BIOPROSTHETIC VALVE IMPLANTATION AS TYPE OF TRANSPLANTATION: IMMUNOLOGICAL CONSEQUENCES OF NEW CONCEPT
https://doi.org/10.17802/2306-1278-2023-12-4S-196-205
Abstract
Highlights
- Immune processes and mechanisms underlying bioprosthetic heart valve degeneration and rejection of allografts and xenografts are similar.
- Manufacturers and surgeons can implement effective approaches to prevent immune rejection in the process of production and implantation of prosthetic heart valves in order to delay the process of structural valve degeneration.
Abstract
Bioprosthetic heart valves (BHV) are characterized by low thrombogenicity, thus circumventing the need for long‐term anticoagulation. However, BHV lifespan is limited to 10–15 years because its tissue components are subject to degeneration. Recent research data indicate that immune responses forming the basis of humoral and cellular rejection of allografts and xenografts play a major role in the development of structural valve degeneration (SVD). This review summarizes up-to-date data on immune processes involved in SVD pathogenesis. Moreover, the latest achievements in the development of strategies to reduce the immunogenicity of BHV, such as data on immune compatibility of allogeneic material and the process of deriving low immunogenic biomaterial from genetically modified animals, decellularization of BHV, and the ways of slowing the process of degeneration are analyzed.
About the Authors
Alexander E. KostyuninRussian Federation
PhD, Researcher at the Laboratory of New Biomaterials, Department of Experimental Medicine, Federal State Budgetary Institution “Research Institute of Complex Issues of Cardiovascular Diseases”, Kemerovo, Russian Federation
Tatiana V. Glushkova
Russian Federation
PhD, Senior Researcher at the Laboratory of New Biomaterials, Department of Experimental Medicine, Federal State Budgetary Institution “Research Institute of Complex Issues of Cardiovascular Diseases”, Kemerovo, Russian Federation
Evgeny A. Ovcharenko
Russian Federation
PhD, Head of the Laboratory of New Biomaterials, Department of Experimental Medicine, Federal State Budgetary Institution “Research Institute of Complex Issues of Cardiovascular Diseases”, Kemerovo, Russian Federation
References
1. Otto C.M., Nishimura R.A., Bonow R.O., Carabello B.A., Erwin J.P. 3rd, Gentile F. et al. 2020 ACC/AHA Guideline for the management of patients with valvular heart disease: a report of the American College of Cardiology/American Heart Association Joint Committee on Clinical Practice Guidelines. Circulation. 2021; 143(5):e72-e227. doi:10.1161/CIR.0000000000000923
2. Bockeria L.A., Milievskaya E.B., Kuzdoeva Z.F., Pryanishnikova V.V. Cardiovascular surgery – 2017. Diseases and congenital anomalies of the circulatory system. Moscow; 2018. 252p. (In Russian) ISBN:978-5-7982-0389-5
3. Bax J.J., Delgado V. Bioprosthetic heart valves, thrombosis, anticoagulation, and imaging surveillance. JACC Cardiovasc. Interv. 2017; 10(4): 388-390. doi:10.1016/j.jcin.2017.01.017
4. Manji R.A., Lee W., Cooper D.K.C. Xenograft bioprosthetic heart valves: past, present and future. Int. J. Surg. 2015; 23(Pt B):280-284. doi:10.1016/j.ijsu.2015.07.009
5. Dvir D., Bourguignon T., Otto C.M., Hahn R.T., Rosenhek R., Webb J.G. et al. Standardized definition of structural valve degeneration for surgical and transcatheter bioprosthetic aortic valves. Circulation. 2018; 137(4):388-399. doi:10.1161/CIRCULATIONAHA.117.030729
6. Barbarash L.S., Zhuravleva I.Yu. Bioprosthetic heart valve evolution: two decades of advances and challenges. Complex Issues of Cardiovascular Diseases. 2012; 1:4-11. (in Russian) doi:10.17802/2306-1278-2012-1-4-11
7. Schoen F.J., Levy R.J. Calcification of tissue heart valve substitutes: progress toward understanding and prevention. Ann. Thorac. Surg. 2005; 79(3):1072-1080. doi:10.1016/j.athoracsur.2004.06.033
8. Rodriguez-Gabella T., Voisine P., Puri R., Pibarot P., Rodés-Cabau J. Aortic bioprosthetic valve durability: incidence, mechanisms, predictors, and management of surgical and transcatheter valve degeneration. J. Am. Coll. Cardiol. 2017; 70(8):1013-1028. doi:10.1016/j.jacc.2017.07.715
9. Lisy M., Kalender G., Schenke-Layland K., Brockbank K.G., Biermann A., Stock U.A. Allograft heart valves: current aspects and future applications. Biopreserv. Biobank. 2017; 15(2):148-157. doi:10.1089/bio.2016.0070
10. Fiala R., Kochova P., Kubíkova T., Cimrman R., Tonar Z., Spatenka J. et al. Mechanical and structural properties of human aortic and pulmonary allografts do not deteriorate in the first 10 years of cryopreservation and storage in nitrogen. Cell Tissue Bank. 2019; 20(2):221-241. doi:10.1007/s10561-019-09762-x
11. Mazine A., El-Hamamsy I., Verma S., Peterson M.D., Bonow R.O., Yacoub M.H. et al. Ross procedure in adults for cardiologists and cardiac surgeons: JACC state-of-the-art review. J. Am. Coll. Cardiol. 2018; 72(22):2761-2777. doi:10.1016/j.jacc.2018.08.2200
12. Naso F., Gandaglia A., Bottio T., Tarzia V., Nottle M.B., d'Apice A.J. et al. First quantification of alpha-Gal epitope in current glutaraldehyde-fixed heart valve bioprostheses. Xenotransplantation. 2013; 20(4):252-261. doi:10.1111/xen.12044
13. Reuven E.M., Leviatan Ben-Arye S., Marshanski T., Breimer M.E., Yu H., Fellah-Hebia I. et al. Characterization of immunogenic Neu5Gc in bioprosthetic heart valves. Xenotransplantation. 2016; 23(5):381-92. doi:10.1111/xen.12260
14. Barone A., Benktander J., Whiddon C., Jin C., Galli C., Teneberg S. et al. Glycosphingolipids of porcine, bovine, and equine pericardia as potential immune targets in bioprosthetic heart valve grafts. Xenotransplantation. 2018; 25(5):e12406. doi:10.1111/xen.12406
15. Galili U. Anti-Gal: an abundant human natural antibody of multiple pathogeneses and clinical benefits. Immunology. 2013; 140(1):1-11. doi:10.1111/imm.12110
16. Taylor R.E., Gregg C.J., Padler-Karavani V., Ghaderi D., Yu H., Huang S. et al. Novel mechanism for the generation of human xeno-autoantibodies against the nonhuman sialic acid N-glycolylneuraminic acid. J. Exp. Med. 2010; 207(8):1637-1646. doi:10.1084/jem.20100575
17. Lu T., Yang B., Wang R., Qin C. Xenotransplantation: current status in preclinical research. Front. Immunol. 2020; 10:3060. doi:10.3389/fimmu.2019.03060
18. Böer U., Buettner F.F.R., Schridde A., Klingenberg M., Sarikouch S., Haverich A. et al Antibody formation towards porcine tissue in patients implanted with crosslinked heart valves is directed to antigenic tissue proteins and αGal epitopes and is reduced in healthy vegetarian subjects. Xenotransplantation. 2017; 24(2). doi:10.1111/xen.12288
19. Gates K.V., Xing Q., Griffiths L.G. Immunoproteomic identification of noncarbohydrate antigens eliciting graft-specific adaptive immune responses in patients with bovine pericardial bioprosthetic heart valves. Proteomics Clin. Appl. 2019; 13(4):e1800129. doi:10.1002/prca.201800129
20. Manji R.A., Ekser B., Menkis A.H., Cooper D.K.C. Bioprosthetic heart valves of the future. Xenotransplantation. 2014; 21(1):1-10. doi:10.1111/xen.12080
21. Nair V., Law K.B., Li A.Y., Phillips K.R., David T.E., Butany J. Characterizing the inflammatory reaction in explanted Medtronic Freestyle stentless porcine aortic bioprosthesis over a 6-year period. Cardiovasc. Pathol. 2012; 21(3):158-168. doi:10.1016/j.carpath.2011.05.003
22. Sakaue T., Nakaoka H., Shikata F., Aono J., Kurata M., Uetani T. et al. Biochemical and histological evidence of deteriorated bioprosthetic valve leaflets: the accumulation of fibrinogen and plasminogen. Biol. Open. 2018; 7(8):pii:bio034009. doi:10.1242/bio.034009
23. Shetty R., Pibarot P., Audet A., Janvier R., Dagenais F., Perron J. et al. Lipid-mediated inflammation and degeneration of bioprosthetic heart valves. Eur. J. Clin. Invest. 2009; 39(6):471-480. doi:10.1111/j.1365-2362.2009.02132.x
24. Simionescu A., Simionescu D.T., Deac R.F. Matrix metalloproteinases in the pathology of natural and bioprosthetic cardiac valves. Cardiovasc. Pathol. 1996; 5(6):323-332.
25. Fournier P.E., Thuny F., Grisoli D., Lepidi H., Vitte J., Casalta J.P. et al. A deadly aversion to pork. Lancet. 2011; 377(9776):1542. doi:10.1016/S0140-6736(11)60021-4
26. Hoekstra F., Knoop C., Vaessen L., Wassenaar C., Jutte N., Bos E. et al. Donor-specific cellular immune response against human cardiac valve allografts. J. Thorac. Cardiovasc. Surg. 1996; 112(2):281-286. doi:10.1016/S0022-5223(96)70250-7
27. Kneib C., von Glehn C.Q., Costa F.D., Costa M.T., Susin M.F. Evaluation of humoral immune response to donor HLA after implantation of cellularized versus decellularized human heart valve allografts. Tissue Antigens. 2012; 80(2):165-174. doi:10.1111/j.1399-0039.2012.01885.x
28. Dignan R., O'Brien M., Hogan P., Passage J., Stephens F., Thornton A. et al. Influence of HLA matching and associated factors on aortic valve homograft function. J. Heart Valve Dis. 2000; 9(4):504-511.
29. Saleem N., Das R., Tambur A.R. Molecular histocompatibility beyond tears: the next generation version. Hum Immunol. 2022; 83(3):233-240. doi:10.1016/j.humimm.2021.12.005
30. Lee W., Long C., Ramsoondar J., Ayares D., Cooper D.K., Manji R.A. et al. Human antibody recognition of xenogeneic antigens (NeuGc and Gal) on porcine heart valves: could genetically modified pig heart valves reduce structural valve deterioration? Xenotransplantation. 2016; 23(5):370-380. doi:10.1111/xen.12254
31. Perota A., Lagutina I., Duchi R., Zanfrini E., Lazzari G., Judor J.P. et al. Generation of cattle knockout for galactose-α1,3-galactose and N-glycolylneuraminic acid antigens. Xenotransplantation. 2019; 26(5):e12524. doi:10.1111/xen.12524
32. Adams A.B., Kim S.C., Martens G.R., Ladowski J.M., Estrada J.L., Reyes L.M. et al. Xenoantigen deletion and chemical immunosuppression can prolong renal xenograft survival. Ann Surg. 2018; 268(4):564-573. doi:10.1097/SLA.0000000000002977
33. Längin M., Mayr T., Reichart B., Michel S., Buchholz S., Guethoff S. et al. Consistent success in life-supporting porcine cardiac xenotransplantation. Nature. 2018; 564(7736):430-433. doi:10.1038/s41586-018-0765-z
34. Kuwaki K., Tseng Y.L., Dor F.J., Shimizu A., Houser S.L., Sanderson T.M. et al. Heart transplantation in baboons using alpha1,3-galactosyltransferase gene-knockout pigs as donors: initial experience. Nat. Med. 2005; 11(1):29-31. doi:10.1038/nm1171
35. Reardon S. First pig-to-human heart transplant: what can scientists learn? Nature. 2022; 601(7893):305-306. doi:10.1038/d41586-022-00111-9
36. Zhang R., Wang Y., Chen L., Wang R., Li C., Li X. et al. Reducing immunoreactivity of porcine bioprosthetic heart valves by genetically-deleting three major glycan antigens, GGTA1/β4GalNT2/CMAH. Acta Biomater. 2018; 72:196-205. doi:10.1016/j.actbio.2018.03.055
37. McGregor C.G., Kogelberg H., Vlasin M., Byrne G.W. Gal-knockout bioprostheses exhibit less immune stimulation compared to standard biological heart valves. J. Heart Valve Dis. 2013; 22(3):383-390.
38. McGregor C., Byrne G., Rahmani B., Chisari E., Kyriakopoulou K., Burriesci G. Physical equivalency of wild type and galactose α 1,3 galactose free porcine pericardium; a new source material for bioprosthetic heart valves. Acta Biomater. 2016; 41:204-209. doi:10.1016/j.actbio.2016.06.007
39. Rahmani B., McGregor C., Byrne G., Burriesci G. A durable porcine pericardial surgical bioprosthetic heart valve: a proof of concept. J. Cardiovasc. Transl. Res. 2019; 12(4):331-337. doi:10.1007/s12265-019-09868-3
40. Crapo P.M., Gilbert T.W., Badylak S.F. An overview of tissue and whole organ decellularization processes. Biomaterials. 2011; 32(12):3233-3243. doi:10.1016/j.biomaterials.2011.01.057
41. Kim M.S., Lim H.G., Kim Y.J. Calcification of decellularized and alpha-galactosidase-treated bovine pericardial tissue in an alpha-Gal knock-out mouse implantation model: comparison with primate pericardial tissue. Eur. J. Cardiothorac. Surg. 2016; 49(3):894-900. doi:10.1093/ejcts/ezv189
42. Helder M.R.K., Stoyles N.J., Tefft B.J., Hennessy R.S., Hennessy R.R.C., Dyer R. et al. Xenoantigenicity of porcine decellularized valves. J. Cardiothorac. Surg. 2017; 12(1):56. doi:10.1186/s13019-017-0621-5
43. Heuschkel M.A., Leitolis A., Roderjan J.G., Suss P.H., Luzia C.A.O., da Costa F.D.A. et al. In vitro evaluation of bovine pericardium after a soft decellularization approach for use in tissue engineering. Xenotransplantation. 2019; 26(2):e12464. doi:10.1111/xen.12464
44. Wu L.C., Kuo Y.J., Sun F.W., Chen C.H., Chiang C.J., Weng P.W. et al. Optimized decellularization protocol including α-Gal epitope reduction for fabrication of an acellular porcine annulus fibrosus scaffold. Cell Tissue Bank. 2017; 18(3):383-396. doi:10.1007/s10561-017-9619-4
45. Bloch O., Golde P., Dohmen P.M., Posner S., Konertz W., Erdbrügger W. Immune response in patients receiving a bioprosthetic heart valve: lack of response with decellularized valves. Tissue Eng. Part A. 2011; 17(19-20):2399-405. doi:10.1089/ten.TEA.2011.0046
46. Bibevski S., Ruzmetov M., Fortuna R.S., Turrentine M.W., Brown J.W., Ohye R.G. Performance of SynerGraft decellularized pulmonary allografts compared with standard cryopreserved allografts: results from multiinstitutional data. Ann. Thorac. Surg. 2017; 103(3):869-874. doi:10.1016/j.athoracsur.2016.07.068
47. Sarikouch S., Horke A., Tudorache I., Beerbaum P., Westhoff-Bleck M., Boethig D. et al. Decellularized fresh homografts for pulmonary valve replacement: a decade of clinical experience. Eur. J. Cardiothorac. Surg. 2016; 50(2):281-290. doi:10.1093/ejcts/ezw050
48. Manji R.A., Zhu L.F., Nijjar N.K., Rayner D.C., Korbutt G.S., Churchill T.A. et al. Glutaraldehyde-fixed bioprosthetic heart valve conduits calcify and fail from xenograft rejection. Circulation. 2006; 114(4):318-327. doi:10.1161/CIRCULATIONAHA.105.549311
49. Eishi K., Ishibashi-Ueda H., Nakano K., Kosakai Y., Sasako Y., Kobayashi J. et al. Calcific degeneration of bioprosthetic aortic valves in patients receiving steroid therapy. J. Heart Valve Dis. 1996; 5(6):668-672.
Supplementary files
Review
For citations:
Kostyunin A.E., Glushkova T.V., Ovcharenko E.A. BIOPROSTHETIC VALVE IMPLANTATION AS TYPE OF TRANSPLANTATION: IMMUNOLOGICAL CONSEQUENCES OF NEW CONCEPT. Complex Issues of Cardiovascular Diseases. 2023;12(4S):196-205. (In Russ.) https://doi.org/10.17802/2306-1278-2023-12-4S-196-205