- Email: [email protected]
Surgical Dissection of the Internal Carotid Artery Under Flow Control by Proximal Vessel Clamping Reduces Embolic Infarcts During Carotid Endarterectomy
Peer-Review Reports
Surgical Dissection of the Internal Carotid Artery Under Flow Control by Proximal Vessel Clamping Reduces Embolic Infarcts During Carotid Endarterectomy Kazumichi Yoshida1, Yoshitaka Kurosaki2, Takeshi Funaki1, Takayuki Kikuchi1, Akira Ishii1, Jun C. Takahashi1, Yasushi Takagi1, Sen Yamagata2, Susumu Miyamoto1
Key words Carotid endarterectomy - Diffusion-weighted imaging - Embolization - Surgical technique
- OBJECTIVE:
Abbreviations and Acronyms CAS: Carotid artery stenting CCA: Common carotid artery CEA: Carotid endarterectomy DWI: Diffusion-weighted image ECA: External carotid artery ICA: Internal carotid artery MES: Microembolic signals NIRS: Near-infrared spectroscopy SEP: Somatosensory-evoked potential STA: Superior thyroid artery TCD: Transcranial Doppler sonography
- METHODS:
From the 1Department of Neurosurgery, Kyoto University Graduate School of Medicine, Kyoto; and 2Department of Neurosurgery, Kurashiki Central Hospital, Okayama, Japan
- RESULTS:
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To whom correspondence should be addressed to: Kazumichi Yoshida, M.D., Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2014). http://dx.doi.org/10.1016/j.wneu.2013.06.018 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2014 Elsevier Inc. All rights reserved.
INTRODUCTION Approximately 20% of ischemic strokes are caused by atherosclerosis of the carotid artery, and the benefits of carotid endarterectomy (CEA) for symptomatic and asymptomatic carotid stenosis have been widely proven by several major clinical trials (1-3, 27). The absolute benefit of CEA, however, is limited by the morbidity and mortality, among which the leading is embolic stroke during CEA (24). Wolf et al. (32) investigated the correlation between microembolic signals (MES) detected by transcranial Doppler sonography (TCD) during CEA and cerebral ischemia confirmed by postoperative diffusion-weighted imaging (DWI) and concluded that dissection and shunting were the most vulnerable stages of
To evaluate the efficacy of flow control of the internal carotid artery (ICA) by the clamping of the common carotid artery, external carotid artery, and superior thyroid artery during surgical ICA dissection to reduce ischemic complications after carotid endarterectomy (CEA). Sixty-seven patients (59 men; age, 70.5 6.2 years) who underwent CEA by the same surgeon were retrospectively studied. Both conventional CEA (n [ 29) and flow-control CEA (n [ 38) were performed with the patient under general anesthesia and with the use of somatosensory-evoked potential and near-infrared spectroscopy monitoring as a guide for selective shunting. The number of new postoperative infarcts was assessed with preoperative and postoperative diffusion-weighted images (DWIs) obtained within 3 days of surgery. In addition to surgical technique, the effects of the following factors on new infarcts also were examined: age, side of ICA stenosis, high-grade stenosis, symptoms, and application of shunting.
New postoperative DWI lesions were observed in 7 of 67 patients (10.4%), and none of them was symptomatic. With respect to operative technique, the incidence rate of DWI spots was significantly lower in the flowcontrol group (2.6%) than in the conventional group (20.7%), odds ratio: 0.069; 95% confidence interval: 0.006e0.779; P [ 0.031). On multiple logistic regression analysis, age, side of ICA stenosis, high-grade stenosis, symptoms, and the use of internal shunting did not have significant effects on new postoperative DWI lesions, whereas technique did have an effect.
- CONCLUSION:
The proximal flow-control technique for CEA helps avoid embolic complications during surgical ICA dissection.
CEA with respect to cerebral embolism. In the light of the fact that early CEA for symptomatic carotid stenosis, if done safely, is more beneficial than delayed CEA for preventing recurrence (13, 28) and early CEA is associated with a significantly increased rate of perioperative stroke (26), the type of surgical technique to reduce the risk of embolization during CEA will be of increasing significance. Several reports in which the authors examined CEA procedures of early surgical dissection and clamping of the distal internal carotid artery (ICA) aimed at reduction of intraoperative embolization have been reported (8, 19, 21).The efficacy of the early distal ICA control technique compared with the conventional CEA
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technique, however, is still controversial. In contrast, many articles on the effect of different neuroprotection systems on microembolization during carotid artery stenting (CAS) have demonstrated the superiority of proximal endovascular clamping devices to distal filter devices or distal balloon protection systems (20, 29, 31). The author was inspired by these reports on protection systems for CAS and designed a “flow-control” CEA technique for the surgical dissection of ICA by clamping the common carotid artery (CCA), external carotid artery (ECA), and superior thyroid artery (STA). The aim of the present study was to evaluate the efficacy of flow-control CEA in reduction of new ischemic lesions detected by postoperative DWI.
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METHODS Patients Sixty-eight consecutive patients with carotid stenosis who underwent CEA by the same operator (K.Y.) were identified initially. One with a serious intraoperative cardiac complication was excluded. The rationale for exclusion was that it was not possible to conclusively attribute perioperative infarcts to the operative technique itself. Thus, the data of 67 patients (59 men; age, 70.5 6.2 years) were analyzed. The severity of carotid artery stenosis was evaluated by either of carotid duplex ultrasonography, computed tomography angiography, and digital subtraction angiography using the North American Symptomatic Trial Collaborators criteria (1), and the stenosis rate was 72.6% 20.1% (average SD). The characteristics of the 67 consecutive CEA cases are summarized in Table 1. The study was approved by the hospital ethics committee, and informed consent was obtained from all patients. Conventional CEA Technique Under general anesthesia, somatosensoryevoked potentials (SEP) and near-infrared spectroscopy (NIRS) monitoring was used to guide selective use of the internal shunt. After a longitudinal curvilinear incision along the sternocleidomastoid muscle, the focus of surgical dissection was initially centered on the proximal
Table 1. Patient Characteristics of the Study Population Number of Patients (%) Age, years, mean SD Male
70.5 6.2 59 (88.1)
Right-sided stenosis % stenosis, mean SD
31 (46.3) 72.6 20.1
Symptomatic patients
36 (53.7)
Early CEA
18 (26.9)
Hypertension
50 (74.6)
Hyperlipidemia
34 (50.7)
Diabetes
23 (34.3)
Coronary artery disease
18 (26.9)
CEA, carotid endarterectomy.
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CCA. Once the CCA was confirmed, the carotid sheath was then gently dissected from the CCA to the distal ICA and ECA tracing on the outer wall of the arteries. The extent of ICA plaque was evaluated with preoperative carotid magnetic resonance imaging (34). to minimize the use of palpation for identification of the distal plaque end. After the CCA was identified, the STA, ECA, and ICA were completely exposed; the patient was heparinized; and an increase of the activated coagulation time to more than double the control value was confirmed. The CCA and ECA were clamped with a “bull-dog” clamp, and the ICA and STA were each clamped with a vascular clip. Then, the SEP and NIRS changes were observed carefully for approximately 5 minutes. When the SEP/NIRS values showed no substantial changes during these first minutes, standard longitudinal endarterectomy was subsequently started. Monitoring with SEP/NIRS was continued to ensure safety during endarterectomy. When the amplitude of SEP showed a >50% decrease and/or the value of NIRS decreased >20%, a shunt was inserted before the start of endarterectomy. Preoperatively administered antithrombotics were not interrupted during the perioperative period, and single antiplatelet therapy was continued in principle after CEA. Flow-Control CEA Technique The preparation and surgical procedure for flow control CEA were the same as for conventional CEA until a longitudinal skin incision was made and the surgical dissection was started in the vicinity of the proximal CCA. After the proximal CCA was completely dissected, the carotid sheath was then carefully divided longitudinally toward the carotid bifurcation and the ECA. Special attention was paid to ensure that the carotid sheath dissection did not extend over the ICA at this stage to avoid inadvertent compression of the carotid bifurcation or the ICA enclosing fragile plaque. After the CCA, ECA, and STA were completely exposed, the patient was heparinized, and these proximal three vessels were clamped in this order (Figure 1). The dissection of the carotid sheath around the ICA was then begun, and exposure and isolation of the distal ICA were completed under flow control. The time required to
accomplish this final stage of vessel exposure was 8.5 3.4 minutes in the most recent 15 flow-control CEA procedures. The additional occlusion time needed in flowcontrol CEA compared with conventional CEA with a 5 minutes’ test clump to evaluate the necessity of an internal shunt was approximately 3.5 minutes. SEP and NIRS changes were monitored carefully during this time. If SEP and NIRS monitoring showed no significant changes, a vascular clip was then applied to the ICA distal enough to the limit of the plaque, and an endarterectomy was performed. When SEP/ NIRS values reached the levels described previously, a shunt was inserted before the endarterectomy. The procedure of flowcontrol CEA is shown in Figure 2.
Comparison of Flow-Control CEA and Conventional CEA Conventional CEA was used in 29 patients, mainly during the first half of the study duration, and flow-control CEA was used in latter 38 patients. CEA techniques were changed in mid-stream after publication of several articles on effect of different protection systems during CAS as described previously. The incidence rate of new postoperative infarcts confirmed by perioperative DWIs was compared between flow-control CEA
Figure 1. Operative photograph of a patient with symptomatic right carotid artery stenosis. It shows selective dissection and control of the common carotid artery, external carotid artery, and superior thyroid artery with “bull-dog” clamps and a vascular clip. At this point, the plaque-bearing internal carotid artery (asterisk) is totally covered with the carotid sheath and connective tissue. Ansa Cer., ansa cervicalis; Com. Car. A., common carotid artery; CN, cranial nerve; Ext. Car. A., external carotid artery; Int. Jug. V., internal jugular vein; Sup. Ther. A., superior thyroid artery.
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Figure 2. Schematic illustrations of flow-control carotid endarterectomy. (A) The common carotid artery, external carotid artery, and superior thyroid artery are isolated and controlled before the plaque-bearing internal carotid artery is dissected. (B) The carotid sheath over the internal carotid artery is dissected under flow control by clamping proximal vessels while
and conventional CEA by an experienced investigator (Y.K.) who was blinded to the clinical information. Both pre- and postoperative DWIs were obtained within 3 days of surgery with the use of a 1.5-T whole-body MR imaging unit (Gyroscan Intera Philips Medical Systems, Best, The Netherlands). The parameters of DWI were as follows: single-shot EPI, field of view 250e280 mm, matrix size 128 256, TR/TE 3500e5000/90 milliseconds, flip angle 90 , slice thickness 4e5 mm, and bfactor 1600. In addition to surgical technique, the effects of the following factors on new infarcts were also examined: age, side of ICA stenosis, high-grade stenosis defined as 70%, symptoms, and use of shunting. Symptomatic patients were defined as those who had experienced amaurosis fugax, a transient ischemic attack, or a stroke in the territory of the ipsilateral carotid artery within 6 months. As for timing of surgery, early CEA was defined as that performed within 14 days of the last ischemic event, and elective CEA was defined as that performed 15 or more days after the last ischemic event. Statistical Analysis All data were statistically analyzed using SPSS 12.0 for Windows (SPSS Institute, Chicago, Illinois, USA). Multiple logistic regression analysis was performed to adjust for other predictors of new infarcts during CEA (age, side of ICA stenosis, high-grade stenosis, symptoms, shunting). The results are expressed as odds ratios with 95% confidence intervals.
somatosensory-evoked potential and near infrared spectroscopy changes are carefully monitored. (C) After exposure and isolation of the distal internal carotid artery are completed, standard longitudinal endarterectomy is then begun.
RESULTS
DISCUSSION
No postoperative symptomatic ischemic events, including those in the contralateral hemisphere, were confirmed during the course of hospitalization. New asymptomatic ischemic lesions, all of which were small, high-signal spots on DWI, were confirmed in 7 of 67 patients (10.4%). With respect to operative technique, flow-control CEA was adopted in 18 of 36 symptomatic patients (50%) and 20 of 31 asymptomatic patients (64.5%), respectively, with no significant difference in use ratio. New DWI spots were detected in 6 of 29 patients (20.7%) with conventional CEA and one of 38 patients (2.6%) with flow-control CEA. With respect to side of ICA stenosis, DWI lesions detected in 4 of 31 (12.9%) with right-sided ICA stenosis and 3 of 37 (8.1%) with left-sided ICA stenosis. With respect to symptoms, DWI spots were observed in 5 of 36 symptomatic patients (13.9%) and 2 of 31 asymptomatic patients (6.5%). Of the 36 symptomatic patients, DWI lesions were demonstrated in 3 of 18 patients (16.7%) with early CEA and 2 of 18 patients (11.1%) with elective CEA. Concerning the rate of stenosis, the incidence of DWI spots was 5 of 46 (10.9%) with high-grade stenosis and 2 of 21 (9.5%) with nonhigh-grade stenosis. Finally, with respect to use of shunting, the incidence of DWI spots was one of 9 (11.1%) with shunting CEA and 6 of 58 (10.3%) with nonshunting CEA. On multiple logistic regression analysis, only CEA technique (flow-control CEA) was associated with a low incidence of new DWI abnormalities (odds ratio 0.069; 95% confidence interval 0.006e0.779; P ¼ 0.031; Table 2)
The leading causes of ischemic complications associated with CEA are embolism, mainly during (and infrequently) after the procedure, and cerebral hypoperfusion attributable to cross-clamping (25). Although it is controversial whether a shunt should be used routinely or selectively because of complications associated with shunt insertion itself, cerebral hypoperfsion can be addressed by shunting even in cases when patients have insufficient intracranial collateral circulation, (17, 33). As for embolization during CEA, it is generally accepted that a meticulous surgical procedure is essential for its reduction. Few reports, however, have addressed
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Table 2. Multivariate Logistic Regression Analysis of Factors associated with New DWI Lesions Odds Ratio
95% CI
P Value
Age
1.120 0.930e1.349 0.234
Right-sided ICS
1.715 0.286e10.301 0.555
High-grade stenosis
0.773 0.109e5.508 0.797
Symptomatic ICS
1.646 0.255e10.635 0.600
Use of internal shunt
0.486 0.041e5.754 0.567
Flow control CEA 0.069 0.006e0.779 0.031* CEA, carotid endarterectomy; CI, confidence interval; DWI, diffusion-weighted image; ICS, internal carotid artery stenosis. *P < 0.05 is statistically significant.
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the specific procedural measures to reduce intraoperative embolization (8, 19, 21). Studies of transcranial Doppler monitoring during CEA offer valuable insight into questions concerning which procedure has the most significant effect on intraoperative embolization (5, 10, 11, 14, 32). Wolf et al. (32) reported that the rate of MES at each step during CEA was 97% with declamping, followed by 69.7% with shunting, and 45.5% with dissection. A significant correlation between MES and postoperative DWI lesions, however, was found only with dissection, which was referred to as being the most vulnerable stage of CEA. It is, therefore, reasonable to speculate that early control of the ICA will be effective for prevention of embolization. In fact, so far, all reports examining surgical procedures aimed at reduction of intraoperative embolization analyzed the efficacy of early surgical dissection and clamping of the distal ICA (8, 19, 21). Bourke and Crimmins (8) and Pratesi et al. (21) reported that early distal control of the ICA might have benefit for reducing intraoperative ischemic events, whereas Mommertz et al. (19) confirmed that it had no advantage but also no disadvantage as compared to the conventional CEA technique. Our concept of the CEA procedure is the same as that of the previous three reports, in that the ICA in which fragile atherosclerotic plaque exists should be dissected under flow control, but the CEA technique used in the present study was entirely different in that flow of the ICA was indirectly controlled by dissecting and clamping the proximal ECA, STA, and CCA. As a result, the incidence of new DWI lesions confirmed by early postoperative magnetic resonance imaging decreased sharply compared with conventional CEA. Compared with the CEA technique advocated in previous studies, the present flow-control technique has two advantages. First, the present technique requires no manipulation of the area between the carotid bifurcation and the ICA distal enough to the limit of plaque before completion of flow control, whereas the earlier methods, in which the distal ICA is dissected first for early ICA flow control, cannot help applying stress to the ICA itself before flow control is achieved. The situation might be quite similar to the preventive effect against embolization in
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DISSECTION OF THE ICA UNDER FLOW CONTROL
carotid stenting, where the proximal protection methods are safer than the distal protection methods in which embolization cannot be prevented during the passage of the protection device per se (20, 31). Second, the interruption time of ICA blood flow of the present method is shorter than that of the previous methods. Only the dissection of the carotid sheath between the bifurcation and the distal ICA, when the ICA is under the most intense stress by manipulation, is done under flow control in the present technique, whereas the entire dissection procedure from the distal ICA to the CCA, ECA, and STA is performed under flow control in the other methods. In the present conventional CEA, all related arteries were dissected, and then SEP and NIRS changes were carefully monitored for approximately 5 minutes before starting endarterectomy to evaluate the necessity of shunting. There was no much difference between our conventional and the flow-control technique in the interruption time of the ICA because distal ICA dissection in the flow-control CEA is almost completed while SEP and NIRS changes are observed after clamping of the CCA, ECA and STA to determine the need for selective shunting. In the past major clinical trials, postoperative ischemic events after CEA were examined mainly through assessments by neurologists, which basically cannot detect “silent” ischemic events within brain areas without primary motor, sensory, or speech function. Therefore, the monitoring of postoperative infarcts with DWI was used in the present study to evaluate the safety of CEA techniques more accurately and objectively (6, 12). With respect to so-called silent infarcts after CEA, some reports demonstrated the associations between “silent” ischemic lesions and long-term cognitive dysfunctions, while others found no such associations (7, 15, 16, 18). In the current circumstances where available studies cannot provide a definite answer to the question whether “silent” DWI lesions are really silent in the long term, CEA techniques should be continuously improved, with evaluations not only by neurologists but also by the assessment of asymptomatic DWI lesions, to achieve a zero ischemic event rate.
In the review article on new brain lesions comprising 754 CEA procedures, the author demonstrated the incidence of any DWI lesion after CEA was 10%, while the data about the timing of the CEA were not available, and most of CEAs seemed to be elective (30). Although the incidence of a new DWI lesion after early CEA remains to be reported to our knowledge, a large cohort of independently monitored patients undergoing early CEA demonstrated that the rate of death/stroke at 30 days was 8.4%, which indicates a considerably high incidence of DWI (22) The positive DWI rate in the present study can compare favorably with the results reported until now, because more than half of the cases was symptomatic (36/67), and approximately 30% of procedures (18/67) were early CEA in this study. Moreover, the DWI-positive rate of flow-control CEA in the present study was considerably lower (2.6%) than in other studies (30). These results of the present study suggest that flow-control CEA is reasonably effective for reducing intraoperative ischemic complications. Recent outstanding progress in multifaceted medical treatment for atherosclerotic vascular disease has brought an argument against wide-ranging application of CEA for asymptomatic stenosis (4). On the other hand, for symptomatic cases, the demonstration of the benefit of CEA performed soon after ischemic events will naturally cause an increase in the percentage of early CEA performed (9, 13). Furthermore, the risk of embolic complications has been shown to be greater in CEA for symptomatic stenosis than for asymptomatic stenosis and also greater in early CEA than in elective CEA for symptomatic patients (23). Considering these circumstances, the importance of technical innovation for safer CEA will necessarily increase as vascular surgeons have increasing opportunities to perform CEA in patients with a greater risk of intraoperative embolization. The present study assessing the efficacy of flow-control CEA has several limitations. First, intraoperative emboli were not confirmed directly by TCD monitoring. In the assessment of the difference in emboli, including DWI-negative ones, with different surgical techniques, TCD monitoring is more accurate than DWI evaluation. Moreover, it is impossible with
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DWI to differentiate between emboli occurring during CEA and those occurring in the early pre- and postoperative periods (11). Nevertheless, the present finding that a broad distinction in DWI-positive rates was confirmed because of a difference only in surgical techniques substantially supports the efficacy of flow-control CEA. Second, this study was a retrospective analysis of surgical results by the same surgeon, and we could not eliminate the influence of the learning curve effect. With respect to postoperative DWI spots of consecutive 29 patients with conventional CEA, those of the first 15 patients were 3 and those of the latter 14 patients were 3, with no significant difference depending on the surgeon’s experience in this study period. Although the impact of the learning curve effect seems to be relatively low, a prospective study is mandatory to make the efficacy of flow control CEA more clear, adopting randomization of CEA techniques and regular TCD monitoring. CONCLUSION The proximal flow-control technique, in which the ICA is surgically dissected after clamping of the proximal CCA, ECA, and STA, is efficacious for avoiding embolic complications during CEA. REFERENCES 1. Beneficial effect of carotid endarterectomy in symptomatic patients with high-grade carotid stenosis. N Engl J Med 325:445-453, 1991. 2. Endarterectomy for asymptomatic carotid artery stenosis. JAMA 273:1421-1428, 1995. 3. MRC European Carotid Surgery Trial: interim results for symptomatic patients with severe (7099%) or with mild (0-29%) carotid stenosis. Lancet 337:1235-1243, 1991. 4. Abbott AL: Medical (nonsurgical) intervention alone is now best for prevention of stroke associated with asymptomatic severe carotid stenosis: results of a systematic review and analysis. Stroke 40:e573-583, 2009. 5. Ackerstaff RG, Moons KG, van de Vlasakker CJ, Moll FL, Vermeulen FE, Algra A, Spencer MP: Association of intraoperative transcranial Doppler monitoring variables with stroke from carotid endarterectomy. Stroke 31:1817-1823, 2000. 6. Barth A, Remonda L, Lovblad KO, Schroth G, Seiler RW: Silent cerebral ischemia detected by diffusion-weighted MRI after carotid endarterectomy. Stroke 31:1824-1828, 2000.
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19. Mommertz G, Das M, Langer S, Koeppel TA, Krings T, Mess WH, Schiefer J, Jacobs MJ: Early control of distal internal carotid artery during carotid endarterectomy: does it reduce cerebral microemboli? J Cardiovasc Surg (Torino) 51: 369-375, 2010. 20. Montorsi P, Caputi L, Galli S, Ciceri E, Ballerini G, Agrifoglio M, Ravagnani P, Trabattoni D, Pontone G, Fabbiocchi F, Loaldi A, Parati E, Andreini D, Veglia F, Bartorelli AL: Microembolization during carotid artery stenting in patients with high-risk, lipid-rich plaque. A randomized trial of proximal versus distal cerebral protection. J Am Coll Cardiol 58:1656-1663, 2011. 21. Pratesi C, Dorigo W, Innocenti AA, Azas L, Barbanti E, Lombardi R, Pratesi G, Pulli R: Reducing the risk of intraoperative neurological complications during carotid endarterectomy with early distal control of the internal carotid artery. Eur J Vasc Endovasc Surg 28:670-673, 2004. 22. Rantner B, Eckstein HH, Ringleb P, Woelfle KD, Bruijnen H, Schmidauer C, Fraedrich G: American society of anesthesiology and rankin as predictive parameters for the outcome of carotid endarterectomy within 28 days after an ischemic stroke. J Stroke Cerebrovasc Dis 15:114-120, 2006. 23. Rerkasem K, Rothwell PM: Systematic review of the operative risks of carotid endarterectomy for recently symptomatic stenosis in relation to the timing of surgery. Stroke 40:e564-572, 2009. 24. Rerkasem K, Rothwell PM: Temporal trends in the risks of stroke and death due to endarterectomy for symptomatic carotid stenosis: an updated systematic review. Eur J Vasc Endovasc Surg 37:504-511, 2009. 25. Riles TS, Imparato AM, Jacobowitz GR, Lamparello PJ, Giangola G, Adelman MA, Landis R: The cause of perioperative stroke after carotid endarterectomy. J Vasc Surg 19:206-214; discussion 215-206, 1994. 26. Rockman CB, Maldonado TS, Jacobowitz GR, Cayne NS, Gagne PJ, Riles TS: Early carotid endarterectomy in symptomatic patients is associated with poorer perioperative outcomes. J Vasc Surg 44:480-487, 2006. 27. Rothwell PM, Eliasziw M, Gutnikov SA, Fox AJ, Taylor DW, Mayberg MR, Warlow CP, Barnett HJ: Analysis of pooled data from the randomised controlled trials of endarterectomy for symptomatic carotid stenosis. Lancet 361:107-116, 2003. 28. Rothwell PM, Eliasziw M, Gutnikov SA, Warlow CP, Barnett HJ: Endarterectomy for symptomatic carotid stenosis in relation to clinical subgroups and timing of surgery. Lancet 363: 915-924, 2004. 29. Schmidt A, Diederich KW, Scheinert S, Braunlich S, Olenburger T, Biamino G, Schuler G, Scheinert D: Effect of two different neuroprotection systems on microembolization during carotid artery stenting. J Am Coll Cardiol 44: 1966-1969, 2004. 30. Schnaudigel S, Groschel K, Pilgram SM, Kastrup A: New brain lesions after carotid stenting versus carotid endarterectomy: a systematic review of the literature. Stroke 39:1911-1919, 2008.
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31. Tallarita T, Rabinstein AA, Cloft H, Kallmes D, Oderich GS, Brown RD, Lanzino G: Are distal protection devices ’protective’ during carotid angioplasty and stenting? Stroke 42:1962-1966, 2011. 32. Wolf O, Heider P, Heinz M, Poppert H, Sander D, Greil O, Weiss W, Hanke M, Eckstein HH: Microembolic signals detected by transcranial Doppler sonography during carotid endarterectomy and correlation with serial diffusionweighted imaging. Stroke 35:e373-375, 2004. 33. Woodworth GF, McGirt MJ, Than KD, Huang J, Perler BA, Tamargo RJ: Selective versus routine
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intraoperative shunting during carotid endarterectomy: a multivariate outcome analysis. Neurosurgery 61:1170-1176; discussion 1176-1177, 2007. 34. Yoshida K, Endo H, Sadamasa N, Narumi O, Chin M, Inoue K, Mitsudo K, Yamagata S: Evaluation of carotid artery atherosclerotic plaque distribution by using long-axis high-resolution black-blood magnetic resonance imaging. J Neurosurg 109:1042-1048, 2008.
commercial or financial relationships that could be construed as a potential conflict of interest. Received 24 December 2012; accepted 29 June 2013 Citation: World Neurosurg. (2014). http://dx.doi.org/10.1016/j.wneu.2013.06.018 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2014 Elsevier Inc. All rights reserved.
Conflict of interest statement: The authors declare that the article content was composed in the absence of any
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2013.06.018
Surgical Dissection of the Internal Carotid Artery Under Flow Control by Proximal Vessel Clamping Reduces Embolic Infarcts During Carotid Endarterectomy Kazumichi Yoshida1, Yoshitaka Kurosaki2, Takeshi Funaki1, Takayuki Kikuchi1, Akira Ishii1, Jun C. Takahashi1, Yasushi Takagi1, Sen Yamagata2, Susumu Miyamoto1
Key words Carotid endarterectomy - Diffusion-weighted imaging - Embolization - Surgical technique
- OBJECTIVE:
Abbreviations and Acronyms CAS: Carotid artery stenting CCA: Common carotid artery CEA: Carotid endarterectomy DWI: Diffusion-weighted image ECA: External carotid artery ICA: Internal carotid artery MES: Microembolic signals NIRS: Near-infrared spectroscopy SEP: Somatosensory-evoked potential STA: Superior thyroid artery TCD: Transcranial Doppler sonography
- METHODS:
From the 1Department of Neurosurgery, Kyoto University Graduate School of Medicine, Kyoto; and 2Department of Neurosurgery, Kurashiki Central Hospital, Okayama, Japan
- RESULTS:
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To whom correspondence should be addressed to: Kazumichi Yoshida, M.D., Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2014). http://dx.doi.org/10.1016/j.wneu.2013.06.018 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2014 Elsevier Inc. All rights reserved.
INTRODUCTION Approximately 20% of ischemic strokes are caused by atherosclerosis of the carotid artery, and the benefits of carotid endarterectomy (CEA) for symptomatic and asymptomatic carotid stenosis have been widely proven by several major clinical trials (1-3, 27). The absolute benefit of CEA, however, is limited by the morbidity and mortality, among which the leading is embolic stroke during CEA (24). Wolf et al. (32) investigated the correlation between microembolic signals (MES) detected by transcranial Doppler sonography (TCD) during CEA and cerebral ischemia confirmed by postoperative diffusion-weighted imaging (DWI) and concluded that dissection and shunting were the most vulnerable stages of
To evaluate the efficacy of flow control of the internal carotid artery (ICA) by the clamping of the common carotid artery, external carotid artery, and superior thyroid artery during surgical ICA dissection to reduce ischemic complications after carotid endarterectomy (CEA). Sixty-seven patients (59 men; age, 70.5 6.2 years) who underwent CEA by the same surgeon were retrospectively studied. Both conventional CEA (n [ 29) and flow-control CEA (n [ 38) were performed with the patient under general anesthesia and with the use of somatosensory-evoked potential and near-infrared spectroscopy monitoring as a guide for selective shunting. The number of new postoperative infarcts was assessed with preoperative and postoperative diffusion-weighted images (DWIs) obtained within 3 days of surgery. In addition to surgical technique, the effects of the following factors on new infarcts also were examined: age, side of ICA stenosis, high-grade stenosis, symptoms, and application of shunting.
New postoperative DWI lesions were observed in 7 of 67 patients (10.4%), and none of them was symptomatic. With respect to operative technique, the incidence rate of DWI spots was significantly lower in the flowcontrol group (2.6%) than in the conventional group (20.7%), odds ratio: 0.069; 95% confidence interval: 0.006e0.779; P [ 0.031). On multiple logistic regression analysis, age, side of ICA stenosis, high-grade stenosis, symptoms, and the use of internal shunting did not have significant effects on new postoperative DWI lesions, whereas technique did have an effect.
- CONCLUSION:
The proximal flow-control technique for CEA helps avoid embolic complications during surgical ICA dissection.
CEA with respect to cerebral embolism. In the light of the fact that early CEA for symptomatic carotid stenosis, if done safely, is more beneficial than delayed CEA for preventing recurrence (13, 28) and early CEA is associated with a significantly increased rate of perioperative stroke (26), the type of surgical technique to reduce the risk of embolization during CEA will be of increasing significance. Several reports in which the authors examined CEA procedures of early surgical dissection and clamping of the distal internal carotid artery (ICA) aimed at reduction of intraoperative embolization have been reported (8, 19, 21).The efficacy of the early distal ICA control technique compared with the conventional CEA
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technique, however, is still controversial. In contrast, many articles on the effect of different neuroprotection systems on microembolization during carotid artery stenting (CAS) have demonstrated the superiority of proximal endovascular clamping devices to distal filter devices or distal balloon protection systems (20, 29, 31). The author was inspired by these reports on protection systems for CAS and designed a “flow-control” CEA technique for the surgical dissection of ICA by clamping the common carotid artery (CCA), external carotid artery (ECA), and superior thyroid artery (STA). The aim of the present study was to evaluate the efficacy of flow-control CEA in reduction of new ischemic lesions detected by postoperative DWI.
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METHODS Patients Sixty-eight consecutive patients with carotid stenosis who underwent CEA by the same operator (K.Y.) were identified initially. One with a serious intraoperative cardiac complication was excluded. The rationale for exclusion was that it was not possible to conclusively attribute perioperative infarcts to the operative technique itself. Thus, the data of 67 patients (59 men; age, 70.5 6.2 years) were analyzed. The severity of carotid artery stenosis was evaluated by either of carotid duplex ultrasonography, computed tomography angiography, and digital subtraction angiography using the North American Symptomatic Trial Collaborators criteria (1), and the stenosis rate was 72.6% 20.1% (average SD). The characteristics of the 67 consecutive CEA cases are summarized in Table 1. The study was approved by the hospital ethics committee, and informed consent was obtained from all patients. Conventional CEA Technique Under general anesthesia, somatosensoryevoked potentials (SEP) and near-infrared spectroscopy (NIRS) monitoring was used to guide selective use of the internal shunt. After a longitudinal curvilinear incision along the sternocleidomastoid muscle, the focus of surgical dissection was initially centered on the proximal
Table 1. Patient Characteristics of the Study Population Number of Patients (%) Age, years, mean SD Male
70.5 6.2 59 (88.1)
Right-sided stenosis % stenosis, mean SD
31 (46.3) 72.6 20.1
Symptomatic patients
36 (53.7)
Early CEA
18 (26.9)
Hypertension
50 (74.6)
Hyperlipidemia
34 (50.7)
Diabetes
23 (34.3)
Coronary artery disease
18 (26.9)
CEA, carotid endarterectomy.
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CCA. Once the CCA was confirmed, the carotid sheath was then gently dissected from the CCA to the distal ICA and ECA tracing on the outer wall of the arteries. The extent of ICA plaque was evaluated with preoperative carotid magnetic resonance imaging (34). to minimize the use of palpation for identification of the distal plaque end. After the CCA was identified, the STA, ECA, and ICA were completely exposed; the patient was heparinized; and an increase of the activated coagulation time to more than double the control value was confirmed. The CCA and ECA were clamped with a “bull-dog” clamp, and the ICA and STA were each clamped with a vascular clip. Then, the SEP and NIRS changes were observed carefully for approximately 5 minutes. When the SEP/NIRS values showed no substantial changes during these first minutes, standard longitudinal endarterectomy was subsequently started. Monitoring with SEP/NIRS was continued to ensure safety during endarterectomy. When the amplitude of SEP showed a >50% decrease and/or the value of NIRS decreased >20%, a shunt was inserted before the start of endarterectomy. Preoperatively administered antithrombotics were not interrupted during the perioperative period, and single antiplatelet therapy was continued in principle after CEA. Flow-Control CEA Technique The preparation and surgical procedure for flow control CEA were the same as for conventional CEA until a longitudinal skin incision was made and the surgical dissection was started in the vicinity of the proximal CCA. After the proximal CCA was completely dissected, the carotid sheath was then carefully divided longitudinally toward the carotid bifurcation and the ECA. Special attention was paid to ensure that the carotid sheath dissection did not extend over the ICA at this stage to avoid inadvertent compression of the carotid bifurcation or the ICA enclosing fragile plaque. After the CCA, ECA, and STA were completely exposed, the patient was heparinized, and these proximal three vessels were clamped in this order (Figure 1). The dissection of the carotid sheath around the ICA was then begun, and exposure and isolation of the distal ICA were completed under flow control. The time required to
accomplish this final stage of vessel exposure was 8.5 3.4 minutes in the most recent 15 flow-control CEA procedures. The additional occlusion time needed in flowcontrol CEA compared with conventional CEA with a 5 minutes’ test clump to evaluate the necessity of an internal shunt was approximately 3.5 minutes. SEP and NIRS changes were monitored carefully during this time. If SEP and NIRS monitoring showed no significant changes, a vascular clip was then applied to the ICA distal enough to the limit of the plaque, and an endarterectomy was performed. When SEP/ NIRS values reached the levels described previously, a shunt was inserted before the endarterectomy. The procedure of flowcontrol CEA is shown in Figure 2.
Comparison of Flow-Control CEA and Conventional CEA Conventional CEA was used in 29 patients, mainly during the first half of the study duration, and flow-control CEA was used in latter 38 patients. CEA techniques were changed in mid-stream after publication of several articles on effect of different protection systems during CAS as described previously. The incidence rate of new postoperative infarcts confirmed by perioperative DWIs was compared between flow-control CEA
Figure 1. Operative photograph of a patient with symptomatic right carotid artery stenosis. It shows selective dissection and control of the common carotid artery, external carotid artery, and superior thyroid artery with “bull-dog” clamps and a vascular clip. At this point, the plaque-bearing internal carotid artery (asterisk) is totally covered with the carotid sheath and connective tissue. Ansa Cer., ansa cervicalis; Com. Car. A., common carotid artery; CN, cranial nerve; Ext. Car. A., external carotid artery; Int. Jug. V., internal jugular vein; Sup. Ther. A., superior thyroid artery.
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Figure 2. Schematic illustrations of flow-control carotid endarterectomy. (A) The common carotid artery, external carotid artery, and superior thyroid artery are isolated and controlled before the plaque-bearing internal carotid artery is dissected. (B) The carotid sheath over the internal carotid artery is dissected under flow control by clamping proximal vessels while
and conventional CEA by an experienced investigator (Y.K.) who was blinded to the clinical information. Both pre- and postoperative DWIs were obtained within 3 days of surgery with the use of a 1.5-T whole-body MR imaging unit (Gyroscan Intera Philips Medical Systems, Best, The Netherlands). The parameters of DWI were as follows: single-shot EPI, field of view 250e280 mm, matrix size 128 256, TR/TE 3500e5000/90 milliseconds, flip angle 90 , slice thickness 4e5 mm, and bfactor 1600. In addition to surgical technique, the effects of the following factors on new infarcts were also examined: age, side of ICA stenosis, high-grade stenosis defined as 70%, symptoms, and use of shunting. Symptomatic patients were defined as those who had experienced amaurosis fugax, a transient ischemic attack, or a stroke in the territory of the ipsilateral carotid artery within 6 months. As for timing of surgery, early CEA was defined as that performed within 14 days of the last ischemic event, and elective CEA was defined as that performed 15 or more days after the last ischemic event. Statistical Analysis All data were statistically analyzed using SPSS 12.0 for Windows (SPSS Institute, Chicago, Illinois, USA). Multiple logistic regression analysis was performed to adjust for other predictors of new infarcts during CEA (age, side of ICA stenosis, high-grade stenosis, symptoms, shunting). The results are expressed as odds ratios with 95% confidence intervals.
somatosensory-evoked potential and near infrared spectroscopy changes are carefully monitored. (C) After exposure and isolation of the distal internal carotid artery are completed, standard longitudinal endarterectomy is then begun.
RESULTS
DISCUSSION
No postoperative symptomatic ischemic events, including those in the contralateral hemisphere, were confirmed during the course of hospitalization. New asymptomatic ischemic lesions, all of which were small, high-signal spots on DWI, were confirmed in 7 of 67 patients (10.4%). With respect to operative technique, flow-control CEA was adopted in 18 of 36 symptomatic patients (50%) and 20 of 31 asymptomatic patients (64.5%), respectively, with no significant difference in use ratio. New DWI spots were detected in 6 of 29 patients (20.7%) with conventional CEA and one of 38 patients (2.6%) with flow-control CEA. With respect to side of ICA stenosis, DWI lesions detected in 4 of 31 (12.9%) with right-sided ICA stenosis and 3 of 37 (8.1%) with left-sided ICA stenosis. With respect to symptoms, DWI spots were observed in 5 of 36 symptomatic patients (13.9%) and 2 of 31 asymptomatic patients (6.5%). Of the 36 symptomatic patients, DWI lesions were demonstrated in 3 of 18 patients (16.7%) with early CEA and 2 of 18 patients (11.1%) with elective CEA. Concerning the rate of stenosis, the incidence of DWI spots was 5 of 46 (10.9%) with high-grade stenosis and 2 of 21 (9.5%) with nonhigh-grade stenosis. Finally, with respect to use of shunting, the incidence of DWI spots was one of 9 (11.1%) with shunting CEA and 6 of 58 (10.3%) with nonshunting CEA. On multiple logistic regression analysis, only CEA technique (flow-control CEA) was associated with a low incidence of new DWI abnormalities (odds ratio 0.069; 95% confidence interval 0.006e0.779; P ¼ 0.031; Table 2)
The leading causes of ischemic complications associated with CEA are embolism, mainly during (and infrequently) after the procedure, and cerebral hypoperfusion attributable to cross-clamping (25). Although it is controversial whether a shunt should be used routinely or selectively because of complications associated with shunt insertion itself, cerebral hypoperfsion can be addressed by shunting even in cases when patients have insufficient intracranial collateral circulation, (17, 33). As for embolization during CEA, it is generally accepted that a meticulous surgical procedure is essential for its reduction. Few reports, however, have addressed
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Table 2. Multivariate Logistic Regression Analysis of Factors associated with New DWI Lesions Odds Ratio
95% CI
P Value
Age
1.120 0.930e1.349 0.234
Right-sided ICS
1.715 0.286e10.301 0.555
High-grade stenosis
0.773 0.109e5.508 0.797
Symptomatic ICS
1.646 0.255e10.635 0.600
Use of internal shunt
0.486 0.041e5.754 0.567
Flow control CEA 0.069 0.006e0.779 0.031* CEA, carotid endarterectomy; CI, confidence interval; DWI, diffusion-weighted image; ICS, internal carotid artery stenosis. *P < 0.05 is statistically significant.
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the specific procedural measures to reduce intraoperative embolization (8, 19, 21). Studies of transcranial Doppler monitoring during CEA offer valuable insight into questions concerning which procedure has the most significant effect on intraoperative embolization (5, 10, 11, 14, 32). Wolf et al. (32) reported that the rate of MES at each step during CEA was 97% with declamping, followed by 69.7% with shunting, and 45.5% with dissection. A significant correlation between MES and postoperative DWI lesions, however, was found only with dissection, which was referred to as being the most vulnerable stage of CEA. It is, therefore, reasonable to speculate that early control of the ICA will be effective for prevention of embolization. In fact, so far, all reports examining surgical procedures aimed at reduction of intraoperative embolization analyzed the efficacy of early surgical dissection and clamping of the distal ICA (8, 19, 21). Bourke and Crimmins (8) and Pratesi et al. (21) reported that early distal control of the ICA might have benefit for reducing intraoperative ischemic events, whereas Mommertz et al. (19) confirmed that it had no advantage but also no disadvantage as compared to the conventional CEA technique. Our concept of the CEA procedure is the same as that of the previous three reports, in that the ICA in which fragile atherosclerotic plaque exists should be dissected under flow control, but the CEA technique used in the present study was entirely different in that flow of the ICA was indirectly controlled by dissecting and clamping the proximal ECA, STA, and CCA. As a result, the incidence of new DWI lesions confirmed by early postoperative magnetic resonance imaging decreased sharply compared with conventional CEA. Compared with the CEA technique advocated in previous studies, the present flow-control technique has two advantages. First, the present technique requires no manipulation of the area between the carotid bifurcation and the ICA distal enough to the limit of plaque before completion of flow control, whereas the earlier methods, in which the distal ICA is dissected first for early ICA flow control, cannot help applying stress to the ICA itself before flow control is achieved. The situation might be quite similar to the preventive effect against embolization in
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carotid stenting, where the proximal protection methods are safer than the distal protection methods in which embolization cannot be prevented during the passage of the protection device per se (20, 31). Second, the interruption time of ICA blood flow of the present method is shorter than that of the previous methods. Only the dissection of the carotid sheath between the bifurcation and the distal ICA, when the ICA is under the most intense stress by manipulation, is done under flow control in the present technique, whereas the entire dissection procedure from the distal ICA to the CCA, ECA, and STA is performed under flow control in the other methods. In the present conventional CEA, all related arteries were dissected, and then SEP and NIRS changes were carefully monitored for approximately 5 minutes before starting endarterectomy to evaluate the necessity of shunting. There was no much difference between our conventional and the flow-control technique in the interruption time of the ICA because distal ICA dissection in the flow-control CEA is almost completed while SEP and NIRS changes are observed after clamping of the CCA, ECA and STA to determine the need for selective shunting. In the past major clinical trials, postoperative ischemic events after CEA were examined mainly through assessments by neurologists, which basically cannot detect “silent” ischemic events within brain areas without primary motor, sensory, or speech function. Therefore, the monitoring of postoperative infarcts with DWI was used in the present study to evaluate the safety of CEA techniques more accurately and objectively (6, 12). With respect to so-called silent infarcts after CEA, some reports demonstrated the associations between “silent” ischemic lesions and long-term cognitive dysfunctions, while others found no such associations (7, 15, 16, 18). In the current circumstances where available studies cannot provide a definite answer to the question whether “silent” DWI lesions are really silent in the long term, CEA techniques should be continuously improved, with evaluations not only by neurologists but also by the assessment of asymptomatic DWI lesions, to achieve a zero ischemic event rate.
In the review article on new brain lesions comprising 754 CEA procedures, the author demonstrated the incidence of any DWI lesion after CEA was 10%, while the data about the timing of the CEA were not available, and most of CEAs seemed to be elective (30). Although the incidence of a new DWI lesion after early CEA remains to be reported to our knowledge, a large cohort of independently monitored patients undergoing early CEA demonstrated that the rate of death/stroke at 30 days was 8.4%, which indicates a considerably high incidence of DWI (22) The positive DWI rate in the present study can compare favorably with the results reported until now, because more than half of the cases was symptomatic (36/67), and approximately 30% of procedures (18/67) were early CEA in this study. Moreover, the DWI-positive rate of flow-control CEA in the present study was considerably lower (2.6%) than in other studies (30). These results of the present study suggest that flow-control CEA is reasonably effective for reducing intraoperative ischemic complications. Recent outstanding progress in multifaceted medical treatment for atherosclerotic vascular disease has brought an argument against wide-ranging application of CEA for asymptomatic stenosis (4). On the other hand, for symptomatic cases, the demonstration of the benefit of CEA performed soon after ischemic events will naturally cause an increase in the percentage of early CEA performed (9, 13). Furthermore, the risk of embolic complications has been shown to be greater in CEA for symptomatic stenosis than for asymptomatic stenosis and also greater in early CEA than in elective CEA for symptomatic patients (23). Considering these circumstances, the importance of technical innovation for safer CEA will necessarily increase as vascular surgeons have increasing opportunities to perform CEA in patients with a greater risk of intraoperative embolization. The present study assessing the efficacy of flow-control CEA has several limitations. First, intraoperative emboli were not confirmed directly by TCD monitoring. In the assessment of the difference in emboli, including DWI-negative ones, with different surgical techniques, TCD monitoring is more accurate than DWI evaluation. Moreover, it is impossible with
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DWI to differentiate between emboli occurring during CEA and those occurring in the early pre- and postoperative periods (11). Nevertheless, the present finding that a broad distinction in DWI-positive rates was confirmed because of a difference only in surgical techniques substantially supports the efficacy of flow-control CEA. Second, this study was a retrospective analysis of surgical results by the same surgeon, and we could not eliminate the influence of the learning curve effect. With respect to postoperative DWI spots of consecutive 29 patients with conventional CEA, those of the first 15 patients were 3 and those of the latter 14 patients were 3, with no significant difference depending on the surgeon’s experience in this study period. Although the impact of the learning curve effect seems to be relatively low, a prospective study is mandatory to make the efficacy of flow control CEA more clear, adopting randomization of CEA techniques and regular TCD monitoring. CONCLUSION The proximal flow-control technique, in which the ICA is surgically dissected after clamping of the proximal CCA, ECA, and STA, is efficacious for avoiding embolic complications during CEA. REFERENCES 1. Beneficial effect of carotid endarterectomy in symptomatic patients with high-grade carotid stenosis. N Engl J Med 325:445-453, 1991. 2. Endarterectomy for asymptomatic carotid artery stenosis. JAMA 273:1421-1428, 1995. 3. MRC European Carotid Surgery Trial: interim results for symptomatic patients with severe (7099%) or with mild (0-29%) carotid stenosis. Lancet 337:1235-1243, 1991. 4. Abbott AL: Medical (nonsurgical) intervention alone is now best for prevention of stroke associated with asymptomatic severe carotid stenosis: results of a systematic review and analysis. Stroke 40:e573-583, 2009. 5. Ackerstaff RG, Moons KG, van de Vlasakker CJ, Moll FL, Vermeulen FE, Algra A, Spencer MP: Association of intraoperative transcranial Doppler monitoring variables with stroke from carotid endarterectomy. Stroke 31:1817-1823, 2000. 6. Barth A, Remonda L, Lovblad KO, Schroth G, Seiler RW: Silent cerebral ischemia detected by diffusion-weighted MRI after carotid endarterectomy. Stroke 31:1824-1828, 2000.
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31. Tallarita T, Rabinstein AA, Cloft H, Kallmes D, Oderich GS, Brown RD, Lanzino G: Are distal protection devices ’protective’ during carotid angioplasty and stenting? Stroke 42:1962-1966, 2011. 32. Wolf O, Heider P, Heinz M, Poppert H, Sander D, Greil O, Weiss W, Hanke M, Eckstein HH: Microembolic signals detected by transcranial Doppler sonography during carotid endarterectomy and correlation with serial diffusionweighted imaging. Stroke 35:e373-375, 2004. 33. Woodworth GF, McGirt MJ, Than KD, Huang J, Perler BA, Tamargo RJ: Selective versus routine
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commercial or financial relationships that could be construed as a potential conflict of interest. Received 24 December 2012; accepted 29 June 2013 Citation: World Neurosurg. (2014). http://dx.doi.org/10.1016/j.wneu.2013.06.018 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2014 Elsevier Inc. All rights reserved.
Conflict of interest statement: The authors declare that the article content was composed in the absence of any
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