewanjee, 1986, Effect of diphosphonate binding to collagen upon inhibition of calcification and promotion of spontaneous endothelial cell coverage on tissue valve prostheses, ASAIO Trans, 32, 24
  41. Ogle, 2003, Calcification resistance with aluminum-ethanol treated porcine aortic valve bioprostheses in juvenile sheep, The Annals of thoracic surgery, 75, 1267, 10.1016/S0003-4975(02)04489-2 · DOI
  42. Sung, 1996, Cross-linking characteristics of biological tissues fixed with monofunctional or multifunctional epoxy compounds, Biomaterials, 17, 1405, 10.1016/0142-9612(96)87282-6 · DOI
  43. Michelson, 1994, REVERSIBLE INHIBITION OF HUMAN PLATELET ACTIVATION BY HYPOTHERMIA IN-VIVO AND IN-VITRO, Thromb. Haemost, 71, 633, 10.1055/s-0038-1642495 · DOI
  44. Nie, 2015, Nanofibrous heparin and heparin-mimicking multilayers as highly effective endothelialization and antithrombogenic coatings, Biomacromolecules, 16, 992, 10.1021/bm501882b · DOI
  45. Dangas, 2016, Prosthetic Heart Valve Thrombosis, J. Am. Coll. Cardiol, 68, 2670, 10.1016/j.jacc.2016.09.958 · DOI
  46. Zoghbi, 2009, J. Am. Soc. Echocardiogr., 22, 975, 10.1016/j.echo.2009.07.013 · DOI
  47. Deviri, 1991, Obstruction of mechanical heart valve prostheses: Clinical aspects and surgical management, J, Am. Coll. Cardiol., 17, 646, 10.1016/S0735-1097(10)80178-0 · DOI
  48. Werner, 2007, Current strategies towards hemocompatible coatings, J. Mater. Chem., 17, 3376, 10.1039/b703416b · DOI
  49. M.B. Gorbet, M.V. Sefton, Review: Biomaterial-associated thrombosis: roles of coagulation factors, complement, platelets and leukocytes, (2004) 219-241. · DOI
  50. Chang, 2011, Zwitterionic sulfobetaine-grafted poly(vinylidene fluoride) membrane with highly effective blood compatibility via atmospheric plasma-induced surface copolymerization, ACS Appl Mater Interfaces, 3, 1228, 10.1021/am200055k · DOI
  51. Seo, 2008, Surface tethering of phosphorylcholine groups onto poly (dimethylsiloxane) through swelling–deswelling methods with phospholipids moiety containing ABA-type block copolymers, Biomaterials, 29, 1367, 10.1016/j.biomaterials.2007.11.039 · DOI
  52. Zhu, 2015, Surface zwitterionization of hemocompatible poly(lactic acid) membranes for hemodiafiltration, J, Membr. Sci., 475, 469, 10.1016/j.memsci.2014.11.004 · DOI
  53. Fischlein, 1994, Endothelialization of cardiac valve bioprostheses, The International journal of artificial organs, 17, 345, 10.1177/039139889401700606 · DOI
  54. Liao, 1993, Spontaneous host endothelial growth on bioprosthetic valves and its relation to calcification, European journal of cardio-thoracic surgery: official journal of the European Association for Cardio-thoracic Surgery, 7, 591, 10.1016/1010-7940(93)90245-7 · DOI
  55. Kipshidze, 2004, Role of the endothelium in modulating neointimal formation: vasculoprotective approaches to attenuate restenosis after percutaneous coronary interventions, J, Am. Coll. Cardiol., 44, 733
  56. Bostroem, 2011, The Regulation of Valvular and Vascular Sclerosis by Osteogenic Morphogens, Circulation Research, 109, 564, 10.1161/CIRCRESAHA.110.234278 · DOI
  57. Eybl, 1989, Toxic effects of aldehydes released from fixed pericardium on bovine aortic endothelial cells, J, Biomed. Mater. Res., 23, 1355, 10.1002/jbm.820231111 · DOI
  58. Allen, 2010, Toward engineering a human neoendothelium with circulating progenitor cells, Stem Cells, 28, 318, 10.1002/stem.275 · DOI
  59. Motlagh, 2007, Hemocompatibility evaluation of poly (diol citrate) in vitro for vascular tissue engineering, Journal of Biomedical Materials Research Part A: An Official Journal of The Society for Biomaterials, The Japanese Society for Biomaterials, and The Australian Society for Biomaterials and the Korean Society for Biomaterials, 82, 907, 10.1002/jbm.a.31211 · DOI
  60. Anderson, 2002, A novel phenotype for an activated macrophage: the type 2 activated macrophage, J, Leukocyte Biol, 72, 101, 10.1189/jlb.72.1.101 · DOI
  61. Gordon, 2005, Monocyte and macrophage heterogeneity, Nature reviews immunology, 5, 953, 10.1038/nri1733 · DOI · Paper page
  62. Zhang, 2013, Zwitterionic hydrogels implanted in mice resist the foreign-body reaction, Nat. Biotechnol., 31, 553, 10.1038/nbt.2580 · DOI · Paper page
  63. Martinez, 2014, The M1 and M2 paradigm of macrophage activation: time for reassessment, F1000prime reports, 6
  64. Badylak, 2008, Immune response to biologic scaffold materials, Semin. Immunol., 20, 109, 10.1016/j.smim.2007.11.003 · DOI · Paper page
  65. Ardans, 2002, Oxidized low‐density and high‐density lipoproteins regulate the production of matrix metalloproteinase‐1 and‐9 by activated monocytes, J, Leukocyte Biol, 71, 1012, 10.1189/jlb.71.6.1012 · DOI
  66. Mills, 2000, M-1/M-2 macrophages and the Th1/Th2 paradigm, The Journal of Immunology, 164, 6166, 10.4049/jimmunol.164.12.6166 · DOI · Paper page
  67. Ludwig, 2009, Therapeutic use of heparin beyond anticoagulation, Curr. Drug Disc. Technol., 6, 281, 10.2174/157016309789869001 · DOI
  68. Young, 2008, The anti-inflammatory effects of heparin and related compounds, Thromb. Res., 122, 743, 10.1016/j.thromres.2006.10.026 · DOI
  69. Mousavi, 2015, Anti-Inflammatory Effects of Heparin and Its Derivatives: A Systematic Review, Adv. Pharmacol. Sci., 2015
  70. Li, 2018, Mitigation of Inflammatory Immune Responses with Hydrophilic Nanoparticles, Angew. Chem. Int. Ed. Engl., 57, 4527, 10.1002/anie.201710068 · DOI
  71. Schoen, 2005, Calcification of tissue heart valve substitutes: progress toward understanding and prevention, The Annals of thoracic surgery, 79, 1072, 10.1016/j.athoracsur.2004.06.033 · DOI
  72. Gong, 1991, Aldehyde tanning: The villain in bioprosthetic calcification, Eur. J. Cardiothorac. Surg., 5, 288, 10.1016/1010-7940(91)90037-K · DOI
  73. Hénaut, 2016, Targeting local vascular and systemic consequences of inflammation on vascular and cardiac valve calcification, Expert Opin. Ther. Targets, 20, 89, 10.1517/14728222.2015.1081685 · DOI
  74. Goldbarg, 2007, Insights into degenerative aortic valve disease, J. Am. Coll. Cardiol., 50, 1205, 10.1016/j.jacc.2007.06.024 · DOI
  75. Kaden, 2005, Inflammatory regulation of extracellular matrix remodeling in calcific aortic valve stenosis, Cardiovasc. Pathol., 14, 80, 10.1016/j.carpath.2005.01.002 · DOI

Cited by

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Metadata

Authors
Guo, G., Jin, L., Wu, B., He, H., Yang, F., Xu, L., Lei, Y., & Wang, Y.
Affiliations
Sichuan University (CN)
Corresponding author
Wang, Yunbing
Venue
Acta Biomaterialia
Publisher
Elsevier BV
Published
2021-01
Volume
119
Pages
89-100
ISSN
1742-7061 (ISSN-L)
OpenAlex
W3094421007
Cited by
45
References
6
Citations by year
2026: 2 · 2025: 11 · 2024: 6 · 2023: 9 · 2022: 9 · 2021: 8
FWCI
5.95
Type
journal article
Language
en
Open access
closed
Locations
  • Acta Biomaterialia (publishedVersion)
  • PubMed (publishedVersion)
Topics
  • Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
  • Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac Valve Diseases and Treatments
  • Physical Sciences › Materials Science › Biomaterials › Hydrogels: synthesis, properties, applications
Keywords
bioprosthetic heart valves, extracellular matrix, in situ polymerization, glutaraldehyde crosslinking, endothelialization, human umbilical vein endothelial cells, valve calcification, immune response, biocompatibility
MeSH terms
Animals, Biocompatible Materials, Bioprosthesis, Extracellular Matrix, Heart Valve Prosthesis, Heart Valves, Humans, Inflammation, Rats, Sprague-Dawley, Endothelial Cells, Mice, Rats

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