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Seungwon Yoon, Jan-Karl Burkhardt, and Michael T. Lawton

OBJECTIVE

Large cohort analysis concerning intracerebral bypass patency in patients with long-term follow-up (FU) results is rarely reported in the literature. The authors analyzed the long-term patency of extracranial-to-intracranial (EC-IC) and intracranial-to-intracranial (IC-IC) bypass procedures.

METHODS

All intracranial bypass procedures performed between 1997 and 2017 by a single surgeon were screened. Patients with postoperative imaging (CT angiography, MR angiography, or catheter angiography) were included and grouped into immediate (< 7 days), short-term (7 days–1 year), and long-term (> 1 year) FU groups. Data on patient demographics, bypass type, interposition graft type, bypass indication, and radiological patency were collected and analyzed with univariate and multivariate (adjusted multiple regression) models.

RESULTS

In total, 430 consecutive bypass procedures were performed during the study period (FU time [mean ± SD] 0.9 ± 2.2 years, range 0–17 years). Twelve cases were occluded at FU imaging, resulting in an overall cumulative patency rate of 97%. All bypass occlusions occurred within a week of revascularization. All patients in the short-term FU group (n = 76, mean FU time 0.3 ± 0.3 years) and long-term FU group (n = 89, mean FU time 4.1 ± 3.5 years) had patent bypasses at last FU. Patients who presented with aneurysms had a lower rate of patency than those with moyamoya disease or chronic vessel occlusion (p = 0.029). Low-flow bypasses had a significantly higher patency rate than high-flow bypasses (p = 0.033). In addition, bypasses with one anastomosis site compared to two anastomosis sites showed a significantly higher bypass patency (p = 0.005). No differences were seen in the patency rate among different grafts, single versus bilateral, or between EC-IC and IC-IC bypasses.

CONCLUSIONS

The overall bypass patency of 97% indicates a high likelihood of success with microsurgical revascularization. Surgical indication (ischemia), low-flow bypass, and number of anastomosis (one site) were associated with higher patency rates. EC-IC and IC-IC bypasses have comparable patency rates, supporting the use of intracranial reconstructive techniques. Bypasses that remain patent 1 week postoperatively and have the opportunity to mature have a high likelihood of remaining patent in the long term. In experienced hands, cerebral revascularization is a durable treatment option with high patency rates.

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Jan-Karl Burkhardt, Ethan A. Winkler, and Michael T. Lawton

OBJECTIVE

Deep medial parietooccipital arteriovenous malformations (AVMs) and cerebral cavernous malformations (CCMs) are traditionally resected through an ipsilateral posterior interhemispheric approach (IPIA), which creates a deep, perpendicular perspective with limited access to the lateral margins of the lesion. The contralateral posterior interhemispheric approach (CPIA) flips the positioning, with the midline positioned horizontally for retraction due to gravity, but with the AVM on the upper side and the approach from the contralateral, lower side. The aim of this paper was to analyze whether the perpendicular angle of attack that is used in IPIA would convert to a parallel angle of attack with the CPIA, with less retraction, improved working angles, and no significant increase in risk.

METHODS

A retrospective review of pre- and postoperative clinical and radiographic data was performed in 8 patients who underwent a CPIA.

RESULTS

Three AVMs and 5 CCMs were resected using the CPIA, with an average nidus size of 2.3 cm and CCM diameter of 1.7 cm. All lesions were resected completely, as confirmed on postoperative catheter angiography or MRI. All patients had good neurological outcomes, with either stable or improved modified Rankin Scale scores at last follow-up.

CONCLUSIONS

The CPIA is a safe alternative approach to the IPIA for deep medial parietooccipital vascular malformations that extend 2 cm or more off the midline. Contralaterality and retraction due to gravity optimize the interhemispheric corridor, the surgical trajectory to the lesion, and the visualization of the lateral margin, without resection or retraction of adjacent normal cortex. Although the falx is a physical barrier to accessing the lesion, it stabilizes the ipsilateral hemisphere while gravity delivers the dissected lesion through the transfalcine window. Patient positioning, CSF drainage, venous preservation, and meticulous dissection of the deep margins are critical to the safety of this approach.

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David Bellut, Jan-Karl Burkhardt, Anne F. Mannion, and François Porchet

OBJECT

The aim of this study was to evaluate outcome in patients undergoing surgical treatment for intradural spinal tumor using a patient-oriented, self-rated, outcome instrument and a physician-based disease-specific instrument.

METHODS

Prospectively collected data from 63 patients with intradural spinal tumor were analyzed in relation to scores on the multidimensional patient-rated Core Outcome Measures Index (COMI) and the physician-rated modified McCormick Scale, before and at 3 and 12 months after surgery.

RESULTS

There was no statistically significant difference between the scores on the modified McCormick Scale preoperatively and at the 3-month follow-up, though there was a trend for improvement (p = 0.073); however, comparisons between the scores determined preoperatively and at the 12-month follow-up, as well as 3- versus 12-month follow-ups, showed a statistically significant improvement in each case (p < 0.004). The COMI scores for axial pain, peripheral pain, and back-related function showed a significant reduction (p < 0.001) from before surgery to 3 months after surgery, and thereafter showed no further change (p > 0.05) up to 12 months postoperatively. In contrast, the overall COMI score, “worst pain,” quality of life, and social disability not only showed a significant reduction from before surgery to 3 months after surgery (p < 0.001), but also a further significant reduction up to 12 months postoperatively (p < 0.001). The scores for work disability showed no significant improvement from before surgery to the 3-month follow-up (p > 0.05), but did show a significant improvement (p = 0.011) from 3 months to 12 months after surgery. At the 3- and 12-month follow-ups, 85.2% and 83.9% of patients, respectively, declared that the surgical procedure had helped/helped a lot; 95.1% and 95.2%, respectively, declared that they were satisfied/very satisfied with their care.

CONCLUSIONS

COMI is a feasible tool to use in the evaluation of baseline symptoms and outcome in patients undergoing surgery for intradural spinal tumor. COMI was able to detect changes in outcome at 3 months after surgery (before changes were apparent on the modified McCormick Scale) and on later postoperative follow-up. The COMI subdomains are valuable for monitoring the patient’s reintegration into society and the work environment. The addition of an item that specifically covers neurological deficits may further increase the value of COMI in patients with spinal tumors.

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Kavelin Rumalla, Visish M. Srinivasan, Monica Gaddis, Peter Kan, Michael T. Lawton, and Jan-Karl Burkhardt

OBJECTIVE

Extracranial-intracranial (EC-IC) bypass surgery remains an important treatment option for patients with moyamoya disease (MMD), intracranial arteriosclerotic disease (ICAD) with symptomatic stenosis despite the best medical management, and complex aneurysms. The therapeutic benefit of cerebral bypass surgery depends on optimal patient selection and the minimization of periprocedural complications. The nationwide burden of readmissions and associated complications following EC-IC bypass surgery has not been previously described. Therefore, the authors sought to analyze a nationwide database to describe the national rates, causes, risk factors, complications, and morbidity associated with readmission following EC-IC bypass surgery for MMD, ICAD, and aneurysms.

METHODS

The Nationwide Readmissions Database (NRD) was queried for the years 2010–2014 to identify patients who had undergone EC-IC bypass for MMD, medically failed symptomatic ICAD, or unruptured aneurysms. Predictor variables included demographics, preexisting comorbidities, indication for surgery, and hospital bypass case volume. A high-volume center (HVC) was defined as one that performed 10 or more cases/year. Outcome variables included perioperative stroke, discharge disposition, length of stay, total hospital costs, and readmission (30 days, 90 days). Multivariable analysis was used to identify predictors of readmission and to study the effect of treatment at HVCs on quality outcomes.

RESULTS

In total, 2500 patients with a mean age of 41 years were treated with EC-IC bypass surgery for MMD (63.1%), ICAD (24.5%), or unruptured aneurysms (12.4%). The 30- and 90-day readmission rates were 7.5% and 14.0%, respectively. Causes of readmission included new stroke (2.5%), wound complications (2.5%), graft failure (1.5%), and other infection (1.3%). In the multivariable analysis, risk factors for readmission included Medicaid/self-pay (OR 1.6, 95% CI 1.1–2.4, vs private insurance), comorbidity score (OR 1.2, 95% CI 1.1–1.4, per additional comorbidity), and treatment at a non-HVC (OR 1.9, 95% CI 1.1–3.0). Treatment at an HVC (17% of patients) was associated with significantly lower rates of nonroutine discharge dispositions (13.4% vs 26.7%, p = 0.004), ischemic stroke within 90 days (0.8% vs 2.9%, p = 0.03), 30-day readmission (3.9% vs 8.2%, p = 0.03), and 90-day readmission (8.6% vs 15.2%, p = 0.01). These findings were confirmed in a multivariable analysis. The authors estimate that centralization to HVCs may result in 333 fewer nonroutine discharges (50% reduction), 12,000 fewer hospital days (44% reduction), 165 fewer readmissions (43%), and a cost savings of $15.3 million (11% reduction).

CONCLUSIONS

Readmission rates for patients after EC-IC bypass are comparable with those after other common cranial procedures and are primarily driven by preexisting comorbidities, socioeconomic status, and treatment at low-volume centers. Periprocedural complications, including stroke, graft failure, and wound complications, occurred at the expected rates, consistent with those in prior clinical series. The centralization of care may significantly reduce perioperative complications, readmissions, and hospital resource utilization.

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Jan-Karl Burkhardt, Michelle H. Chua, Ethan A. Winkler, W. Caleb Rutledge, and Michael T. Lawton

OBJECTIVE

During the microsurgical clipping of known aneurysms, angiographically occult (AO) aneurysms are sometimes found and treated simultaneously to prevent their growth and protect the patient from future rupture or reoperation. The authors analyzed the incidence, treatment, and outcomes associated with AO aneurysms to determine whether limited surgical exploration around the known aneurysm was safe and justified given the known limitations of diagnostic angiography.

METHODS

An AO aneurysm was defined as a saccular aneurysm detected using the operative microscope during dissection of a known aneurysm, and not detected on preoperative catheter angiography. A prospective database was retrospectively reviewed to identify patients with AO aneurysms treated microsurgically over a 20-year period.

RESULTS

One hundred fifteen AO aneurysms (4.0%) were identified during 2867 distinct craniotomies for aneurysm clipping. The most common locations for AO aneurysms were the middle cerebral artery (60 aneurysms, 54.1%) and the anterior cerebral artery (20 aneurysms, 18.0%). Fifty-six AO aneurysms (50.5%) were located on the same artery as the known saccular aneurysm. Most AO aneurysms (95.5%) were clipped and there was no attributed morbidity. The most common causes of failed angiographic detection were superimposition of a large aneurysm (type 1, 30.6%), a small aneurysm (type 2, 18.9%), or an adjacent normal artery (type 3, 36.9%). Multivariate analysis identified multiple known aneurysms (odds ratio [OR] 3.45, 95% confidence interval [CI] 2.16–5.49, p < 0.0001) and young age (OR 0.981, 95% CI 0.965–0.997, p = 0.0226) as independent predictors of AO aneurysms.

CONCLUSIONS

Meticulous inspection of common aneurysm sites within the surgical field will identify AO aneurysms during microsurgical dissection of another known aneurysm. Simultaneous identification and treatment of these additional undiagnosed aneurysms can spare patients later rupture or reoperation, particularly in those with multiple known aneurysms and a history of subarachnoid hemorrhage. Limited microsurgical exploration around a known aneurysm can be performed safely without additional morbidity.

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Tomoya Kamide, Halima Tabani, Michael M. Safaee, Jan-Karl Burkhardt, and Michael T. Lawton

OBJECTIVE

While most paraclinoid aneurysms can be clipped with excellent results, new postoperative visual deficits are a concern. New technology, including flow diverters, has increased the popularity of endovascular therapy. However, endovascular treatment of paraclinoid aneurysms is not without procedural risks, is associated with higher rates of incomplete aneurysm occlusion and recurrence, and may not address optic nerve compression symptoms that surgical debulking can. The increasing endovascular management of paraclinoid aneurysms should be justified by comparisons to surgical benchmarks. The authors, therefore, undertook this study to define patient, visual, and aneurysm outcomes in the most common type of paraclinoid aneurysm: ophthalmic artery (OphA) aneurysms.

METHODS

Results from microsurgical clipping of 208 OphA aneurysms in 198 patients were retrospectively reviewed. Patient demographics, aneurysm morphology (size, calcification, etc.), clinical characteristics, and patient outcomes were recorded and analyzed.

RESULTS

Despite 20% of these aneurysms being large or giant in size, complete aneurysm occlusion was accomplished in 91% of 208 cases, with OphA patency preserved in 99.5%. The aneurysm recurrence rate was 3.1% and the retreatment rate was 0%. Good outcomes (modified Rankin Scale score 0–2) were observed in 96.2% of patients overall and in all 156 patients with unruptured aneurysms. New visual field defects (hemianopsia or quadrantanopsia) were observed in 8 patients (3.8%), decreased visual acuity in 5 (2.4%), and monocular blindness in 9 (4.3%). Vision improved in 9 (52.9%) of the 17 patients with preoperative visual deficits.

CONCLUSIONS

The most important risk associated with clipping OphA aneurysms is a new visual deficit. Meticulous microsurgical technique is necessary during anterior clinoidectomy, aneurysm dissection, and clip application to optimize visual outcomes, and aggressive medical management postoperatively might potentially decrease the incidence of delayed visual deficits. As the results of endovascular therapy and specifically flow diverters become known, they warrant comparison with these surgical benchmarks to determine best practices.

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Jan-Karl Burkhardt, George F. Lasker, Ethan A. Winkler, Helen Kim, and Michael T. Lawton

OBJECTIVE

Few outcomes studies have been published on microsurgical resection of arteriovenous malformations (AVMs) in elderly patients, and most are limited by a small sample size and the heterogeneous application of treatment modalities. This study aimed to determine whether functional outcomes at last follow-up (LFU) in patients 60 years or older differed when stratified by age.

METHODS

Patients 60 years or older (n = 104) who had undergone microsurgical AVM resection (total, n = 72; 60–65 years, n = 35; and > 65 years, n = 37) or observation (n = 32) were identified from a prospective database. Age, sex, Spetzler-Martin (SM) grade, supplemented SM grade, clinical presentation, AVM location, AVM-associated aneurysms, and functional outcome measured using the modified Rankin Scale (mRS score 0–2 [favorable] vs mRS score > 2 [unfavorable]) at LFU were analyzed.

RESULTS

AVM patients undergoing microsurgical resection were younger, had lower AVM grades, and were more likely to present with rupture. Overall outcome in the surgical group was favorable in 71% of the patients and was statistically significantly better in patients 60–65 years old (p = 0.039). In patients older than 65 years, outcome was dependent on SM grade and level of preexisting functional dependence. Patients with supplemented SM grades of greater than 6 points had favorable outcomes that were age dependent (p = 0.029). This difference was not observed in patients with lower supplemented SM grades or in those with low or high preoperative SM grades (SM grade ≤ 2 and grade ≥ 4, respectively).

CONCLUSIONS

This study demonstrates that favorable outcomes can be achieved with microsurgical resection of AVMs in elderly patients, with careful patient selection. Outcomes in more elderly patients (> 65 years of age) are more dependent on preoperative SM and supplemented SM grading than those in younger cohorts.

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Gyang Markus Bot, Jan-Karl Burkhardt, Nalin Gupta, and Michael T. Lawton

OBJECTIVE

Revascularization is indicated in the management of moyamoya disease (MMD), with options that include direct and indirect techniques. Indirect bypass is popular in young children because the diminutive caliber of donors and recipients makes direct bypass difficult. The authors reviewed a series of patients treated with direct superficial temporal artery (STA)–to–middle cerebral artery (MCA) bypass in combination with encephalomyosynangiosis (EMS) in children 3 years or younger to demonstrate feasibility and safety.

METHODS

A retrospective review of all surgeries for MMD over a 19-year period identified 11 procedures in 6 patients. Surgical results, angiographic outcomes, and clinical outcomes were analyzed.

RESULTS

Patients had a mean age of 22.4 months. The symptomatic hemisphere was revascularized first, and the contralateral hemisphere was revascularized on average 2.8 months later in 5 patients. All direct bypasses were patent postoperatively and remained patent at late follow-up (mean 4.1 years), with both STA and MCA diameters increasing significantly (n = 5, p < 0.03). At last follow-up (mean follow-up duration, 5.0 years), favorable outcomes (modified Rankin Scale scores 0–2) were observed in 5 of the 6 patients (83%), with 1 dependent patient remaining unchanged postoperatively.

CONCLUSIONS

Direct STA-MCA bypass in combination with EMS for MMD is feasible and safe in patients 3 years or younger, based on favorable clinical and radiological outcomes in this patient cohort. Direct bypass should be considered when immediate revascularization is needed, without the biological delay associated with indirect bypass.

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R. Michael Scott and Edward R. Smith