Biochemistry (Moscow)

, Volume 76, Issue 6, pp 677–685 | Cite as

Free radical reaction products and antioxidant capacity in beating heart coronary artery surgery compared to conventional bypass

  • A. GonencEmail author
  • A. Hacışevki
  • H. R. Griffiths
  • M. Torun
  • B. Bakkaloglu
  • B. Simsek


Oxygen-derived free radicals are important agents of tissue injury during ischemia and reperfusion. The aim of this study was to investigate changes in protein and lipid oxidation and antioxidant status in beating heart coronary artery surgery and conventional bypass and to compare oxidative stress parameters between the two bypass methods. Serum lipid hydroperoxide, nitric oxide, protein carbonyl, nitrotyrosine, vitamin E, and β-carotene levels and total antioxidant capacity were measured in blood of 30 patients undergoing beating heart coronary artery surgery (OPCAB, off-pump coronary artery bypass grafting) and 12 patients undergoing conventional bypass (CABG, on-pump coronary artery bypass grafting). In the OPCAB group, nitric oxide and nitrotyrosine levels decreased after reperfusion. Similarly, β-carotene level and total antioxidant capacity also decreased after anesthesia and reperfusion. In the CABG group, nitric oxide and nitrotyrosine levels decreased after ischemia and reperfusion. However, protein carbonyl levels elevated after ischemia and reperfusion. Vitamin E, β-carotene, and total antioxidant capacity decreased after ischemia and reperfusion. Significantly decreased nitration and impaired antioxidant status were seen after reperfusion in both groups. Moreover, elevated protein carbonyls were found in the CABG group. The off-pump procedure is associated with lower degree of oxidative stress than on-pump coronary surgery.

Key words

oxidative stress coronary artery bypass antioxidant protein carbonyls nitrotyrosine 



on-pump coronary artery bypass grafting


lipid hydroperoxide


nitric oxide




off-pump coronary artery bypass grafting


reactive oxygen species


total antioxidant capacity


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  1. 1.
    Garlick, P. B., Davies, M. J., Hearse, D. J., and Slater, T. F. (1987) Circ. Res., 61, 757–760.PubMedGoogle Scholar
  2. 2.
    Flaherty, J. T., and Weisfeldt, M. L. (1988) Free Radic. Biol. Med., 5, 409–419.PubMedCrossRefGoogle Scholar
  3. 3.
    McCord, J. M. (1988) Free Radic. Biol. Med., 4, 9–14.PubMedCrossRefGoogle Scholar
  4. 4.
    Kuzuya, T., Hoshida, S., Kim, Y., Nishida, M., Fuji, H., Kitabatake, A., Tada, M., and Kamada, T. (1990) Circ. Res., 66, 1160–1165.PubMedGoogle Scholar
  5. 5.
    Ambrosio, G., Zweier, J. L., and Flaherty, J. T. (1991) J. Mol. Cell Cardiol., 23, 1359–1374.PubMedCrossRefGoogle Scholar
  6. 6.
    Henry, T. D., Archer, S. L., Nelson, D., Weir, E. K., and From, A. H. L. (1993) Am. J. Physiol., 264, H1478–H1484.PubMedGoogle Scholar
  7. 7.
    Tosaki, A., Bagchi, D., Pali, T., Cordis, G. A., and Das, D. K. (1993) Biochem. Pharmacol., 45, 961–969.PubMedCrossRefGoogle Scholar
  8. 8.
    Xia, Y., Khatchikian, G., and Zweier, J. L. (1996) J. Biol. Chem., 271, 10096–10102.PubMedCrossRefGoogle Scholar
  9. 9.
    Hawkins, C. L., and Davies, M. J. (2001) Biochim. Biophys. Acta, 899, 196–219.Google Scholar
  10. 10.
    Kaneda, H., Taguchi, J., Ogasawara, K., Aizawa, T., and Ohno, M. (2002) Atherosclerosis, 162, 221–225.PubMedCrossRefGoogle Scholar
  11. 11.
    Hayashi, Y., Sawa, Y., Ohtake, S., Fukuyama, N., Nakazawa, H., and Matsuda, H. (2001) Ann. Thorac. Surg., 72, 571–576.PubMedCrossRefGoogle Scholar
  12. 12.
    Hayashi, Y., Sawa, Y., Fukuyama, N., Miyamoto, Y., Takahashi, T., Nakazawa, H., and Matsuda, H. (2003) J. Thorac. Cardiovasc. Surg., 126, 1813–1821.PubMedCrossRefGoogle Scholar
  13. 13.
    Gutteridge, J. M. C. (1995) Clin. Chem., 41, 1819–1828.PubMedGoogle Scholar
  14. 14.
    Nagel, E., Meyer, Z. U., Vilsendorf, A., Bartels, M., and Pichlmayr, R. (1997) Int. J. Vitam. Nutr. Res., 67, 298–306.PubMedGoogle Scholar
  15. 15.
    Muzakova, V., Kandar, R., Vojtisek, P., Skalicky, J., Vankova, R., Cegan, A., and Certinkova, Z. (2001) Physiol. Res., 50, 389–396.PubMedGoogle Scholar
  16. 16.
    Mezzetti, A., Lapenna, D., Pierdomenico, S. D., Di Giammarco, G., Bosco, G., Di Ilio, C., Santarelli, P., Calafiore, A. M., and Cuccurullo, F. (1993) J. Card. Surg., 8, 167–171.PubMedCrossRefGoogle Scholar
  17. 17.
    Coghlan, J. G., Flitter, W. D., Clutton, S. M., Panda, R., Daly, R., Wright, G., Ilsley, C. D., and Slater, T. F. (1994) J. Thorac. Cardiovasc. Surg., 107, 248–256.PubMedGoogle Scholar
  18. 18.
    De Vecchi, E., Pala, M. G., Di Credico, G., Agape, V., Paolini, G., Bonini, P. A., Grossi, A., and Paroni, R. (1998) Heart, 79, 242–247.PubMedGoogle Scholar
  19. 19.
    Nourooz-Zadeh, J., Tajaddini-Sarmadi, J., and Wolff, S. P. (1994) Anal. Biochem., 220, 403–409.PubMedCrossRefGoogle Scholar
  20. 20.
    Carty, J. L., Bevan, R., Waller, H., Mistry, N., Cooke, M., Lunec, J., and Griffiths, H. R. (2000) Biochem. Biophys. Res. Commun., 273, 729–735.PubMedCrossRefGoogle Scholar
  21. 21.
    Griffiths, H. R., Aldred, S., Dale, C., Nakano, E., Kitas, G. D., Grant, M. G., Nugent, D., Taiwo, F. A., Li, L., and Powers, H. J. (2006) Free Radic. Biol. Med., 40, 488–500.PubMedCrossRefGoogle Scholar
  22. 22.
    Lee, B. L., Chua, S. C., Ong, H. Y., and Ong, C. N. (1992) J. Chromatogr., 581, 41–47.PubMedCrossRefGoogle Scholar
  23. 23.
    Re, R., Pellegrini, N., Proteggente, A., Pannala, A., Yang, M., and Rice-Evans, C. (1999) Free Radic. Biol. Med., 26, 1231–1237.PubMedCrossRefGoogle Scholar
  24. 24.
    Halliwell, B., and Gutteridge, J. (1999) Free Radicals in Biology and Medicine, Oxford University Press, New York.Google Scholar
  25. 25.
    Tortolani, A. J., Powell, S. R., Misik, V., Weglicki, W. B., Pogo, G. J., and Kramer, J. H. (1993) Free Radic. Biol. Med., 14, 421–426.PubMedCrossRefGoogle Scholar
  26. 26.
    Cavarrochi, N. C., England, M. D., and O’Brain, J. F. (1986) J. Surg. Res., 40, 519–527.CrossRefGoogle Scholar
  27. 27.
    Coghlan, J. G., Flitter, W. D., Clutton, S. M., Ilsley, C. D., Rees, A., and Slater, T. F. (1993) J. Thorac. Cardiovasc. Surg., 106, 268–274.PubMedGoogle Scholar
  28. 28.
    Davies, S. W., Duffy, J. P., Wickens, D. G., Underwood, S. M., Hill, A., Alladine, M. F., Feneck, R. O., Dormandy, T. L., and Walesby, R. K. (1993) J. Thorac. Cardiovasc. Surg., 105, 979–987.PubMedGoogle Scholar
  29. 29.
    Eiselt, J., Racek, J., and Opatrny, K. J. (2001) Cas. Lek. Cesk., 140, 238.PubMedGoogle Scholar
  30. 30.
    Matata, B. M., Sosnowski, A. W., and Galinanes, M. (2000) Ann. Thorac. Surg., 69, 785–791.PubMedCrossRefGoogle Scholar
  31. 31.
    Starkopf, J., Tamme, K., Zilmer, M., Talvik, R., and Samarutel, J. (1997) Clin. Chim. Acta, 262, 77–88.PubMedCrossRefGoogle Scholar
  32. 32.
    Hadjinikolaou, L., Alexiou, C., Cohen, A. S., Standbridge, R. D. L., McColl, A. J., and Richmond, W. (2003) Eur. J. CardioThoracic Surg., 23, 969–975.CrossRefGoogle Scholar
  33. 33.
    Carlucci, F., Tabucchi, A., Biagioli, B., Simeone, F., Scoletta, S., Rosi, F., and Marinello, E. (2002) Biomed. Pharmacother., 56, 483–491.PubMedCrossRefGoogle Scholar
  34. 34.
    Gerritsen, W. B., Boven, W. J., Driessen, A. H., Haas, J. F., and Aarts, L. P. (2001) Eur. J. Cardio-Thorac., 20, 923–929.CrossRefGoogle Scholar
  35. 35.
    Stadtman, E. R., and Oliver, C. N. (1991) J. Biol. Chem., 266, 2005–2008.PubMedGoogle Scholar
  36. 36.
    Berlett, B. S., and Stadtman, E. R. (1997) J. Biol. Chem., 272, 20313–20316.PubMedCrossRefGoogle Scholar
  37. 37.
    Uchida, K. (2000) Free Radic. Biol. Med., 28, 1685–1696.PubMedCrossRefGoogle Scholar
  38. 38.
    Stadtman, E. R., and Berlett, B. S. (1997) Chem. Res. Toxicol., 10, 485–494.PubMedCrossRefGoogle Scholar
  39. 39.
    Serdar, Z., Aslan, K., Dirican, M., Sarandol, E., Yesilbursa, D., and Serdar, A. (2006) Clin. Biochem., 39, 794–803.PubMedCrossRefGoogle Scholar
  40. 40.
    Fu, S., Davies, M. J., Stocker, R., and Dean, R. T. (1998) Biochem. J., 333, 519–525.PubMedGoogle Scholar
  41. 41.
    Kinlay, S., Libby, P., and Ganz, P. (2001) Curr. Opin. Lipidol., 12, 383–389.PubMedCrossRefGoogle Scholar
  42. 42.
    Moncada, S. (1999) J. R. Soc. Med., 92, 164–169.PubMedGoogle Scholar
  43. 43.
    Ignarro, L. J., Napoli, C., and Loscalzo, J. (2002) Circ. Res., 90, 21–28.PubMedCrossRefGoogle Scholar
  44. 44.
    Node, K., Kitakaze, M., Kosaka, H., Komamura, K., Minamino, T., Tada, M., Inoue, M., Hori, M., and Kamada, T. (1995) Biochem. Biophys. Res. Commun., 211, 370–374.PubMedCrossRefGoogle Scholar
  45. 45.
    Node, K., Kitakaze, M., Sato, H., Koretsune, Y., Karita, M., Kosaka, H., and Hori, M. (1998) J. Am. Coll. Cardiol., 32, 63–68.PubMedCrossRefGoogle Scholar
  46. 46.
    Ma, X. L., Weyrich, A. S., Lefer, D. J., and Lefer, A. M. (1993) Circ. Res., 72, 403–412.PubMedGoogle Scholar
  47. 47.
    Gohra, H., Fujimura, Y., Hamano, K., Hiroshi, N., Tomoe, K., Nobuya, Z., Kensuke, E., Toshiko, U., Daikai, S., and Tsuyoshi, M. (1999) World J. Surg., 23, 1249–1253.PubMedCrossRefGoogle Scholar
  48. 48.
    Fukuyama, N., Takebayashi, Y., Hida, M., Ishida, H., Ichimori, K., and Nakazawa, H. (1997) Free Radic. Biol. Med., 22, 771–774.PubMedCrossRefGoogle Scholar
  49. 49.
    Miwa, K., Igawa, A., Nakagawa, K., Hirai, T., and Inoue, H. (1999) Cardiovasc. Res., 41, 291–298.PubMedCrossRefGoogle Scholar
  50. 50.
    Persad, S., Takeda, S., Panagia, V., and Dhalla, N. S. (1997) J. Mol. Cell. Cardiol., 29, 545–558.PubMedCrossRefGoogle Scholar
  51. 51.
    Price, J. E., and Fowkes, F. G. (1997) Eur. Heart J., 18, 719–727.PubMedGoogle Scholar
  52. 52.
    Marchioli, R. (1999) Pharmacol. Res., 40, 227–238.PubMedCrossRefGoogle Scholar
  53. 53.
    Tribble, D. L., AHA Science Advisory (1999) Circulation, 99, 591–595.PubMedGoogle Scholar
  54. 54.
    Haramaki, N., Stewart, D. B., Aggarwal, S., Ikeda, H., Reznick, A. Z., and Packer, L. (1998) Free Radic. Biol. Med., 25, 329–339.PubMedCrossRefGoogle Scholar
  55. 55.
    Barsacchi, R., Pelosi, G., Maffei, S., Baroni, M., Salvatore, L., Ursini, F., Verunelli, F., and Biagini, A. (1992) Int. J. Cardiol., 37, 339–343.PubMedCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2011

Authors and Affiliations

  • A. Gonenc
    • 1
    Email author
  • A. Hacışevki
    • 1
  • H. R. Griffiths
    • 2
  • M. Torun
    • 1
  • B. Bakkaloglu
    • 3
  • B. Simsek
    • 1
  1. 1.Department of Biochemistry, Faculty of PharmacyGazi UniversityAnkaraTurkey
  2. 2.Life and Health SciencesAston UniversityAston Triangle, BirminghamUK
  3. 3.Department of Cardiac SurgeryGuven HospitalAnkaraTurkey

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