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Joseph Georges, Xiaodong Qi, Xiaowei Liu, Yu Zhou, Eric C. Woolf, Amber Valeri, Zein Al-Atrache, Evgenii Belykh, Burt G. Feuerstein, Mark Preul, Adrienne C. Scheck, Mark Reiser, Trent Anderson, Jonas Gopez, Denah Appelt, Steven Yocom, Jennifer Eschbacher, Hao Yan and Peter Nakaji

OBJECTIVE

Differentiating central nervous system (CNS) lymphoma from other intracranial malignancies remains a clinical challenge in surgical neuro-oncology. Advances in clinical fluorescence imaging contrast agents and devices may mitigate this challenge. Aptamers are a class of nanomolecules engineered to bind cellular targets with antibody-like specificity in a fraction of the staining time. Here, the authors determine if immediate ex vivo fluorescence imaging with a lymphoma-specific aptamer can rapidly and specifically diagnose xenografted orthotopic human CNS lymphoma at the time of biopsy.

METHODS

The authors synthesized a fluorescent CNS lymphoma-specific aptamer by conjugating a lymphoma-specific aptamer with Alexa Fluor 488 (TD05-488). They modified human U251 glioma cells and Ramos lymphoma cells with a lentivirus for constitutive expression of red fluorescent protein and implanted them intracranially into athymic nude mice. Three to 4 weeks postimplantation, acute slices (biopsies, n = 28) from the xenografts were collected, placed in aptamer solution, and imaged with a Zeiss fluorescence microscope. Three aptamer staining concentrations (0.3, 1.0, and 3.0 μM) and three staining times (5, 10, and 20 minutes) followed by a 1-minute wash were tested. A file of randomly selected images was distributed to neurosurgeons and neuropathologists, and their ability to distinguish CNS lymphoma from negative controls was assessed.

RESULTS

The three staining times and concentrations of TD05-488 were tested to determine the diagnostic accuracy of CNS lymphoma within a frozen section time frame. An 11-minute staining protocol with 1.0-μM TD05-488 was most efficient, labeling 77% of positive control lymphoma cells and less than 1% of negative control glioma cells (p < 0.001). This protocol permitted clinicians to positively identify all positive control lymphoma images without misdiagnosing negative control images from astrocytoma and normal brain.

CONCLUSIONS

Ex vivo fluorescence imaging is an emerging technique for generating rapid histopathological diagnoses. Ex vivo imaging with a novel aptamer-based fluorescent nanomolecule could provide an intraoperative tumor-specific diagnosis of CNS lymphoma within 11 minutes of biopsy. Neurosurgeons and neuropathologists interpreted images generated with this molecular probe with high sensitivity and specificity. Clinical application of TD05-488 may permit specific intraoperative diagnosis of CNS lymphoma in a fraction of the time required for antibody staining.

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Xiaochun Zhao, Ali Tayebi Meybodi, Mohamed A. Labib, Sirin Gandhi, Evgenii Belykh, Komal Naeem, Mark C. Preul, Peter Nakaji and Michael T. Lawton

OBJECTIVE

Aneurysms that arise on the medial surface of the paraclinoid segment of the internal carotid artery (ICA) are surgically challenging. The contralateral interoptic trajectory, which uses the space between the optic nerves, can partially expose the medial surface of the paraclinoid ICA. In this study, the authors quantitatively measure the area of the medial ICA accessible through the interoptic triangle and propose a potential patient-selection algorithm that is based on preoperative measurements on angiographic imaging.

METHODS

The contralateral interoptic trajectory was studied on 10 sides of 5 cadaveric heads, through which the medial paraclinoid ICA was identified. The falciform ligament medial to the contralateral optic canal was incised, the contralateral optic nerve was gently elevated, and the medial surface of the paraclinoid ICA was inspected via different viewing angles to obtain maximal exposure. The accessible area on the carotid artery was outlined. The distance from the distal dural ring (DDR) to the proximal and distal borders of this accessible area was measured. The superior and inferior borders were measured using the clockface method relative to a vertical line on the coronal plane. To validate these parameters, preoperative measurements and intraoperative findings were reviewed in 8 clinical cases.

RESULTS

In the sagittal plane, the mean (SD) distances from the DDR to the proximal and distal ends of the accessible area on the paraclinoid ICA were 2.5 (1.52) mm and 8.4 (2.32) mm, respectively. In the coronal plane, the mean (SD) angles of the superior and inferior ends of the accessible area relative to a vertical line were 21.7° (14.84°) and 130.9° (12.75°), respectively. Six (75%) of 8 clinical cases were consistent with the proposed patient-selection algorithm.

CONCLUSIONS

The contralateral interoptic approach is a feasible route to access aneurysms that arise from the medial paraclinoid ICA. An aneurysm can be safely clipped via the contralateral interoptic trajectory if 1) both proximal and distal borders of the aneurysm neck are 2.5–8.4 mm distal to the DDR, and 2) at least one border of the aneurysm neck on the coronal clockface is 21.7°–130.9° medial to the vertical line.

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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.

Open access

Xiaochun Zhao, Robert T. Wicks, Evgenii Belykh, Colin J. Przybylowski, Mohamed A. Labib and Peter Nakaji

Neurocysticercosis is primarily managed with anthelminthic, antiepileptic, and corticosteroid therapies. Surgical removal of the larval cyst is indicated when associated mass effect causes neurological symptoms, as demonstrated in two cases. Cyst resection was achieved via the far lateral approach for a cervicomedullary cyst in one patient and via the subtemporal approach for a mesencephalic cyst in another. The cyst wall should be kept intact, when possible, to avoid dissemination of the inflammation-evoking contents. As the contents are usually semisolid and can be removed via suction, it is not necessary to remove the gliotic capsule or adherent portions of the cyst wall in highly eloquent locations.

The video can be found here: https://youtu.be/GqbaJu5sy1o.

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Michael A. Bohl, Nikolay L. Martirosyan, Zachary W. Killeen, Evgenii Belykh, Joseph M. Zabramski, Robert F. Spetzler and Mark C. Preul

Despite an overwhelming history demonstrating the potential of hypothermia to rescue and preserve the brain and spinal cord after injury or disease, clinical trials from the last 50 years have failed to show a convincing benefit. This comprehensive review provides the historical context needed to consider the current status of clinical hypothermia research and a view toward the future direction for this field. For millennia, accounts of hypothermic patients surviving typically fatal circumstances have piqued the interest of physicians and prompted many of the early investigations into hypothermic physiology. In 1650, for example, a 22-year-old woman in Oxford suffered a 30-minute execution by hanging on a notably cold and wet day but was found breathing hours later when her casket was opened in a medical school dissection laboratory. News of her complete recovery inspired pioneers such as John Hunter to perform the first complete and methodical experiments on life in a hypothermic state. Hunter’s work helped spark a scientific revolution in Europe that saw the overthrow of the centuries-old dogma that volitional movement was created by hydraulic nerves filling muscle bladders with cerebrospinal fluid and replaced this theory with animal electricity. Central to this paradigm shift was Giovanni Aldini, whose public attempts to reanimate the hypothermic bodies of executed criminals not only inspired tremendous scientific debate but also inspired a young Mary Shelley to write her novel Frankenstein. Dr. Temple Fay introduced hypothermia to modern medicine with his human trials on systemic and focal cooling. His work was derailed after Nazi physicians in Dachau used his results to justify their infamous experiments on prisoners of war. The latter half of the 20th century saw the introduction of hypothermic cerebrovascular arrest in neurosurgical operating rooms. The ebb and flow of neurosurgical interest in hypothermia that has since persisted reflect our continuing struggle to achieve the neuroprotective benefits of cooling while minimizing the systemic side effects.

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Eberval G. Figueiredo, Manoel J. Teixeira and Leonardo C. Welling

Free access

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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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.

Free access

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.