Calcification resistance, biostability, and low immunogenic potential of porcine heart valves modified by dye-mediated photooxidation

Journal of Biomedical Materials Research

Volumn 56, Issue 1, 2001, Pages 24-30

  Moore, M A ^a   Adams, A K ^a  

^a Sulzer Carbomedics   (United States)

Author keywords

Calcification; Collagen; Crosslinking; Heart valves; Photodynamic

Indexed keywords

BIOLOGICAL ORGANS; FLAMMABILITY; SODIUM CHLORIDE; TISSUE;

BIOSTABILITY;

BIOMATERIALS;

CALCIUM; COLLAGEN; GLUTARALDEHYDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOCOMPATIBILITY; BIOPROSTHESIS; CALCIFICATION; CONTROLLED STUDY; CROSS LINKING; GRAFT SURVIVAL; HEART VALVE PROSTHESIS; IMMUNOGENICITY; INFLAMMATION; NONHUMAN; PHOTOOXIDATION; VASCULARIZATION;

ANIMALS; BIOCOMPATIBLE MATERIALS; BIOPROSTHESIS; CALCINOSIS; CALCIUM; COLLAGEN; COLORING AGENTS; FIXATIVES; FOLLOW-UP STUDIES; GLUTARAL; GUINEA PIGS; HEART VALVE PROSTHESIS; IMMUNIZATION; OXIDATION-REDUCTION; PHOTOCHEMISTRY; RATS; SWINE;

EID: 0035025057     PISSN: 00219304     EISSN: None     Source Type: Journal    
DOI: 10.1002/1097-4636(200107)56:1<24::AID-JBM1064>3.0.CO;2-Q     Document Type: Article

References (70)

1. Nimni ME, Cheung DT, Strates B, Kodama M, Sheikh K. Bioprosthesis derived from cross-linked and chemically modified collagenous tissues. In: Nimni ME, editor. Collagen III: biotechnology. Boca Raton, FL: CRC; 1988. p 1-38.
2. Hubert SL, Ferrans VJ, Jones M. Tissue-derived biomaterials and their use in cardiovascular prosthetic devices. Med Prog Technol 1988;14:115-163.
3. Nimni ME, Cheung DT. Chemically modified collagen: a natural biomaterial for tissue replacement. Tissue Eng 1988;137-143.
4. Buch WS, Kosek JC, Angell WW. Deterioration of formalin-treated aortic valve homografts. J Thorac Cardiovasc Surg 1970;60:673-682.
5. Rose AG. Pathology of the formalin-treated heterograft porcine aortic valve in the mitral position. Thorax 1972;27:401-409.
6. Schoen FJ, Tsao J, Levy RJ. Calcification of bovine pericardium used in cardiac valve bioprosthesis: role of glutaraldehyde-modified structural components in bioprosthetic tissue mineralization. Am J Pathol 1986;123:134-145.
7. Levy RJ, Schoen FJ, Anderson HC, Harasaki H, Koch TD, Brown W, Lian J, Cumming R, Gavin JB. Cardiovascular implant calcification: a survey and update. Biomaterials 1991;12: 707-714.
8. Schoen FJ. Pathologic findings in explanted clinical bioprosthetic valves fabricated from photooxidized bovine pericardium. J Heart Valve Dis 1998;7:174-179.
9. Talman EA, Boughner DR. Glutaraldehyde fixation alters the internal shear properties of porcine aortic heart valve tissue. Ann Thorac Surg 1995;60:S369-S373.
10. Vesely I, Boughner D, Song T. Tissue buckling as a mechanism of bioprosthetic valve failure. Ann Thorac Surg 1988;46:302-308.
11. Golomb G, Schoen FJ, Smith MS, Linden J, Dixon M, Levy RJ. The role of glutaraldehyde-induced cross-links in calcification of bovine pericardium used in cardiac valve bioprosthesis. Am J Pathol 1987;127:122-130.
12. Gong G, Ling Z, Seifter E, Factor SM, Frater RWM. Aldehyde tanning: the villain in bioprosthetic calcification. Eur J Cardio-Thorac Surg 1991;5:288-293.
13. Schryer PJ, Thomas ER, Starr JA, Wright JTM. Anticalcification effect of glutaraldehyde-preserved valve tissue stored for increasing time in glutaraldehyde. In: Bodnar E, editor. Biological and bioprosthetic valves. New York: York Medical; 1986. p 471-477.
14. Girardot MN, Torrianni M, Dillehay D, Girardot JM. Role of glutaraldehyde in calcification of porcine heart valves: comparing cusp and wall. J Biomed Mater Res 1995;29:793-801.
15. Zilla P, Weissenstein C, Bracher M, Zhang Y, Koen W, Human P, von Oppell U. High glutaraldehyde concentrations reduce rather than increase the calcification of aortic wall tissue. J Heart Valve Dis 1997;6:502-509.
16. Vasudev SC, Chandy T, Sharma CP, Mohanty M, Umasankar PR. Synergistic effect of released aspirin/heparin for preventing bovine pericardial calcification. Artif Organs 2000;24:129-136.
17. Zilla P, Fullard L, Trescony P, Meinhart J, Bezuidenhout D, Gorlitzer M, Human P, von Oppell U. Glutaraldehyde detoxification of aortic wall tissue: a promising perspective of emerging bioprosthetic valve concepts. J Heart Valve Dis 1997;6:510-520.
18. Rao KP, Shanthi C. Reduction of calcification by various treatments in cardiac valves. J Biomater Appl 1999;13:238-268.
19. Chanda J, Kuribayashi R, Abe T. Heparin coupling in inhibition of calcification of vascular bioprostheses. Biomaterials 1999;20:1753-1757.
20. Liao K, Seifter E, Hoffman D, Yellin EL, Frater RWM. Improved postfixation treatment of glutaraldehyde fixed porcine aortic valves by monosodium glutamate. Artif Organs 1992;6: 267-272.
21. Lee CH, Vyavahare NR, Kruth H, Schoen FJ, Bianco R, Levy RJ. Inhibition of aortic wall calcification in bioprosthetic heart valves by ethanol pretreatment: biochemical and biophysical mechanisms. J Biomed Mater Res 1998;43:30-37.
22. Vyavahare NR, Chen W, Joshi RR, Lee CH, Hirsch D, Levy J, Schoen FJ, Levy RJ. Current progress in anticalcification of bioprosthetic and polymeric heart valves. Cardiovasc Pathol 1997;6:219-229.
23. Golomb G, Ezra V. Prevention of bioprosthetic heart valve tissue calcification by charge modification: effects of protamine binding by formaldehyde. J Biomed Mater Res 1991;25:85-98.
24. Levy RJ, Wolfrum J, Schoen FJ, Hawley MA, Lund SA, Langer R. Inhibition of calcification of bioprosthetic heart valves by local controlled-release diphosphonate. Science 1985;228:190-192.
25. Grabenwöger M, Grimm M, Eybl E, Leukauf C, Müller MM, Plenck H Jr, Bock P. Decreased tissue reaction to bioprosthetic heart valve material after glutamic acid treatment: a morphological study. J Biomed Mater Res 1992;26:1231-1240.
26. Rossi MA, Braile DM, Teixeira MDR, Souza DRS, Peres LC. Lipid extraction attenuates the calcific degeneration of bovine pericardium used in cardiac valve bioprosthesis. J Exp Pathol 1990;71:187-196.
27. Schnen FJ, Levy R. Tissue heart valves: current challenges and future research prospectives. J Biomed Mater Res 1999;47:439-465.
28. Petite H, Rault I, Huc A, Menasche P, Herbage D. Use of the acyl azide method for cross-linking collagen-rich tissues such as pericardium. J Biomed Mater Res 1990;24:179-187.
29. Zeeman R, Dijkstra PJ, van Wachem PB, van Luyn MJA, Hendriks M, Cahalan PT, Feijen J. Successive epoxy and carbodiimide cross-linking of dermal sheep collagen. Biomaterials 1999;20:921-931.
30. van Wachem PB, Brouwer LA, Zeeman R, Dijkstra PJ, Feijen J, Hendriks M, Cahalan PT, van Luyn MJA. In vivo behavior of epoxy-crosslinked porcine heart valve cusps and walls. J Biomed Mater Res Appl Biomater 2000;53:18-27.
31. Thyagarajan K, Nguyen H, Tu R, Lohre J, Guida S, Sagartz JW, Quijano RC. Preliminary evaluation of calcification potential of Denacol treated small diameter biological vascular grafts. Trans Soc Biomater 1992;15:686.
32. Pereira CA, Lee JM, Haberer S. Effect of alternative crosslinking methods on the strain rate viscoelastic properties of bovine pericardial bioprosthetic material. J Biomed Mater Res 1990;24: 345-361.
33. Ferrans VJ, Milei J, Ishihara T, Storino R. Structural changes in implanted cardiac valvular bioprostheses constructed of glycerol-treated dura mater. Fur J Cardio-Thorac Surg 1991;5:144-154.
34. Lee WK, Park JC, Park YH, Cho BK, Kim JK, Park KD, Kim YH, Shu H. Crosslinking of porcine valve by UV irradiation. Trans Soc Biomater 1998;22:293.
35. Sung HW, Chang Y, Chiu CT, Chen CN, Liang HC. Mechanical properties of a porcine aortic valve fixed with a naturally occurring crosslinking agent. Biomaterials 1999;20:1759-1772.
36. Sung HW, Chang Y, Chiu CT, Chen CN, Liang HC. Crosslinking characteristics and mechanical properties of a bovine pericardium fixed with a naturally occurring crosslinking agent. J Biomed Mater Res 1999;47:116-126.
37. Ramshaw JAM, Stephens LJ, Tulloch PA. Methylene blue sensitized photo-oxidation of collagen fibrils. Biochim Biophys Acta 1994;1206:225-230.
38. Moore MA, Bohachevsky IK, Cheung DT, Boyan BD, Chen W, Bickers RR, McIlroy BK. Stabilization of pericardial tissue by dye-mediated photooxidation. J Biomed Mater Res 1994;28: 611-618.
39. Bengtsson L, Phillips R, Hægerstrand A. In vitro endothelialization of photooxidatively stabilized xenogeneic pericardium. Ann Thorac Surg 1995;60:S365-S368.
40. Bianco R, Mrachek J, Blee T, Phillips RE, Schoen F. Preclinical evaluation of a new pericardial bioprosthetic with dye mediated photooxidized bovine pericardial tissue. ASAIO J 1995;41: 30.
41. Moore MA, Chen W-M, Phillips RE, Bohachevsky IK, McIlroy BK. Shrinkage temperature vs. protein extraction assay as a measure of stabilization of photooxidized tissue. J Biomed Mater Res 1996;32:209-214.
42. Moore MA, Phillips RE. Biocompatibility and immunological properties of pericardial tissue stabilized by dye-mediated photooxidation. J Heart Valve Dis 1997;6:307-315.
43. Moore MA. Pericardial tissue stabilized by dye-mediated photooxidation: a review article. J Heart Valve Dis 1997;6:521-526.
44. McIlroy BK, Robinson MD, Chen W-M, Moore MA. Chemical modification of bovine tissues by dye-mediated photooxidation. J Heart Valve Dis 1997;6:416-423.
45. Lee JM, Kujath MF, Doherty PA, McIlroy BK, Grear DA, Moore MA. Hydrothermal isometric tension (HIT) testing demonstrates collagen crosslinking by dye-mediated photooxidation. Trans Soc Biomater 1997;20:177.
46. Weil L, Gordon WC, Buchert AR. Photooxidation of amino acids in the presence of methylene blue. Arch Biochem Biophys 1951;33:90-109.
47. Weil L, James S, Buchert AR. Photooxidation of crystalline chymotrypsin in the presence of methylene blue. Arch Biochem Biophys 1953;46:266-278.
48. Ray WJ Jr. Photochemical oxidation. Methods Enzymol 1967; 11:490-497.
49. Spikes JD, Straight R. Sensitized photochemical processes in biological systems. Annu Rev Phys Chem 1967;18:409-436.
50. Foote CS. Photosensitized oxidation and singlet oxygen: consequences in biological systems. In: Pryor CS, editor. Free radicals in biology. Volume III. New York: Academic; 1976. p 85-133.
51. Tomita M, Irie M, Ukita T. Sensitized photooxidation of histidine and its derivatives: products and mechanism of reaction. Biochemistry 1969;8:5149-5160.
52. Gurnani S, Arifuddin M, Augusti KT. Effect of visible light on amino acids - I tryptophan. Photochem Photobiol 1966;5:495-505.
53. Weil L, Seibles TS, Hesrkovits TT. Photooxidation of bovine insulin sensitized with methylene blue. Arch Biochem Biophys 1965;111:308-320.
54. Jori G, Galiazzo G, Marzotto A, Scoffone E. Selective and reversible photo-oxidation of the methionyl residues in lysozyme. J Biol Chem 1968;243:4272-4278.
55. Neumann NP, Moore S, Stein WH. Modification of methionine residues in ribonuclease. Biochemistry 1962;1:68-75.
56. Bernstein PH, Mechanic GL. A natural histidine-based imminium cross-link in collagen and its location. J Biol Chem 1980;255:10414-10422.
57. Akiba J, Ueno N, Chakrabarti B. Mechanisms of photo-induced vitreous liquefaction. Curr Eye Res 1994;13:505-512.
58. Zook DE, Fahrenstock SF. Covalent cross-linking of ribosomal RNA and proteins by methylene blue-sensitized photooxidation. Biochim Biophys Acta 1978;517:400-406.
59. Girotti AW, Lyman S, Deziel MR. Methylene blue-sensitized photooxidation of hemoglobin: evidence for cross-link formation. Photochem Photobiol 1979;29:1119-1125.
60. Cross-linking of collagenous products. U.S. patent 5,332,475. 1492.
61. Moore MA, Phillips RE Jr, McIlroy BK, Walley VM, Hendry PJ. Evaluation of porcine valves prepared by dye-mediated photooxidation. Ann Thorac Surg 1998;66:S245-S248.
62. Bianco RW, Phillips R, Mrachek J, Wilson J. Feasibility evaluation of a new pericardial bioprosthetic with dye mediated photo-oxidized bovine pericardial tissue. J. Heart Valve Dis 1996;5:317-322.
63. Moore MA, McIlroy BK, Bianco RW, Phillips RE Jr. Improved calcification performance of heart valve material prepared by dye-mediated photooxidation. In: Gabbay S, Wheatley D, editors. Advances in anti-calcific and anti-degenerative treatment of heart valve bioprostheses. Austin, TX: Silent Partners; 1997. p 125-136.
64. Grabenwöger M, Sider J, Fitzal F, Zelenka C, Windberger U, Grimm M, Moritz A, Bock P, Wolner E. Impact of glutaraldehyde on calcification of pericardial bioprosthetic heart valve material. Ann Thorac Surg 1996;62:772-777.
65. McIlroy BK, Ashton TR, Phillips RE, Bianco R, Weinberg SL, Anderson JM. Canine implant performance of photooxidized bovine arteries. Int Soc Appl Cardiovasc Biol 1996;5:46.
66. Klein K, Carnagey J, Hern-Anderson D, Ranieri J. Evaluation of autologous endothelial cell seeded photo-oxidized small-bore vascular grafts in the canine CABG model. Cardiovasc Pathol 2000;9(4):200.
67. Moazami N, Argenziano M, Williams M, Cabreriza SB, Oz. MC, Nowygrod R. Photo-oxidized bovine arterial grafts, short-term results. ASAIO J 1998;44(1):89-93.
68. Westaby S, Bianco RW, Katsumata T, Termin P. The Carbomedics "Oxford" photofix stentless valve (PSV). Semin Thorac Cardiovasc Surg 1999;11 Suppl 1:206-209.
69. Magnusson B, Kligman A. Allergic contact dermatitis in the guinea pig. Springfield: Charles C Thomas; 1970.
70. Schoen FJ, Levy RJ, Nelson AC, Bernhard WF, Nashef A, Hawley M. Onset and progression of experimental bioprosthetic heart valve calcification. Lab Invest 1985;52:523-532.