Limb ischemia in patients with COVID-19

This narrative review covers the life-threatening thromboembolic events associated with SARS-CoV-2 infection/COVID-19. It addresses the physical changes that cause vascular and arterial damage to limbs, laboratory management of coagulation, and management of anticoagulation. COVID-19’s relationship with deep venous thrombosis and arterial thrombosis is also emphasized. The main thromboembolic events described in the literature are illustrated with examples from our experience with COVID-19 patients.

Keywords:
SARS-CoV-2; COVID-19; vascular diseases; endovascular techniques; anticoagulants; embolisms and thrombosis

Authorship

Julio Cesar Peclat de Oliveira

Universidade Federal do Rio de Janeiro – UFRJ, Rio de Janeiro, RJ, Brasil.Universidade Federal do Rio de JaneiroBrasilRio de Janeiro, RJ, BrasilUniversidade Federal do Rio de Janeiro – UFRJ, Rio de Janeiro, RJ, Brasil.

http://orcid.org/0000-0003-1504-8763

Walter Jr. Boim Araujo

Universidade Federal do Paraná – UFPR, Curitiba, PR, Brasil.Universidade Federal do ParanáBrasilCuritiba, PR, BrasilUniversidade Federal do Paraná – UFPR, Curitiba, PR, Brasil.

http://orcid.org/0000-0003-1537-0285

Sergio Quilici Belczak

Instituto de Aprimoramento e Pesquisa em Angiorradiologia e Cirurgia Endovascular – IAPACE, São Paulo, SP, Brasil.Instituto de Aprimoramento e Pesquisa em Angiorradiologia e Cirurgia EndovascularBrasilSão Paulo, SP, BrasilInstituto de Aprimoramento e Pesquisa em Angiorradiologia e Cirurgia Endovascular – IAPACE, São Paulo, SP, Brasil.

Fabiano Luiz Erzinger

Hospital Erasto Gaertner, Curitiba, PR, Brasil.Hospital Erasto GaertnerBrasilCuritiba, PR, BrasilHospital Erasto Gaertner, Curitiba, PR, Brasil.

http://orcid.org/0000-0002-6650-1145

Lucas Maia Peclat de Oliveira

Universidade Federal do Estado do Rio de Janeiro – UNIRIO, Rio de Janeiro, RJ, Brasil.Universidade Federal do Estado do Rio de JaneiroBrasilRio de Janeiro, RJ, BrasilUniversidade Federal do Estado do Rio de Janeiro – UNIRIO, Rio de Janeiro, RJ, Brasil.

http://orcid.org/0000-0002-5454-3129

Marcos Arêas Marques

Universidade do Estado do Rio de Janeiro – UERJ, Rio de Janeiro, RJ, Brasil.Universidade do Estado do Rio de JaneiroBrasilRio de Janeiro, RJ, BrasilUniversidade do Estado do Rio de Janeiro – UERJ, Rio de Janeiro, RJ, Brasil.

Lucas Mansano Sarquis

Hospital do Trabalhador, Curitiba, PR, Brasil.Hospital do TrabalhadorBrasilCuritiba, PR, BrasilHospital do Trabalhador, Curitiba, PR, Brasil.

http://orcid.org/0000-0001-9703-1732

Bianca Gutfilen

http://orcid.org/0000-0001-8632-7474

Conflicts of interest: JCPO, WJBA, MAM and FLE are speakers from the pharmaceutical industry.

Correspondence Julio Cesar Peclat de Oliveira Av. Lucio Costa, 2260, Bloco 3, apartamento 3001 CEP 22630-010 - Rio de Janeiro (RJ), Brasil Tel.: +55 (21) 99997-5754 E-mail: juliocpeclat@yahoo.com.br

Author information JCPO - Doctoral student, Department of Radiology, Medicine School, Centre of Health Sciences, Universidade Federal do Rio de Janeiro (UFRJ). WJBA - Sector of Angioradiology and Endovascular Surgery, Department of Surgery, University Hospital of Universidade Federal do Paraná (UFPR). SQB – Vascular and Endovascular Surgery, Instituto de Aprimoramento e Pesquisa em Angiorradiologia e Cirurgia Endovascular (IAPACE). FLE - Vascular and Endovascular Surgery, Hospital Erasto Gaertner. LMPO - Medicine School, Universidade Federal do Estado do Rio de Janeiro (UNIRIO). MAM – Vascular medicine, Unidade Docente Assistencial de Angiologia, Hospital Universitário Pedro Ernesto, Universidade do Estado do Rio de Janeiro (UERJ), Hospital Universitário Gafrée e Guinle, Universidade Federal do Estado do Rio de Janeiro (UNIRIO). LMS - Vascular Surgery Resident, Hospital do Trabalhador. BG - Department of Radiology, Medicine School, Universidade Federal do Rio de Janeiro (UFRJ).

Author contributions Conception and design: JCPO, WJBA, SQB, FLE, LMPO, MAM, LMS, BG Analysis and interpretation: JCPO, WJBA, SQB, FLE, LMPO, MAM, LMS, BG Data collection: JCPO, WJBA, SQB, FLE, LMPO, LMS Writing the article: JCPO, WJBA, SQB, FLE, MAM Critical revision of the article: JCPO, WJBA, SQB, FLE, MAM, BG Final approval of the article^* * All authors have read and approved of the final version of the article submitted to J Vasc Bras. : JCPO, WJBA, SQB, FLE, LMPO, MAM, LMS, BG Statistical analysis: JCPO, WJBA, SQB, BG Overall responsibility: JCPO, BG

*
All authors have read and approved of the final version of the article submitted to J Vasc Bras.

SCIMAGO INSTITUTIONS RANKINGS

Universidade Federal do Paraná – UFPR, Curitiba, PR, Brasil.Universidade Federal do ParanáBrasilCuritiba, PR, BrasilUniversidade Federal do Paraná – UFPR, Curitiba, PR, Brasil.

Hospital Erasto Gaertner, Curitiba, PR, Brasil.Hospital Erasto GaertnerBrasilCuritiba, PR, BrasilHospital Erasto Gaertner, Curitiba, PR, Brasil.

Hospital do Trabalhador, Curitiba, PR, Brasil.Hospital do TrabalhadorBrasilCuritiba, PR, BrasilHospital do Trabalhador, Curitiba, PR, Brasil.

Figures | Tables

Figures (3)
Tables (2)

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Figure 1
Female patient, 62 years old, hospitalized due to COVID-19, developed an ischemic plaque and possible infectious spot in the left heel, and erythrocyanosis of the forefoot. She was given clinical treatment with full IV heparinization and venous prostaglandin for three weeks. Her clinical condition improved, and she was discharged after 30 days.

Thumbnail

Figure 2
A young female patient using hormonal contraceptives was admitted to the Emergency with COVID-19 and pain and critical edema in the left lower limb, and absence of distal pulses with no other symptoms (A). Emergency Fogarty thrombectomy was successfully performed on the venous iliac femoral segment (B). Postoperatively, she coursed with worsening laboratory tests and pneumonia. She was discharged after 3 weeks and the limb remains healthy, on oral anticoagulation with rivaroxaban (C).

Thumbnail

Figure 3
Male patient, 61 years old, with controlled hypertension, hospitalized due to edema and pain in the left upper limb (A), tested positive for COVID-19. Color Doppler ultrasound revealed extensive arterial thrombosis of the left upper limb, absence of flow in radial and ulnar arteries, and palmar arch. The examination showed evidence of forearm compartment syndrome. The patient underwent decompressive fasciotomy (B) and arterial Fogarty catheter thrombectomy. He progressed well and was discharged on oral anticoagulants.

Thumbnail

Table 1
Considerations on prophylactic anticoagulation in COVID-19 patients.

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Table 2
An approach based on bedside ultrasound screening dividing patients into three categories.

Figure 1 Female patient, 62 years old, hospitalized due to COVID-19, developed an ischemic plaque and possible infectious spot in the left heel, and erythrocyanosis of the forefoot. She was given clinical treatment with full IV heparinization and venous prostaglandin for three weeks. Her clinical condition improved, and she was discharged after 30 days.

Figure 2 A young female patient using hormonal contraceptives was admitted to the Emergency with COVID-19 and pain and critical edema in the left lower limb, and absence of distal pulses with no other symptoms (A). Emergency Fogarty thrombectomy was successfully performed on the venous iliac femoral segment (B). Postoperatively, she coursed with worsening laboratory tests and pneumonia. She was discharged after 3 weeks and the limb remains healthy, on oral anticoagulation with rivaroxaban (C).

Figure 3 Male patient, 61 years old, with controlled hypertension, hospitalized due to edema and pain in the left upper limb (A), tested positive for COVID-19. Color Doppler ultrasound revealed extensive arterial thrombosis of the left upper limb, absence of flow in radial and ulnar arteries, and palmar arch. The examination showed evidence of forearm compartment syndrome. The patient underwent decompressive fasciotomy (B) and arterial Fogarty catheter thrombectomy. He progressed well and was discharged on oral anticoagulants.

Table 1 Considerations on prophylactic anticoagulation in COVID-19 patients.

Low-molecular-weight heparin (LMWH): Consider 30 mg twice daily or 40 mg once daily with standard adjustments for renal failure or obesity patients.

Obese patients: (Body Mass Index [BMI] >30) at high risk (Caprini score >8): consider double the usual anticoagulation dose LMWH 60mg from once daily to twice daily. If there is a severe renal failure (ClCr <30 mL/min) or acute renal failure, consider Unfractionated Heparin (UFH) 5,000 IU, subcutaneous, three times a day.

If there is a history of or concern about the occurrence of heparin-induced thrombocytopenia, use fondaparinux.

If the platelet count is less than 30,000 mm³, there is significant bleeding, or contraindication to anticoagulation, use mechanical compressive methods.

Direct Oral AntiCoagulants (DOACS) should not be used as prophylaxis in hospitalized patients.

Table 2 An approach based on bedside ultrasound screening dividing patients into three categories.

Category	D-Dimer	Treatment
I	< 3.000 ng/mL and no evidence of venous thromboembolism (VTE)	Patients receive standard deep vein thrombosis (DVT) prophylaxis (enoxaparin 40 mg once a day) and are monitored with serial D-Dimer (DD) testing
II	> 3.000 ng/mL and negative ultrasound	Patients receive intensified prophylaxis against deep vein thrombosis (DVT) (enoxaparin 40 mg every 12 hours)
III	Confirmed thrombosis	Full anticoagulation

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Limb ischemia in patients with COVID-19

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[1] Conflicts of interest: JCPO, WJBA, MAM and FLE are speakers from the pharmaceutical industry.