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COVID-19 and Acute Limb Ischemia: A Systematic Review

Pramod Theetha Kariyanna, Apoorva Jayarangaiah, Anahat Kaur, Amog Jayarangaiah, Sushruth Das, Ruchi Yadav, Neema Jayachamarajapura Onkaramurthy, Ashkan Tadayoni, Moro O. Salifu, Isabel M. McFarlane
American Journal of Medical Case Reports. 2021, 9(6), 312-317. DOI: 10.12691/ajmcr-9-6-2
Received February 03, 2021; Revised March 09, 2021; Accepted March 18, 2021

Abstract

The extraordinary prothrombotic manifestations of Coronavirus Disease-2019 (COVID-19), caused by severe acute respiratory syndrome CoV (SARS-CoV-2) virus, presenting as venous and arterial thrombosis have been reported in the literature. The incidence of arterial thrombosis is reported to be 4% in critically ill COVID-19 patients.. Arterial thrombosis in the setting of COVID-19 has been reported to occur in a multitude of organs leading to ischemic strokes, ST-segment elevation myocardial infarction, aortic thrombus and acute limb ischemia. Diffuse endothelial activation, along with aberrant immuno-thrombotic mechanisms have been implicated in the widespread thrombosis occurring in COVID-19 patients. We performed a literature review of 55 reported cases to delineate the clinical characteristics, management patterns and outcomes of patients with COVID-19 who developed complications of acute limb thrombosis and ischemia. Our systematic review revealed that acute limb ischemia had a male predominance, with either hypertension or diabetes mellitus as the most common underlying cardiovascular risk factors. Aortic thrombus was reported in 23.6% of the cases. The majority of the cases involved thrombosis in more than one limb, indicative of a diffuse thrombotic state. The most common artery affected was the left popliteal artery. Upper limb thrombosis occurred in 40% of the cases. Most of the cases (74.5%) were managed with urgent revascularization interventions and anticoagulation. Negative outcomes, including amputations (14.9%) and death (26.5%) occurred at a higher rate in this population, despite the use of standard management.

1. Introduction

Since the spread of severe acute respiratory syndrome CoV (SARS-CoV-2) virus, various manifestations of this novel entity; Coronavirus Disease-2019 (COVID-19) have been reported, including acute respiratory distress syndrome, cytokine storm, multiorgan failure and notably, diffuse venous and arterial thrombosis. The degree of widespread thrombosis reported in COVID-19 has not been previously seen with the SARS-CoV and Middle Eastern respiratory syndrome (MERS) in 2002 and 2012 1. Diffuse organ involvement in SARS-CoV2 is likely due the virus’ high affinity to bind to the human angiotensin-converting enzyme 2 receptor (ACE 2) 2. ACE-2 is widely expressed throughout the body, including the endothelium 3. Direct viral infection and endothelial inflammation is hypothesized to result in the vascular pathologies seen in COVID-19 3. We perform a literature review to delineate the clinical characteristics, management patterns and outcomes of patients with COVID-19 who developed complications of acute limb thrombosis and ischemia 3, 4, 5, 6, 7.

2. Methods

A comprehensive computer-based literature search of English language studies was performed, using PubMed, Google Scholar, CINAHL, Cochrane CENTRAL, and Web of Science databases, to identify the relevant literature from December 2019 to November 2020. Our search keywords, “Covid-19”, “Coronavirus” “acute limb ischemia”, and “acute limb thrombosis” were used to determine cases of patients with Covid-19 infection who experienced stent thrombosis. Relevant cases were selected by reviewing the reference list of each article. All non-English and non-human studies were excluded. Furthermore, all meta-analysis, review articles, and abstracts were excluded from this study. The data regarding demographic information, affected vessel and limb, angiogram findings, surgical and medical management methods and patient outcomes were reviewed and analyzed.

3. Results

A total of 35 papers were found which featured 55 cases [4-41] [Table 1]. Patients’ ages range from 29-83 with the mean age being 58.8 years. Patients were predominantly male (73%). The most common presentation of acute limb ischemia was limb pain in 45.5%. Most patients had at least one cardiovascular risk factor; 27.3% of the patients had hypertension and 23.6% had diabetes mellitus. D-Dimer was elevated in 69.09% of the cases. The majority of the cases (67.3%) presented with more than one affected artery while 32.7% of the cases had only one artery affected. Aortic thrombus was reported in 23.6% of the cases. The most commonly affected artery was L Popliteal artery (21.82%), followed by R popliteal artery (18.18%) and left common iliac artery (18.18%). Upper extremity thrombus were reported in 40% of the cases, most commonly involving brachial artery and radial artery.

  • Table 1. Illustrating patient characteristics and management strategies employed in patients with COVID-19 who presented with acute limb ischemia

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76.4% of the cases presented with unilateral limb involvement. 43.6% of the cases also had complications of respiratory failure. 85.5% received anticoagulation, while 12.7% of the cases also received antiplatelet therapy and 10.9% received thrombolytics (tpa, alteplase). 41 patients (74.5%) underwent emergent revascularization including surgical/catheter based thrombectomy/embolectomy (50.9%), catheter directed thrombolysis (10.9%), angioplasty (7.3%), stent placement (3.6%) and bypass surgery (1.8%). 49 cases reported outcomes. Clinical recovery occurred in 73.4% of the cases and limb amputation resulted in 14.9% of the patients. Death occurred in 26.5% of the reported cases.

4. Discussion

There have been many serious and fatal complications of Coronavirus disease 2019 (COVID-19) affecting various organ systems. In addition to admission to intensive care units and multi-organ failure, laboratory parameters such as elevation of acute phase reactants such as C-reactive protein and ferritin, aberrancy in hematologic parameters such as elevation of D-dimer and thrombocytopenia has also been associated with severity of infection 42. Additionally, the occurrence of thrombosis appears to correlate with severity of illness and elevation of D-Dimer 36.

The incidence of arterial thrombosis is reported to be 4% in critically ill COVID-19 patients, based on a systematic review of literature 43, 44. Arterial thrombosis in COVID-19 patients have been less commonly described. Nevertheless, there are still reports of arterial thrombosis manifesting as ischemic strokes, coronary artery disease, aortic thrombus, acute limb ischemia as well as arterial thrombi in unusual sites resulting in acute mesenteric ischemia and splenic infarct 45, 46. Many pathophysiologic mechanisms have been implicated in the hypercoagulable state which leads to diffuse thrombosis including direct viral-related endothelial injury, leukocyte- and cytokine-mediated platelet activation, unchecked complement activation and more recently, elevated Von Willebrand factor antigen to ADAMTS13 (a disintegrin and metallo-proteinase with a thrombospondin type 1 motif, member 13) activity ratio 47, 48.

In COVID-19 infection, it is unclear which patients will develop arterial thromboembolism, as opposed to the more common presentation of venous thromboembolism. Some risk factors which have been implicated include advanced age and cardiovascular risk factors, however in the setting of severe COVID-19, there are also reports of younger patients without risk factors developing arterial thrombotic manifestations 24.

We attempt to describe the patient and clinical characteristics associated with patients with COVID-19 who present with acute limb ischemia. Consistent with prior reports, there was a male preponderance. Most of the patients had at least one cardiovascular risk factor, with the most predominant being hypertension and diabetes. Only three patients had a prior diagnosis of peripheral vascular disease. This further highlights that the hyper-coagulable state in COVID-19 infection operates via mechanisms independent of atherosclerosis and plaque rupture. In one large prospective study involving 18000 patients, hypertension was identified as an independent risk factor for deep vein thrombosis 49.

Although autopsy reports in COVID-19 patients revealed extensive microvascular thrombosis 50, our review found that aortic thrombus, whether isolated or when present concomitantly with other large vessels, occurred in 13 of the cases.

Laboratory parameters such as D-Dimer, prolongation of PT/PTT and the presence of antiphospholipid antibodies have been implicated as predictive markers of venous and arterial thrombosis 1.

Emergent revascularization along with antiplatelet and anticoagulation are part of the standard management for acute limb ischemia. Lower success rates with revascularization have been reported with COVID-19 associated acute limb ischemia 51. This is likely due to a widespread, ongoing hypercoagulable state. In the patients with acute limb ischemia, post-intervention heparin appeared to provide better outcomes 51.

Additionally, several of the thrombotic events occurred despite the administration of prophylactic anticoagulation. This may be suggestive that prophylactic doses of anticoagulation may not be sufficient to counteract the prothrombotic state. However, there is still a lack of evidence as to how to determine which patients may benefit from therapeutic anticoagulation. Additionally, while most patients are managed on intravenous heparin or subcutaneous LMWH during admission, many patients are discharged on novel anticoagulants. The long-term outcomes of these patients are yet to be determined.

5. Conclusion

COVID-19 confers a hyper-coagulable state which leads to acute limb ischemia. Physicians should maintain a high index of suspicion for the diagnosis of acute limb ischemia, in both upper and lower limbs in patients developing acute limb pain, despite the absence of prior cardiovascular risk factors. Undesirable outcomes, including amputations and death occurred at a higher rate in this population.

Acknowledgements

This work is supported in part by Dr. Moro O. Salifu's efforts through NIH Grant # S21MD012474.

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In article      
 
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In article      View Article  PubMed
 
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In article      View Article
 
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In article      View Article  PubMed
 
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In article      View Article  PubMed
 
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In article      View Article  PubMed
 
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In article      View Article
 
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In article      View Article  PubMed
 
[30]  Van Mecl, Amanda, et al. “A Case of COVID-19-Associated Acute Limb Ischemia.” Chest 158.4 (2020): A550.
In article      View Article  PubMed
 
[31]  Soares, Rafael de Athayde, et al. “COVID-19 diagnosis in a patient with critical limb ischemia: complications and clinical outcomes.” Jornal Vascular Brasileiro 19 (2020).
In article      View Article
 
[32]  Veerasuri, Sowmya, et al. “Bilateral Acute Lower Limb Ischemia Secondary to COVID-19.” Vascular and Endovascular Surgery (2020): 1538574420954301.
In article      View Article  PubMed
 
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In article      View Article
 
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Published with license by Science and Education Publishing, Copyright © 2021 Pramod Theetha Kariyanna, Apoorva Jayarangaiah, Anahat Kaur, Amog Jayarangaiah, Sushruth Das, Ruchi Yadav, Neema Jayachamarajapura Onkaramurthy, Ashkan Tadayoni, Moro O. Salifu and Isabel M. McFarlane

Creative CommonsThis work is licensed under a Creative Commons Attribution 4.0 International License. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

Cite this article:

Normal Style
Pramod Theetha Kariyanna, Apoorva Jayarangaiah, Anahat Kaur, Amog Jayarangaiah, Sushruth Das, Ruchi Yadav, Neema Jayachamarajapura Onkaramurthy, Ashkan Tadayoni, Moro O. Salifu, Isabel M. McFarlane. COVID-19 and Acute Limb Ischemia: A Systematic Review. American Journal of Medical Case Reports. Vol. 9, No. 6, 2021, pp 312-317. http://pubs.sciepub.com/ajmcr/9/6/2
MLA Style
Kariyanna, Pramod Theetha, et al. "COVID-19 and Acute Limb Ischemia: A Systematic Review." American Journal of Medical Case Reports 9.6 (2021): 312-317.
APA Style
Kariyanna, P. T. , Jayarangaiah, A. , Kaur, A. , Jayarangaiah, A. , Das, S. , Yadav, R. , Onkaramurthy, N. J. , Tadayoni, A. , Salifu, M. O. , & McFarlane, I. M. (2021). COVID-19 and Acute Limb Ischemia: A Systematic Review. American Journal of Medical Case Reports, 9(6), 312-317.
Chicago Style
Kariyanna, Pramod Theetha, Apoorva Jayarangaiah, Anahat Kaur, Amog Jayarangaiah, Sushruth Das, Ruchi Yadav, Neema Jayachamarajapura Onkaramurthy, Ashkan Tadayoni, Moro O. Salifu, and Isabel M. McFarlane. "COVID-19 and Acute Limb Ischemia: A Systematic Review." American Journal of Medical Case Reports 9, no. 6 (2021): 312-317.
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  • Table 1. Illustrating patient characteristics and management strategies employed in patients with COVID-19 who presented with acute limb ischemia
[1]  Miesbach, Wolfgang, and Michael Makris. “COVID-19: coagulopathy, risk of thrombosis, and the rationale for anticoagulation.” Clinical and Applied Thrombosis/Hemostasis 26 (2020): 1076029620938149.
In article      View Article  PubMed
 
[2]  Kariyanna, Pramod Theetha, et al. “A Systematic Review of COVID-19 and Myocarditis.” American journal of medical case reports 8.9 (2020): 299.
In article      View Article
 
[3]  Varga, Zsuzsanna, et al. “Endothelial cell infection and endotheliitis in COVID-19.” The Lancet 395.10234 (2020): 1417-1418.
In article      View Article
 
[4]  Alosaimi, R., A. Albajri, and R. M. Albalwi. “Acute Upper Limb Ischemia in a Patient with COVID-19 Pneumonia.” MedRead J Fam Med 1.4 (2020): 1015.
In article      
 
[5]  Anwar, Shamsuddin, et al. “Acute limb ischemia in COVID-19 disease: a mysterious coagulopathy.” Cureus 12.7 (2020).
In article      View Article
 
[6]  Baccellieri, Domenico, et al. “A case of Covid-19 patient with acute limb ischemia and heparin resistance.” Annals of Vascular Surgery 68 (2020): 88-92.
In article      View Article  PubMed
 
[7]  Bhoriwal, Sandeep, et al. “Acute arterial thrombosis in a breast cancer survivor with coronavirus disease 2019 (COVID-19).” Surgery 168.5 (2020): e19-e20.
In article      View Article  PubMed
 
[8]  Cañas, E. Gonzalez, et al. “Acute peripheral arterial thrombosis in COVID‐19. Role of endothelial inflammation.” The British Journal of Surgery (2020).
In article      View Article  PubMed
 
[9]  Essa, Rawand Abdulrahman, and Sirwan Khalid Ahmed. “Case Report: Acute lower limb ischemia in a recovered COVID-19 patient.” F1000Research 9.1253 (2020): 1253.
In article      View Article
 
[10]  Fahad, Ahmed Muhi, et al. “Case report: COVID-19 in a female patient who presented with acute lower limb ischemia.” F1000Research 9.778 (2020): 778.
In article      View Article
 
[11]  Galanis, Nikiforos, et al. “Coagulopathy in COVID-19 infection: a case of acute upper limb ischemia.” Journal of surgical case reports 2020.6 (2020): rjaa204.
In article      View Article  PubMed
 
[12]  Del Giudice, P., et al. “Catastrophic acute bilateral lower limbs necrosis associated with COVID‐19 as a likely consequence of both vasculitis and coagulopathy.” Journal of the European Academy of Dermatology and Venereology 34.11 (2020): e679-e680.
In article      View Article  PubMed
 
[13]  Hanif, Muhammad, et al. “Acute Upper Limb Ischemia Due To Arterial Thrombosis in a Mild COVID-19 Patient: A Case Report.” Cureus 12.9 (2020).
In article      View Article
 
[14]  Kaur, Parminder, et al. “COVID-19 presenting as acute limb ischaemia.” European journal of case reports in internal medicine 7.6 (2020).
In article      
 
[15]  Kaur, Parminder, et al. “Acute upper limb ischemia in a patient with COVID-19.” Hematology/oncology and stem cell therapy (2020).
In article      View Article  PubMed
 
[16]  Warrior, Krishnan, et al. “Acute Limb Ischemia Due to Arterial Thrombosis Associated With Coronavirus Disease 2019.” Critical Care Explorations 2.6 (2020).
In article      View Article  PubMed
 
[17]  Levolger, Stef, et al. “Arterial thrombotic complications in COVID-19 patients.” Journal of Vascular Surgery Cases and Innovative Techniques 6.3 (2020): 454-459.
In article      View Article  PubMed
 
[18]  Maurera, Annabella H., et al. “Acute Limb Ischemia in Minimally Symptomatic SARS-CoV-2 Infection.” Journal of Vascular and Interventional Radiology (2020).
In article      View Article  PubMed
 
[19]  Merz, Lauren E., et al. “Extensive Arterial Thrombosis in Covid-19.” American Journal of Cardiology 134 (2020): 148-149.
In article      View Article  PubMed
 
[20]  Mietto, Cristina, et al. “Acute lower limb ischemia as clinical presentation of COVID-19 infection.” Annals of Vascular Surgery 69 (2020): 80-84.
In article      View Article  PubMed
 
[21]  Muhammad, Kamel, et al. “Successful Catheter-directed thrombolysis for acute lower limb ischemia secondary to COVID-19 infection.” Annals of vascular surgery (2020).
In article      View Article  PubMed
 
[22]  Parekh et al. “Can COVID-19 cause limb ischemia? MeddyIzzyJournal (2020)
In article      
 
[23]  Patel, Priya, et al. “Systemic Thrombolysis as Initial Treatment of COVID-19 Associated Acute Aortoiliac and Lower Extremity Arterial Thrombosis.” Annals of Vascular Surgery 70 (2020): 297-301.
In article      View Article  PubMed
 
[24]  Perini, Paolo, et al. “Acute limb ischaemia in two young, non-atherosclerotic patients with COVID-19.” The Lancet 395.10236 (2020): 1546.
In article      View Article
 
[25]  Qian, Song-Zan, and Jing-Ye Pan. “COVID-19 with limb ischemic necrosis.” Journal of cardiothoracic and vascular anesthesia 34.10 (2020): 2846-2847.
In article      View Article  PubMed
 
[26]  Schultz, Kathryn, and Jennifer Moriatis Wolf. “Digital ischemia in COVID-19 patients: case report.” The Journal of hand surgery 45.6 (2020): 518-522.
In article      View Article  PubMed
 
[27]  Singh, Balraj, et al. “COVID-19 Infection and Arterial Thrombosis: Report of three cases.” Annals of vascular surgery 70 (2020): 314-317.
In article      View Article  PubMed
 
[28]  Singh, Balraj, et al. “Covid-19 presenting as acute limb ischemia.” Cureus 12.7 (2020).
In article      View Article
 
[29]  Vacirca, Andrea, et al. “Unheralded lower limb threatening ischemia in a COVID-19 patient.” International Journal of Infectious Diseases 96 (2020): 590-592.
In article      View Article  PubMed
 
[30]  Van Mecl, Amanda, et al. “A Case of COVID-19-Associated Acute Limb Ischemia.” Chest 158.4 (2020): A550.
In article      View Article  PubMed
 
[31]  Soares, Rafael de Athayde, et al. “COVID-19 diagnosis in a patient with critical limb ischemia: complications and clinical outcomes.” Jornal Vascular Brasileiro 19 (2020).
In article      View Article
 
[32]  Veerasuri, Sowmya, et al. “Bilateral Acute Lower Limb Ischemia Secondary to COVID-19.” Vascular and Endovascular Surgery (2020): 1538574420954301.
In article      View Article  PubMed
 
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In article      View Article
 
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