Panamerican Journal of Trauma, Critical Care & Emergency Surgery
Volume 12 | Issue 03 | Year 2023

Descriptive Analysis of Thromboembolic Events in COVID-19 Patients in Qatar

Ahmed F Ramzee1, Ayman El-Menyar2, Mohammad Asim3, Hassan Al-Thani4, Fakhar Shahid5, Areen Fino6, Yaser M Ata7, Hamzah El Baba8, Arun P Nair9, Muna S Al Maslamani10, Ruben Peralta11, Sandro Rizoli12

1,4,12Trauma Surgery Section, Department of Surgery, Hamad Medical Corporation, Doha, Qatar

2Clinical Research, Trauma & Vascular Surgery, Department of Surgery, Hamad Medical Corporation; Department of Clinical Medicine, Weill Cornell Medical College, Doha, Qatar

3Clinical Research, Trauma & Vascular Surgery, Department of Surgery, Hamad Medical Corporation, Doha, Qatar

5,7,8Department of Surgery, Hamad Medical Corporation, Doha, Qatar

6Department of Family Medicine, Hamad Medical Corporation, Doha, Qatar

9,10Communicable Disease Center (CDC), Department of Infectious Diseases, Hamad Medical Corporation, Doha, Qatar

11Trauma Surgery Section, Hamad Medical Corporation, Doha, Qatar; Department of Surgery, Universidad Nacional Pedro Henriquez Urena, Santo Domingo, Dominican Republic

Corresponding Author: Ayman El-Menyar, Clinical Research, Trauma & Vascular Surgery, Department of Surgery, Hamad Medical Corporation; Department of Clinical Medicine, Weill Cornell Medical College, Doha, Qatar, Phone: +974 44396130, e-mail: aymanco65@yahoo.com

Received: 15 June 2023; Accepted: 02 December 2023; Published on: 30 December 2023


Background: Current literature shows an increased risk of thromboembolic events (TEE) with coronavirus disease of 2019 (COVID-19) infection, possibly due to a unique interplay between the virus and the coagulation system.

Materials and methods: A retrospective observational study of all patients with COVID-19 infection in the State of Qatar between February and August 2020 was performed. Analysis of all patients with TEE was carried out to identify other potential inciting factors for TEE.

Results: There were 210 out of 16,903 (1.2%) patients with COVID-19 infection who developed TEE. Myocardial infarction (MI) was the most common event (76.2), with 11% deep vein thrombosis (DVT) and <10% with pulmonary embolism (PE), stroke, and other thrombotic events.

Conclusion: Our study showed a low incidence of TEE compared to current literature. Patients with a previous history of thrombotic events were at a higher risk of developing a second event. Other significant contributing factors may have had a role in the development of TEE in the rest of the group. This questions the current belief that COVID-19 significantly increases the risk of TEE in the healthy population.

How to cite this article: Ramzee FA, El-Menyar A, Asim M, et al. Descriptive Analysis of Thromboembolic Events in COVID-19 Patients in Qatar. Panam J Trauma Crit Care Emerg Surg 2023;12(3):120–130.

Source of support: Nil

Conflict of interest: Dr Sandro Rizoli and Dr Ruben Peralta are associated as the Editorial board members of this journal and this manuscript was subjected to this journal’s standard review procedures, with this peer review handled independently of these Editorial board members and their research group.

Keywords: Coronavirus disease of 2019, Epidemic, Infarction, Infection, Qatar, Thromboembolic


The coronavirus disease of 2019 (COVID-19) pandemic by the novel severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) virus has disrupted the world since December 2019.1 COVID-19 disease ranges from asymptomatic to mild respiratory tract infections to pneumonia and even acute respiratory distress syndrome, shock, and multiorgan failure.2 Several risk factors are known to increase susceptibility to developing a more severe course of illness, including old age, diabetes, chronic kidney disease, obesity, and chronic cardiovascular disease.3

COVID-19 is predominantly a disease of the respiratory system; however, it has the potential to become a multisystem disorder.4 A large number of studies have shown an increased risk of thromboembolic events (TEE) in patients with severe COVID-19 disease, with several recommendations being made on subduing this supposed hypercoagulable state.57 The coagulation derangement in patients with COVID-19 has been linked to the hyperinflammatory response, cytokine storm, and increased platelet activation induced by SARS-CoV-2 viral particles that gain entry into the circulatory system via endothelial angiotensin-converting enzyme 2 receptors, mainly in the lungs.7,8

The pathology of coagulation defects is poorly understood and has been labeled as COVID-19-associated coagulopathy (CAC) owing to differences in other critical illness coagulopathies.59 This has prompted recommendations for prophylactic anticoagulation, regardless of thromboembolism risk assessment in severe cases of COVID-19.10 The National Institute of Health (NIH) recommends the same routine thromboprophylaxis for non-COVID-19 to be applied to COVID-19 patients.11

Most existing literature does not provide detailed background information on patients’ baseline characteristics as well as management interventions during hospitalization for COVID-19 disease, which may have implications for the development of TEE.

In the State of Qatar, COVID-19 response and management are provided by a single centralized healthcare system that sets standards and protocols for all hospitals. During the first wave of COVID-19 (2019–2020), all symptomatic patients were admitted to hospitals managed by the central health system. Asymptomatic patients were placed in quarantine facilities under the purview of the same corporation. This ensured that all patients with COVID-19 infection in the country were monitored and cared for by a single body and according to the same standard of care that was applied to all patients. Given these findings, we set out to study the incidence and describe the characteristics of patients with COVID-19 who developed TEE in Qatar.


This was a retrospective observational study of all consecutive adult patients (≥18 years of age) admitted to the treatment and quarantine centers with COVID-19 infection and who developed thromboembolic complications during the hospital course between February and August 2020. In Qatar, the COVID-19 pandemic management is coordinated by the Hamad Medical Corporation (HMC), which is under the purview of the Ministry of Public Health. Four main hospitals were designated as COVID-19 treatment facilities (Hazm Mebaireek General Hospital, Communicable Disease Center, Mesaieed Hospital, and Ras Laffan Hospital). All quarantine centers were managed under the Communicable Disease Center, which has a centralized database from where the data were retrieved. The study included all COVID-19-positive TEE patients admitted to a regular ward or intensive care unit (ICU). Patients initially admitted for non-COVID-19 conditions and tested positive for COVID-19 infection were transferred to the designated COVID-19 facilities and were also included in our analysis. COVID-19 infections were confirmed by reverse transcription polymerase chain reaction test on a nose/throat swab. Patients were categorized as asymptomatic, mild, severe, and critically ill according to the HMC-CDC protocol. Briefly, COVID-19 was considered mild if there was evidence of lower respiratory disease during clinical assessment or imaging and who have an peripheral oxygen saturation (SpO2) of >94% on room air or at sea level. Severe COVID-19 cases referred to those who had SpO2 of <94% on room air or at sea level, a ratio of arterial partial pressure of oxygen to fraction of inspired oxygen (partial pressure of oxygen/fraction of inspired oxygen) <300 mm Hg, a respiratory rate >30 breaths/minute, or lung infiltrates >50%. COVID-19-associated pneumonia with respiratory failure, septic shock, and/or multiple organ dysfunction were considered critical cases. A routine thromboprophylaxis protocol was the standard of care for all COVID-19 patients, which is outlined in Figure 1.

Fig. 1: Coronavirus disease of 2019 (COVID-19) thromboprophylaxis protocol in Qatar during the first wave

TEE were retrospectively identified by clinical presentation (recorded in the patient’s charts by physicians and nurses), laboratory, and/or radiologic findings. Myocardial infarction (MI) was diagnosed by clinical symptoms, electrocardiogram changes, and elevated troponin T levels above 10 ng/mL. Pulmonary embolism (PE) was detected by computed tomography (CT) pulmonary angiography ordered to investigate deteriorating respiratory status. Deep vein thromboses (DVT) and arterial thromboses by clinical findings and duplex ultrasonography, while stroke was identified by clinical presentation and CT imaging of the brain.

The medical records of all patients were explored to extract pertinent information related to their baseline characteristics, including comorbidities and interventions and procedures relevant to the development of TEE. All medical visits and admissions for 2 years after the COVID-19 infection were reviewed for major events. Detailed information can be found in the Table S1. Ethical approval for this study was obtained from the Institutional Review Board (MRC-01-20-1047) at the Medical Research Center, HMC, Doha, Qatar.

Table S1: Details of individual patients, including major co-risk factors for VTE, VTE prophylaxis, and outcome
S. no. Gender Age Severity of COVID-19 Type of TEE Anatomic location of TEE VTE prophylaxis History of previous VTE History of cancer Access lines Other procedures Outcome (alive or dead) Duration of anticoagulation Follow-up Doppler Last follow-up + outcome Comments
1 Male 42 Severe DVT CFV, SFV, POPV, and PTV Heparin 5000 U, twice daily, then enoxaparin 40 mg daily Yes, at the same site 2 years prior No RA line; IJV None Alive Rivaroxaban for 6 months At 6 months: complete recanalization of CFV + SFV, partial recanalization of POPV + PTV Alive + asymptomatic at 29 months
2 Male 74 Critical DVT + arterial thrombus All deep veins of the upper limb extending to IJV; right RA Enoxaparin 40 mg daily No No Left IJV central line None Death within a month of admission None
3 Female 70 Asymptomatic Arterial thrombus Femoral artery No, presented to the hospital with an ischemic limb No No IJV Embolectomy + four-compartment fasciotomy Death None BMI: 54 ESRD
4 Male 49 Mild PE Segmental branches of the right lower lobar artery Enoxaparin 40 mg daily No No No None Alive Lost to follow-up after 2 months None Lost to follow-up after 2 months
5 Male 35 Asymptomatic PVT PVT None No HCC with lung mets Femoral vein None Death
6 Male 52 Critical DVT CFV Heparin 5000 U twice daily No No ECMO cannulation in the femoral vein None Death Critical COVID-19 presented with severe respiratory failure and cardiac arrest; on long-term ECMO but eventually succumbed
7 Male 66 Mild DVT Axillary + subclavian Enoxaparin 40 mg daily No No No Alive On rivaroxaban; the patient returned to his home country after 5 months None Alive at 5 months The patient had axillary lymphadenopathy with an abscess on the same side; benign.
8 Female 55 Mild DVT–2 months after recovery External iliac, common femoral + superficial femoral. None No Ovarian cancer with metastasis No No Alive Rivaroxaban ongoing At 10 months: partial recanalization Alive at 28 months
9 Male 33 Mild Abdominal vein thrombus PVT, splenic, SMV Enoxaparin 40 mg daily No Metastatic gastric cancer No No Death Death within 1 month of admission
10 Female 63 Mild superficial vein thrombus GSV Enoxaparin 30 mg daily No Metastatic breast cancer No No Alive Enoxaparin 6 weeks Complete resolution in 1 year Alive at 30 months
11 Male 31 Mild Hepatic vein thrombosis Hepatic vein None No No No No Alive Rivaroxaban ongoing Cavernous transformation of the portal vein Alive at 28 months The patient developed PVT postsleeve gastrectomy prior to COVID-19 infection
12 Male 51 Critical DVT SFV, POPV, PTV Dalteparin 7500 U daily No No IJV None Alive No follow-up after discharge No follow up
13 Male 65 Critical DVT Left IJV Dalteparin 5000 U daily No No Left IJV line, kinked, nonfunctional None Death
14 Male 47 Mild Stroke + DVT Right MCA,Right common carotid artery,CFV + SFV Enoxaparin 40 mg daily No No Femoral None Alive Ongoing Neurological deficit; returned to home country after discharge Presented to hospital with a stroke
15 Male 45 Mild DVT Perforator vein Enoxaparin 40 mg daily No No None None Alive Rivaroxaban for 6 months None No follow-up after 6 months
16 Male 58 Severe DVT Subclavian, axillary, and brachial veins; central line-associated pseudoaneurysm with large hematoma Dalteparin 7500 U daily No No IJV Thrombin injection at pseudoaneurysm Alive Ongoing upon discharge None Returned to home country after discharge Compression neuropathy of brachial plexus due to large hematoma/pseudoaneurysm
17 Female 66 Critical DVT IJV Enoxaparin 120 mg daily Yes; same site Gastric cancer Femoral vein None Death Died within a month due to mixed shock and multiorgan failure Morbidly obese
18 Male 55 Mild DVT PVT+ mesenteric vein Enoxaparin 100 mg twice daily No No No None Alive Rivaroxaban ongoing Alive 29 months Multiple comorbidities: AF, CAD, CVA, renal transplant; presented with abdominal pain; DVT diagnosed on admission
19 Female 30 Mild DVT External Iliac + CFV Enoxaparin 40 mg daily No No IJV,RA None Alive IVC filter + enoxaparin: 1 month Complete resolution within 3 months Alive at 30 months
20 Male 30 Critical DVT CFV Enoxaparin 40 mg daily No No IJV,ECMO None Alive Last follow-up: 2 months after discharge
21 Male 58 Critical DVT IJV Enoxaparin 40 mg daily No Leukemia Femoral + IJV None Alive dabigatran, 150 mg Last follow-up: 28 months postdischarge Developed AF after COVID-19
22 Male 27 Mild Superficial vein thrombosis Cephalic Enoxaparin 40 mg daily No Nu None None Alive None None Last follow-up–4 months postdischarge
23 Male 63 Mild Large artery thrombosis Circumferential abdominal aortic aneurysm with thrombus Enoxaparin 40 mg daily No SCC of head and neck None None Died The patient had a GI bleed 6 months: persistent Died 6 months later due to complications of cancer
24 Male 31 Mild DVT Brachial vein Enoxaparin 40 mg daily No Acute leukemia No None Died No due to thrombocytopenia Recovered from COVID-19 but died 4 months later due to complications of cancer
25 Male 86 Critical DVT + PE POPV, PTV, SFV, saddle embolus Enoxaparin 40 mg daily No No No No Died Dabigatran for 6 months None Died 7 months after COVID-19 recovery from massive GI bleeding
26 Male 55 Critical Arterial Splenic artery embolism Dalteparin 5000 U daily History of DVT, PE, and ischemic stroke 3 years prior No IJV No Died after 3 months in ICU Ongoing till death No multiple preexisting cardiac issues: amyloidosis, PE, AF
27 Male 50 Mild Arterial Embolic stroke, splenic artery, bilateral popliteal artery No, as the presentation to the hospital was with ischemia No No No Embolectomy Alive Dabigatran No Presented with ischemic symptoms + AF; the last follow-up 12 months postrecovery
28 Male 65 Critical DVT Bilateral IJV Dalteparin 5000 U daily No No IJV, femoral None Died Ongoing No
29 Male 85 Severe DVT CFV, SFV, POPV, PTV Dalteparin 7500 U daily No No IJV IVC filter Alive No Duplex scan 3 months later: complete resolution Alive at 26 months
30 Male 51 Critical DVT + PE CFV, bilateral segmental PE Enoxaparin 40 mg daily No No ECMO: femoral None Alive Rivaroxaban No follow-up 1 month after recovery
31 Male 74 Mild Arterial SFA, POP, TIB-ANT Dalteparin 5000 U daily No No None CO2 angioplasty + anterior tibial artery angioplasty Died Ongoing till death None Cardiac arrest 3 months later
32 Male 64 Mild DVT CFV, POPV On rivaroxaban Yes, same site 3 months prior to COVID-19 infection No None None Alive Ongoing At 1 year–partial recanalization Alive at 28 months postrecovery
33 Male 40 Critical PE Left lower segmental Enoxaparin 40 mg daily No No ECMO, IJV None Alive Rivaroxaban No Alive at 4 months postrecovery
34 Male 40 Mild DVT Portal vein Enoxaparin 40 mg daily No HCC IJV None Died Ongoing till death No Presented with symptoms of cancer. Died within a month of admission due to cancer-related complications
35 Female 67 Mild DVT External iliac, CFV, SFV, POPVe, and PTV Enoxaparin 40 mg daily No Uterine cancer, metastatic No None Died Enoxaparin 80 mg twice daily Expired 1-year postrecovery from COVID-19 due to cancer complications
36 Male 61 Severe DVT CFV, SFV, POPV, PTV Enoxaparin 40 mg daily No No No None Alive Rivaroxaban Alive at 24 months
37 Male 55 Mild DVT Portal vein Enoxaparin 40 mg daily No HCC No None Alive Rivaroxaban for 6 months None No follow-up after discharge
38 Male 62 Mild DVT Portal vein Enoxaparin 40 mg daily No HCC No No Died Died within 2 months of hospitalization due to cancer complications
39 Female 28 Mild DVT SFJ, SFV, POPV, EIV The patient was on dabigatran Preexisting DVT at same site No No None Alive Dabigatran ongoing No improvement in 24 months Alive at 27 months postrecovery
40 Male 81 Mild DVT SFV The patient presented with DVT No No No No Alive Rivaroxaban–1 year Alive at 17 months postrecovery; the patient was s/p ex. laparotomy, immobile; presented to hospital with DVT
41 Female 41 Mild Arterial Subclavian artery Enoxaparin 40 mg daily No No No Embolectomy Alive Warfarin No Alive at 7 months; history of Takayasu arteritis
42 Female 65 Mild CVA Lacunar infarct No, presented with symptoms No No No No Alive No No Alive at 4 months postdischarge
43 Male 58 Severe DVT Bilateral IJV Enoxaparin 40 mg daily No Leukemia Bilateral IJV No Alive Dabigatran No Alive at 16 months
44 Male 66 Severe CVA Cerebellar Dalteparin 5000 U daily No No IJV No Alive No Alive at 28 months
45 Male 52 Mild CVA Frontoparietal infarct Presented to hospital with CVA symptoms No No No No Alive No Alive at 5 months
46 Male 49 Mild Arterial MI + celiac artery Presented to hospital with symptoms Previous MI No No Pacemaker Alive No Alive at 10 months
47 Male 47 Critical Arterial Femoral On fondaparinux for AF No No ECMO None Alive Rivaroxaban: 6 months Alive at 16 months
48 Male 59 Mild CVA Right MCA Presented with stroke symptoms No No No None Alive Alive at 9 months
49 Male 60 Mild CVA MCA Presented with stroke symptoms No No No No Alive Alive at 29 months
50 Male 54 Mild PE Left lower segmental Enoxaparin 40 mg daily No No Right IJV None Alive No Alive at 6 months postrecovery
51 Male 54 Mild CVA MCA Enoxaparin 60 mg daily No No None None Alive Warfarin Alive at 29 months
52 Female 55 Mild DVT+ PE Left lower lobe; IIV + CFV Presented with symptoms No Metastatic ovarian cancer None None Alive Tenzaparin 6000 U daily Alive at 25 months

AF, atrial fibrillation; BMI, body mass index; CFV, common femoral vein; CVA, cerebrovascular accident; DVT, deep vein thrombosis; EIV, external iliac vein; ESRD, end stage renal disease; GSV, great saphenous vein; HCC, hepatocellular carcinoma; IIV, internal iliac vein; IVC, inferior vena cava; IJV, internal jugular vein; SFV, superficial femoral vein; MCA, middle cerebral artery; MI, myocardial infarction; PE, pulmonary embolism; POPV, popliteal vein; PTV, posterior tibial vein; PVT, portal vein thrombosis; RA, radial artery; SCC, squamous cell carcinoma; SFA, superficial femoral artery; SMV, superior mesenteric vein; TIB-ANT, tibialis anterior

Statistical Analysis

Data were presented using descriptive statistics as proportions, medians (range), or mean (±standard deviation) as appropriate. Data analysis was carried out using the Statistical Package for Social Sciences (SPSS) version 21 (SPSS Inc., Chicago, Illinois, United States of America).


Between February and August 2020, 16,903 patients with COVID-19 infection were identified and treated in the State of Qatar, out of which 210 (1.2%) were diagnosed with thromboembolic complications.

Characteristics of patients with TEE are shown in Table 1. The mean age was 54.1, predominantly male (>80%). A total of 153 out of the 210 patients were of South Asia origin (72%). The mean body mass index was 26.6 kg/m2. Approximately one-fifth were smokers (19%). The majority of patients had a history of MI (80.5%). Mortality in the TEE group was 16.2%.

Table 1: Clinical characteristics, comorbidities, management, and outcomes of COVID-19 patients who developed thromboembolism (n = 210)
Variables Value Variables Value
Age 54.1 ± 13.4 Treatment
Females 23 (11.0%) Enoxaparin 186 (88.6%)
Males 187 (89.0%) Dalteparin 25 (11.9%)
Non-Qatari 191 (91.0%) Rivaroxaban 11 (5.2%)
Qatari 19 (9.0%) Dabigatran 5 (2.4%)
BMI 26.6 ± 5.4 Apixaban 2 (1.0%)
Padua prediction score 4.02 ± 1.78 Heparin 127 (60.5%)
Comorbidities Aspirin 168 (80.0%)
MI 169 (80.5%) No prophylaxis 32 (15.2%)
Hypertension 135 (64.3%) Prophylaxis 178 (84.8%)
Diabetes mellitus 127 (60.5%) Hospital stay (days) 17.1 (0.4–238)
Rheumatological diseases 3 (1.4%) ICU admission 123 (59.7%)
Congestive heart failure 15 (7.1%) ICU length of stay (days) 4.5 (0.2–89.7)
Peripheral vascular disease 2 (1.0%) Mechanical ventilation 58 (69.0%)
Connective tissue disorders 1 (0.5%) Ventilatory days 1 (1–49)
Peptic ulcer disease 5 (2.4%) Death 34 (16.2%)
Chronic kidney disease 31 (14.8%)
Lymphoma 1 (0.5%)
Liver disease 2 (1.0%)
Cancer 11 (5.2%)
AIDS 1 (0.5%)
Smokers 40 (19.0%)
Severity of COVID-19
Asymptomatic 0 (0.0%)
Mild 142 (68.3%)
Moderate 32 (15.4%)
Severe 34 (16.3%)

Thromboprophylaxis coverage, according to the protocol, was high (85%).

Figure 2 shows the distribution of thromboembolic complications. The majority had an acute MI (76.2%). About 80.5% of these patients had a previous history of MI. Eleven percent developed DVT, 3.8% had a stroke, and only 1.9% had PE. The remaining 7.1% had other small to medium vessel thromboses. Table 2 shows the breakdown of non-MI-related TEEs.

Table 2: Distribution of non-MI thromboembolic event cases (n = 52)
Type of events Anatomic location Number of cases
Deep vein thrombosis Lower limbs 15
Upper limbs 4
Portal vein 6
Hepatic vein 1
Internal jugular 5
Superficial vein Cephalic 1
Arterial events Lower limb 3
Upper limb 1
Aortic 1
Splenic 1
Celiac 1
Cerebrovascular accident 8
PE 5

Fig. 2: Distribution of TEE in COVID-19 cases; *others included femoral artery ischemia (n = 2), PVT (n = 5), hepatic vein thrombosis (n = 1), internal jugular vein thrombosis (n = 2), cephalic vein thrombosis (n = 1), circumferential mural thrombosis (n = 1), splenic artery embolism (n = 1), and subclavian artery thrombosis (n = 1)

Considering that the cohort of patients with MI was in a high-risk category for such an event independent of the COVID-19 infection—over 80% had had a previous MI, we attempted to identify non-COVID-19 TEE risk factors in the remaining patients. A total of 52 patients had non-MI TEE and were further analyzed. Of them, 33 patients (63.5%) had other non-COVID-19-related risk factors for TEE. A total of 14 patients were being treated for an active malignancy at the time of the COVID-19 infection. Of these patients, four patients with advanced hepatocellular carcinoma had portal vein thrombosis (PVT). Another five patients had a prior history of significant TEE, and 12 patients had DVT at the site of large bore central access lines, including five patients with femoral vein thrombosis linked to extracorporeal membrane oxygenation (ECMO) catheters. One patient suffered an iatrogenic injury during central line insertion, resulting in a large pseudoaneurysm of the subclavian and axillary veins. Lastly, one patient had axillary and subclavian vein thrombosis secondary to a large abscess in the axilla.

A total of 40 of the 52 patients received thromboprophylaxis doses of anticoagulants during their hospital stay. Nine of the remaining 13 patients were given full anticoagulant doses from admission as part of the TEE management. A total of 16 patients (30%) died, eight of cancer complications. None of the deaths were attributed to any of the TEE.


Given that the COVID-19 pandemic in Qatar was wholly managed by a centralized healthcare system under the Ministry of Public Health with uniform standards and protocols applied to all patients, it allowed us to obtain data on all patients with clinically significant TEE and COVID-19 identified in the country. Current evidence points to a high but variable incidence of TEE associated with COVID-19 disease, ranging from 3 to 85%.5,6 We identified a remarkably low incidence of 1.2% TEE in our patient population. A study from the Netherlands reported an incidence of 49% of thrombotic complications in 184 COVID-19 patients admitted to the ICU despite prophylactic anticoagulation.5 Reports from France identified a high prevalence of thromboembolic complications (20%) in COVID-19 patients admitted to the ICU. Nearly twice that of patients admitted a year before the pandemic.7 A possible explanation for this notable difference in our population could be due to adherence to a single, strict chemical thromboprophylaxis protocol with dose adjusted according to D-dimer levels measured daily at all institutions within the country with the same standardized critical care and COVID-19 management protocols applied to all patients. In a study from China of 81 ICU patients not receiving routine thromboprophylaxis, the incidence of venous thromboembolism (VTE) was 25%.12 Another possibility for this difference could be due to the fact that routine TEE screening tests were not performed, and all investigations for TEE were performed only after clinical suspicion arose; therefore, clinically silent TEE may have been missed. Centers that had routine mandatory TEE screening, particularly in ICU patients, were found to have higher incidences of TEE.6

COVID-19 may result in a complex interplay between the immune and coagulation systems, resulting in a prothrombotic state.13 Multiple mechanisms have been described regarding the process of the development of thrombotic microangiopathy and the development of TEE.4,14,15 Direct endothelial injury followed by a hyperinflammatory response may have a role in the development of a unique coagulopathic effect which is distinct from other coagulopathies such as disseminated intravascular coagulation and sepsis-induced coagulopathy (SIC) and has been termed CAC.4,9 Direct viral injury to the endothelium leads to the release of plasminogen activator, which is probably responsible for the high D-dimer levels noted in multiple studies, along with large von Willebrand factor (vWF) multimers.4 The surge in vWF exceeds the capacity of its cleavage regulators, ADAMTS13 (a disintegrin metalloproteinase), leading to a positive balance of vWF, which contributes to the large increase in microvascular platelet thrombi deposition. The hyperinflammatory response is mediated by an exaggerated complement activation, which results in increased cytokine production (cytokine storm).14,15 An increase in pro-inflammatory cytokines, especially interleukin 6, stimulates tissue factor release by mononuclear cells, resulting in thrombin generation, which compounds the systemic coagulopathic process.4 This has been shown in autopsy studies, which revealed lung injury to involve not only the interstitium as previously thought but the endothelium as well.16,17 These studies demonstrated diffuse alveolar damage as a predominant pattern of lung injury, but more importantly, the majority of specimens showed the presence of platelet–fibrin thrombi, which supports the notion that SARS-CoV-2 promotes a thrombogenic response by direct and cytokine-mediated endothelial injury and platelet and fibrin complex deposition.1518 Despite the multiple theories present, no conclusive evidence links the COVID-19 infection as being solely responsible for an increased thromboembolic risk. Most studies to date fail to comment on other potential confounding factors that may compound the risk of thrombosis. In our cohort, nearly two-thirds of the patients had coexisting disease or iatrogenic factors that could have a role in the TEE.

Most of our patients with TEE (76.2%) suffered an MI; however, nearly 81% of them had a previous MI. These findings are similar to those of a large study (86,742 patients) from Sweden reporting a correlation between COVID-19 and MI. The study showed an increased risk of first MI during the 3 days preceding disease onset until 14 days later. The manuscript hypothesized that COVID-19 was an inciting factor for the development of MI.19 The pathophysiology cannot be fully explained with the existing evidence, except for the stress of acute illness and the potential psychological impact leading to a second event in a vulnerable population.

When considering non-MI-related TEE, the incidence was very low (52 patients). We analyzed the medical records of these patients and noted that the majority (80%) of them had other significant sources that may have put them at an increased risk of developing TEE (Fig. 3). The supplementary table provides a detailed analysis of each patient. About >25% had an active malignancy, with others developing TEE at sites of cannulation. These factors are known risk factors for TEE. Until the completion of this manuscript, the authors were unable to identify studies that investigated other underlying causes for TEE in their patients. This brings into question the actual role of COVID-19 infection in increasing the risk of TEE as opposed to other acute illnesses.

Fig. 3: Proportion of cases with and without co-factors for the development of TEE

Routine chemical thromboprophylaxis for hospitalized patients with COVID-19 is now the standard of care in most centers across the world.11,19 A study by Tang et al. reported a significantly lower 28-day mortality in patients receiving heparin thromboprophylaxis. The study included high-risk patients defined as having a SIC score of >4 or D-dimer levels more than six times the normal level.20 Heparin and its related products are anticoagulants but also have anti-inflammatory properties.21 Whether such anti-inflammatory properties have a role in TEE prevention is unknown.

Evidence is also conflicting with regard to administering therapeutic (full anticoagulation) or prophylactic doses of anticoagulants in patients with COVID-19. The current NIH guidelines for COVID-19 hospitalized patients recommend prophylactic doses of low-molecular-weight heparin (LMWH) or unfractionated heparin (UFH), as used in non-COVID-19 settings while discouraging full anticoagulation even in high-risk patients.11 There is also insufficient data to recommend routine screening for TEE, regardless of the lab coagulation parameters.11 A randomized controlled trial of 1,191 patients from Brazil compared therapeutic vs prophylactic anticoagulation in COVID-19 patients. Patients were randomly assigned to rivaroxaban, if clinically stable or subcutaneous LMWH/intravenous UFH if unstable and were compared to prophylactic doses of LMWH/UFH. There was no difference in mortality, duration of hospitalization, or duration of supplemental oxygenation. The study, however, reported a significant increase in major bleeding in patients receiving therapeutic doses of anticoagulants (8 vs 2%, p = 0.001).19

Ethnic disparities in the incidence of TEE in the general population are well known. Higher rates are reported in African Americans, while the lowest are among Asians. Still, no evidence-based recommendations can presently be made regarding thromboprophylaxis in different ethnic groups.22 Most TEE patients in the present study were originally coming from the South Asian region, reflecting the structural distribution of the population in Qatar.

Study Limitations

While the present analysis could be done in the entire population of a country due to the existence of a centralized healthcare system, it is possible that patients admitted to other health facilities may have been missed. However, even considering this possibility, the number of such patients was certainly small. Another limitation is that all TEE investigations were only ordered for patients based on clinical suspicion. While this pragmatic approach may have discarded clinically insignificant TEE, it may also have excluded patients who were not investigated for TEE.


The present study analyzed the COVID-19 disease over a 6-month period in 2020 (first wave). In comparison to many recent studies, we found a low prevalence of TEE of 1.2%. Acute MI was the most common TEE, compared to DVT, PE, stroke, and others. Despite the limitations, the present study questions a major contribution of COVID-19 infection in TEE beyond that expected for other similar infections or critical illnesses. The study findings raise attention to patients with major thrombotic risk factors, like cancer or previous thrombotic vent.


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