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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