The characteristics of thrombosis in severe patients with omicron infection and the therapeutic value of preventive low molecular weight heparin_Chinese Journal of Respiratory and Critical Care Medicine

Authors：

WANG Junhong ¹ , ZHANG Hua ² , DONG Shujie ³ , FU Yuanwei ¹ , ZENG Lin ² , ZHAO Rongsheng ³ ,  MA Qingbian ¹

1. Emergency Department, Peking University Third Hospital, Beijing 100191, P. R. China;
2. Clinical Epidemiology Research Center, Peking University Third Hospital, Beijing 100191, P. R. China;
3. Pharmacy Department, Peking University Third Hospital, Beijing 100191, P. R. China;

Corresponding author：

MA Qingbian, Email: maqingbian@126.com

Keywords：

SARS-CoV-2; low molecular weight heparin; critically ill; thrombosis; mortality

DOI：

10.7507/1671-6205.202307012

Video：

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Objectives To explore the characteristics of thrombosis in critically ill patients with Omicron infection and the therapeutic value of prophylactic low molecular weight heparin (LMWH) treatment. Methods A single center, retrospective cohort study included critically ill adult patients with Omicron variant of SARS-CoV-2 admitted to Peking University Third Hospital from December 7, 2022, to February 8, 2023. The patients were categorized into two groups based prophylactic LMWH. Propensity score (PS) matching was used to match patients (1: 1 ratio) based on the predefined criteria. General clinical information and laboratory parameters were compared. This study was retrospectively registered at Chinese Clinical Trail Registry (ChiCTR2300067434). Results Four hundred and fifty-two patients and 360 patients were included before and after PS matching. There were no statistical differences in mortality, the incidence of pulmonary embolism, arterial thrombosis or bleeding between the anticoagulation group and non-coagulation group before and after PS matching. There were 91 thrombotic events in 82 patients (18.14%), of which 54 cases (59.34%) were lower limb intermuscular vein thrombosis, 3 cases (3.30%) were pulmonary embolism, 14 cases (15.38%) were acute myocardial infarction and 3 cases (3.30%) were acute cerebral infarction. The thrombotic event resulted in the death of 5 patients. D-dimer increased in 385 cases (85.56%). On the 1^st, 3^rd, 6^th and 9^th day, the concentration of D-dimer in the anticoagulant group was higher than that in the non-anticoagulant group (P=0.006, 0.001, 0.024 and 0.006, respectively). Conclusions Although thrombosis and coagulation disorders are still common complications of COVID-19, it is not the direct cause of most death in COVID-19 patients caused by Omicron. The role of prophylactic anticoagulation treatment for Omicron-infected patients needs further study.

Citation： WANG Junhong, ZHANG Hua, DONG Shujie, FU Yuanwei, ZENG Lin, ZHAO Rongsheng, MA Qingbian. The characteristics of thrombosis in severe patients with omicron infection and the therapeutic value of preventive low molecular weight heparin. Chinese Journal of Respiratory and Critical Care Medicine, 2024, 23(1): 15-23. doi: 10.7507/1671-6205.202307012 Copy

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22.	Guan WA, Ni ZY, Hu Y, et al. Clinical characteristics of Coronavirus Disease 2019 in China. N Engl J Med, 2020, 382(18): 1708-1720.
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25.	Dufour I, Werion A, Belkhir L, et al. Serum uric acid, disease severity and outcomes in COVID-19. Crit Care, 2021, 25(1): 212.
26.	Trofin F, Nastase E, Roșu MF, et al. Inflammatory response in COVID-19 depending on the severity of the disease and the vaccination status. Int J Mol Sci, 2023, 24(10): 8550.
27.	Abou Hassan FF, Bou Hamdan M, Melhem NM. Clinical characteristics and serum cytokines profiling in hospitalized COVID-19 patients in Lebanon. J Immunol Res, 2023, 2023: 7258585.

1. WHO coronavirus (COVID-19) dashboard. Available at: https: //covid19. who. int.
2. Tang N, Li DJ, Wang X, et al. Abnormal coagulation parameters are associated with poor prognosis in patients with novel coronavirus pneumonia. J Thromb Haemost, 2020, 18(4): 844-847.
3. Léonard Lorant I, Delabranche X, Séverac F, et al. Acute pulmonary embolism in patients with COVID-19 at CT angiography and relationship to D-dimer levels. Radiology, 2020, 296(3): E189-E191.
4. Poissy J, Goutay J, Caplan M, et al. Pulmonary embolism in patients with COVID-19: awareness of an increased prevalence. Circulation, 2020, 142(2): 184-186.
5. Thachil J, Tang N, Gando S, et al. ISTH interim guidance on recognition and management of coagulopathy in COVID-19. J Thromb Haemost, 2020, 18(5): 1023-1026.
6. Tang N, Bai H, Chen X, et al. Anticoagulant treatment is associated with decreased mortality in severe coronavirus disease 2019 patients with coagulopathy. J Thromb Haemost, 2020, 18(5): 1094-1099.
7. Ionescu F, Jaiyesimi I, Petrescu I, et al. Association of anticoagulation dose and survival in hospitalized COVID-19 patients: a retrospective propensity score-weighted analysis. Eur J Haematol, 2021, 106(2): 165-174.
8. Hara H, Uemura Y, Hayakawa K, et al. Evaluation of the efficacy of anticoagulation therapy in reducing mortality in a nationwide cohort of hospitalized patients with coronavirus disease in Japan. Int J Infect Dis, 2021, 112: 111-116.
9. Subramoney K, Mtileni N, Giandhari J, et al. Molecular epidemiology of SARS-CoV-2 during five COVID-19 waves and the significance of low-frequency lineages. Viruses, 2023, 15(5): 1194.
10. Davies E, Ryan K, Bewley K, et al. The omicron sub-variant BA.4 displays a remarkable lack of clinical signs in a Golden Syrian hamster model of SARS-CoV-2 infection. Viruses, 2023, 15(5): 1133.
11. Lu G, Ling Y, Jiang MH, et al. Primary assessment of the diversity of Omicron sublineages and the epidemiologic features of autumn/winter 2022 COVID-19 wave in Chinese mainland. Front Med, 2023, 17(4): 758-767.
12. https://www.who.int/publications/i/item/WHO-2019-nCoV-therapeutics-2023.2.
13. Thygesen K, Alpert JS, Jaffe AS, et al. Fourth Universal Definition of Myocardial Infarction (2018). Circulation, 2018, 138(20): e618-e651.
14. Tsaplin S, Schastlivtsev I, Zhuravlev S, et al. The original and modified Caprini score equally predicts venous thromboembolism in COVID-19 patients. J Vasc Surg Venous Lymphat Disord, 2021, 9(6): 1371-1381. e4.
15. Cao YL, Wang J, Jian FC, et al. Omicron escapes the majority of existing SARS-CoV-2 neutralizing antibodies. Nature, 2022, 602(7898): 657-663.
16. Kloka JA, Blum LV, Old O, et al. Characteristics and mortality of 561, 379 hospitalized COVID-19 patients in Germany until December 2021 based on real-life data. Sci Rep, 2022, 12(1): 11116.
17. Wichmann D, Sperhake JP, Lütgehetmann M, et al. Autopsy findings and venous thromboembolism in patients with COVID-19: a prospective cohort study. Ann Intern Med, 2020, 173(4): 268-277.
18. Lax SF, Skok K, Zechner P, et al. Pulmonary arterial thrombosis in COVID-19 with fatal outcome: results from a prospective, single-center, clinicopathologic case series. Ann Intern Med, 2020, 173(5): 350-361.
19. Bilaloglu S, Aphinyanaphongs Y, Jones S, et al. Thrombosis in hospitalized patients with COVID-19 in a New York City Health System. JAMA, 2020, 324(8): 799-801.
20. Wang H, Liu CC, Xie XW, et al. Multi-omics blood atlas reveals unique features of immune and platelet responses to SARS-CoV-2 Omicron breakthrough infection. Immunity, 2023, 56(6): 1410-1428. e8.
21. Levi M, Thachil J, Iba T, et al. Coagulation abnormalities and thrombosis in patients with COVID-19. Lancet Haematol, 2020, 7(6): e438-e440.
22. Guan WA, Ni ZY, Hu Y, et al. Clinical characteristics of Coronavirus Disease 2019 in China. N Engl J Med, 2020, 382(18): 1708-1720.
23. Billett HH, Reyes-Gil M, Szymanski J, et al. Anticoagulation in COVID-19: effect of enoxaparin, heparin, and apixaban on mortality. Thromb Haemost, 2020, 120(12): 1691-1699.
24. Godino C, Scotti A, Maugeri N, et al. Antithrombotic therapy in patients with COVID-19? -Rationale and evidence. Int J Cardiol, 2021, 324: 261-266.
25. Dufour I, Werion A, Belkhir L, et al. Serum uric acid, disease severity and outcomes in COVID-19. Crit Care, 2021, 25(1): 212.
26. Trofin F, Nastase E, Roșu MF, et al. Inflammatory response in COVID-19 depending on the severity of the disease and the vaccination status. Int J Mol Sci, 2023, 24(10): 8550.
27. Abou Hassan FF, Bou Hamdan M, Melhem NM. Clinical characteristics and serum cytokines profiling in hospitalized COVID-19 patients in Lebanon. J Immunol Res, 2023, 2023: 7258585.

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