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Robert Lynagh, Mark Ishak, Joseph Georges, Danielle Lopez, Hany Osman, Michael Kakareka, Brandon Boyer, H. Warren Goldman, Jennifer Eschbacher, Mark C. Preul, Peter Nakaji, Alan Turtz, Steven Yocom and Denah Appelt

OBJECTIVE

Accurate histopathological diagnoses are often necessary for treating neuro-oncology patients. However, stereotactic biopsy (STB), a common method for obtaining suspicious tissue from deep or eloquent brain regions, fails to yield diagnostic tissue in some cases. Failure to obtain diagnostic tissue can delay initiation of treatment and may result in further invasive procedures for patients. In this study, the authors sought to determine if the coupling of in vivo optical imaging with an STB system is an effective method for identification of diagnostic tissue at the time of biopsy.

METHODS

A minimally invasive fiber optic imaging system was developed by coupling a 0.65-mm-diameter coherent fiber optic fluorescence microendoscope to an STB system. Human U251 glioma cells were transduced for stable expression of blue fluorescent protein (BFP) to produce U251-BFP cells that were utilized for in vitro and in vivo experiments. In vitro, blue fluorescence was confirmed, and tumor cell delineation by fluorescein sodium (FNa) was quantified with fluorescence microscopy. In vivo, transgenic athymic rats implanted with U251-BFP cells (n = 4) were utilized for experiments. Five weeks postimplantation, the rats received 5–10 mg/kg intravenous FNa and underwent craniotomies overlying the tumor implantation site and contralateral normal brain. A clinical STB needle containing our 0.65-mm imaging fiber was passed through each craniotomy and images were collected. Fluorescence images from regions of interest ipsilateral and contralateral to tumor implantation were obtained and quantified.

RESULTS

Live-cell fluorescence imaging confirmed blue fluorescence from transduced tumor cells and revealed a strong correlation between tumor cells quantified by blue fluorescence and FNa contrast (R2 = 0.91, p < 0.001). Normalized to background, in vivo FNa-mediated fluorescence intensity was significantly greater from tumor regions, verified by blue fluorescence, compared to contralateral brain in all animals (301.7 ± 34.18 relative fluorescence units, p < 0.001). Fluorescence intensity measured from the tumor margin was not significantly greater than that from normal brain (p = 0.89). Biopsies obtained from regions of strong fluorescein contrast were histologically consistent with tumor.

CONCLUSIONS

The authors found that in vivo fluorescence imaging with an STB needle containing a submillimeter-diameter fiber optic fluorescence microendoscope provided direct visualization of neoplastic tissue in an animal brain tumor model prior to biopsy. These results were confirmed in vivo with positive control cells and by post hoc histological assessment. In vivo fluorescence guidance may improve the diagnostic yield of stereotactic biopsies.

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Evgenii Belykh, Kaan Yağmurlu, Ting Lei, Sam Safavi-Abbasi, Mark E. Oppenlander, Nikolay L. Martirosyan, Vadim A. Byvaltsev, Robert F. Spetzler, Peter Nakaji and Mark C. Preul

OBJECTIVE

The best approach to deep-seated lateral and third ventricle lesions is a function of lesion characteristics, location, and relationship to the ventricles. The authors sought to examine and compare angles of attack and surgical freedom of anterior ipsilateral and contralateral interhemispheric transcallosal approaches to the frontal horn of the lateral ventricle using human cadaveric head dissections. Illustrative clinical experiences with a contralateral interhemispheric transcallosal approach and an anterior interhemispheric transcallosal transchoroidal approach are also related.

METHODS

Five formalin-fixed human cadaveric heads (10 sides) were examined microsurgically. CT and MRI scans obtained before dissection were uploaded and fused into the navigation system. The authors performed contralateral and ipsilateral transcallosal approaches to the lateral ventricle. Using the navigation system, they measured areas of exposure, surgical freedom, angles of attack, and angle of view to the surgical surface. Two clinical cases are described.

RESULTS

The exposed areas of the ipsilateral (mean [± SD] 313.8 ± 85.0 mm2) and contralateral (344 ± 87.73 mm2) interhemispheric approaches were not significantly different (p = 0.12). Surgical freedom and vertical angles of attack were significantly larger for the contralateral approach to the most midsuperior reachable point (p = 0.02 and p = 0.01, respectively) and to the posterosuperior (p = 0.02 and p = 0.04) and central (p = 0.04 and p = 0.02) regions of the lateral wall of the lateral ventricle. Surgical freedom and vertical angles of attack to central and anterior points on the floor of the lateral ventricle did not differ significantly with approach. The angle to the surface of the caudate head region was less steep for the contralateral (135.6° ± 15.6°) than for the ipsilateral (152.0° ± 13.6°) approach (p = 0.02).

CONCLUSIONS

The anterior contralateral interhemispheric transcallosal approach provided a more expansive exposure to the lower two-thirds of the lateral ventricle and striothalamocapsular region. In normal-sized ventricles, the foramen of Monro and the choroidal fissure were better visualized through the lateral ventricle ipsilateral to the craniotomy than through the contralateral approach.

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Michael A. Mooney, Joseph Georges, Mohammedhassan Izady Yazdanabadi, Katherine Y. Goehring, William L. White, Andrew S. Little, Mark C. Preul, Stephen W. Coons, Peter Nakaji and Jennifer M. Eschbacher

OBJECTIVE

The objective of this study was to evaluate the feasibility of using confocal reflectance microscopy (CRM) ex vivo to differentiate adenoma from normal pituitary gland in surgical biopsy specimens. CRM allows for rapid, label-free evaluation of biopsy specimens with cellular resolution while avoiding some limitations of frozen section analysis.

METHODS

Biopsy specimens from 11 patients with suspected pituitary adenomas were transported directly to the pathology department. Samples were immediately positioned and visualized with CRM using a confocal microscope located in the same area of the pathology department where frozen sections are prepared. An H & E–stained slide was subsequently prepared from imaged tissue. A neuropathologist compared the histopathological characteristics of the H & E–stained slide and the matched CRM images. A second neuropathologist reviewed images in a blinded fashion and assigned diagnoses of adenoma or normal gland.

RESULTS

For all specimens, CRM contrasted cellularity, tissue architecture, nuclear pleomorphism, vascularity, and stroma. Pituitary adenomas demonstrated sheets and large lobules of cells, similar to the matched H & E–stained slides. CRM images of normal tissue showed scattered small lobules of pituitary epithelial cells, consistent with matched H & E–stained images of normal gland. Blinded review by a neuropathologist confirmed the diagnosis in 15 (94%) of 16 images of adenoma versus normal gland.

CONCLUSIONS

CRM is a simple, reliable approach for rapidly evaluating pituitary adenoma specimens ex vivo. This technique can be used to accurately differentiate between pituitary adenoma and normal gland while preserving biopsy tissue for future permanent analysis, immunohistochemical studies, and molecular studies.

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Kaan Yagmurlu, Sam Safavi-Abbasi, Evgenii Belykh, M. Yashar S. Kalani, Peter Nakaji, Albert L. Rhoton Jr., Robert F. Spetzler and Mark C. Preul

OBJECTIVE

The aim of this investigation was to modify the mini-pterional and mini-orbitozygomatic (mini-OZ) approaches in order to reduce the amount of tissue traumatization caused and to compare the use of the 2 approaches in the removal of circle of Willis aneurysms based on the authors' clinical experience and quantitative analysis.

METHODS

Three formalin-fixed adult cadaveric heads injected with colored silicone were examined. Surgical freedom and angle of attack of the mini-pterional and mini-OZ approaches were measured at 9 anatomical points, and the measurements were compared. The authors also retrospectively reviewed the cases of 396 patients with ruptured and unruptured single aneurysms in the circle of Willis treated by microsurgical techniques at their institution between January 2006 and November 2014.

RESULTS

A significant difference in surgical freedom was found in favor of the mini-pterional approach for access to the ipsilateral internal carotid artery (ICA) and middle cerebral artery (MCA) bifurcations, the most distal point of the ipsilateral posterior cerebral artery (PCA), and the basilar artery (BA) tip. No statistically significant differences were found between the mini-pterional and mini-OZ approaches for access to the posterior clinoid process, the most distal point of the superior cerebellar artery (SCA), the anterior communicating artery (ACoA), the contralateral ICA bifurcation, and the most distal point of the contralateral MCA. A trend toward increasing surgical freedom was found for the mini-OZ approach to the ACoA and the contralateral ICA bifurcation. The lengths exposed through the mini-OZ approach were longer than those exposed by the mini-pterional approach for the ipsilateral PCA segment (11.5 ± 1.9 mm) between the BA and the most distal point of the P2 segment of the PCA, for the ipsilateral SCA (10.5 ± 1.1 mm) between the BA and the most distal point of the SCA, and for the contralateral anterior cerebral artery (ACA) (21 ± 6.1 mm) between the ICA bifurcation and the most distal point of the A2 segment of the ACA. The exposed length of the contralateral MCA (24.2 ± 8.6 mm) between the contralateral ICA bifurcation and the most distal point of the MCA segment was longer through the mini-pterional approach. The vertical angle of attack (anteroposterior direction) was significantly greater with the mini-pterional approach than with the mini-OZ approach, except in the ACoA and contralateral ICA bifurcation. The horizontal angle of attack (mediolateral direction) was similar with both approaches, except in the ACoA, contralateral ICA bifurcation, and contralateral MCA bifurcation, where the angle was significantly increased in the mini-OZ approach.

CONCLUSIONS

The mini-pterional and mini-OZ approaches, as currently performed in select patients, provide less tissue traumatization (i.e., less temporal muscle manipulation, less brain parenchyma retraction) from the skin to the aneurysm than standard approaches. Anatomical quantitative analysis showed that the mini-OZ approach provides better exposure to the contralateral side for controlling the contralateral parent arteries and multiple aneurysms. The mini-pterional approach has greater surgical freedom (maneuverability) for ipsilateral circle of Willis aneurysms.

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Ali M. Elhadi, Hasan A. Zaidi, Kaan Yagmurlu, Shah Ahmed, Albert L. Rhoton Jr., Peter Nakaji, Mark C. Preul and Andrew S. Little

OBJECTIVE

Endoscopic transmaxillary approaches (ETMAs) address pathology of the anterolateral skull base, including the cavernous sinus, pterygopalatine fossa, and infratemporal fossa. This anatomically complex region contains branches of the trigeminal nerve and external carotid artery and is in proximity to the internal carotid artery. The authors postulated, on the basis of intraoperative observations, that the infraorbital nerve (ION) is a useful surgical landmark for navigating this region; therefore, they studied the anatomy of the ION and its relationships to critical neurovascular structures and the maxillary nerve (V2) encountered in ETMAs.

METHODS

Endoscopic anatomical dissections were performed bilaterally in 5 silicone-injected, formalin-fixed cadaveric heads (10 sides). Endonasal transmaxillary and direct transmaxillary (Caldwell-Luc) approaches were performed, and anatomical correlations were analyzed and documented. Stereotactic imaging of each specimen was performed to correlate landmarks and enable precise measurement of each segment.

RESULTS

The ION was readily identified in the roof of the maxillary sinus at the beginning of the surgical procedure in all specimens. Anatomical dissections of the ION and the maxillary branch of the trigeminal nerve (V2) to the cavernous sinus suggested that the ION/V2 complex has 4 distinct segments that may have implications in endoscopic approaches: 1) Segment I, the cutaneous segment of the ION and its terminal branches (5–11 branches) to the face, distal to the infraorbital foramen; 2) Segment II, the orbitomaxillary segment of the ION within the infraorbital canal from the infraorbital foramen along the infraorbital groove (length 12 ± 3.2 mm); 3) Segment III, the pterygopalatine segment within the pterygopalatine fossa, which starts at the infraorbital groove to the foramen rotundum (13 ± 2.5 mm); and 4) Segment IV, the cavernous segment from the foramen rotundum to the trigeminal ganglion (15 ± 4.1 mm), which passes in the lateral wall of the cavernous sinus. The relationship of the ION/V2 complex to the contents of the cavernous sinus, carotid artery, and pterygopalatine fossa is described in the text.

CONCLUSIONS

The ION/V2 complex is an easily identifiable and potentially useful surgical landmark to the foramen rotundum, cavernous sinus, carotid artery, pterygopalatine fossa, and anterolateral skull base during ETMAs.

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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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Ting Lei, Evgenii Belykh, Alexander B. Dru, Kaan Yagmurlu, Ali M. Elhadi, Peter Nakaji and Mark C. Preul

Chen Jingrun (1933–1996), perhaps the most prodigious mathematician of his time, focused on the field of analytical number theory. His work on Waring's problem, Legendre's conjecture, and Goldbach's conjecture led to progress in analytical number theory in the form of “Chen's Theorem,” which he published in 1966 and 1973. His early life was ravaged by the Second Sino-Japanese War and the Chinese Cultural Revolution. On the verge of solving Goldbach's conjecture in 1984, Chen was struck by a bicyclist while also bicycling and suffered severe brain trauma. During his hospitalization, he was also found to have Parkinson's disease. Chen suffered another serious brain concussion after a fall only a few months after recovering from the bicycle crash. With significant deficits, he remained hospitalized for several years without making progress while receiving modern Western medical therapies. In 1988 traditional Chinese medicine experts were called in to assist with his treatment. After a year of acupuncture and oxygen therapy, Chen could control his basic bowel and bladder functions, he could walk slowly, and his swallowing and speech improved. When Chen was unable to produce complex work or finish his final work on Goldbach's conjecture, his mathematical pursuits were taken up vigorously by his dedicated students. He was able to publish Youth Math, a mathematics book that became an inspiration in Chinese education. Although he died in 1996 at the age of 63 after surviving brutal political repression, being deprived of neurological function at the very peak of his genius, and having to be supported by his wife, Chen ironically became a symbol of dedication, perseverance, and motivation to his students and associates, to Chinese youth, to a nation, and to mathematicians and scientists worldwide.

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Nikolay L. Martirosyan, Jennifer M. Eschbacher, M. Yashar S. Kalani, Jay D. Turner, Evgenii Belykh, Robert F. Spetzler, Peter Nakaji and Mark C. Preul

OBJECTIVE

This study evaluated the utility, specificity, and sensitivity of intraoperative confocal laser endomicroscopy (CLE) to provide diagnostic information during resection of human brain tumors.

METHODS

CLE imaging was used in the resection of intracranial neoplasms in 74 consecutive patients (31 male; mean age 47.5 years; sequential 10-month study period). Intraoperative in vivo and ex vivo CLE was performed after intravenous injection of fluorescein sodium (FNa). Tissue samples from CLE imaging–matched areas were acquired for comparison with routine histological analysis (frozen and permanent sections). CLE images were classified as diagnostic or nondiagnostic. The specificities and sensitivities of CLE and frozen sections for gliomas and meningiomas were calculated using permanent histological sections as the standard.

RESULTS

CLE images were obtained for each patient. The mean duration of intraoperative CLE system use was 15.7 minutes (range 3–73 minutes). A total of 20,734 CLE images were correlated with 267 biopsy specimens (mean number of images/biopsy location, in vivo 84, ex vivo 70). CLE images were diagnostic for 45.98% in vivo and 52.97% ex vivo specimens. After initiation of CLE, an average of 14 in vivo images and 7 ex vivo images were acquired before identification of a first diagnostic image. CLE specificity and sensitivity were, respectively, 94% and 91% for gliomas and 93% and 97% for meningiomas.

CONCLUSIONS

CLE with FNa provided intraoperative histological information during brain tumor removal. Specificities and sensitivities of CLE for gliomas and meningiomas were comparable to those for frozen sections. These data suggest that CLE could allow the interactive identification of tumor areas, substantially improving intraoperative decisions during the resection of brain tumors.

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Ali M. Elhadi, Joseph M. Zabramski, Kaith K. Almefty, George A. C. Mendes, Peter Nakaji, Cameron G. McDougall, Felipe C. Albuquerque, Mark C. Preul and Robert F. Spetzler

OBJECT

Hemorrhagic origin is unidentifiable in 10%–20% of patients presenting with spontaneous subarachnoid hemorrhage (SAH). While the patients in such cases do well clinically, there is a lack of long-term angiographic followup. The authors of the present study evaluated the long-term clinical and angiographic follow-up of a patient cohort with SAH of unknown origin that had been enrolled in the Barrow Ruptured Aneurysm Trial (BRAT).

METHODS

The BRAT database was searched for patients with SAH of unknown origin despite having undergone two or more angiographic studies as well as MRI of the brain and cervical spine. Follow-up was available at 6 months and 1 and 3 years after treatment. Analysis included demographic details, clinical outcome (Glasgow Outcome Scale, modified Rankin Scale [mRS]), and repeat vascular imaging.

RESULTS

Subarachnoid hemorrhage of unknown etiology was identified in 57 (11.9%) of the 472 patients enrolled in the BRAT study between March 2003 and January 2007. The mean age for this group was 51 years, and 40 members (70%) of the group were female. Sixteen of 56 patients (28.6%) required placement of an external ventricular drain for hydrocephalus, and 4 of these subsequently required a ventriculoperitoneal shunt. Delayed cerebral ischemia occurred in 4 patients (7%), leading to stroke in one of them. There were no rebleeding events. Eleven patients were lost to followup, and one patient died of unrelated causes. At the 3-year follow-up, 4 (9.1%) of 44 patients had a poor outcome (mRS > 2), and neurovascular imaging, which was available in 33 patients, was negative.

CONCLUSIONS

Hydrocephalus and delayed cerebral ischemia, while infrequent, do occur in SAH of unknown origin. Long-term neurological outcomes are generally good. A thorough evaluation to rule out an etiology of hemorrhage is necessary; however, imaging beyond 6 weeks from ictus has little utility, and rebleeding is unexpected.