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Joshua S. Catapano, Dimitri Benner, Emmajane G. Rhodenhiser, Kavelin Rumalla, Christopher S. Graffeo, Visish M. Srinivasan, Ethan A. Winkler, and Michael T. Lawton

OBJECTIVE

Safe entry zones (SEZs) enable safe tissue transgression to lesions beneath the brainstem surface. However, evidence for the safety of SEZs is scarce and is based on anatomical studies, case reports, and small series.

METHODS

A cohort of 154 patients who underwent microsurgical brainstem cavernous malformation (BSCM) treatment during a 23-year period and who had preoperative MR images and intraoperative photographs or videos was retrospectively examined. This study assessed the safety of SEZs for access to deep BSCMs, preoperative MRI to predict BSCM surface proximity, and the relationships between BSCM subtype, surgical approach, and SEZs. Lesions were characterized as exophytic, superficial, or deep on the basis of preoperative MRI and intraoperative inspection. Outcomes were scored as good (modified Rankin Scale [mRS] score ≤ 2) or poor (mRS score > 2) and relative outcomes as stable/improved or worse relative to baseline (± 1 point).

RESULTS

Resections included 34 (22%) in the midbrain, 102 (66%) in the pons, and 18 (12%) in the medulla. Of those, 23 (15%) were exophytic, 57 (37%) were superficial, and 74 (48%) were deep. Established SEZs were used for 97% (n = 72) of deep lesions; the preferred SEZ associated with its subtype was used for 91% (n = 67). MR images accurately depicted exophytic BSCMs that did not require SEZ approaches (sensitivity, 96%) but overestimated the proximity of lesions superficial to brainstem surfaces (specificity, 67%), resulting in unanticipated SEZ use. Final neurological outcomes were good in 80% of patients with follow-up data (119/149), and relative outcomes were stable/improved in 93% (139/149). Outcomes for patients with brainstem transgression through an SEZ did not differ from outcomes for patients with superficial or exophytic lesions that did not require SEZ use (final mRS score ≤ 2 in 72% of all patients with deep lesions vs 82% of all patients with superficial or exophytic lesions [p = 0.10]). Among patients with follow-up, the rates of permanent new cranial nerve deficits in patients with deep BSCMs and superficial or exophytic BSCMs were 21% and 20%, respectively (p = 0.81), with no significant change in overall cranial nerve deficit (0 and −1, p = 0.65).

CONCLUSIONS

Neurological outcomes for patients with deep BSCMs were equivalent to those for superficial or exophytic BSCMs, validating the safety of SEZs for deep BSCMs. Preoperative T1-weighted MR images overestimated the lesion’s surface proximity, necessitating detailed knowledge of SEZs and readiness to use them in cases of radiological-microsurgical discordance. Most patients achieved favorable outcomes despite the transgression of eloquent brainstem tissue in and around SEZs.

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Michael T. Lawton, Christopher S. Graffeo, Visish M. Srinivasan, Benjamin K. Hendricks, Joshua S. Catapano, Lea Scherschinski, Peter M. Lawrence, Kristen Larson Keil, Danielle VanBrabant, and Michael D. Hickman

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Dimitri Benner, Benjamin K. Hendricks, Arnau Benet, Christopher S. Graffeo, Lea Scherschinski, Visish M. Srinivasan, Joshua S. Catapano, Peter M. Lawrence, Mark Schornak, and Michael T. Lawton

OBJECTIVE

Anatomical triangles defined by intersecting neurovascular structures delineate surgical routes to pathological targets and guide neurosurgeons during dissection steps. Collections or systems of anatomical triangles have been integrated into skull base surgery to help surgeons navigate complex regions such as the cavernous sinus. The authors present a system of triangles specifically intended for resection of brainstem cavernous malformations (BSCMs). This system of triangles is complementary to the authors’ BSCM taxonomy that defines dissection routes to these lesions.

METHODS

The anatomical triangle through which a BSCM was resected microsurgically was determined for the patients treated during a 23-year period who had both brain MRI and intraoperative photographs or videos available for review.

RESULTS

Of 183 patients who met the inclusion criteria, 50 had midbrain lesions (27%), 102 had pontine lesions (56%), and 31 had medullary lesions (17%). The craniotomies used to resect these BSCMs included the extended retrosigmoid (66 [36.1%]), midline suboccipital (46 [25.1%]), far lateral (30 [16.4%]), pterional/orbitozygomatic (17 [9.3%]), torcular (8 [4.4%]), and lateral suboccipital (8 [4.4%]) approaches. The anatomical triangles through which the BSCMs were most frequently resected were the interlobular (37 [20.2%]), vallecular (32 [17.5%]), vagoaccessory (30 [16.4%]), supracerebellar-infratrochlear (16 [8.7%]), subtonsillar (14 [7.7%]), oculomotor-tentorial (11 [6.0%]), infragalenic (8 [4.4%]), and supracerebellar-supratrochlear (8 [4.4%]) triangles. New but infrequently used triangles included the vertebrobasilar junctional (1 [0.5%]), supratrigeminal (3 [1.6%]), and infratrigeminal (5 [2.7%]) triangles. Overall, 15 BSCM subtypes were exposed through 6 craniotomies, and the approach was redirected to the BSCM by one of the 14 triangles paired with the BSCM subtype.

CONCLUSIONS

A system of BSCM triangles, including 9 newly defined triangles, was introduced to guide dissection to these lesions. The use of an anatomical triangle better defines the pathway taken through the craniotomy to the lesion and refines the conceptualization of surgical approaches. The triangle concept and the BSCM triangle system increase the precision of dissection through subarachnoid corridors, enhance microsurgical execution, and potentially improve patient outcomes.

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Evgenii Belykh, Irakliy Abramov, Liudmila Bardonova, Ruchi Patel, Sarah McBryan, Lara Enriquez Bouza, Neil Majmundar, Xiaochun Zhao, Vadim A. Byvaltsev, Stephen A. Johnson, Amit Singla, Gaurav Gupta, Hai Sun, James K. Liu, Anil Nanda, Mark C. Preul, and Michael T. Lawton

OBJECTIVE

Microsurgical training remains indispensable to master cerebrovascular bypass procedures, but simulation models for training that accurately replicate microanastomosis in narrow, deep-operating corridors are lacking. Seven simulation bypass scenarios were developed that included head models in various surgical positions with premade approaches, simulating the restrictions of the surgical corridors and hand positions for microvascular bypass training. This study describes these models and assesses their validity.

METHODS

Simulation models were created using 3D printing of the skull with a designed craniotomy. Brain and external soft tissues were cast using a silicone molding technique from the clay-sculptured prototypes. The 7 simulation scenarios included: 1) temporal craniotomy for a superficial temporal artery (STA)–middle cerebral artery (MCA) bypass using the M4 branch of the MCA; 2) pterional craniotomy and transsylvian approach for STA-M2 bypass; 3) bifrontal craniotomy and interhemispheric approach for side-to-side bypass using the A3 branches of the anterior cerebral artery; 4) far lateral craniotomy and transcerebellomedullary approach for a posterior inferior cerebellar artery (PICA)–PICA bypass or 5) PICA reanastomosis; 6) orbitozygomatic craniotomy and transsylvian-subtemporal approach for a posterior cerebral artery bypass; and 7) extended retrosigmoid craniotomy and transcerebellopontine approach for an occipital artery–anterior inferior cerebellar artery bypass. Experienced neurosurgeons evaluated each model by practicing the aforementioned bypasses on the models. Face and content validities were assessed using the bypass participant survey.

RESULTS

A workflow for model production was developed, and these models were used during microsurgical courses at 2 neurosurgical institutions. Each model is accompanied by a corresponding prototypical case and surgical video, creating a simulation scenario. Seven experienced cerebrovascular neurosurgeons practiced microvascular anastomoses on each of the models and completed surveys. They reported that actual anastomosis within a specific approach was well replicated by the models, and difficulty was comparable to that for real surgery, which confirms the face validity of the models. All experts stated that practice using these models may improve bypass technique, instrument handling, and surgical technique when applied to patients, confirming the content validity of the models.

CONCLUSIONS

The 7 bypasses simulation set includes novel models that effectively simulate surgical scenarios of a bypass within distinct deep anatomical corridors, as well as hand and operator positions. These models use artificial materials, are reusable, and can be implemented for personal training and during microsurgical courses.

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Visish M. Srinivasan, Katherine Karahalios, Vamsi P. Reddy, Lea Scherschinski, Joseph D. DiDomenico, Redi Rahmani, Joshua S. Catapano, Mohamed A. Labib, Kavelin Rumalla, Christopher S. Graffeo, and Michael T. Lawton

OBJECTIVE

The objective of this paper was to assess applications of the supratentorial-infraoccipital (STIO) approach for cerebrovascular neurosurgery.

METHODS

The authors conducted a cohort study of all consecutive cases in which the STIO approach was used during the study period, December 1995 to January 2021, as well as a systematic review of the literature.

RESULTS

Twenty-five cerebrovascular cases were identified in which the STIO approach was used. Diagnoses included arteriovenous malformation (n = 15), cerebral cavernous malformation (n = 5), arteriovenous fistula (n = 4), and aneurysm (n = 1). The arteriovenous malformations consisted of Spetzler-Martin grade II (n = 3), grade III (n = 8), and grade IV (n = 4) lesions. Lesion locations included the occipital lobe (n = 15), followed by the tentorial dural (n = 4), temporal-occipital (n = 3), temporal (n = 1), thalamic (n = 1), and quadrigeminal cistern (n = 1) regions. Many patients (75%) experienced transient visual deficits attributable to retraction of the occipital lobe, all of which resolved. As of last follow-up (n = 12), modified Rankin Scale scores had improved for 6 patients and were unchanged for 6 patients compared with the preoperative baseline.

CONCLUSIONS

The STIO approach is a safe and effective skull base approach that provides a specialized access corridor for appropriately selected cerebrovascular lesions.

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Irakliy Abramov, Marian T. Park, Evgenii Belykh, Alexander B. Dru, Yuan Xu, Timothy C. Gooldy, Lea Scherschinski, S. Harrison Farber, Andrew S. Little, Randall W. Porter, Kris A. Smith, Michael T. Lawton, Jennifer M. Eschbacher, and Mark C. Preul

OBJECTIVE

The authors evaluated the feasibility of using the first clinical-grade confocal laser endomicroscopy (CLE) system using fluorescein sodium for intraoperative in vivo imaging of brain tumors.

METHODS

A CLE system cleared by the FDA was used in 30 prospectively enrolled patients with 31 brain tumors (13 gliomas, 5 meningiomas, 6 other primary tumors, 3 metastases, and 4 reactive brain tissue). A neuropathologist classified CLE images as interpretable or noninterpretable. Images were compared with corresponding frozen and permanent histology sections, with image correlation to biopsy location using neuronavigation. The specificities and sensitivities of CLE images and frozen sections were calculated using permanent histological sections as the standard for comparison. A recently developed surgical telepathology software platform was used in 11 cases to provide real-time intraoperative consultation with a neuropathologist.

RESULTS

Overall, 10,713 CLE images from 335 regions of interest were acquired. The mean duration of the use of the CLE system was 7 minutes (range 3–18 minutes). Interpretable CLE images were obtained in all cases. The first interpretable image was acquired within a mean of 6 (SD 10) images and within the first 5 (SD 13) seconds of imaging; 4896 images (46%) were interpretable. Interpretable image acquisition was positively correlated with study progression, number of cases per surgeon, cumulative length of CLE time, and CLE time per case (p ≤ 0.01). The diagnostic accuracy, sensitivity, and specificity of CLE compared with frozen sections were 94%, 94%, and 100%, respectively, and the diagnostic accuracy, sensitivity, and specificity of CLE compared with permanent histological sections were 92%, 90%, and 94%, respectively. No difference was observed between lesion types for the time to first interpretable image (p = 0.35). Deeply located lesions were associated with a higher percentage of interpretable images than superficial lesions (p = 0.02). The study met the primary end points, confirming the safety and feasibility and acquisition of noninvasive digital biopsies in all cases. The study met the secondary end points for the duration of CLE use necessary to obtain interpretable images. A neuropathologist could interpret the CLE images in 29 (97%) of 30 cases.

CONCLUSIONS

The clinical-grade CLE system allows in vivo, intraoperative, high-resolution cellular visualization of tissue microstructure and identification of lesional tissue patterns in real time, without the need for tissue preparation.

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Ethan A. Winkler, Mark A. Pacult, Joshua S. Catapano, Lea Scherschinski, Visish M. Srinivasan, Christopher S. Graffeo, S. Paul Oh, and Michael T. Lawton

A variety of pathogenic mechanisms have been described in the formation, maturation, and rupture of brain arteriovenous malformations (bAVMs). While the understanding of bAVMs has largely been formulated based on animal models of rare hereditary diseases in which AVMs form, a new era of “omics” has permitted large-scale examinations of contributory genetic variations in human sporadic bAVMs. New findings regarding the pathogenesis of bAVMs implicate changes to endothelial and mural cells that result in increased angiogenesis, proinflammatory recruitment, and breakdown of vascular barrier properties that may result in hemorrhage; a greater diversity of cell populations that compose the bAVM microenvironment may also be implicated and complicate traditional models. Genomic sequencing of human bAVMs has uncovered inherited, de novo, and somatic activating mutations, such as KRAS, which contribute to the pathogenesis of bAVMs. New droplet-based, single-cell sequencing technologies have generated atlases of cell-specific molecular derangements. Herein, the authors review emerging genomic and transcriptomic findings underlying pathologic cell transformations in bAVMs derived from human tissues. The application of multiple sequencing modalities to bAVM tissues is a natural next step for researchers, although the potential therapeutic benefits or clinical applications remain unknown.

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Satvir Saggi, Ethan A. Winkler, Simon G. Ammanuel, Ramin A. Morshed, Joseph H. Garcia, Jacob S. Young, Alexa Semonche, Heather J. Fullerton, Helen Kim, Daniel L. Cooke, Steven W. Hetts, Adib Abla, Michael T. Lawton, and Nalin Gupta

OBJECTIVE

Ruptured brain arteriovenous malformations (bAVMs) in a child are associated with substantial morbidity and mortality. Prior studies investigating predictors of hemorrhagic presentation of a bAVM during childhood are limited. Machine learning (ML), which has high predictive accuracy when applied to large data sets, can be a useful adjunct for predicting hemorrhagic presentation. The goal of this study was to use ML in conjunction with a traditional regression approach to identify predictors of hemorrhagic presentation in pediatric patients based on a retrospective cohort study design.

METHODS

Using data obtained from 186 pediatric patients over a 19-year study period, the authors implemented three ML algorithms (random forest models, gradient boosted decision trees, and AdaBoost) to identify features that were most important for predicting hemorrhagic presentation. Additionally, logistic regression analysis was used to ascertain significant predictors of hemorrhagic presentation as a comparison.

RESULTS

All three ML models were consistent in identifying bAVM size and patient age at presentation as the two most important factors for predicting hemorrhagic presentation. Age at presentation was not identified as a significant predictor of hemorrhagic presentation in multivariable logistic regression. Gradient boosted decision trees/AdaBoost and random forest models identified bAVM location and a concurrent arterial aneurysm as the third most important factors, respectively. Finally, logistic regression identified a left-sided bAVM, small bAVM size, and the presence of a concurrent arterial aneurysm as significant risk factors for hemorrhagic presentation.

CONCLUSIONS

By using an ML approach, the authors found predictors of hemorrhagic presentation that were not identified using a conventional regression approach.

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Irakliy Abramov, Marian T. Park, Timothy C. Gooldy, Yuan Xu, Michael T. Lawton, Andrew S. Little, Randall W. Porter, Kris A. Smith, Jennifer M. Eschbacher, and Mark C. Preul

OBJECTIVE

Communication between neurosurgeons and pathologists is mandatory for intraoperative decision-making and optimization of resection, especially for invasive masses. Handheld confocal laser endomicroscopy (CLE) technology provides in vivo intraoperative visualization of tissue histoarchitecture at cellular resolution. The authors evaluated the feasibility of using an innovative surgical telepathology software platform (TSP) to establish real-time, on-the-fly remote communication between the neurosurgeon using CLE and the pathologist.

METHODS

CLE and a TSP were integrated into the surgical workflow for 11 patients with brain masses (6 patients with gliomas, 3 with other primary tumors, 1 with metastasis, and 1 with reactive brain tissue). Neurosurgeons used CLE to generate video-flow images of the operative field that were displayed on monitors in the operating room. The pathologist simultaneously viewed video-flow CLE imaging using a digital tablet and communicated with the surgeon while physically located outside the operating room (1 pathologist was in another state, 4 were at home, and 6 were elsewhere in the hospital). Interpretations of the still CLE images and video-flow CLE imaging were compared with the findings on the corresponding frozen and permanent H&E histology sections.

RESULTS

Overall, 24 optical biopsies were acquired with mean ± SD 2 ± 1 optical biopsies per case. The mean duration of CLE system use was 1 ± 0.3 minutes/case and 0.25 ± 0.23 seconds/optical biopsy. The first image with identifiable histopathological features was acquired within 6 ± 0.1 seconds. Frozen sections were processed within 23 ± 2.8 minutes, which was significantly longer than CLE usage (p < 0.001). Video-flow CLE was used to correctly interpret tissue histoarchitecture in 96% of optical biopsies, which was substantially higher than the accuracy of using still CLE images (63%) (p = 0.005).

CONCLUSIONS

When CLE is employed in tandem with a TSP, neurosurgeons and pathologists can view and interpret CLE images remotely and in real time without the need to biopsy tissue. A TSP allowed neurosurgeons to receive real-time feedback on the optically interrogated tissue microstructure, thereby improving cross-functional communication and intraoperative decision-making and resulting in significant workflow advantages over the use of frozen section analysis.

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Joshua S. Catapano, Kavelin Rumalla, Visish M. Srinivasan, Peter M. Lawrence, Kristen Larson Keil, and Michael T. Lawton

OBJECTIVE

Medullary cavernous malformations are the least common of the brainstem cavernous malformations (BSCMs), accounting for only 14% of lesions in the authors’ surgical experience. In this article, a novel taxonomy for these lesions is proposed based on clinical presentation and anatomical location.

METHODS

The taxonomy system was applied to a large 2-surgeon experience over a 30-year period (1990–2019). Of 601 patients who underwent microsurgical resection of BSCMs, 551 were identified who had the clinical and radiological information needed for inclusion. These 551 patients were classified by lesion location: midbrain (151 [27%]), pons (323 [59%]), and medulla (77 [14%]). Medullary lesions were subtyped on the basis of their predominant surface presentation. Neurological outcomes were assessed according to the modified Rankin Scale (mRS), with an mRS score ≤ 2 defined as favorable.

RESULTS

Five distinct subtypes were defined for the 77 medullary BSCMs: pyramidal (3 [3.9%]), olivary (35 [46%]), cuneate (24 [31%]), gracile (5 [6.5%]), and trigonal (10 [13%]). Pyramidal lesions are located in the anterior medulla and were associated with hemiparesis and hypoglossal nerve palsy. Olivary lesions are found in the anterolateral medulla and were associated with ataxia. Cuneate lesions are located in the posterolateral medulla and were associated with ipsilateral upper-extremity sensory deficits. Gracile lesions are located outside the fourth ventricle in the posteroinferior medulla and were associated with ipsilateral lower-extremity sensory deficits. Trigonal lesions in the ventricular floor were associated with nausea, vomiting, and diplopia. A single surgical approach was preferred (> 90% of cases) for each medullary subtype: the far lateral approach for pyramidal and olivary lesions, the suboccipital-telovelar approach for cuneate lesions, the suboccipital-transcisterna magna approach for gracile lesions, and the suboccipital-transventricular approach for trigonal lesions. Of these 77 patients for whom follow-up data were available (n = 73), 63 (86%) had favorable outcomes and 67 (92%) had unchanged or improved functional status.

CONCLUSIONS

This study confirms that the constellation of neurological signs and symptoms associated with a hemorrhagic medullary BSCM subtype is useful for defining the BSCM clinically according to a neurologically recognizable syndrome at the bedside. The proposed taxonomical classifications may be used to guide the selection of surgical approaches, which may enhance the consistency of clinical communications and help improve patient outcomes.