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Letter to the Editor. Sophisticated data acquisition and analytics in neurosurgery: beneficial but expect challenges

Nicolas I. Gonzalez-Romo and Mark C. Preul

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Interactive microsurgical anatomy education using photogrammetry 3D models and an augmented reality cube

Muhammet Enes Gurses, Nicolas I. Gonzalez-Romo, Yuan Xu, Giancarlo Mignucci-Jiménez, Sahin Hanalioglu, José E. Chang, Habib Rafka, Kerry A. Vaughan, Dilantha B. Ellegala, Michael T. Lawton, and Mark C. Preul

OBJECTIVE

This study sought to assess the use of an augmented reality (AR) tool for neurosurgical anatomical education.

METHODS

Three-dimensional models were created using advanced photogrammetry and registered onto a handheld AR foam cube imprinted with scannable quick response codes. A perspective analysis of the cube anatomical system was performed by loading a 3D photogrammetry model over a motorized turntable to analyze changes in the surgical window area according to the horizontal rotation. The use of the cube as an intraoperative reference guide for surgical trainees was tested during cadaveric dissection exercises. Neurosurgery trainees from international programs located in Ankara, Turkey; San Salvador, El Salvador; and Moshi, Tanzania, interacted with and assessed the 3D models and AR cube system and then completed a 17-item graded user experience survey.

RESULTS

Seven photogrammetry 3D models were created and imported to the cube. Horizontal turntable rotation of the cube translated to measurable and realistic perspective changes in the surgical window area. The combined 3D models and cube system were used to engage trainees during cadaveric dissections, with satisfactory user experience. Thirty-five individuals (20 from Turkey, 10 from El Salvador, and 5 from Tanzania) agreed that the cube system could enhance the learning experience for neurosurgical anatomy.

CONCLUSIONS

The AR cube combines tactile and visual sensations with high-resolution 3D models of cadaveric dissections. Inexpensive and lightweight, the cube can be effectively implemented to allow independent co-visualization of anatomical dissection and can potentially supplement neurosurgical education.

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Infragalenic triangle as a gateway to dorsal midbrain and posteromedial thalamic lesions: descriptive and quantitative analysis of microsurgical anatomy

Sahin Hanalioglu, Muhammet Enes Gurses, Giancarlo Mignucci-Jiménez, Nicolas I. González-Romo, Ethan A. Winkler, Mark C. Preul, and Michael T. Lawton

OBJECTIVE

Anatomical triangles provide neurosurgeons with the specificity required to access deep targets, supplementing more general instructions, such as craniotomy and approach. The infragalenic triangle (IGT), bordered by the basal vein of Rosenthal (BVR), precentral cerebellar vein (PCV), and the quadrangular lobule of the cerebellum, is one of a system of anatomical triangles recently introduced to guide dissection to brainstem cavernous malformations and has not been described in detail. This study aimed to quantitatively analyze the anatomical parameters of the IGT and present key nuances for its microsurgical use.

METHODS

A midline supracerebellar infratentorial (SCIT) approach through a torcular craniotomy was performed on 5 cadaveric heads, and the IGT was identified in each specimen bilaterally. Anatomical measurements were obtained with point coordinates collected using neuronavigation. Three cadaveric brains were used to illustrate relevant brainstem anatomy, and 3D virtual modeling was used to simulate various perspectives of the IGT through different approach angles. In addition, 2 illustrative surgical cases are presented.

RESULTS

The longest edge of the IGT was the lateral edge formed by the BVR (mean ± SD length 19.1 ± 2.3 mm), and the shortest edge was the medial edge formed by the PCV (13.9 ± 3.6 mm). The mean surface area of the IGT was 110 ± 34.2 mm2 in the standard exposure. Full expansion of all 3 edges (arachnoid dissection, mobilization, and retraction) resulted in a mean area of 226.0 ± 48.8 mm2 and a 2.5-times increase in surface area exposure of deep structures (e.g., brainstem and thalamus). Thus, almost the entire tectal plate and its relevant safe entry zones can be exposed through an expanded unilateral IGT except for the contralateral inferior colliculus, access to which is usually hindered by PCV tributaries. Exposure of bilateral IGTs may be required to resect larger midline lesions to increase surgical maneuverability or to access the contralateral pulvinar.

CONCLUSIONS

The IGT provides a safe access route to the dorsal midbrain and reliable intraoperative guidance in the deep and complex anatomy of the posterior tentorial incisura. Its potential for expansion makes it a versatile anatomical corridor not only for intrinsic brainstem lesions but also for tumors and vascular malformations of the pineal region, dorsal midbrain, and posteromedial thalamus.

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Intraoperative in vivo confocal laser endomicroscopy imaging at glioma margins: can we detect tumor infiltration?

Yuan Xu, Andrea M. Mathis, Bianca Pollo, Jürgen Schlegel, Theoni Maragkou, Kathleen Seidel, Philippe Schucht, Kris A. Smith, Randall W. Porter, Andreas Raabe, Andrew S. Little, Nader Sanai, Dennis C. Agbanyim, Nikolay L. Martirosyan, Jennifer M. Eschbacher, Karl Quint, Mark C. Preul, and Ekkehard Hewer

OBJECTIVE

Confocal laser endomicroscopy (CLE) is a US Food and Drug Administration–cleared intraoperative real-time fluorescence-based cellular resolution imaging technology that has been shown to image brain tumor histoarchitecture rapidly in vivo during neuro-oncological surgical procedures. An important goal for successful intraoperative implementation is in vivo use at the margins of infiltrating gliomas. However, CLE use at glioma margins has not been well studied.

METHODS

Matching in vivo CLE images and tissue biopsies acquired at glioma margin regions of interest (ROIs) were collected from 2 institutions. All images were reviewed by 4 neuropathologists experienced in CLE. A scoring system based on the pathological features was implemented to score CLE and H&E images from each ROI on a scale from 0 to 5. Based on the H&E scores, all ROIs were divided into a low tumor probability (LTP) group (scores 0–2) and a high tumor probability (HTP) group (scores 3–5). The concordance between CLE and H&E scores regarding tumor probability was determined. The intraclass correlation coefficient (ICC) and diagnostic performance were calculated.

RESULTS

Fifty-six glioma margin ROIs were included for analysis. Interrater reliability of the scoring system was excellent when used for H&E images (ICC [95% CI] 0.91 [0.86–0.94]) and moderate when used for CLE images (ICC [95% CI] 0.69 [0.40–0.83]). The ICCs (95% CIs) of the LTP group (0.68 [0.40–0.83]) and HTP group (0.68 [0.39–0.83]) did not differ significantly. The concordance between CLE and H&E scores was 61.6%. The sensitivity and specificity values of the scoring system were 79% and 37%. The positive predictive value (PPV) and negative predictive value were 65% and 53%, respectively. Concordance, sensitivity, and PPV were greater in the HTP group than in the LTP group. Specificity was higher in the newly diagnosed group than in the recurrent group.

CONCLUSIONS

CLE may detect tumor infiltration at glioma margins. However, it is not currently dependable, especially in scenarios where low probability of tumor infiltration is expected. The proposed scoring system has excellent intrinsic interrater reliability, but its interrater reliability is only moderate when used with CLE images. These results suggest that this technology requires further exploration as a method for consistent actionable intraoperative guidance with high dependability across the range of tumor margin scenarios. Specific-binding and/or tumor-specific fluorophores, a CLE image atlas, and a consensus guideline for image interpretation may help with the translational utility of CLE.

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The biportal transorbital approach: quantitative comparison of the anterior subfrontal craniotomy, bilateral transorbital endoscopic, and microscopic approaches

Lena Mary Houlihan, Thanapong Loymak, Irakliy Abramov, Jubran H. Jubran, Ann J. Staudinger Knoll, Jacob T. Howshar, Michael G. J. O’Sullivan, Michael T. Lawton, and Mark C. Preul

OBJECTIVE

The aim of this study was to assess the surgical use and applicability of a biportal bitransorbital approach. Single-portal transorbital and combined transorbital transnasal approaches have been used in clinical practice, but no study has assessed the surgical use and applicability of a biportal bitransorbital approach.

METHODS

Ten cadaver specimens underwent midline anterior subfrontal (ASub), bilateral transorbital microsurgery (bTMS), and bilateral transorbital neuroendoscopic surgery (bTONES) approaches. Morphometric analyses included the length of the bilateral cranial nerves I and II, the optic tract, and A1; the area of exposure of the anterior cranial fossa floor; craniocaudal and mediolateral angles of attack (AOAs); and volume of surgical freedom (VSF; maximal available working volume for a specific surgical corridor and surgical target structure normalized to a height of 10 mm) of the bilateral paraclinoid internal carotid arteries (ICAs), bilateral terminal ICAs, and anterior communicating artery (ACoA). Analyses were conducted to determine whether the biportal approach was associated with greater instrument freedom.

RESULTS

The bTMS and bTONES approaches provided limited access to the bilateral A1 segments and the ACoA, which were inaccessible in 30% (bTMS) and 60% (bTONES) of exposures. The average total frontal lobe area of exposure (AOE) was 1648.4 mm2 (range 1516.6–1958.8 mm2) for ASub, 1658.9 mm2 (1274.6–1988.2 mm2) for bTMS, and 1914.9 mm2 (1834.2–2014.2 mm2) for bTONES exposures, with no statistically significant superiority between any of the 3 approaches (p = 0.28). The bTMS and bTONES approaches were significantly associated with decreases of 8.7 mm3 normalized volume (p = 0.005) and 14.3 mm3 normalized volume (p < 0.001) for VSF of the right paraclinoid ICA compared with the ASub approach. No statistically significant difference in surgical freedom was noted between all 3 approaches when targeting the bilateral terminal ICA. The bTONES approach was significantly associated with a decrease of 105% in the (log) VSF of the ACoA compared with the ASub (p = 0.009).

CONCLUSIONS

Although the biportal approach is intended to improve maneuverability within these minimally invasive approaches, these results illustrate the pertinent issue of surgical corridor crowding and the importance of surgical trajectory planning. A biportal transorbital approach provides improved visualization but does not improve surgical freedom. Furthermore, although it affords impressive anterior cranial fossa AOE, it is unsuitable for addressing midline lesions because the preserved orbital rim restricts lateral movement. Further comparative studies will elucidate whether a combined transorbital transnasal route is preferable to minimize skull base destruction and maximize instrument access.

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Quantification of motion during microvascular anastomosis simulation using machine learning hand detection

Nicolas I. Gonzalez-Romo, Sahin Hanalioglu, Giancarlo Mignucci-Jiménez, Grant Koskay, Irakliy Abramov, Yuan Xu, Wonhyoung Park, Michael T. Lawton, and Mark C. Preul

OBJECTIVE

Microanastomosis is one of the most technically demanding and important microsurgical skills for a neurosurgeon. A hand motion detector based on machine learning tracking technology was developed and implemented for performance assessment during microvascular anastomosis simulation.

METHODS

A microanastomosis motion detector was developed using a machine learning model capable of tracking 21 hand landmarks without physical sensors attached to a surgeon’s hands. Anastomosis procedures were simulated using synthetic vessels, and hand motion was recorded with a microscope and external camera. Time series analysis was performed to quantify the economy, amplitude, and flow of motion using data science algorithms. Six operators with various levels of technical expertise (2 experts, 2 intermediates, and 2 novices) were compared.

RESULTS

The detector recorded a mean (SD) of 27.6 (1.8) measurements per landmark per second with a 10% mean loss of tracking for both hands. During 600 seconds of simulation, the 4 nonexperts performed 26 bites in total, with a combined excess of motion of 14.3 (15.5) seconds per bite, whereas the 2 experts performed 33 bites (18 and 15 bites) with a mean (SD) combined excess of motion of 2.8 (2.3) seconds per bite for the dominant hand. In 180 seconds, the experts performed 13 bites, with mean (SD) latencies of 22.2 (4.4) and 23.4 (10.1) seconds, whereas the 2 intermediate operators performed a total of 9 bites with mean (SD) latencies of 31.5 (7.1) and 34.4 (22.1) seconds per bite.

CONCLUSIONS

A hand motion detector based on machine learning technology allows the identification of gross and fine movements performed during microanastomosis. Economy, amplitude, and flow of motion were measured using time series data analysis. Technical expertise could be inferred from such quantitative performance analysis.

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Erratum. Artery of Uchimura: origin and evolution of identification of the vascular supply to the hippocampus

Mark C. Preul

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Artery of Uchimura: origin and evolution of identification of the vascular supply to the hippocampus

Ali Tayebi Meybodi, Giancarlo Mignucci-Jiménez, Yuan Xu, and Mark C. Preul

In 1928, neuroscientist Yushi Uchimura (1897–1980) published a landmark study detailing the hippocampal vasculature. Working in Walther Spielmeyer’s Munich laboratory (1925–1927), Uchimura sought evidence for a vascular theory of Ammon’s horn sclerosis (AHS). He described an artery supplying the vulnerable sector of the hippocampus, where pathognomonic changes of AHS were noted, and characterized the artery as particularly susceptible to circulatory disturbances. Discovery of this artery led to new concepts and new terminology pertaining to the hippocampus. In addition to having a distinguished career in psychiatry and academia (including a position as University of Tokyo dean), Uchimura was, before attending medical school, one of Japan’s best baseball pitchers; he was eventually named Nippon Professional Baseball Organization commissioner and inducted into the Japan Baseball Hall of Fame. Uchimura’s description of hippocampal vasculature, which is still subject to debate after nearly a century, brought international attention to AHS and epilepsy and showed the hippocampal vasculature to be variable and vulnerable; important considerations for later neurosurgeons in the development of selective mesial temporal surgery. Prominent figures in neurosurgery have since developed classification systems for the hippocampal vasculature in which the artery of Uchimura remains central. Perhaps no other brain artery has been the nexus for such intense investigation and debate about its association to structure, function, disease, and treatment methodology.

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Combined subtarsal contralateral transmaxillary retroeustachian and endoscopic endonasal approaches to the infrapetrous region

Mohamed A. Labib, Irakliy Abramov, Lena Mary Houlihan, Visish M. Srinivasan, Lea Scherschinski, Daniel M. Prevedello, Ricardo L. Carrau, Hussam Abou-Al-Shaar, Mark C. Preul, and Michael T. Lawton

OBJECTIVE

The eustachian tube (ET) limits endoscopic endonasal access to the infrapetrous region. Transecting or mobilizing the ET may result in morbidities. This study presents a novel approach in which a subtarsal contralateral transmaxillary (ST-CTM) corridor is coupled with the standard endonasal approach to facilitate access behind the intact ET.

METHODS

Eight cadaveric head specimens were dissected. Endoscopic endonasal approaches (EEAs) (i.e., transpterygoid and inferior transclival) were performed on one side, followed by ST-CTM and sublabial contralateral transmaxillary (SL-CTM) approaches on the opposite side, along with different ET mobilization techniques on the original side. Seven comparative groups were generated. The length of the cranial nerves, areas of exposure, and volume of surgical freedom (VSF) in the infrapetrous regions were measured and compared.

RESULTS

Without ET mobilization, the combined ST-CTM/EEA approach provided greater exposure than EEA alone (mean ± SD 288.9 ± 40.66 mm2 vs 91.7 ± 49.9 mm2; p = 0.001). The VSFs at the ventral jugular foramen (JF), entrance to the petrous internal carotid artery (ICA), and lateral to the parapharyngeal ICA were also greater in ST-CTM/EEA than in EEA alone (p = 0.002, p = 0.002, and p < 0.001, respectively). EEA alone, however, provided greater VSF at the hypoglossal canal (HGC) than did ST-CTM/EEA (p = 0.01). The SL-CTM approach did not increase the EEA exposure (p = 0.48). The ST-CTM/EEA approach provided greater exposure than EEA with extended inferolateral (EIL) or anterolateral (AL) ET mobilization (p = 0.001 and p = 0.02, respectively). The ST-CTM/EEA also increased the VSF lateral to the parapharyngeal ICA in comparison with EEA/EIL ET mobilization (p < 0.001) but not with EEA/AL ET mobilization (p = 0.36). Finally, the VSFs at the HGC and JF were greater in EEA/AL ET mobilization than in ST-CTM/EEA without ET mobilization (p = 0.002 and p = 0.004, respectively).

CONCLUSIONS

Combining the EEA with the more laterally and superiorly originating ST-CTM approach allows greater exposure of the infrapetrous and ventral JF regions while obviating the need for mobilizing the ET. The surgical freedom afforded by the combined approaches is greater than that obtained by EEA alone.

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Introduction. On forging a new specialty from the crucible of war

Charles J. Prestigiacomo, Mark C. Preul, T. Forcht Dagi, Chris J. Neal, Jeffrey V. Rosenfeld, and Melissa Meister