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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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David G. Brachman, Emad Youssef, Christopher J. Dardis, Nader Sanai, Joseph M. Zabramski, Kris A. Smith, Andrew S. Little, Andrew G. Shetter, Theresa Thomas, Heyoung L. McBride, Stephen Sorensen, Robert F. Spetzler and Peter Nakaji

OBJECTIVE

Effective treatments for recurrent, previously irradiated intracranial meningiomas are limited, and resection alone is not usually curative. Thus, the authors studied the combination of maximum safe resection and adjuvant radiation using permanent intracranial brachytherapy (R+BT) in patients with recurrent, previously irradiated aggressive meningiomas.

METHODS

Patients with recurrent, previously irradiated meningiomas were treated between June 2013 and October 2016 in a prospective single-arm trial of R+BT. Cesium-131 (Cs-131) radiation sources were embedded in modular collagen carriers positioned in the operative bed on completion of resection. The Cox proportional hazards model with this treatment as a predictive term was used to model its effect on time to local tumor progression.

RESULTS

Nineteen patients (median age 64.5 years, range 50–78 years) with 20 recurrent, previously irradiated tumors were treated. The WHO grade at R+BT was I in 4 (20%), II in 14 (70%), and III in 2 (10%) cases. The median number of prior same-site radiation courses and same-site surgeries were 1 (range 1–3) and 2 (range 1–4), respectively; the median preoperative tumor volume was 11.3 cm3 (range 0.9–92.0 cm3). The median radiation dose from BT was 63 Gy (range 54–80 Gy). At a median radiographic follow-up of 15.4 months (range 0.03–47.5 months), local failure (within 1.5 cm of the implant bed) occurred in 2 cases (10%). The median treatment-site time to progression after R+BT has not been reached; that after the most recent prior therapy was 18.3 months (range 3.9–321.9 months; HR 0.17, p = 0.02, log-rank test). The median overall survival after R+BT was 26 months, with 9 patient deaths (47% of patients). Treatment was well tolerated; 2 patients required surgery for complications, and 2 experienced radiation necrosis, which was managed medically.

CONCLUSIONS

R+BT utilizing Cs-131 sources in modular carriers represents a potentially safe and effective treatment option for recurrent, previously irradiated aggressive meningiomas.

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Seungwon Yoon, Michael A. Mooney, Michael A. Bohl, John P. Sheehy, Peter Nakaji, Andrew S. Little and Michael T. Lawton

OBJECTIVE

With drastic changes to the health insurance market, patient cost sharing has significantly increased in recent years. However, the patient financial burden, or out-of-pocket (OOP) costs, for surgical procedures is poorly understood. The goal of this study was to analyze patient OOP spending in cranial neurosurgery and identify drivers of OOP spending growth.

METHODS

For 6569 consecutive patients who underwent cranial neurosurgery from 2013 to 2016 at the authors’ institution, the authors created univariate and multivariate mixed-effects models to investigate the effect of patient demographic and clinical factors on patient OOP spending. The authors examined OOP payments stratified into 10 subsets of case categories and created a generalized linear model to study the growth of OOP spending over time.

RESULTS

In the multivariate model, case categories (craniotomy for pain, tumor, and vascular lesions), commercial insurance, and out-of-network plans were significant predictors of higher OOP payments for patients (all p < 0.05). Patient spending varied substantially across procedure types, with patients undergoing craniotomy for pain ($1151 ± $209) having the highest mean OOP payments. On average, commercially insured patients spent nearly twice as much in OOP payments as the overall population. From 2013 to 2016, the mean patient OOP spending increased 17%, from $598 to $698 per patient encounter. Commercially insured patients experienced more significant growth in OOP spending, with a cumulative rate of growth of 42% ($991 in 2013 to $1403 in 2016).

CONCLUSIONS

Even after controlling for inflation, case-mix differences, and partial fiscal periods, OOP spending for cranial neurosurgery patients significantly increased from 2013 to 2016. The mean OOP spending for commercially insured neurosurgical patients exceeded $1400 in 2016, with an average annual growth rate of 13%. As patient cost sharing in health insurance plans becomes more prevalent, patients and providers must consider the potential financial burden for patients receiving specialized neurosurgical care.

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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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Robert F. Spetzler, Joseph M. Zabramski, Cameron G. McDougall, Felipe C. Albuquerque, Nancy K. Hills, Robert C. Wallace and Peter Nakaji

OBJECTIVE

The Barrow Ruptured Aneurysm Trial (BRAT) is a prospective, randomized trial in which treatment with clipping was compared to treatment with coil embolization. Patients were randomized to treatment on presentation with any nontraumatic subarachnoid hemorrhage (SAH). Because all other randomized trials comparing these 2 types of treatments have been limited to saccular aneurysms, the authors analyzed the current BRAT data for this subgroup of lesions.

METHODS

The primary BRAT analysis included all sources of SAH: nonaneurysmal lesions; saccular, blister, fusiform, and dissecting aneurysms; and SAHs from an aneurysm associated with either an arteriovenous malformation or a fistula. In this post hoc review, the outcomes for the subgroup of patients with saccular aneurysms were further analyzed by type of treatment. The extent of aneurysm obliteration was adjudicated by an independent neuroradiologist not involved in treatment.

RESULTS

Of the 471 patients enrolled in the BRAT, 362 (77%) had an SAH from a saccular aneurysm. Patients with saccular aneurysms were assigned equally to the clipping and the coiling cohorts (181 each). In each cohort, 3 patients died before treatment and 178 were treated. Of the 178 clip-assigned patients with saccular aneurysms, 1 (1%) was crossed over to coiling, and 64 (36%) of the 178 coil-assigned patients were crossed over to clipping. There was no statistically significant difference in poor outcome (modified Rankin Scale score > 2) between these 2 treatment arms at any recorded time point during 6 years of follow-up. After the initial hospitalization, 1 of 241 (0.4%) clipped saccular aneurysms and 21 of 115 (18%) coiled saccular aneurysms required retreatment (p < 0.001). At the 6-year follow-up, 95% (95/100) of the clipped aneurysms were completely obliterated, compared with 40% (16/40) of the coiled aneurysms (p < 0.001). There was no difference in morbidity between the 2 treatment groups (p = 0.10).

CONCLUSIONS

In the subgroup of patients with saccular aneurysms enrolled in the BRAT, there was no significant difference between modified Rankin Scale outcomes at any follow-up time in patients with saccular aneurysms assigned to clipping compared with those assigned to coiling (intent-to-treat analysis). At the 6-year follow-up evaluation, rates of retreatment and complete aneurysm obliteration significantly favored patients who underwent clipping compared with those who underwent coiling.

Clinical trial registration no.: NCT01593267 (clinicaltrials.gov)

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Sam Safavi-Abbasi, M. Yashar S. Kalani, Ben Frock, Hai Sun, Kaan Yagmurlu, Felix Moron, Laura A. Snyder, Randy J. Hlubek, Joseph M. Zabramski, Peter Nakaji and Robert F. Spetzler

OBJECTIVE

Fusiform cerebral aneurysms represent a small portion of intracranial aneurysms; differ in natural history, anatomy, and pathology; and can be difficult to treat compared with saccular aneurysms. The purpose of this study was to examine the techniques of treatment of ruptured and unruptured fusiform intracranial aneurysms and patient outcomes.

METHODS

In 45 patients with fusiform aneurysms, the authors retrospectively reviewed the presentation, location, and shape of the aneurysm; the microsurgical technique; the outcome at discharge and last follow-up; and the change in the aneurysm at last angiographic follow-up.

RESULTS

Overall, 48 fusiform aneurysms were treated in 45 patients (18 male, 27 female) with a mean age of 49 years (median 51 years; range 6 months–76 years). Twelve patients (27%) had ruptured aneurysms and 33 (73%) had unruptured aneurysms. The mean aneurysm size was 8.9 mm (range 6–28 mm). The aneurysms were treated by clip reconstruction (n = 22 [46%]), clip-wrapping (n = 18 [38%]), and vascular bypass (n = 8 [17%]). The mean (SD) hospital stay was 19.0 ± 7.4 days for the 12 patients with subarachnoid hemorrhage and 7.0 ± 5.6 days for the 33 patients with unruptured aneurysms. The mean follow-up was 38.7 ± 29.5 months (median 36 months; range 6–96 months). The mean Glasgow Outcome Scale score for the 12 patients with subarachnoid hemorrhage was 3.9; for the 33 patients with unruptured aneurysms, it was 4.8. No rehemorrhages occurred during follow-up. The overall annual risk of recurrence was 2% and that of rehemorrhage was 0%.

CONCLUSIONS

Fusiform and dolichoectatic aneurysms involving the entire vessel wall must be investigated individually. Although some of these aneurysms may be amenable to primary clipping and clip reconstruction, these complex lesions often require alternative microsurgical and endovascular treatment. These techniques can be performed with acceptable morbidity and mortality rates and with low rates of early rebleeding and recurrence.

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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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M. Yashar S. Kalani, John E. Wanebo, Nikolay L. Martirosyan, Peter Nakaji, Joseph M. Zabramski and Robert F. Spetzler

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Or Cohen-Inbar, Cheng-Chia Lee, Seyed H. Mousavi, Hideyuki Kano, David Mathieu, Antonio Meola, Peter Nakaji, Norissa Honea, Matthew Johnson, Mahmoud Abbassy, Alireza M. Mohammadi, Danilo Silva, Huai-Che Yang, Inga Grills, Douglas Kondziolka, Gene H. Barnett, L. Dade Lunsford and Jason Sheehan

OBJECTIVE

Hemangiopericytomas (HPCs) are rare tumors widely recognized for their aggressive clinical behavior, high recurrence rates, and distant and extracranial metastases even after a gross-total resection. The authors report a large multicenter study, through the International Gamma Knife Research Foundation (IGKRF), reviewing management and outcome following stereotactic radiosurgery (SRS) for recurrent or newly discovered HPCs.

METHODS

Eight centers participating in the IGKRF participated in this study. A total of 90 patients harboring 133 tumors were identified. Patients were included if they had a histologically diagnosed HPC managed with SRS during the period 1988–2014 and had a minimum of 6 months' clinical and radiological follow-up. A de-identified database was created. The patients' median age was 48.5 years (range 13–80 years). Prior treatments included embolization (n = 8), chemotherapy (n = 2), and fractionated radiotherapy (n = 34). The median tumor volume at the time of SRS was 4.9 cm3 (range 0.2–42.4 cm3). WHO Grade II (typical) HPCs formed 78.9% of the cohort (n = 71). The median margin and maximum doses delivered were 15 Gy (range 2.8–24 Gy) and 32 Gy (range 8–51 Gy), respectively. The median clinical and radiographic follow-up periods were 59 months (range 6–190 months) and 59 months (range 6–183 months), respectively. Prognostic variables associated with local tumor control and post-SRS survival were evaluated using Cox univariate and multivariate analysis. Actuarial survival after SRS was analyzed using the Kaplan-Meier method.

RESULTS

Imaging studies performed at last follow-up demonstrated local tumor control in 55% of tumors and 62.2% of patients. New remote intracranial tumors were found in 27.8% of patients, and 24.4% of patients developed extracranial metastases. Adverse radiation effects were noted in 6.7% of patients. During the study period, 32.2% of the patients (n = 29) died. The actuarial overall survival was 91.5%, 82.1%, 73.9%, 56.7%, and 53.7% at 2, 4, 6, 8, and 10 years, respectively, after initial SRS. Local progression–free survival (PFS) was 81.7%, 66.3%, 54.5%, 37.2%, and 25.5% at 2, 4, 6, 8, and 10 years, respectively, after initial SRS. In our cohort, 32 patients underwent 48 repeat SRS procedures for 76 lesions. Review of these 76 treated tumors showed that 17 presented as an in-field recurrence and 59 were defined as an out-of-field recurrence. Margin dose greater than 16 Gy (p = 0.037) and tumor grade (p = 0.006) were shown to influence PFS. The development of extracranial metastases was shown to influence overall survival (p = 0.029) in terms of PFS; repeat (multiple) SRS showed additional benefit.

CONCLUSIONS

SRS provides a reasonable rate of local tumor control and a low risk of adverse effects. It also leads to neurological stability or improvement in the majority of patients. Long-term close clinical and imaging follow-up is necessary due to the high probability of local recurrence and distant metastases. Repeat SRS is often effective for treating new or recurrent HPCs.