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Joshua S. Catapano, Mohamed A. Labib, Visish M. Srinivasan, Candice L. Nguyen, Kavelin Rumalla, Redi Rahmani, Tyler S. Cole, Jacob F. Baranoski, Caleb Rutledge, Kristina M. Chapple, Andrew F. Ducruet, Felipe C. Albuquerque, Joseph M. Zabramski, and Michael T. Lawton

OBJECTIVE

The Barrow Ruptured Aneurysm Trial (BRAT) was a single-center trial that compared endovascular coiling to microsurgical clipping in patients treated for aneurysmal subarachnoid hemorrhage (aSAH). However, because patients in the BRAT were treated more than 15 years ago, and because there have been advances since then—particularly in endovascular techniques—the relevance of the BRAT today remains controversial. Some hypothesize that these technical advances may reduce retreatment rates for endovascular intervention. In this study, the authors analyzed data for the post-BRAT (PBRAT) era to compare microsurgical clipping with endovascular embolization (coiling and flow diverters) in the two time periods and to examine how the results of the original BRAT have influenced the practice of neurosurgeons at the study institution.

METHODS

In this retrospective cohort study, the authors evaluated patients with saccular aSAHs who were treated at a single quaternary center from August 1, 2007, to July 31, 2019. The saccular aSAH diagnoses were confirmed by cerebrovascular experts. Patients were separated into two cohorts for comparison on the basis of having undergone microsurgery or endovascular intervention. The primary outcome analyzed for comparison was poor neurological outcome, defined as a modified Rankin Scale (mRS) score > 2. The secondary outcomes that were compared included retreatment rates for both therapies.

RESULTS

Of the 1014 patients with aSAH during the study period, 798 (79%) were confirmed to have saccular aneurysms. Neurological outcomes at ≥ 1-year follow-up did not differ between patients treated with microsurgery (n = 451) and those who received endovascular (n = 347) treatment (p = 0.51). The number of retreatments was significantly higher among patients treated endovascularly (32/347, 9%) than among patients treated microsurgically (6/451, 1%) (p < 0.001). The retreatment rate after endovascular treatment was lower in the PBRAT era (9%) than in the BRAT (18%).

CONCLUSIONS

Similar to results from the BRAT, results from the PBRAT era showed equivalent neurological outcomes and increased rates of retreatment among patients undergoing endovascular embolization compared with those undergoing microsurgery. However, the rate of retreatment after endovascular intervention was much lower in the PBRAT era than in the BRAT.

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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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Joseph H. Garcia, Ramin A. Morshed, Ethan A. Winkler, Yi Li, Christine K. Fox, Heather J. Fullerton, Caleb Rutledge, Angad S. Beniwal, Michael T. Lawton, Adib A. Abla, Nalin Gupta, and Steven W. Hetts

OBJECTIVE

Moyamoya is a progressive arteriopathy that predisposes patients to stroke due to stenosis of the intracranial internal carotid arteries and their proximal branches. Despite the morbidity caused by this condition, the ability to accurately predict prognosis for individual patients remains challenging. The goal of this study was to develop a systematic scoring method based on parenchymal findings on preoperative brain MRI to predict long-term outcomes for surgically treated pediatric patients with moyamoya.

METHODS

A retrospective surgical cohort of pediatric patients (≤ 18 years of age at the time of the initial surgery) with moyamoya from a single center were studied. Radiological variables with existing correlations between outcomes in moyamoya or other vascular diseases were chosen to score preoperative MRI based on easily defined parenchymal findings that could be rapidly assessed and used to make a numeric score. Calculated scores were correlated with clinical outcome measures using the Pearson correlation coefficient and area under the receiver operating characteristic curve (AUROC).

RESULTS

A total of 35 children with moyamoya disease or moyamoya syndrome were included in the study, with a median follow-up time of 2.6 years from the time of surgery. The pediatric moyamoya MRI score (PMMS) consists of ischemic changes (0–2; 0 = none, 1 = focal, 2 = diffuse), encephalomalacia (0–2; 0 = none, 1 = focal, 2 = diffuse), and hemorrhage (0–1; 0 = not present, 1 = present). PMMSs were highly correlated with pediatric modified Rankin Scale scores at the last follow-up (r = 0.7, 95% CI 0.44–0.84; p < 0.001) as a six-point scale, and when dichotomized (AUROC = 0.85).

CONCLUSIONS

The PMMS was found to be a simple tool based on preoperative MRI data that could be quickly and easily calculated and correlated with disability. This scoring method may aid future development of predictive models of outcomes for children with moyamoya disease and moyamoya syndrome.

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Visish M. Srinivasan, Phiroz E. Tarapore, Stefan W. Koester, Joshua S. Catapano, Caleb Rutledge, Kunal P. Raygor, and Michael T. Lawton

OBJECTIVE

Rare arteriovenous malformations (AVMs) of the optic apparatus account for < 1% of all AVMs. The authors conducted a systematic review of the literature for cases of optic apparatus AVMs and present 4 cases from their institution. The literature is summarized to describe preoperative characteristics, surgical technique, and treatment outcomes for these lesions.

METHODS

A comprehensive search of the English-language literature was performed in accordance with established Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines to identify all published cases of AVM in the optic apparatus in the PubMed, Web of Science, and Cochrane databases. The authors also searched their prospective institutional database of vascular malformations for such cases. Data regarding the clinical and radiological presentation, visual acuity, visual fields, extent of resection, and postoperative outcomes were gathered.

RESULTS

Nine patients in the literature and 4 patients in the authors’ single-surgeon series who fit the inclusion criteria were identified. The median age at presentation was 29 years (range 8–39 years). Among these patients, 11 presented with visual disturbance, 9 with headache, and 1 with multiple prior subarachnoid hemorrhages; the AVM in 1 case was found incidentally. Four patients described prior symptoms of headache or visual disturbance consistent with sentinel events. Visual acuity was decreased from baseline in 10 patients, and 11 patients had visual field defects on formal visual field testing. The most common visual field defect was temporal hemianopia, found in one or both eyes in 7 patients. The optic chiasm was affected in 10 patients, the hypothalamus in 2 patients, the optic nerve (unilaterally) in 8 patients, and the optic tract in 2 patients. Six patients underwent gross-total resection; 6 patients underwent subtotal resection; and 1 patient underwent craniotomy, but no resection was attempted. Postoperatively, 9 of the patients had improved visual function, 1 had no change, and 3 had worse visual acuity. Eight patients demonstrated improved visual fields, 1 had no change, and 4 had narrowed fields.

CONCLUSIONS

AVMs of the optic apparatus are rare lesions. Although they reside in a highly eloquent region, surgical outcomes are generally good; the majority of patients will see improvement in their visual function postoperatively. Microsurgical technique is critical to the successful removal of these lesions, and preservation of function sometimes requires subtotal resection of the lesion.

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Sen Gao, Jeffrey Nelson, Shantel Weinsheimer, Ethan A. Winkler, Caleb Rutledge, Adib A. Abla, Nalin Gupta, Joseph T. Shieh, Daniel L. Cooke, Steven W. Hetts, Tarik Tihan, Christopher P. Hess, Nerissa Ko, Brian P. Walcott, Charles E. McCulloch, Michael T. Lawton, Hua Su, Ludmila Pawlikowska, and Helen Kim

OBJECTIVE

Sporadic brain arteriovenous malformation (BAVM) is a tangled vascular lesion characterized by direct artery-to-vein connections that can cause life-threatening intracerebral hemorrhage (ICH). Recently, somatic mutations in KRAS have been reported in sporadic BAVM, and mutations in other mitogen-activated protein kinase (MAPK) signaling pathway genes have been identified in other vascular malformations. The objectives of this study were to systematically evaluate somatic mutations in MAPK pathway genes in patients with sporadic BAVM lesions and to evaluate the association of somatic mutations with phenotypes of sporadic BAVM severity.

METHODS

The authors performed whole-exome sequencing on paired lesion and blood DNA samples from 14 patients with sporadic BAVM, and 295 genes in the MAPK signaling pathway were evaluated to identify genes with somatic mutations in multiple patients with BAVM. Digital droplet polymerase chain reaction was used to validate KRAS G12V and G12D mutations and to assay an additional 56 BAVM samples.

RESULTS

The authors identified a total of 24 candidate BAVM-associated somatic variants in 11 MAPK pathway genes. The previously identified KRAS G12V and G12D mutations were the only recurrent mutations. Overall, somatic KRAS G12V was present in 14.5% of BAVM lesions and G12D was present in 31.9%. The authors did not detect a significant association between the presence or allelic burden of KRAS mutation and three BAVM phenotypes: lesion size (maximum diameter), age at diagnosis, and age at ICH.

CONCLUSIONS

The authors confirmed the high prevalence of somatic KRAS mutations in sporadic BAVM lesions and identified several candidate somatic variants in other MAPK pathway genes. These somatic variants may contribute to understanding of the etiology of sporadic BAVM and the clinical characteristics of patients with this condition.