References

emcardio

Неотложная кардиология и кардиоваскулярные риски

Emergency Cardiology and Cardiovascular Risks journal

2616-633X

Белорусский государственный медицинский университет

10.51922/2616-633X.2021.5.2.1223

emcardio-140

Research Article

Обзоры и лекции

Reviews and lectures

Коронавирусная инфекция (SARS-CoV-2): фокус на СОVID-19 ассоциированную коагулопатию

Coronavirus infection (SARS-CoV-2): focus on COVID-19 associated coagulopathy

Плешко

А. А.

Pleshko

A. A.

Петрова

Е. Б.

Petrova

E. B.

Гунич

С. В.

Gunich

S. V.

Ракович

С. В.

Rakovich

S. V.

Григоренко

Е. А.

Grigorenko

E. A.

Митьковская

Н. П.

Mitkovskaya

N. P.

Белорусский государственный медицинский университетBelarusian State Medical University

УЗ «4-я городская клиническая больница им. Н.Е. Савченко»4th city clinical hospital named after N.E. Savchenko

УЗ «Городская клиническая инфекционная больница»City Clinical Hospital of Infectious Diseases

ГУ «РНПЦ «Кардиология»"Republican Scientific and Practical Center" Cardiology"

2021

22102025

5112231233

2025

Плешко А.А., Петрова Е.Б., Гунич С.В., Ракович С.В., Григоренко Е.А., Митьковская Н.П.

Pleshko A.A., Petrova E.B., Gunich S.V., Rakovich S.V., Grigorenko E.A., Mitkovskaya N.P.

Данная работа распространяется под лицензией Creative Commons Attribution 4.0.

This work is licensed under a Creative Commons Attribution 4.0 License.

https://emcardio.bsmu.by/jour/article/view/140

Пандемия coronavirus disease 2019 (COVID-19), официально объявленная Всемирной организацией здравоохранения в марте 2020 года, потрясает немыслимой скоростью распространения коронавирусной инфекции и большим числом жертв. С начала пандемии по всему миру зарегистрировано более 171 млн подтвержденных случаев COVID-19, включая более 3,6 млн смертельных исходов. Высокая частота венозных тромбоэмболических осложнений и не ОРДС (острый респираторный дистресс-синдром) – ассоциированной гибели пациентов с коронавирусной инфекцией SARS-CoV-2 (severe acute respiratory syndrome coronavirus 2), несмотря на проводимую антитромботическую терапию, может свидетельствовать о необходимости более интенсифицированного персонифицированного режима профилактических мероприятий.

Officially announced by the World Health Organization (WHO) in March 2020, the coronavirus disease 2019 (COVID-19) pandemic is terrifying with the unimaginable rate of spreading and the large number of deaths. Morethan 171 million COVID-19 cases including more than 3,6 million deaths have been confirmed worldwide since the start of the pandemic. The high incidence of venous thromboembolic events and non-ARDS (acute respiratory distress syndrome) associated death of patients with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection, despite prophylactic antithrombotic therapy, may indicate the need for a more intensified personalized regime of preventive measures.

коронавирусная инфекцияSARS-CoV-2COVID-19коагулопатиягемостазвенозная тромбоэмболиятромбоэмболия легочной артерииострый респираторный дистресс-синдром

coronavirus infectionSARS-CoV-2COVID-19coagulopathyhemostasisvenous thromboembolismpulmonary embolismacute respiratory distress syndrome

References1

Liu, Q., Liu D., Yang Z. Characteristics of human infection with avian influenza viruses and development of new antiviral agents. Acta Pharmacol Sin, 2013, vol. 34, no. 10, pp. 1257-1269. doi: 10.1038/aps.2013.121.

Graham-Rowe, D. Epidemiology: Racing against the flu. Nature, 2011, vol. 480, no. 7376, pp. S2-S3. doi: 10.1038/480S2a.

Esparza, J. Lessons from history: what can we learn from 300 years of pandemic flu that could inform the response to COVID-19? Am J Public Health, 2020, vol. 110, no. 8, pp. 1160-1161. doi: 10.2105/AJPH.2020.305761.

Polyakov A.S., Tyrenko V.V., Noskov Ya. A., Shirokov V.V. Patogeneticheskie podchody k korrekzii narusheniy gemostaza i assoziirovannych oslozhneniy pri infekzii, vyzvannoy SARS-COV-2 (COVID-19). Obzor literatury i aktualnych klinicheskich rekomendaziy [Pathogenetic approaches to the correction of hemostasis disorders and associated complications in infection caused by sars-cov-2 (covid-19). Review of literature and current clinical guidelines]. Klinicheskaya patofiziologiya, 2020, vol. 26, no. 2, pp. 55-65. (in Russian).

Liu, Y.-C., Kuo R.-L., Shih S.-R. COVID-19: The first documented coronavirus pandemic in history. Biomed J, 2020, vol. 43, no. 4, pp. 328-333. doi: 10.1016/j.bj.2020.04.007.

Puranik A., Niesen M.J.M., Lindemer E., Lenehan P., Cristea-Platon T., Pawlowski C., Soundararajan V. Case fatality rates for COVID-19 are higher than case fatality rates for motor vehicle accidents for individuals over 40 years of age. medRxiv, 2021, pp. 2021.04.09.21255193. doi: 10.1101/2021.04.09.21255193.

WHO Coronavirus (COVID-19) Dashboard [electronic resource]. Available at: https://covid19.who.int. (accessed 05.06.2021).

Rawal, G., Yadav S., Kumar R. Acute Respiratory Distress Syndrome: An Update and Review. J Transl Int Med, 2018, vol. 6, no. 2, pp. 74-77. doi: 10.1515/jtim-2016-0012.

Brower R.G., Matthay M.A., Morris A., Schoenfeld D., Thompson B.T., Wheeler Arthur. Ventilation with lower tidal volumes as compared with traditional tidal volumes for acute lung injury and the acute respiratory distress syndrome. N Engl J Med, 2000, vol. 342, no. 18, pp. 1301-1308. doi: 10.1056/NEJM200005043421801.

Grasselli G., Tonetti T., Protti A., Langer T., Girardis M., Bellani G., Laffey J., Carrafiello G., Carsana L., Rizzuto C. et al. Pathophysiology of COVID-19-associated acute respiratory distress syndrome: a multicentre prospective observational study. Lancet Respir Med, 2020, vol. 8, no. 12, pp. 1201-1208. doi: 10.1016/S2213-2600(20)30370-2.

Torres Acosta M.A., Singer B.D. Pathogenesis of COVID-19-induced ARDS: implications for an ageing population. Eur Respir J, 2020, vol. 56, no. 3, pp. 2002049. doi: 10.1183/13993003.02049-2020.

Grieco D.L., Bongiovanni F., Chen L., Menga L.S., Cutuli S.L., Pintaudi G., Carelli S., Michi T., Torrini F., Lombardi G., Anzellotti G.M., De Pascale G., Urbani A., Bocci M.G., Tanzarella E.S., Bello G., Dell’Anna A.M., Maggiore S.M., Brochard L., Antonelli M. Respiratory physiology of COVID-19-induced respiratory failure compared to ARDS of other etiologies. Crit Care, 2020, vol. 24, no. 1, pp. 529. doi: 10.1186/s13054-020-03253-2.

Mackman N., Antoniak S., Wolberg A.S., Kasthuri R., Key N.S. Coagulation Abnormalities and Thrombosis in Patients Infected With SARS-CoV-2 and Other Pandemic Viruses. Arterioscler Thromb Vasc Biol, 2020, vol. 40, no. 9, pp. 2033-2044. doi: 10.1161/ATVBAHA.120.314514.

Ackermann M., Verleden S.E., Kuehnel M., Haverich A., Welte T., Laenger F., Vanstapel A., Werlein C., Stark H., Tzankov A., Li W.W., Li V.W., Mentzer S.J., Jonigk D. Pulmonary Vascular Endothelialitis, Thrombosis, and Angiogenesis in Covid-19. N Engl J Med, 2020, vol. 383, no. 2, pp. 120-128. doi: 10.1056/NEJMoa2015432.

Cook, D.J., Crowther M.A. Thromboprophylaxis in the intensive care unit: focus on medical-surgical patients. Crit Care Med, 2010, vol. 38, pp. S76-S82. doi: 10.1097/CCM.0b013e3181c9e344.

Bunce P.E., High S.M., Nadjafi M., Stanley K., Liles W.C., Christian M.D. Pandemic H1N1 influenza infection and vascular thrombosis. Clin Infect Dis, 2011, vol. 52, no. 2, pp. e14-e17. doi: 10.1093/cid/ciq125.

Obi A.T., Tignanelli C.J., Jacobs B.N., Arya S., Park P.K., Wakefield T.W., Henke P.K., Napolitano L.M. Empirical systemic anticoagulation is associated with decreased venous thromboembolism in critically ill influenza A H1N1 acute respiratory distress syndrome patients. J Vasc Surg Venous Lymphat Disord, 2019. vol. 7, no. 3, pp. 317-324. doi: 10.1016/j.jvsv.2018.08.010.

Giannis, D., Ziogas I.A., Gianni P. Coagulation disorders in coronavirus infected patients: COVID-19, SARS-CoV-1, MERS-CoV and lessons from the past. J Clin Virol, 2020, vol. 127, pp. 104362. doi: 10.1016/j.jcv.2020.104362.

Pek Yoon Chong, Paul Chui, Ai E. Ling, Teri J. Franks, Dessmon Y. H. Tai, Yee Sin Leo, Gregory J. L. Kaw, Gervais Wansaicheong, Kwai Peng Chan, Lynette Lin Ean Oon, Eng Swee Teo, Kong Bing Tan, Noriko Nakajima, Tetsutaro Sata, William D. Travis. Analysis of Deaths During the Severe Acute Respiratory Syndrome (SARS) Epidemic in Singapore: Challenges in Determining a SARS Diagnosis. Arch Pathol Lab Med 1 February 2004; 128 (2): 195–204. doi: https://doi.org/10.5858/2004-128-195-AODDTS.

Umapathi T., Kor A.C., Venketasubramanian N., Lim C.C.T., Pang B.C., Yeo T.T., Lee C.C., Lim P.L., Ponnudurai K., Chuah K.L., Tan P.H., Tai D.Y.H., Ang S.P.B. Large artery ischaemic stroke in severe acute respiratory syndrome (SARS). J Neurol, 2004, vol. 251, no. 10, pp. 1227-1231. doi: 10.1007/s00415-004-0519-8.

Nematzoda O., Gaibov A.D., Kalmykov E.L., Baratov A.K. Covid-19-assoziirovannyy arterialnyy tromboz [Covid-19-related arterial thrombosis ]. Vestnik Avizenny, 2021, vol. 23, no.1, pp. 85-94. (in Russian).

Li Y., Zhao K., Wei H., Chen W., Wang W., Jia L., Liu Q., Zhang J., Shan T., Peng Z., Liu Y., Yan X. Dynamic relationship between D-dimer and COVID-19 severity. Br J Haematol, 2020, vol. 190, no. 1, pp e24-e27. doi: 10.1111/bjh.16811.

Chaudhary R., Garg J., Houghton D.E., Murad M.H., Kondur A., Chaudhary R., Wysokinski W.E., McBane R.D.2nd Thromboinflammatory Biomarkers in COVID-19: Systematic Review and Meta-analysis of 17,052 Patients. Mayo Clin Proc Innov Qual Outcomes, 2021, vol. 5, no. 2, pp. 388-402. doi: 10.1016/j.mayocpiqo.2021.01.009.

Guan W.-J., Ni Z.-Y., Hu Y., Liang W.-H., Ou C.-Q., He J.-X., Liu L., Shan H., Lei C.-L., Hui D.S.C. et al. Clinical Characteristics of Coronavirus Disease 2019 in China. N Engl J Med, 2020, vol. 382, no. 18, pp. 1708-1720. doi: 10.1056/NEJMoa2002032.

Tang N., Li D., Wang X., Sun Z. Abnormal coagulation parameters are associated with poor prognosis in patients with novel coronavirus pneumonia. J Thromb Haemost, 2020, vol. 18, no. 4, pp. 844-847. doi: 10.1111/jth.14768.

Zhang L., Yan X., Fan Q., Liu H., Liu X., Liu Z., Zhang Z. D-dimer levels on admission to predict in-hospital mortality in patients with Covid-19. J Thromb Haemost, 2020, vol. 18, no. 6, pp. 1324-1329. doi: 10.1111/jth.14859.

Huang C., Wang Y., Li X., Ren L., Zhao J., Hu Y., Zhang L., Fan G., Xu J., Gu X., Cheng Z., Yu T., Xia J., Wei Y., Wu W., Xie X., Yin W., Li H., Liu M., Xiao Y., Gao H., Guo L., Xie J., Wang G., Jiang R., Gao Z., Jin Q., Wang J., Cao B. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet, 2020, vol. 395, no. 10223, pp. 497-506. doi: 10.1016/S0140-6736(20)30183-5.

Dario Di Minno M.N., Calcaterra I., Lupoli R., Storino A., Spedicato G.A., Maniscalco M., Di Minno A., Ambrosino P. Hemostatic Changes in Patients with COVID-19: A Meta-Analysis with Meta-Regressions. J Clin Med, 2020, vol. 9, no. 7, pp. 2244. doi: 10.3390/jcm9072244.

Tripodi A., Chantarangkul V., Martinelli I., Bucciarelli P., Mannucci P.M. A shortened activated partial thromboplastin time is associated with the risk of venous thromboembolism. Blood, 2004, vol. 104, no. 12, pp. 3631-3634. doi: 10.1182/blood-2004-03-1042.

Mitkovskaya N., Grigorenko E., Ruzanov D., Statkevich T. Koronavirusnaya infekziya COVID-19 i komorbidnost [Coronavirus infection COVID-19 and comorbidity].Nauka i innovazii, 2020, no. 7, pp. 50-60. doi: 10.29235/1818-9857-2020-7-50-60. (in Russian).

Williamson D.R., Albert M., Heels-Ansdell D., Arnold D., Lauzier F., Zarychanski R., Crowther M., Warkentin T.E., Dodek P., Cade J. et al. Thrombocytopenia in Critically Ill Patients Receiving Thromboprophylaxis. Chest, 2013, vol. 144, no. 4, pp. 1207-1215. doi: 10.1378/chest.13-0121.

Goswami J., MacArthur T.A., Sridharan M., Pruthi R.K., McBane R.D.2nd, Witzig T.E., Park M.S. A Review of Pathophysiology, Clinical Features, and Management Options of COVID-19 Associated Coagulopathy. Shock, 2020, vol. 55, no. 6, pp. 700-716. doi: 10.1097/SHK.0000000000001680.

Yang X., Yang Q., Wang Y., Wu Y., Xu J., Yu Y., Shang Y. Thrombocytopenia and its association with mortality in patients with COVID-19. J Thromb Haemost, 2020, vol. 18, no. 6, pp. 1469-1472. doi: 10.1111/jth.14848.

Lippi G., Plebani M., Henry B.M. Thrombocytopenia is associated with severe coronavirus disease 2019 (COVID-19) infections: A meta-analysis. Clin Chim Acta, 2020, vol. 506, pp. 145-148. doi: 10.1016/j.cca.2020.03.022.

Wada H., Thachil J., Di Nisio M., Mathew P., Kurosawa S., Gando S., Kim H.K., Nielsen J.D., Dempfle C.-E., Levi M., Toh C.-H. Guidance for diagnosis and treatment of disseminated intravascular coagulation from harmonization of the recommendations from three guidelines. J Thromb Haemost, 2013, vol. 11, no. 4, pp. 761-767. doi: 10.1111/jth.12155.

Iba T., Levy J.H., Warkentin T.E., Thachil J., van der Poll T., Levi M. Diagnosis and management of sepsis-induced coagulopathy and disseminated intravascular coagulation. J Thromb Haemost, 2019, vol. 17, no. 11, pp. 1989-1994. doi: 10.1111/jth.14578.

Thachil J., Tang N., Gando S, Falanga A, Cattaneo M., Levi M., Clark C., Iba T. ISTH interim guidance on recognition and management of coagulopathy in COVID-19. J Thromb Haemost, 2020, vol. 18, no. 5, pp. 1023-1026. doi: 10.1111/jth.14810.

Mitkovskaya N.P., Karpov I.A., Arutyunov G.P., Grigorenko Ye.A., Ruzanov D.Yu., Statkevich T.V., Tarlovskaya E.I. COVID-19 coronavirus infection (overview of international research data). Neotlozhnaya kardiologiya i kardiovaskulyarnye riski, 2020, vol. 4, no. 1, pp. 784-815. (in Russian).

Varga Z., Flammer A.J., Steiger P., Haberecker M., Andermatt R., Zinkernagel A.S., Mehra M.R., Schuepbach R.A., Ruschitzka F., Moch H. Endothelial cell infection and endotheliitis in COVID-19. Lancet, 2020, vol. 395, no. 10234, pp. 1417-1418. doi: 10.1016/S0140-6736(20)30937-5.

McBane R.D.2nd, Roldan V.D.T., Niven A.S., Pruthi R.K., Franco P.M., Linderbaum J.A., Casanegra A.I., Oyen L.J., Houghton D.E., Marshall A.L. et al. Anticoagulation in COVID-19: A Systematic Review, Meta-analysis, and Rapid Guidance From Mayo Clinic. Mayo Clinic Proceedings, 2020, vol. 95, no. 11, pp. 2467-2486. doi: 10.1016/j.mayocp.2020.08.030.

Renzi S., Landoni G., Zangrillo A., Ciceri F. MicroCLOTS pathophysiology in COVID 19. Korean J Intern Med, 2020, vol. 9. doi: 10.3904/kjim.2020.336.

Hoppensteadt D., Tsuruta K., Hirman J., Kaul I., Osawa Y., Fareed J. Dysregulation of Inflammatory and Hemostatic Markers in Sepsis and Suspected Disseminated Intravascular Coagulation. Clin Appl Thromb Hemost, 2015, vol. 21, no. 2, pp. 120-127. doi: 10.1177/1076029613509476.

Petrischev N.N., Chalepo O.V., Vavilenkova Yu.A., Vlasov T.D. COVID-19 i sosudistye narusheniya (obzor literatury) [COVID-19 and vascular disorders (literature review)]. Regional blood circulation and microcirculation, 2020, vol. 19, no. 3, pp. 90-98. doi: 10.24884/1682-6655-2020-19-3-90-98. (in Russian).

Liu P.P., Blet A., Smyth D., Li H. The Science Underlying COVID-19: Implications for the Cardiovascular System. Circulation, 2020, vol. 142, no. 1, pp. 68-78. doi: 10.1161/CIRCULATIONAHA.120.047549

Helms J., Tacquard C., Severac F., Leonard-Lorant I., Ohana M., Delabranche X., Merdji H., Clere-Jehl R., Schenck M., Gandet F.F. et al. High risk of thrombosis in patients with severe SARS-CoV-2 infection: a multicenter prospective cohort study / CRICS TRIGGERSEP Group (Clinical Research in Intensive Care and Sepsis Trial Group for Global Evaluation and Research in Sepsis). Intensive Care Med, 2020, vol. 46, no. 6, pp. 1089-1098. doi: 10.1007/s00134-020-06062-x.

Escher R., Breakey N., Lämmle B. Severe COVID-19 infection associated with endothelial activation. Thromb Res, 2020, vol. 190, pp. 62. doi: 10.1016/j.thromres.2020.04.014.

Spiezia L., Boscolo A., Poletto F., Cerruti L., Tiberio I., Campello E., Navalesi P., Simioni P. COVID-19-Related Severe Hypercoagulability in Patients Admitted to Intensive Care Unit for Acute Respiratory Failure. Thromb Haemost, 2020, vol. 120, n. 6, pp. 998-1000. doi: 10.1055/s-0040-1710018.

Panigada M., Bottino N., Tagliabue P., Grasselli G., Novembrino C., Chantarangkul V., Pesenti A., Peyvandi F., Tripodi A. Hypercoagulability of COVID-19 patients in intensivecare unit: A report of thromboelastography findings and other parameters of hemostasis. J Thromb Haemost, 2020, vol. 18, no. 7, pp. 1738-1742. doi: 10.1111/jth.14850.

Goshua G., Pine A.B., Meizlish M.L., Chang C.-H., Zhang H., Bahel P., Baluha A., Bar N., Bona R.D., Burns A.J. et al. Endotheliopathy in COVID-19-associated coagulopathy: evidence from a single-centre, cross-sectional study / G. Goshua. Lancet Haematol, 2020, vol. 7, no. 8, pp. e575-e582. doi: 10.1016/S2352-3026(20)30216-7.

Helms J., Tacquard C., Severac F., Leonard-Lorant I., Ohana M., Delabranche X., Merdji H., Clere-Jehl R., Schenck M., Gandet F.F. et al. High risk of thrombosis in patients with severe SARS-CoV-2 infection: a multicenter prospective cohort study. Intensive Care Med, 2020, vol. 46, no. 6, pp. 1089-1098. doi: 10.1007/s00134-020-06062-x.

Tang N., Bai H., Chen X., Gong J., Li D., Sun Z. Anticoagulant treatment is associated with decreased mortality in severe coronavirus disease 2019 patients with coagulopathy. J Thromb Haemost, 2020, vol. 18, no. 5, pp. 1094-1099. doi: 10.1111/jth.14817.

Chang J.C. Acute Respiratory Distress Syndrome as an Organ Phenotype of Vascular Microthrombotic Disease: Based on Hemostatic Theory and Endothelial Molecular Pathogenesis. Clin Appl Thromb Hemost, 2019, vol. 25, 107602961988743. doi: 10.1177/1076029619887437.

Fogarty H., Townsend L., Cheallaigh C.N., Bergin C., Martin-Loeches I., Browne P., Bacon C.L., Gaule R., Gillett A., Byrne M., Ryan K., O’Connell N., O’Sullivan J.M., Conlon N., O’Donnell J.S. COVID19 coagulopathy in Caucasian patients. Br J Haematol, 2020, vol. 189, no. 6, pp. 1044-1049. doi: 10.1111/bjh.16749.

Joly B.S., Siguret V., Veyradier A. Understanding pathophysiology of hemostasis disorders in critically ill patients with COVID-19. Intensive Care Med, 2020, vol. 46, no. 8, pp. 1603-1606. doi: 10.1007/s00134-020-06088-1.

Brugliera L., Spina A., Castellazzi P., Cimino P., Tettamanti A., Houdayer E., Arcuri P., Alemanno F., Mortini P., Iannaccone S. Rehabilitation of COVID-19 patients. J Rehabil Med, 2020, vol. 52, no. 4, pp. jrm00046. doi: 10.2340/16501977-2678.

The authors declare that there are no conflicts of interest present.