Hemostasis and blood rheological properties: Relationship with the metabolism of gasotransmitters (NO and H2S) in hypertension and in the post-COVID period
DOI:
https://doi.org/10.33910/2687-1270-2026-7-2-206-219Keywords:
gasotransmitters, nitric oxide, hydrogen sulfide, blood rheological properties, hemostasis, hypertensionAbstract
In cardiovascular disease, the metabolism and regulatory potential of gasotransmitters, together with blood fluidity and hemostatic potential, acquire high significance. The aim of this study was to assess the interrelation between metabolism of gasotransmitters and blood rheological properties and the hemostasis system under normal conditions and in hypertension (HT), with an evaluation of the long-term consequences of COVID-19. Whole blood coagulation parameters were assessed by low-frequency piezothromboelastography using the ARP-01M Mednord analyzer (Russia), platelet aggregation was assessed using the ALAT-2 Biola laser analyzer (Russia), blood and plasma viscosity was measured with a Brookfield DV2T rotational viscometer (USA), and erythrocyte deformability and aggregation were assessed using the RheoScan D300 system (South Korea). H2S and NOx levels in blood plasma were determined photometrically. In healthy control, a stable balance of NO and H2S was observed. Their role in regulating blood rheological properties and coagulation, as well as their close interrelation and cross-talk, were confirmed by numerous correlations of rheological and hemostasis parameters with NO and H2S levels in plasma. An increase in plasma viscosity (by 12%, p<0.05), NOx level (by 51%, p<0.01), the intensity of the contact phase of coagulation and the polymerization stage of blood coagulation was recorded in HT compared to controls. In the post-COVID period, Hct, plasma viscosity, and NO levels in HT decreased, while erythrocyte and platelet aggregation activity remained high. The imbalance of gasotransmitters in HT manifests as a decrease in their regulatory effects on blood rheology and the hemostasis system.
References
Ali, M. Y., Ping, C. Y., Mok, Y. Y. et al. (2006) Regulation of vascular nitric oxide in vitro and in vivo; A new role for endogenous hydrogen sulfide? British Journal of Pharmacology, vol. 149, no. 6, pp. 625–634. https://doi.org/10.1038/sj.bjp.0706906 (In English)
Al-Kuraishy, H. M., Al-Gareeb, A. I., El-Bouseary, M. M. et al. (2023) Hyperviscosity syndrome in COVID-19 and related vaccines: Exploring of uncertainties. Clinical and Experimental Medicine, vol. 23, no. 3, pp. 679–688. https://doi.org/10.1007/s10238-022-00836-x (In English)
Arrigo, E., Comità, S., Pagliaro, P. et al. (2023) Clinical applications for gasotransmitters in the cardiovascular system: Are we there yet? International Journal of Molecular Sciences, vol. 24, no. 15, article 12480. https://doi.org/10.3390/ijms241512480 (In English)
Baskurt, O. K., Boynard, M., Cokelet, G. C. et al. (2009) New guidelines for hemorheological laboratory techniques. Clinical Hemorheology and Microcirculation, vol. 42, no. 2, pp. 75–97. https://doi.org/10.3233/CH-2009-1202 (In English)
Bosek, M., Wybranowski, T., Napiórkowska-Mastalerz, M. et al. (2023) The impact of COVID-19 on cellular factors influencing red blood cell aggregation examined in dextran: Possible causes and consequences. International Journal of Molecular Sciences, vol. 24, no. 19, article 14952. https://doi.org/10.3390/ijms241914952 (In English)
Cebová, M., Košútová, M., Pecháňová, O. (2016) Cardiovascular effects of gasotransmitter donors. Physiological Research, vol. 65, no. 3, pp. S291–S307. https://doi.org/10.33549/physiolres.933441 (In English)
Cirino, G., Szabo, C., Papapetropoulos, A. (2023) Physiological roles of hydrogen sulfide in mammalian cells, tissues, and organs. Physiological Reviews, vol. 103, no. 1, pp. 31–276. https://doi.org/10.1152/physrev.00028.2021 (In English)
COVIDSurg Collaborative; GlobalSurg Collaborative (2022) SARS-CoV-2 infection and venous thromboembolism after surgery: an international prospective cohort study. Anaesthesia, vol. 77, no. 1, pp. 28–39. https://doi.org/10.1111/anae.15563 (In English)
Fang, W., Jiang, J., Su, L. et al. (2021) The role of NO in COVID-19 and potential therapeutic strategies. Free Radical Biology and Medicine, vol. 1, no. 163, pp. 153–162. https://doi.org/10.1016/j.freeradbiomed.2020.12.008 (In English)
Gabbasov, Z. A., Popov, E. G., Gavrilov, I. Yu. et al. (1989) New high sensitive method of analysis of platelet aggregation. Laboratornoe delo, no. 10, pp. 15–18. (In Russian)
Giuffrè, A., Vicente, J. B. (2018) Hydrogen sulfide biochemistry and interplay with other gaseous mediators in mammalian physiology. Oxidative Medicine and Cellular Longevity, vol. 2018, article 6290931. https://doi.org/10.1155/2018/6290931 (In English)
Gusakova, S. V., Kovalev, I. V., Smagliy, L. V. et al. (2015Gas signalling in mammalian cells. Progress in Physiological Science, vol. 46, no. 4, pp. 53–73. (In Russian)
Jacobs, J. W., Booth, G. S. (2022) COVID-19 and immune-mediated RBC destruction. American Journal of Clinical Pathology, vol. 157, no. 6, pp. 844–851. https://doi.org/10.1093/ajcp/aqab210 (In English)
Kolluru, G. K., Shen, X., Kevil, C. G. (2020) Reactive sulfur species: A new redox player in cardiovascular pathophysiology. Arteriosclerosis, Thrombosis and Vascular Biology, vol. 40, no. 4, pp. 874–884. https://doi.org/10.1161/ATVBAHA.120.314084 (In English)
Lechner-Scott, J., Levy, M., Hawkes, C. et al. (2021) Long COVID or post COVID-19 syndrome. Multipled Sclerosis and Related Disorders, vol. 55, article 103268. https://doi.org/10.1016/j.msard.2021.103268 (In English)
LoBue, A., Heuser, S. K., Lindemann, M. et al. (2026) Red blood cell endothelial nitric oxide synthase: A major player in regulating cardiovascular health. British Journal of Pharmacology, vol. 183, no. 1, pp. 40–56. https://doi.org/10.1111/bph.16230 (In English)
Mahdi, A., Collado, A., Tengbom, J. et al. (2022) Erythrocytes induce vascular dysfunction in COVID-19. JACC: Basic to Translational Science, vol. 7, no. 3, pp. 193–204. https://doi.org/10.1016/j.jacbts.2021.12.003 (In English)
Miranda, K. M., Espey, M. G., Wink, D. A. (2001) A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide, vol. 5, no. 1, pp. 62–71. https://doi.org/10.1006/niox.2000.0319 (In English)
Muravyov, A. V., Antonova, N., Tikhomirova, I. A. (2019) Red blood cell micromechanical responses to hydrogen sulfide and nitric oxide donors: Analysis of crosstalk of two gasotransmitters (H2S and NO). Series on Biomechanics, vol. 33, no. 2, pp. 34–40. (In English)
Nikolaidis, A., Kramer, R., Ostojic, S. (2021) Nitric oxide: The missing factor in COVID-19 severity? Medical Sciences (Basel), vol. 10, no. 1, article 3. https://doi.org/10.3390/medsci10010003 (In English)
Norris, E. J. Culberson, C. R., Narasimhan, S. (2011) The liver as a central regulator of hydrogen sulfide. Shock, vol. 36, no. 3, pp. 242–250. https://doi.org/10.1097/SHK.0b013e3182252ee7 (In English)
Pozhilova, E. V., Novikov, V. E. (2015) Physiological and pathological value of cellular synthase of nitrogen oxide and endogenous nitrogen oxide. Vestnik Smolenskoy Gosudarstvennoy Medicinskoy Academii, vol. 14, no. 4, pp. 35–41. (In Russian)
Schmid-Schönbein, H., Kline, K. A., Heinich, L. et al. (1975) Microrheology and light transmission of blood. III. The velocity of red cell aggregate formation. Pflügers Archiv: European Journal of Physiology, vol. 354, no. 4, pp. 299–317. https://doi.org/10.1007/BF00587849 (In English)
Shibuya, N., Milkanai, Y., Kimura, Y. et al. (2009). Vascular endothelium expresses 3-mercaptopyruvate sulfurtransferase and produces hydrogen sulfide. International Journal of Biochemistry Research, vol. 146, no. 5, pp. 623–626. https://doi.org/10.1093/jb/mvp111 (In English)
Shin, S., Hou, J. X., Suh, J. S. et al. (2007) Validation and application of a microfluidic ektacytometer (RheoScan-D) in measuring erythrocyte deformability. Clinical Hemorheolology and Microcirculation, vol. 37, no. 4, pp. 319–328. (In English)
Shin, S., Nam, J. H., Hou, J. X., Suh, J. S. (2009) A transient, microfluidic approach to the investigation of erythrocyte aggregation: the threshold shear-stress for erythrocyte disaggregation. Clinical Hemorheolology and Microcirculation, vol. 42, no. 2, pp. 117–125. https://doi.org/10.3233/CH-2009-1191 (In English)
Tikhomirova, I. A., Petrochenko, E. P., Petrochenko, A. S. (2021) Hydrogen sulfide as a signaling molecule in the cardiovascular system. Regional blood Circulation and Microcirculation, vol. 20, no. 1, pp. 5–16. https://doi.org/10.24884/1682-6655-2021-20-1-5-16 (In Russian)
Tyutrin, I. I., Udut, V. V. (2016) Low-frequency piezothromboelastography of whole blood: Algorhytms of diagnostics and corrections of hemostasiological disorders. Tomsk: Tomsk State University Publ., 170 p. (In Russian)
Wang, R. (2010) Hydrogen sulfide: THE third gasotransmitter in biology and medicine. Antioxidants & Redox Signaling, vol. 12, no. 9, pp. 1061–1064. https://doi.org/10.1089/ars.2009.2938 (In English)
Whiteman, M., Moore, P. K. (2009) Hydrogen sulfide and the vasculature: a novel vasculoprotective entity and regulator of nitric oxide bioavailability? Journal of Cellular and Molecular Medicine, vol. 13, no. 3, pp. 488–507. https://doi.org/10.1111/j.1582-4934.2009.00645.x (In English)
Yuan, S., Shen, X., Kevil, C. G. (2017) Hydrogen sulfide and polysulfide in cardiovascular health and immune response. Antioxidants & Redox Signaling, vol. 27, no. 10, pp. 634–653. https://doi.org/10.1089/ars.2017.7096 (In English)
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