Application of antibiotics in the sterilization of homogeneic heart valves
Artur Turek 1 , Justyna Wilińska 1 , Aleksandra Borecka 2 , Lucyna Pawlus-Łachecka 3Abstract
A significant deficit in the availability of human tissues has not resulted in less general interest in homogeneous heart valves. The application of homografts still remains the optimal solution in the surgical treatment of congenital and acquired defects. Obtaining the optimal properties of these valves is followed by processing, including sterilization. This method provides sterility with rewarding cell viability and maintenance of the tissues’ native features. The prepared material possesses appropriate properties at the level of structure and surface, which results in correct functioning in vivo. During the past several decades, sterilization conditions and the compositions of antibiotic mixtures have changed significantly. In this period, significant progress in the development of this method was achieved; however, in the last few years, various flaws in antibiotic sterilization of homografts have been revealed. The release of the antibiotic during microbiological tests of tissue evaluated for implantation or the possibility of side effects as a result of antibiotic release after implantation remain the most important issues here. In this work we characterized the main antibiotic mixtures that are currently in use.
References
- 1. Aguirregoicoa V., Kearney J.N., Davies G.A., Gowland G.: Effects of antifungals on the viability of heart valve cusp derived fibroblasts. Cardiovasc. Res., 1989; 23: 1058-1061
Google Scholar - 2. Al-Janabi N., Gonzalez-Lavin L., Neirotti R., Ross D.N.: Viability of fresh aortic valve homografts: a quantitative assessment. Thorax, 1972; 27: 83-86
Google Scholar - 3. Angell W.W., Oury J.H., Duran C.G., Infantes-Alcon C.: Twenty-year comparison of the human allograft and porcine xenograft. Ann. Thorac. Surg., 1989; 48: S89-S90
Google Scholar - 4. Barratt-Boyes B.G., Roche A.H.: A review of aortic valve homografts over a six and one-half year period. Ann. Surg., 1969; 170: 483-492
Google Scholar - 5. Barratt-Boyes B.G., Roche A.H., Brandt P.W., Smith J.C., Lowe J.B.: Aortic homograft valve replacement. A long-term follow-up of an initial series of 101 patients. Circulation, 1969; 40: 763-775
Google Scholar - 6. Barratt-Boyes B.G., Roche A.H., Whitlock R.M.: Six-year review of the results of freehand aortic valve replacement using an antibiotic sterilized homograft valve. Circulation, 1977; 55: 353-361
Google Scholar - 7. Beech P.M. Jr., Bowman F.O. Jr., Kaiser G.A., Malm J.R.: Frozen irradiated aortic valve homografts. Long-term evaluation. N. Y. State J. Med., 1973; 73: 651-654
Google Scholar - 8. Bellahsene A., Forsgren A.: Effect of doxycycline on immune response in mice. Infect. Immun., 1985; 48: 556-559
Google Scholar - 9. Bolooki H., Rubinson R.M., Prochazka J., Jude J.R.: A simple method of aortic homograft valve sterilization and preservation. J. Thorac. Cardiovasc. Surg., 1972; 63: 249-257
Google Scholar - 10. Breitenbach I., Wimmer-Greinecker G., Bockeria L.A., Sadowski J., Schmitz C., Kapelak B., Bartus K., Muratov R., Harringer W.: Sutureless aortic valve replacement with the Trilogy Aortic Valve System: multicenter experience. J. Thorac. Cardiovasc. Surg., 2010; 140: 878-884
Google Scholar - 11. Brockbank K.G., Dawson P.E.: Cytotoxicity of amphotericin B for fibroblasts in human heart valve leaflets. Cryobiology, 1993; 30: 19-24
Google Scholar - 12. Chitsaz S., Gundiah N., Blackshear C., Tegegn N., Yan K.S., Azadani A.N., Hope M., Tseng E.E.: Correlation of calcification on excised aortic valves by micro-computed tomography with severity of aortic stenosis. J. Heart Valve Dis., 2012; 21: 320-327
Google Scholar - 13. Christie G.W., Barratt-Boyes B.G.: Biaxial mechanical properties of explanted aortic allograft leaflets. Ann. Thorac. Surg., 1995; 60: S160-S164
Google Scholar - 14. Christie G.W., Barratt-Boyes B.G.: Identification of a failure mode of the antibiotic sterilized aortic allograft after 10 years: implication for their long-term survival. J. Card. Surg., 1991; 6: 462-467
Google Scholar - 15. Corrao S., Messina S., Pistone G., Calvo L., Scaglione R., Licata G.: Heart involvement in Rheumatoid Arthritis: Systematic review and meta-analysis. Int. J. Cardiol., 2013; 167: 2031-2038
Google Scholar - 16. da Costa F.D., da Costa M.B., da Costa I.A., Poffo R., Sardeto E.A., Matte E.: Clinical experience with heart valve homografts in Brazil. Artif. Organs, 2001; 25: 895-900
Google Scholar - 17. Dainese L., Biglioli P.: Human or animal homograft: could they have a future as a biological scaffold for engineered heart valves? J. Cardiovasc. Surg., 2010; 51: 449-456
Google Scholar - 18. de By T.M., Parker R., Delmo Walter E.M., Hetzer R.: Cardiovascular tissue banking in Europe. HSR Proc Intensive Care Cardiovasc Anesth., 2012; 4: 251-260
Google Scholar - 19. Delmo Walter E.M., de By T.M., Meyer R., Hetzer R.: The future of heart valve banking and of homografts: perspective from the Deutsches Herzzentrum Berlin. HSR Proc. Intensive Care Cardiovasc. Anesth., 2012; 4: 97-108
Google Scholar - 20. Díaz Rodríguez R., Van Hoeck B., Mujaj B., Ngakam R., Fan Y., Bogaerts K., Jashari R.: Bacteriology testing of cardiovascular tissues: comparison of transport solution versus tissue testing. Cell Tissue Bank, 2016; 17: 211-218
Google Scholar - 21. Doty J.R., Salazar J.D., Liddicoat J.R., Flores J.H., Doty D.B.: Aortic valve replacement with cryopreserved aortic allograft: ten-year experience. J. Thorac. Cardiovasc. Surg., 1998; 115: 371-379
Google Scholar - 22. Dziedzic-Gocławska A., Stachowicz W.: Sterylizacja radiacyjna przeszczepów tkankowych. W: Pawlicki G., Pałko T., Golnik N., Gwiazdowska B., Królicki L. (red. tomu). Fizyka medyczna. Tom 9. W: Nałęcz M. (red. serii). Biocybernetyka i inżynieria biomedyczna. 2000. Akademicka Oficyna Wydawnicza Exit, Warszawa 2002, 329-347
Google Scholar - 23. Easlund T.: Bacterial infection transmitted by human tissue allograft transplantation. Cell Tissue Bank, 2006, 7: 147-166
Google Scholar - 24. Englberger L., Carrel T.P., Doss M., Sadowski J., Bartus K., Eckstein F.F., Asch F.M., Martens S.:: Clinical performance of a sutureless aortic bioprosthesis: five-year results of the 3f Enable long-term follow-up study. J. Thorac. Cardiovasc. Surg., 2014; 148: 1681-1687
Google Scholar - 25. Fan Y.D., Van Hoeck B., Holovska V., Jashari R.: Evaluation of decontamination process of heart valve and artery tissues in European Homograft Bank (EHB): a retrospective study of 1, 055 cases. Cell Tissue Bank, 2012; 13: 297-304
Google Scholar - 26. Friess W.: Collagen – biomaterial for drug delivery. Eur. J. Pharm. Biopharm., 1998; 45: 113-136
Google Scholar - 27. Gall K.L., Smith S.E., Willmette C.A., O’Brien M.F.: Allograft heart valve viability and valve-processing variables. Ann. Thorac. Surg., 1998; 65: 1032-1038
Google Scholar - 28. Gall K., Smith S., Willmette C., Wong M., O’Brien M.: Allograft heart valve sterilisation: a six-year in-depth analysis of a twenty-five-year experience with low-dose antibiotics. J. Thorac. Cardiovasc. Surg., 1995; 110: 680-687
Google Scholar - 29. Gatto C., Giurgola L., D’Amato Tothova J.: A suitable and efficient procedure for the removal of decontaminating antibiotics from tissue allografts. Cell Tissue Bank, 2013; 14: 107-115
Google Scholar - 30. Gavin J.B., Barratt-Boyes B.G., Hitchcock G.C., Herdson P.B.: Histopathology of “fresh” human aortic valve allografts. Thorax, 1973; 28: 482-487
Google Scholar - 31. Gavin J.B., Herdson P.B., Monro J.L., Barratt-Boyes P.G.: Pathology of antibiotic-treated human heart valve allografts. Thorax, 1973; 28: 473-481
Google Scholar - 32. Gavin J.B., Monro J.L., Wall F.M., Chalcroft S.C.: Fine structural changes in the fibroblasts of canine heart valves prepared for grafting. Thorax, 1973; 28: 748-755
Google Scholar - 33. Germain M., Thibault L., Jacques A., Tremblay J., Bourgeois R.: Heart valve allograft decontamination with antibiotics: impact of the temperature of incubation on efficacy. Cell Tissue Bank, 2010; 11: 197-204
Google Scholar - 34. Goffin Y.A., Hoeck van B., Jashari R., Soots G., Kalmar P.: Banking of cryopreserved heart valves in Europe: assessment of a 10-year operation in the European Homograft Bank (EHB). J. Heart Valve Dis., 2000; 9: 207-214
Google Scholar - 35. Heng W.L., Seck T., Tay C.P., Chua A., Song C., Lim C.H., Lim Y.P.: Homograft banking in Singapore: two years of cardiovascular tissue banking in Southeast Asia. Cell. Tissue Bank, 2013; 14: 187-194
Google Scholar - 36. Hickey E., Langley S.M., Allemby-Smith O., Livesey S.A., Monro J.L.: Subcoronary allograft aortic valve replacement: parametric risk-hazard outcome analysis to a minimum of 20 years. Ann. Thorac. Surg., 2007; 84: 1564-1570
Google Scholar - 37. Hunt C.J., Caffrey E.A., Large S.R.: Factors affecting the yield of cardiac valve allografts from living unrelated donors. Eur. J. Cardiothorac. Surg., 1998; 13: 71-77
Google Scholar - 38. Jashari R., Faucon F., Hoeck B.V., Gelas S.D., Fan Y., Vandenbulcke S.: Determination of residual antibiotics in cryopreserved heart valve allografts. Transfus. Med. Hemother., 2011; 38: 379-386
Google Scholar - 39. Jashari R., Tabaku M., Van Hoeck B., Cochéz C., Callant M., Vanderkelen A.: Decontamination of heart valve and arterial allografts in the European Homograft Bank (EHB): comparison of two different antibiotic cocktails in low temperature conditions. Cell Tissue Bank, 2007; 8: 247-255
Google Scholar - 40. Jashari R., Van Hoeck B., Ngakam R., Goffin Y., Fan Y.: Banking of cryopreserved arterial allografts in Europe: 20 years of operation in the European Homograft Bank (EHB) in Brussels. Cell Tissue Bank, 2013; 14: 589-599
Google Scholar - 41. Jonas R.A., Ziemer G., Britton L., Armiger L.C.: Cryopreserved and fresh antibiotic-sterilized valved aortic homograft conduits in a long-term sheep model. Hemodynamic, angiographic, and histologic comparisons. J. Thorac. Cardiovasc. Surg., 1988; 96: 746-755
Google Scholar - 42. Kosuga T.: The effect of allogeneic or xenogeneic immune responses and preservation techniques on transplanted aortic valve grafts. Kurume Med. J., 2000; 47: 13-23
Google Scholar - 43. Lang S.J., Giordano M.S., Cardon-Cardo C., Summers B.D., Staiano-Coico L., Hajjar D.P.: Biochemical and cellular characterization of cardiac valve tissue after cryopreservation or antibiotic preservation. J. Thorac. Cardiovasc. Surg., 1994; 108: 63-67
Google Scholar - 44. Langley S.M., Livesey S.A., Tsang V.T., Barron D.J., Lamb R.K., Ross J.K., Monro J.L.: Long-term results of valve replacement using antibiotic-sterilised homografts in the aortic position. Eur. J. Cardiothorac. Surg., 1996; 10: 1097-1106
Google Scholar - 45. Langley S.M., McGuirk S.P., Chaudhry M.A., Livesey S.A., Ross J.K., Monro J.L.: Twenty-year follow-up of aortic valve replacement with antibiotic sterilized homografts in 200 patients. Semin. Thorac. Cardiovasc. Surg., 1999; 11: 28-34
Google Scholar - 46. Lee H.B., Khang G., Lee J.H.: Polymeric biomaterials. W: Park J.B., Bronzino J.D. (red.). Biomaterials. Principles and applications. CRC Press, Boca Raton 2003
Google Scholar - 47. Leeming J.P., Lovering A.M., Hunt C.J.: Residual antibiotics in allograft heart valve tissue samples following antibiotic disinfection. J. Hosp. Infect., 2005; 60: 231-234
Google Scholar - 48. Lockey E., Al-Janabi N., Gonzalez-Lavin L., Ross D.N.: A method of sterilizing and preserving fresh allograft heart valves. Thorax, 1972; 27: 398-400
Google Scholar - 49. Lockey E., Gonzalez-Lavin L., Ray I., Chen R.: Bacteraemia after open-heart surgery. Thorax, 1973; 28: 183-187
Google Scholar - 50. Longmore D.B., Lockey E., Ross D.N., Pickering B.N.: The preparation of aortic-valve homografts. Lancet, 1966; 2: 463-464
Google Scholar - 51. Manhas D.R., Mohri H., Merendino K.A.: Late results of beta-propiolactone sterilized aortic homograft valves. A study of fifty-one patients followed up five to seven and a half years. Am. J. Surg., 1973; 126: 255-262
Google Scholar - 52. McNally R.T., Brockbank K.G.: Issues surrounding the preservation of viable allograft heart valves. J. Med. Eng. Technol., 1992; 16: 34-38
Google Scholar - 53. Mestres C.A., Agusti E., Martinez A., Cabrer C., Manyalich M., Cartaña R., Pomar J.L.: Cardiovascular tissue banking in the non-cadaveric setting: ten-year experience of a university hospital-based bank with active organ donation program. J. Heart Valve Dis., 2000; 9: 523-529
Google Scholar - 54. Mirabet V., Carda C., Solves P., Novella-Maestre E., Carbonell-Uberos F., Caffarena J.M., Hornero F., Montero J.A., Roig R.J.: Long-term storage in liquid nitrogen does not affect cell viability in cardiac valve allografts. Cryobiology, 2008; 57: 113-121
Google Scholar - 55. O’Brien M.F.: Heterograft aortic valves for human use. Valve bank, techniques of measurement, and implantation. J. Thorac. Cardiovasc. Surg., 1967; 53: 392-397
Google Scholar - 56. O’Brien M.F., Harrocks S., Stafford E.G., Gardner M.A., Pohlner P.G., Tesar P.J., Stephens F.: The homograft aortic valve: 29-year, 99.3% follow up of 1.022 valve replacements. J. Heart Valve Dis., 2001; 10: 334-344
Google Scholar - 57. O’Brien M.F., McGiffin D.C., Stafford E.G., Gardner M.A., Pohlner P.G., McLachlan G.J., Gall K., Smith S., Murphy E.: Allograft aortic valve replacement: long term comparative clinical analysis of the viable cryopreserved and antibiotic 4˚C stored valves. J. Card. Surg., 1991; 6: 534-543
Google Scholar - 58. Paluch D.: Polimery naturalne. W: Kuś H. (red. tomu). Biomateriały. Tom 4. W: Nałęcz M. (red. serii). Problemy biocybernetyki i inżynierii biomedycznej. Wydawnictwa Komunikacji i Łączności, Warszawa 1990, 44-57
Google Scholar - 59. Pompilio G., Polvani G., Piccolo G., Guarino A., Nocco A., Innocente A., Porqueddu M., Dainese L., Veglia F., Sala A., Biglioli P.: Six-year monitoring of the donor-specific immune response to cryopreserved aortic allograft valves: implications with valve dysfunction. Ann. Thorac. Surg., 2004; 78: 557-563
Google Scholar - 60. Rendal Vázquez M.E., Román T.D., Cuesta M.G., Botta C.Z., Ibáñez J.S., Díaz S.P., Nuñez C.A.: Viability and histologic structure of porcine valves after cryopreservation. Ann. Thorac. Surg., 2004; 77: 186-190
Google Scholar - 61. Rennenberg R.J., Kessels A.G., Schurgers L.J., van Engelshoven J.M., de Leeuw P.W., Kroon A.A.: Vascular calcifications as a marker of increased cardiovascular risk: a meta-analysis. Vasc. Health Risk Manag., 2009; 5: 185-197
Google Scholar - 62. Rosenthal J.T., Shaw B.W. Jr, Hardesty R.L., Griffith B.P., Starzl T.E., Hakala T.R.: Principles of multiple organ procurement from cadaver donors. Ann. Surg., 1983; 198: 617-621
Google Scholar - 63. Sadowski J., Kapelak B., Bartus K., Podolec P., Rudzinski P., Myrdko T., Wierzbicki K., Dziatkowiak A.: Reoperation after fresh homograft replacement: 23 years’ experience with 655 patients. Eur. J. Cardiothorac. Surg., 2003; 23: 996-1000
Google Scholar - 64. Sadowski J., Kapelak B., Pfitzner R., Bartuś K.: Sutureless aortic valve bioprothesis ‘3F/ATS Enable’ – 4.5 years of a single-centre experience. Kardiol Pol., 2009; 67: 956-963
Google Scholar - 65. Schenke-Layland K., Madershahian N., Riemann I., Starcher B., Halbhuber K.J., König K., Stock U.A.: Impact of cryopreservation on extracellular matrix structures of heart valve leaflets. Ann. Thorac. Surg., 2006; 81: 918-926
Google Scholar - 66. Schenke-Layland K., Xie J., Heydarkhan-Hagvall S., Hamm-Alvarez S.F., Stock U.A., Brockbank K.G., MacLellan W.R.: Optimized preservation of extracellular matrix in cardiac tissues: implications for long-term graft durability. Ann. Thorac. Surg., 2007; 83: 1641-1650
Google Scholar - 67. Smith J.C.: The pathology of human aortic valve homografts. Thorax, 1967; 22: 114-138
Google Scholar - 68. Stock U.A., Degenkolbe I., Attmann T., Schenke-Layland K., Freitag S., Lutter G.: Prevention of device-related tissue damage during percutaneous deployment of tissue-engineered heart valves. J. Thorac. Cardiovasc. Surg., 2006; 131: 1323-1330
Google Scholar - 69. Strickett M.G., Barratt-Boyes B.G., MacCulloch D.: Disinfection of human heart valve allografts with antibiotics in low concentration. Pathology, 1983; 15: 457-462
Google Scholar - 70. Stuart P.M., Pan F., Yin X., Haskova Z., Plambeck S., Ferguson T.A.: Effect of metalloprotease inhibitors on corneal allograft survival. Invest. Ophthalmol. Vis. Sci., 2004; 45: 1169-1173
Google Scholar - 71. Suh H., Lee J.E., Park J.C., Han D.W., Yoon C.S., Park Y.H., Cho B.K.: Viability and enzymatic activity of cryopreserved porcine heart valve. Yonsei Med. J.: 1999; 40: 184-190
Google Scholar - 72. Sypniewski D., Bednarek I., Gałka S., Bryła A., Machnik G., Loch T., Sołtysik D., Błaszczyk D.: Expression of gelatinases A and B and the invasiveness of in vitro cultured lung cancer and bladder cancer cells treated with selected tetracyclines. Farm. Przegl. Nauk., 2009; 8: 17-23
Google Scholar - 73. The need is real: Data. http://organdonor.gov/about/data.html (20.05.2016)
Google Scholar - 74. Turek A., Cwalina B., Kobielarz M.: Radioisotopic investigation of crosslinking density in bovine pericardium used as a biomaterial. Nukleonika, 2013; 58: 511-517
Google Scholar - 75. Turek A., Kasperczyk J., Dzierżewicz Z.: Collagen application in drug formulation technology. Achievements and perspectives. Chemik, 2010; 64: 229-237
Google Scholar - 76. Ustawa z dnia 1 lipca 2005 r. o pobieraniu, przechowywaniu i przeszczepianiu komórek, tkanek i narządów. Dziennik Ustaw, 2005; nr 169: poz. 1411
Google Scholar - 77. Ustawa z dnia 17 lipca 2009 r. o zmianie ustawy o pobieraniu, przechowywaniu i przeszczepianiu komórek, tkanek i narządów oraz o zmianie ustawy – Przepisy wprowadzające Kodeks Karny. Dziennik Ustaw, 2009; nr 141: poz. 1149
Google Scholar - 78. van Kats J.P., van Tricht C., van Dijk A., van der Schans M., van den Bogaerdt A., Petit P.L., Bogers A.J.: Microbiological examination of donated human cardiac tissue in heart valve banking. Eur. J. Cardiothorac. Surg., 2010; 37: 163-169
Google Scholar - 79. Verghese S., Padmaja P., Sindhu B., Elizabeth S.J., Lesley N., Cherian K.M.: Homograft valve bank: our experience in valve banking. Indian Heart J., 2004; 56: 299-306
Google Scholar - 80. Villalba R., Solis F., Fornés G., Jimenez A., Eisman M., González AI., Linares M.J., Casal M., Gómez Villagrán J.L.: In vitro susceptibility of high virulence microorganisms isolated in heart valve banking. Cell Tissue Bank, 2012; 13: 441-445
Google Scholar - 81. Virdi I.S., Monro J.L., Ross J.K.: Eleven year experience of aortic valve replacement with antibiotic sterilized homograft valve in Southampton. Thorac. Cardiovasc. Surg., 1986; 34: 277-282
Google Scholar - 82. Wachol-Drewek Z., Pfeiffer M., Scholl E.: Comparative investigation of drug delivery of collagen implants saturated in antibiotic solutions and a sponge containing gentamicin. Biomaterials, 1996; 17: 1733-1738
Google Scholar - 83. Wain W.H., Pearce H.M., Riddell R.W., Ross D.N.: A re-evaluation of antibiotic sterilisation of heart valve allografts. Thorax, 1977; 32, 740-742
Google Scholar - 84. Warwick R.M., Magee J.G., Leeming J.P., Graham J.C., Hannan M.M., Chadwick M., Crook D.W., Yearsley C.P., Rayner A., Parker R.: Mycobacteria and allograft heart valve banking: an international survey. J. Hosp. Infect., 2008; 68: 255-261
Google Scholar - 85. Waterworth P.M., Lockey E., Berry E.M., Pearce H.M.: A critical investigation into the antibiotic sterilization of heart valve homografts. Thorax, 1974; 29: 432-436
Google Scholar - 86. Welters M.J., Oei F.B., Witvliet M.D., Vaessen L.M., Cromme-Dijkhuis A.H., Bogers A.J., Weimar W., Claas F.H.: A broad and strong humoral immune response to donor HLA after implantation of cryopreserved human heart valve allografts. Hum. Immunol., 2002; 63: 1019-1025
Google Scholar - 87. Yacoub M., Kittle C.F.: Sterilization of valve homografts by antibiotic solutions. Circulation, 1970; 41: II29-II32
Google Scholar - 88. Yacoub M., Knight E., Towers M.: Aortic valve replacement using fresh unstented homografts. Thoraxchir. Vask. Chir., 1973; 21: 451-457
Google Scholar - 89. Yang J.H., Jun T.G., Sung K., Kim W.S., Lee Y.T., Park P.W.: Midterm results of size-reduced cryopreserved homografts for right ventricular outflow tract reconstruction. Ann. Thorac. Surg., 2010; 89: 1821-1826
Google Scholar - 90. Yankah A.C., Klose H., Petzina R., Musci M., Siniawski H., Hetzer R.: Surgical management of acute aortic root endocarditis with viable homograft: 13-year experience. Eur. J. Cardiothorac. Surg., 2002; 21: 260-267
Google Scholar