Skip to main content
Top
Published in: Journal of Cardiovascular Translational Research 2/2020

01-04-2020 | Indomethacin | Original Article

Surgical Preparation Reduces Hydrogen Sulfide Released from Human Saphenous Veins in Coronary Artery Bypass Grafting

Authors: Chao Yuan, Hai-Tao Hou, Huan-Xin Chen, Jun Wang, Zheng-Qing Wang, Tie-Nan Chen, Xiao-Cheng Liu, Qin Yang, Guo-Wei He

Published in: Journal of Cardiovascular Translational Research | Issue 2/2020

Login to get access

Abstract

The long-term patency rate of saphenous vein (SV) grafts is poor compared to arterial grafts. To investigate the effects of surgical preparation (distention) of SV on hydrogen sulfide (H2S) released from the endothelium, human SV segments were harvested from 43 patients during coronary artery bypass surgery (CABG). Acetylcholine (ACh) induced relaxation that was inhibited by NG-nitro-L-arginine + indomethacin and cysteine aminotransferase inhibitor aminooxyacetic acid in the normal SV. In contrast, ACh did not evoke relaxation in the distended SV (DSV). The concentration of H2S quantified by methylene blue assay in DSV was significantly lower than that in control. Transmission electron microscope and immunohistochemistry studies showed that the preparation destroyed the endothelium, smooth muscle, organelle, and vasa vasorum. We conclude that surgical preparation injures the endothelium and smooth muscle of the SV grafts and reduces H2S release from SV. These effects may contribute to the poor long-term patency of the SV graft.
Literature
1.
go back to reference Gaudino, M., Antoniades, C., Benedetto, U., Deb, S., Di Franco, A., Di Giammarco, G., et al. (2017). ATLANTIC (Arterial Grafting International Consortium) Alliance. Mechanisms, consequences, and prevention of coronary graft failure. Circulation., 136, 1749–1764.CrossRef Gaudino, M., Antoniades, C., Benedetto, U., Deb, S., Di Franco, A., Di Giammarco, G., et al. (2017). ATLANTIC (Arterial Grafting International Consortium) Alliance. Mechanisms, consequences, and prevention of coronary graft failure. Circulation., 136, 1749–1764.CrossRef
2.
go back to reference Lytle, B. W., Loop, F. D., Cosgrove, D. M., Ratliff, N. B., Easley, K., & Taylor, P. C. (1985). Long-term (5 to 12 years) serial studies of internal mammary artery and saphenous vein coronary bypass grafts. The Journal of Thoracic and Cardiovascular Surgery, 89, 248–258.CrossRef Lytle, B. W., Loop, F. D., Cosgrove, D. M., Ratliff, N. B., Easley, K., & Taylor, P. C. (1985). Long-term (5 to 12 years) serial studies of internal mammary artery and saphenous vein coronary bypass grafts. The Journal of Thoracic and Cardiovascular Surgery, 89, 248–258.CrossRef
3.
go back to reference Gaudino, M., Benedetto, U., Fremes, S., Biondi-Zoccai, G., Sedrakyan, A., Puskas, J. D., et al. (2018). Radial-artery or saphenous-vein grafts in coronary-artery bypass surgery. The New England Journal of Medicine, 378, 2069–2077.CrossRef Gaudino, M., Benedetto, U., Fremes, S., Biondi-Zoccai, G., Sedrakyan, A., Puskas, J. D., et al. (2018). Radial-artery or saphenous-vein grafts in coronary-artery bypass surgery. The New England Journal of Medicine, 378, 2069–2077.CrossRef
4.
go back to reference Yamane, Y., Uchida, N., Okubo, S., Morimoto, H., & Mukai, S. (2017). Impact of the size mismatch between saphenous vein graft and coronary artery on graft patency. General Thoracic and Cardiovascular Surgery, 65, 25–31.CrossRef Yamane, Y., Uchida, N., Okubo, S., Morimoto, H., & Mukai, S. (2017). Impact of the size mismatch between saphenous vein graft and coronary artery on graft patency. General Thoracic and Cardiovascular Surgery, 65, 25–31.CrossRef
5.
go back to reference Hata, M., Yoshitake, I., Wakui, S., Unosawa, S., Kimura, H., Hata, H., et al. (2011). Long-term patency rate for radial artery vs. saphenous vein grafts using same-patient materials. Circulation Journal, 75, 1373–1377.CrossRef Hata, M., Yoshitake, I., Wakui, S., Unosawa, S., Kimura, H., Hata, H., et al. (2011). Long-term patency rate for radial artery vs. saphenous vein grafts using same-patient materials. Circulation Journal, 75, 1373–1377.CrossRef
6.
go back to reference He, G. W., Angus, J. A., & Rosenfeldt, F. L. (1988). Reactivity of the canine isolated internal mammary artery, saphenous vein, and coronary artery to constrictor and dilator substances: relevance to coronary bypass graft surgery. Journal of Cardiovascular Pharmacology, 12, 12–22.CrossRef He, G. W., Angus, J. A., & Rosenfeldt, F. L. (1988). Reactivity of the canine isolated internal mammary artery, saphenous vein, and coronary artery to constrictor and dilator substances: relevance to coronary bypass graft surgery. Journal of Cardiovascular Pharmacology, 12, 12–22.CrossRef
7.
go back to reference Van Son, J. A., Smedts, F., Vincent, J. G., van Lier, H. J., & Kubat, K. (1990). Comparative anatomic studies of various arterial conduits for myocardial revascularization. The Journal of Thoracic and Cardiovascular Surgery, 99, 703–707.CrossRef Van Son, J. A., Smedts, F., Vincent, J. G., van Lier, H. J., & Kubat, K. (1990). Comparative anatomic studies of various arterial conduits for myocardial revascularization. The Journal of Thoracic and Cardiovascular Surgery, 99, 703–707.CrossRef
8.
go back to reference Lüscher, T. F., Diederich, D., Siebenmann, R., Lehmann, K., Stulz, P., von Segesser, L., et al. (1988). Difference between endothelium-dependent relaxation in arterial and in venous coronary bypass grafts. The New England Journal of Medicine, 319, 462–467.CrossRef Lüscher, T. F., Diederich, D., Siebenmann, R., Lehmann, K., Stulz, P., von Segesser, L., et al. (1988). Difference between endothelium-dependent relaxation in arterial and in venous coronary bypass grafts. The New England Journal of Medicine, 319, 462–467.CrossRef
9.
go back to reference Liu, Z. G., Ge, Z. D., & He, G. W. (2000). Difference in endothelium-derived hyperpolarizing factor-mediated hyperpolarization and nitric oxide release between human internal mammary artery and saphenous vein. Circulation, 102, 296–301. Liu, Z. G., Ge, Z. D., & He, G. W. (2000). Difference in endothelium-derived hyperpolarizing factor-mediated hyperpolarization and nitric oxide release between human internal mammary artery and saphenous vein. Circulation, 102, 296–301.
10.
go back to reference Zhang, R. Z., Yang, Q., Yim, A. P., Huang, Y., & He, G. W. (2004). Different role of nitric oxide and endothelium-derived hyperpolarizing factor in endothelium-dependent hyperpolarization and relaxation in porcine coronary arterial and venous system. Journal of Cardiovascular Pharmacology, 43, 839–850.CrossRef Zhang, R. Z., Yang, Q., Yim, A. P., Huang, Y., & He, G. W. (2004). Different role of nitric oxide and endothelium-derived hyperpolarizing factor in endothelium-dependent hyperpolarization and relaxation in porcine coronary arterial and venous system. Journal of Cardiovascular Pharmacology, 43, 839–850.CrossRef
11.
go back to reference Chester, A. H., Buttery, L. D., Borland, J. A., Springall, D. R., Rothery, S., Severs, N. J., et al. (1998). Structural, biochemical and functional effects of distending pressure on human saphenous vein: implications for bypass grafting. Coronary Artery Disease, 9, 143–151.PubMed Chester, A. H., Buttery, L. D., Borland, J. A., Springall, D. R., Rothery, S., Severs, N. J., et al. (1998). Structural, biochemical and functional effects of distending pressure on human saphenous vein: implications for bypass grafting. Coronary Artery Disease, 9, 143–151.PubMed
12.
go back to reference Liu, Z. G., Liu, X. C., Yim, A. P., & He, G. W. (2001). Direct measurement of nitric oxide release from saphenous vein: abolishment by surgical preparation. The Annals of Thoracic Surgery, 71, 133–137.CrossRef Liu, Z. G., Liu, X. C., Yim, A. P., & He, G. W. (2001). Direct measurement of nitric oxide release from saphenous vein: abolishment by surgical preparation. The Annals of Thoracic Surgery, 71, 133–137.CrossRef
13.
go back to reference Zhao, J., Andreasen, J. J., Yang, J., Rasmussen, B. S., Liao, D., & Gregersen, H. (2007). Manual pressure distension of the human saphenous vein changes its biomechanical properties-implication for coronary artery bypass grafting. Journal of Biomechanics, 40, 2268–2276.CrossRef Zhao, J., Andreasen, J. J., Yang, J., Rasmussen, B. S., Liao, D., & Gregersen, H. (2007). Manual pressure distension of the human saphenous vein changes its biomechanical properties-implication for coronary artery bypass grafting. Journal of Biomechanics, 40, 2268–2276.CrossRef
14.
go back to reference Dashwood, M. R., Savage, K., Tsui, J. C., Dooley, A., Shaw, S. G., Fernández Alfonso, M. S., Bodin, L., & Souza, D. S. (2009). Retaining perivascular tissue of human saphenous vein grafts protects against surgical and distension-induced damage and preserves endothelial nitric oxide synthase and nitric oxide synthase activity. The Journal of Thoracic and Cardiovascular Surgery, 138, 334–340.CrossRef Dashwood, M. R., Savage, K., Tsui, J. C., Dooley, A., Shaw, S. G., Fernández Alfonso, M. S., Bodin, L., & Souza, D. S. (2009). Retaining perivascular tissue of human saphenous vein grafts protects against surgical and distension-induced damage and preserves endothelial nitric oxide synthase and nitric oxide synthase activity. The Journal of Thoracic and Cardiovascular Surgery, 138, 334–340.CrossRef
15.
go back to reference Chello, M., Mastroroberto, P., Frati, G., Patti, G., D’Ambrosio, A., Di Sciascio, G., & Covino, E. (2003). Pressure distension stimulates the expression of endothelial adhesion molecules in the human saphenous vein graft. The Annals of Thoracic Surgery, 76, 453–458.CrossRef Chello, M., Mastroroberto, P., Frati, G., Patti, G., D’Ambrosio, A., Di Sciascio, G., & Covino, E. (2003). Pressure distension stimulates the expression of endothelial adhesion molecules in the human saphenous vein graft. The Annals of Thoracic Surgery, 76, 453–458.CrossRef
16.
go back to reference Dreifaldt, M., Souza, D. S., Loesch, A., Muddle, J. R., Karlsson, M. G., Filbey, D., et al. (2011). The “no-touch” harvesting technique for vein grafts in coronary artery bypass surgery preserves an intact vasa vasorum. The Journal of Thoracic and Cardiovascular Surgery, 141, 145–150.CrossRef Dreifaldt, M., Souza, D. S., Loesch, A., Muddle, J. R., Karlsson, M. G., Filbey, D., et al. (2011). The “no-touch” harvesting technique for vein grafts in coronary artery bypass surgery preserves an intact vasa vasorum. The Journal of Thoracic and Cardiovascular Surgery, 141, 145–150.CrossRef
17.
go back to reference Souza, D. S., Johansson, B., Bojö, L., Karlsson, R., Geijer, H., Filbey, D., et al. (2006). Harvesting the saphenous vein with surrounding tissue for CABG provides long-term graft patency comparable to the left internal thoracic artery: results of a randomized longitudinal trial. The Journal of Thoracic and Cardiovascular Surgery, 132, 373–378.CrossRef Souza, D. S., Johansson, B., Bojö, L., Karlsson, R., Geijer, H., Filbey, D., et al. (2006). Harvesting the saphenous vein with surrounding tissue for CABG provides long-term graft patency comparable to the left internal thoracic artery: results of a randomized longitudinal trial. The Journal of Thoracic and Cardiovascular Surgery, 132, 373–378.CrossRef
18.
go back to reference Coletta, C., Papapetropoulos, A., Erdelyi, K., Olah, G., Módis, K., Panopoulos, P., et al. (2012). Hydrogen sulfide and nitric oxide are mutually dependent in the regulation of angiogenesis and endothelium-dependent vasorelaxation. Proceedings of the National Academy of Sciences of the United States of America, 109, 9161–9166.CrossRef Coletta, C., Papapetropoulos, A., Erdelyi, K., Olah, G., Módis, K., Panopoulos, P., et al. (2012). Hydrogen sulfide and nitric oxide are mutually dependent in the regulation of angiogenesis and endothelium-dependent vasorelaxation. Proceedings of the National Academy of Sciences of the United States of America, 109, 9161–9166.CrossRef
19.
go back to reference Shibuya, N., Mikami, Y., Kimura, Y., et al. (2009). Vascular endothelium expresses 3-mercaptopyruvate sulfurtransferase and produces hydrogen sulfide. Journal of Biochemistry, 146, 623–626.CrossRef Shibuya, N., Mikami, Y., Kimura, Y., et al. (2009). Vascular endothelium expresses 3-mercaptopyruvate sulfurtransferase and produces hydrogen sulfide. Journal of Biochemistry, 146, 623–626.CrossRef
20.
go back to reference Webb, G. D., Lim, L. H., Oh, V. M., Yeo, S. B., Cheong, Y. P., Ali, M. Y., et al. (2008). Contractile and vasorelaxant effects of hydrogen sulfide and its biosynthesis in the human internal mammary artery. The Journal of Pharmacology and Experimental Therapeutics, 324, 876–882.CrossRef Webb, G. D., Lim, L. H., Oh, V. M., Yeo, S. B., Cheong, Y. P., Ali, M. Y., et al. (2008). Contractile and vasorelaxant effects of hydrogen sulfide and its biosynthesis in the human internal mammary artery. The Journal of Pharmacology and Experimental Therapeutics, 324, 876–882.CrossRef
21.
go back to reference Ariyaratnam, P., Loubani, M., & Morice, A. H. (2013). Hydrogen sulphide vasodilates human pulmonary arteries: a possible role in pulmonary hypertension? Microvascular Research, 90, 135–137.CrossRef Ariyaratnam, P., Loubani, M., & Morice, A. H. (2013). Hydrogen sulphide vasodilates human pulmonary arteries: a possible role in pulmonary hypertension? Microvascular Research, 90, 135–137.CrossRef
22.
go back to reference Materazzi, S., Zagli, G., Nassini, R., Bartolini, I., Romagnoli, S., Chelazzi, C., et al. (2017). Vasodilator activity of hydrogen sulfide (H2S) in human mesenteric arteries. Microvascular Research, 109, 38–44.CrossRef Materazzi, S., Zagli, G., Nassini, R., Bartolini, I., Romagnoli, S., Chelazzi, C., et al. (2017). Vasodilator activity of hydrogen sulfide (H2S) in human mesenteric arteries. Microvascular Research, 109, 38–44.CrossRef
23.
go back to reference Gomez, I., Ozen, G., Deschildre, C., Amgoud, Y., Boubaya, L., Gorenne, I., et al. (2016). Reverse regulatory pathway (H2S/PGE2/MMP) in human aortic aneurysm and saphenous vein varicosity. PLoS One, 11, e0158421.CrossRef Gomez, I., Ozen, G., Deschildre, C., Amgoud, Y., Boubaya, L., Gorenne, I., et al. (2016). Reverse regulatory pathway (H2S/PGE2/MMP) in human aortic aneurysm and saphenous vein varicosity. PLoS One, 11, e0158421.CrossRef
24.
go back to reference Yang, J. A., & He, G. W. (1997). Surgical preparation abolishes endothelium-derived hyperpolarizing factor-mediated hyperpolarization in the human saphenous vein. The Annals of Thoracic Surgery, 63, 429–433.CrossRef Yang, J. A., & He, G. W. (1997). Surgical preparation abolishes endothelium-derived hyperpolarizing factor-mediated hyperpolarization in the human saphenous vein. The Annals of Thoracic Surgery, 63, 429–433.CrossRef
25.
go back to reference He, G. W., & Liu, Z. G. (2001). Comparison of nitric oxide release and endothelium-derived hyperpolarizing factor-mediated hyperpolarization between human radial and internal mammary arteries. Circulation., 104, 344–349.CrossRef He, G. W., & Liu, Z. G. (2001). Comparison of nitric oxide release and endothelium-derived hyperpolarizing factor-mediated hyperpolarization between human radial and internal mammary arteries. Circulation., 104, 344–349.CrossRef
26.
go back to reference Gao, G., Bai, X. Y., Xuan, C., Liu, X. C., Jing, W. B., Novakovic, A., et al. (2012). Role of TRPC3 channel in human internal mammary artery. Archives of Medical Research, 43, 431–437.CrossRef Gao, G., Bai, X. Y., Xuan, C., Liu, X. C., Jing, W. B., Novakovic, A., et al. (2012). Role of TRPC3 channel in human internal mammary artery. Archives of Medical Research, 43, 431–437.CrossRef
27.
go back to reference Chen, Z. W., Huang, Y., Yang, Q., Li, X., Wei, W., & He, G. W. (2005). Urocortin-induced relaxation in the human internal mammary artery. Cardiovascular Research, 65, 913–920.CrossRef Chen, Z. W., Huang, Y., Yang, Q., Li, X., Wei, W., & He, G. W. (2005). Urocortin-induced relaxation in the human internal mammary artery. Cardiovascular Research, 65, 913–920.CrossRef
28.
go back to reference Lechuga, T. J., Zhang, H. H., Sheibani, L., Karim, M., Jia, J., Magness, R. R., et al. (2015). Estrogen replacement therapy in ovariectomized nonpregnant ewes stimulates uterine artery hydrogen sulfide biosynthesis by selectively up-regulating cystathionine β-synthase expression. Endocrinology., 156, 2288–2298.CrossRef Lechuga, T. J., Zhang, H. H., Sheibani, L., Karim, M., Jia, J., Magness, R. R., et al. (2015). Estrogen replacement therapy in ovariectomized nonpregnant ewes stimulates uterine artery hydrogen sulfide biosynthesis by selectively up-regulating cystathionine β-synthase expression. Endocrinology., 156, 2288–2298.CrossRef
29.
go back to reference Yuan, C., Hou, H. T., Chen, H. X., Wang, J., Wang, Z. Q., Chen, T. N., et al. (2019). Hydrogen sulfide-mediated endothelial function and the interaction with eNOS and PDE5A activity in human internal mammary arteries. The Journal of International Medical Research, 02. Yuan, C., Hou, H. T., Chen, H. X., Wang, J., Wang, Z. Q., Chen, T. N., et al. (2019). Hydrogen sulfide-mediated endothelial function and the interaction with eNOS and PDE5A activity in human internal mammary arteries. The Journal of International Medical Research, 02.
30.
go back to reference Sellke, F. W., DiMaio, J. M., Caplan, L. R., Ferguson, T. B., Gardner, T. J., Hiratzka, L. F., et al. (2005). American Heart Association. Comparing on-pump and off-pump coronary artery bypass grafting: numerous studies but few conclusions: a scientific statement from the American Heart Association council on cardiovascular surgery and anesthesia in collaboration with the interdisciplinary working group on quality of care and outcomes research. Circulation., 111, 2858–2864.CrossRef Sellke, F. W., DiMaio, J. M., Caplan, L. R., Ferguson, T. B., Gardner, T. J., Hiratzka, L. F., et al. (2005). American Heart Association. Comparing on-pump and off-pump coronary artery bypass grafting: numerous studies but few conclusions: a scientific statement from the American Heart Association council on cardiovascular surgery and anesthesia in collaboration with the interdisciplinary working group on quality of care and outcomes research. Circulation., 111, 2858–2864.CrossRef
31.
go back to reference Ramos, J. R., Berger, K., Mansfield, P. B., & Savage, L. R. (1976). Histologic fate and endothelial changes of distended and nondistended vein grafts. Annals of Surgery, 183, 205–228.CrossRef Ramos, J. R., Berger, K., Mansfield, P. B., & Savage, L. R. (1976). Histologic fate and endothelial changes of distended and nondistended vein grafts. Annals of Surgery, 183, 205–228.CrossRef
32.
go back to reference He, G. W., & Taggart, D. P. (2016). Antispastic management in arterial grafts in coronary artery bypass grafting surgery. The Annals of Thoracic Surgery, 102, 659–668.CrossRef He, G. W., & Taggart, D. P. (2016). Antispastic management in arterial grafts in coronary artery bypass grafting surgery. The Annals of Thoracic Surgery, 102, 659–668.CrossRef
33.
go back to reference Angelini, G. D., Bryan, A. J., Williams, H. M. J., Morgan, R., & Newby, A. C. (1990). Distension promotes platelet and leukocyte adhesion and reduces short-term patency in pig arteriovenous bypass grafts. The Journal of Thoracic and Cardiovascular Surgery, 99, 433–439.CrossRef Angelini, G. D., Bryan, A. J., Williams, H. M. J., Morgan, R., & Newby, A. C. (1990). Distension promotes platelet and leukocyte adhesion and reduces short-term patency in pig arteriovenous bypass grafts. The Journal of Thoracic and Cardiovascular Surgery, 99, 433–439.CrossRef
34.
go back to reference Fernández-Alfonso, M. S., Gil-Ortega, M., Aranguez, I., Souza, D., Dreifaldt, M., Somoza, B., et al. (2017). Role of PVAT in coronary atherosclerosis and vein graft patency: friend or foe? British Journal of Pharmacology, 174, 3561–3572.CrossRef Fernández-Alfonso, M. S., Gil-Ortega, M., Aranguez, I., Souza, D., Dreifaldt, M., Somoza, B., et al. (2017). Role of PVAT in coronary atherosclerosis and vein graft patency: friend or foe? British Journal of Pharmacology, 174, 3561–3572.CrossRef
35.
go back to reference Zaborska, K. E., Wareing, M., & Austin, C. (2017). Comparisons between perivascular adipose tissue and the endothelium in their modulation of vascular tone. British Journal of Pharmacology, 174, 3388–3397.CrossRef Zaborska, K. E., Wareing, M., & Austin, C. (2017). Comparisons between perivascular adipose tissue and the endothelium in their modulation of vascular tone. British Journal of Pharmacology, 174, 3388–3397.CrossRef
Metadata
Title
Surgical Preparation Reduces Hydrogen Sulfide Released from Human Saphenous Veins in Coronary Artery Bypass Grafting
Authors
Chao Yuan
Hai-Tao Hou
Huan-Xin Chen
Jun Wang
Zheng-Qing Wang
Tie-Nan Chen
Xiao-Cheng Liu
Qin Yang
Guo-Wei He
Publication date
01-04-2020
Publisher
Springer US
Published in
Journal of Cardiovascular Translational Research / Issue 2/2020
Print ISSN: 1937-5387
Electronic ISSN: 1937-5395
DOI
https://doi.org/10.1007/s12265-019-09925-x

Other articles of this Issue 2/2020

Journal of Cardiovascular Translational Research 2/2020 Go to the issue