Abstract
This study aimed to report the clinical features and early and long-term outcomes of patients treated with carotid endarterectomy (CEA) combined with a routine shunt for carotid stenosis with the occlusion of the contralateral carotid artery (CCO), and to compare them with patients without contralateral occlusion (NO-CCO). A retrospective analysis included 301 patients who had carotid artery stenosis treated with CEA using a routine shunt. Of these patients, 35 patients and 266 patients were categorized into a CCO group and NO-CCO group, respectively. Demographics and short-term and long-term outcomes were documented and compared. The demographic characteristics were not significantly different between the two groups. The periprocedural mortality, stroke rate, and rate of periprocedural myocardial infarction were not significantly different between both groups. The mean follow-up period for long-term outcomes was 34.45 ± 22.99 months, and the Kaplan–Meier analysis showed no statistical difference between both groups regarding stroke, myocardial infarction, and mortality. CEA combined with the routine shunt is an effective and durable procedure for carotid artery stenosis patients with CCO.
Keywords: carotid artery stenosis, contralateral occlusion, routine shunt, carotid endarterectomy
Introduction
The benefits of carotid endarterectomy (CEA) for patients with severe carotid atherosclerosis have been demonstrated by the European Carotid Surgery Trial (ECST)1) and The North American Symptomatic Carotid Trial (NASCET).2) The treatment for high-risk carotid artery stenosis, such as occlusion of the contralateral carotid artery (CCO) remains unclear.3–5) Approximately, 10% of patients with carotid stenosis have coexisting CCO.6) A study which focused on the natural history of patients with carotid stenosis and CCO reported that patients with CCO had a higher incidence of stroke compared to those without CCO.7) The increased stroke rates of patients with CCO may be due to their impaired cerebral functional reserves, making the brain more fragile.7) A routine intraoperative shunt could provide reliable cerebral protection8) and may benefit the carotid stenosis patients with CCO.
Consequently, we reviewed our experience of 301 CEAs performed using a routine intraoperative shunt and compared the clinical outcomes between patients with and without CCO. This study aimed to analyze the clinical features and perioperative and long-term outcomes of patients treated with CEA and routine shunt for carotid stenosis, and compared patients with CCO to those without CCO (NO-CCO).
Materials and Methods
Patient selection and diagnostic criteria
Between January 2011 and December 2014, 301 consecutive patients who underwent CEA and routine shunt at the China-Japan Friendship Hospital of Beijing, China were retrospectively reviewed. The protocol was approved by the Medical Ethics Committee of the China-Japan Friendship Hospital of Beijing, China. All carotid stenosis cases were treated with a first CEA and a routine intraoperative shunt, and were diagnosed with duplex ultrasonography combined with computed tomography (CT) computed tomography angiography (CTA), and/or magnetic resonance angiography (MRA). The patients with CCO were categorized into a CCO group, whereas the remaining patients with patent contralateral vessels were classified into group NO-CCO. Patient clinical characteristics were recorded and compared between both groups (Table 1). The clinical characteristics included age, gender, in-hospital days, and smoking which was defined as either the patient smoked >1 cigarette per day or had quit smoking for <2 years. Hypertension was defined as a systolic blood pressure >140 mmHg and/or diastolic blood pressure >90 mmHg. Peripheral artery disease was defined as any atherosclerotic disease leading to peripheral artery obstruction and an ankle-brachial index <0.9. Dyslipidemia was defined as a patient having one of the following: total cholesterol >200 mg/dL, low-density lipoprotein >120 mg/dL, or taking lipid-lowering medication. Renal insufficiency was described as a creatinine level >2 mg/dL. Symptomatic status was defined as having one of the following neurologic events within 6 months prior to the operation: amaurosis fugax, transient ischemic attack (TIA), and stroke.
Table 1. Demographic data and comorbidities of patients.
| Group CCO (n = 35) n (%) | Group NO-CCO (n = 266) n (%) | Total % (n) (n = 301) n (%) | P value | |
|---|---|---|---|---|
| Group distribution | 35 (11.6) | 266 (88.4) | 301 (100) | |
| Patients’ characteristics | ||||
| Men | 27 (77.1) | 219 (82.3) | 246 (81.7) | 0.485 |
| Age (years) | 65.1 ± 7.13 | 66.1 ± 8.89 | 65.97 ± 8.71 | 0.51 |
| Smoker | 19 (54.3) | 99 (37.2) | 118 (39.2) | 0.065 |
| In-hospital days | 22.0 ± 9.4 | 20.7 ± 11.6 | 20.85 ± 11.39 | 0.515 |
| Comorbidities | ||||
| CAD | 12 (34.3) | 71 (26.7) | 83 (27.6) | 0.345 |
| PAD | 8 (22.9) | 35 (13.2) | 43 (14.3) | 0.123 |
| Hypertension | 24 (68.6) | 199 (74.8) | 223 (74.1) | 0.428 |
| Diabetes | 16 (45.7) | 111 (41.7) | 127 (42.2) | 0.853 |
| Previous CI | 12 (34.3) | 81 (30.5) | 93 (30.9) | 0.644 |
| Dyslipidemia | 11 (31.4) | 77 (28.9) | 88 (29.2) | 0.762 |
| Renal insufficiency | 1 (2.9) | 15 (5.6) | 16 (5.3) | 0.490 |
| Symptoms | ||||
| Asymptomatic | 21 (60.0) | 136 (51.1) | 157 (52.2) | 0.323 |
| TIA | 7 (20.0) | 57 (21.4) | 64 (21.3) | |
| Amaurosis | 0 (0) | 21 (7.9) | 21 (6.9) | |
| Stroke | 7 (20.0) | 52 (19.5) | 59 (19.6) | |
CAD: coronary artery disease; PAD: peripheral artery disease; TIA: transient ischemic attack; CI: cerebral infarction; CCO: contralateral carotid occlusion; NO-CCO: without CCO
Surgical procedures
CEA was performed for carotid stenosis ≥50% in symptomatic patients or ≥70% (NASCET9) stenosis evaluation criteria) in asymptomatic patients. All operations complied with the principles of the Declaration of Helsinki and written informed consent was acquired from all patients. All patients were under general anesthesia and were operated using conventional endarterectomy techniques with routine intraoperative shunting (Edwards, VASCUSHUNT, 9F–11F, Fig. 1) for cerebral protection and the cross-clamp time was less than 3 minutes in all cases. All the carotid arteries were closed with a polyester–urethane vascular patch. If a postoperative neurological deficit was noted, neuroimaging such as CT was performed.
Fig. 1. (A) Exposure of the common carotid, internal carotid, and external carotid artery; (B) insertion of the carotid shunt; and (C) the shunt has been inserted and we are removing the plaque.
Follow-up and outcomes
All patients were carefully followed and the main short-term outcomes were stroke, myocardial infarction, and death within 30 days after surgery. Incidences of perioperative cranial nerve injury and hematoma were also recorded. Long-term complications were followed through either a clinical check or telephonic interview 6 and 12 months after surgery and then annually during follow-up. Mortality, stroke, or myocardial infarction, and the date of every event were all documented.
Statistical analyses
Continuous data are reported as mean ± standard deviation and were compared using the student’s t-test. Categorical variables are described as percentage and frequency and were compared via the chi-square test. The survival curves were estimated using the Kaplan–Meier method and curves were compared using the log-rank test. SPSS version 21.0 (IBM, Armonk, NY, USA) was used for statistical analyses and P <0.05 was considered significant.
Results
Data for 301 patients admitted in our hospital for CEA from January 2011 to December 2014 were collected. The mean age of the whole population was 66.0 ± 8.7 years. The percentage of male patients was 81.7% (n = 246) and the mean in-hospital stay was 20.9 ± 11.4 days. The mean stenosis grade was 87.2 ± 11.9%. The CCO group included 35 patients and the NO-CCO group included 266 patients. The demographic characteristics of the two groups are shown in Table 1. The mean age was 65.1 ± 7.1 years in the group CCO and 66.1 ± 8.9 years in the NO-CCO group. The percentage of male patients was 77.1% and 82.3%, respectively, and the percentage of smokers was 54.3% and 37.2%, respectively, in the CCO and NO-CCO groups. A total of 125 patients (47%) received right CEA in the NO-CCO group, whereas 16 patients (45.7%) received right CEA in the CCO group. In all, 60% and 51.1% of the patients were symptomatic in the CCO and NO-CCO groups, respectively. All the patient characteristics were not significantly different between the two groups (Table 1).
Perioperative outcomes
Perioperative stroke occurred in one case in the CCO group and in six cases in the NO-CCO group. Perioperative TIA occurred in three cases and all the three cases were in the NO-CCO group. There were two cases of myocardial infraction and three cases of death, and all were in the NO-CCO group. Perioperative cranial nerve injury occurred in one case in the CCO group and 12 cases in the NO-CCO group. There were four cases of hematoma and all occurred in the NO-CCO group. All complications within the first 30 days are shown in Table 2, and there was no significant difference in any complications between both groups (Table 2).
Table 2. Adverse events within 30 days.
| In-hospital adverse event | Group O (n = 35) n (%) | Group C (n = 266) n (%) | P value |
|---|---|---|---|
| TIA | 0 (0) | 3 (1.1) | 0.528 |
| Stroke | 1 (2.9) | 6 (2.3) | 0.824 |
| Mortality | 0 (0) | 3 (1.1) | 0.528 |
| MI | 0 (0) | 2 (0.8) | 0.607 |
| Cranial nerve injury | 1 (2.9) | 12 (4.5) | 0.651 |
| Hematoma | 0 (0) | 4 (1.5) | 0.465 |
MI: myocardial infarction; TIA: transient ischemic attack
Long-term follow-up
A total of 286 patients were included in the analysis. Two patients (5.7%) in the CCO group and 13 patients (4.9%) in the NO-CCO group were lost to follow-up and could not be contacted by telephone. The mean follow-up period was 29.27 ± 16.62 months and about 57% patients were followed for more than 2 years. In all, 22 patients (7.7%) had a stroke during the follow-up (two patients, 6.1%, in the CCO group and 20 patients, 7.9%, in the NO-CCO group). Kaplan–Meier curves for stroke are shown in Fig. 2A and there were no significant differences between both groups. In all, 15 patients (5.2%) had myocardial infarction during the follow-up (one patient, 3%, in the CCO group and 14 patients, 5.5%, in the NO-CCO group). Kaplan–Meier curves for myocardial infarction are shown in Fig. 2B and there were no statistical differences between the two groups. The overall mortality rate was 5.2% (15 patients) during the follow-up (two patients, 6.1%, in the CCO group and 13 patients, 5.1%, in the NO-CCO group) and there were no significant differences between both groups. The Kaplan–Meier curves for mortality are shown in Fig. 2C.
Fig. 2. (A) Survival curves (Kaplan–Meier) for stroke in patients with CCO and without CCO; (B) survival curves (Kaplan–Meier) for myocardial infarction in patients with CCO and without CCO; (C) survival curves (Kaplan–Meier) for mortality in patients with CCO and without CCO. CCO: contralateral carotid occlusion; NO-CCO: without CCO.
Discussion
Our results suggest that CEA combined with a routine intraoperative shunt may be a safe and effective procedure for carotid stenosis with CCO. CEA has been confirmed as a durable procedure for carotid stenosis by many prospective randomized control trials (RCTs), such as NASCET, ECST, etc.1,2,10) The presence of CCO has been traditionally regarded as a risk factor for perioperative complications after CEA.11) NASCET reported that the patients with CCO had a significantly higher incidence of 30-day complications. AbuRahma et al.7) reported on the natural history of carotid stenosis patients with CCO and found that patients in this group who received maximal medical therapy had a higher incidence of complications compared to carotid stenosis patients without CCO.
Although a number of centers have reported their experience regarding the treatment of patients with CCO, their conclusions have not been consistent.4,5,12–14) There were no clear indications for the treatment of this subgroup of patients. Some researchers found that CCO did not increase the incidence of complications during carotid artery stenting procedure and argued that this procedure was superior to CEA for the treatment of patients with CCO. Ricotta reported that in CEA patients, CCO was a risk factor because the stroke rates were higher than in patients without CCO in symptomatic (1.7% vs. 4.9%, P = 0.0012) and asymptomatic (0.7% vs. 2.0%, P = 0.0095) patients.13) Unlike the routine shunt in our department, Ricotta selectively performed shunting in 63.5% of patients with CCO and in 55.7% of patients without CCO. Contrastingly, in carotid stenosis patients, CCO did not significantly increase the stroke rates (2.1% vs. 2.3% for patients with and without CCO). Capoccia et al.12) reported that patients with CCO were at high risk for perioperative complications, and selective shunting was used for cerebral protection in their series. Thus, they concluded that in patients with CCO, the benefit of CEA was lost. A meta-analysis by Maatz et al.15) revealed that the perioperative stroke rate in patients with CCO was significantly greater than that in patients without CCO (3.7% vs. 2.4%, P = 0.002). There is some debate regarding the safety of CEA in patients with CCO although some authors have published short-term studies on CEA with CCO that show no significant increase in complications in these patients.
CCO might be a risk factor for perioperative complications during CEA for many reasons. Patients with CCO have a significant reduction in both cerebrovascular reactivity16) and cerebral function reserve.12) Kretz et al. demonstrated that CCO impaired the cerebral functional reserves and made the brains more fragile. CCO was identified as an independent predictor of intolerance to clamping; thus, shunt use increased due to the decreased tolerance of carotid clamping.17) Intracranial collateral pathways and cerebral hemodynamics could also be influenced by the CCO.13) Oka showed the improvement of cerebral blood flow during the follow-up of carotid stenosis treatment and further supported the theory of hemodynamic impairment.18) Increased perfusion instability further highlighted the importance of cerebral protection methods such as shunting.
There is considerable debate about the shunting strategies during CEA, including routine shunting, selective shunting, and no shunting.19) Routine shunting has been used for cerebral protection during CEA for a long time.8) Its advantages include the avoidance of intraoperative neurologic monitoring and ease of shunt insertion.8) A report by Goodney et al.20) showed that surgeons using routine shunting during CEA in patients with CCO achieved a lower incidence of perioperative complications compared with surgeons who used selective shunting during CEA. However, another study showed that shunts are not necessary and are associated with air embolization, distal flap creation, displacement of embolic material, etc.4) Our center has ample experience in shunt usage and none of these complications occurred in our 301 patients who underwent routine shunting. Consequently, we believe that the shunt should be safe if it is applied correctly and carefully. Conflicting data have been reported in the treatment of carotid stenosis with CCO. Our results did not identify CCO as a risk factor for complications during CEA combined with a routine shunt, and suggests that carotid artery stenting is not superior to CEA for patients with carotid stenosis.
There were several limitations to our study. First, the study was a single-center retrospective study and randomization could not be used in this study. Second, the sample size was relatively small so it may be difficult to reach a definitive conclusion from our results. Further studies with larger sample sizes and randomization are needed to verify our results. Third, Willis circle was not evaluated in every patient. Finally, glomerular filtration rate measurement is not routinely performed, so our diagnosis of renal insufficiency was based on creatinine levels.21)
Conclusion
The CCO and NO-CCO groups had similar perioperative and long-term outcomes when the patients were treated using CEA and routine shunting. Moreover, the presence of CCO cannot be considered a risk factor for carotid surgery. CEA with routine shunting is an effective and durable procedure for carotid stenosis patients with CCO compared with those without CCO.
Acknowledgment
This work was supported by grants from the International S&T cooperation program (2013DFA31900) and the National Natural Science Foundation of China (nos. 81670443, 81670275) and National Science and Technology support program of China (No. 2015BAI12B03).
Disclosure Statement
The authors declare no competing financial interests and no conflict of interest.
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