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The Egyptian Journal of Internal Medicine
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A systematic review of the venous thromboembolism prevalence and related risk factors in patients with Covid-19

The Egyptian Journal of Internal Medicine volume 35, Article number: 54 (2023) Cite this article

Abstract

Introduction

The present study was performed to evaluate the pooled prevalence of the venous thromboembolism (VTE) and the factors affecting its incidence in patients who are affected with coronavirus disease (Covid-19).

Patients and methods

A systematic review and meta-analysis were carried out by searching all the authentic online databases. The study includes papers worldwide since 2019 to 2022. After assessing related articles, the required information was collected based on a prepared checklist and analyzed by STATA software.

Result

According to the estimates, pooled prevalence of VTE among patients with Covid-19 was 0.17 (95% CI = 0.13–0.22, P = 0.000). Analysis of prevalence values of VTE in patients with Covid-19 based on geographical areas showed statistically significant differences emerged from the study results. Analyses showed that stroke is a significant risk factor.

Discussion

The present study showed a relatively high prevalence of VTE in patients infected with coronavirus. Results of study showed that prevalence of VTE is significantly differ according to geographical areas; it can be concluded that racial differences and genetic factors can affect the VTE incidence in Covid-19-affected patients. Additionally, a history of stroke and cerebrovascular events can be a risk factor indicating the need for prophylactic anticoagulant treatment in these patients, but history of respiratory disease, cardiovascular disease, hypertension, diabetes, dyslipidemia, liver disease, malignancy, and smoking is not risk factors of VTE in patients affected with Covid-19.

Introduction

Initially spotted in Wuhan in December, Covid-19 spread rapidly worldwide [1]. Coronavirus is a fast-mutating single-stranded RNA virus that acts by linking with angiotensin-converting enzyme 2 (ACE2) receptors, particularly in the lungs and heart [2]. The Covid-19 virus uses ACE2 receptors to enter cells through add of the virus. However, it may bind to other receptors. Studies demonstrated that ACE2 is essential in viral proliferation [3].

Covid-19 involves various organs in the body and is not limited to the lungs [4]. A wide variety of disorders can be caused by the virus, including asymptomatic affection to severe systemic involvement and acute respiratory distress syndrome [5]. Systemic manifestations of this disease include hematologic disorders and increased incidence of thrombotic complications [6, 7]. A high prevalence of thrombotic complications has been reported in critically ill patients [8]. Patients admitted to intensive care units (ICUs) are more likely to suffer from VTE [9]. Covid-19 is most commonly associated with pulmonary embolism [10]. Studies on autopsies have also shown a high prevalence of thromboembolic events leading to respiratory failure [11]. The exact pathophysiology and the primary mechanism of clinical responses to Covid-19 are still unclear [12]. In severe cases, Covid-19 leads to cytokine release, platelet activation, endothelial dysfunction, and sepsis-related coagulopathy [13]. Coronavirus causes pneumonia in almost all patients and leads to cytokine storms in much more serious cases where inflammation stimulates the activation of coagulation [14]. During the early stages of the disease, inflammation of the alveolar vascular endothelium can stimulate the development of pulmonary clots and activate neutrophils to inhibit viral invasion [15]. In addition, the virus itself can trigger the coagulation cascade [16]. Studies have been performed to investigate the prevalence of thrombotic complications in Covid-19 disease and the factors affecting the occurrence of these complications. As comprehensive and complete results are unavailable, this meta-analysis can be helpful for researchers and scientists.

Patients and methods

Study outline

The present study was conducted based on Meta-analysis Of Observational Studies in Epidemiology (MOOSE) standards. It was reported using the Preferred Reporting Items for Systematic Reviews and Meta-analysis (PRISMA) published guidelines [17, 18]. The study was conducted by two independent researchers at all stages, and any discrepancies were examined by a third person.

Search strategy

The comprehensive search was operated using exact MeSH keywords, including "Covid-19"[MeSH], "venous thromboembolism"[MeSH], "deep vein thrombosis"[MeSH], and "pulmonary thromboembolism "[MeSH] in all confirmed online databases like CINAHL, Web of Science (ISI), and PubMed/Medline. Additionally, without considering any time limitation, our MeSH terms were searched in international publishers such as Wiley online library, Science Direct, and Springer since 2019 until February 2022. All databases were searched in English, and all articles were retrieved in English to remove any potential language bias. References from the retrieved articles were also analyzed.

Eligibility criteria for inclusion and exclusion

Cohort studies that assessed the prevalence and risk factors of VTE [deep vein thrombosis (DVT) or pulmonary thromboembolism (PTE)] in Covid-19 patients were taken into consideration. Exclusion criteria were as follows:

  1. 1.

    Non-English language articles

  2. 2.

    Non-cohort articles

  3. 3.

    Insufficient data

  4. 4.

    Non-related subject

  5. 5.

    Thesis, case studies, review articles, conference presentations, and letters to editors

Data extraction

The extracted data for this meta-analysis were as follows: Author’s name, study period, year of publication, number of Covid-19 patients, country, patient’s admission in ICU or ward, characteristics of samples [e.g., mean age and standard deviation (SD), total sample size, men and women, body mass index (BMI), underline disease, history of smoking], and VTE rate. These data were collected for VTE and non-VTE patients in studies assessing the risk factors of VTE in Covid-19 patients.

Quality assessment

Study quality was assessed using the Newcastle–Ottawa scale (NOS), and studies with a score of 5 were included in the analysis [19].

Statistical analysis

The studies collected were grouped into two categories: the prevalence of VTE in patients with Covid-19 and the risk factors associated with VTE in these patients. In order to combine the results of different studies, the random-effects model was utilized. As a result of the Q Cochrane test and the I2 index, heterogeneity was assessed and interpreted [20]. To elucidate the causes of heterogeneity between studies, subgroup analyses were conducted based on geographical localization. Analyzing the data was done using STATA version 12. Data analyses were displayed as plots, flowcharts, and tables. The significance threshold was set at less than 0.05.

Results

Search results and characteristics

After the comprehensive search in mentioned databases, 765 papers were gathered, of which 336 articles were excluded due to duplication. According to the abstracts, 129 studies were removed for not being related to the topic, having insufficient information, or not being in English. A total of 214 studies were excluded because of inadequate information, leaving 86 studies for the final analysis. Finally, in two groups (cohort and RCT), studies were analyzed (Fig. 1). Table 1 summarizes the collected data.

Fig. 1
figure 1

PRISMA flowchart

Full size image
Table 1 Data obtained from review of studies on prevalence of VTE patients with COVID-19
Full size table

By analyzing the data of 37 studies, there was a 0.17 prevalence rate of VTE among Covid-19 patients (95% CI = 0.13–0.22, P < 0.0001), and the heterogeneity rate in this study was 98.8% which was statistically significant (P < 0.0001) (Fig. 2).

Fig. 2
figure 2

Prevalence of VTE in patients with COVID-19

Full size image

VTE prevalence in Covid-19 patients by geographical distribution

In studies conducted in Europe, a prevalence rate of 0.23 was calculated for VTE among patients with Covid-19 (95% CI = 0.15–0.32). In studies conducted in the USA, Asia, and Australia, the prevalence was estimated to be 0.093 (95% CI = 0.043–0.16), 0.073 (95% CI = 0.21–0.003), and 0.03 (95% CI = 0.025–0.04), respectively. Statistically significant differences emerged from the study results (P < 0.0001) (Table 2).

Table 2 Prevalence of VTE in Covid-19 patients in different geographical areas
Full size table

Risk factors for VTE prevalence among patients with Covid-19 affecting the VTE incidence among patients with Covid-19

The analysis of 49 studies, the factors affecting the incidence of VTE in Covid-19 patients, was examined; analysis showed that immunodeficiency, history of kidney disease, and history of stroke were significant risk factors with prevalences of 0.52 (95% CI = 0.28–0.98), 0.36 (95% CI = 0.26–0.5), and 2.04 (95% CI = 1.09–3.8), respectively (Table 3).

Table 3 Analysis of VTE risk factors in patients with COVID-19
Full size table

Discussion

A large number of Covid-19 patients develop VTE despite the use of anticoagulants [7, 106]. Timely detection and treatment of VTE in these patients can reduce mortality. Also, using anticoagulants as prophylaxis can be effective [107]. In addition to the risk of thrombotic complications, patients with Covid-19 are also at risk of bleeding, so anticoagulants should be used with caution in these patients [42]. The current study showed average prevalence of VTE in patients with Covid-19 was 17%. Based on the analysis by geographic region, racial differences and genetic factors can affect the occurrence of VTE in patients affected with Covid-19. A history of stroke and cerebrovascular events can be an influential risk factor.

Another meta-analysis study by Kefale B. et al. showed 33% prevalence of thrombotic events in patients with Covid-19 [106]. This investigation revealed that hospitalization in ICU, increased D-dimer levels, and mechanical ventilation are associated with a higher risk of developing thrombotic events. Another study showed that ICU patients were more likely than ward-hospitalized patients to experience major thromboembolism (17.2% versus 12.5%) [108]. This study showed that using a therapeutic dose of anticoagulant is more effective than a prophylactic dose in preventing VTE in all hospitalized patient.

Another meta-analysis study of Zhang R. et al. reported a 13% prevalence of VTE in non-ICU patients and 31% in ICU patients [109]. Severe underlying diseases, inactivity, senescence, and obesity have been reported as risk factors for VTE [110].

Several causes have been proposed to explain hypercoagulability in patients with Covid-19, including systemic inflammation, endothelial damage, and cytokine release that activate coagulation cascades [6, 111, 112]. Studies have shown that thrombosis occurs due to various biological pathways, including endothelial damage, macrophage/monocyte, and neutrophil activation. Researchers have found that prolonged immobility and the formation of antiphospholipid antibodies exacerbate thrombosis [113]. Another study that was conducted on patients undergoing extracorporeal membrane oxygenation (ECMO) showed that 50% of patients who have evidence of pulmonary ischemia do not have visible thrombus in the pulmonary artery. The possible cause of their pulmonary ischemia is immune-mediated microvascular thrombosis [114]. Studies have also investigated the laboratory parameters that indicate the increase in the incidence of VTE, which can be effective in selecting a therapeutic approach for these patients [115]. It is more likely that Covid-19 patients who have increased D-dimer and C-reactive protein (CRP) levels will develop VTE [116]. Fibrinogen level has been increased in hyper coagulopathy [117]. Fibrinogen and D-dimer levels are elevated in inflammatory conditions. Patients at risk for VTE may benefit from prophylactic anticoagulant therapy, and the appropriate anticoagulant should be determined. In a study, high doses of enoxaparin reduced mortality and incidence of VTE but were associated with a greater risk of major bleeding [118]. Another study showed that using a high dose of prophylactic anticoagulant in critically ill Covid-19 patients reduces the risk of thrombotic complications without an increase in the risk of bleeding [119]. It has been found that the risk of thrombosis and peripheral vascular disease in patients receiving moderate prophylactic or therapeutic doses of anticoagulants was similar to that of patients receiving standard prophylactic doses [120].

Studies have also reported an increased risk of arterial thromboses such as myocardial infarction, stroke, splenic infarction, splenic artery thrombosis, limb ischemia, and mesenteric ischemia in coronavirus-infected patients [121, 122]. There is an increased risk of cerebral venous sinus thrombosis in these patients, especially those with neurological symptoms [123].

In Covid-19 patients, various risk factors for VTE were investigated, and since patients were in different phases of the disease and it was not mentioned in the studies, it can affect the outcome. Additionally, VTE may be challenging to diagnose, especially in critically ill patients or those with low consciousness, and diagnostic measures may not be appropriate in some cases. Further studies are recommended to examine the risk factors in more details.

Conclusion

The current study showed a considerable prevalence of VTE in coronavirus-infected patients. According to variety in prevalences of VTE according to geographic areas, it showed that racial differences and genetic factors can affect the occurrence of VTE in these patients. In addition, a history of stroke and cerebrovascular accidents can be a serious risk factor, indicating the need for prophylactic anticoagulant treatment in these patients, but past medical history of respiratory disease, cardiovascular disease, hypertension, diabetes, dyslipidemia, liver disease, malignancy, and smoking is not risk factors of VTE in patients affected with Covid-19. We recommend further research into the underlying pathophysiology and risk factors involved.

Availability of data and materials

Not applicable.

Abbreviations

VTE:

Venous thromboembolism

ACE2:

Angiotensin-converting enzyme2

MOOSE:

Meta-analysis Of Observational Studies in Epidemiology

PRISMA:

Preferred Reporting Items for Systematic Reviews and Meta-Analysis

PTE:

Pulmonary thromboembolism

MeSH:

Medical Subject Headings

ISI:

Institute for Scientific Information

SD:

Standard deviation

BMI:

Body mass index

NOS:

Newcastle-Ottawa scale

RCT:

Randomized controlled trial

ECMO:

Extracorporeal membrane oxygenation

CRP:

C-reactive protein

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Authors and Affiliations

  1. Vascular & Endovascular Surgery, Clinical Research Development Center, Imam Reza Hospital, Kermanshah University of Medical Sciences, Kermanshah, Iran

    Mohammad Reza Sobhiyeh

  2. Department of Epidemiology, School of Health, Kermanshah University of Medical Sciences, Kermanshah, Iran

    Yahya Salimi

  3. Department of General Surgery, Imam Reza Hospital, Kermanshah University of Medical Sciences, Kermanshah, Iran

    Zeinab Tardeh

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  1. Mohammad Reza Sobhiyeh
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MS and ZT acquired the data. YS analyzed data. YS and ZT interpreted the data. MS and ZT drafted the manuscript; MS, YS, and ZT critically revised the manuscript for important intellectual content. MS supervised the study. All authors have read and approved the manuscript.

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Correspondence to Zeinab Tardeh.

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Sobhiyeh, M.R., Salimi, Y. & Tardeh, Z. A systematic review of the venous thromboembolism prevalence and related risk factors in patients with Covid-19. Egypt J Intern Med 35, 54 (2023). https://doi.org/10.1186/s43162-023-00239-8

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