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The endoscopic endonasal eustachian tube anterolateral mobilization strategy: minimizing the cost of the extreme-medial approach

Mohamed A. Labib, Evgenii Belykh, Claudio Cavallo, Xiaochun Zhao, Daniel M. Prevedello, Ricardo L. Carrau, Andrew S. Little, Mauro A. T. Ferreira, Mark C. Preul, A. Samy Youssef, and Peter Nakaji

OBJECTIVE

The ventral jugular foramen and the infrapetrous region are difficult to access through conventional lateral and posterolateral approaches. Endoscopic endonasal approaches to this region are obstructed by the eustachian tube (ET). This study presents a novel strategy for mobilizing the ET while preserving its integrity. Qualitative and quantitative comparisons with previous ET management paradigms are also presented.

METHODS

Ten dry skulls were analyzed. Four ET management strategies were sequentially performed on a total of 6 sides of cadaveric head specimens. Four measurement groups were generated: in group A, the ET was intact and not mobilized; in group B, the ET was mobilized inferolaterally; in group C, the ET underwent anterolateral mobilization; and in group D, the ET was resected. ET range of mobilization, surgical exposure area, and surgical freedom were measured and compared among the groups.

RESULTS

Wide exposure of the infrapetrous region and jugular foramen was achieved by removing the pterygoid process, unroofing the cartilaginous ET up to the level of the posterior aspect of the foramen ovale, and detaching the ET from the skull base and soft palate. Anterolateral mobilization of the ET facilitated significantly more retraction (a 126% increase) of the ET than inferolateral mobilization (mean ± SD: 20.8 ± 11.2 mm vs 9.2 ± 3.6 mm [p = 0.02]). Compared with group A, groups C and D had enhanced surgical exposure (142.5% [1176.9 ± 935.7 mm2] and 155.9% [1242.0 ± 1096.2 mm2], respectively, vs 485.4 ± 377.6 mm2 for group A [both p = 0.02]). Furthermore, group C had a significantly larger surgical exposure area than group B (p = 0.02). No statistically significant difference was found between the area of exposure obtained by ET removal and anterolateral mobilization. Anterolateral mobilization of the ET resulted in a 39.5% increase in surgical freedom toward the exocranial jugular foramen compared with that obtained through inferolateral mobilization of the ET (67.2° ± 20.5° vs 48.1° ± 6.7° [p = 0.047]) and a 65.4% increase compared with that afforded by an intact ET position (67.2° ± 20.5° vs 40.6° ± 14.3° [p = 0.03]).

CONCLUSIONS

Anterolateral mobilization of the ET provides excellent access to the ventral jugular foramen and infrapetrous region. The surgical exposure obtained is superior to that achieved with other ET management strategies and is comparable to that obtained by ET resection.

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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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Function and organization in dysgenic cortex

Case report

Mark C. Preul, Richard Leblanc, Fernando Cendes, Francois Dubeau, David Reutens, Roberto Spreafico, Giorgio Battaglia, Massimo Avoli, Pierre Langevin, Douglas L. Arnold, and Jean-Guy Villemure

✓ Cerebral dysgenesis is a subject of interest because of its relationship to cerebral development and dysfunction and to epilepsy. The authors present a detailed study of a 16-year-old boy who underwent surgery for a severe seizure disorder. This patient had dysgenesis of the right hemisphere, which was composed of a giant central frontoparietal nodular gray matter heterotopia with overlying large islands of cortical dysplasia around a displaced central fissure. Exceptional insight into the function, biochemistry, electrophysiology, and histological structure of this lesion was obtained from neurological studies that revealed complementary information: magnetic resonance (MR) imaging, [18]fluoro-2-deoxy-d-glucose positron emission tomography (PET), functional PET scanning, proton MR spectroscopic (1H-MRS) imaging, intraoperative cortical mapping and electrocorticography, in vitro electrophysiology, and immunocytochemistry. These studies demonstrated compensatory cortical reorganization and showed that large areas of heterotopia and cortical dysplasia in the central area may retain normal motor and sensory function despite strikingly altered cytoarchitectonic organization and neuronal metabolism. Such lesions necessitate appropriate functional imaging studies prior to surgery and cortical mapping to avoid creating neurological deficits. Integrated studies, such as PET, 1H-MRS imaging, cortical mapping, immunocytochemistry, and electrophysiology may provide information on the function of developmental disorders of cerebral organization.

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Low-flow and high-flow neurosurgical bypass and anastomosis training models using human and bovine placental vessels: a histological analysis and validation study

Evgenii Belykh, Ting Lei, Sam Safavi-Abbasi, Kaan Yagmurlu, Rami O. Almefty, Hai Sun, Kaith K. Almefty, Olga Belykh, Vadim A. Byvaltsev, Robert F. Spetzler, Peter Nakaji, and Mark C. Preul

OBJECTIVE

Microvascular anastomosis is a basic neurosurgical technique that should be mastered in the laboratory. Human and bovine placentas have been proposed as convenient surgical practice models; however, the histologic characteristics of these tissues have not been compared with human cerebral vessels, and the models have not been validated as simulation training models. In this study, the authors assessed the construct, face, and content validities of microvascular bypass simulation models that used human and bovine placental vessels.

METHODS

The characteristics of vessel segments from 30 human and 10 bovine placentas were assessed anatomically and histologically. Microvascular bypasses were performed on the placenta models according to a delineated training module by “trained” participants (10 practicing neurosurgeons and 7 residents with microsurgical experience) and “untrained” participants (10 medical students and 3 residents without experience). Anastomosis performance and impressions of the model were assessed using the Northwestern Objective Microanastomosis Assessment Tool (NOMAT) scale and a posttraining survey.

RESULTS

Human placental arteries were found to approximate the M2–M4 cerebral and superficial temporal arteries, and bovine placental veins were found to approximate the internal carotid and radial arteries. The mean NOMAT performance score was 37.2 ± 7.0 in the untrained group versus 62.7 ± 6.1 in the trained group (p < 0.01; construct validity). A 50% probability of allocation to either group corresponded to 50 NOMAT points. In the posttraining survey, 16 of 17 of the trained participants (94%) scored the model's replication of real bypass surgery as high, and 16 of 17 (94%) scored the difficulty as “the same” (face validity). All participants, 30 of 30 (100%), answered positively to questions regarding the ability of the model to improve microsurgical technique (content validity).

CONCLUSIONS

Human placental arteries and bovine placental veins are convenient, anatomically relevant, and beneficial models for microneurosurgical training. Microanastomosis simulation using these models has high face, content, and construct validities. A NOMAT score of more than 50 indicated successful performance of the microanastomosis tasks.

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Letter to the Editor: Screw fixation technique

Paul A. Gardner, Juan C. Fernandez-Miranda, Carl H. Snyderman, and Eric W. Wang

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Endogenous stem cell proliferation induced by intravenous hedgehog agonist administration after contusion in the adult rat spinal cord

Laboratory investigation

Nicholas C. Bambakidis, Eric M. Horn, Peter Nakaji, Nicholas Theodore, Elizabeth Bless, Tammy Dellovade, Chiyuan Ma, Xukui Wang, Mark C. Preul, Stephen W. Coons, Robert F. Spetzler, and Volker K. H. Sonntag

Object

Sonic hedgehog (Shh) is a glycoprotein molecule that upregulates the transcription factor Gli1. The Shh protein plays a critical role in the proliferation of endogenous neural precursor cells when directly injected into the spinal cord after a spinal cord injury in adult rodents. Small-molecule agonists of the hedgehog (Hh) pathway were used in an attempt to reproduce these findings through intravenous administration.

Methods

The expression of Gli1 was measured in rat spinal cord after the intravenous administration of an Hh agonist. Ten adult rats received a moderate contusion and were treated with either an Hh agonist (10 mg/kg, intravenously) or vehicle (5 rodents per group) 1 hour and 4 days after injury. The rats were killed 5 days postinjury. Tissue samples were immediately placed in fixative. Samples were immunohistochemically stained for neural precursor cells, and these cells were counted.

Results

Systemic dosing with an Hh agonist significantly upregulated Gli1 expression in the spinal cord (p < 0.005). After spinal contusion, animals treated with the Hh agonist had significantly more nestin-positive neural precursor cells around the rim of the lesion cavity than in vehicle-treated controls (means ± SDs, 46.9 ± 12.9 vs 20.9 ± 8.3 cells/hpf, respectively, p < 0.005). There was no significant difference in the area of white matter injury between the groups.

Conclusions

An intravenous Hh agonist at doses that upregulate spinal cord Gli1 transcription also increases the population of neural precursor cells after spinal cord injury in adult rats. These data support previous findings based on injections of Shh protein directly into the spinal cord.

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Comparative anatomical analysis of the transcallosal-transchoroidal and transcallosal-transforniceal-transchoroidal approaches to the third ventricle

João Luiz Vitorino Araujo, José C. E. Veiga, Hung Tzu Wen, Almir F. de Andrade, Manoel J. Teixeira, José P. Otoch, Albert L. Rhoton Jr., Mark C. Preul, Robert F. Spetzler, and Eberval G. Figueiredo

OBJECTIVE

Access to the third ventricle is a veritable challenge to neurosurgeons. In this context, anatomical and morphometric studies are useful for establishing the limitations and advantages of a particular surgical approach. The transchoroidal approach is versatile and provides adequate exposure of the middle and posterior regions of the third ventricle. However, the fornix column limits the exposure of the anterior region of the third ventricle. There is evidence that the unilateral section of the fornix column has little effect on cognitive function. This study compared the anatomical exposure afforded by the transforniceal-transchoroidal approach with that of the transchoroidal approach. In addition, a morphometric evaluation of structures that are relevant to and common in the 2 approaches was performed.

METHODS

The anatomical exposure provided by the transcallosal-transchoroidal and transcallosal-transforniceal-transchoroidal approaches was compared in 8 fresh cadavers, using a neuronavigation system. The working area, microsurgical exposure area, and angular exposure on the longitudinal and transversal planes of 2 anatomical targets (tuber cinereum and cerebral aqueduct) were compared. Additionally, the thickness of the right frontal lobe parenchyma, thickness of the corpus callosum trunk, and longitudinal diameter of the interventricular foramen were measured. The values obtained were submitted to statistical analysis using the Wilcoxon test.

RESULTS

In the quantitative evaluation, compared with the transchoroidal approach, the transforniceal-transchoroidal approach provided a greater mean working area (transforniceal-transchoroidal 150 ± 11 mm2; transchoroidal 121 ± 8 mm2; p < 0.05), larger mean microsurgical exposure area (transforniceal-transchoroidal 101 ± 9 mm2; transchoroidal 80 ± 5 mm2; p < 0.05), larger mean angular exposure area on the longitudinal plane for the tuber cinereum (transforniceal-transchoroidal 71° ± 7°; transchoroidal 64° ± 6°; p < 0.05), and larger mean angular exposure area on the longitudinal plane for the cerebral aqueduct (transforniceal-transchoroidal 62° ± 6°; transchoroidal 55° ± 5°; p < 0.05). No differences were observed in angular exposure along the transverse axis for either anatomical target (tuber cinereum and cerebral aqueduct; p > 0.05). The mean thickness of the right frontal lobe parenchyma was 35 ± 3 mm, the mean thickness of the corpus callosum trunk was 10 ± 1 mm, and the mean longitudinal diameter of the interventricular foramen was 4.6 ± 0.4 mm. In the qualitative assessment, it was noted that the transforniceal-transchoroidal approach led to greater exposure of the third ventricle anterior region structures. There was no difference between approaches in the exposure of the structures of the middle and posterior region.

CONCLUSIONS

The transforniceal-transchoroidal approach provides greater surgical exposure of the third ventricle anterior region than that offered by the transchoroidal approach. In the population studied, morphometric analysis established mean values for anatomical structures common to both approaches.

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Intraoperative confocal laser endomicroscopy: prospective in vivo feasibility study of a clinical-grade system for brain tumors

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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Comparative anatomical analysis of the transcallosal-transchoroidal and transcallosal-transforniceal-transchoroidal approaches to the third ventricle

João Luiz Vitorino Araujo, José C. E. Veiga, Hung Tzu Wen, Almir F. de Andrade, Manoel J. Teixeira, José P. Otoch, Albert L. Rhoton Jr., Mark C. Preul, Robert F. Spetzler, and Eberval G. Figueiredo

OBJECTIVE

Access to the third ventricle is a veritable challenge to neurosurgeons. In this context, anatomical and morphometric studies are useful for establishing the limitations and advantages of a particular surgical approach. The transchoroidal approach is versatile and provides adequate exposure of the middle and posterior regions of the third ventricle. However, the fornix column limits the exposure of the anterior region of the third ventricle. There is evidence that the unilateral section of the fornix column has little effect on cognitive function. This study compared the anatomical exposure afforded by the transforniceal-transchoroidal approach with that of the transchoroidal approach. In addition, a morphometric evaluation of structures that are relevant to and common in the 2 approaches was performed.

METHODS

The anatomical exposure provided by the transcallosal-transchoroidal and transcallosal-transforniceal-transchoroidal approaches was compared in 8 fresh cadavers, using a neuronavigation system. The working area, microsurgical exposure area, and angular exposure on the longitudinal and transversal planes of 2 anatomical targets (tuber cinereum and cerebral aqueduct) were compared. Additionally, the thickness of the right frontal lobe parenchyma, thickness of the corpus callosum trunk, and longitudinal diameter of the interventricular foramen were measured. The values obtained were submitted to statistical analysis using the Wilcoxon test.

RESULTS

In the quantitative evaluation, compared with the transchoroidal approach, the transforniceal-transchoroidal approach provided a greater mean working area (transforniceal-transchoroidal 150 ± 11 mm2; transchoroidal 121 ± 8 mm2; p < 0.05), larger mean microsurgical exposure area (transforniceal-transchoroidal 101 ± 9 mm2; transchoroidal 80 ± 5 mm2; p < 0.05), larger mean angular exposure area on the longitudinal plane for the tuber cinereum (transforniceal-transchoroidal 71° ± 7°; transchoroidal 64° ± 6°; p < 0.05), and larger mean angular exposure area on the longitudinal plane for the cerebral aqueduct (transforniceal-transchoroidal 62° ± 6°; transchoroidal 55° ± 5°; p < 0.05). No differences were observed in angular exposure along the transverse axis for either anatomical target (tuber cinereum and cerebral aqueduct; p > 0.05). The mean thickness of the right frontal lobe parenchyma was 35 ± 3 mm, the mean thickness of the corpus callosum trunk was 10 ± 1 mm, and the mean longitudinal diameter of the interventricular foramen was 4.6 ± 0.4 mm. In the qualitative assessment, it was noted that the transforniceal-transchoroidal approach led to greater exposure of the third ventricle anterior region structures. There was no difference between approaches in the exposure of the structures of the middle and posterior region.

CONCLUSIONS

The transforniceal-transchoroidal approach provides greater surgical exposure of the third ventricle anterior region than that offered by the transchoroidal approach. In the population studied, morphometric analysis established mean values for anatomical structures common to both approaches.

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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.