Risk Profile In Extracranial/Intracranial Bypass Surgery—The Role of Antiplatelet Agents, Disease Pathology, and Surgical Technique In 168 Direct Revascularization Procedures

doi:10.1016/j.wneu.2013.06.010

World Neurosurgery

Volume 82, Issue 5, November 2014, Pages 672-677

https://doi.org/10.1016/j.wneu.2013.06.010 Get rights and content

Objective

Cerebral revascularization procedures are a treatment option in moyamoya disease patients, but recent studies failed to show an immediate benefit in cerebrovascular atherosclerotic disease. To facilitate optimal efficacy of the procedure, a detailed characterization of a representative perioperative complication rate and the role of potential risk factors such as underlying pathology, antiplatelet therapy, and the type of surgery performed is warranted and the purpose of this study.

Methods

We included 158 consecutive patients with moyamoya disease or cerebrovascular atherosclerotic disease undergoing 168 direct revascularization procedures. Type of disease, antiplatelet therapy, coagulation disorders, surgical technique, intraoperative complications, postoperative imaging, the need for revision, and outcome at time of discharge were analyzed.

Results

Complication rate was low, with a high patency rate of 97%. Six hemispheres (3.6%) needed to undergo surgical revision; early morbidity was 10.7% with no mortality, with evidence of ischemia in 6.9% of patients. Type of pathology treated and surgical technique did not influence outcome. Antiplatelet treatment was not associated with an increased risk for hemorrhage or revision, but improved outcome (P < 0.05). Ischemia, hemorrhage, and the need for revision aggravated outcome at time of discharge.

Conclusion

Extra-/intracranial bypass surgery remains a treatment option in patients with moyamoya disease, although its use in the context of atherosclerotic disease was recently put into question. Regardless, a detailed characterization of perioperative risk factors is needed to optimize a potential long-term benefit of surgery. At a high-volume center, the complication rate is low independent from the underlying pathology with a high patency rate. Antiplatelet treatment does not increase the risk of hemorrhagic complications, but may improve outcome. Longer follow-up is required to adequately assess the true efficacy of revascularization on stroke prevention.

Introduction

Revascularization procedures, and extra-/intracranial (EC-IC) bypass surgery in particular (Figure 1), were originally devised to treat patients with internal carotid artery or middle cerebral artery stenosis or occlusion (9). The EC-IC bypass trial in 1985 (5), however, demonstrated that broad application of this procedure based on angiographic and clinical findings alone does not improve outcome, compared to conservative treatment alone. Later studies provided evidence that specific, high-risk subgroups of patients may still be amenable to surgical intervention and that stricter selection criteria are crucial to effectively filter those patients at highest risk for impending ischemic stroke, despite maximized medical treatment. Patients with angiographic evidence of cerebrovascular atherosclerotic disease (CAD) or moyamoya disease (MMD) may present with a history of (mostly transitory) neurologic events and borderzone infarctions on recent imaging. However, one of the most important selection criteria—which was not included in the EC-IC bypass trial—is evidence of cerebrovascular hemodynamic insufficiency, as the risk of future stroke increases dramatically (15), oftentimes despite aggressive antiplatelet treatment and high-normal blood pressure management. Hemodynamic insufficiency or the failure of an adequate response to a vasodilatory stimulus as characterized by the cerebrovascular reserve capacity constitutes a mandatory selection criterion (12), and EC-IC bypasses have repeatedly been shown to effectively improve cerebrovascular reserve capacity 3, 13.

As more data such as those from the recent Carotid Occlusion Surgery Study (COSS) study emerge (11), questioning the immediate efficacy of bypass surgery to reduce stroke risk in atherosclerotic patients and at the same time pointing out the inherent perioperative risks of the procedure, it is not only of the essence to define and agree on the most appropriate selection criteria. Although an evaluation of selection criteria particularly for patients with CAD is beyond the scope of this study, it is mandatory to determine a representative and likely more detailed complication rate of the surgical procedure itself in dedicated neurovascular centers as well as the association with potential risk factors, in order to optimize a potential long-term benefit over medical treatment alone.

It is the purpose of this observational analysis to describe the complication rate at our institution, and—as a next step—to identify a potential association with variables such as surgical technique, disease pathology (CAD vs. MMD), and antiplatelet treatment.

Section snippets

Material and Methods

For this purpose, we retrospectively analyzed patients undergoing a direct revascularization procedure at the Department of Neurosurgery, Universitätsmedizin Mannheim, University of Heidelberg, Germany. To be considered for a surgical procedure at our institution, among other considerations patients have to have evidence of recurrent ischemic symptoms with watershed but not territorial infarctions on magnetic resonance imaging, with the last neurologic event more than 6 weeks ago. Patients

Results

Of a total of 280 revascularization procedures performed on 246 patients at our institution from 2004 to 2009, only 158 patients (mean age 51.4 ± 13.2 years) undergoing a total of 168 direct revascularization procedures (demographic data, Table 2) were eligible for inclusion into this particular analysis, and only CAD or MMD patients were considered for our risk stratification. Of the remaining patients, all of the above-mentioned criteria were observed and complete data sets were available for

Discussion

The EC-IC bypass procedure was originally devised to reduce the subsequent stroke rate in patients with cerebral artery stenosis or occlusion 14, 17. Moyamoya patients in particular constitute an entity where surgical revascularization remains the most effective mainstay of treatment 6, 8, 10. Recently, the COSS study failed to show a significant improvement in outcome for patients with symptomatic atherosclerotic internal carotid artery occlusion when EC-IC bypass surgery was added to best

Conclusion

EC-IC bypass surgery remains a treatment option in patients with MMD, although its use in the context of atherosclerotic disease was recently put into question. Regardless, a detailed characterization of perioperative risk factors is needed to optimize a potential long-term surgical benefit. At a high-volume center, the complication rate is low with a high rate of successful primary revascularization. The risk profile is comparable for patients with MMD and CAD. EMS does not aggravate the risk

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Cited by (31)

Efficacy and Safety of Extracranial-Intracranial Bypass Surgery for Posterior Circulation Aneurysms: A Systematic Review and Single-Arm Meta-Analysis
2024, World Neurosurgery
Treating complex posterior circulation aneurysms poses challenges, and extracranial to intracranial (EC-IC) bypass techniques are potential therapeutic options. However, the safety and efficacy of this approach for posterior circulation aneurysms remain unclear. The study's objective was to assess the safety and efficacy of EC-IC bypass in these aneurysms.
Adhering to Preferred Reporting Items for Systematic Reviews and Meta-Analysis guidelines, we conducted a systematic review on EC-IC revascularization for posterior circulation aneurysms. Included studies had at least 4 patients and reported data on mortality, patency, complications, or clinical outcomes. Favorable clinical outcomes were defined as modified Rankin Scale below 3 or Glasgow Outcome Scale above 3, and complications were any issues related to the bypass procedure.
From 3036 articles reviewed, 22 studies involving 196 patients who underwent 210 EC-IC bypass procedures for posterior circulation aneurysms were selected. The median follow-up period of 14 studies was 31.66 months (6–61 months). Final follow-up indicated a high bypass patency rate of 96% [95% confidence interval [CI]: 91%–100%; I² = 12%], with a mortality rate of 5% [95% CI: 1%–9%; I² = 0%]. Additionally, 83% [95% CI: 70%–96%; I² = 77%] of patients showed good outcomes at the last follow-up. Complications were observed in 40% [95% CI: 26%–55%; I² = 80%]. Heterogeneity was associated with specific studies.
EC-IC bypass procedures are a viable treatment option for posterior circulation aneurysms, with high bypass patency rates and favorable clinical outcomes. However, complications, especially neurological deficits, exist. Open revascularization remains essential for neurovascular surgeons dealing with complex aneurysms.
Extracranial-Intracranial Cerebral Revascularization for Atherosclerotic Vessel Occlusion: An Updated Systematic Review of the Literature
2023, World Neurosurgery
Atherosclerotic steno-occlusive cerebrovascular disease includes extracranial carotid occlusive and intracranial atherosclerotic disease. Despite the negative findings in Carotid Occlusion Surgery Study (COSS), many large centers continue to report favorable results for revascularization surgery in select groups of patients. The aim of our study was to perform an updated systematic review to investigate the role of revascularization surgery for atherosclerotic steno-occlusive patients in the modern era.
Five independent reviewers performed Preferred Reporting Items for Systematic Reviews and Meta-Analyses–guided literature searches in October 2022 to identify articles reporting clinical outcomes in adult patients undergoing bypass for atherosclerotic steno-occlusive disease. Primary endpoints used were perioperative and long-term ischemic strokes, intracerebral hemorrhage, bypass patency, and favorable clinical outcomes. Study quality was evaluated with Newcastle-Ottawa, JADAD, and the Oxford Center for Evidence-Based Medicine scales.
A total of 6709 articles were identified in the initial search. Of these articles, 50 met the inclusion criteria and were included in the systematic review. A notable increase in the proportion of articles published over the past 10 years was observed. There were 6046 total patients with 4447 bypasses performed over the period from 1978 to 2022. The average length of follow-up was 2.75 ± 2.71 years. The average Newcastle-Ottawa was 6.23 out of 9 stars. There was a significant difference in perioperative stroke (odds ratio [OR], 0.65 [0.48–0.87]; P = 0.004), long-term ischemia (OR, 0.32 [0.23–0.44]; P < 0.0001), overall ischemia (OR, 0.36 [0.28–0.44]; P < 0.0001), and favorable outcomes (OR, 3.63 [2.84–4.64]; P < 0.0001) when comparing pre-COSS to post-COSS time frames in favor of post-COSS.
Based on a systematic review of 50 articles, the existing literature indicates that long-term stroke rates and favorable outcomes for surgical revascularization for steno-occlusive disease have improved over time and are lower than previously reported. Improved patient selection, perioperative care, and surgical techniques may contribute to improved outcomes.
Complementary Tools in Cerebral Bypass Surgery
2022, World Neurosurgery
Citation Excerpt :
While utilizing angiographic dyes has substantial buy-in costs, both dyes are ultimately far less expensive than DSA (i.e., ∼$100 per ICG vial).98 Regarding perioperative anticoagulation and antiplatelet management, reported regimens vary across the cerebral bypass and microsurgical free flap literature—at least partly due to a paucity of quality evidence.99,100 Variable usage patterns reflect an effort to achieve anastomosis patency while avoiding hemorrhagic complications, which have been reported following intraoperative heparinization during bypass.101
Cerebral revascularization surgery has been advanced by the refinement of several adjunctive tools. These tools include perioperative blood thinners, intraoperative spasmolytic agents, electrophysiological monitoring, and methods for assessing bypass patency or marking arteriotomies. Despite the array of options, the proper usage and comparative advantages of different complements in cerebral bypass have not been well-cataloged elsewhere. In this literature review, we describe the appropriate usage, benefits, and limitations of various bypass adjuncts. Understanding these adjuncts can help surgeons ensure that they receive reliable intraoperative information about bypass function and minimize the risk of serious complications. Overall, this review provides a succinct reference for neurosurgeons on various cerebrovascular bypass adjuncts.
Imaging Pattern and the Mechanisms of Postoperative Infarction After Indirect Revascularization in Patients with Moyamoya Disease
2021, World Neurosurgery
Citation Excerpt :
Antiplatelets were reported to decrease microembolic signals37 that might be related to the postoperative infarction caused by artery-to-artery embolization. In other studies, antiplatelets were reported not to increase the risk of hemorrhagic complications during revascularization surgery in MMD.38,39 After this study, we changed our perioperative management to continue antiplatelet therapy during the perioperative period.
To develop preventive strategies against postoperative infarction after indirect revascularization surgery in patients with moyamoya disease (MMD), we evaluated clinical information, with a specific focus on the imaging pattern of postoperative infarction.
We retrospectively evaluated 421 surgical procedures performed in 354 (262 pediatric and 159 adult) patients with MMD from April 1991 to March 2021 at our institute. In addition to clinical information, raw images of postoperative infarction were collected and categorized into subtypes by the location of the infarction.
Symptomatic and asymptomatic postoperative infarction occurred in 47 and 12 patients (11.1% and 2.6%), respectively, and more than half (51.7%) of these cases of postoperative infarction occurred immediately or the day after the surgery. Cortical infarction around the craniotomy site was the most frequent pattern observed (50/59, 84.8%), and some of these cases seemed to occur under local compression from epidural or subdural hematomas (15/50, 30.0%). Ipsilateral white matter infarctions located in the watershed area (9/59, 15.3%) and contralateral infarctions (3/59, 5.1%) were also observed. Four patients (1.0%) showed sudden occlusions of ipsilateral or contralateral large intracranial arteries immediately after surgery. Postoperative infarction caused permanent neurologic deficits in 7 patients (1.7%), and all included the cortex outside the craniotomy site.
Local cortical irritation, hemodynamic fluctuation, and thromboembolic events were suggested as possible mechanisms of postoperative infarction after indirect revascularization in patients with MMD. Minimizing cortical irritation, maintaining adequate cerebral blood flow, and perioperative antiplatelet agents might decrease the incidence of postoperative infarction.
Risk factors for ischemic complications in vascular reconstructive surgeries
2020, Clinical Neurology and Neurosurgery
Citation Excerpt :
Patients taking aspirin, cilostazol, warfarin, clopidogrel, and ethyl icosapentate as antithrombotic agents 3 days prior to the surgery were classified as taking preoperative antithrombotic agents. Usually, antithrombotic therapy was employed in all ischemic disease cases, and aneurysm treatment was used as well, except when there were multiple old ICH scars observed in the T2* MRI or a past history of ICH [10,11]. If patients took the antithrombotic drug before surgery, we continued the same drug because changing the drug itself has risks.
There have been reports on postoperative ischemic complications with vascular reconstructive surgery. However, various factors, such as lesions, operative technique, and perioperative treatment, prevent analyzing the causes of ischemic complications in vascular reconstruction surgeries. In the present study, we analyzed the cause of ischemic complications for vascular reconstruction surgeries with the same operator, surgical procedure, and perioperative treatment and without focusing on the lesions.
We retrospectively reviewed 66 patients, including 24 aneurysm cases and 42 ischemic disease cases, between 2008 and 2018. The patient group comprised 35 males and 31 females, and the patient mean age was 63.3 (23–87) years. We investigated the postoperative presence of symptomatic and asymptomatic cerebral ischemia on MRIDWI performed within 4 postoperative days. We conducted a statistical analysis of the ischemic complications and clinical and treatment factors.
Symptomatic cerebral ischemia was detected in 3 cases, whereas asymptomatic ischemic findings were identified in 8 cases. All cases of symptomatic cerebral ischemia involved cerebral aneurysms. Results of a univariate analysis revealed an association between symptomatic cerebral ischemia and preoperative antithrombotic therapy (OR, 0.07; p =  0.049 (95 %CI; 0.007–0.8794)), clipping (OR, 4.8; p =  0.0501 (95 %CI; 1.641–342.9)), and aneurysm (OR, 14.16; p =  0.0423 (95 %CI; 0.6991–286.9)). Significant associations were found between asymptomatic cerebral ischemia and preoperative antithrombotic therapy [OR, 0.2941; p =  0.0514 (95 %CI; 0.08335–1.038)], aneurysms [OR, 7.8; p =  0.0146 (95 %CI; 1.414–43.04)] and radial artery grafts (RAGs) [OR, 6.8; p =  0.0192 (95 %CI; 1.410–32.98)]. Multivariate analysis identified clipping [OR, 5.462; p =  0.045 (95 %CI; 1.01–78.25] and preoperative antithrombotic therapy [OR, 0.187; p =  0.037 (95 %CI; 0.004–0.813)] as the risk factors for symptomatic cerebral ischemia. Further, a correlation was found between asymptomatic cerebral ischemia and RAGs [OR, 9.244; p =  0.00013 (95 %CI; 2.34–29.44)].
Ischemic complications associated with combined vascular reconstruction surgeries for cerebral aneurysms are possibly associated with procedures related to aneurysmal occlusions. Thus, vascular reconstruction surgeries can be performed relatively safely. Further, preoperative antithrombotic treatment should be considered, and caution is required for asymptomatic cerebral ischemia in RAG cases.
Medical Management Versus Surgical Bypass for Symptomatic Intracranial Atherosclerotic Disease: A Systematic Review
2019, World Neurosurgery
Intracranial atherosclerotic disease (ICAD) is a major cause of stroke worldwide. The optimal management of patients with symptomatic ICAD is controversial. Therefore, the aim of this systematic review is to compare medical management versus surgical bypass for the treatment of symptomatic ICAD.
A literature review was performed to identify studies reporting outcomes of patients with ICAD who were managed medically or surgically with either direct or indirect bypass. Baseline, treatment, and outcomes data were analyzed. Complications included ischemic stroke, intracranial hemorrhage, and cerebrovascular death. Secondary analyses of the surgically treated cohort were performed to compare the outcomes of direct versus indirect bypass.
The pooled analysis was derived from 18 studies, comprising a total of 2160 patients with ICAD, including 1790 managed medically and 370 treated with surgical bypass. The rates of ischemic stroke, intracranial hemorrhage, and cerebrovascular death were 16%, 1%, and 4.5% in the medical cohort, respectively, versus 8%, 0.6%, and 1.9% in the surgical cohort, respectively. Among patients with ICAD who underwent bypass surgery, the rates of ischemic stroke and cerebrovascular death were 7% and 1.9% in the direct bypass group, respectively, versus 19% and 2.1% in the indirect bypass group, respectively.
Direct or indirect bypass surgery is a reasonable treatment option for appropriately selected patients with ICAD. Careful preoperative evaluation of hemodynamic parameters and the relevant donor and recipient vessels is crucial to maximizing the success of bypass for ICAD. Further studies remain necessary to clarify the roles of medical versus surgical management for ICAD.

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: Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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Peer-Review ReportRisk Profile In Extracranial/Intracranial Bypass Surgery—The Role of Antiplatelet Agents, Disease Pathology, and Surgical Technique In 168 Direct Revascularization Procedures

Objective

Methods

Results

Conclusion

Introduction

Section snippets

Material and Methods

Results

Discussion

Conclusion

J Am Coll Cardiol

EC-IC bypass for stroke—is this the end of the line or a bump in the road?

Neurosurgery

Failure of cerebral hemodynamic selection in general or of specific positron emission tomography methodology? Carotid Occlusion Surgery Study (COSS)

Stroke

Characterization of direct and indirect cerebral revascularization for the treatment of European patients with moyamoya disease

Cerebrovasc Dis

Compensatory mechanisms for chronic cerebral hypoperfusion in patients with carotid occlusion

Stroke

Failure of extracranial-intracranial arterial bypass to reduce the risk of ischemic stroke. Results of an international randomized trial. The EC/IC Bypass Study Group

N Engl J Med

Impact of extracranial-intracranial bypass on cerebrovascular reactivity and clinical outcome in patients with symptomatic moyamoya vasculopathy

Stroke

Risk of intraoperative ischemia due to temporary vessel occlusion during standard extracranial-intracranial arterial bypass surgery

J Neurosurg

Peer-Review Report
Risk Profile In Extracranial/Intracranial Bypass Surgery—The Role of Antiplatelet Agents, Disease Pathology, and Surgical Technique In 168 Direct Revascularization Procedures