Surgical Outcomes for Cervical Carotid Artery Stenosis: Treatment Strategy for Bilateral Cervical Carotid Artery Stenosis Masaaki Hokari, MD, PhD,* Naoki Nakayama, MD, PhD,* Ken Kazumata, MD, PhD,* Toshiya Osanai, MD, PhD,* Toshitaka Nakamura, MD, PhD,† Hiroshi Yasuda, MD, PhD,‡ Satoshi Ushikoshi, MD, PhD,‡ Hideo Shichinohe, MD, PhD,* Takeo Abumiya, MD, PhD,* Satoshi Kuroda, MD, PhD,x and Kiyohiro Houkin, MD, PhD*
Background: Carotid endarterectomy (CEA) and carotid stenting (CAS) are beneficial procedures for patients with high-grade cervical carotid stenosis. However, it is sometimes difficult to manage patients with bilateral carotid stenosis. To decide the treatment strategy, one of the most important questions is whether contralateral stenosis increases the risk of patients undergoing CEA. Methods: This retrospective study included 201 patients with carotid stenosis who underwent a total of 219 consecutive procedures (CEA 189/CAS 30). We retrospectively analyzed outcomes in patients with carotid stenosis who were treated with either CEA or CAS and evaluated whether or not contralateral lesions increases the risk of patients undergoing CEA or CAS. Furthermore, we retrospectively verified our treatment strategy for bilateral carotid stenosis. Results: The incidences of perioperative complications were 5.3% in the CEA patients and 6.7% in the CAS patients, respectively. There was no significant difference between these 2 groups. The existences of contralateral occlusion and/or contralateral stenosis were not associated with perioperative complications in both the groups. There were 32 patients with bilateral severe carotid stenosis (.50%). Of those, 13 patients underwent bilateral revascularizations; CEA followed by CEA in 8, CEA followed by CAS in 3, CAS followed by CEA 1 coronary artery bpass grafting in 1, and CAS followed by CAS in 1. Conclusions: Our date showed that the existence of contralateral carotid lesion was not associated with perioperative complications, and most of our cases with bilateral carotid stenosis initially underwent CEA. Key Words: Carotid endareterectomy— bilateral carotid stenosis—carotid stenting—risk factors. Ó 2015 by National Stroke Association
From the *Department of Neurosurgery, Hokkaido University Graduate School of Medicine, Sapporo; †Department of Neurosurgery, Azabu Neurosurgical Hospital, Sapporo; ‡Department of Neurosurgery, Hokkaido Medical Center, Sapporo; and xDepartment of Neurosurgery, Graduate School of Medicine and Pharmaceutical Science, University of Toyama, Toyama, Japan. Received December 10, 2014; accepted March 31, 2015. There is no conflict of interest to report. Address correspondence to Masaaki Hokari, MD, PhD, Department of Neurosurgery, Hokkaido University Graduate School of Medicine, North 15 West 7, Kita-ku, Sapporo 060-8638, Japan. E-mail: [email protected]. 1052-3057/$ - see front matter Ó 2015 by National Stroke Association http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2015.03.052
Introduction Carotid endarterectomy (CEA) and carotid stenting (CAS) are beneficial procedures for patients with highgrade cervical carotid stenosis.1-4 Procedural selection should be determined by age, general condition, symptoms, plaque characteristics, anatomic situation, hemodynamic state, and other factors. In fact, radiationinduced carotid stenosis and restenosis after CEA are considered as a high risk for CEA, and CAS is usually performed on those patients.5-7 On the contrary, one of the remaining issues of CAS is the relatively higher incidence of ipsilateral ischemic lesions after the
Journal of Stroke and Cerebrovascular Diseases, Vol. -, No. - (---), 2015: pp 1-7
1
M. HOKARI ET AL.
2 8
procedure, even under embolic protection. Despite neurologic protection during the procedure, there have been several reports about delayed plaque protrusion after CAS, especially in the patients with carotid vulnerable plaque.9-11 Therefore, CAS is associated with a higher procedural risk of stroke than CEA in symptomatic patients and in elderly patients,12,13 thus making CEA more suitable for these lesions. Recently, an appropriate procedural selection has been making the overall outcome of carotid artery reconstruction improve as a result of complement to each other. However, it is sometimes difficult to manage patients with bilateral carotid stenosis. Its treatment strategy is complex, and there are several possible approaches that have yet to be decided, which side to treat first, which procedure to perform, and so forth. To decide the treatment strategy, one of the most important questions is whether contralateral stenosis (CCS) increases the risk of patients undergoing CEA. There have been a few reports regarding the perioperative risks to the patients with contralateral internal carotid artery (ICA) severe stenosis, and these have resulted in conflicting results.9,10 Therefore, in our retrospective study, we analyzed outcomes in patients with carotid stenosis that were treated with either CEA or CAS and evaluate whether or not contralateral lesions increases the risk of patients undergoing CEA or CAS. Furthermore, we retrospectively verified our treatment strategy for bilateral carotid stenosis.
Patients and Methods Patients This retrospective study included 201 patients with carotid stenosis who underwent a total of 219 consecutive procedures (both CEA and CAS) at Hokkaido University Hospital and its affinitive hospitals between January 2007 and April 2014. This study group comprised 177 males and 24 females with a mean age of 70.0 years (range, 4985 years). CEA and CAS were performed for 189 and 30 lesions, respectively. All participants provided written informed consent. On the basis of previous studies, CEA was principally the first choice for reconstructive treatment although patients who experienced restenosis after CEA, radiationinduced carotid stenosis, or medical complications intolerable for general anesthesia underwent CAS. Among them, 13 patients had contralateral carotid occlusion (CCO), and 32 patients had bilateral severe carotid stenosis (.50%). In these 32 patients with bilateral severe carotid stenosis, 13 patients underwent bilateral carotid reconstructions. For those patients, we retrospectively verified our treatment strategy for bilateral carotid stenosis.
Clinical Characteristics Clinical data were collected from the patients’ medical records. In this study, the authors used the following factors: age, gender, stenosis degree, plaque characteristics, contralateral lesion, hypertension (HT) (systolic blood pressure .140 mm Hg or diastolic blood pressure .90 mm Hg) or current treatment status, diabetes mellitus (DM; hemoglobin A1C, 6.5) or current treatment status, hyperlipidemia (HL; serum low-density lipoprotein cholesterol .140 mg/dL) or current treatment status, and ischemic heart disease (IHD) or current treatment status. All patients underwent preoperative screening for IHD to prevent perioperative cardiac complications. We then consulted the cardiology department and, if required, performed a treadmill stress electrography and coronary digital subtraction angiography. Regardless of the presence or the absence of symptoms of angina pectoris, the patients with severe stenosis of the coronary artery were regarded as having IHD. The degree of stenosis was determined according to the North American Symptomatic Carotid Endarterectomy Trial criteria1 and estimated using 3-dimensional computed tomography angiography or digital subtraction angiography. CCS was defined as a presence of more than 50% stenosis of contralateral ICA. Magnetic resonance imaging (MRI) or carotid ultrasonography was performed for the evaluation of plaque characteristics. Black-blood MRI used a fat-suppressed T1-weighted fast spin-echo sequence. The MR signal intensity of the carotid plaque in the area with the highest rate of stenosis was classified as low or high compared with the intensity of the ipsilateral sternocleidomastoid muscle. Ultrasonography was also performed on the patients to evaluate carotid plaque characteristics. Carotid plaque was defined as an arterial wall lesion that projected into the vessel lumen. The plaque was qualitatively assessed as being predominantly (.50% area of plaque images) low (blood-like echogenicity), intermediate, or high (intensely bright echogenicity).
CEA Procedures All CEAs were performed under general anesthesia. Carotid shunts with intraoperative monitors of near infrared spectroscopy and sensory-evoked potential or motor-evoked potential were used as a matter of routine. CEA was performed as previously described.14 Briefly, the carotid bifurcation was dissected, and then, an intravenous bolus of heparin (3000 units) was administered before carotid clamping. For precise and delicate plaque dissection, we routinely insert internal shunt tubes. The superior thyroid and external carotid arteries were occluded with aneurysmal clips. The common carotid artery and ICA were occluded with vascular clamps. Arteriotomy was subsequently performed, and a 3-way internal shunt tube (Furui 3.0 or 3.5) was inserted in all
TREATMENT STRATEGY FOR BILATERAL CAROTID STENOSIS
18.0 13.3 17.4 5.8 10.0 6.4 43.4 46.7 43.8 52.9 46.7 52.1 70.9 56.7 68.9 35.4 33.3 35.2 45.5 23.3 42.5
HT (%) DM (%) Soft plaque (%)
48.1 43.3 47.5 69.9 6 8.3 70.6 6 5.6 70.0 6 7.9
Stenosis (%)
Abbreviations: CAS, carotid stenting; CCO, contralateral carotid occlusion; CCS, contralateral carotid stenosis (.50%); CEA, carotid endarterectomy; DM, diabetes mellitus; HL, hyperlipidemia; HT, hypertension; IHD, ischemic heart disease.
Characteristics of the patients in this study are represented in Table 1. The mean age of all subjects was 70.0 6 7.9 years; the mean age for the patients on whom CEA was performed was 69.9 6 8.3 years; the mean age for the patients on whom CAS was performed 70.6 6 5.6 years. The percentage of symptomatic patients and stenosis degree were slightly greater in the CEA patients than in the CAS patients (48.1% and 84.5% versus 43.3% and 80.2%, respectively) without significant
87.3 90.0 87.7
Clinical Data
Symptom (%)
Results
Age, y
All data are expressed as mean 6 standard deviation. Clinical variables, including age, gender, stenosis degree, symptom, plaque characteristic, contralateral lesions, HT, DM, HL, and IHD, were compared by using c2 test or unpaired t test as appropriate. Univariate analysis was also performed to determine whether the incidence of perioperative complications was associated with the clinical variables. Differences with a P value of less than .05 were considered statistically significant.
Male (%)
Statistics
Treatment
In this study, surgical complications included any perioperative episode or death within 30 days after operation. Patients with presenting temporary or permanent neurologic deterioration and/or patients who had to undergo additional surgical therapies were considered as having surgical complications, and patients with worsening of modified Rankin Scale of more than 2 were considered surgical morbidity. Perioperative stroke was defined as an acute neurologic event with focal symptoms and signs that were consistent with focal cerebral lesion detected on MRI or computed tomography.
Table 1. Characteristics of the patients in this study
Perioperative Complications
HL (%)
IHD (%)
CCO (%)
Principally, CAS was performed under local anesthesia, with oral dual-anticoagulation drugs. During CAS, systemic heparinization was performed after inserting a sheath for catheter insertion, and predilation was performed after neurologic protection (distal or proximal) was inserted in the ICA, after which a stent was placed.
CEA CAS Total
CAS Procedures
84.5 6 12.4 80.2 6 11.6 84.0 6 18.1
CCS (%)
CCO 1 CCS (%)
patients. The duration of carotid clamping was 3-7 minutes. Blood pressure was maintained within the normal range during carotid clamping. The plaque was carefully dissected and removed under a surgical microscope. The arteriotomy was closed with a running suture, and an internal shunt tube was removed immediately before the arteriotomy closure was completed.
23.8 23.3 23.7
3
M. HOKARI ET AL.
4
Table 2. Perioperative complications Complication (%) Contralateral caroid artery Total CCL (2) CCO (1) CCS (1) CEA CCL (2) CCO (1) CCS (1) CAS CCL (2) CCO (1) CCS (1)
Number of cases
Transient
Minor
Major (mRS .2)
Total (permanent)
219 174 13 32 189 151 10 28 30 23 3 4
8 (3.7) 4 (2.3) 1 (7.7) 3 (9.4) 8 (4.2) 4 (2.7)* 1 (10.0)x 3 (10.7)k 0 (0) 0 (0) 0 (0) 0 (0)
9 (4.1) 7 (4.0) 0 (0) 2 (6.3) 8 (4.2) 6 (4.0)y 0 (0) 2 (7.1){ 1 (3.3) 1 (4.3)# 0 (0) 0 (0)
3 (1.4) 3 (1.7) 0 (0) 0 (0) 2 (1.1) 2 (1.3)z 0 (0) 0 (0) 1 (3.3) 1 (4.3)** 0 (0) 0 (0)
12 (5.5) 10 (5.7) 0 (0) 2 (6.3) 10 (5.3) 8 (5.3) 0 (0) 2 (7.1) 2 (6.6) 2 (8.7) 0 (0) 0 (0)
Abbreviations: CAS, carotid stenting; CCL, contralateral carotid lesion (occlusion or severe stenosis); CCO, contralateral carotid occlusion; CCS, contralateral carotid stenosis; CEA, carotid endarterectomy; mRS, modified Rankin Scale. *Restlessness, 1; hoarseness, 1; and respirator administration, 2 (neck swelling, 1 and hyperperfusion, 1). yHoarseness, 5 and dysphagia 1. zmRS worsens due to respirator administration (wound bleeding, 1 and laryngeal edema, 1). xRestlessness, 1. kMinor infarction, 1; restlessness, 1; and hoarseness 1. {Minor infarction, 1 and hoarseness, 1. # Minor infarction, 1. **Major infarction, 1.
differences. Occurrence of soft plaque was significantly higher in the CEA patients than in CAS patients (45.5% in the CEA patients versus 23.3% in the CAS patients, respectively). The percentage of the patients with CCO was slightly higher in the CAS patients than in the CEA patients (10.0% in the CAS patients versus 5.8% in the CEA patients), and those with CCS was higher in the CEA patients than in the CAS patients (18.0% in the CEA patients versus 13.3% in the CAS patients). However, there were no significant differences. Incidences of contralateral steno-occlusive lesion (CCL) (CCS or CCL) were almost the same in the both groups (23.8% in the CEA patients and 23.3% in the CAS patients). Moreover, there were no significant differences in other factors, such as history of HT, DM, HL, and IHD. Thus, soft plaque ratio was the only significant different variable between the 2 groups (P 5 .023).
Perioperative Complications Table 2 shows the results of perioperative complications in each group. There was no surgical mortality in this study. Perioperative complications were noted in 12 patients (5.5%). The incidences of perioperative complications were 5.3% in the CEA patients and 6.7% in the CAS patients, respectively. There was no significant difference between these 2 groups. Permanent surgical complications in the CEA patients were noted in 10 patients (5.3%); vocal nerve injuries in
7, worsening of modified Rankin Scale of more than 2 due to respirator administration (wound bleeding, 1 and laryngeal edema, 1) in 2, and high-order brain dysfunction due to small infarction and hyperperfusion syndrome in 1. Morbidity occurred in 2 (1.1%) of the CEA patients. Transient neurologic deteriorations occurred in 8 of the CEA patients; transient vocal nerve paresis in 2, transient restlessness in 3, temporarily high-order brain dysfunction due to respirator administration (wound swelling, 1 and hyperperfusion syndrome, 1) in 2, and transient neurologic deficit due to small infarction in 1. The percentage of the patients with transient neurologic deteriorations was slightly higher in the CEA patients with CCL than in those without CCL (10.5% versus 2.7%, respectively) without significant differences. There were no significant perioperative risk factors in the CEA patients, and existence of CCO and/ or CCS was not associated with perioperative complications. ICA occlusion just after CEA occurred in one (.5%). Fortunately, the patients presented only transient hemi numbness due to small parietal infarction. Restenosis after CEA occurred in 5 (2.6%); 1 symptomatic patient and 4 asymptomatic patients underwent CAS with no complications. Perioperative complications in the CAS patients were noted in 2 patients (6.7%), who experienced symptomatic cerebral infarction. Morbidity occurred in 1 (3.3%) of the CAS patients. There were no significant perioperative risk factors in the CAS patients, and existence of CCO
TREATMENT STRATEGY FOR BILATERAL CAROTID STENOSIS
Table 3. Treatment strategy for bilateral carotid steno-occlusive lesions Bilateral stenotic lesion 32 Unilateral reconstruction (another side under observation) 19 CEA 17 CAS 2 Bilateral reconstruction 13 CEA / CEA 8 (mean interval, 7 mo [range, 4-12 mo]) CEA / CAS 3 (mean interval, 7 wk [range, 3-12 wk]) CAS / coronary artery bpass grafting 1 CEA 1 (interval, 2 d) CAS / CAS 1 (interval, 10 mo) Abbreviations: CAS, carotid stenting; CEA, carotid endarterectomy.
and/or CCS was not associated with perioperative complications. Restenosis after CAS did not occur in this study.
Treatment Strategy for Bilateral Carotid Steno-occlusive Lesions As described previously, 14 patients had CCO. Ten patients underwent CEA, and 3 patients underwent CAS. As shown in Table 3, in these 32 patients with bilateral severe carotid stenosis (.50%), 19 patients underwent unilateral reconstruction (CEA, 17; CAS, 2) and were carefully followed up for contralateral asymptomatic moderate carotid stenosis. The remaining13 patients underwent bilateral carotid reconstructions; CEA followed by CEA in 8, CEA followed by CAS in 3, CAS followed by CEA 1 coronary artery bpass grafting in 1, and CAS followed by CAS in 1. Thus, most of the cases with bilateral carotid stenosis were initially performed with CEA. The mean interval in CEA followed by CEA was 7 months (range, 4-12 months) whereas that of CEA followed by CAS was 7 weeks (range, 3-12 weeks). Thus, procedural interval was shorter in the patients who were performed with CEA followed by CAS.
Discussion There have been a few reports regarding the perioperative risks in the patients with contralateral ICA severe stenosis, and these have resulted in conflicting results.15,16 Several investigators thought that CAS would be better for the first revascularization procedure for bilateral carotid severe stenosis than CEA because CCS would adversely affect CEA.17,18 However, our data showed that the existence of contralateral carotid lesion was not associated with perioperative complications. Furthermore, most of our cases with bilateral carotid stenosis were initially performed CEA, and most of the patients who had
5
bilateral carotid reconstructions underwent CEA followed by CEA or CEA followed by CAS. There are 4 treatment strategies for bilateral cervical carotid artery stenosis: (1) CEA / CEA, (2) CAS / CAS, (3) CAS / CEA, and (4) CEA / CAS. There have been several reports on the reconstruction of bilateral ICA stenosis.10,17-26 In our previous case series report,26 the merits and demerits of each treatment strategy were thoroughly discussed, and we suggested that a combined therapy using CEA for the symptomatic side followed by CAS for the asymptomatic side can be one beneficial treatment option for patients with bilateral carotid stenosis. Recently, however, the combined therapy of CAS and then CEA has been recommended by several authors.17,18,24,25 Most of their patients underwent CAS for the asymptomatic side and then CEA for the symptomatic side because symptomatic plaques are often vulnerable and sometimes unsafe for CAS.17,18 However, the early risk of recurrent strokes during medical treatment is also high in patients with recent symptomatic carotid severe stenosis; relatively early surgery is therefore recommended.27,28 Symptomatic carotid plaques often consist of lipid-rich and intraplaque hematoma. Therefore, we suggest that these vulnerable plaques should be primarily treated by CEA. On the other hand, they thought that CAS would be better for the first revascularization procedure than CEA because CCS would adversely affect CEA.17,18 Although CCO does not adversely impact CAS,29-31 there have been no reports indicating that CAS is safer in patients with contralateral severe ICA stenosis than is CEA. In fact, contralateral occlusion is one of the risk factors in Protected Carotid-Artery Stenting versus Endarterectomy in High-Risk Patients (SAPPHIRE) trial but not CCS.4 The frequency of postprocedural hemodynamic complications such as hypotension and bradycardia was more than 50%.19,23 Thus, we think that hypotension after CAS for the asymptomatic side may be dangerous for the symptomatic hemisphere because CAS for the asymptomatic side usually does not improve hemodynamics in the symptomatic cerebral hemisphere. One of the most important questions is whether CCS increases the risk of patients undergoing CEA. There have been a few reports regarding the perioperative risks in the patients with contralateral ICA severe stenosis, and these have resulted in conflicting results.15,16 Interestingly, Goodney et al, who had previously reported contralateral occlusion increasing the risk of patients undergoing CEA,32 analyzed the perioperative risk of CEA with contralateral ICA occlusion, and they had suggested that routine shunt use during CEA was associated with fewer complications. However, surgeons who place shunts selectively during CEA have higher rates of complication.33 Estruch-Perez et al34 reported,
M. HOKARI ET AL.
6
moreover that patients with severe CCS (.50%) have a higher risk of requiring shunt use during CEA. Therefore, we think that the perioperative risk of CEA using shunts routinely may not adversely affect in an exceptional group of patients with contralateral ICA severe stenosis because cerebral hemodynamic impairment and cognitive dysfunction are more severe in patients with bilateral carotid stenosis than those with unilateral stenosis.35 In fact, our data showed that the existence of contralateral carotid lesion was not associated with perioperative complications, and most of our cases with bilateral carotid stenosis initially underwent CEA. Moreover, most of our patients who were performed with bilateral carotid reconstructions underwent CEA followed either by CEA or by CAS. We suggest that a combined therapy using CEA for the symptomatic side followed by CAS for the asymptomatic side can be one beneficial treatment option for patients who require early treatments with bilateral carotid stenosis, who need early treatment because procedural interval was shorter in the patients who were performed with CEA followed by CAS. This study has limitations, in that there are no data to be used for comparison analysis among the strategies. Thus, we cannot suggest that CEA would be better for the first revascularization procedure than CAS in the patients with bilateral carotid severe stenosis. Besides, this is neither prospective nor randomized study. Therefore, we cannot conclude that the existence of contralateral carotid lesion was not associated with perioperative complications in both CEA and CAS. In conclusion, we demonstrated that the existence of contralateral carotid lesion was not associated with perioperative complications, and most of our cases with bilateral carotid stenosis initially underwent CEA. We suggest that CEA would be better for the first revascularization procedure for the symptomatic or severe stenotic side than CAS on most of the patients with bilateral carotid severe stenosis.
References 1. Collaborators NASCET. 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. 2. Group ECSTC. MRC European Carotid Surgery Trial: interim results for symptomatic patients with severe (70-99%) or with mild (0-29%) carotid stenosis. European carotid surgery trialists’ collaborative group. Lancet 1991; 337:1235-1243. 3. Sheffet AJ, Roubin G, Howard G, et al. Design of the Carotid Revascularization Endarterectomy vs. Stenting Trial (CREST). Int J Stroke 2010;5:40-46. 4. Yadav JS, Wholey MH, Kuntz RE, et al. Protected carotidartery stenting versus endarterectomy in high-risk patients. N Engl J Med 2004;351:1493-1501.
5. Alric P, Branchereau P, Berthet JP, et al. Carotid artery stenting for stenosis following revascularization or cervical irradiation. J Endovasc Ther 2002;9:14-19. 6. Melliere D, Becquemin JP, Berrahal D, et al. Management of radiation-induced occlusive arterial disease: a reassessment. J Cardiovasc Surg (Torino) 1997;38:261-269. 7. Meyer FB, Piepgras DG, Fode NC. Surgical treatment of recurrent carotid artery stenosis. J Neurosurg 1994;80: 781-787. 8. Maleux G, Demaerel P, Verbeken E, et al. Cerebral ischemia after filter-protected carotid artery stenting is common and cannot be predicted by the presence of substantial amount of debris captured by the filter device. AJNR Am J Neuroradiol 2006;27:1830-1833. 9. Aikawa H, Kodama T, Nii K, et al. Intraprocedural plaque protrusion resulting in cerebral embolism during carotid angioplasty with stenting. Radiat Med 2008;26: 318-323. 10. Ogata N, Harashima K, Kanetani K, et al. Delayed plaque protrusion after carotid artery stenting for the patient with symptomatic bi-lateral carotid artery stenosis. Cardiovasc Interv Ther 2014;29:65-69. 11. Takigawa T, Matsumaru Y, Kubo T, et al. Recurrent subacute in-stent restenosis after carotid artery stenting due to plaque protrusion. Neurol Med Chir (Tokyo) 2009; 49:413-417. 12. Antoniou GA, Georgiadis GS, Georgakarakos EI, et al. Meta-analysis and meta-regression analysis of outcomes of carotid endarterectomy and stenting in the elderly. JAMA Surg 2013;148:1140-1152. 13. Touze E, Trinquart L, Felgueiras R, et al. A clinical rule (sex, contralateral occlusion, age, and restenosis) to select patients for stenting versus carotid endarterectomy: systematic review of observational studies with validation in randomized trials. Stroke 2013;44:3394-3400. 14. Iwasaki M, Kuroda S, Nakayama N, et al. Clinical characteristics and outcomes in carotid endarterectomy for internal carotid artery stenosis in a Japanese population: 10-year microsurgical experience. J Stroke Cerebrovasc Dis 2011;20:55-61. 15. Burke PE, Prendiville E, Tadros E, et al. Contralateral stenosis and stump pressures: Parameters to identify the high risk patient undergoing carotid endarterectomy under local anaesthesia. Eur J Vasc Surg 1993;7:317-319. 16. Gasecki AP, Eliasziw M, Ferguson GG, et al. Long-term prognosis and effect of endarterectomy in patients with symptomatic severe carotid stenosis and contralateral carotid stenosis or occlusion: results from NASCET. North American Symptomatic Carotid Endarterectomy Trial (NASCET) group. J Neurosurg 1995;83:778-782. 17. Kawabata Y, Nagata I, Sakai N, et al. Treatment of bilateral internal carotid artery stenosis. Surgery for Cerebral Stroke 2001;29:339-344. 18. Tsukahara T, Hatano T, Ogino E, et al. Surgical treatment for bilateral carotid arterial stenosis. Acta Neurochir Suppl 2005;94:133-136. 19. Alurkar A, Karanam LS, Nayak S, et al. Simultaneous bilateral carotid stenting in a series of 9 patients: a single-center experience with review of literature. J Clin Imaging Sci 2013;2:72. 20. Dong H, Jiang XJ, Peng M, et al. Comparison of the safety of simultaneous bilateral carotid artery stenting versus unilateral carotid artery stenting: 30-day and 6-month results. Chin Med J (Engl) 2012;125:1010-1015. 21. Henry M, Gopalakrishnan L, Rajagopal S, et al. Bilateral carotid angioplasty and stenting. Catheter Cardiovasc Interv 2005;64:275-282.
TREATMENT STRATEGY FOR BILATERAL CAROTID STENOSIS 22. Ille O, Woimant F, Pruna A, et al. Hypertensive encephalopathy after bilateral carotid endarterectomy. Stroke 1995;26:488-491. 23. Qureshi AI, Luft AR, Sharma M, et al. Frequency and determinants of postprocedural hemodynamic instability after carotid angioplasty and stenting. Stroke 1999;30: 2086-2093. 24. Shichinohe H, Kuroda S, Asano T, et al. [Novel stent/ CEA strategy for patients with bilateral carotid artery stenosis and coronary artery disease: report of 2 cases]. No Shinkei Geka 2005;33:149-153. 25. Kiris I, Gulmen S, Yilmaz S, et al. Management of concomitant coronary and bilateral carotid artery disease: a case report. J Card Surg 2007;22:149-151. 26. Hokari M, Isobe M, Asano T, et al. Treatment strategy for bilateral carotid stenosis: 2 cases of carotid endarterectomy for the symptomatic side followed by carotid stenting. J Stroke Cerebrovasc Dis 2014;23:2851-2856. 27. Rantner B, Pavelka M, Posch L, et al. Carotid endarterectomy after ischemic stroke–is there a justification for delayed surgery? Eur J Vasc Endovasc Surg 2005;30:36-40. 28. Rothwell PM, Slattery J, Warlow CP. A systematic comparison of the risks of stroke and death due to carotid endarterectomy for symptomatic and asymptomatic stenosis. Stroke 1996;27:266-269.
7
29. Faggioli G, Pini R, Mauro R, et al. Contralateral carotid occlusion in endovascular and surgical carotid revascularization: a single centre experience with literature review and meta-analysis. Eur J Vasc Endovasc Surg 2013;46:10-20. 30. Keldahl ML, Park MS, Garcia-Toca M, et al. Does a contralateral carotid occlusion adversely impact carotid artery stenting outcomes? Ann Vasc Surg 2012;26:40-45. 31. Yang SS, Kim YW, Kim DI, et al. Impact of contralateral carotid or vertebral artery occlusion in patients undergoing carotid endarterectomy or carotid artery stenting. J Vasc Surg 2014;59:749-755. 32. Goodney PP, Likosky DS, Cronenwett JL. Factors associated with stroke or death after carotid endarterectomy in Northern New England. J Vasc Surg 2008;48:1139-1145. 33. Goodney PP, Wallaert JB, Scali ST, et al. Impact of practice patterns in shunt use during carotid endarterectomy with contralateral carotid occlusion. J Vasc Surg 2012;55:61-71.e61. 34. Estruch-Perez MJ, Plaza-Martinez A, HernandezCadiz MJ, et al. Interaction of cerebrovascular disease and contralateral carotid occlusion in prediction of shunt insertion during carotid endarterectomy. Arch Med Sci 2012;8:236-243. 35. Balucani C, Viticchi G, Falsetti L, et al. Cerebral hemodynamics and cognitive performance in bilateral asymptomatic carotid stenosis. Neurology 2012;79:1788-1795.
Background: Carotid endarterectomy (CEA) and carotid stenting (CAS) are beneficial procedures for patients with high-grade cervical carotid stenosis. However, it is sometimes difficult to manage patients with bilateral carotid stenosis. To decide the treatment strategy, one of the most important questions is whether contralateral stenosis increases the risk of patients undergoing CEA. Methods: This retrospective study included 201 patients with carotid stenosis who underwent a total of 219 consecutive procedures (CEA 189/CAS 30). We retrospectively analyzed outcomes in patients with carotid stenosis who were treated with either CEA or CAS and evaluated whether or not contralateral lesions increases the risk of patients undergoing CEA or CAS. Furthermore, we retrospectively verified our treatment strategy for bilateral carotid stenosis. Results: The incidences of perioperative complications were 5.3% in the CEA patients and 6.7% in the CAS patients, respectively. There was no significant difference between these 2 groups. The existences of contralateral occlusion and/or contralateral stenosis were not associated with perioperative complications in both the groups. There were 32 patients with bilateral severe carotid stenosis (.50%). Of those, 13 patients underwent bilateral revascularizations; CEA followed by CEA in 8, CEA followed by CAS in 3, CAS followed by CEA 1 coronary artery bpass grafting in 1, and CAS followed by CAS in 1. Conclusions: Our date showed that the existence of contralateral carotid lesion was not associated with perioperative complications, and most of our cases with bilateral carotid stenosis initially underwent CEA. Key Words: Carotid endareterectomy— bilateral carotid stenosis—carotid stenting—risk factors. Ó 2015 by National Stroke Association
From the *Department of Neurosurgery, Hokkaido University Graduate School of Medicine, Sapporo; †Department of Neurosurgery, Azabu Neurosurgical Hospital, Sapporo; ‡Department of Neurosurgery, Hokkaido Medical Center, Sapporo; and xDepartment of Neurosurgery, Graduate School of Medicine and Pharmaceutical Science, University of Toyama, Toyama, Japan. Received December 10, 2014; accepted March 31, 2015. There is no conflict of interest to report. Address correspondence to Masaaki Hokari, MD, PhD, Department of Neurosurgery, Hokkaido University Graduate School of Medicine, North 15 West 7, Kita-ku, Sapporo 060-8638, Japan. E-mail: [email protected]. 1052-3057/$ - see front matter Ó 2015 by National Stroke Association http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2015.03.052
Introduction Carotid endarterectomy (CEA) and carotid stenting (CAS) are beneficial procedures for patients with highgrade cervical carotid stenosis.1-4 Procedural selection should be determined by age, general condition, symptoms, plaque characteristics, anatomic situation, hemodynamic state, and other factors. In fact, radiationinduced carotid stenosis and restenosis after CEA are considered as a high risk for CEA, and CAS is usually performed on those patients.5-7 On the contrary, one of the remaining issues of CAS is the relatively higher incidence of ipsilateral ischemic lesions after the
Journal of Stroke and Cerebrovascular Diseases, Vol. -, No. - (---), 2015: pp 1-7
1
M. HOKARI ET AL.
2 8
procedure, even under embolic protection. Despite neurologic protection during the procedure, there have been several reports about delayed plaque protrusion after CAS, especially in the patients with carotid vulnerable plaque.9-11 Therefore, CAS is associated with a higher procedural risk of stroke than CEA in symptomatic patients and in elderly patients,12,13 thus making CEA more suitable for these lesions. Recently, an appropriate procedural selection has been making the overall outcome of carotid artery reconstruction improve as a result of complement to each other. However, it is sometimes difficult to manage patients with bilateral carotid stenosis. Its treatment strategy is complex, and there are several possible approaches that have yet to be decided, which side to treat first, which procedure to perform, and so forth. To decide the treatment strategy, one of the most important questions is whether contralateral stenosis (CCS) increases the risk of patients undergoing CEA. There have been a few reports regarding the perioperative risks to the patients with contralateral internal carotid artery (ICA) severe stenosis, and these have resulted in conflicting results.9,10 Therefore, in our retrospective study, we analyzed outcomes in patients with carotid stenosis that were treated with either CEA or CAS and evaluate whether or not contralateral lesions increases the risk of patients undergoing CEA or CAS. Furthermore, we retrospectively verified our treatment strategy for bilateral carotid stenosis.
Patients and Methods Patients This retrospective study included 201 patients with carotid stenosis who underwent a total of 219 consecutive procedures (both CEA and CAS) at Hokkaido University Hospital and its affinitive hospitals between January 2007 and April 2014. This study group comprised 177 males and 24 females with a mean age of 70.0 years (range, 4985 years). CEA and CAS were performed for 189 and 30 lesions, respectively. All participants provided written informed consent. On the basis of previous studies, CEA was principally the first choice for reconstructive treatment although patients who experienced restenosis after CEA, radiationinduced carotid stenosis, or medical complications intolerable for general anesthesia underwent CAS. Among them, 13 patients had contralateral carotid occlusion (CCO), and 32 patients had bilateral severe carotid stenosis (.50%). In these 32 patients with bilateral severe carotid stenosis, 13 patients underwent bilateral carotid reconstructions. For those patients, we retrospectively verified our treatment strategy for bilateral carotid stenosis.
Clinical Characteristics Clinical data were collected from the patients’ medical records. In this study, the authors used the following factors: age, gender, stenosis degree, plaque characteristics, contralateral lesion, hypertension (HT) (systolic blood pressure .140 mm Hg or diastolic blood pressure .90 mm Hg) or current treatment status, diabetes mellitus (DM; hemoglobin A1C, 6.5) or current treatment status, hyperlipidemia (HL; serum low-density lipoprotein cholesterol .140 mg/dL) or current treatment status, and ischemic heart disease (IHD) or current treatment status. All patients underwent preoperative screening for IHD to prevent perioperative cardiac complications. We then consulted the cardiology department and, if required, performed a treadmill stress electrography and coronary digital subtraction angiography. Regardless of the presence or the absence of symptoms of angina pectoris, the patients with severe stenosis of the coronary artery were regarded as having IHD. The degree of stenosis was determined according to the North American Symptomatic Carotid Endarterectomy Trial criteria1 and estimated using 3-dimensional computed tomography angiography or digital subtraction angiography. CCS was defined as a presence of more than 50% stenosis of contralateral ICA. Magnetic resonance imaging (MRI) or carotid ultrasonography was performed for the evaluation of plaque characteristics. Black-blood MRI used a fat-suppressed T1-weighted fast spin-echo sequence. The MR signal intensity of the carotid plaque in the area with the highest rate of stenosis was classified as low or high compared with the intensity of the ipsilateral sternocleidomastoid muscle. Ultrasonography was also performed on the patients to evaluate carotid plaque characteristics. Carotid plaque was defined as an arterial wall lesion that projected into the vessel lumen. The plaque was qualitatively assessed as being predominantly (.50% area of plaque images) low (blood-like echogenicity), intermediate, or high (intensely bright echogenicity).
CEA Procedures All CEAs were performed under general anesthesia. Carotid shunts with intraoperative monitors of near infrared spectroscopy and sensory-evoked potential or motor-evoked potential were used as a matter of routine. CEA was performed as previously described.14 Briefly, the carotid bifurcation was dissected, and then, an intravenous bolus of heparin (3000 units) was administered before carotid clamping. For precise and delicate plaque dissection, we routinely insert internal shunt tubes. The superior thyroid and external carotid arteries were occluded with aneurysmal clips. The common carotid artery and ICA were occluded with vascular clamps. Arteriotomy was subsequently performed, and a 3-way internal shunt tube (Furui 3.0 or 3.5) was inserted in all
TREATMENT STRATEGY FOR BILATERAL CAROTID STENOSIS
18.0 13.3 17.4 5.8 10.0 6.4 43.4 46.7 43.8 52.9 46.7 52.1 70.9 56.7 68.9 35.4 33.3 35.2 45.5 23.3 42.5
HT (%) DM (%) Soft plaque (%)
48.1 43.3 47.5 69.9 6 8.3 70.6 6 5.6 70.0 6 7.9
Stenosis (%)
Abbreviations: CAS, carotid stenting; CCO, contralateral carotid occlusion; CCS, contralateral carotid stenosis (.50%); CEA, carotid endarterectomy; DM, diabetes mellitus; HL, hyperlipidemia; HT, hypertension; IHD, ischemic heart disease.
Characteristics of the patients in this study are represented in Table 1. The mean age of all subjects was 70.0 6 7.9 years; the mean age for the patients on whom CEA was performed was 69.9 6 8.3 years; the mean age for the patients on whom CAS was performed 70.6 6 5.6 years. The percentage of symptomatic patients and stenosis degree were slightly greater in the CEA patients than in the CAS patients (48.1% and 84.5% versus 43.3% and 80.2%, respectively) without significant
87.3 90.0 87.7
Clinical Data
Symptom (%)
Results
Age, y
All data are expressed as mean 6 standard deviation. Clinical variables, including age, gender, stenosis degree, symptom, plaque characteristic, contralateral lesions, HT, DM, HL, and IHD, were compared by using c2 test or unpaired t test as appropriate. Univariate analysis was also performed to determine whether the incidence of perioperative complications was associated with the clinical variables. Differences with a P value of less than .05 were considered statistically significant.
Male (%)
Statistics
Treatment
In this study, surgical complications included any perioperative episode or death within 30 days after operation. Patients with presenting temporary or permanent neurologic deterioration and/or patients who had to undergo additional surgical therapies were considered as having surgical complications, and patients with worsening of modified Rankin Scale of more than 2 were considered surgical morbidity. Perioperative stroke was defined as an acute neurologic event with focal symptoms and signs that were consistent with focal cerebral lesion detected on MRI or computed tomography.
Table 1. Characteristics of the patients in this study
Perioperative Complications
HL (%)
IHD (%)
CCO (%)
Principally, CAS was performed under local anesthesia, with oral dual-anticoagulation drugs. During CAS, systemic heparinization was performed after inserting a sheath for catheter insertion, and predilation was performed after neurologic protection (distal or proximal) was inserted in the ICA, after which a stent was placed.
CEA CAS Total
CAS Procedures
84.5 6 12.4 80.2 6 11.6 84.0 6 18.1
CCS (%)
CCO 1 CCS (%)
patients. The duration of carotid clamping was 3-7 minutes. Blood pressure was maintained within the normal range during carotid clamping. The plaque was carefully dissected and removed under a surgical microscope. The arteriotomy was closed with a running suture, and an internal shunt tube was removed immediately before the arteriotomy closure was completed.
23.8 23.3 23.7
3
M. HOKARI ET AL.
4
Table 2. Perioperative complications Complication (%) Contralateral caroid artery Total CCL (2) CCO (1) CCS (1) CEA CCL (2) CCO (1) CCS (1) CAS CCL (2) CCO (1) CCS (1)
Number of cases
Transient
Minor
Major (mRS .2)
Total (permanent)
219 174 13 32 189 151 10 28 30 23 3 4
8 (3.7) 4 (2.3) 1 (7.7) 3 (9.4) 8 (4.2) 4 (2.7)* 1 (10.0)x 3 (10.7)k 0 (0) 0 (0) 0 (0) 0 (0)
9 (4.1) 7 (4.0) 0 (0) 2 (6.3) 8 (4.2) 6 (4.0)y 0 (0) 2 (7.1){ 1 (3.3) 1 (4.3)# 0 (0) 0 (0)
3 (1.4) 3 (1.7) 0 (0) 0 (0) 2 (1.1) 2 (1.3)z 0 (0) 0 (0) 1 (3.3) 1 (4.3)** 0 (0) 0 (0)
12 (5.5) 10 (5.7) 0 (0) 2 (6.3) 10 (5.3) 8 (5.3) 0 (0) 2 (7.1) 2 (6.6) 2 (8.7) 0 (0) 0 (0)
Abbreviations: CAS, carotid stenting; CCL, contralateral carotid lesion (occlusion or severe stenosis); CCO, contralateral carotid occlusion; CCS, contralateral carotid stenosis; CEA, carotid endarterectomy; mRS, modified Rankin Scale. *Restlessness, 1; hoarseness, 1; and respirator administration, 2 (neck swelling, 1 and hyperperfusion, 1). yHoarseness, 5 and dysphagia 1. zmRS worsens due to respirator administration (wound bleeding, 1 and laryngeal edema, 1). xRestlessness, 1. kMinor infarction, 1; restlessness, 1; and hoarseness 1. {Minor infarction, 1 and hoarseness, 1. # Minor infarction, 1. **Major infarction, 1.
differences. Occurrence of soft plaque was significantly higher in the CEA patients than in CAS patients (45.5% in the CEA patients versus 23.3% in the CAS patients, respectively). The percentage of the patients with CCO was slightly higher in the CAS patients than in the CEA patients (10.0% in the CAS patients versus 5.8% in the CEA patients), and those with CCS was higher in the CEA patients than in the CAS patients (18.0% in the CEA patients versus 13.3% in the CAS patients). However, there were no significant differences. Incidences of contralateral steno-occlusive lesion (CCL) (CCS or CCL) were almost the same in the both groups (23.8% in the CEA patients and 23.3% in the CAS patients). Moreover, there were no significant differences in other factors, such as history of HT, DM, HL, and IHD. Thus, soft plaque ratio was the only significant different variable between the 2 groups (P 5 .023).
Perioperative Complications Table 2 shows the results of perioperative complications in each group. There was no surgical mortality in this study. Perioperative complications were noted in 12 patients (5.5%). The incidences of perioperative complications were 5.3% in the CEA patients and 6.7% in the CAS patients, respectively. There was no significant difference between these 2 groups. Permanent surgical complications in the CEA patients were noted in 10 patients (5.3%); vocal nerve injuries in
7, worsening of modified Rankin Scale of more than 2 due to respirator administration (wound bleeding, 1 and laryngeal edema, 1) in 2, and high-order brain dysfunction due to small infarction and hyperperfusion syndrome in 1. Morbidity occurred in 2 (1.1%) of the CEA patients. Transient neurologic deteriorations occurred in 8 of the CEA patients; transient vocal nerve paresis in 2, transient restlessness in 3, temporarily high-order brain dysfunction due to respirator administration (wound swelling, 1 and hyperperfusion syndrome, 1) in 2, and transient neurologic deficit due to small infarction in 1. The percentage of the patients with transient neurologic deteriorations was slightly higher in the CEA patients with CCL than in those without CCL (10.5% versus 2.7%, respectively) without significant differences. There were no significant perioperative risk factors in the CEA patients, and existence of CCO and/ or CCS was not associated with perioperative complications. ICA occlusion just after CEA occurred in one (.5%). Fortunately, the patients presented only transient hemi numbness due to small parietal infarction. Restenosis after CEA occurred in 5 (2.6%); 1 symptomatic patient and 4 asymptomatic patients underwent CAS with no complications. Perioperative complications in the CAS patients were noted in 2 patients (6.7%), who experienced symptomatic cerebral infarction. Morbidity occurred in 1 (3.3%) of the CAS patients. There were no significant perioperative risk factors in the CAS patients, and existence of CCO
TREATMENT STRATEGY FOR BILATERAL CAROTID STENOSIS
Table 3. Treatment strategy for bilateral carotid steno-occlusive lesions Bilateral stenotic lesion 32 Unilateral reconstruction (another side under observation) 19 CEA 17 CAS 2 Bilateral reconstruction 13 CEA / CEA 8 (mean interval, 7 mo [range, 4-12 mo]) CEA / CAS 3 (mean interval, 7 wk [range, 3-12 wk]) CAS / coronary artery bpass grafting 1 CEA 1 (interval, 2 d) CAS / CAS 1 (interval, 10 mo) Abbreviations: CAS, carotid stenting; CEA, carotid endarterectomy.
and/or CCS was not associated with perioperative complications. Restenosis after CAS did not occur in this study.
Treatment Strategy for Bilateral Carotid Steno-occlusive Lesions As described previously, 14 patients had CCO. Ten patients underwent CEA, and 3 patients underwent CAS. As shown in Table 3, in these 32 patients with bilateral severe carotid stenosis (.50%), 19 patients underwent unilateral reconstruction (CEA, 17; CAS, 2) and were carefully followed up for contralateral asymptomatic moderate carotid stenosis. The remaining13 patients underwent bilateral carotid reconstructions; CEA followed by CEA in 8, CEA followed by CAS in 3, CAS followed by CEA 1 coronary artery bpass grafting in 1, and CAS followed by CAS in 1. Thus, most of the cases with bilateral carotid stenosis were initially performed with CEA. The mean interval in CEA followed by CEA was 7 months (range, 4-12 months) whereas that of CEA followed by CAS was 7 weeks (range, 3-12 weeks). Thus, procedural interval was shorter in the patients who were performed with CEA followed by CAS.
Discussion There have been a few reports regarding the perioperative risks in the patients with contralateral ICA severe stenosis, and these have resulted in conflicting results.15,16 Several investigators thought that CAS would be better for the first revascularization procedure for bilateral carotid severe stenosis than CEA because CCS would adversely affect CEA.17,18 However, our data showed that the existence of contralateral carotid lesion was not associated with perioperative complications. Furthermore, most of our cases with bilateral carotid stenosis were initially performed CEA, and most of the patients who had
5
bilateral carotid reconstructions underwent CEA followed by CEA or CEA followed by CAS. There are 4 treatment strategies for bilateral cervical carotid artery stenosis: (1) CEA / CEA, (2) CAS / CAS, (3) CAS / CEA, and (4) CEA / CAS. There have been several reports on the reconstruction of bilateral ICA stenosis.10,17-26 In our previous case series report,26 the merits and demerits of each treatment strategy were thoroughly discussed, and we suggested that a combined therapy using CEA for the symptomatic side followed by CAS for the asymptomatic side can be one beneficial treatment option for patients with bilateral carotid stenosis. Recently, however, the combined therapy of CAS and then CEA has been recommended by several authors.17,18,24,25 Most of their patients underwent CAS for the asymptomatic side and then CEA for the symptomatic side because symptomatic plaques are often vulnerable and sometimes unsafe for CAS.17,18 However, the early risk of recurrent strokes during medical treatment is also high in patients with recent symptomatic carotid severe stenosis; relatively early surgery is therefore recommended.27,28 Symptomatic carotid plaques often consist of lipid-rich and intraplaque hematoma. Therefore, we suggest that these vulnerable plaques should be primarily treated by CEA. On the other hand, they thought that CAS would be better for the first revascularization procedure than CEA because CCS would adversely affect CEA.17,18 Although CCO does not adversely impact CAS,29-31 there have been no reports indicating that CAS is safer in patients with contralateral severe ICA stenosis than is CEA. In fact, contralateral occlusion is one of the risk factors in Protected Carotid-Artery Stenting versus Endarterectomy in High-Risk Patients (SAPPHIRE) trial but not CCS.4 The frequency of postprocedural hemodynamic complications such as hypotension and bradycardia was more than 50%.19,23 Thus, we think that hypotension after CAS for the asymptomatic side may be dangerous for the symptomatic hemisphere because CAS for the asymptomatic side usually does not improve hemodynamics in the symptomatic cerebral hemisphere. One of the most important questions is whether CCS increases the risk of patients undergoing CEA. There have been a few reports regarding the perioperative risks in the patients with contralateral ICA severe stenosis, and these have resulted in conflicting results.15,16 Interestingly, Goodney et al, who had previously reported contralateral occlusion increasing the risk of patients undergoing CEA,32 analyzed the perioperative risk of CEA with contralateral ICA occlusion, and they had suggested that routine shunt use during CEA was associated with fewer complications. However, surgeons who place shunts selectively during CEA have higher rates of complication.33 Estruch-Perez et al34 reported,
M. HOKARI ET AL.
6
moreover that patients with severe CCS (.50%) have a higher risk of requiring shunt use during CEA. Therefore, we think that the perioperative risk of CEA using shunts routinely may not adversely affect in an exceptional group of patients with contralateral ICA severe stenosis because cerebral hemodynamic impairment and cognitive dysfunction are more severe in patients with bilateral carotid stenosis than those with unilateral stenosis.35 In fact, our data showed that the existence of contralateral carotid lesion was not associated with perioperative complications, and most of our cases with bilateral carotid stenosis initially underwent CEA. Moreover, most of our patients who were performed with bilateral carotid reconstructions underwent CEA followed either by CEA or by CAS. We suggest that a combined therapy using CEA for the symptomatic side followed by CAS for the asymptomatic side can be one beneficial treatment option for patients who require early treatments with bilateral carotid stenosis, who need early treatment because procedural interval was shorter in the patients who were performed with CEA followed by CAS. This study has limitations, in that there are no data to be used for comparison analysis among the strategies. Thus, we cannot suggest that CEA would be better for the first revascularization procedure than CAS in the patients with bilateral carotid severe stenosis. Besides, this is neither prospective nor randomized study. Therefore, we cannot conclude that the existence of contralateral carotid lesion was not associated with perioperative complications in both CEA and CAS. In conclusion, we demonstrated that the existence of contralateral carotid lesion was not associated with perioperative complications, and most of our cases with bilateral carotid stenosis initially underwent CEA. We suggest that CEA would be better for the first revascularization procedure for the symptomatic or severe stenotic side than CAS on most of the patients with bilateral carotid severe stenosis.
References 1. Collaborators NASCET. 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. 2. Group ECSTC. MRC European Carotid Surgery Trial: interim results for symptomatic patients with severe (70-99%) or with mild (0-29%) carotid stenosis. European carotid surgery trialists’ collaborative group. Lancet 1991; 337:1235-1243. 3. Sheffet AJ, Roubin G, Howard G, et al. Design of the Carotid Revascularization Endarterectomy vs. Stenting Trial (CREST). Int J Stroke 2010;5:40-46. 4. Yadav JS, Wholey MH, Kuntz RE, et al. Protected carotidartery stenting versus endarterectomy in high-risk patients. N Engl J Med 2004;351:1493-1501.
5. Alric P, Branchereau P, Berthet JP, et al. Carotid artery stenting for stenosis following revascularization or cervical irradiation. J Endovasc Ther 2002;9:14-19. 6. Melliere D, Becquemin JP, Berrahal D, et al. Management of radiation-induced occlusive arterial disease: a reassessment. J Cardiovasc Surg (Torino) 1997;38:261-269. 7. Meyer FB, Piepgras DG, Fode NC. Surgical treatment of recurrent carotid artery stenosis. J Neurosurg 1994;80: 781-787. 8. Maleux G, Demaerel P, Verbeken E, et al. Cerebral ischemia after filter-protected carotid artery stenting is common and cannot be predicted by the presence of substantial amount of debris captured by the filter device. AJNR Am J Neuroradiol 2006;27:1830-1833. 9. Aikawa H, Kodama T, Nii K, et al. Intraprocedural plaque protrusion resulting in cerebral embolism during carotid angioplasty with stenting. Radiat Med 2008;26: 318-323. 10. Ogata N, Harashima K, Kanetani K, et al. Delayed plaque protrusion after carotid artery stenting for the patient with symptomatic bi-lateral carotid artery stenosis. Cardiovasc Interv Ther 2014;29:65-69. 11. Takigawa T, Matsumaru Y, Kubo T, et al. Recurrent subacute in-stent restenosis after carotid artery stenting due to plaque protrusion. Neurol Med Chir (Tokyo) 2009; 49:413-417. 12. Antoniou GA, Georgiadis GS, Georgakarakos EI, et al. Meta-analysis and meta-regression analysis of outcomes of carotid endarterectomy and stenting in the elderly. JAMA Surg 2013;148:1140-1152. 13. Touze E, Trinquart L, Felgueiras R, et al. A clinical rule (sex, contralateral occlusion, age, and restenosis) to select patients for stenting versus carotid endarterectomy: systematic review of observational studies with validation in randomized trials. Stroke 2013;44:3394-3400. 14. Iwasaki M, Kuroda S, Nakayama N, et al. Clinical characteristics and outcomes in carotid endarterectomy for internal carotid artery stenosis in a Japanese population: 10-year microsurgical experience. J Stroke Cerebrovasc Dis 2011;20:55-61. 15. Burke PE, Prendiville E, Tadros E, et al. Contralateral stenosis and stump pressures: Parameters to identify the high risk patient undergoing carotid endarterectomy under local anaesthesia. Eur J Vasc Surg 1993;7:317-319. 16. Gasecki AP, Eliasziw M, Ferguson GG, et al. Long-term prognosis and effect of endarterectomy in patients with symptomatic severe carotid stenosis and contralateral carotid stenosis or occlusion: results from NASCET. North American Symptomatic Carotid Endarterectomy Trial (NASCET) group. J Neurosurg 1995;83:778-782. 17. Kawabata Y, Nagata I, Sakai N, et al. Treatment of bilateral internal carotid artery stenosis. Surgery for Cerebral Stroke 2001;29:339-344. 18. Tsukahara T, Hatano T, Ogino E, et al. Surgical treatment for bilateral carotid arterial stenosis. Acta Neurochir Suppl 2005;94:133-136. 19. Alurkar A, Karanam LS, Nayak S, et al. Simultaneous bilateral carotid stenting in a series of 9 patients: a single-center experience with review of literature. J Clin Imaging Sci 2013;2:72. 20. Dong H, Jiang XJ, Peng M, et al. Comparison of the safety of simultaneous bilateral carotid artery stenting versus unilateral carotid artery stenting: 30-day and 6-month results. Chin Med J (Engl) 2012;125:1010-1015. 21. Henry M, Gopalakrishnan L, Rajagopal S, et al. Bilateral carotid angioplasty and stenting. Catheter Cardiovasc Interv 2005;64:275-282.
TREATMENT STRATEGY FOR BILATERAL CAROTID STENOSIS 22. Ille O, Woimant F, Pruna A, et al. Hypertensive encephalopathy after bilateral carotid endarterectomy. Stroke 1995;26:488-491. 23. Qureshi AI, Luft AR, Sharma M, et al. Frequency and determinants of postprocedural hemodynamic instability after carotid angioplasty and stenting. Stroke 1999;30: 2086-2093. 24. Shichinohe H, Kuroda S, Asano T, et al. [Novel stent/ CEA strategy for patients with bilateral carotid artery stenosis and coronary artery disease: report of 2 cases]. No Shinkei Geka 2005;33:149-153. 25. Kiris I, Gulmen S, Yilmaz S, et al. Management of concomitant coronary and bilateral carotid artery disease: a case report. J Card Surg 2007;22:149-151. 26. Hokari M, Isobe M, Asano T, et al. Treatment strategy for bilateral carotid stenosis: 2 cases of carotid endarterectomy for the symptomatic side followed by carotid stenting. J Stroke Cerebrovasc Dis 2014;23:2851-2856. 27. Rantner B, Pavelka M, Posch L, et al. Carotid endarterectomy after ischemic stroke–is there a justification for delayed surgery? Eur J Vasc Endovasc Surg 2005;30:36-40. 28. Rothwell PM, Slattery J, Warlow CP. A systematic comparison of the risks of stroke and death due to carotid endarterectomy for symptomatic and asymptomatic stenosis. Stroke 1996;27:266-269.
7
29. Faggioli G, Pini R, Mauro R, et al. Contralateral carotid occlusion in endovascular and surgical carotid revascularization: a single centre experience with literature review and meta-analysis. Eur J Vasc Endovasc Surg 2013;46:10-20. 30. Keldahl ML, Park MS, Garcia-Toca M, et al. Does a contralateral carotid occlusion adversely impact carotid artery stenting outcomes? Ann Vasc Surg 2012;26:40-45. 31. Yang SS, Kim YW, Kim DI, et al. Impact of contralateral carotid or vertebral artery occlusion in patients undergoing carotid endarterectomy or carotid artery stenting. J Vasc Surg 2014;59:749-755. 32. Goodney PP, Likosky DS, Cronenwett JL. Factors associated with stroke or death after carotid endarterectomy in Northern New England. J Vasc Surg 2008;48:1139-1145. 33. Goodney PP, Wallaert JB, Scali ST, et al. Impact of practice patterns in shunt use during carotid endarterectomy with contralateral carotid occlusion. J Vasc Surg 2012;55:61-71.e61. 34. Estruch-Perez MJ, Plaza-Martinez A, HernandezCadiz MJ, et al. Interaction of cerebrovascular disease and contralateral carotid occlusion in prediction of shunt insertion during carotid endarterectomy. Arch Med Sci 2012;8:236-243. 35. Balucani C, Viticchi G, Falsetti L, et al. Cerebral hemodynamics and cognitive performance in bilateral asymptomatic carotid stenosis. Neurology 2012;79:1788-1795.
