key: cord-339695-3ij5pjjy
authors: Nopp, Stephan; Moik, Florian; Jilma, Bernd; Pabinger, Ingrid; Ay, Cihan
title: Risk of venous thromboembolism in patients with COVID‐19: A systematic review and meta‐analysis
date: 2020-09-25
journal: Res Pract Thromb Haemost
DOI: 10.1002/rth2.12439
sha: 
doc_id: 339695
cord_uid: 3ij5pjjy

BACKGROUND: Venous thromboembolism (VTE) is frequently observed in patients with coronavirus disease 2019 (COVID‐19). However, reported VTE‐rates differ substantially. OBJECTIVES: We aimed at evaluating available data and estimating the prevalence of VTE in COVID‐19 patients. METHODS: We conducted a systematic literature search (MEDLINE, EMBASE, WHO COVID‐19 database) to identify studies reporting VTE‐rates in COVID‐19 patients. Studies with suspected high risk of bias were excluded from quantitative synthesis. Pooled outcome rates were obtained within a random effects meta‐analysis. Subgroup analyses were performed for different settings (intensive care unit (ICU) vs. non‐ICU hospitalization and screening vs. no screening) and the association of D‐dimer levels and VTE‐risk was explored. RESULTS: Eighty‐six studies (33,970 patients) were identified and 66 (28,173 patients, mean age: 62.6 years, 60% men, 20% ICU‐patients) were included in quantitative analysis. The overall VTE‐prevalence estimate was 14.1% (95%CI 11.6‐16.9), 40.3% (95%CI 27.0‐54.3) with ultrasound‐screening and 9.5% (95%CI 7.5‐11.7) without screening. Subgroup analysis revealed high heterogeneity, with a VTE‐prevalence of 7.9% (95%CI 5.1‐11.2) in non‐ICU and 22.7% (95%CI 18.1‐27.6) in ICU patients. Prevalence of pulmonary embolism (PE) in non‐ICU and ICU patients was 3.5% (95%CI 2.2‐5.1) and 13.7% (95%CI 10.0‐17.9). Patients developing VTE had higher D‐dimer levels (weighted mean difference 3.26 µg/ml (95%CI 2.76‐3.77) than non‐VTE patients. CONCLUSION: VTE occurs in 22.7% of patients with COVID‐19 in the ICU, but VTE risk is also increased in non‐ICU hospitalized patients. Patients developing VTE had higher D‐dimer levels. Studies evaluating thromboprophylaxis strategies in patients with COVID‐19 are needed to improve prevention of VTE.

The coronavirus disease 2019 , caused by the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and formally declared a pandemic by the World Health Organization (WHO) in March 2020, is an infectious disease with a global impact on public health. It affects primarily the respiratory system, however, involvement of other organ systems may occur, especially with increasing severity of the disease. The high inflammatory burden associated with COVID-19 and inflammation in the vascular system can also result in cardiovascular complications with a variety of clinical presentations. [1] [2] [3] Early studies already reported on coagulation abnormalities and coagulopathy with a rather prothrombotic phenotype in patients with 5] With the better understanding of COVID-19 and its clinical course, venous thromboembolism (VTE), a disease entity covering pulmonary embolism (PE) and deep vein thrombosis (DVT), has been recognized as a particular complication of the disease.

Initial studies have found alarmingly high rates of PE in patients with severe COVID-19 treated at intensive care units (ICU), reporting VTE incidences of up to 50%. [6] In response to the clinical challenges and the absence of high-quality evidence, experts groups and scientific societies have released guidance statements to address questions concerning diagnosis, prevention, and treatment of VTE in patients with COVID-19 which suggest the broad application of thromboprophylaxis in patients with severe COVID-19 in the absence of high bleeding risk. [7, 8] In several studies of different design, size, and quality, rates of VTE in patients with COVID-19 have been reported. However, a definitive and robust estimate of the VTE risk in patients with COVID-19 is currently not available as of the high variability of reported rates. Therefore, the true underlying burden of VTE in COVID-19 patients is still not fully understood. In the light of the ever-growing infection rates worldwide and the clinical challenges in patient management, understanding of the true frequency of VTE in COVID-19 is important and may help to support clinical decision making.

We conducted a systematic review of the literature and meta-analysis of available data to determine the prevalence of VTE in patients with COVID-19. Our aim was to provide an overall estimate of VTE by aggregating reported rates and to thoroughly Accepted Article explore differences in the VTE prevalence according to study design and the health care setting, which may account for the high degree of heterogeneity in reported rates. This article is protected by copyright. All rights reserved

We conducted a systematic review of the literature and meta-analysis of published data on the prevalence of VTE in patients with COVID-19. The study protocol was prepared prior to the initiation of the literature research according to the Preferred Reporting Items for Systematic review and Meta-analysis Protocols (PRISMA-P) 2015 [9] and submitted to PROSEPERO (International prospective register of systematic reviews) on June 11 th , 2020 (protocol-ID: CRD42020191652). The study was conducted according to the "Preferred Reporting Items for Systematic Reviews and Meta-Analyses" (PRISMA) and the guidance for reporting meta-analysis of observational studies in epidemiology (MOOSE) . [10, 11] 

Full-text articles, letters, brief reports, editorials, and correspondences published in 2019 or 2020 with available title and abstract in English were eligible for inclusion.

Inclusion criteria comprised studies reporting on patients with objectively confirmed COVID-19 in combination with reporting rates of VTE as outcome of the study (DVT and/or PE). Study designs eligible for inclusion were cohort studies (prospective and retrospective), cross-sectional studies, and interventional studies with VTE reported as an outcome or adverse event. Study designs that did not allow prevalence estimates such as case reports and case-series including autopsy studies were excluded.

We systematically searched EMBASE, MEDLINE, and the WHO COVID-19 research database with distinct predefined search algorithms to identify relevant publications. The exact search protocol is available in the Supplementary Methods.

Search for additional studies not identified by the search criteria (e.g. due to pre-print status) was conducted by inquiring databases of pre-print servers (medRxiv) and by manual research of relevant journals. Publications in pre-print status were only eligible if they had undergone full peer-review at the date of literature research. Duplicate search

This article is protected by copyright. All rights reserved results were excluded prior to eligibility screening. Two researchers (SN, FM) screened title and abstract of the identified studies and potentially eligible studies underwent fulltext evaluation. The inclusion of a study was based on the consensus of its suitability by the two researchers. Where consensus opinion could not be reached, a third reviewer was consulted to make the final decision (CA). All three literature researchers are medical doctors with a thorough research background in the field of thrombosis. The most recent literature research was conducted on August 26 th , 2020. Figure 1 displays the process of study identification following a PRISMA flow-diagram.

Studies that fulfilled the predefined inclusion criteria and did not meet any exclusion criteria were subjected to data extraction. In the case of multiple studies reporting on the same patient cohort, results were merged and considered only once. Data extraction of pre-defined baseline and outcome variables was performed. These included methodological specifics of the studies (study design, health care setting), clinical information of the study population (demographics, comorbidities, disease severity, use of pharmacological thromboprophylaxis, ultrasound screening, and D-dimer levels), and outcome specifics (definition, type, and rate of VTE). The full list of extracted variables is provided in the Supplementary Methods. All data were independently extracted from eligible studies by two authors (SN, FM) to ensure data reliability, with inconsistencies resolved by discussion with a third author (CA).

Methodology of identified studies was assessed independently by two researchers (FM & SN) . Risk of bias of included studies was independently rated with a validated tool for assessing studies reporting prevalence data (Joanna Briggs Institute Critical Appraisal Checklist; Supplementary Appendix). [12] This tool consists of 9 categories each classifying the study as low risk of bias, high risk of bias, or unclear. Subsequently, an overall evaluation based on these categories was derived. Studies with suspected high risk of bias were excluded from the subsequent quantitative data synthesis. Potential

This article is protected by copyright. All rights reserved publication bias was assessed graphically within a Funnel-plot, plotting the prevalence estimate of VTE against its' standard error (Supplementary Figure S1A&B) .

The primary outcome of the present meta-analysis is VTE, defined as DVT (including catheter-related thrombosis), PE, or the composite of both, as defined within the respective study. Thrombotic occlusions of mechanical components of extracorporeal devices such as dialysis machines or ECMO devices were not counted as outcome event. The prevalence estimate of the primary outcome is reported stratified by the use of systematic ultrasound screening for thrombosis in the respective studies.

Secondary outcomes included (i) the pooled prevalence of VTE (excluding studies only reporting isolated PE or isolated DVT rates), (ii) the pooled rate of PE, and (iii) the pooled rate of DVT. Outcomes of the secondary analyses were reported stratified for ICU patients and non-ICU hospitalized patients at study baseline and by the performance of DVT screening. The ICU cohort comprised patients admitted to the ICU, or alternatively those who were defined as being critically ill, or in need of mechanical ventilation at baseline. Further, an exploratory analysis of differences between baseline levels of Ddimer between patients experiencing VTE and those who did not was conducted.

Outcome definitions throughout the different studies were varying. Some studies reported pure incidence, while others reported prevalence, e.g. including patients who have been admitted due to VTE and COVID-19. In this systematic review, we have decided to aggregate the proportion of patients, who have been diagnosed with VTE as reported in the included studies.

All statistical analyses were performed with the commercially available package STATA 15.0 (Stata Corp., Houston, TX, USA). Summary statistics were aggregated from included studies. Pooled prevalence of outcome variables was estimated by aggregating study results within a random-effects meta-analysis utilizing the STATA package

This article is protected by copyright. All rights reserved metaprop.

[13] The Freeman-Tukey double arcsine transformation was utilized to normalize variance, and 95% confidence intervals (CI) were estimated by the score method. Heterogeneity of included studies is reported by I 2 as a measure of betweenstudy variability beyond random variation. To explore differences in baseline D-dimer between VTE and non-VTE patients, mean D-dimer levels and corresponding standard deviation were calculated from reported median, interquartile range (IQR) and sample size according to Wan et al. [14] Weighted mean differences (WMD) in baseline D-dimer levels were calculated within a pooled-analysis weighted by corresponding sample sizes.

Lastly, differences in VTE risk according to sex and comorbidities was explored within a random effects meta-analysis utilizing the Mantel-Haenszel procedure.

We identified 2018 records upon literature research after the removal of duplicates. Title and abstract of these identified studies were screened for conformity with our predefined in-and exclusion criteria and 86 records were subsequently included in the full-text evaluation. From those, 66 studies were included in the qualitative data synthesis. Figure 1 displays the screening and selection process, and the reasons for excluding studies.

Pooled summary characteristics of the 86 eligible studies reporting on VTE in COVID-19 patients are displayed in Table 1 

This article is protected by copyright. All rights reserved A comprehensive summary of each study including the respective study design, demographics, thromboprophylaxis strategy, and outcome rates is presented in Tables S1&2.

Pooled patient characteristics and comorbidity data are displayed in Table 2 . The overall weighted mean age of patients was 62.6 years (standard deviation [SD] 3.8) and 60% were male. Weighted mean age of patients in ICU-only studies was 62.6 years (SD 2.9) and 71.3% were male.

Risk of publication bias was evaluated separately for studies on non-ICU hospitalized and ICU patients to enhance interpretability. Upon visual inspection of the Funnel plots, no indication for publication bias was detected, with outliers in the distribution being explained by differences in ultrasound screening strategies. (Figures S1A&B) Secondly, we conducted an exploration of potential time-dependencies in VTE rates of published studies suggesting a decrease of VTE rates over time upon visual inspection and fitting a regression line of the VTE rate and the last patient inclusion date of each respective study. (Figure S2) Thirdly, a methodological assessment of included studies was conducted in order to evaluate the risk of underlying bias regarding the reported rate of VTE. Importantly, this evaluation is not to be regarded as a general evaluation of quality and goodness of included studies but rather an evaluation of the generalizability of reported VTE rates.

In our quality assessment, low risk of bias was attributed to our identified studies in median in 7 of 9 categories (range: 3-9, maximum: low risk of bias in all 9 categories).

The results of our structured methodological assessment of all 86 studies are presented in Table S3 . In consensus among the 3 reviewers, 20 studies were excluded from quantitative synthesis upon a strong suspicion of bias in the structured assessment.

Reasons for exclusion include selection bias (19 studies), reporting/information bias (1 study), and lack of background information on setting and outcomes (1 study). Therefore, the 66 remaining studies (including 43 studies reporting on ICU patients and 43 studies

This article is protected by copyright. All rights reserved reporting on non-ICU hospitalized patients) were included in quantitative data synthesis.

[6, 16-81]

After excluding studies with a high risk of underlying bias, quantitative results from 66 studies were aggregated within a meta-analysis, including 28,173 patients (1, Figure 2 shows a Forrest plot of VTE rates, together with information on health care setting, the performance of screening and outcome definition of respective studies.

The rates of VTE within our primary analysis strongly differed between studies, depending on the specifics of the study setting, design, and outcome definition. Therefore, in order to further explore heterogeneity of the reported VTE rates, we conducted detailed subgroup analyses based on the health care setting (non-ICU hospitalized vs. ICU patients), and the performance of DVT screening (screening vs. no screening). In addition, within these subgroup analyses, we have separately estimated rates of VTE, PE, and DVT. 

Available baseline characteristics of patients with VTE compared to those without VTE were aggregated and analyzed weighted by sample size of the respective study (Table 4) . Mean weighted age of VTE and non-VTE patients was similar, with a mean age of 63.3 years (SD 3.9) and 63.4 years (SD 2.8), respectively. Men were 1.5 times more likely to develop VTE (95%CI: 1.22-1.72), while comorbidities did not differ between the two groups.

D-dimer levels at baseline were available in 21 studies, including 6,633 patients. Patients developing VTE had higher baseline D-dimer levels compared to those without VTE (weighted mean D-dimer levels: 5.18 µg/ml (SD 2.59) vs. 1.13 µg/ml (SD 0.95)) with a WMD of 3.26 µg/ml ([95%CI: 2.76-3.77], p < 0.001; I²: 87.3%). (Figure 3) 

This article is protected by copyright. All rights reserved

In this systematic review and meta-analysis, data from studies reporting on rates of VTE in patients with COVID-19 were aggregated to estimate the prevalence of VTE.

We found that the burden of VTE associated with COVID-19 is substantial, with an overall VTE prevalence estimate of 14.1% across all identified studies. However, rates of VTE varied across different health care settings (ICU vs. non-ICU hospitalized patients), depending on whether systematic screening was performed or not, and on outcome definitions in the selected studies. In subgroup analysis, rates of VTE ranged from 5.5% in non-ICU hospitalized patients without ultrasound screening to 45.6% in ICU patients undergoing screening strategies. Since no PE screening was performed, the PE prevalence of 3.5% in non-ICU hospitalized patients and 13.7% in ICU patients might provide a robust estimate and strongly highlights the high risk of VTE in patients with COVID-19, especially in those requiring intensive medical care.

It is known from large clinical trials in critically ill patients with various underlying diseases that the rate of VTE in the ICU setting is elevated, with VTE rates ranging from 5 to 15%. [82] [83] [84] [85] [86] Higher VTE rates in COVID-19 patients in the ICU and also non-ICU 

This article is protected by copyright. All rights reserved Interestingly, autopsy studies in COVID-19 patients revealed severe endothelial injury, endotheliitis, increased angiogenesis, and widespread vascular thrombosis with microangiopathy and occlusion of alveolar capillaries. [1, 2, [90] [91] [92] Based on such findings, the aetiology of the increased PE rates reported in COVID-19 patients has been discussed and two not mutually exclusive pathomechanisms have been proposed. On the one hand, it has been suggested that in-situ pulmonary thrombi, which develop on the basis of diffuse alveolar and local vascular damage, microangiopathy, and inflammation in the pulmonary circulation triggered by the virus, rather than "classical" PE itself may contribute to the high prevalence of PE observed in patients with On the other hand, DVT rates of up to 90% in studies, where ultrasound screening was performed in ICU patients, support the hypothesis of embolism originating from peripheral thrombosis rather than pulmonary in-situ thrombosis largely contributes to the substantial burden of pulmonary artery occlusion observed in patients with COVID-19. However, the exact role, data on frequency, and clinical consequences of in-situ pulmonary thrombosis in COVID-19 need further investigations.

We believe that our meta-analysis is representative of COVID-19 patients requiring hospitalization, as our systematic review confirmed the previously reported sex differences in COVID-19 patients (higher proportion of men among more severe disease).

[98] The sex differences further increased among patients admitted to the ICU suggesting that men were more likely to suffer from greater disease severity than women.

[99] Correspondingly, men were at higher risk to develop VTE, but we observed no association between comorbidities and risk of VTE. Interestingly, age did not differ between the groups. This suggests that in contrast to the general population, age did not contribute to the VTE risk in COVID-19 patients. [100] Similar results have been reported for VTE risk in patients with cancer suggesting that the high VTE baseline risk of the underlying disease overwhelms general risk factors such as age. [101] Furthermore, explorative analysis has revealed that D-dimer levels were higher in patients developing VTE compared to those who remained free from a VTE event.

Our findings support guidance statements from experts and scientific societies which suggest that thromboprophylaxis is a key element in the medical care of patients with COVID-19, especially in those with severe illness. [7, 8, [102] [103] [104] However, VTE

This article is protected by copyright. All rights reserved occurred in many patients despite the use of thromboprophylaxis, and even patients with therapeutic anticoagulation developed VTE. Therefore, the ideal anticoagulation approach to reduce the high risk of VTE in patients with COVID-19 needs to be established. Further, the observed higher baseline D-dimer levels in patients who had VTE strengthens the idea that D-dimer-guided thromboprophylaxis strategies should be evaluated in prospective randomized-controlled trials.

The main limitation of our meta-analysis is the high heterogeneity of included studies with regard to design, clinical setting, local practice (e.g. with respect to thromboprophylaxis strategies), and consequently highly variable event rates.

Additionally, the disproportionate number of ICU studies with higher VTE rates than the general ward population may confound the overall estimation of VTE prevalence in patients with COVID-19. To address this issue, we aimed at thoroughly describing the respective clinical settings and provide subgroup analysis, e.g. ICU vs. non-ICU hospitalized patients or according to diagnostic approaches (studies with screening vs.

no screening for DVT) to provide a more precise estimate of VTE rates. Further, early reports of high VTE rates in patients with COVID-19 might have led to the implementation of more specific and intensive thromboprophylaxis approaches over time, which might have confounded the outcomes in subsequently conducted studies. We have analyzed studies according to the date of the last patient recruitment and visual inspection reveals a decrease of VTE rates of reported studies over time ( Figure S2) . We also provided data on thromboprophylaxis modalities for the respective studies to allow a better interpretation of differences observed in the studies. However, the generalizability of the results of our systematic review and meta-analysis still needs to be interpreted with caution, because only data from patients in North America, Europe, and Asia were available and included in the meta-analysis. Upon visual inspection, VTE rates across continents and countries seem to be mainly related to between-study heterogeneity with respect to study design, clinical setting, and local clinical practice with regard to thromboprophylaxis ( Figure S4) .

Given the high mortality especially in ICU patients with COVID-19, competing risk of death might lead to an underdiagnosis of VTE. Further, the concern of restricting the use of imaging to avoid disease exposure to healthcare worker might further lead to

This article is protected by copyright. All rights reserved false-low rates of VTE in patients with COVID-19. These uncontrollable factors in a study level analysis should be considered upon interpreting and generalizing our findings. Also, the practice of avoiding imaging due to concerns about healthcare worker exposure should be critically reviewed given the risk of underdiagnosis and consequently undertreatment of patients.

Furthermore, exploratory analysis of D-dimer levels between patients developing VTE and those who did not is limited by the lack of patient-level data and the inability to adjust for between assay variability. Therefore, this exploration should be interpreted with appropriate caution and regarded as hypothesis generating.

Lastly, there is some evidence that non-hospitalized COVID-19 patients are at increased risk of developing VTE as well. [105] As of the unavailability of sufficient data within our meta-analysis, we were unable to provide prevalence estimates for this population of patients and our findings are therefore not representative for the outpatient setting of COVID-19.

In summary, we found a high prevalence of VTE in patients with COVID-19 in hospitalized non-ICU patients, and especially high VTE rates in those being critically ill and requiring intensive medical care. There is a clinical need for further research to better understand the risk and prevent VTE in patients with COVID-19. These findings support the broad use of thromboprophylaxis, specifically in ICU patients. Future randomized clinical trials are needed to assess whether patients with COVID-19 may benefit from an intensified anticoagulation approach compared to standard thromboprophylaxis or whether a biomarker-based personalized thromboprophylaxis regimen reduces the high prevalence of VTE in patients with COVID-19.

This article is protected by copyright. All rights reserved Addendum Author contributions: S. Nopp and F. Moik contributed to study design, data collection, data interpretation, statistical analysis, and drafting of the manuscript. C. Ay contributed to study design, data interpretation, and critical review of the manuscript. I. Pabinger contributed to data interpretation and critical review of the manuscript. S. Nopp, F. Moik, C. Ay are the guarantor of this work and, as such, had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. All authors have read the manuscript and approved its submission. 

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/Total (%) of patients No./Total (%) of ICU

Dyslipidaemia 2,993

ICU, intensive care unit

This study was supported by research funding from the Austrian Science Fund (FWF)

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