Original ResearchFree Access

Vascular and Interventional Radiology

Lower-extremity Arterial Thrombosis Associated with COVID-19 Is Characterized by Greater Thrombus Burden and Increased Rate of Amputation and Death

Published Online:Jul 16 2020https://doi.org/10.1148/radiol.2020202348

Abstract

Background

During the peak of the coronavirus disease 2019 (COVID-19) pandemic, the authors noted an increase in positive lower-extremity CT angiography examinations in patients who presented with leg ischemia. The goal of this study was to determine whether lower-extremity arterial thrombosis was associated with COVID-19 and whether it was characterized by greater severity in these patients.

Materials and Methods

In this retrospective propensity score–matched study approved by the institutional review board, 16 patients who tested positive for severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and who underwent CT angiography of the lower extremities and 32 patients who tested negative for SARS-CoV-2 observed from January to April 2018, January to April 2019, and January to April 2020 were compared using three scoring systems: two systems including all vessels, with weighting in one system given to more proximal vessels and with weighting in the other system given to more distal vessels, and a third system in which only the common iliac through popliteal arteries were considered. Correlation with presenting symptoms and outcomes was computed. Fisher exact tests were used to compare patients who tested positive for COVID-19 with patients who tested negative for COVID-19 regarding the presence of clots and presenting symptoms. A Mantel-Haenszel test was used to associate outcome of death and/or amputation with COVID-19 adjusted according to history of peripheral vascular disease (PVD).

Results

Sixteen patients with confirmed COVID-19 (70 years ± 14 [standard deviation]; seven women) who underwent CT angiography and 32 propensity score–matched control patients (71 years ± 15; 16 women) were included. All patients with COVID-19 (100%, 95% confidence interval [CI]: 79%, 100%) had at least one thrombus, and only 69% of control patients (95% CI: 50%, 84%) had thrombi (P = .02). Ninety-four percent of patients with COVID-19 (95% CI: 70%, 99.8%) had proximal thrombi compared with 47% of control patients (95% CI: 29%, 65%) (P < .001). The mean thrombus score using any of the three scoring systems yielded greater scores in patients with COVID-19 (P < .001). Adjusted for history of PVD, death or limb amputation was more common in patients with COVID-19 (odds ratio = 25; 95% CI: 4.3, 147; P < .001). Patients with COVID-19 who presented with symptoms of leg ischemia only were more likely to avoid amputation or death than patients who also presented with pulmonary or systemic symptoms (P = .001).

Conclusion

Coronavirus disease 2019 is associated with lower-extremity arterial thrombosis characterized by a greater clot burden and a more dire prognosis.

Summary

Patients with coronavirus disease 2019 had lower-extremity arterial thrombosis characterized by a higher clot burden, involvement of proximal lower-extremity arteries, and a worse prognosis compared with control patients.

Key Results

■ All patients with coronavirus disease 2019 (COVID-19) infection who underwent lower-extremity CT angiography had at least one lower-extremity clot (100%), whereas only 69% of control patients had clots (P = .02).
■ The mean clot score for lower-extremity vessels in patients with COVID-19 was greater than that of propensity score–matched controls (P < .001).
■ Adjusted for history of peripheral vascular disease, death or limb amputation was more common in patients with COVID-19 infection (odds ratio = 25; P < .001).

Introduction

Coronavirus disease 2019 (COVID-19) caused by the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is characterized by the respiratory symptoms implicit in the name severe acute respiratory syndrome. Still, with the increasing number of cases, it has also been linked to nonpulmonary targets, including cardiac, gastrointestinal, skin, renal, and neurologic manifestations (1–5). Venous thromboembolism has also been shown to be an important cause of morbidity and mortality in patients with COVID-19, both in the general inpatient and in the intensive care unit (ICU) setting, and even in patients receiving therapeutic anticoagulation (6–8). For example, in one autopsy series, unsuspected deep vein thrombosis was found in the majority of patients with COVID-19, and pulmonary embolism was the cause of death in one-fourth of these patients (9). Arterial thrombosis has also been reported within coronary arteries (6,10) and within the brain (6,11) in patients with COVID-19. There have also been case reports regarding mesenteric (12–14) and aortoiliac (6,12) thrombosis.

In our practice, in a COVID-19 hotspot, where at its peak (April 12, 2020) our hospital system had 1194 inpatients with diagnosed COVID-19, we have observed an increased number of patients presenting with lower-extremity ischemia and extensive arterial thromboses during the current pandemic. These patients typically presented to the emergency department with new symptoms of leg pain, coldness, discoloration, and ulceration, and they underwent lower-extremity CT angiography. Diagnostic work-ups in many of these patients showed them to be positive for the SARS-CoV-2 virus. With growing evidence of coagulopathy or vasculopathy (15) in patients with COVID-19, we investigated whether these cases were also due to COVID-19–related thrombosis. The goal of our study was to determine whether lower-extremity arterial thrombosis is associated with SARS-CoV-2 infection and if differences exist in severity of lower-extremity clot burden in patients who test positive for the virus.

Materials and Methods

Our institutional review board approved this propensity score–matched retrospective cohort study at an urban tertiary care medical center located in an epicenter of the COVID-19 pandemic. The requirement for written informed consent was waived.

Patients

Included in the study are all emergency department and inpatient cases of CT angiography of the abdominal aorta with lower-extremity run-off performed during March–April 2020, identified in the picture archiving and communications system. This study covers the peak 2020 months of the pandemic in the New York City metro region (16). Thirty-eight patients underwent lower-extremity CT angiography. Of these, 10 were not tested for the SARS-CoV-2 virus, 11 tested negative, and one underwent a nondiagnostic CT angiographic examination (Fig 1). The diagnosis in the 16 patients was based on reverse transcription polymerase chain reaction (RT-PCR) test results as follows: nine patients using the Cepheid Xpert Xpress SARS-CoV-2 assay (Cepheid, Sunnyvale, Calif), two patients using the Hologic Panther Fusion real-time RT-PCR SARS-COV-2 assay (Hologic, Marlborough, Mass), two patients using the Abbott RealTime SARS-COV-2 assay (Abbott Molecular, Des Plaines, Ill), and three patients diagnosed outside our hospital system (one at an urgent care clinic, one at an outside hospital, and one at a nursing home) for whom details of the test used were not available.

For control patients, a pool was assembled of all lower-extremity CT angiography performed in emergency department patients and inpatients from January through April 2018 and from January through April 2019 and in those who tested negative for SARS-CoV-2 from January through April 2020, totaling 108 cases. Our institution is not a level 1 trauma center, and all CT angiographic examinations were performed for ischemia. We chose control patients from these time periods in consecutive years to avoid seasonal variation, which has been reported for cardiovascular disease (17,18). To reduce the potential confounding from demographic characteristics that differ between COVID-19 patients and control patients, we used a method similar to propensity matching. We selected a total of 32 control patients from a pool of 108 patients aged 40–95 with 2:1 matching of demographic data. The matching for 15 COVID-cases was conducted with propensity scores using the nearest neighbor method (19). The propensity scores were created by fitting a logistic regression model to the disease status with sex, age, and body mass index as the covariables. For the only COVID-19 case for which body mass index was not available, matching was performed using ethnicity, sex, and age. Among the selected 32 control patients, only two patients who presented in March 2020 were tested for SARS-CoV-2 virus; one tested negative once with the Hologic Panther Fusion real-time RT-PCR SARS-COV-2 assay, and the other tested negative twice with the Cepheid Xpert Xpress SARS-CoV-2 assay.

All CT angiographic examinations were performed with GE LightSpeed VCT 64-slice MDCT scanners (GE Healthcare, Milwaukee, Wis) following injection of 120 mL of Iopamidol 370 at 4–5 mL/second. When multiple examinations were performed of the same patient, only the first diagnostic examination was considered for this analysis. Images from each case were reviewed in consensus by two radiology attending physicians (I.A.G., with fellowship training in body imaging and 14 years of posttraining experience, and M.H.S., with fellowship training in emergency radiology and 9 years of posttraining experience) who were blinded to COVID-19 status. Only initial CT angiography images were used for scoring. Delayed images were available for only one case and were not used.

Case Scoring

To the best of our knowledge, no validated scoring system exists for calculating the arterial clot burden in the lower extremities; therefore, we used three different systems to perform this task. Vessels were categorized into three zones: (a) aortic (thoracic aorta and abdominal aorta), (b) proximal (common iliac arteries, external iliac arteries, common femoral arteries, superficial femoral arteries, and popliteal arteries), and (c) distal (anterior tibial, peroneal, and posterior tibial arteries). Arteries of the foot were not assessed. Complete thrombosis of a single cross-section within the vessel was assigned the full score for that vessel whereas incomplete thrombosis of a vessel was assigned half the value. In the first system (“proximally weighted”), each aortic vessel was given a value of 3, each proximal vessel was given a value of 2, and each distal vessel was given a value of 1. In the second system (“distally weighted”), each aortic vessel was given a value of 1, each proximal vessel was given a value of 2, and each distal vessel was given a value of 3. In the third system (“unweighted, proximal only”), only proximal vessels were considered, and each vessel was given a value of 2.

Imaging evidence of a chronic thrombosis included calcification within the walls and lumen of the vessel, decreased arterial caliber, and presence of collaterals. Previous studies, if available, and clinical notes were used to help determine whether the thrombus was acute or chronic. The availability of previous examination results was similar between the groups; two of 16 patients with COVID-19 (13%) and five of 32 control patients (16%) had previous studies available (P > .99). Acute graft thrombosis was scored equivalent to the size of the vessel that it was replacing (eg, an acutely thrombosed femoral-popliteal graft was scored as 4 as it was spanning 2 vessels, each with a value of 2), whereas a native chronically occluded vessel was scored as 0 (as it was chronic). If no previous studies were available for comparison, occlusion was deemed chronic if the nonenhancing vessel was diminutive in appearance, compared with the contralateral side, and peripherally calcified.

Chart Review

Medical records were reviewed for COVID-19 status (based on RT-PCR testing of nasopharyngeal samples), demographic information (age and sex), socioeconomic status expressed as standard deviations from the New York State mean income based on census tract data (20), laboratory tests, history of PVD, presenting symptoms, ICU stay, and outcomes of death or leg amputation. The diagnostic test used to detect SARS-CoV-2 infection was recorded. SARS-CoV-2 immunoglobulin M or immunoglobulin G antibody testing was not in use during the time of our study. A history of PVD was defined as having had a previous vascular surgical consultation, having had previous testing, or having undergone a procedure because of symptoms of lower-extremity arterial insufficiency. Presenting symptoms were classified as those pertaining to leg ischemia only versus a combination of leg symptoms and additional respiratory or systemic symptoms such as fever, cough, hypoxia, tachypnea, tachycardia, respiratory distress, and/or altered mental status. An ICU stay was considered present if the patient spent any time during the admission in the ICU. The outcome of death or amputation was considered present only if it occurred during the index hospital admission.

Statistical Analysis

We treated the patients with COVID-19 and the control patients as independent observations. Differences in patient characteristics between the two groups were assessed using the Fisher exact test for dichotomous variables and the Welch t test for continuous variables. Fisher exact tests were used to compare the presence and absence of clots in the two groups. Clot scores between SARS-Cov-2 positive and negative groups were compared using a linear regression model with history of PVD as a covariable. Association of serious outcomes (death or amputation) with COVID-19 status was tested using the Mantel-Haenszel test conditional on history of PVD. Association of presenting symptoms of patients with COVID-19 and their outcome was assessed using the Fisher exact test. All statistical analyses were performed using R statistical software (version 3.6; The R Project for Statistical Computing, Vienna, Austria).

Results

Patient Characteristics and Presentation

Tables 1 and 2 show the demographic and clinical characteristics of the two groups. Of the 16 patients with COVID-19, five presented only with complaints of leg pain or discoloration, whereas the other 11 presented with additional systemic or respiratory symptoms (Table 3).

**Table 1: Demographic Variables in Case and Control Patients**

**Table 2: Clinical Variables in Patients with COVID-19 and Control Patients**

**Table 3: Association between Presenting Symptoms and Limb Amputation or Death in Patients with COVID-19**

Presence of Clots and Clot Scores

All sixteen patients with COVID-19 (100%, 95% confidence interval [CI]: 79%, 100%) had at least one clot (Fig 2), while only 22 of 32 patients (69%, 95% CI: 50%, 84%) had at least one clot among the control patients (P = .02). When looking only at clots within the popliteal artery and more proximally, 15 of 16 patients with COVID-19 had clots (94%, 95% CI: 70%, 99.8%), while 15 of 32 control patients (47%, 95% CI: 29%, 65%) had clots (P = .002). Clot scores using the three systems are tabulated in Table 4. Echocardiography was performed in seven of 16 patients with COVID-19 (44%) and in 10 of 22 control patients (45%) (the value 22 represents the number of control patients with leg clots). P >.99 indicated no statistically significant difference in echo performance rate. No examination resulted in the detection of cardiac clots.

CT angiographic images in a 63-year-old woman with coronavirus disease 2019. (a–e) Images through distal abdominal aorta (a), proximal common iliac arteries (b), external iliac arteries (c), popliteal arteries (d), and anterior tibial, posterior tibial, and peroneal arteries (e) demonstrate lack of contrast opacification on left side (arrows). High attenuation along periphery of vessels in a and b corresponds to contrast material rather than calcium. Note that arrows in e point to expected location of vessels. (f) Oblique coronal reformatted CT angiographic image demonstrates clot at aortic bifurcation (arrow). — Figure 2a: CT angiographic images in a 63-year-old woman with coronavirus disease 2019. **(a–e)** Images through distal abdominal aorta (a), proximal common iliac arteries (b), external iliac arteries (c), popliteal arteries (d), and anterior tibial, posterior tibial, and peroneal arteries (e) demonstrate lack of contrast opacification on left side (arrows). High attenuation along periphery of vessels in a and b corresponds to contrast material rather than calcium. Note that arrows in e point to expected location of vessels. **(f)** Oblique coronal reformatted CT angiographic image demonstrates clot at aortic bifurcation (arrow).

**Table 4: Clot Scores Using the Three Scoring Systems**

Treatment and Outcomes

Patients either underwent surgery, anticoagulation (heparin or oral agents), or no treatment (one patient could not receive heparin because of concomitant stroke; two patients received palliative treatment only). Seven of 16 patients with COVID-19 (44%) underwent surgery (three underwent thrombectomy, three others underwent thrombectomy followed by amputation, and one required amputation). Eleven of 32 control patients (34%) underwent surgery (six underwent thrombectomy, two underwent thrombectomy and bypass, two underwent angioplasty, and one underwent bypass). P = .54 indicated no statistically significant difference in surgical intervention between groups.

Table 5 summarizes presence of death or amputation in patients with and without COVID-19. After adjusting for history of PVD using the Mantel-Haenszel method, death or limb amputation was significantly more common in patients with COVID-19 (P < .001). As it is possible that the association between the combined end point of death and amputation was due to an overwhelming contribution from the death end point, we excluded these patients and looked at the association between COVID-19 and amputation alone. We found that even when patients who died were excluded, limb amputation was significantly more common in patients with COVID-19 (P = .02). Patients with COVID-19 who presented with symptoms of limb ischemia only were significantly more likely to avoid amputation or death than patients who presented with symptoms of limb ischemia along with respiratory or systemic symptoms (Table 3) (P = .001).

**Table 5: Summary of Limb Amputation or Death in Patients with COVID-19 and Control Patients Stratified by Presence of PVD**

Discussion

Results of this study are concordant with the growing body of evidence demonstrating an increase in thromboembolic events in patients with coronavirus disease 2019 (COVID-19) (6–9,21). Although venous thromboembolic events in patients with COVID-19 are well recognized, this study demonstrates an association between lower-extremity arterial thromboses and severe acute respiratory syndrome coronavirus 2 infection. Prominent features of this association are not only a high incidence of arterial thrombosis in patients with COVID-19 who present with ischemic leg symptoms (100% of cases in our cohort), but also a large thrombus burden (Table 4) and a high frequency of thromboses involving proximal vessels.

To test our hypothesis of a larger thrombus burden in patients with COVID-19, we needed to design a system to quantify the severity of arterial thrombosis in the lower extremities as, to the best of our knowledge, no such grading system exists. We used three systems to approach this problem. First, using analogy with venous thrombosis grading (22), we created a system (“proximally weighted”) in which larger-capacity vessels (eg, the aorta) were given a higher score than calf vessels that have lower capacity. Second, as it can be argued that thrombosis of the more distal vessels leads to critical ischemia, ultimately resulting in the threat of limb loss, and that more distal vessels therefore need to be assigned higher values, we created a second system (“distally weighted”) in which calf vessels were assigned a higher score than the aorta. However, an inherent limitation of this system, which assigns a higher weighting to distal vessels, is the inability to always accurately differentiate between acute thrombosis or embolism and chronic occlusion in the lower leg due to atherosclerotic plaques and calcifications. In addition, issues with contrast opacification of the distal vessels may exist because of PVD, low cardiac output, or technical issues related to bolus timing, rather than actual occlusion. To mitigate this factor, we used a third system (“unweighted, proximal only”) in which only nonaortic proximal vessels were included, as diagnosis of acute thrombosis usually does not pose difficulty in vessels of larger caliber. All three grading methods yielded concordant statistically significant results that verified our findings (Table 4).

In this study, a significantly increased rate of leg amputation (25%) and death (38%) was found in patients with COVID-19 compared with the control group (3% for both) irrespective of the time elapsed between presentation to the hospital and diagnosis with imaging. A similar high mortality rate (40%) was also shown by Bellosta et al (23) in their cohort of patients presenting with symptoms of acute lower-extremity ischemia and COVID-19 pneumonia. Our case and control groups were well matched for age, sex, body mass index, socioeconomic status, race, ethnicity, and history of smoking. Also, no significant difference existed in the prevalence of preexisting conditions such as PVD, congestive heart failure, diabetes mellitus, hypertension, chronic renal failure, hyperlipidemia, or rate of ICU stay between the two groups. The latter parameter, however, is of uncertain relevance, as during the peak of the pandemic, some patients may have been denied ICU entry because of a bed shortage, or they may not have received ICU-level care because of stresses on staffing (including intensivists, nurses, and respiratory therapists). A greater percentage of patients with COVID-19 were intubated and were documented as having acute respiratory distress syndrome in comparison with the control group; however, this difference did not reach statistical significance.

Among the assessed laboratory tests, statistically significant differences between the two groups were observed in white blood cell count, hematocrit level, and creatinine level (median value), which were mildly elevated in the patients with COVID-19. It is uncertain whether the mildly elevated mean white blood cell value of 13.5 × 10³/μL (13.5 × 10⁹/L) was a symptom of lower-extremity ischemia or an indication of concurrent infection, which would portend a worse outcome. Mild elevation in blood urea nitrogen and creatinine levels (median value) in the patients with COVID-19 seen in conjunction with an elevation in hematocrit may be due to dehydration and volume depletion in these patients, along with associated prerenal azotemia. Dehydration has been proposed as a contributor to venous thromboembolic disease (24); however, the correlation between dehydration and arterial thromboses in adult patients has not been established.

Although the more severe outcomes in patients with COVID-19 may reflect a greater arterial thrombus burden, which may be a marker of increased mortality by itself (25), they can also be attributed to the aggressive nature of severe COVID-19 disease, which has been associated with cytokine storms, fulminant myocarditis (26), and atypical hypercoagulability causing development of thromboses despite patients taking therapeutic doses of anticoagulation (8). Additionally, it is possible that unprecedented stressors on the health care system, particularly in the epicenter of the pandemic at its peak, may have indirectly contributed to these outcomes, for example, by delaying a patient’s presentation following the onset of symptoms (27).

This study also suggests that pulmonary or systemic symptoms accompanying the lower-extremity symptoms for which CT angiography was indicated portend a worse prognosis regarding death and limb amputation. Conversely, a potentially important observation of this study was that if the presenting symptoms were related to the leg only, then amputation or death could be avoided. It is unclear according to our data within what time period from the initial SARS-CoV-2 infection thromboses may set in, but awareness that leg ischemia may be associated with COVID-19 should prompt evaluation and treatment for limb ischemia.

One potential limitation of our study was a relatively small cohort of patients with COVID-19 because for our analysis, we chose patients with COVID-19 who underwent CT angiography of the lower extremities during March and April 2020. However, this choice was dictated by the timing of the peak of disease in our area, for which the leading edge of patients was not tested because of limited testing availability. Indeed, this necessitated exclusion of 10 patients presenting for CT angiography of the lower extremities in early March 2020 from our analysis because they were never tested for SARS-CoV-2 infection. Still, we would expect that this cohort would be one of the larger ones available, as our hospital system has seen approximately 6000 patients with COVID-19 at the time of this writing.

This study demonstrates an association between coronavirus disease 2019 (COVID-19) and lower-extremity arterial thrombosis with a greater thrombus burden characterized by a predilection for proximal arteries. Additionally, the incidence of death and amputation is significantly more common in patients with COVID-19, especially if systemic or respiratory symptoms also exist at presentation. Recognition of lower-extremity ischemia as a symptom or complication of COVID-19 may allow for prompt diagnosis and treatment of this condition.

Disclosures of Conflicts of Interest: I.A.G. disclosed no relevant relationships. K.Y. disclosed no relevant relationships. M.H.S. disclosed no relevant relationships.

Author Contributions

Author contributions: Guarantors of integrity of entire study, I.A.G., M.H.S.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; approval of final version of submitted manuscript, all authors; agrees to ensure any questions related to the work are appropriately resolved, all authors; literature research, I.A.G., M.H.S.; clinical studies, I.A.G., M.H.S.; statistical analysis, K.Y.; and manuscript editing, all authors

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Article History

Received: May 22 2020
Revision requested: May 22 2020
Revision received: July 9 2020
Accepted: July 10 2020
Published online: July 16 2020
Published in print: Nov 2020

Vol. 297, No. 2

Abbreviations

Abbreviations:
CI	confidence interval
COVID-19	coronavirus disease 2019
ICU	intensive care unit
PVD	peripheral vascular disease
RT-PCR	reverse transcription polymerase chain reaction
SARS-CoV-2	severe acute respiratory syndrome coronavirus 2

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