Abstract
Introduction
Carotid endarterectomy (CEA) is the standard treatment for patients with symptomatic carotid stenosis. Data from low- and middle-income countries are sparse on CEA and its outcomes. We aimed to describe the profile of our patients and factors associated with periprocedural cerebral ischemic events in patients with symptomatic carotid stenosis who underwent CEA in our institute.
Methods
Retrospective review of patients with symptomatic carotid stenosis (50–99%) who underwent CEA between January 2011 and December 2021 was done. Clinical and imaging parameters and their influence on periprocedural cerebral ischemic events were analyzed.
Results
Of the 319 patients (77% males) with a mean age of 64 years (SD±8.6), 207 (65%) presented only after a stroke. Majority (85%) had high-grade stenosis (≥70%) of the symptomatic carotid. The mean time to CEA was 50 days (SD±36); however, only 26 patients (8.2%) underwent surgery within 2 weeks. Minor strokes and TIA occurred in 2.2%, while major strokes and death occurred in 4.1% patients. None of the clinical or imaging parameters predicted the periprocedural cerebral ischemic events. The presence of co-existing significant (≥50%) tandem intracranial atherosclerosis (n = 77, 24%) or contralateral occlusion (n = 24, 7.5%) did not influence the periprocedural stroke risk.
Conclusion
There is a delay in patients undergoing CEA for symptomatic carotid stenosis. Majority have high-grade stenosis and present late only after a stroke reflecting a lack of awareness. CEA can be performed safely even in patients with significant intracranial tandem stenosis and contralateral carotid occlusion.
Keywords: Carotid endarterectomy, Symptomatic carotid stenosis, Perioperative events
Introduction
Large vessel atherosclerotic disease constitutes approximately 20–30% of all ischemic strokes [1]. Based on the three major trials (the North American Symptomatic Carotid Endarterectomy Trial (NASCET), European Carotid Surgery Trial (ECST), and Veteran Affairs Trial 309) [2–4] and a pooled analysis of the same [5], the current recommendation is to perform carotid endarterectomy (CEA) in patients with symptomatic carotid stenosis (≥50%) in centers with perioperative morbidity and mortality less than 6% [6]. Recent trials also affirm that CEA is the standard of care with a lower incidence of periprocedural stroke [7]. However, randomized controlled trials (RCTs) include large volume centers with highly specialized surgeons and their results may not be replicable in all patient populations. While the majority of patients in the Western world undergo CEA even after a transient ischemic attack (TIA) [8–11], it is the reverse in low- and middle-income countries where CEA is done most often after a stroke [12–14] and tends to be delayed compared to the guideline recommended timing within 2 weeks. In this background, the application of these guidelines in low- and middle-income countries requires an understanding of the profile of patients who undergo carotid revascularization. There is lack of data on the clinical profile, imaging characteristics, timing, and outcome of CEA in patients who present with symptomatic carotid stenosis from a country like India. We aimed to describe the clinical profile of patients with symptomatic carotid stenosis who underwent CEA in our institute and analyzed the factors associated with perioperative vascular events.
Methods
This study was a retrospective review of prospectively collected data of all patients aged >18 years with symptomatic carotid artery stenosis (≥50%) who underwent CEA in the comprehensive stroke care center, Department of Neurology, Sree Chitra Tirunal Institute for Medical Sciences and Technology (SCTIMST), Kerala, between 2011 and 2021. The clinical profile of the patients, including the vascular risk factors, clinical characteristics, the admission stroke severity assessed using the National Institute of Health Stroke Scale (NIHSS), disability status assessed using modified Rankin Scale (mRS) were collected. The imaging characteristics such as the pattern of infarcts were assessed by computed tomography (CT) or magnetic resonance imaging of the brain. The vessels affected, both ipsilateral and contralateral, percentage of luminal stenosis, both extra- and intracranial, were assessed through imaging modalities like CT angiography, MR angiography, digital subtraction angiography (DSA), or neck vessel Doppler. In patients with more than one vascular imaging assessments, DSA was chosen as the modality of review whenever available. When DSA was unavailable, CT angiogram or contrast-enhanced MR angiography was used with equal weightage given to both. MR TOF angiogram was taken for assessment only when other modalities of vessel assessment were unavailable. The NASCET method for estimating the percentage of stenosis was used in the study. An extracranial carotid stenosis ≥70% was taken as high grade. Both intracranial and extracranial stenosis as well as the presence or absence of ulcer or thrombus of ipsilateral and contralateral vessels were noted. The presence of intracranial stenosis ≥50% was considered significant. The patterns of infarcts were classified as embolic or hemodynamic or a combination of both. Territorial infarcts with or without fragmentation, multiple small infarcts in ICA territory were taken as embolic pattern and those infarcts in cortical watershed and internal watershed areas were included under hemodynamic pattern. The timing of CEA from the onset of the symptoms and periprocedural TIA/stroke, cardiac events, or any other procedural complications including reperfusion injury, wound hematoma, or cranial neuropathy was also collected. Post-procedural cardiac events were defined by presence of typical cardiac chest pain, with rise in troponins or dynamic changes in electrocardiogram or new-onset regional wall motion abnormalities in echocardiogram. The primary outcome was the occurrence of perioperative cerebral ischemic events that included TIA and stroke. The secondary outcome included a composite of stroke, TIA, cardiac events, or death perioperatively.
Statistical Analysis
The statistical analysis was performed using Intercooled STATA 14.1 software package (StataCorp, TX, USA). The timing of CEA was divided into early (≤14 days) and late (>14 days) after the onset of symptoms, for analyzing the relationship to perioperative events. The association of demographic, clinical, and radiological characteristics of the patients with perioperative cerebral ischemic events was assessed using χ2 test or Fisher’s exact test as appropriate. A p value <0.05 was deemed significant.
Results
Between 2011 and 2021, there were 472 patients who were taken up for carotid revascularization. Of these, 61 underwent carotid stenting while 411 had CEA. Among 411 patients, we excluded those who underwent the procedure for asymptomatic carotid stenosis and those with remote symptomatic carotid stenosis, defined by last symptom onset more than 6 months ago. There were 319 patients of whom 247 (77%) were males. The mean age of the patients was 64 years (SD ± 8.6). The most common presentation was stroke (n = 208, 65%). Of those who had presented with stroke, 40% had prior TIAs. The median time to undergo CEA was 39 days (range 4–180), and 26 patients (8.2%) underwent surgery within 2 weeks. Majority of the patients (n = 270, 85%) had high-grade stenosis (≥70%) of the symptomatic carotid, while 77 (24%) had co-existent tandem significant (>50%) intracranial stenosis. About 63 patients (19.75%) had an ulcerated plaque in ipsilateral carotid while 24 patients (7.5%) had a contralateral carotid artery occlusion. The demographic, clinical, risk factor profile and imaging patterns of our patients are shown in Table 1.
Table 1.
Clinical and imaging characteristics of the study population
| Characteristics | Number (N = 319) | 
|---|---|
| Mean age (SD) | 64 (±8.6) | 
| Males (%) | 247 (77%) | 
| Hypertension (%) | 269 (84.3%) | 
| Diabetes (%) | 198 (62%) | 
| Smoking (%) | 71 (22.2%) | 
| Coronary artery disease (%) | 70 (21.9%) | 
| Post-coronary artery bypass surgery (%) | 18 (5.6%) | 
| Dyslipidemia (%) | 99 (31%) | 
| Peripheral vascular disease (%) | 33 (10.3%) | 
| Renal dysfunction (%) | 51 (15.9%) | 
| Initial event | |
| Retinal TIA | 20 (6%) | 
| Hemispheric TIA | 117 (37%) | 
| Stroke | 183 (57%) | 
| Presenting event | |
| Retinal TIA | 16 (5%) | 
| Hemispheric TIA | 93 (29%) | 
| Stroke | 208 (65%) | 
| Median NIHSS prior to surgery (IQR) | 1 (0–3) | 
| Median duration of timing of procedure from the initial event in days (range) | 39 (4–180) | 
| Underwent surgery within 2 weeks (%) | 26 (8.2%) | 
| Median duration of hospital stay in days(SD) | 9 (±4.9) | 
| Side of surgery | |
| Left CEA | 161 (50.5%) | 
| Right CEA | 158 (49.5%) | 
| Infarcts | |
| Single | 47 (15%) | 
| Multiple | 230 (72%) | 
| Pattern of infarcts | |
| Embolic | 211 (66%) | 
| Hemodynamic | 195 (61%) | 
| Combination of embolic and hemodynamic | 129 (40%) | 
| Contralateral infarcts | 46 (14%) | 
| Vessel imaging | |
| Digital subtraction angiography | 23 (7.2%) | 
| Computed tomography angiography | 258 (80.8%) | 
| Magnetic resonance angiography | 104 (32.6%) | 
| Neck vessel Doppler | 230 (72.1%) | 
| High-grade (≥70%) stenosis of symptomatic carotid | 270 (85%) | 
| Ulcerated plaque | 63 (20%) | 
| Tandem intracranial (≥50%) stenosis of symptomatic side | 77 (24%) | 
| Contralateral carotid occlusion | 24 (7.5%) | 
The primary endpoint of perioperative cerebral ischemic events was noted in 6.1% patients, with minor strokes and TIA in 2.1% and major strokes in 4% patients. Post-procedural acute coronary syndromes were noted in 15 (4.7%) patients. A composite endpoint of periprocedural stroke, death, or cardiac event was noted in 31 patients (9.7%). There were 2 patients who had perioperative mortality, one of whom had a preoperative renal failure and succumbed to an acute coronary syndrome post-procedure. The other patient had a major ipsilateral stroke. Other complications like transient cranial neuropathy, wound hematoma, and hyperperfusion syndrome occurred in 7.8%, 3.1%, and 0.9% of patients respectively.
The baseline vascular risk factors or the type of the initial vascular event (TIA or stroke) did not influence the risk of post-operative ischemic events as detailed in Table 2. However, there was a trend for a higher incidence of post-operative stroke or TIA among those who underwent the procedure within 2 weeks, although not statistically significant (p = 0.068). The presence of co-existing significant tandem intracranial atherosclerosis did not predict the risk of periprocedural cerebral ischemic events (p = 0.691). No patient with a contralateral ICA occlusion had an adverse event (p = 0.398).
Table 2.
Factors associated with perioperative ischemic events
| Variable | Total (N = 319) | Patients with ischemic events, n (%) | p value | 
|---|---|---|---|
| Study population | 319 | 20 (6.3) | |
| Age | 0.278 | ||
| <65 years | 149 | 7 (4.7) | |
| ≥65 years | 170 | 13 (7.7) | |
| Sex | 0.969 | ||
| Male | 247 | 15 (6.1) | |
| Female | 72 | 5 (6.9) | |
| Hypertension | 0.376 | ||
| No | 50 | 5 (10) | |
| Yes | 269 | 15 (5.6) | |
| Diabetes mellitus | 0.844 | ||
| No | 121 | 8 (6.6) | |
| Yes | 198 | 12 (6.1) | |
| Smoking | 0.267 | ||
| No | 248 | 18 (7.3) | |
| Yes | 71 | 2 (2.8) | |
| Coronary artery disease | 0.288 | ||
| No | 249 | 18 (7.2) | |
| Yes | 70 | 2 (2.9) | |
| Peripheral arterial disease | 0.728 | ||
| No | 286 | 19 (6.6) | |
| Yes | 33 | 1 (3.8) | |
| Dyslipidemia | 0.163 | ||
| No | 220 | 11 (5) | |
| Yes | 99 | 9 (9.1) | |
| Serum creatinine | 0.801 | ||
| ≤1.3 mg/dL | 268 | 16 (5.9) | |
| >1.3 mg/dL | 51 | 4 (7.8) | |
| Timing of CEA | 0.068 | ||
| ≤14 days | 26 | 4 (15.4) | |
| >14 days | 293 | 16 (5.5) | |
| Type of initial ischemic event | >0.999 | ||
| Retinal TIA | 13 | 0 (0) | |
| Hemispheric TIA | 99 | 6 (6.1) | |
| Stroke | 207 | 14 (6.8) | |
| Symptomatic extracranial stenosis | >0.999 | ||
| <70% stenosis | 49 | 3 (6.1) | |
| ≥70% stenosis | 270 | 17 (6.3) | |
| Ulcerated plaque | 0.715 | ||
| No | 256 | 15 (5.9) | |
| Yes | 63 | 5 (7.9) | |
| Ipsilateral intracranial stenosis | 0.691 | ||
| <50% stenosis | 242 | 14 (5.8) | |
| ≥50% stenosis | 77 | 6 (7.8) | |
| Contralateral carotid occlusion | 0.398 | ||
| No | 295 | 20 (6.8) | |
| Yes | 24 | 0 (0) | |
| Pattern of infarcts embolic | 0.707 | ||
| No | 108 | 6 (5.6) | |
| Yes | 211 | 14 (6.6) | |
| Hemodynamic | 0.189 | ||
| No | 124 | 5 (4.8) | |
| Yes | 195 | 15 (7.7) | 
Discussion
The major findings in our study was that a large proportion of our patients for CEA presented late after the ischemic event, mostly after a stroke rather than TIA, and had high-grade stenosis of the symptomatic carotid. None of the clinical or imaging features including co-existent tandem significant intracranial atherosclerotic disease or a contralateral carotid occlusion (CCO) predicted perioperative cerebral ischemic events.
Our patients were predominantly elderly males, that is, similar to the existing literature. Similar to the data from large registries, there was no difference in the perioperative outcomes with respect to gender [15, 16]. Only 23% of our patients were females, and this may be attributed to the prevailing gender and cultural bias, the perception that women are at higher risk for periprocedural events and the lesser benefit in women referred late for surgery.
Our study provides real-world data on the timing of CEA which does not reflect the guideline recommended timing of less than 2 weeks and instead emphasizes the delay. Compared to the Western data of about 39–72% of patients undergoing early CEA [8–10], only 8% in our cohort underwent CEA within 2 weeks. On the contrary, we found a trend for a higher incidence of perioperative events in those who underwent the procedure within 2 weeks of onset of symptoms, without statistical significance (p = 0.068). The reason for this is less clear, although except for one patient, all had high-grade stenosis of the ipsilateral carotid, 3 of them had ulcerated plaques, features that are deemed to have higher perioperative risks. As the number of patients with an adverse perioperative event in those who had early CEA was small (n = 4), further statistical analysis on predictors could not be done.
About two-thirds of our patients presented after a stroke, despite 40% of them having preceding TIAs. Since patients recover completely after a TIA, they may not appreciate the gravity of the situation and often ignore it until they have a stroke. An Indian study had previously reported that the lack of recognition of stroke symptoms by the patients, delay in seeking medical care and referral to a stroke neurologist or vascular surgeon, delay in decision-making for the procedure, getting a second opinion from another specialist, and financial constraints were factors contributing to delay in endarterectomy [17]. A study from Pakistan reported that 15% of patients were not aware of a surgical option for carotid stenosis [18]. Our results were similar to that of few other studies in Asian countries, where the predominant presentation was with a stroke [12–14, 19]. This is in contrast to the Western world wherein more than 50% of patients undergo CEA after a hemispheric or a retinal TIA [8–11].
The Asian population is known to have a higher prevalence of intracranial atherosclerosis as compared to the Western world with about 18–48% of patients having co-existent significant intracranial and extracranial atherosclerotic disease [20, 21]. Our findings replicated the same with about one-fourth of our cohort having significant co-existent tandem intracranial atherosclerosis. An analysis from the NASCET cohort reported that the benefit of CEA was less certain in those with severe intracranial atherosclerosis in view of smaller numbers [22]. Our results were similar to a large single-center Italian study that reported no difference in the occurrence of perioperative events among those with and without co-existent tandem intracranial atherosclerosis, who underwent CEA [11]. The presence of a proximal lesion may overestimate a distal lesion due to reduced flow. The fact that tandem intracranial lesion did not influence the outcomes in our study may suggest that there might be overestimation of the percentage of intracranial stenosis at least in some of them.
In the absence of RCTs, there is still a debate on the choice of carotid revascularization in patients with CCO with some studies favoring CEA [23, 24] and others favoring carotid artery stenting [25, 26]. The Western world recommends carotid artery stenting over CEA in such patient groups as reflected by the policies of Medicare and Medicaid services in the USA. However, none of our patients with a CCO had an adverse periprocedural event. This finding is reassuring and suggests that CEA is a safe procedure in these patients.
We had a higher post-operative stroke or death rate (6.7%) than the recommended guidelines. This reflects a real-world scenario as opposed to RCT data. However, none of the clinical or imaging factors predicted the occurrence of post-operative cerebral ischemic events (TIA or stroke). About 9.4% of our patients had near occlusion of the symptomatic carotid who were taken up for CEA. Chen et al. [27] had performed CEA in 14.7% patients with near occlusion with a periprocedural stroke/death rate of 4.08% while a study from Pakistan reported perioperative stroke rates of 4.8% [28]. It is possible that the higher event rate in our population may be explained by the much higher preprocedural risk factors, although there was no statistically significant association for the same.
About 4.7% of our patients had cardiac events post-procedure which is higher than the 3.63% reported by Chen et al. [27]. The presence of coronary artery disease was similar between the two cohorts, although we had a higher proportion of patients with peripheral vascular disease (10%) which is a marker for occult cardiovascular disease. All our patients underwent surgery under general anesthesia, which has been reported to have more incidence of cardiac complications [29].
Ours is the largest Indian study and one among the largest single-center Asian series [27, 30] on the clinic-radiological profile of patients with symptomatic carotid stenosis who underwent CEA, looking at profile of the patients and the perioperative events. Our study highlights the need for public awareness on TIA and stroke and policies on early referral of patients for CEA. The limitations of our study include retrospective review of data and its potential confounding factors. We did not review the intraoperative characteristics such as cross-clamping time, technique of surgery, the histopathology of the excised plaque, and hemodynamic fluctuations during the procedure that could have given us a better insight into the reasons for the perioperative events.
Conclusion
There is a delay in patients undergoing CEA in our country, with majority presenting only after a stroke and high-grade stenosis of the symptomatic carotid. CEA can be safely performed in patients with CCO and those with co-existent significant tandem intracranial atherosclerotic lesions.
Statement of Ethics
The study protocol was reviewed and approved by the Institutional Ethics Committee, approval number: SCT/IEC/1896/AUGUST/2022. The study was granted an exemption from requiring informed consent by our Institutional Ethics Committee as it was a review of retrospective data.
Conflict of Interest Statement
The authors report no conflict of interest.
Funding Sources
There was no funding received for this study.
Author Contributions
Naveen Kumar Paramasivan and PN Sylaja conceived and designed the study and drafted the manuscript; Naveen Kumar Paramasivan collected the data; Jissa VT did the statistical analysis; and Naveen Kumar Paramasivan, PN Sylaja, Shivanesan Pitchai, Unnikrishnan Madathipat, Sapna Erat Sreedharan, and Sajith Sukumaran critically revised the manuscript.
Funding Statement
There was no funding received for this study.
Data Availability Statement
All data generated or analyzed during this study are included in this article. Further inquiries can be directed to the corresponding author.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
All data generated or analyzed during this study are included in this article. Further inquiries can be directed to the corresponding author.
