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Joshua S. Catapano, Stefan W. Koester, Visish M. Srinivasan, Mohamed A. Labib, Neil Majmundar, Candice L. Nguyen, Caleb Rutledge, Tyler S. Cole, Jacob F. Baranoski, Andrew F. Ducruet, Felipe C. Albuquerque, Robert F. Spetzler, and Michael T. Lawton

OBJECTIVE

Ophthalmic artery (OA) aneurysms are surgically challenging lesions that are now mostly treated using endovascular procedures. However, in specialized tertiary care centers with experienced neurosurgeons, controversy remains regarding the optimal treatment of these lesions. This study used propensity adjustment to compare microsurgical and endovascular treatment of unruptured OA aneurysms in experienced tertiary and quaternary settings.

METHODS

The authors retrospectively reviewed the medical records of all patients who underwent microsurgical treatment of an unruptured OA aneurysm at the University of California, San Francisco, from 1997 to 2017 and either microsurgical or endovascular treatment at Barrow Neurological Institute from 2011 to 2019. Patients were categorized into two cohorts for comparison: those who underwent open microsurgical clipping, and those who underwent endovascular flow diversion or coil embolization. Outcomes included neurological or visual outcomes, residual or recurrent aneurysms, retreatment, and severe complications.

RESULTS

A total of 345 procedures were analyzed: 247 open microsurgical clipping procedures (72%) and 98 endovascular procedures (28%). Of the 98 endovascular procedures, 16 (16%) were treated with primary coil embolization and 82 (84%) with flow diversion. After propensity adjustment, microsurgical treatment was associated with higher odds of a visual deficit (OR 8.5, 95% CI 1.1–64.9, p = 0.04) but lower odds of residual aneurysm (OR 0.06, 95% CI 0.01–0.28, p < 0.001) or retreatment (OR 0.12, 95% CI 0.02–0.58, p = 0.008) than endovascular therapy. No difference was found between the two cohorts with regard to worse modified Rankin Scale score, modified Rankin Scale score greater than 2, or severe complications.

CONCLUSIONS

Compared with endovascular therapy, microsurgical clipping of unruptured OA aneurysms is associated with a higher rate of visual deficits but a lower rate of residual and recurrent aneurysms. In centers experienced with both open microsurgical and endovascular treatment of these lesions, the treatment choice should be based on patient preference and aneurysm morphology.

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Joshua S. Catapano, Caleb Rutledge, Kavelin Rumalla, Kunal P. Raygor, Visish M. Srinivasan, Stefan W. Koester, Anna R. Kimata, Kevin L. Ma, Mohamed A. Labib, Robert F. Spetzler, and Michael T. Lawton

OBJECTIVE

The brainstem cavernous malformation (BSCM) grading system predicts neurological outcomes associated with microsurgical resection and assists neurosurgeons in selecting patients for treatment. The predictive accuracy of the BSCM grading system should be validated in a large cohort from high-volume centers to generalize its use.

METHODS

An external validation cohort comprised patients with a BSCM resected by the senior author (M.T.L.) since the publication of the BSCM grading system and those resected by another neurosurgeon (R.F.S.) over a 16-year period. Size, crossing the axial midpoint, the presence of a developmental venous anomaly, patient age, and timing of last hemorrhage were used to assign BSCM grades from 0 to VII. Poor neurological outcomes were recorded as modified Rankin Scale scores > 2 at last follow-up examination.

RESULTS

A total of 277 patients were included in the study. The average BSCM grade was 3.9, and the majority of BSCMs (181 patients, 65%) were intermediate grade (grades III–V). Outcomes were predicted by BSCM grade, with good outcomes observed in 47 of 54 patients (87%) with low-grade BSCMs, in 135 of 181 patients (75%) with intermediate-grade BSCMs, and in 21 of 42 patients (50%) with high-grade BSCMs. Conversely, proportions of patients with neurological deterioration increased with increasing BSCM grade, with worsening observed in 2 of 54 patients (4%) with low-grade BSCMs, in 29 of 181 patients (16%) with intermediate-grade BSCMs, and in 17 of 42 patients (40%) with high-grade BSCMs. In the chi-square analysis, high-grade BSCMs were associated with increased odds of neurological worsening compared to low- and intermediate-grade BSCMs (OR 5.0, 95% CI 2.4–10.4; p < 0.001). The receiver operating characteristic analysis demonstrated acceptable discrimination for predicting unfavorable functional outcomes (modified Rankin Scale score > 2) with an area under the curve of 0.74 (95% CI 0.68–0.80; p < 0.001).

CONCLUSIONS

This study validates the BSCM grading system in a large cohort of patients from two high-volume surgeons. BSCM grade predicted neurological outcomes with accuracy comparable to that of other grading systems in widespread use. The BSCM grading system establishes categories of low-, intermediate-, and high-grade BSCMs and a boundary or cutoff for surgery at BSCM grade V. BSCM grading guides the analysis of a particular patient’s condition, but treatment recommendations must be individualized, and neurosurgeons must calibrate BSCM grading to their own outcome results, unique abilities, and practices.

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Philipp Dammann, Adib A. Abla, Rustam Al-Shahi Salman, Hugo Andrade-Barazarte, Vladimir Benes, Marco Cenzato, E. Sander Connolly Jr., Jan F. Cornelius, William T. Couldwell, Rafael G. Sola, Santiago Gomez-Paz, Erik Hauck, Juha Hernesniemi, Juri Kivelev, Giuseppe Lanzino, R. Loch Macdonald, Jacques J. Morcos, Christopher S. Ogilvy, Hans-Jakob Steiger, Gary K. Steinberg, Alejandro N. Santos, Laurèl Rauschenbach, Marvin Darkwah Oppong, Börge Schmidt, Robert F. Spetzler, Karl Schaller, Michael T. Lawton, and Ulrich Sure

OBJECTIVE

Indication for surgery in brainstem cavernous malformations (BSCMs) is based on many case series, few comparative studies, and no randomized controlled trials. The objective of this study was to seek consensus about surgical management aspects of BSCM.

METHODS

A total of 29 experts were invited to participate in a multistep Delphi consensus process on the surgical treatment of BSCM.

RESULTS

Twenty-two (76%) of 29 experts participated in the consensus. Qualitative analysis (content analysis) of an initial open-ended question survey resulted in 99 statements regarding surgical treatment of BSCM. By using a multistep survey with 100% participation in each round, consensus was reached on 52 (53%) of 99 statements. These were grouped into 4 categories: 1) definitions and reporting standards (7/14, 50%); 2) general and patient-related aspects (11/16, 69%); 3) anatomical-, timing of surgery–, and BSCM-related aspects (22/37, 59%); and 4) clinical situation–based decision-making (12/32, 38%). Among other things, a consensus was reached for surgical timing, handling of associated developmental venous anomalies, handling of postoperative BSCM remnants, assessment of specific anatomical BSCM localizations, and treatment decisions in typical clinical BSCM scenarios.

CONCLUSIONS

A summary of typical clinical scenarios and a catalog of various BSCM- and patient-related aspects that influence the surgical treatment decision have been defined, rated, and interpreted.

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Joshua S. Catapano, Fabio A. Frisoli, Candice L. Nguyen, Mohamed A. Labib, Tyler S. Cole, Jacob F. Baranoski, Helen Kim, Robert F. Spetzler, and Michael T. Lawton

OBJECTIVE

Supplemented Spetzler-Martin grading (Supp-SM), which is the combination of Spetzler-Martin and Lawton-Young grades, was validated as being more accurate than stand-alone Spetzler-Martin grading, but an operability cutoff was not established. In this study, the authors surgically treated intermediate-grade AVMs to provide prognostic factors for neurological outcomes and to define AVMs at the boundary of operability.

METHODS

Surgically treated Supp-SM intermediate-grade (5, 6, and 7) AVMs were analyzed from 2011 to 2018 at two medical centers. Worsened neurological outcomes were defined as increased modified Rankin Scale (mRS) scores on postoperative examinations. A second analysis of 2000–2011 data for Supp-SM grade 6 and 7 AVMs was performed to determine the subtypes with improved or unchanged outcomes. Patients were separated into three groups based on nidus size (S1: < 3 cm, S2: 3–6 cm, S3: > 6 cm) and age (A1: < 20 years, A2: 20–40 years, A3: > 40 years), followed by any combination of the combined supplemented grade: low risk (S1A1, S1A2, S2A1), intermediate risk (S2A2, S1A3, S3A1, or high risk (S3A3, S3A2, S2A3).

RESULTS

Two hundred forty-six patients had intermediate Supp-SM grade AVMs. Of these patients, 102 had Supp-SM grade 5 (41.5%), 99 had Supp-SM grade 6 (40.2%), and 45 had Supp-SM grade 7 (18.3%). Significant differences in the proportions of patients with worse mRS scores at follow-up were found between the groups, with 24.5% (25/102) of patients in Supp-SM grade 5, 29.3% (29/99) in Supp-SM grade 6, and 57.8% (26/45) in Supp-SM grade 7 (p < 0.001). Patients with Supp-SM grade 7 AVMs had significantly increased odds of worse postoperative mRS scores (p < 0.001; OR 3.7, 95% CI 1.9–7.3). In the expanded cohort of 349 Supp-SM grade 6 AVM patients, a significantly higher proportion of older patients with larger Supp-SM grade 6 AVMs (grade 6+, 38.6%) had neurological deterioration than the others with Supp-SM grade 6 AVMs (22.9%, p = 0.02). Conversely, in an expanded cohort of 197 Supp-SM grade 7 AVM patients, a significantly lower proportion of younger patients with smaller Supp-SM grade 7 AVMs (grade 7–, 19%) had neurological deterioration than the others with Supp-SM grade 7 AVMs (44.9%, p = 0.01).

CONCLUSIONS

Patients with Supp-SM grade 7 AVMs are at increased risk of worse postoperative neurological outcomes, making Supp-SM grade 6 an appropriate operability cutoff. However, young patients with small niduses in the low-risk Supp-SM grade 7 group (grade 7−) have favorable postoperative outcomes. Outcomes in Supp-SM grade 7 patients did not improve with surgeon experience, indicating that the operability boundary is a hard limit reflecting the complexity of high-grade AVMs.

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Jan-Karl Burkhardt, Ethan A. Winkler, Joshua S. Catapano, Robert F. Spetzler, and Michael T. Lawton

OBJECTIVE

Studies of resection of brain arteriovenous malformations (AVMs) in the elderly population are scarce. This study examined factors influencing patient selection and surgical outcome among elderly patients.

METHODS

Patients 65 years of age and older who underwent resection of an unruptured or ruptured brain AVM treated by two surgeons at two centers were identified. Patient demographic characteristics, AVM characteristics, clinical presentation, and outcomes measured using the modified Rankin Scale (mRS) were analyzed. For subgroup analyses, patients were dichotomized into two age groups (group 1, 65–69 years old; group 2, ≥ 70 years old).

RESULTS

Overall, 112 patients were included in this study (group 1, n = 61; group 2, n = 51). Most of the patients presented with hemorrhage (71%), a small nidus (< 3 cm, 79%), and a low Spetzler-Martin (SM) grade (grade I or II, 63%) and were favorable surgical candidates according to the supplemented SM grade (supplemented SM grade < 7, 79%). A smaller AVM nidus was statistically significantly more likely to be present in patients with infratentorial AVMs (p = 0.006) and with a compact AVM nidus structure (p = 0.02). A larger AVM nidus was more likely to be treated with preoperative embolization (p < 0.001). Overall outcome was favorable (mRS scores 0–3) in 71% of the patients and was statistically independent from age group or AVM grading. Patients with ruptured AVMs at presentation had significantly better preoperative mRS scores (p < 0.001) and more favorable mRS scores at the last follow-up (p = 0.04) than patients with unruptured AVMs.

CONCLUSIONS

Outcomes were favorable after AVM resection in both groups of patients. Elderly patients with brain AVMs treated microsurgically were notable for small nidus size, AVM rupture, and low SM grades. Microsurgical resection is an important treatment modality for elderly patients with AVMs, and supplemented SM grading is a useful tool for the selection of patients who are most likely to achieve good neurological outcomes after resection.

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Peyton L. Nisson, Salman A. Fard, Christina M. Walter, Cameron M. Johnstone, Michael A. Mooney, Ali Tayebi Meybodi, Michael Lang, Helen Kim, Heidi Jahnke, Denise J. Roe, Travis M. Dumont, G. Michael Lemole Jr., Robert F. Spetzler, and Michael T. Lawton

OBJECTIVE

The objective of this study was to evaluate the existing Spetzler-Martin (SM), Spetzler-Ponce (SP), and Lawton-Young (LY) grading systems for cerebellar arteriovenous malformations (AVMs) and to propose a new grading system to estimate the risks associated with these lesions.

METHODS

Data for patients with cerebellar AVMs treated microsurgically in two tertiary medical centers were retrospectively reviewed. Data from patients at institution 1 were collected from September 1999 to February 2013, and at institution 2 from October 2008 to October 2015. Patient outcomes were classified as favorable (modified Rankin Scale [mRS] score 0–2) or poor (mRS score 3–6) at the time of discharge. Using chi-square and logistic regression analysis, variables associated with poor outcomes were assigned risk points to design the proposed grading system. The proposed system included neurological status prior to treatment (poor, +2 points), emergency surgery (+1 point), age > 60 years (+1 point), and deep venous drainage (deep, +1 point). Risk point totals of 0–1 comprised grade 1, 2–3 grade 2, and 4–5 grade 3.

RESULTS

A total of 125 cerebellar AVMs of 1328 brain AVMs were reviewed in 125 patients, 120 of which were treated microsurgically and included in the study. With our proposed grading system, we found poor outcomes differed significantly between each grade (p < 0.001), while with the SM, SP, and LY grading systems they did not (p = 0.22, p = 0.25, and p = 1, respectively). Logistic regression revealed grade 2 had 3.3 times the risk of experiencing a poor outcome (p = 0.008), while grade 3 had 9.9 times the risk (p < 0.001). The proposed grading system demonstrated a superior level of predictive accuracy (area under the receiver operating characteristic curve [AUROC] of 0.72) compared with the SM, SP, and LY grading systems (AUROC of 0.61, 0.57, and 0.51, respectively).

CONCLUSIONS

The authors propose a novel grading system for cerebellar AVMs based on emergency surgery, venous drainage, preoperative neurological status, and age that provides a superior prognostication power than the formerly proposed SM, SP, and LY grading systems. This grading system is clinically predictive of patient outcomes and can be used to better guide vascular neurosurgeons in clinical decision-making.

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M. Yashar S. Kalani, Michael T. Lawton, and Robert F. Spetzler

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Michael A. Mooney, Elias D. Simon, Scott Brigeman, Peter Nakaji, Joseph M. Zabramski, Michael T. Lawton, and Robert F. Spetzler

OBJECTIVE

A direct comparison of endovascular versus microsurgical treatment of ruptured middle cerebral artery (MCA) aneurysms in randomized trials is lacking. As endovascular treatment strategies continue to evolve, the number of reports of endovascular treatment of these lesions is increasing. Herein, the authors report a detailed post hoc analysis of ruptured MCA aneurysms treated by microsurgical clipping from the Barrow Ruptured Aneurysm Trial (BRAT).

METHODS

The cases of patients enrolled in the BRAT who underwent microsurgical clipping for a ruptured MCA aneurysm were reviewed. Characteristics of patients and their clinical outcomes and long-term angiographic results were analyzed.

RESULTS

Fifty patients underwent microsurgical clipping of a ruptured MCA aneurysm in the BRAT, including 21 who crossed over from the endovascular treatment arm. Four patients with nonsaccular (e.g., dissecting, fusiform, or blister) aneurysms were excluded, leaving 46 patients for analysis. Most (n = 32; 70%) patients presented with a Hunt and Hess grade II or III subarachnoid hemorrhage, with a high prevalence of intraparenchymal blood (n = 23; 50%), intraventricular blood (n = 21; 46%), or both. At the last follow-up (up to 6 years after treatment), clinical outcomes were good (modified Rankin Scale score 0–2) in 70% (n = 19) of 27 Hunt and Hess grades I–III patients and in 36% (n = 4) of 11 Hunt and Hess grade IV or V patients. There were no instances of rebleeding after the surgical clipping of aneurysms in this series at the time of last clinical follow-up.

CONCLUSIONS

Microsurgical clipping of ruptured MCA aneurysms has several advantages over endovascular treatment, including durability over time. The authors report detailed outcome data of patients with ruptured MCA aneurysms who underwent microsurgical clipping as part of a prospective, randomized trial. These results should be used for comparison with future endovascular and surgical series to ensure that the best results are being achieved for patients with ruptured MCA aneurysms.

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Jonathan J. Russin, Robert F. Spetzler, Steven Giannotta, Fredric B. Meyer, Michael T. Lawton, and Aaron A. Cohen-Gadol

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Carlos A. David, A. Giancarlo Vishteh, Robert F. Spetzler, Michael Lemole, Michael T. Lawton, and Shahram Partovi

Object. This study was undertaken to evaluate the long-term angiographic outcome of surgically treated aneurysms, which is unknown. Specifically, the incidence of recurrent aneurysms, the fate of residual necks, and the de novo formation of aneurysms were evaluated.

Methods. One hundred two patients (80 females and 22 males; mean age 49 years; range 12–78 years) harboring a total of 167 aneurysms underwent late follow-up angiography; 160 aneurysms were surgically treated. Late angiographic follow-up review was obtained at a mean of 4.4 ± 1.6 years postsurgery (range 2.6–9.7 years). Late follow-up angiography revealed two recurrent aneurysms (1.5%) of 135 clipped aneurysms without residua. Of 12 aneurysms with known residua, there were eight “dog-ear” residua, of which two (25%) enlarged. One hemorrhage was noted, yielding a hemorrhage risk of 1.9% per year. A second subgroup with broad-based residua revealed dramatic regrowth in three of four cases. Eight de novo aneurysms were found in six patients, for an annual risk of 1.8% per year. A history of multiple aneurysms was associated with de novo aneurysm formation (p = 0.049, chi-square analysis).

Conclusions. This study confirms the long-term efficacy of aneurysm clip ligation. In addition, the authors found there is a small but significant risk of de novo aneurysm formation, particularly in patients with multiple aneurysms. Most residual aneurysm rests appear to remain stable, although a subset may enlarge or rupture. These findings support the rationale for late angiographic follow-up review in patients with aneurysms.