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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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Marco Cenzato, Davide Colistra, Giorgia Iacopino, Christian Raftopoulos, Ulrich Sure, Marcos Tatagiba, Robert F. Spetzler, Alexander N. Konovalov, Andriy Smolanka, Volodymir Smolanka, Roberto Stefini, Carlo Bortolotti, Paolo Ferroli, Giampietro Pinna, Angelo Franzini, Philipp Dammann, Georgios Naros, Davide Boeris, Paolo Mantovani, Domenico Lizio, Mariangela Piano, and Enrica Fava

OBJECTIVE

In this paper, the authors aimed to illustrate how Holmes tremor (HT) can occur as a delayed complication after brainstem cavernoma resection despite strict adherence to the safe entry zones (SEZs).

METHODS

After operating on 2 patients with brainstem cavernoma at the Great Metropolitan Hospital Niguarda in Milan and noticing a similar pathological pattern postoperatively, the authors asked 10 different neurosurgery centers around the world to identify similar cases, and a total of 20 were gathered from among 1274 cases of brainstem cavernomas. They evaluated the tremor, cavernoma location, surgical approach, and SEZ for every case. For the 2 cases at their center, they also performed electromyographic and accelerometric recordings of the tremor and evaluated the post-operative tractographic representation of the neuronal pathways involved in the tremorigenesis. After gathering data on all 1274 brainstem cavernomas, they performed a statistical analysis to determine if the location of the cavernoma is a potential predicting factor for the onset of HT.

RESULTS

From the analysis of all 20 cases with HT, it emerged that this highly debilitating tremor can occur as a delayed complication in patients whose postoperative clinical course has been excellent and in whom surgical access has strictly adhered to the SEZs. Three of the patients were subsequently effectively treated with deep brain stimulation (DBS), which resulted in complete or almost complete tremor regression. From the statistical analysis of all 1274 brainstem cavernomas, it was determined that a cavernoma location in the midbrain was significantly associated with the onset of HT (p < 0.0005).

CONCLUSIONS

Despite strict adherence to SEZs, the use of intraoperative neurophysiological monitoring, and the immediate success of a resective surgery, HT, a severe neurological disorder, can occur as a delayed complication after resection of brainstem cavernomas. A cavernoma location in the midbrain is a significant predictive factor for the onset of HT. Further anatomical and neurophysiological studies will be necessary to find clues to prevent this complication.

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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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Tyler S. Cole and Robert F. Spetzler

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Nícollas Nunes Rabelo, Manoel Jacobsen Teixeira, Robert F. Spetzler, and Eberval Gadelha Figueiredo

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Nícollas Nunes Rabelo, Manoel Jacobsen Teixeira, Robert F. Spetzler, and Eberval Gadelha Figueiredo

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Tim E. Darsaut and Jean Raymond