Abstract
Objectives
The benefit of carotid endarterectomy (CEA) may be diminished by cranial nerve injury (CNI). Using a quality improvement registry, we aimed to identify the nerves affected, duration of symptoms (transient vs. persistent), and clinical predictors of CNI.
Methods
We identified all patients undergoing CEA in the Vascular Study Group of New England (VSGNE) between 2003 and 2011. Surgeon-observed CNI rate was determined at discharge (postoperative CNI) and at follow-up to determine persistent CNI (CNIs that persisted at routine follow-up visit). Hierarchical multivariable model controlling for surgeon and hospital was used to assess independent predictors for postoperative CNI.
Results
A total of 6,878 patients (33.8% symptomatic) were included for analyses. CNI rate at discharge was 5.6% (n = 382). Sixty patients (0.7%) had more than one nerve affected. The hypoglossal nerve was most frequently involved (n = 185, 2.7%), followed by the facial (n = 128, 1.9%), the vagus (n = 49, 0.7%), and the glossopharyngeal (n = 33, 0.5%) nerve. The vast majority of these CNIs were transient; only 47 patients (0.7%) had a persistent CNI at their follow-up visit (median 10.0 months, range 0.3–15.6 months). Patients with perioperative stroke (0.9%, n = 64) had significantly higher risk of CNI (n = 15, CNI risk 23.4%, p < .01). Predictors for CNI were urgent procedures (OR 1.6, 95% CI 1.2–2.1, p < .01), immediate re-exploration after closure under the same anesthetic (OR 2.0, 95% CI 1.3–3.0, p < .01), and return to the operating room for a neurologic event or bleeding (OR 2.3, 95% CI 1.4–3.8, p < .01), but not redo CEA (OR 1.0, 95% CI 0.5–1.9, p = .90) or prior cervical radiation (OR 0.9, 95% CI 0.3–2.5, p = .80).
Conclusions
As patients are currently selected in the VSGNE, persistent CNI after CEA is rare. While conditions of urgency and (sub)acute reintervention carried increased risk for postoperative CNI, a history of prior ipsilateral CEA or cervical radiation was not associated with increased CNI rate.
Keywords: Cranial nerve injury, Endarterectomy, Carotid
INTRODUCTION
Carotid endarterectomy (CEA) has been established as the standard of care for long-term stroke prevention in patients with severe carotid stenosis in an average risk population.1,2 Carotid artery stenting (CAS) has emerged as an alternative to CEA, but the comparative effectiveness of these modalities remains controversial.
The advantage of a lower perioperative stroke rate with CEA than with CAS may be somewhat offset by the added risk of postoperative myocardial infarction (MI) and cranial nerve injury (CNI) after surgery.3–5 However, the clinical importance of CNI as a relevant safety endpoint is debatable.3,6–8 Although most postoperative nerve lesions seem transient, the actual rate of persistent CNI following CEA remains unclear.8–11 Postoperative CNI rates vary between 3% and 27%, depending on the observer, definition of CNI, and study design.11,12 Prior studies have been limited to single institution observations with small sample size and highly selected surgeons or patients participating in randomized controlled trials. Very few studies commented on the patient characteristics or operative conditions associated with increased risk for CNI.11,13 Higher rates are often reported after redo CEA and prior radiation, but most of these studies were not designed to identify independent predictors for CNI given its low event rate.14–16 Using a large quality improvement registry reflective of real-world vascular surgery practice, we aimed to (a) establish rates of surgeon-observed postoperative and persistent CNI after CEA, (b) identify the specific nerves at risk for injury, and (c) identify clinical predictors for postoperative CNI.
MATERIALS AND METHODS
Database
We used prospective data collected by the Vascular Study Group of New England (VSGNE). The VSGNE is a regional quality improvement initiative developed by vascular surgeons in 2001, and currently involves over 180 physicians (vascular surgeons, radiologists, and cardiologists) at 30 centers (14 academic, 16 community). The goal of this cooperative group of clinicians, hospital administrators, and research personnel is to continuously improve the quality, safety, effectiveness, and cost of caring for patients with vascular disease. Preoperative clinical characteristics, imaging studies, perioperative outcome noted at discharge, and follow-up data are collected from eight vascular procedures (including CEA) and entered in the registry by trained nurses or clinical data abstractors. Surgeons enter operative details including complications. Research analysts are blinded to patient, surgeon, and hospital identity. Further details on this registry have been published previously and are available at http://www.vascularweb.org/regionalgroups/vsgne. VSGNE data have been validated for completeness using audits of discharge claims data from each participating institution to ensure entry of all patients.17,18
Patients
Our study sample included all patients in the VSGNE who underwent CEA between January 2003 and December 2011 for whom information on CNI was available at time of discharge and at one later time point after discharge (nerve injury recorded during surgical follow-up visit). This was done to obtain a valid sample to determine CNI rate at discharge and to assess the proportion of CNIs that resolved or persisted after discharge.
Endpoints and measurements
Primary endpoints were any CNI at discharge and the rate of persistent CNI at follow-up for both symptomatic and asymptomatic patients. The surgeon identified the clinical manifestation of the nerve injury after surgery. A CNI will be reported to the VSGNE if there was no palsy present before surgery. Injury to the following nerves are distinguished: facial nerve (VII), facial droop; glossopharyngeal nerve (IX), swallowing difficulty unless other diagnosis confirmed; vagus nerve (X), hoarseness unless laryngoscopy normal; hypoglossal nerve (XII), any tongue deviation or discoordination. The VSGNE also records other “non-specified” cranial nerve injuries (e.g. accessory nerve [XI], trigeminal nerve [V], or injuries to one of the abovementioned cranial nerves that were not further specified during data entry). The real-world nature of our database does not allow routine examination of patients postoperatively by a neurologist or otolaryngologist to identify CNI. Therefore, objective tests such as laryngoscopy for vocal cord function were not used routinely and their use was not recorded. Persistent CNI was identified by the vascular surgeon and defined as a CNI at discharge that was not resolved at the time of the surgical follow-up visit. In the VSGNE, the status of the CNI has to be entered in the registry as a categorical variable during regular follow-up visits, specifying “no CNI” versus “resolved CNI” versus “persistent CNI”. Because no exact time to event is calculated for CNI at follow-up, the median time with corresponding interquartile ranges (IQRs) to follow-up was calculated. Although the VSGNE aims to collect follow-up data at 1 year after the procedure, the time to follow-up in the database varies between patients, reflecting real-world practice. Symptomatic patients were defined as having preoperative ipsilateral cortical neurological symptoms prior to surgery.17 “Immediate reoperation” included surgical revision after closure of the artery in the operating room. Reasons for immediate reoperation may include intimal flap, debris, or residual plaque on completion imaging studies.19 “Return to the operating room” included reoperations after a patient had left the operating room. Causes for return to the operating room included neurologic events or bleeding that required reintervention. The surgeon performing the CEA made the designation of urgent cases versus elective cases. Urgent cases may include patients with stroke in evolution or crescendo transient ischemic attacks (TIAs). This was reflected by the fact that the vast majority of urgent cases were symptomatic and admitted to the hospital preoperatively (as opposed to same-day admissions) (Supplementary Appendix).
Statistical analysis
Associations of preoperative patient characteristics, operative details, and perioperative outcome with postoperative CNI were examined using the χ2 test and the Fisher exact test for categorical variables. To gain insight into factors independently associated with CNI, all variables with values of p < .2 in the previously described bivariate analyses were used to develop a multivariable regression model. A multilevel hierarchical model (data structure: patient, surgeon, center) was used to adjust for surgeon and centers within the VSGNE.20 This type of modeling uses a random intercept that accounts for all variable factors between hospitals and surgeons in the VSGNE, including surgeon and hospital volume.
Associations were calculated using manual elimination procedures, in which all candidate variables were entered in the first step and removed stepwise based on the highest non-significant p value. A p value <.05 was considered significant. Odds ratios (OR) and corresponding 95% confidence interval (CI) were reported. SPSS version 20.0 statistical software (IBM, SPSS Inc, Chicago, IL, USA) was used for statistical analyses.
RESULTS
Of all 9,362 patients undergoing isolated CEAs, 2,484 (26.5%) had missing data for CNI and were therefore excluded from this analysis. Of those, 1% died (n = 24) during hospital admission and 14.9% (n = 370) after discharge. For the remaining missing patients (84.1%), CNI information was not available at one later time point after discharge due to lack of follow-up. We performed a subgroup analysis of these excluded patients confirming that no important information on CNI was lost for the purpose of this study. In particular, the CNI rate at discharge in these excluded patients was similar to the CNI rate in our final study sample (n = 136, 5.5%). This also had no impact on the predictors for CNI.
In total, 6,878 CEAs (33.8% symptomatic) from 23 centers performed by 104 surgeons were included. Median caseload per center and surgeon were 85 and 27 respectively. The mean age was 69 years (SD ± 9.3 years) and 60.2% were men. A total of 152 (2.2%) patients underwent redo surgery following prior ipsilateral CEA, and 88 (1.3%) had a history of previous cervical radiation therapy (Table 1); 10% of the patients were operated under locoregional anesthesia and 10% were urgent procedures (as opposed to elective procedures). In 217 (3.2%) patients, immediate re-exploration after closure was performed. Another 111 patients (1.6%) were taken back to the operating room for neurologic events (TIA or stroke, n = 26), bleeding (n = 62), or unknown (n = 23) complications after awakening from anesthesia. Median length of stay was 1.5 days (IQR 0). At 30 days, the stroke rate was 0.9% (n = 64) (symptomatic 1.2% [n = 29] and asymptomatic 0.8% [n = 35]) and MI rate was 0.9% (n = 63).
Table 1.
Bivariate associations of preoperative patient characteristics with cranial nerve injury (CNI) of 6878 patients undergoing carotid endarterectomy (CEA).
| Total | CNI | p | OR | 95% CI | |||
|---|---|---|---|---|---|---|---|
| N | % | N | % | ||||
| Age >80 years | 972 | 14.1 | 59 | 6.1 | .45 | 1.1 | 0.8–1.5 |
| Gender (male) | 4,141 | 60.2 | 288 | 5.5 | .83 | 1.0 | 0.8–1.3 |
| Race (white) | 6,778 | 98.6 | 376 | 5.5 | .82 | 0.9 | 0.4–2.1 |
| Ipsilateral symptoms | 2,325 | 33.8 | 148 | 6.4 | .03 | 1.3 | 1.02–1.6 |
| Smoking (prior or current) | 5,481 | 79.8 | 311 | 5.7 | .39 | 1.1 | 0.9–1.5 |
| Hypertension | 6,034 | 87.8 | 354 | 5.9 | <.01 | 1.8 | 1.3–2.7 |
| Diabetes | 2,090 | 30.4 | 106 | 5.1 | .30 | 0.9 | 0.7–1.1 |
| BMI | .12 | ||||||
| <18.5 | 205 | 3.1 | 13 | 6.3 | |||
| 18.5–24.9 | 1,822 | 27.4 | 123 | 6.8 | |||
| 25–29.9 | 2,591 | 39.0 | 138 | 5.3 | |||
| 30–34.9 | 1,346 | 20.2 | 67 | 5.0 | |||
| 35–40 | 472 | 7.1 | 23 | 4.9 | |||
| >40 | 214 | 3.2 | 7 | 3.3 | |||
| Contralateral occlusion | 417 | 6.1 | 28 | 6.7 | .3 | 1.2 | 0.8–1.8 |
| Previous radiation | 88 | 1.3 | 4 | 4.5 | 1 | 0.8 | 0.3–2.2 |
| Previous ipsilateral CEA | 152 | 2.2 | 8 | 5.3 | 1 | 0.9 | 0.5–1.9 |
Note. BMI = body mass index; CI = confidence interval; OR = odds ratio.
Cranial nerve injury
Overall, 382 patients had any CNI at discharge (5.6%). Symptomatic patients had higher rates (6.4%) than asymptomatic patients (5.1%, p < .05). The hypoglossal nerve (injured in 185 [2.7%]) and the facial nerve (injured in 128 [1.9%]) were most frequently involved, followed by the vagus nerve (injured in 49 [0.7%]) and the glossopharyngeal nerve (injured in 33 [0.5%]). Another 0.5% (n = 31) involved unspecified cranial nerves. Of all patients, 296 (4.3%) had a single deficit, 42 had two nerves (0.6%), and 13 patients (0.1%) had three or more nerves affected. Of the 382 patients who had a nerve injury at discharge, the deficit resolved over time in 88% (n = 335). Only 47 patients (0.7%) had a persistent injury at their follow-up visit (median 10.0 months, range 0.3–15.6 months). Median time to follow-up for all patients was 12.1 months (range 0.3– 57.6). Lesions of the hypoglossal (n = 7, 0.1%) and the facial nerve (n = 6, 0.1%) were the most persistent, followed by the vagus (n = 3, 0.1%) and the glossopharyngeal nerves (n = 1, 0.02%). Length of hospital stay was prolonged in patients with CNI compared with those without (2 days vs. 1.5 day, p < .01).
Predictors for postoperative nerve injury
On bivariate analyses of preoperative patient characteristics with CNI, no clinical relevant associations were identified for CNI (Table 1). Urgent procedures, immediate re-exploration and return to the operating room were associated with increased risk for CNI (Table 2). Type of procedure (eversion vs. longitudinal), shunt use, patch use (vs. primary closure of longitudinal endarterectomy), and type of anesthesia (locoregional vs. general) did not influence CNI. Patients with a perioperative stroke within 30 days (n = 64, 0.9%) had increased CNI (23.4% vs. no stroke 5.4%, p < .01). On multivariable regression, urgent procedures (OR 1.6, 95% CI, 1.2–2.1, p = .006), re-exploration (OR 2.0, 95% CI 1.3–3.0, p = .004), and return to the operating room (OR 2.3, 95% CI 1.4–3.8, p = .004) were independent risk factors for CNI (Table 3). Specifically, return to the operating room for stroke or TIA was predictive of CNI (OR 4.8, 95% CI 2.1–11.2, p = .002), while return to the operating room for bleeding did not reach significance (OR 1.6, 95% CI 0.8–3.3, p = .3). In a subgroup analyses among urgent cases, symptomatic patients had increased CNI compared with asymptomatic patients (8.5% vs. 4.0%, OR 2.3, 95% CI 0.9–5.4, p = .08). Among elective cases, a CNI rate between symptomatic and asymptomatic patients was comparable (5.7% vs. 5.2%, OR 1.1, 95% CI 0.9–1.4, p = .4). Because others have previously reported that prior radiation therapy and redo CEA can be predictive conditions for CNI, we forced them into our prediction model.15,16,21 However, no impact on CNI was identified among these variables: prior radiation therapy, OR 0.9, 95% CI 0.3–2.5, p = .8; and redo CEA, OR 1.0, 95% CI 0.5–2.1, p = .9.
Table 2.
Bivariate associations of procedural variables and outcome with cranial nerve injury (CNI) of 6,878 patients undergoing carotid endarterectomy (CEA).
| Total | CNI | p | OR | 95% CI | |||
|---|---|---|---|---|---|---|---|
| N | % | N | % | ||||
| Anesthesia | .60 | 0.9 | 0.6–1.3 | ||||
| General | 6,189 | 90.0 | 347 | 5.6 | |||
| Locoregional | 689 | 10.0 | 35 | 5.1 | |||
| Urgency | .02 | 1.4 | 1.1–2.0 | ||||
| Elective | 6,186 | 89.9 | 330 | 5.3 | |||
| Urgent | 692 | 10.1 | 42 | 7.5 | |||
| CEA type | .37 | 1.2 | 0.8–1.6 | ||||
| Longitudinal endarterectomy | 6,226 | 90.5 | 341 | 5.5 | |||
| Eversion technique | 651 | 9.5 | 41 | 6.3 | |||
| Shunt use | .37 | 0.9 | 0.7–1.1 | ||||
| No | 3,641 | 52.9 | 211 | 5.8 | |||
| Yes | 3,237 | 46.8 | 171 | 5.3 | |||
| Patch use | .32 | 0.8 | 0.5–1.2 | ||||
| No (primary closure of longitudinal endarterectomy) | 327 | 5.3 | 22 | 6.7 | |||
| Yes | 5,899 | 94.4 | 319 | 5.4 | |||
| Drain | .33 | 0.5 | 0.1–1.7 | ||||
| No | 655 | 79.6 | 23 | 3.5 | |||
| Yes | 168 | 20.4 | 3 | 1.8 | |||
| Re-exploration after closure | 217 | 3.2 | 21 | 9.7 | .01 | 1.9 | 1.2–3.0 |
| Return to the operating room | 111 | 1.6 | 16 | 14.4 | <.001 | 2.9 | 1.7–5.1 |
Note. CI =confidence interval; CNI =cranial nerve injury; OR =odds ratio.
Table 3.
Independent predictors for cranial nerve injury following carotid endarterectomy.
| Odds ratio | 95% CI | pa | |
|---|---|---|---|
| Urgent casesb | 1.6 | 1.2–2.1 | .006 |
| Immediate re-exploration | 2.0 | 1.3–3.0 | .004 |
| Return to the operating room | 2.3 | 1.4–3.8 | .004 |
Based on a hierarchical multilevel regression model accounting for surgeon and centers within the Vascular Study Group of New England.
vs. elective procedures.
Nerves at risk
In the situation of immediate reintervention after closure, a significant increased risk for vagus injury (n = 6, 2.8%) was identified. Patients who had to returned to the operating room after surgery were at increased risk for facial (n = 9, 8.1%), glossopharyngeal (n = 4, 3.6%), vagus (n = 5, 4.5%), and other non-specified nerves (n = 4, 3.6%), but not for hypoglossal nerve (n = 5, 4.5%) injury (Fig. 1). Urgent procedures were not associated with specific nerve injuries.
Figure 1.
Cranial nerve injury per predictor. *p < .05.
DISCUSSION
The postoperative risk for any CNI was 5.6% among patients undergoing CEA in the VSGNE. While most lesions were transient, 0.7% of patients had a persistent lesion at their follow-up consultation. Independent risk factors for post-operative cranial nerve injury were urgent cases, immediate re-exploration after closure, and return to the operating room.
The reported frequency of CNI in the published literature ranges from 3% to 27%.11,12 Variable study design (prospective vs. retrospective), the use of objective measurements (e.g. otolaryngeal examinations), the observer, and variation in the definition of CNI (sensory deficits vs. purely motor injuries) contribute to this wide variability. Yet, cranial (motor) nerve injury at discharge in the VSGNE (5.6%) was similar to prior large studies, such as the New York Carotid Artery Surgery study (NYCAS, 5.5%),22 the European Carotid Surgery Trial (ECST, 5.1%),13 the North American Symptomatic Carotid Endarterectomy Trial (8.6%),23 and the Carotid Revascularization Endarterectomy versus Stenting Trial (CREST, 4.7%).5 In the randomized trials, CNI was identified by an independent stroke neurologist that was not involved in the performance of the CEA itself, as opposed to surgeon-observed CNI in the large registries such as the NYCAS and the VSGNE. We found that symptomatic patients had higher rates of postoperative CNI than asymptomatic patients (6.4% vs. 5.1%), which was also seen in CREST (5.1% vs. 4.3%). This can be explained by a high CNI risk among symptomatic patients who underwent urgent procedures (8.5%), which proved to be independent predictor for CNI in our study.
Among the aforementioned studies, only the ECST reported CNI rates beyond hospital discharge. The ECST showed a persistent CNI rate of 0.5% at 4 months and 1 year.13 We found a comparable persistent CNI rate of 0.7% at a median interval of 10 months, confirming that most lesions are transient.8,9 The transient nature of most lesions suggests that the majority of CNIs are related to traction or cautery rather than transections.12,24 In CREST, CNI was not associated with a sustained impact on quality of life at 1 year, but at 2 weeks CAS patients reported less difficulty eating or swallowing than CEA patients.6 However, some have suggested that the effects from a CNI can be likened to having a minor stroke.3,7,8
Our results indicate that patients are at greatest risk for CNI during times of surgeon stress, and that surgeons should take particular care to protect specific nerves in conditions of urgency, re-exploration, and return to the operating room. In particular, the vagus nerve was at greatest risk in re-exploration cases, while all nerves but the facial nerve were at risk in patients who were taken back to the operating room. Patients who returned to the operating room for stroke had greater risk for CNI than patients who were taken back for bleeding. The relation of local complications (e.g. CNI) with stroke has previously been shown.22
Only one prior study with preoperative and postoperative examinations by an otolaryngologist reported on associations of specific nerves with patients or operative factors.11 They showed an overall CNI risk of 27% (51/190) at 2 days after surgery and found that plaque extension >2 cm was related to lesions of the vagus nerve (OR = 3.5; CI 1.09– 12.3, p = .03). The ESCT analyzed a limited number of risk factors to identify predictors for all nerve injuries. Operation longer than 2 hours was found to be the only predictive factor (HR 1.56, 95% CI 1.31–1.81 per 30-minute increment).13 While others have previously reported an increased risk for CNI after redo CEA and prior radiation,14,15,25 in this study we did not. Theoretically, these conditions can lead to more complex CEA procedures and, therefore, CNIs may be more frequent.26 Reported causative factors include absent tissue planes in the diseased vessel wall and (radiation-induced) fibrosis.27 The condition of the preoperative tissue in the cervical area could have resulted in differences in patient selection (CAS vs. CEA), and may possibly explain the difference with prior reports.
In reports prior to 1995, CAS was not readily available and accepted for patients with a hostile neck due to extensive radiation or prior neck surgery.21,25 In the current era of carotid stenting, it is likely that those with the most hostile necks are no longer selected for redo CEA.28
While the strength of the VGSNE database is its large size and detailed clinical data, reporting bias is inherent to any registry-based study and potentially leads to under-reporting of events. Yet, the lack of follow-up data on CNI for several patients in the VSGNE is most likely rather a data collection issue then reporting bias, since the postoperative rate of CNI in patients with and without follow-up data was similar (5.5% vs. 5.6%). Our subgroup analysis also affirmed that there was no impact on the identification of predictors. Therefore, it is very unlikely that the subset of excluded patients due to lack of follow-up will change the results of this study. The exact time to recovery remains unknown due to the lack of follow-up at set time points in the VSGNE. Our analysis was also limited by the lack of a formal protocol including objective CNI measurement at set time points. Therefore, it seems reasonable that subtle nerve lesions may have been missed and our rate of 5.6% could be underestimating CNI.24 Some hoarseness may have been incorrectly ascribed to trauma from endotracheal intubation rather than CNI because of the lack of routine otolaryngoscopic evaluation. Since the rate of CNI was similar for those undergoing locoregional and general anesthesia, this is not very likely. The clinical assessment of persistent injury to the vagus nerve also seems difficult, since patients are often able to compensate deficits resulting in a “normal” voice. On the other hand, it has also been suggested that the use of objective methods may lead to the inclusion of several asymptomatic deficits with minor clinical relevance.13,24 Therefore, we believe that the majority of clinically relevant injuries are captured in the VSGNE and that these rates of CNI could serve as a benchmark for everyday practice.
As patients are currently selected in the VSGNE, persistent CNI after CEA is rare. CNI is more likely in urgent procedures and after re-exploration in the operating room, or return to the operating room; while redo CEA and a history of prior cervical radiation were not associated with increased CNI rate.
Supplementary Material
WHAT THIS PAPER ADDS.
The benefit of carotid endarterectomy (CEA) may be diminished by cranial nerve injury (CNI). However, the long-term incidence of postoperative CNI remains unknown and limited data are available on its predictors. Using a quality improvement registry, we identified the nerves affected, duration of symptoms (transient vs. persistent) and clinical predictors of CNI.
Acknowledgments
FUNDING
This work was supported by the NIH T32 Harvard-Longwood Research Training in Vascular Surgery Grant HL007734.
Footnotes
CONFLICT OF INTEREST
Marc L. Schermerhorn is a consultant for Endologix and Medtronic. Frans L. Moll is a consultant for Best Doctors and for Medtronic.
APPENDIX A. SUPPLEMENTARY DATA
Supplementary data related to this article can be found at http://dx.doi.org/10.1016/j.ejvs.2013.09.022.
REFERENCES
- 1.Beneficial effect of carotid endarterectomy in symptomatic patients with high-grade carotid stenosis. North American Symptomatic Carotid Endarterectomy Trial Collaborators. N Engl J Med. 1991;325:445–453. doi: 10.1056/NEJM199108153250701. [DOI] [PubMed] [Google Scholar]
- 2.Endarterectomy for asymptomatic carotid artery stenosis. Executive Committee for the Asymptomatic Carotid Atherosclerosis Study. J Am Med Assoc. 1995;273:1421–1428. [PubMed] [Google Scholar]
- 3.Meier P, Knapp G, Tamhane U, Chaturvedi S, Gurm HS. Short term and intermediate term comparison of endarterectomy versus stenting for carotid artery stenosis: systematic review and meta-analysis of randomised controlled clinical trials. BMJ. 2010;340:c467. doi: 10.1136/bmj.c467. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Economopoulos KP, Sergentanis TN, Tsivgoulis G, Mariolis AD, Stefanadis C. Carotid artery stenting versus carotid endarterectomy: a comprehensive meta-analysis of short-term and long-term outcomes. Stroke. 2011;42:687–692. doi: 10.1161/STROKEAHA.110.606079. [DOI] [PubMed] [Google Scholar]
- 5.Brott TG, Hobson RW, 2nd, Howard G, Roubin GS, Clark WM, Brooks W, et al. Stenting versus endarterectomy for treatment of carotid-artery stenosis. N Engl J Med. 2010;363:11–23. doi: 10.1056/NEJMoa0912321. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Cohen DJ, Stolker JM, Wang K, Magnuson EA, Clark WM, Demaerschalk BM, et al. Health-related quality of life after carotid stenting versus carotid endarterectomy: results from CREST (Carotid Revascularization Endarterectomy Versus Stenting Trial) J Am Coll Cardiol. 2011;58:1557–1565. doi: 10.1016/j.jacc.2011.05.054. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Bangalore S, Kumar S, Wetterslev J, Bavry AA, Gluud C, Cutlip DE, et al. Carotid artery stenting vs carotid endarterectomy: meta-analysis and diversity-adjusted trial sequential analysis of randomized trials. Arch Neurol. 2011;68:172–184. doi: 10.1001/archneurol.2010.262. [DOI] [PubMed] [Google Scholar]
- 8.Schauber MD, Fontenelle LJ, Solomon JW, Hanson TL. Cranial/cervical nerve dysfunction after carotid endarterectomy. J Vasc Surg. 1997;25:481–487. doi: 10.1016/s0741-5214(97)70258-1. [DOI] [PubMed] [Google Scholar]
- 9.Ballotta E, Da Giau G, Renon L, Narne S, Saladini M, Abbruzzese E, et al. Cranial and cervical nerve injuries after carotid endarterectomy: a prospective study. Surgery. 1999;125:85–91. [PubMed] [Google Scholar]
- 10.Forssell C, Takolander R, Bergqvist D, Bergentz SE, Gramming P, Kitzing P. Cranial nerve injuries associated with carotid endarterectomy. A prospective study. Acta Chir Scand. 1985;151:595–598. [PubMed] [Google Scholar]
- 11.Zannetti S, Parente B, De Rango P, Giordano G, Serafini G, Rossetti M, et al. Role of surgical techniques and operative findings in cranial and cervical nerve injuries during carotid endarterectomy. Eur J Vasc Endovasc Surg. 1998;15:528–531. doi: 10.1016/s1078-5884(98)80114-7. [DOI] [PubMed] [Google Scholar]
- 12.Regina G, Angiletta D, Impedovo G, De Robertis G, Fiorella M, Carratu MR. Dexamethasone minimizes the risk of cranial nerve injury during CEA. J Vasc Surg. 2009;49:99–102. doi: 10.1016/j.jvs.2008.08.049. [discussion 3]. [DOI] [PubMed] [Google Scholar]
- 13.Cunningham EJ, Bond R, Mayberg MR, Warlow CP, Rothwell PM. Risk of persistent cranial nerve injury after carotid endarterectomy. J Neurosurg. 2004;101:445–448. doi: 10.3171/jns.2004.101.3.0445. [DOI] [PubMed] [Google Scholar]
- 14.AbuRahma AF, Abu-Halimah S, Hass SM, Nanjundappa A, Stone PA, Mousa A, et al. Carotid artery stenting outcomes are equivalent to carotid endarterectomy outcomes for patients with post-carotid endarterectomy stenosis. J Vasc Surg. 2010;52:1180–1187. doi: 10.1016/j.jvs.2010.06.074. [DOI] [PubMed] [Google Scholar]
- 15.Fokkema M, den Hartog AG, Bots ML, van der Tweel I, Moll FL, de Borst GJ. Stenting versus surgery in patients with carotid stenosis after previous cervical radiation therapy: systematic review and meta-analysis. Stroke. 2012;43:793–801. doi: 10.1161/STROKEAHA.111.633743. [DOI] [PubMed] [Google Scholar]
- 16.AbuRahma AF, Choueiri MA. Cranial and cervical nerve injuries after repeat carotid endarterectomy. J VascSurg. 2000;32:649–654. doi: 10.1067/mva.2000.109751. [DOI] [PubMed] [Google Scholar]
- 17.Nolan BW, De Martino RR, Goodney PP, Schanzer A, Stone DH, Butzel D, et al. Comparison of carotid endarterectomy and stenting in real world practice using a regional quality improvement registry. J Vasc Surg. 2012;56:990–996. doi: 10.1016/j.jvs.2012.03.009. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Goodney PP, Wallaert JB, Scali ST, Stone DH, Patel V, Shaw P, et al. Impact of practice patterns in shunt use during carotid endarterectomy with contralateral carotid occlusion. J Vasc Surg. 2012;55:61 e1–71 e1. doi: 10.1016/j.jvs.2011.07.046. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Wallaert JB, Goodney PP, Vignati JJ, Stone DH, Nolan BW, Bertges DJ, et al. Completion imaging after carotid endarterectomy in the Vascular Study Group of New England. J Vasc Surg. 2011;54:376–385. doi: 10.1016/j.jvs.2011.01.032. 85 e1–3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Douglas L. Multilevel modeling. Thousand Oaks, CA: Sage; 2004. [Google Scholar]
- 21.Das MB, Hertzer NR, Ratliff NB, O’Hara PJ, Beven EG. Recurrent carotid stenosis. A five-year series of 65 reoperations. Ann Surg. 1985;202:28–35. doi: 10.1097/00000658-198507000-00004. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Greenstein AJ, Chassin MR, Wang J, Rockman CB, Riles TS, Tuhrim S, et al. Association between minor and major surgical complications after carotid endarterectomy: results of the New York Carotid Artery Surgery study. J Vasc Surg. 2007;46:1138–1144. doi: 10.1016/j.jvs.2007.08.026. [discussion 45–46]. [DOI] [PubMed] [Google Scholar]
- 23.Ferguson GG, Eliasziw M, Barr HW, Clagett GP, Barnes RW, Wallace MC, et al. The North American Symptomatic Carotid Endarterectomy Trial: surgical results in 1415 patients. Stroke. 1999;30:1751–1758. doi: 10.1161/01.str.30.9.1751. [DOI] [PubMed] [Google Scholar]
- 24.Hertzer NR, Feldman BJ, Beven EG, Tucker HM. A prospective study of the incidence of injury to the cranial nerves during carotid endarterectomy. Surg Gynecol Obstet. 1980;151:781–784. [PubMed] [Google Scholar]
- 25.Meyer FB, Piepgras DG, Fode NC. Surgical treatment of recurrent carotid artery stenosis. J Neurosurg. 1994;80:781–787. doi: 10.3171/jns.1994.80.5.0781. [DOI] [PubMed] [Google Scholar]
- 26.Frego M, Bridda A, Ruffolo C, Scarpa M, Polese L, Bianchera G. The hostile neck does not increase the risk of carotid endarterectomy. J Vasc Surg. 2009;50:40–47. doi: 10.1016/j.jvs.2008.12.053. [DOI] [PubMed] [Google Scholar]
- 27.Friedell ML, Joseph BP, Cohen MJ, Horowitz JD. Surgery for carotid artery stenosis following neck irradiation. Ann Vasc Surg. 2001;15:13–18. doi: 10.1007/s100160010009. [DOI] [PubMed] [Google Scholar]
- 28.Fokkema M, de Borst GJ, Nolan BW, Lo RC, Cambria RA, Powell RJ, et al. Carotid stenting versus endarterectomy in patients undergoing reintervention after prior carotid endarterectomy. J Vasc Surg. 2013 doi: 10.1016/j.jvs.2013.06.070. pii:S0741-5214(13) 01254-01258. [DOI] [PMC free article] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.