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DOI: 10.1055/a-2408-3339
Caseload and In-Hospital Outcome of Carotid Surgery Performed during the COVID-19 Pandemic vs. Previous Years: A Single-Centre Analysis
Fallzahl und Im-Krankenhaus-Ergebnisse der während der COVID-19-Pandemie durchgeführten Karotisoperationen im Vergleich zu den Vorjahren: eine Single-Center-AnalyseAbstract
Introduction
With the beginning of the COVID-19 pandemic in March 2020, restrictions and challenges for elective and emergency vascular surgery as well as worse outcomes were reported. This study aims to compare our single-centre experience with carotid artery surgery during the pandemic and previous years.
Methods
Our retrospective analysis included all consecutive patients undergoing carotid surgery for symptomatic and asymptomatic stenosis between January 2017 and December 2021. Caseload, operation specific parameters, and demographic data as well as in-hospital outcome were compared during the COVID-19 pandemic versus previous years.
Results
A total of 623 consecutive patients were included. The caseload comparison showed an average of 112 carotid artery surgeries per adjusted year (March 16th to December 31st) from 2017 to 2019, prior to the pandemic. The caseload reduction in the first year of the pandemic (2020) was 36.6% (n = 71) and 17.9% (n = 92) in the second year (2021). No rebound effect was observed. There was no significant difference (p = 0.42) in the allocation of symptomatic and asymptomatic patients (asymptomatic patients: 37.1% prior vs. 40.8% during the pandemic; symptomatic patients: 62.9 vs. 59.2%). Major adverse event rates in years prior to the pandemic were postoperative bleeding requiring revision: n = 31 (7.1%); stroke in symptomatic patients: n = 9 (3.3%) and stroke in asymptomatic patients: n = 4 (2.5%); symptomatic myocardial infarction (MCI): n = 1 (0.2%); death: n = 2 (0.5%). During the pandemic, major adverse event rates were postoperative bleeding requiring revision: n = 12 (6.5%); stroke in symptomatic patients: n = 1 (0.9%), stroke in asymptomatic patients: n = 1 (1.3%); symptomatic MCI: n = 1 (0.5%); death: n = 1 (0.5%).
Conclusion
Since the beginning of the COVID-19 pandemic in March 2020, there has been a significant reduction in carotid artery surgery performed both in symptomatic as well as in asymptomatic patients. There was no worsening of the outcome of carotid surgery performed during the COVID-19 pandemic, and this remained safe and feasible.
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Zusammenfassung
Einführung
Mit Beginn der COVID-19-Pandemie im März 2020 wurden Einschränkungen und Herausforderungen für elektive und notfallmäßige Gefäßoperationen sowie eine Verschlechterung der Ergebnisse gemeldet. Diese Studie zielt darauf ab, unsere Single-Center-Erfahrungen während der Pandemie und in früheren Jahren zu vergleichen.
Material und Methoden
Unsere retrospektive Analyse umfasste alle Patient*innen, die sich zwischen Januar 2017 und Dezember 2021 einer Karotisoperation wegen symptomatischer und asymptomatischer Stenose unterzogen. Die Fallzahl, operationsspezifische Parameter und demografische Daten sowie das Ergebnis im Krankenhaus wurden während der COVID-19-Pandemie mit den Vorjahren verglichen.
Ergebnisse
Insgesamt wurden 623 Patient*innen eingeschlossen. Der Fallzahlenvergleich ergab einen Durchschnitt von 112 Halsschlagaderoperationen pro angepasstem Jahr (16. März bis 31. Dezember) von 2017 bis 2019 vor der Pandemie. Die Fallzahlreduktion betrug im 1. Jahr der Pandemie (2020) 36,6% (n = 71) und im 2. Jahr (2021) 17,9% (n = 92). Es wurde kein Rebound-Effekt beobachtet. Es gab keinen signifikanten Unterschied (p = 0,42) bei der Verteilung von symptomatischen und asymptomatischen Patient*innen (asymptomatische Patient*innen: 37,1% vor vs. 40,8% während der Pandemie; symptomatische Patient*innen: 62,9% vs. 59,2%). Die Raten schwerwiegender unerwünschter Komplikationen in den Jahren vor der Pandemie waren: postoperative Blutungen, die eine Revision erforderten: n = 31 (7,1%); Schlaganfall bei symptomatischen Patienten: n = 9 (3,3%) und Schlaganfall bei asymptomatischen Patienten: n = 4 (2,5%); symptomatischer Myokardinfarkt (MCI): n = 1 (0,2%); Tod: n = 2 (0,5%). Während der Pandemie kam es zu folgenden schwerwiegenden unerwünschten Komplikationen: postoperative Blutungen, die eine Revision erforderten: n = 12 (6,5%); Schlaganfall bei symptomatischen Patient*innen: n = 1 (0,9%), Schlaganfall bei asymptomatischen Patient*innen: n = 1 (1,3%); symptomatischer MCI: n = 1 (0,5%); Tod: n = 1 (0,5%).
Schlussfolgerung
Seit Beginn der COVID-19-Pandemie im März 2020 kam es zu einem deutlichen Rückgang der durchgeführten Halsschlagaderoperationen, sowohl bei symptomatischen als auch bei asymptomatischen Patient*innen. In unserem Zentrum kam es zu keiner Verschlechterung der Ergebnisse während der COVID-19-Pandemie durchgeführten Karotisoperationen und verblieben somit sicher durchführbar.
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Introduction
Following the onset of the COVID-19 pandemic in China in December 2019, the disease rapidly spread across the globe. By the 25th of February 2020, the first two cases were reported in Tyrol, Austria. From then onwards, a rapid increase of COVID-19 cases was reported. To stem the spread of the virus, a nationwide lockdown was established, beginning on the 16th of March 2020. Due to the need of intensive care capacities for many COVID-19 patients as well as the associated hygiene measures, a bottleneck in postoperative care was expected.
A survey carried out by the 12 largest vascular surgery centres in Austria during the first lockdown showed that mainly surgeries and interventions on asymptomatic patients were postponed. The treatment of symptomatic patients was unaffected [1]. Different publications show similar results, with a significant caseload reduction during the spring of 2020 [2] [3] [4] [5]. Another primarily unexpected effect of the pandemic was COVID-19-associated coagulopathy leading to carotid thrombosis, requiring intervention [6] [7]. Furthermore, an unusual high mortality of carotid interventions during the pandemic was reported [8].
The aim of this study is to compare our single high-volume centre experience with carotid artery surgery during the COVID-19 pandemic with previous years. Our centre is the only institution performing carotid artery surgery in our district, with 4 major assigning stroke units and 764000 inhabitants as well as many tourists (approximately 45 million overnight stays per year). The centralized care of patients with carotid pathologies enables data collection that is representative for the federal state of our district (Tyrol, Austria).
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Material and Methods
All consecutive patients undergoing surgical treatment of a carotid artery stenosis at the University Hospital Innsbruck between January 2017 and December 2021 were included.
All patients underwent carotid ultrasonography to determine the degree of stenosis. A neurological assessment was attained to determine whether patients experienced symptoms attributable to the stenosis of the internal carotid artery (ICA). Cerebral as well as carotid imaging studies, patient history, and a clinical assessment were used. Patients were deemed symptomatic if they experienced symptoms [amaurosis fugax (AF), transient ischemic attack (TIA), and ischemic stroke] in the last 6 months. If patients did not experience any of the symptoms specified above, they were classified as asymptomatic. All symptomatic and asymptomatic patients were included.
Carotid endarterectomy (CEA) was performed in standard fashion with patch plasty, eversion endarterectomy (EEA), or graft interposition if anatomically suitable or by the surgeon’s preference. The procedure was carried out under regional or general anaesthesia. During general anaesthesia, a shunt was inserted. Under regional anaesthesia, shunts were selectively placed depending on neurological symptoms during carotid clamping.
Intraoperatively, patency was checked via duplex ultrasound or angiography.
Postoperatively, patency was assessed with carotid ultrasound, and a neurological status was attained. Postprocedural complications were defined as “in-hospital” and were categorized as postoperative bleeding requiring revision, stroke, symptomatic MCI, or death.
The years before the COVID-19 pandemic (January 1, 2017 to March 15, 2020) were compared to the first 2 years of the pandemic (March 16, 2020 to December 31, 2021).
Statistical analysis
All gathered data was stored, and statistical analysis was performed using Microsoft Excel 16.65 (Microsoft, Redmond, WA, USA). Case numbers and categorical variables were described as absolute and relative frequencies and analysed using χ2 or Fisher’s exact test. For metric scaled variables, the Mann-Whitney U test was used. Continuous variables were reported as the mean. All p values < 0.05 were considered statistically significant.
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Results
Between January 2017 and December 2021, a total of 623 consecutive patients with a stenosis of the ICA underwent carotid surgery. Before the pandemic, between January 1, 2017 and March 15, 2020, 439 patients were treated compared to 184 individuals during the pandemic (March 16 to December 31, 2021).
The caseload analysis was performed by averaging the years prior to the pandemic (2017–2019), respectively, from the 16th of March to the 31st of December. This resulted in a mean “pre-COVID” caseload of 112 per adjusted year. In 2020, after the beginning of the pandemic on March 16th, a caseload of 71 was observed, deriving a reduction of 36.6% when compared to the pre-COVID era adjusted years. The adjusted year 2021 with a caseload of 92 surgeries still showed a reduction of 17.9% when compared to previous pre-COVID years. No rebound effect was observed.
Epidemiologic data showed no significant differences in age and gender distribution between the pre-COVID cohort and the patients treated during the COVID pandemic (see [Table 1]). In addition, the distribution of symptomatic and asymptomatic patients was similar during both periods (see [Table 1]).
An overview on procedure-specific data is given in [Table 2]. Comparison of operative technique revealed a significant decrease in the use of EEA during the pandemic compared to previous years (28.2 vs.4.9%) and, respectively, an increase of CEAs plus patch plasty (70.4 vs. 94.9%). Carotid artery interposition as well as conversion to carotid artery stenting remained an exception. There was no significant difference in the use of general or regional anaesthesia.
Outcome analysis enclosed the in-hospital period only. Major adverse events such as postoperative bleeding requiring revision, ipsilateral stroke, symptomatic myocardial infarction, and death were recorded (see [Table 3]). There was no significant difference in major adverse event rates during the pandemic compared to previous years.
Carotid surgery in patients with COVID infection and/or testing positive for COVID: During the COVID pandemic, only two patients urgently requiring surgery for a symptomatic ICA stenosis tested positive for COVID-19. In both cases, surgery was postponed until the COVID-19 PCR CT value was above 30, and the waiting period as well as surgery was uneventful with no major adverse events.
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Discussion
The authors’ analysis showed a significant reduction in caseload of carotid surgeries performed during the COVID-19 pandemic when compared to the pre-COVID era. Different publications have shown a similar trend as a consequence of the pandemic-associated lockdowns [2] [3] [4] [5] [9]. Similar to Ball et al., the University Hospital Innsbruck repurposed OR staff to accommodate the higher demand in critical care [2]. Therefore, elective procedures were cancelled. Cai et al. was also able to show a decrease of surgical management of carotid artery disease in the year 2020 compared to previous years as well as in other vascular procedures [4]. Other reasons for the decrease in caseload were thought to be a deterioration of preoperative health status, the elderly being more susceptible to severe infections, or people being afraid of exposure to COVID-19 when visiting a doctor or the hospital, especially with minor symptoms [10] [11].
Crespy et al. were also able to show a rebound effect in symptomatic patients exceeding the caseload prior to the first major lockdown [5]. On the other hand, Krafcik et al. showed a persistent reduction in vascular surgical volume, with still 34% fewer CEAs in the first quarter of 2022 [12]. In the presented cohort, the caseload neither in asymptomatic nor in symptomatic patients ever exceeded the pre-COVID era, but a trend towards a pre-COVID era caseload can be established.
The procedure-specific data shows a significant increase in EEA during the pandemic compared to previous years. Respectively, there was an increase in the use of CEA. Most probably, this shift can be explained by the fact that there was an experienced surgeon in the vascular surgery department at the authors’ institution who preferred to perform EEA and who retired shortly after the start of the COVID-19 pandemic. On the other hand, EEA, although an equivalent alternative method for suitable anatomical constellations, is not traditionally established as a teaching operation at the University Hospital Innsbruck and therefore less often used.
The authors examined the treatment outcomes of carotid surgery during the pandemic. In contrast to previously published data [8], it was observed that, compared to previous years, the treatment results did not differ significantly and there were even fewer perioperative strokes during the period of the COVID-19 pandemic ([Table 3]). This contradicted the results of the international multicentre VERN COVER study (during a period of 12 weeks in the first wave of the pandemic). In that retrospective observational study, it was shown that mortality after vascular procedures was unexpectedly high in the mentioned period. The mortality was 10.7% for all interventions [8].
The North American Symptomatic Carotid Endarterectomy Trial Collaborators [13] described a 2.1% major stroke rate and a fatality rate of 0.6% in their cohort, restricting the analysis to the most serious events. In the ACST 2 trial [14], out of 1788 patients undergoing carotid surgery, 2.7% were fatal or suffered a stroke. In the presented study, however, in 148 operations (March 16, 2020 to December 31, 2021), a single patient (corresponding to 0.5%) died during the carotid operation, and before COVID-19 (January 1, 2017 to March 15, 2020), out of 439 patients, 2 died (also corresponds to 0.5%) perioperatively.
There were many reports of COVID-19-associated intraluminal free-floating thrombi [6] [15] [16] [17] [18] [19] [20] [21] [22] [23] and even total occlusion of the common carotid artery [24] [25]. We were able to identify two patients in our cohort with a symptomatic ICA stenosis that also tested positive for COVID-19. During the pandemic, we encountered no free-floating thrombi in the common carotid artery. This correlates with previous findings that intraluminal free-floating thrombi in the common carotid artery are a rare entity.
The evaluation and comparison of the number of cases and results of operated carotid stenoses is limited by the required determination of the examination periods. We chose to compare the period March 20th until December 31st of all years knowing that lockdowns and lockdown-free periods alternated in 2020 and 2021 and that there was no homogeneous distribution of the number of cases over the investigation period. However, our data corresponds better to the representation of an “overall performance,” which could have recorded reduced and, if necessary, compensatory increased numbers of cases.
Given the retrospective study design, there is also a lack of background information regarding surgical postponements due to reduced capacities and their clinical effects. Restrictions of capacities are an ongoing major problem in many institutions; however, they are only partly a consequence of the COVID-19 pandemic.
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Conclusion
Much of the data published so far has primarily investigated the period of the first lockdown in spring 2020. Our study was able to include 2 years of the COVID-19 pandemic and has the advantage of a large and precisely defined inclusion area for carotid interventions (a unicentric data collection representative for the federal state of Tyrol). We were able to show that significantly fewer carotid reconstructions were carried out since the start of the COVID-19 pandemic. Carotid reconstruction was not required during a florid COVID-19 infection.
Carotid artery surgery remained safe and feasible. The quality was maintained during the COVID-19 pandemic at the Innsbruck University Hospital with consistent treatment results and even numerically fewer perioperative strokes.
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Conflict of Interest
The authors declare that they have no conflict of interest.
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References
- 1 Klocker J, Frech A, Gratl A. et al. Operieren, Absagen, Verschieben oder Selektionieren? Ergebnisse einer Umfrage unter gefäßchirurgischen Zentren während der Covid-19-Krise in Österreich. Gefässchirurgie 2020; 25: 417-422
- 2 Ball S, Banerjee A, Berry C. et al. Monitoring indirect impact of COVID-19 pandemic on services for cardiovascular diseases in the UK. Heart 2020; 106: 1890-1897
- 3 Piazza M, Xodo A, Squizzato F. et al. The challenge of maintaining necessary vascular and endovascular services at a referral center in Northern Italy during the COVID-19 outbreak. Vascular 2021; 29: 477-485
- 4 Cai TY, Fisher G, Loa J. Changing patterns in Australian and New Zealand: vascular surgery during COVID-19. ANZ J Surg 2021; 91: 2389-2396
- 5 Crespy V, Benzenine E, Mariet AS. et al. Impact of the first COVID-19 pandemic peak and lockdown on the interventional management of carotid artery stenosis in France. J Vasc Surg 2022; 75
- 6 Cancer-Perez S, Alfayate-García J, Vicente-Jiménez S. et al. Symptomatic Common Carotid Free-Floating Thrombus in a COVID-19 Patient, Case Report and Literature Review. Ann Vasc Surg 2021; 73: 122-128
- 7 Esenwa C, Cheng NT, Lipsitz E. et al. COVID-19-Associated Carotid Atherothrombosis and Stroke. AJNR Am J Neuroradiol 2020; 41: 1993-1995
- 8 Benson RA, Nandhra S. Outcomes of Vascular and Endovascular Interventions Performed During the Coronavirus Disease 2019 (COVID-19) Pandemic. Ann Surg 2021; 273: 630-635
- 9 Qureshi AI, Agunbiade S, Huang W. et al. Changes in Neuroendovascular Procedural Volume During the COVID-19 Pandemic: An International Multicenter Study. J Neuroimaging 2021; 31: 171-179
- 10 Mesnier J, Cottin Y, Coste P. et al. Hospital admissions for acute myocardial infarction before and after lockdown according to regional prevalence of COVID-19 and patient profile in France: a registry study. Lancet Public Health 2020; 5: e536-e542
- 11 Mariet A-S, Giroud M, Benzenine E. et al. Hospitalizations for Stroke in France During the COVID-19 Pandemic Before, During, and After the National Lockdown. Stroke 2021; 52: 1362-1369
- 12 Krafcik BM, Gladders B, Jarmel I. et al. The Sustained Impact of the COVID-19 Pandemic on Vascular Surgical Care Delivery. Ann Vasc Surg 2024; 108: 26-35
- 13 Barnett HJM, Taylor DW, Haynes RB. North American Symptomatic Carotid Endarterectomy Trial Collaborators. et al. Beneficial effect of carotid endarterectomy in symptomatic patients with high-grade carotid stenosis. N Engl J Med 1991; 325: 445-453
- 14 Halliday A, Bulbulia R, Bonati LH. et al. Second asymptomatic carotid surgery trial (ACST-2): a randomised comparison of carotid artery stenting versus carotid endarterectomy. Lancet 2021; 398: 1065-1073
- 15 Gomez-Arbelaez D, Ibarra-Sanchez G, Garcia-Gutierrez A. et al. COVID-19-related aortic thrombosis: a report of four cases. Ann Vasc Surg 2020; 67: 10-13
- 16 Indes JE, Koleilat I, Hatch AN. J Vasc Surg. et al. Early experience with arterial thromboembolic complications in patients with COVID-19. 2021; 73: 381-389.e1
- 17 Viguier A, Delamarre L, Duplantier J. et al. Acute ischemic stroke complicating common carotid artery thrombosis during a severe COVID-19 infection. J Neuroradiol 2020; 47: 393-394
- 18 Doo FX, Kassim G, Lefton DR. et al. Rare presentations of COVID-19: PRES-like leukoencephalopathy and carotid thrombosis. Clin Imaging 2021; 69: 94-101
- 19 Fara MG, Stein LK, Skliut M. et al. Macrothrombosis and stroke in patients with mild Covid-19 infection. J Thromb Haemost 2020; 18: 2031-2033
- 20 Gulko E, Gomes W, Ali S. et al. Acute common carotid artery bifurcation thrombus: an emerging pattern of acute strokes in patients with COVID-19?. AJNR Am J Neuroradiol 2020; 41: E65-E66
- 21 Mohamud AY, Griffith B, Rehman M. et al. Intraluminal carotid artery thrombus in COVID-19: another danger of cytokine storm?. AJNR Am J Neuroradiol 2020; 41: 1677-1682
- 22 Mowla A, Sizdahkhani S, Sharifian-Dorche M. et al. Unusual pattern of arterial macrothrombosis causing stroke in a young adult recovered from COVID-19. J Stroke Cerebrovasc Dis 2020; 29: 105353
- 23 Hosseini M, Sahajwani S, Zhang J. et al. Delayed stroke after hospitalization for coronavirus disease 2019 pneumonia from common and internal carotid artery thrombosis. J Vasc Surg Cases Innov Tech 2021; 7: 40-45
- 24 Lapergue B, Lyoubi A, Meseguer E. et al. Large vessel stroke in six patients following SARS-CoV-2 infection: a retrospective case study series of acute thrombotic complications on stable underlying atherosclerotic disease. Eur J Neurol 2020; 27: 2308-2311
- 25 Alkhaibary A, Abbas M, Ahmed ME. et al. Common carotid artery occlusion in a young patient: can large-vessel stroke be the initial clinical manifestation of coronavirus disease 2019?. World Neurosurg 2020; 144: 140-142
Correspondence
Publication History
Received: 26 March 2024
Accepted after revision: 29 August 2024
Article published online:
18 September 2024
© 2024. Thieme. All rights reserved.
Georg Thieme Verlag KG
Oswald-Hesse-Straße 50, 70469 Stuttgart, Germany
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References
- 1 Klocker J, Frech A, Gratl A. et al. Operieren, Absagen, Verschieben oder Selektionieren? Ergebnisse einer Umfrage unter gefäßchirurgischen Zentren während der Covid-19-Krise in Österreich. Gefässchirurgie 2020; 25: 417-422
- 2 Ball S, Banerjee A, Berry C. et al. Monitoring indirect impact of COVID-19 pandemic on services for cardiovascular diseases in the UK. Heart 2020; 106: 1890-1897
- 3 Piazza M, Xodo A, Squizzato F. et al. The challenge of maintaining necessary vascular and endovascular services at a referral center in Northern Italy during the COVID-19 outbreak. Vascular 2021; 29: 477-485
- 4 Cai TY, Fisher G, Loa J. Changing patterns in Australian and New Zealand: vascular surgery during COVID-19. ANZ J Surg 2021; 91: 2389-2396
- 5 Crespy V, Benzenine E, Mariet AS. et al. Impact of the first COVID-19 pandemic peak and lockdown on the interventional management of carotid artery stenosis in France. J Vasc Surg 2022; 75
- 6 Cancer-Perez S, Alfayate-García J, Vicente-Jiménez S. et al. Symptomatic Common Carotid Free-Floating Thrombus in a COVID-19 Patient, Case Report and Literature Review. Ann Vasc Surg 2021; 73: 122-128
- 7 Esenwa C, Cheng NT, Lipsitz E. et al. COVID-19-Associated Carotid Atherothrombosis and Stroke. AJNR Am J Neuroradiol 2020; 41: 1993-1995
- 8 Benson RA, Nandhra S. Outcomes of Vascular and Endovascular Interventions Performed During the Coronavirus Disease 2019 (COVID-19) Pandemic. Ann Surg 2021; 273: 630-635
- 9 Qureshi AI, Agunbiade S, Huang W. et al. Changes in Neuroendovascular Procedural Volume During the COVID-19 Pandemic: An International Multicenter Study. J Neuroimaging 2021; 31: 171-179
- 10 Mesnier J, Cottin Y, Coste P. et al. Hospital admissions for acute myocardial infarction before and after lockdown according to regional prevalence of COVID-19 and patient profile in France: a registry study. Lancet Public Health 2020; 5: e536-e542
- 11 Mariet A-S, Giroud M, Benzenine E. et al. Hospitalizations for Stroke in France During the COVID-19 Pandemic Before, During, and After the National Lockdown. Stroke 2021; 52: 1362-1369
- 12 Krafcik BM, Gladders B, Jarmel I. et al. The Sustained Impact of the COVID-19 Pandemic on Vascular Surgical Care Delivery. Ann Vasc Surg 2024; 108: 26-35
- 13 Barnett HJM, Taylor DW, Haynes RB. North American Symptomatic Carotid Endarterectomy Trial Collaborators. et al. Beneficial effect of carotid endarterectomy in symptomatic patients with high-grade carotid stenosis. N Engl J Med 1991; 325: 445-453
- 14 Halliday A, Bulbulia R, Bonati LH. et al. Second asymptomatic carotid surgery trial (ACST-2): a randomised comparison of carotid artery stenting versus carotid endarterectomy. Lancet 2021; 398: 1065-1073
- 15 Gomez-Arbelaez D, Ibarra-Sanchez G, Garcia-Gutierrez A. et al. COVID-19-related aortic thrombosis: a report of four cases. Ann Vasc Surg 2020; 67: 10-13
- 16 Indes JE, Koleilat I, Hatch AN. J Vasc Surg. et al. Early experience with arterial thromboembolic complications in patients with COVID-19. 2021; 73: 381-389.e1
- 17 Viguier A, Delamarre L, Duplantier J. et al. Acute ischemic stroke complicating common carotid artery thrombosis during a severe COVID-19 infection. J Neuroradiol 2020; 47: 393-394
- 18 Doo FX, Kassim G, Lefton DR. et al. Rare presentations of COVID-19: PRES-like leukoencephalopathy and carotid thrombosis. Clin Imaging 2021; 69: 94-101
- 19 Fara MG, Stein LK, Skliut M. et al. Macrothrombosis and stroke in patients with mild Covid-19 infection. J Thromb Haemost 2020; 18: 2031-2033
- 20 Gulko E, Gomes W, Ali S. et al. Acute common carotid artery bifurcation thrombus: an emerging pattern of acute strokes in patients with COVID-19?. AJNR Am J Neuroradiol 2020; 41: E65-E66
- 21 Mohamud AY, Griffith B, Rehman M. et al. Intraluminal carotid artery thrombus in COVID-19: another danger of cytokine storm?. AJNR Am J Neuroradiol 2020; 41: 1677-1682
- 22 Mowla A, Sizdahkhani S, Sharifian-Dorche M. et al. Unusual pattern of arterial macrothrombosis causing stroke in a young adult recovered from COVID-19. J Stroke Cerebrovasc Dis 2020; 29: 105353
- 23 Hosseini M, Sahajwani S, Zhang J. et al. Delayed stroke after hospitalization for coronavirus disease 2019 pneumonia from common and internal carotid artery thrombosis. J Vasc Surg Cases Innov Tech 2021; 7: 40-45
- 24 Lapergue B, Lyoubi A, Meseguer E. et al. Large vessel stroke in six patients following SARS-CoV-2 infection: a retrospective case study series of acute thrombotic complications on stable underlying atherosclerotic disease. Eur J Neurol 2020; 27: 2308-2311
- 25 Alkhaibary A, Abbas M, Ahmed ME. et al. Common carotid artery occlusion in a young patient: can large-vessel stroke be the initial clinical manifestation of coronavirus disease 2019?. World Neurosurg 2020; 144: 140-142