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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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Justin R. Mascitelli, Michael T. Lawton, Benjamin K. Hendricks, Trevor A. Hardigan, James S. Yoon, Kurt A. Yaeger, Christopher P. Kellner, Reade A. De Leacy, Johanna T. Fifi, Joshua B. Bederson, Felipe C. Albuquerque, Andrew F. Ducruet, Lee A. Birnbaum, Jean Louis R. Caron, Pavel Rodriguez, and J Mocco

OBJECTIVE

Randomized controlled trials have demonstrated the superiority of endovascular therapy (EVT) compared to microsurgery (MS) for ruptured aneurysms suitable for treatment or when therapy is broadly offered to all presenting aneurysms; however, wide neck aneurysms (WNAs) are a challenging subset that require more advanced techniques and warrant further investigation. Herein, the authors sought to investigate a prospective, multicenter WNA registry using rigorous outcome assessments and compare EVT and MS using propensity score analysis (PSA).

METHODS

Untreated, ruptured, saccular WNAs were included in the analysis. A WNA was defined as having a neck ≥ 4 mm or a dome/neck ratio (DNR) < 2. The primary outcome was the modified Rankin Scale (mRS) score at 1 year posttreatment, as assessed by blinded research nurses (good outcome: mRS scores 0–2) and compared using PSA.

RESULTS

The analysis included 87 ruptured aneurysms: 55 in the EVT cohort and 32 in the MS cohort. Demographics were similar in the two cohorts, including Hunt and Hess grade (p = 0.144) and modified Fisher grade (p = 0.475). WNA type inclusion criteria were similar in the two cohorts, with the most common type having a DNR < 2 (EVT 60.0% vs MS 62.5%). More anterior communicating artery aneurysms (27.3% vs 18.8%) and posterior circulation aneurysms (18.2% vs 0.0%) were treated with EVT, whereas more middle cerebral artery aneurysms were treated with MS (34.4% vs 18.2%, p = 0.025). Within the EVT cohort, 43.6% underwent stand-alone coiling, 50.9% balloon-assisted coiling, 3.6% stent-assisted coiling, and 1.8% flow diversion. The 1-year mRS score was assessed in 81 patients (93.1%), and the primary outcome demonstrated no increased risk for a poor outcome with MS compared to EVT (OR 0.43, 95% CI 0.13–1.45, p = 0.177). The durability of MS was higher, as evidenced by retreatment rates of 12.7% and 0% for EVT and MS, respectively (p = 0.04).

CONCLUSIONS

EVT and MS had similar clinical outcomes at 1 year following ruptured WNA treatment. Because of their challenging anatomy, WNAs may represent a population in which EVT’s previously demonstrated superiority for ruptured aneurysm treatment is less relevant. Further investigation into the treatment of ruptured WNAs is warranted.

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Chul Han, Michael J. Lang, Candice L. Nguyen, Ernesto Luna Melendez, Shwetal Mehta, Gregory H. Turner, Michael T. Lawton, and S. Paul Oh

OBJECTIVE

Hereditary hemorrhagic telangiectasia is the only condition associated with multiple inherited brain arteriovenous malformations (AVMs). Therefore, a mouse model was developed with a genetics-based approach that conditionally deleted the causative activin receptor-like kinase 1 (Acvrl1 or Alk1) gene. Radiographic and histopathological findings were correlated, and AVM stability and hemorrhagic behavior over time were examined.

METHODS

Alk1-floxed mice were crossed with deleter mice to generate offspring in which both copies of the Alk1 gene were deleted by Tagln-Cre to form brain AVMs in the mice. AVMs were characterized using MRI, MRA, and DSA. Brain AVMs were characterized histopathologically with latex dye perfusion, immunofluorescence, and Prussian blue staining.

RESULTS

Brains of 55 Tagln-Cre+;Alk1 f/f mutant mice were categorized into three groups: no detectable vascular lesions (group 1; 23 of 55, 42%), arteriovenous fistulas (AVFs) with no nidus (group 2; 10 of 55, 18%), and nidal AVMs (group 3; 22 of 55, 40%). Microhemorrhage was observed on MRI or MRA in 11 AVMs (50%). AVMs had the angiographic hallmarks of early nidus opacification, a tangle of arteries and dilated draining veins, and rapid shunting of blood flow. Latex dye perfusion confirmed arteriovenous shunting in all AVMs and AVFs. Microhemorrhages were detected adjacent to AVFs and AVMs, visualized by iron deposition, Prussian blue staining, and macrophage infiltration using CD68 immunostaining. Brain AVMs were stable on serial MRI and MRA in group 3 mice (mean age at initial imaging 2.9 months; mean age at last imaging 9.5 months).

CONCLUSIONS

Approximately 40% of transgenic mice satisfied the requirements of a stable experimental AVM model by replicating nidal anatomy, arteriovenous hemodynamics, and microhemorrhagic behavior. Transgenic mice with AVFs had a recognizable phenotype of hereditary hemorrhagic telangiectasia but were less suitable for experimental modeling. AVM pathogenesis can be understood as the combination of conditional Alk1 gene deletion during embryogenesis and angiogenesis that is hyperactive in developing and newborn mice, which translates to a congenital origin in most patients but an acquired condition in patients with a confluence of genetic and angiogenic events later in life. This study offers a novel experimental brain AVM model for future studies of AVM pathophysiology, growth, rupture, and therapeutic regression.

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Juan Leonardo Serrato-Avila, Juan Alberto Paz Archila, Marcos Devanir Silva da Costa, Paulo Ricardo Rocha, Sergio Ricardo Marques, Luis Otavio Carvalho de Moraes, Sergio Cavalheiro, Kaan Yağmurlu, Michael T. Lawton, and Feres Chaddad-Neto

OBJECTIVE

The cerebellar interpeduncular region (CIPR) is a gate for dorsolateral pontine and cerebellar lesions accessed through the supracerebellar infratentorial approach (SCITa), the occipital transtentorial approach (OTa), or the subtemporal transtentorial approach (STa). The authors sought to compare the exposures of the CIPR region that each of these approaches provided.

METHODS

Three approaches were performed bilaterally in eight silicone-injected cadaveric heads. The working area, area of exposure, depth of the surgical corridor, length of the interpeduncular sulcus (IPS) exposed, and bridging veins were statistically studied and compared based on each approach.

RESULTS

The OTa provided the largest working area (1421 mm2; p < 0.0001) and the longest surgical corridor (6.75 cm; p = 0.0006). Compared with the SCITa, the STa provided a larger exposure area (249.3 mm2; p = 0.0148) and exposed more of the length of the IPS (1.15 cm; p = 0.0484). The most bridging veins were encountered with the SCITa; however, no significant differences were found between this approach and the other approaches (p > 0.05).

CONCLUSIONS

To reach the CIPR, the STa provided a more extensive exposure area and more linear exposure than did the SCITa. The OTa offered a larger working area than the SCIT and the STa; however, the OTa had the most extensive surgical corridor. These data may help neurosurgeons select the most appropriate approach for lesions of the CIPR.

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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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Rohin Singh, Visish M. Srinivasan, Joshua S. Catapano, Joseph D. DiDomenico, Jacob F. Baranoski, and Michael T. Lawton

BACKGROUND

Coccidioidomycosis is a primarily self-limiting fungal disease endemic to the western United States and South America. However, severe disseminated infection can occur. The authors report a severe case of coccidioidal meningitis that appeared to be a subarachnoid hemorrhage (SAH) on initial inspection.

OBSERVATIONS

A man in his early 40s was diagnosed with coccidioidal pneumonia after presenting with pulmonary symptoms. After meningeal spread characterized by declining mental status and hydrocephalus, coccidioidal meningitis was diagnosed. The uniquely difficult aspect of this case was the deceptive appearance of SAH due to the presence of multiple aneurysms and blood draining from the patient’s external ventricular drain.

LESSONS

Coccidioidal infection likely led to the formation of multiple intracranial aneurysms in this patient. Although few reports exist of coccidioidal meningitis progressing to aneurysm formation, patients should be closely monitored for this complication because outcomes are poor. The presence of basal cistern hyperdensities from a coccidioidal infection mimicking SAH makes interpreting imaging difficult. Surgical management of SAH can be considered safe and viable, especially when the index of suspicion is high, such as in the presence of multiple aneurysms. Even if it is unclear whether aneurysmal rupture has occurred, prompt treatment is advisable.

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Sepideh Amin-Hanjani, Howard A. Riina, and Fred G. Barker II

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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.