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Manuri Gunawardena, Jeffrey M. Rogers, Marcus A. Stoodley and Michael K. Morgan

OBJECTIVE

Previous trials rejected a role of extracranial-to-intracranial bypass surgery for managing symptomatic atheromatous disease. However, hemodynamic insufficiency may still be a rationale for surgery, provided the bypass can be performed with low morbidity and patency is robust.

METHODS

Consecutive patients undergoing bypass surgery for symptomatic non-moyamoya intracranial arterial stenosis or occlusion were retrospectively identified. The clinical course and surgical outcomes of the cohort were evaluated at 6 weeks, 6 months, and annually thereafter.

RESULTS

From 1992 to 2017, 112 patients underwent 127 bypasses. The angiographic abnormality was arterial occlusion in 80% and stenosis in 20%. Procedures were performed to prevent future stroke (76%) and stroke reversal (24%), with revascularization using an arterial pedicle graft in 80% and venous interposition graft (VIG) in 20%. A poor outcome (bypass occlusion, new stroke, new neurological deficit, or worsening neurological deficit) occurred in 8.9% of patients, with arterial pedicle grafts (odds ratio [OR] 0.15), bypass for prophylaxis against future stroke (OR 0.11), or anterior circulation bypass (OR 0.17) identified as protective factors. Over the first 8 years following surgery the 66 cases exhibiting all three of these characteristics had minimal risk of a poor outcome (95% confidence interval 0%–6.6%).

CONCLUSIONS

Prophylactic arterial pedicle bypass surgery for anterior circulation ischemia is associated with high graft patency and low stroke and surgical complication rates. Higher risks are associated with acute procedures, typically for posterior circulation pathology and requiring VIGs. A carefully selected subgroup of individuals with hemodynamic insufficiency and ischemic symptoms is likely to benefit from cerebral revascularization surgery.

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Fengping Zhu, Yi Qian, Bin Xu, Yuxiang Gu, Kaavya Karunanithi, Wei Zhu, Liang Chen, Ying Mao and Michael K. Morgan

OBJECTIVE

Although intracranial vessel remodeling has been observed in moyamoya disease, concerns remain regarding the effect of bypass surgery on hemodynamic changes within the internal carotid artery (ICA). The authors aimed to quantify the surgical effect of bypass surgery on bilateral ICAs in moyamoya disease and to estimate pressure drop (PD) along the length of the ICA to predict surgical outcomes.

METHODS

Records of patients who underwent bypass surgery for treatment of moyamoya disease and in whom flow rates were obtained pre- and postsurgery by quantitative MR angiography were retrospectively reviewed. Quantitative MR angiography and computational fluid dynamics were applied to measure morphological and hemodynamic changes during pre- and postbypass procedures. The results for vessel diameter, volumetric flow, PD, and mean wall shear stress along the length of the ICA were analyzed. Subgroup analysis was performed for the circle of Willis (CoW) configurations.

RESULTS

Twenty-three patients were included. The PD in ICAs on the surgical side (surgical ICAs) decreased by 21.18% (SD ± 30.1%) and increased by 11.75% (SD ± 28.6%) in ICAs on the nonsurgical side (contralateral ICAs) (p = 0.001). When the PD in contralateral ICAs was compared between patients with a complete or incomplete CoW, the authors found that the PDI in the former group decreased by 2.45% and increased by 20.88% in the latter (p = 0.05). Regression tests revealed that a greater postoperative decrease in PD corresponded to shrinking of ICAs (R2 = 0.22, p = 0.02).

CONCLUSIONS

PD may be used as a reliable biomechanical indicator for the assessment of surgical treatment outcomes. The vessel remodeling characteristics of contralateral ICA were related to CoW configurations.

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Michael K. Morgan, Markus K. Hermann Wiedmann, Marcus A. Stoodley and Gillian Z. Heller

OBJECTIVE

The purpose of this study was to adapt and apply the extended definition of favorable outcome established for Gamma Knife radiosurgery (GKRS) to surgery for brain arteriovenous malformations (bAVMs). The aim was to derive both an error around the point estimate and a model incorporating angioarchitectural features in order to facilitate comparison among different treatments.

METHODS

A prospective microsurgical cohort was analyzed. This cohort included patients undergoing embolization who did not proceed to microsurgery and patients denied surgery because of perceived risk of treatment. Data on bAVM residual and recurrence during long-term follow-up as well as complications of surgery and preoperative embolization were analyzed. Patients with Spetzler-Ponce Class C bAVMs were excluded because of extreme selection bias. First, patients with a favorable outcome were identified for both Class A and Class B lesions. Patients were considered to have a favorable outcome if they were free of bAVM recurrence or residual at last follow-up, with no complication of surgery or preoperative embolization, and a modified Rankin Scale score of more than 1 at 12 months after treatment. Patients who were denied surgery because of perceived risk, but would otherwise have been candidates for surgery, were included as not having a favorable outcome. Second, the authors analyzed favorable outcome from microsurgery by means of regression analysis, using as predictors characteristics previously identified to be associated with complications. Third, they created a prediction model of favorable outcome for microsurgery dependent upon angioarchitectural variables derived from the regression analysis.

RESULTS

From a cohort of 675 patients who were either treated or denied surgery because of perceived risk of surgery, 562 had Spetzler-Ponce Class A or B bAVMs and were included in the analysis. Logistic regression for favorable outcome found decreasing maximum diameter (continuous, OR 0.62, 95% CI 0.51–0.76), the absence of eloquent location (OR 0.23, 95% CI 0.12–0.43), and the absence of deep venous drainage (OR 0.19, 95% CI 0.10–0.36) to be significant predictors of favorable outcome. These variables are in agreement with previous analyses of microsurgery leading to complications, and the findings support the use of favorable outcome for microsurgery. The model developed for angioarchitectural features predicts a range of favorable outcome at 8 years following microsurgery for Class A bAVMs to be 88%–99%. The same model for Class B bAVMs predicts a range of favorable outcome of 62%–90%.

CONCLUSIONS

Favorable outcome, derived from GKRS, can be successfully used for microsurgical cohort series to assist in treatment recommendations. A favorable outcome can be achieved by microsurgery in at least 90% of cases at 8 years following microsurgery for patients with bAVMs smaller than 2.5 cm in maximum diameter and, in the absence of either deep venous drainage or eloquent location, patients with Spetzler-Ponce Class A bAVMs of all diameters. For patients with Class B bAVMs, this rate of favorable outcome can only be approached for lesions with a maximum diameter just above 6 cm or smaller and without deep venous drainage or eloquent location.

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Nirav J. Patel and Michael K. Morgan

This video shows the surgical repair of a 2.3 cm ICA aneurysm found in a 58-year-old woman, who presented for right eye vision changes. The patient underwent a right modified orbitozygomatic craniotomy and saphenous vein bypass from the common carotid to the temporal M2. The aneurysm was then opened and repaired. However, since the anterior choroidal artery was not filling, a salvage bypass between the anterior choroidal and the PCOM was done. Both bypasses were patent and the patient has done well with a mRS of 1 for vision symptoms.

The video can be found here: http://youtu.be/ciMyzfXgo8I.

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Mohamed Samy Elhammady and Roberto C. Heros

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Michael K. Morgan, Nazih N. Assaad and Andrew S. Davidson

Object

In this paper the authors' goal was to evaluate whether resident neurosurgeons participating in entry-level aneurysm surgery have a negative impact on patient outcomes.

Methods

The authors searched the database for entry-level aneurysm surgeries (that is, those ≤ 10 mm and located in the internal carotid artery [beyond the paraclinoid segment] and middle cerebral artery) performed in 1991 through 2005. The presence or absence of an advanced resident (in his/her last 3 years of residency) was noted. The analysis was examined in 3-year quintiles.

A total of 355 cases (196 with resident participation and 159 without) were evaluated. Permanent adverse outcomes were seen in 11 patients (3.1% of the total study population), all due to branch artery occlusion. The incidence of permanent adverse outcomes in the first 3 years was 10.7% and 2.4% thereafter. This difference was statistically significant (p = 0.015). There was no difference in the incidence of adverse outcomes when comparing surgery performed with and without participation of an advanced resident.

Conclusions

In this study the authors have demonstrated a learning curve in this series of patients. This study also suggests that involving residents in the repair of small unruptured aneurysms will not compromise patient care. In addition, patients can be informed that the team approach to their surgery is at least as good as having the experienced surgeon performing all aspects of the surgery.

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M. Sean Grady

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Brendan Steinfort, Perry P. Ng, Kenneth Faulder, Timothy Harrington, Verity Grinnell, William Sorby and Michael K. Morgan

Object

Symptomatic intracranial vertebral and basilar artery atherosclerotic stenoses carry a high risk of stroke and permanent disability if refractory to maximal medical therapy. The authors conducted a study to determine the technical feasibility and midterm clinical and angiographic outcomes in patients in whom paclitaxel-eluting stents were placed for the treatment of symptomatic intracranial posterior circulation stenoses.

Methods

A retrospective review of medical records and imaging studies was performed for 13 consecutive patients in whom paclitaxel-coated stents were used to treat symptomatic posterior circulation intracranial stenoses between 2002 and 2005. Clinical follow-up data were supplemented by telephone interviews.

The technical success rate for stent placement was 100%. One patient (8%) suffered a periprocedural stroke. Twelve patients (92%) underwent clinical follow up for a minimum of 3 months postsurgery, and 11 (92%) of these patients remained asymptomatic after a mean period of 10.9 months. Nine patients (69%) underwent catheter angiographic follow up, and no patient had significant in-stent recurrence of stenosis after a mean period of 5.4 months.

Conclusions

Treatment of intracranial posterior circulation stenoses with drug-eluting stents is technically feasible, and the rate of clinically significant periprocedural complications is low. Rates of stenosis recurrence are reduced compared with those of bare-metal stents in the midterm. Midterm clinical outcome is excellent; no symptom recurrence was observed in this patient cohort.

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Jian Tu, Marcus A. Stoodley, Michael K. Morgan and Kingsley P. Storer

Object. Ultrastructural characteristics of hemorrhagic, nonhemorrhagic, primary, and recurrent central nervous system cavernous malformations (CMs) were examined in an attempt to clarify their pathological mechanisms.

Methods. Thirteen specimens (nine from samples of CMs and four from healthy control tissue) were processed for ultrastructural study immediately after surgical or postmortem removal, by fixation in glutaraldehyde/formalin and postfixation in OsO4. Transmission electron microscopy was used to examine the vascular walls, endothelium, subendothelium, and cytoplasmic organelles.

The vascular walls in CMs demonstrated abnormal ultrastructure with no basement membranes and astrocytic foot processes. Pericytes were rarely seen. Single-layer lining endothelial cells showed fenestrated luminal surfaces. Large gaps were observed at intercellular junctions between endothelial cells, and large vesicles with extremely thin plasma membranes bordering the lumen were common in the lesions that had previously hemorrhaged. Endothelial cells of recurrent CMs had more Weibel—Palade bodies, filopodia, cytoplasmic processes, micropinocytotic vesicles, and filaments than those in primary lesions and normal control tissues.

Conclusions. The absence of the blood–brain barrier, normal supporting wall structure, and large vesicles bordering the lumen of CM vessels may explain leakage of red blood cells into surrounding brain in the absence of major hemorrhage. Proliferation of residual abnormal endothelial cells may contribute to the recurrence of surgically removed CMs.

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Tor Ingebrigtsen, Michael K. Morgan, Ken Faulder, Linda Ingebrigtsen, Trygve Sparr and Henrik Schirmer

Object. The angles of arterial bifurcations are governed by principles of work minimization (optimality principle). This determines the relationship between the angle of a bifurcation and the radii of the vessels. Nevertheless, the model is predicated on an absence of significant communication between these branches. The circle of Willis changes this relationship because the vessels proximal to the ring of vessels have additional factors that determine work minimization compared with more distal branches. This must have an impact on understanding of the relationship between shear stress and aneurysm formation. The authors hypothesized that normal bifurcations of cerebral arteries beyond the circle of Willis would follow optimality principles of minimum work and that the presence of aneurysms would be associated with deviations from optimum bifurcation geometry. Nevertheless, the vessels participating in (or immediately proximal to) the circle of Willis may not follow the geometric model as it is generally applied and this must also be investigated.

Methods. One hundred seven bifurcations of the middle cerebral artery (MCA), distal internal carotid artery (ICA), and basilar artery (BA) were studied in 55 patients. The authors analyzed three-dimensional reconstructions of digital subtraction angiography images with respect to vessel radii and bifurcation angles. The junction exponent (that is, a calculated measure of the division of flow at the bifurcation) and the difference between the predicted optimal and observed branch angles were used as measures of deviation from the geometry thought best to minimize work.

The mean junction exponent for MCA bifurcations was 2.9 ± 1.2 (mean ± standard deviation [SD]), which is close to the theoretical optimum of 3, but it was significantly smaller (p < 0.001; 1.7 ± 0.8, mean ± SD) for distal ICA bifurcations. In a multilevel multivariate logistic regression analysis, only the observed branch angles were significant independent predictors for the presence of an aneurysm. The odds ratio (OR) (95% confidence interval) for the presence of an aneurysm was 3.46 (1.02–11.74) between the lowest and highest tertile of the observed angle between the parent vessel and the largest branch. The corresponding OR for the smallest branch was 48.06 (9.7–238.2).

Conclusions. The bifurcation beyond the circle of Willis (that is, the MCA) closely approximated optimality principles, whereas the bifurcations within the circle of Willis (that is, the distal ICA and BA) did not. This indicates that the confluence of hemodynamic forces plays an important role in the distribution of work at bifurcations within the circle of Willis. In addition, the observed branch angles were predictors for the presence of aneurysms.