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David T. Asuzu, Adomas Bunevicius, Rithika Kormath Anand, Mohanad Suleiman, Ahmed M. Nabeel, Wael A. Reda, Sameh R. Tawadros, Khaled Abdel Karim, Amr M. N. El-Shehaby, Reem M. Emad Eldin, Tomas Chytka, Roman Liščák, Kimball Sheehan, Darrah Sheehan, Marco Perez Caceres, David Mathieu, Cheng-chia Lee, Huai-che Yang, Piero Picozzi, Andrea Franzini, Luca Attuati, Herwin Speckter, Jeremy Olivo, Samir Patel, Christopher P. Cifarelli, Daniel T. Cifarelli, Joshua D. Hack, Ben A. Strickland, Gabriel Zada, Eric L. Chang, Kareem R. Fakhoury, Chad G. Rusthoven, Ronald E. Warnick, and Jason P. Sheehan

OBJECTIVE

Resection of meningiomas in direct contact with the anterior optic apparatus carries risk of injury to the visual pathway. Stereotactic radiosurgery (SRS) offers a minimally invasive alternative. However, its use is limited owing to the risk of radiation-induced optic neuropathy. Few SRS studies have specifically assessed the risks and benefits of treating meningiomas in direct contact with the optic nerve, chiasm, or optic tract. The authors hypothesized that SRS is safe for select patients with meningiomas in direct contact with the anterior optic apparatus.

METHODS

The authors performed an international multicenter retrospective analysis of 328 patients across 11 institutions. All patients had meningiomas in direct contract with the optic apparatus. Patients were followed for a median duration of 56 months after SRS. Neurological examinations, including visual function evaluations, were performed at follow-up visits. Clinical and treatment variables were collected at each site according to protocol. Tumor volumes were assessed with serial MR imaging. Variables predictive of visual deficit were identified using univariable and multivariable logistic regression.

RESULTS

SRS was the initial treatment modality for 64.6% of patients, and 93% of patients received SRS as a single fraction. Visual information was available for 302 patients. Of these patients, visual decline occurred in 29 patients (9.6%), of whom 12 (41.4%) had evidence of tumor progression. Visual decline in the remaining 17 patients (5.6%) was not associated with tumor progression. Pre-SRS Karnofsky Performance Status predicted visual decline in adjusted analysis (adjusted OR 0.9, 95% CI 0.9–1.0, p < 0.01). Follow-up imaging data were available for 322 patients. Of these patients, 294 patients (91.3%) had radiographic evidence of stability or tumor regression at last follow up. Symptom duration was associated with tumor progression in adjusted analysis (adjusted OR 1.01, adjusted 95% CI 1.0–1.02, adjusted p = 0.02).

CONCLUSIONS

In this international multicenter study, the vast majority of patients exhibited tumor control and preservation of visual function when SRS was used to treat meningioma in direct contact with the anterior optic pathways. SRS is a relatively safe treatment modality for select patients with perioptic meningiomas in direct contact with the optic apparatus.

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I. Jonathan Pomeraniec, Zhiyuan Xu, Cheng-Chia Lee, Huai-Che Yang, Tomas Chytka, Roman Liscak, Roberto Martinez-Alvarez, Nuria Martinez-Moreno, Luca Attuati, Piero Picozzi, Douglas Kondziolka, Monica Mureb, Kenneth Bernstein, David Mathieu, Michel Maillet, Akiyoshi Ogino, Hao Long, Hideyuki Kano, L. Dade Lunsford, Brad E. Zacharia, Christine Mau, Leonard C. Tuanquin, Christopher Cifarelli, David Arsanious, Joshua Hack, Ronald E. Warnick, Ben A. Strickland, Gabriel Zada, Eric L. Chang, Herwin Speckter, Samir Patel, Dale Ding, Darrah Sheehan, Kimball Sheehan, Svetlana Kvint, Love Y. Buch, Alexander R. Haber, Jacob Shteinhart, Mary Lee Vance, and Jason P. Sheehan

OBJECTIVE

Stereotactic radiosurgery (SRS) provides a safe and effective therapeutic modality for patients with pituitary adenomas. The mechanism of delayed endocrine deficits based on targeted radiation to the hypothalamic-pituitary axis remains unclear. Radiation to normal neuroendocrine structures likely plays a role in delayed hypopituitarism after SRS. In this multicenter study by the International Radiosurgery Research Foundation (IRRF), the authors aimed to evaluate radiation tolerance of structures surrounding pituitary adenomas and identify predictors of delayed hypopituitarism after SRS for these tumors.

METHODS

This is a retrospective review of patients with pituitary adenomas who underwent single-fraction SRS from 1997 to 2019 at 16 institutions within the IRRF. Dosimetric point measurements of 14 predefined neuroanatomical structures along the hypothalamus, pituitary stalk, and normal pituitary gland were made. Statistical analyses were performed to determine the impact of doses to critical structures on clinical, radiographic, and endocrine outcomes.

RESULTS

The study cohort comprised 521 pituitary adenomas treated with SRS. Tumor control was achieved in 93.9% of patients over a median follow-up period of 60.1 months, and 22.5% of patients developed new loss of pituitary function with a median treatment volume of 3.2 cm3. Median maximal radiosurgical doses to the hypothalamus, pituitary stalk, and normal pituitary gland were 1.4, 7.2, and 11.3 Gy, respectively. Nonfunctioning adenoma status, younger age, higher margin dose, and higher doses to the pituitary stalk and normal pituitary gland were independent predictors of new or worsening hypopituitarism. Neither the dose to the hypothalamus nor the ratio between doses to the pituitary stalk and gland were significant predictors. The threshold of the median dose to the pituitary stalk for new endocrinopathy was 10.7 Gy in a single fraction (OR 1.77, 95% CI 1.17–2.68, p = 0.006).

CONCLUSIONS

SRS for the treatment of pituitary adenomas affords a high tumor control rate with an acceptable risk of new or worsening endocrinopathy. This evaluation of point dosimetry to adjacent neuroanatomical structures revealed that doses to the pituitary stalk, with a threshold of 10.7 Gy, and doses to the normal gland significantly increased the risk of post-SRS hypopituitarism. In patients with preserved pre-SRS neuroendocrine function, limiting the dose to the pituitary stalk and gland while still delivering an optimal dose to the tumor appears prudent.

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Alexander Micko, Matthew S. Agam, Andrew Brunswick, Ben A. Strickland, Martin J. Rutkowski, John D. Carmichael, Mark S. Shiroishi, Gabriel Zada, Engelbert Knosp, and Stefan Wolfsberger

OBJECTIVE

Given the anatomical complexity and frequently invasive growth of giant pituitary adenomas (GPAs), individually tailored approaches are required. The aim of this study was to assess the treatment strategies and outcomes in a large multicenter series of GPAs in the era of endoscopic transsphenoidal surgery (ETS).

METHODS

This was a retrospective case-control series of 64 patients with GPAs treated at two tertiary care centers by surgeons with experience in ETS. GPAs were defined by a maximum diameter of ≥ 4 cm and a volume of ≥ 10 cm3 on preoperative isovoxel contrast-enhanced MRI.

RESULTS

The primary operation was ETS in all cases. Overall gross-total resection rates were 64% in round GPAs, 46% in dumbbell-shaped GPAs, and 8% in multilobular GPAs (p < 0.001). Postoperative outcomes were further stratified into two groups based on extent of resection: group A (gross-total resection or partial resection with intracavernous remnant; 21/64, 33%) and group B (partial resection with intracranial remnant; 43/64, 67%). Growth patterns of GPAs were mostly round (11/14, 79%) in group A and multilobular (33/37, 89%) in group B. In group A, no patients required a second operation, and 2/21 (9%) were treated with adjuvant radiosurgery. In group B, early transcranial reoperation was required in 6/43 (14%) cases due to hemorrhagic transformation of remnants. For the remaining group B patients with remnants, 5/43 (12%) underwent transcranial surgery and 12/43 (28%) underwent delayed second ETS. There were no deaths in this series. Severe complications included stroke (6%), meningitis (6%), hydrocephalus requiring shunting (6%), and loss or distinct worsening of vision (3%). At follow-up (mean 3 years, range 0.5–16 years), stable disease was achieved in 91% of cases.

CONCLUSIONS

ETS as a primary treatment modality to relieve mass effect in GPAs and extent of resection are dependent on GPA morphology. The pattern of residual pituitary adenoma guides further treatment strategies, including early transcranial reoperation, delayed endoscopic transsphenoidal/transcranial reoperation, and adjuvant radiosurgery.

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Justin Chan, Dhiraj J. Pangal, Tyler Cardinal, Guillaume Kugener, Yichao Zhu, Arman Roshannai, Nicholas Markarian, Aditya Sinha, Anima Anandkumar, Andrew Hung, Gabriel Zada, and Daniel A. Donoho

OBJECTIVE

Virtual reality (VR) and augmented reality (AR) systems are increasingly available to neurosurgeons. These systems may provide opportunities for technical rehearsal and assessments of surgeon performance. The assessment of neurosurgeon skill in VR and AR environments and the validity of VR and AR feedback has not been systematically reviewed.

METHODS

A systematic review following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines was conducted through MEDLINE and PubMed. Studies published in English between January 1990 and February 2021 describing the use of VR or AR to quantify surgical technical performance of neurosurgeons without the use of human raters were included. The types and categories of automated performance metrics (APMs) from each of these studies were recorded.

RESULTS

Thirty-three VR studies were included in the review; no AR studies met inclusion criteria. VR APMs were categorized as either distance to target, force, kinematics, time, blood loss, or volume of resection. Distance and time were the most well-studied APM domains, although all domains were effective at differentiating surgeon experience levels. Distance was successfully used to track improvements with practice. Examining volume of resection demonstrated that attending surgeons removed less simulated tumor but preserved more normal tissue than trainees. More recently, APMs have been used in machine learning algorithms to predict level of training with a high degree of accuracy. Key limitations to enhanced-reality systems include limited AR usage for automated surgical assessment and lack of external and longitudinal validation of VR systems.

CONCLUSIONS

VR has been used to assess surgeon performance across a wide spectrum of domains. The VR environment can be used to quantify surgeon performance, assess surgeon proficiency, and track training progression. AR systems have not yet been used to provide metrics for surgeon performance assessment despite potential for intraoperative integration. VR-based APMs may be especially useful for metrics that are difficult to assess intraoperatively, including blood loss and extent of resection.

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Josh Neman, Meredith Franklin, Zachary Madaj, Krutika Deshpande, Timothy J. Triche Jr., Gal Sadlik, John D Carmichael, Eric Chang, Cheng Yu, Ben A Strickland, and Gabriel Zada

OBJECTIVE

Brain metastasis is the most common intracranial neoplasm. Although anatomical spatial distributions of brain metastasis may vary according to primary cancer subtype, these patterns are not understood and may have major implications for treatment.

METHODS

To test the hypothesis that the spatial distribution of brain metastasis varies according to cancer origin in nonrandom patterns, the authors leveraged spatial 3D coordinate data derived from stereotactic Gamma Knife radiosurgery procedures performed to treat 2106 brain metastases arising from 5 common cancer types (melanoma, lung, breast, renal, and colorectal). Two predictive topographic models (regional brain metastasis echelon model [RBMEM] and brain region susceptibility model [BRSM]) were developed and independently validated.

RESULTS

RBMEM assessed the hierarchical distribution of brain metastasis to specific brain regions relative to other primary cancers and showed that distinct regions were relatively susceptible to metastasis, as follows: bilateral temporal/parietal and left frontal lobes were susceptible to lung cancer; right frontal and occipital lobes to melanoma; cerebellum to breast cancer; and brainstem to renal cell carcinoma. BRSM provided probability estimates for each cancer subtype, independent of other subtypes, to metastasize to brain regions, as follows: lung cancer had a propensity to metastasize to bilateral temporal lobes; breast cancer to right cerebellar hemisphere; melanoma to left temporal lobe; renal cell carcinoma to brainstem; and colon cancer to right cerebellar hemisphere. Patient topographic data further revealed that brain metastasis demonstrated distinct spatial patterns when stratified by patient age and tumor volume.

CONCLUSIONS

These data support the hypothesis that there is a nonuniform spatial distribution of brain metastasis to preferential brain regions that varies according to cancer subtype in patients treated with Gamma Knife radiosurgery. These topographic patterns may be indicative of the abilities of various cancers to adapt to regional neural microenvironments, facilitate colonization, and establish metastasis. Although the brain microenvironment likely modulates selective seeding of metastasis, it remains unknown how the anatomical spatial distribution of brain metastasis varies according to primary cancer subtype and contributes to diagnosis. For the first time, the authors have presented two predictive models to show that brain metastasis, depending on its origin, in fact demonstrates distinct geographic spread within the central nervous system. These findings could be used as a predictive diagnostic tool and could also potentially result in future translational and therapeutic work to disrupt growth of brain metastasis on the basis of anatomical region.

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Shane Shahrestani, Danielle Wishart, Sung Min J. Han, Ben A. Strickland, Joshua Bakhsheshian, William J. Mack, Arthur W. Toga, Nerses Sanossian, Yu-Chong Tai, and Gabriel Zada

OBJECTIVE

Stroke is a leading cause of morbidity and mortality. Current diagnostic modalities include CT and MRI. Over the last decade, novel technologies to facilitate stroke diagnosis, with the hope of shortening time to treatment and reducing rates of morbidity and mortality, have been developed. The authors conducted a systematic review to identify studies reporting on next-generation point-of-care stroke diagnostic technologies described within the last decade.

METHODS

A systematic review was performed according to PRISMA guidelines to identify studies reporting noninvasive stroke diagnostics. The QUADAS-2 (Quality Assessment of Diagnostic Accuracy Studies-2) tool was utilized to assess risk of bias. PubMed, Web of Science, and Scopus databases were utilized. Primary outcomes assessed included accuracy and timing compared with standard imaging, potential risks or complications, potential limitations, cost of the technology, size/portability, and range/size of detection.

RESULTS

Of the 2646 reviewed articles, 19 studies met the inclusion criteria and included the following modalities of noninvasive stoke detection: microwave technology (6 studies, 31.6%), electroencephalography (EEG; 4 studies, 21.1%), ultrasonography (3 studies, 15.8%), near-infrared spectroscopy (NIRS; 2 studies, 10.5%), portable MRI devices (2 studies, 10.5%), volumetric impedance phase-shift spectroscopy (VIPS; 1 study, 5.3%), and eddy current damping (1 study, 5.3%). Notable medical devices that accurately predicted stroke in this review were EEG-based diagnosis, with a maximum sensitivity of 91.7% for predicting a stroke, microwave-based diagnosis, with an area under the receiver operating characteristic curve (AUC) of 0.88 for differentiating ischemic stroke and intracerebral hemorrhage (ICH), ultrasound with an AUC of 0.92, VIPS with an AUC of 0.93, and portable MRI with a diagnostic accuracy similar to that of traditional MRI. NIRS offers significant potential for more superficially located hemorrhage but is limited in detecting deep-seated ICH (2.5-cm scanning depth).

CONCLUSIONS

As technology and computational resources have advanced, several novel point-of-care medical devices show promise in facilitating rapid stroke diagnosis, with the potential for improving time to treatment and informing prehospital stroke triage.

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Shane Shahrestani, Ben A. Strickland, Joshua Bakhsheshian, William J. Mack, Arthur W. Toga, Nerses Sanossian, Yu-Chong Tai, and Gabriel Zada

OBJECTIVE

Spontaneous intracerebral hemorrhage occurs in an estimated 10% of stroke patients, with high rates of associated mortality. Portable diagnostic technologies that can quickly and noninvasively detect hemorrhagic stroke may prevent unnecessary delay in patient care and help rapidly triage patients with ischemic versus hemorrhagic stroke. As such, the authors aimed to develop a rapid and portable eddy current damping (ECD) hemorrhagic stroke sensor for proposed in-field diagnosis of hemorrhagic stroke.

METHODS

A tricoil ECD sensor with microtesla-level magnetic field strengths was constructed. Sixteen gelatin brain models with identical electrical properties to live brain tissue were developed and placed within phantom skull replicas, and saline was diluted to the conductivity of blood and placed within the brain to simulate a hemorrhage. The ECD sensor was used to detect modeled hemorrhages on benchtop models. Data were saved and plotted as a filtered heatmap to represent the lesion location. The individuals performing the scanning were blinded to the bleed location, and sensors were tangentially rotated around the skull models to localize blood. Data were also used to create heatmap images using MATLAB software.

RESULTS

The sensor was portable (11.4-cm maximum diameter), compact, and cost roughly $100 to manufacture. Scanning time was 2.43 minutes, and heatmap images of the lesion were produced in near real time. The ECD sensor accurately predicted the location of a modeled hemorrhage in all (n = 16) benchtop experiments with excellent spatial resolution.

CONCLUSIONS

Benchtop experiments demonstrated the proof of concept of the ECD sensor for rapid transcranial hemorrhagic stroke diagnosis. Future studies with live human participants are warranted to fully establish the feasibility findings derived from this study.

Open access

Krista Lamorie-Foote, Shivani D. Rangwala, Alexandra Kammen, Esteban Gnass, Daniel R. Kramer, Martin Rutkowski, Ben A. Strickland, John D. Carmichael, and Gabriel Zada

BACKGROUND

Metastases to the central nervous system are often multiple in number and typically favor the gray-white matter junction. Collision tumors, defined as the coexistence of two morphologically different tumors, such as metastases to a known pituitary adenoma (PA), are exceedingly rare. Only a few reported cases of metastases to a PA exist in the literature.

OBSERVATIONS

The authors present the case of a 64-year-old man with a known history of stage IV metastatic melanoma who was found to have hypermetabolic activity in the sellar region on surveillance positron emission tomography. On laboratory evaluation, he had clear evidence of pituitary axis dysfunction without diabetes insipidus. Subsequent magnetic resonance imaging showed a 2.4-cm sellar mass with features of a pituitary macroadenoma and internal hemorrhage, although no clinical symptoms of apoplexy were noted. He underwent a transsphenoidal endoscopic endonasal approach for resection of the sellar lesion. Final pathology showed a collision tumor with melanoma cells intermixed with PA cells.

LESSONS

Histological analysis verified the rare presence of a collision tumor of a melanoma metastasis to a nonfunctional pituitary macroadenoma. Metastasis to a preexisting PA, although rare, should be considered in the differential diagnosis in patients with sellar lesions and a known cancer history.

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Ben A. Strickland, Shane Shahrestani, Robert G. Briggs, Anna Jackanich, Sherwin Tavakol, Kyle Hurth, Mark S. Shiroishi, Chia-Shang J. Liu, John D. Carmichael, Martin Weiss, and Gabriel Zada

OBJECTIVE

Silent corticotroph adenomas (SCAs) are a distinct subtype of nonfunctioning pituitary adenomas (NFAs) that demonstrate positive immunohistochemistry for adrenocorticotropic hormone (ACTH) without causing Cushing’s disease. SCAs are hypothesized to exhibit more aggressive behavior than standard NFAs. The authors analyzed their institution’s surgical experience with SCAs in an effort to characterize rates of invasion, postoperative clinical outcomes, and patterns of disease recurrence and progression. The secondary objectives were to define the best treatment strategies in the event of tumor recurrence and progression.

METHODS

A retrospective analysis of patients treated at the authors’ institution identified 100 patients with SCAs and 841 patients with NFAs of other subtypes who were treated surgically from 2000 to 2019. Patient demographics, tumor characteristics, surgical and neuroimaging data, rates of endocrinopathy, and neurological outcomes were recorded. Cohorts of patients with SCAs and patients with standard NFAs were compared with regard to these characteristics and outcomes.

RESULTS

The SCA cohort presented with cranial neuropathy (13% vs 5.7%, p = 0.0051) and headache (53% vs 42.3%, p = 0.042) compared to the NFA cohort, despite similar rates of apoplexy. The SCA cohort included a higher proportion of women (SCA 60% vs NFA 45.8%, p = 0.0071) and younger age at presentation (SCA 50.5 ± 13.3 vs NFA 54.6 ± 14.9 years of age, p = 0.0082). Reoperations were comparable between the cohorts (SCA 16% vs NFA 15.7%, p = 0.98). Preoperative pituitary function was comparable between the cohorts with the exception of higher rates of preoperative panhypopituitarism in NFA patients (2% vs 6.1%, respectively; p = 0.0033). The mean tumor diameter in SCA patients was 24 ± 10.8 mm compared to 26 ± 11.3 mm in NFA patients (p = 0.05). Rates of cavernous sinus invasion were higher in the SCA group (56% vs 49.7%), although this result did not reach statistical significance. There were no significant differences in extent of resection, intraoperative CSF leak rates, endocrine or neurological outcomes, or postoperative complications. Ki-67 rates were significantly increased in the SCA cohort (2.88 ± 2.79) compared to the NFA cohort (1.94 ± 1.99) (p = 0.015). Although no differences in overall rates of progression or recurrence were noted, SCAs had a significantly lower progression-free survival (24.5 vs 51.1 months, p = 0.0011). Among the SCA cohort, progression was noted despite the use of adjuvant radiosurgery in 33% (n = 4/12) of treated tumors. Adequate tumor control was not achieved in half (n = 6) of the SCA progression cohort despite radiosurgery or multiple resections.

CONCLUSIONS

In this study, to the authors’ knowledge the largest surgical series to assess outcomes in SCAs to date, the findings suggest that SCAs are more biologically aggressive tumors than standard NFAs. The progression-free survival duration of patients with SCAs is only about half that of patients with other NFAs. Therefore, close neuroimaging and clinical follow-up are warranted in patients with SCAs, and residual disease should be considered for early postoperative adjuvant radiosurgery, particularly in younger patients.

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Daniel A. Donoho, Dhiraj J. Pangal, Guillaume Kugener, Martin Rutkowski, Alexander Micko, Shane Shahrestani, Andrew Brunswick, Michael Minneti, Bozena B. Wrobel, and Gabriel Zada

OBJECTIVE

Internal carotid artery injury (ICAI) is a rare, life-threatening complication of endoscopic endonasal approaches that will be encountered by most skull base neurosurgeons and otolaryngologists. Rates of surgical proficiency for managing ICAI are not known, and the role of simulation to improve performance has not been studied on a nationwide scale.

METHODS

Attending and resident neurosurgery and otorhinolaryngology surgeons (n = 177) were recruited from multicenter regional and national training courses to assess training outcomes and validity at scale of a prospective educational intervention to improve surgeon technical skills using a previously validated, perfused human cadaveric simulator. Participants attempted an initial trial (T1) of simulated ICAI control using their preferred technique. An educational intervention including personalized instruction was performed. Participants attempted a second trial (T2). Task success (dichotomous), time to hemostasis (TTH), estimated blood loss (EBL), and surgeon heart rate were measured.

RESULTS

Participant rating scales confirmed that the simulation retained face and construct validity across eight instructional settings. Trial success (ICAI control) improved from 56% in T1 to 90% in T2 (p < 0.0001). EBL and TTH decreased by 37% and 38%, respectively (p < 0.0001). Postintervention resident surgeon performance (TTH, EBL, and success rate) was superior to preintervention attending surgeon performance. The most improved quartile of participants achieved 62% improvement in TTH and 73% improvement in EBL, with trial success improvement from 25.6% in T1 to 100% in T2 (p < 0.0001). Baseline surgeon confidence was uncorrelated with T1 success, while posttraining confidence correlated with T2 success. Tachycardia was measured in 57% of surgeon participants, but was attenuated during T2, consistent with development of resiliency.

CONCLUSIONS

Prior to training, many attending and most resident surgeons could not manage the rare, life-threatening intraoperative complication of ICAI. A simulated educational intervention significantly improved surgeon performance and remained valid when deployed at scale. Simulation also promoted the development of favorable cognitive skills (accurate perception of skill and resiliency). Rare, life-threatening intraoperative complications may be optimal targets for educational interventions using surgical simulation.