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Table 2 Summary of cohort studies reporting the epidemiology and outcome of thromboembolic complications in patients with COVID-19

From: Pulmonary embolism in patients with coronavirus disease-2019 (COVID-19) pneumonia: a narrative review

Authors, year Country Design Number of patients Incidence of PE Remarks
Grillet et al. France [29] Retrospective study
SARS-CoV-2 according to + ve RT-PCR or high clinical suspicion
SARS-CoV-2 + ve: 2003 pts
Hosp. adm..: 280 pts
CTA performed: 100 pts
23% (among patients with CTA)
8.9% (among hosp. admissions)
1.1% (among all COVID-19 + ve pts)
Radiologic study, no clinical correlates
Average time to CTA: 12 days
PE pts.: ICU admissions, 74%, MV: 65%
No differences in comorbidities between PE and no PE
Selection bias (only severe cases/clinical deterioration with CTA)
Leonard-Lorant et al. France [30] Retrospective study
2 French hospitals
SARS-CoV-2 + ve: 961 pts
COVID-19 with CTA: 106 pts (97 + ve RT-PCR, 9 high clinical suspicion)
30% (among patients with CTA)
3.4% (among SARS-CoV-2 + ve pts)
PE pts.: ICU admissions, 75%
PE: 22% main PA, 34% lobar, 28% segmental, 16% subsegmental
No differences in comorbidities between PE and no PE
Selection bias (only severe cases/clinical deterioration with CTA)
d-Dimer levels associated with PE
Helms et al. France [31] Prospective cohort
4 ICUs in 2 hospitals
150 pts 16.7% Short follow-up in some patients (7 days)
PE mostly men (24/25, mean age 62 years old)
PE: 36% main PA, 32% lobar, 20% segmental and 12% subsegmental
PE: detected at a median of 5.5 days after ICU admission
Thromboembolic events more common in COVID-19 ARDS compared to historic ARDS cohort
All patients received at least standard dose thromboprophylaxis
Klok et al. Netherlands* [32] Retrospective cohort
ICUs in 3 hospitals
184 pts 13.6% 31% thrombotic complications
Age and coagulopathy were independent predictors of thrombotic complications
Median duration of follow-up per patient was 7 days
All patients received at least standard doses thromboprophylaxis
Lodigiani et al. Italy [33] Retrospective single-center cohort 388 pts (61 ICU pts) 2.6% overall
4.2% (of 48 closed ICU cases)
Thromboprophylaxis was used in 100% of ICU patients and 75% of those on the general ward
Incidence may have been highly under-estimated due to the low number of specific imaging tests performed
Llitjos et al. France [34] Retrospective cohort
2 ICUs
26 pts 23% Duplex ultrasound performed as standard of care
31% (n = 8) of prophylactic anticoagulation and 69% (n = 18) of therapeutic anticoagulation
Poissy et al. France [35] Retrospective cohort
ICU
107 pts 20.6% PE occurred within a median 6 days after ICU admission
Despite a similar severity on admission to the ICU, the frequency of PE in COVID-19 patients was twice higher than the frequency in the control period and in 40 influenza patients
All patients received at least standard doses thromboprophylaxis
Low number of associated DVTs
d-Dimer levels, plasma factor VIII activity, and factor Willebrand antigen levels were associated with a greater PE risk
Beun et al. Netherlands [36] Retrospective cohort
ICU
75 pts 26.6% High-dose UFH of more than 35,000 IU/day reported in 4 patients with PE due to heparin resistance
Factor VIII, fibrinogen, and d-dimer levels were elevated, while almost all of the antithrombin levels were in the normal range in all patients
Middeldorp et al. Netherlands [37] Retrospective single-center cohort
COVID-19 according to +ve RT-PCR or high clinical suspicion
198 pts (75 ICU) 6.6% overall
15% ICU
All patients received at least standard doses thromboprophylaxis
Median follow-up duration was 15 days in ICU patients and 4 days in ward patients
PE: 8% central, 77% segmental, 15% subsegmental
High d-dimer levels, low lymphocytic count associated with thromboembolic manifestations
Wichmann et al. Germany [38] Autopsy study
COVID-19 according to +ve RT-PCR
12 pts 33.3% DVT in 7 of 12 patients (58%) in whom venous thromboembolism was not suspected before death
In all patients, SARS–CoV-2 RNA was detected in the lung at high concentrations
5 of 12 patients demonstrated high viral RNA titers in the liver, kidney, or heart
Klok et al. Netherlands* [39] Retrospective cohort
- ICUs in 3 hospitals
184 pts 35.3% Increasing follow-up from 7 to 14 days increased the incidence of PE from 13.6 to 35.3%
PE: 70.8 segmental or more proximal arteries, 29.8% subsegmental arteries
Bompard et al. France [40] Retrospective cohort
2 Hospitals
135 pts
COVID-19 + CTA
23.7% Sixty-three pts (47%) were outpatients seen at the emergency department
Fifteen PE were diagnosed in outpatients at initial presentation whereas the remaining 17 were diagnosed in patients who had presented clinical deterioration during hospitalization
PE: 31% proximal, 56% segmental, 13% multiple sub segmental pulmonary arteries
4 patients with PE died (13%) within a median of 26 days
All patients received prophylactic anticoagulation
Thomas et al. UK [41] Retrospective
Single center
63 pts 7.9% PE, 20% sub-segmental, 40% segmental, 20% multiple segmental and 20% in a main pulmonary artery
None of the patients that developed thrombosis had a history of either active cancer or VTE
Very short follow-up (median 8 days)
Poyiadi et al. USA [42] Retrospective
Multicenter
328 pts
COVID-19 + CTA
22% PE: 51% segmental, 31% lobar, 13% central, 5.5% subsegmental
28/122 (23%) of all patients that were on venous thromboprophylaxis developed a PE
Statin therapy associated with lower and BMI > 30 kg/m2, d-dimer of 6 μg/mL with higher risk of developing PE
Galeano-Valle et al. Spain [43] Prospective
Single center
785 pts
COVID-19
1.9% PE: 40% had intermediate–high risk PE and 60% patients had low risk PE
Non-ICU setting, low severity of illness
Stoneham et al. UK [44] Retrospective
2 hospitals
274 pts
Confirmed or highly suspected COVID-19
5.8% White cell count, d-dimer, and fibrinogen associated with the occurrence of VTE in COVID-19 patients
Almost all patients had an abnormal d-dimer result at baseline, defined as a d-dimer > 0.5 µg/mL
Three patients were described to have resistance to anticoagulation
Lax et al. Austria [45] Autopsy study 11 pts 100% Ten of the 11 patients received prophylactic anticoagulant therapy; Venous thromboembolism was not clinically suspected antemortem in any of the patients
Thrombosis of small and mid-sized pulmonary arteries was found in various degrees in all 11 patients and was associated with infarction in 8 patients
  1. ARDS: acute respiratory distress syndrome, CTA: angiographic computed tomography, DVT: deep venous thrombosis, ICU: intensive care unit, PA: pulmonary artery, PE: pulmonary embolism, pts: patients, MV: mechanical ventilation, RT-PCT: real-time reverse transcriptase polymerase chain reaction, UK: United Kingdom
  2. * Same cohort, analysis updated to increase the follow-up period from 7 to 14 days