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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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Colin J. Przybylowski, Xiaochun Zhao, Jacob F. Baranoski, Leandro Borba Moreira, Sirin Gandhi, Kristina M. Chapple, Kaith K. Almefty, Nader Sanai, Andrew F. Ducruet, Felipe C. Albuquerque, Andrew S. Little and Peter Nakaji

OBJECTIVE

The controversy continues over the clinical utility of preoperative embolization for reducing tumor vascularity of intracranial meningiomas prior to resection. Previous studies comparing embolization and nonembolization patients have not controlled for detailed tumor parameters before assessing outcomes.

METHODS

The authors reviewed the cases of all patients who underwent resection of a WHO grade I intracranial meningioma at their institution from 2008 to 2016. Propensity score matching was used to generate embolization and nonembolization cohorts of 52 patients each, and a retrospective review of clinical and radiological outcomes was performed.

RESULTS

In total, 52 consecutive patients who underwent embolization (mean follow-up 34.8 ± 31.5 months) were compared to 52 patients who did not undergo embolization (mean follow-up 32.8 ± 28.7 months; p = 0.63). Variables controlled for included patient age (p = 0.82), tumor laterality (p > 0.99), tumor location (p > 0.99), tumor diameter (p = 0.07), tumor invasion into a major dural sinus (p > 0.99), and tumor encasement around the internal carotid artery or middle cerebral artery (p > 0.99). The embolization and nonembolization cohorts did not differ in terms of estimated blood loss during surgery (660.4 ± 637.1 ml vs 509.2 ± 422.0 ml; p = 0.17), Simpson grade IV resection (32.7% vs 25.0%; p = 0.39), perioperative procedural complications (26.9% vs 19.2%; p = 0.35), development of permanent new neurological deficits (5.8% vs 7.7%; p = 0.70), or favorable modified Rankin Scale (mRS) score (a score of 0–2) at last follow-up (96.0% vs 92.3%; p = 0.43), respectively. When comparing the final mRS score to the preoperative mRS score, patients in the embolization group were more likely than patients in the nonembolization group to have an improvement in mRS score (50.0% vs 28.8%; p = 0.03).

CONCLUSIONS

After controlling for patient age, tumor size, tumor laterality, tumor location, tumor invasion into a major dural sinus, and tumor encasement of the internal carotid artery or middle cerebral artery, preoperative meningioma embolization intended to decrease tumor vascularity did not improve the surgical outcomes of patients with WHO grade I intracranial meningiomas, but it did lead to a greater chance of clinical improvement compared to patients not treated with embolization.

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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.

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Mohamed A. Labib, Leandro Borba Moreira, Xiaochun Zhao, Sirin Gandhi, Claudio Cavallo, Ali Tayebi Meybodi, A. Samy Youssef, Andrew S. Little, Peter Nakaji, Mark C. Preul and Michael T. Lawton

OBJECTIVE

The pretemporal transcavernous approach (PTA) and the endoscopic endonasal transcavernous approach (EETA) are both used to access the retroclival region. A direct quantitative comparison of both approaches has not been made. The authors compared the technical nuances of, and surgical exposure afforded by, each approach and identified the key elements of the approach selection process.

METHODS

Fourteen cadaveric specimens underwent either PTA (group A) or EETA with unilateral (group B) followed by bilateral (group C) interdural pituitary gland transposition. The percentage of drilled clivus; length of exposed oculomotor nerve (cranial nerve [CN] III), posterior cerebral artery (PCA), and superior cerebellar artery (SCA); and surgical area of exposure of both cerebral peduncles and the pons for the 3 groups were measured and compared.

RESULTS

Group A had a significantly lower percentage of drilled area than group B (mean [SD], 35.6% [11.2%] vs 91.3% [4.9%], p < 0.01). In group C, 100% of the upper third of the clivus was drilled in all specimens. Significantly longer segments of the ipsilateral PCA (p < 0.01) and SCA (p < 0.01) were exposed in group A than in group B. There was no significant difference in the length of the ipsilateral CN III exposed among the 3 groups. There was also no significant difference between group A and either group B or group C for the contralateral CN III or PCA exposure. However, longer segments of the contralateral SCA were exposed in group C than in group A (p = 0.02). Furthermore, longer segments of CN III (p < 0.01), PCA (p < 0.01), and SCA (p < 0.01) were exposed in group C than in group B. For brainstem exposure, there was greater exposure of the pons in group C than in group A (mean [SD], 211.4 [19.5] mm2 vs 157.7 [25.3] mm2, p < 0.01) and group B (211.4 [19.5] mm2 vs 153.9 [34.1] mm2, p < 0.01). However, significantly greater exposure of the ipsilateral peduncle was observed in group A (mean [SD], 125.6 [43.1] mm2) than in groups B and C (56.3 [6.0] mm2, p < 0.01). Group C had significantly greater exposure of the contralateral peduncle than group B (p = 0.02).

CONCLUSIONS

This study is the first to quantitatively identify the advantages and limitations of the PTA and EETA from an anatomical perspective. Understanding these data may help the skull base surgeon design a maximally effective yet minimally invasive approach to individual lesions.

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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Qing Sun, Xiaochun Zhao, Sirin Gandhi, Ali Tayebi Meybodi, Evgenii Belykh, Daniel Valli, Claudio Cavallo, Leandro Borba Moreira, Peter Nakaji, Michael T. Lawton and Mark C. Preul

OBJECTIVE

The cisternal pulvinar is a challenging location for neurosurgery. Four approaches for reaching the pulvinar without cortical transgression are the ipsilateral supracerebellar infratentorial (iSCIT), contralateral supracerebellar infratentorial (cSCIT), ipsilateral occipital transtentorial (iOCTT), and contralateral occipital transtentorial/falcine (cOCTF) approaches. This study quantitatively compared these approaches in terms of surgical exposure and maneuverability.

METHODS

Each of the 4 approaches was performed in 4 cadaveric heads (8 specimens in total). A 6-sided anatomical polygonal region was configured over the cisternal pulvinar, defined by 6 reachable anatomical points in different vectors. Multiple polygons were subsequently formed to calculate the areas of exposure. The surgical freedom of each approach was calculated as the maximum allowable working area at the proximal end of a probe, with the distal end fixed at the posterior pole of the pulvinar. Areas of exposure, surgical freedom, and the working distance (surgical depth) of all approaches were compared.

RESULTS

No significant difference was found among the 4 different approaches with regard to the surgical depth, surgical freedom, or medial exposure area of the pulvinar. In the pairwise comparison, the cSCIT approach provided a significantly larger lateral exposure (39 ± 9.8 mm2) than iSCIT (19 ± 10.3 mm2, p < 0.01), iOCTT (19 ± 8.2 mm2, p < 0.01), and cOCTF (28 ± 7.3 mm2, p = 0.02) approaches. The total exposure area with a cSCIT approach (75 ± 23.1 mm2) was significantly larger than with iOCTT (43 ± 16.4 mm2, p < 0.01) and iSCIT (40 ± 20.2 mm2, p = 0.01) approaches (pairwise, p ≤ 0.01).

CONCLUSIONS

The cSCIT approach is preferable among the 4 compared approaches, demonstrating better exposure to the cisternal pulvinar than ipsilateral approaches and a larger lateral exposure than the cOCTF approach. Both contralateral approaches described (cSCIT and cOCTF) provided enhanced lateral exposure to the pulvinar, while the cOCTF provided a larger exposure to the lateral portion of the pulvinar than the iOCTT. Medial exposure and maneuverability did not differ among the approaches. A short tentorium may negatively impact an ipsilateral approach because the cingulate isthmus and parahippocampal gyrus tend to protrude, in which case they can obstruct access to the cisternal pulvinar ipsilaterally.

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Xiaochun Zhao, Evgenii Belykh, Colin J. Przybylowski, Leandro Borba Moreira, Sirin Gandhi, Ali Tayebi Meybodi, Claudio Cavallo, Daniel Valli, Robert T. Wicks and Peter Nakaji

OBJECTIVE

Meningiomas at the falcotentorial junction represent a rare subgroup of complex meningiomas. Debate remains regarding the appropriate treatment strategy for and optimal surgical approach to these tumors, and surgical outcomes have not been well described in the literature. The authors reviewed their single-institution experience in the management, approach selection, and outcomes for patients with falcotentorial meningiomas.

METHODS

From the medical records, the authors identified all patients with falcotentorial meningiomas treated with resection at the Barrow Neurological Institute between January 2007 and October 2017. Perioperative clinical, surgical, and radiographic data were retrospectively collected. For patients who underwent the supracerebellar infratentorial approach, the tentorial angle was defined as the angle between the line joining the nasion with the tuberculum sellae and the tentorium in the midsagittal plane.

RESULTS

Falcotentorial meningiomas occurred in 0.97% (14/1441) of the patients with meningiomas. Most of the patients (13/14) were female, and the mean patient age was 59.8 ± 11.3 years. Of 17 total surgeries (20 procedures), 11 were single-stage primary surgeries, 3 were two-stage primary surgeries (6 procedures), 2 were reoperations for recurrence, and 1 was a reoperation after surgery had been aborted because of brain edema. Hydrocephalus was present in 5 of 17 cases, 4 of which required additional treatment. Various approaches were used, including the supracerebellar infratentorial (4/17), occipital transtentorial/transfalcine (4/17), anterior interhemispheric transsplenial (3/17), parietal transventricular (1/17), torcular (2/17), and staged supracerebellar infratentorial and occipital transtentorial/transfalcine (3/17) approaches. Of the 17 surgeries, 9 resulted in Simpson grade IV resection, and 3, 1, and 4 surgeries resulted in Simpson grades III, II, and I resection, respectively. The tentorial angle in cases with Simpson grade I resection was significantly smaller than in those with an unfavorable resection grade (43.3° ± 4.67° vs 54.0° ± 3.67°, p = 0.04). Complications occurred in 10 of 22 approaches (17 surgeries) and included visual field defects (6 cases, 2 permanent and 4 transient), hemiparesis (2 cases), hemidysesthesia (1 case), and cerebellar hematoma (1 case).

CONCLUSIONS

Falcotentorial meningiomas are challenging lesions. A steep tentorial angle is an unfavorable preoperative radiographic factor for achieving maximal resection with the supracerebellar infratentorial approach. Collectively, the study findings show that versatility is required to treat patients with falcotentorial meningiomas and that treatment goals and surgical approach must be individualized to obtain optimal surgical results.

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Ali Tayebi Meybodi, Michael T. Lawton, Leandro Borba Moreira, Xiaochun Zhao, Michael J. Lang, Peter Nakaji and Mark C. Preul

OBJECTIVE

Harvesting the occipital artery (OA) is challenging. The subcutaneous OA is usually found near the superior nuchal line and followed proximally, requiring a large incision and risking damage to the superficially located OA. The authors assessed the anatomical feasibility and safety of exposing the OA through a retromastoid-transmuscular approach.

METHODS

Using 10 cadaveric heads, 20 OAs were harvested though a 5-cm retroauricular incision placed 5 cm posterior to the external auditory meatus. The underlying muscle layers were sequentially cut and recorded before exposing the OA. Changes in the orientation of muscle fibers were used as a roadmap to expose the OA without damaging it.

RESULTS

The suboccipital segment of the OA was exposed without damage after incising two consecutive layers of muscles and their investing fasciae. These muscles displayed different fiber directions: the superficially located sternocleidomastoid muscle with vertically oriented fibers, and the underlying splenius capitis with anteroposteriorly (and mediolaterally) oriented fibers. The OA could be harvested along the entire length of the skin incision in all specimens. If needed, the incision can be extended proximally and/or distally to follow the OA and harvest greater lengths.

CONCLUSIONS

This transmuscular technique for identification of the OA is a reliable method and may facilitate exposure and protection of the OA during a retrosigmoid approach. This technique may obviate the need for larger incisions when planning a bypass to nearby arteries in the posterior circulation via a retrosigmoid craniotomy. Additionally, the small skin incision can be enlarged when a different craniotomy and/or bypass is planned or when a greater length of the OA is needed to be harvested.

Open access

Peyton L. Nisson, Robert T. Wicks, Xiaochun Zhao, Whitney S. James, David Xu and Peter Nakaji

Cavernous malformations of the brain are low-flow vascular lesions that have a propensity to hemorrhage. Extensive surgical approaches are often required for operative cure of deep-seated lesions. A 23-year-old female presented with a cavernous malformation of the left posterior insula with surrounding hematoma measuring up to 3 cm. A minimally invasive (mini-)pterional craniotomy with a transsylvian approach was selected. Endoscopic assistance was utilized to confirm complete resection of the lesion. The minipterional craniotomy is a minimally invasive approach that provides optimal exposure for sylvian fissure dissection and resection of many temporal and insular lesions.

The video can be found here: https://youtu.be/9z6_EhU6lxs.