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Pituitary surgery and volumetric assessment of extent of resection: a paradigm shift in the use of intraoperative magnetic resonance imaging

Carlo Serra, Jan-Karl Burkhardt, Giuseppe Esposito, Oliver Bozinov, Athina Pangalu, Antonios Valavanis, David Holzmann, Christoph Schmid, and Luca Regli

OBJECTIVE

The aim of this study was to quantitatively assess the role of intraoperative high-field 3-T MRI (3T-iMRI) in improving the gross-total resection (GTR) rate and the extent of resection (EOR) in endoscopic transsphenoidal surgery (TSS) for pituitary adenomas.

METHODS

Radiological and clinical data from a prospective database were retrospectively analyzed. Volumetric measurements of adenoma volumes pre-, intraoperatively, and 3 months postoperatively were performed in a consecutive series of patients who had undergone endoscopic TSS. The quantitative contribution of 3T-iMRI was measured as a percentage of the additional rate of GTR and of the EOR achieved after 3T-iMRI.

RESULTS

The cohort consisted of 50 patients (51 operations) harboring 33 nonfunctioning and 18 functioning pituitary adenomas. Mean adenoma diameter and volume were 21.1 mm (range 5–47 mm) and 5.23 cm3 (range 0.09–22.14 cm3), respectively. According to Knosp's classification, 10 cases were Grade 0; 8, Grade 1; 17, Grade 2; 12, Grade 3; and 4, Grade 4. Gross-total resection was the surgical goal (targeted [t]GTR) in 34 of 51 operations and was initially achieved in 16 (47%) of 34 at 3T-iMRI and in 30 (88%) of 34 cases after further resection. In this subgroup, the EOR increased from 91% at 3T-iMRI to 99% at the 3-month MRI (p < 0.05). In the 17 cases in which subtotal resection (STR) had been planned (tSTR), the EOR increased from 79% to 86% (p < 0.05) and GTR could be achieved in 1 case. Intrasellar remnants were present in 20 of 51 procedures at 3T-iMRI and in only 5 (10%) of 51 procedures after further resection (median volume 0.15 cm3). Overall, the use of 3T-iMRI led to further resection in 27 (53%) of 51 procedures and permitted GTR in 15 (56%) of these 27 procedures; thus, the GTR rate in the entire cohort increased from 31% (16 of 51) to 61% (31 of 51) and the EOR increased from 87% to 95% (p < 0.05).

CONCLUSIONS

The use of high-definition 3T-iMRI allowed precise visualization and quantification of adenoma remnant volume. It helped to increase GTR and EOR rates in both tGTR and tSTR patient groups. Moreover, it helped to achieve low rates of intrasellar remnants. These data support the use of 3T-iMRI to achieve maximal, safe adenoma resection.

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Validation of the Clavien-Dindo grading system of complications for microsurgical treatment of unruptured intracranial aneurysms

Martina Sebök, Patricia Blum, Johannes Sarnthein, Jorn Fierstra, Menno R. Germans, Carlo Serra, Niklaus Krayenbühl, Luca Regli, and Giuseppe Esposito

OBJECTIVE

Microsurgery plays an essential role in managing unruptured intracranial aneurysms (UIAs). The Clavien-Dindo classification is a therapy-oriented grading system that rates any deviation from the normal postoperative course in five grades. In this study, the authors aimed to test the applicability of the Clavien-Dindo grade (CDG) in patients who underwent microsurgical treatment of UIAs.

METHODS

The records of patients who underwent microsurgery for UIAs (January 2013–November 2018) were retrieved from a prospective database. Complications at discharge and at short-term follow-up (3 months) were rated according to the Clavien-Dindo system. Patient outcomes were graded using the modified Rankin Scale (mRS) and the National Institutes of Health Stroke Scale (NIHSS). A descriptive statistic was used for data analysis.

RESULTS

Overall, 156 patients underwent 157 surgeries for 201 UIAs (size range 4–42 mm). Thirty-nine patients (25%) had complex UIAs. An adverse event (CDG ≥ I) occurred in 21 patients (13.5%) by the time of discharge. Among these, 10 patients (6.4%) presented with a new neurological deficit. Significant correlations existed between a CDG ≥ I and an increase in mRS and NIHSS scores (p < 0.001). Patients treated for complex aneurysms had a significantly higher risk of developing new neurological deficits (20.5% vs 1.7%, p = 0.007). At the 3-month follow-up, a CDG ≥ I was registered in 16 patients (10.3%); none presented with a new neurological deficit. A CDG ≥ I was associated with a longer hospital length of stay (LOS) (no complication vs CDG ≥ I, 6.2 ± 3.5 days vs 9.3 ± 7.7 days, p = 0.02).

CONCLUSIONS

The CDG was applicable to patients who received microsurgery of UIAs. A significant correlation existed between CDG and outcome scales, as well as LOS. The aneurysm complexity was significantly associated with a higher risk for new neurological deficit.

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Role of stereotactic radiosurgery and fractionated stereotactic radiotherapy for the treatment of recurrent glioblastoma multiforme

Pantaleo Romanelli, Alfredo Conti, Antonio Pontoriero, Giuseppe Kenneth Ricciardi, Francesco Tomasello, Costantino De Renzis, Gualtiero Innocenzi, Vincenzo Esposito, and Giampaolo Cantore

Glioblastoma multiforme (GBM) is a devastating malignant brain tumor characterized by resistance to available therapeutic approaches and relentless malignant progression that includes widespread intracranial invasion, destruction of normal brain tissue, progressive disability, and death. Stereotactic radiosurgery (SRS) and fractionated stereotactic radiotherapy (fSRT) are increasingly used in patients with recurrent GBM to complement traditional treatments such as resection, conventional external beam radiotherapy, and chemotherapy. Both SRS and fSRT are powerful noninvasive therapeutic modalities well suited to treat focal neoplastic lesions through the delivery of precise, highdose radiation. Although no randomized clinical trials have been performed, a variety of retrospective studies have been focused on the use of SRS and fSRT for recurrent GBMs. In addition, state-of-the-art neuroimaging techniques, such as MR spectroscopic imaging, diffusion tensor tractography, and nuclear medicine imaging, have enhanced treatment planning methods leading to potentially improved clinical outcomes. In this paper the authors reviewed the current applications and efficacy of SRS and fSRT in the treatment of GBM, highlighting the value of these therapies for recurrent focal disease.

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Flow augmentation STA-MCA bypass evaluation for patients with acute stroke and unilateral large vessel occlusion: a proposal for an urgent bypass flowchart

Martina Sebök, Giuseppe Esposito, Christiaan Hendrik Bas van Niftrik, Jorn Fierstra, Tilman Schubert, Susanne Wegener, Jeremia Held, Zsolt Kulcsár, Andreas R. Luft, and Luca Regli

OBJECTIVE

Endovascular recanalization trials have shown a positive impact on the preservation of ischemic penumbra in patients with acute large vessel occlusion (LVO). The concept of penumbra salvation can be extended to surgical revascularization with bypass in highly selected patients. For selecting these patients, the authors propose a flowchart based on multimodal MRI.

METHODS

All patients with acute stroke and persisting internal carotid artery (ICA) or M1 occlusion after intravenous lysis or mechanical thrombectomy undergo advanced neuroimaging in a time window of 72 hours after stroke onset including perfusion MRI, blood oxygenation level–dependent functional MRI to evaluate cerebrovascular reactivity (BOLD-CVR), and noninvasive optimal vessel analysis (NOVA) quantitative MRA to assess collateral circulation.

RESULTS

Symptomatic patients exhibiting persistent hemodynamic impairment and insufficient collateral circulation could benefit from bypass surgery. According to the flowchart, a bypass is considered for patients 1) with low or moderate neurological impairment (National Institutes of Health Stroke Scale score 1–15, modified Rankin Scale score ≤ 3), 2) without large or malignant stroke, 3) without intracranial hemorrhage, 4) with MR perfusion/diffusion mismatch > 120%, 5) with paradoxical BOLD-CVR in the occluded vascular territory, and 6) with insufficient collateral circulation.

CONCLUSIONS

The proposed flowchart is based on the patient’s clinical condition and multimodal MR neuroimaging and aims to select patients with acute stroke due to LVO and persistent inadequate collateral flow, who could benefit from urgent bypass.

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Is age an additional factor in the treatment of elderly patients with glioblastoma? A new stratification model: an Italian Multicenter Study

Tamara Ius, Teresa Somma, Roberto Altieri, Filippo Flavio Angileri, Giuseppe Maria Barbagallo, Paolo Cappabianca, Francesco Certo, Fabio Cofano, Alessandro D’Elia, Giuseppe Maria Della Pepa, Vincenzo Esposito, Marco Maria Fontanella, Antonino Germanò, Diego Garbossa, Miriam Isola, Giuseppe La Rocca, Francesco Maiuri, Alessandro Olivi, Pier Paolo Panciani, Fabrizio Pignotti, Miran Skrap, Giannantonio Spena, and Giovanni Sabatino

OBJECTIVE

Approximately half of glioblastoma (GBM) cases develop in geriatric patients, and this trend is destined to increase with the aging of the population. The optimal strategy for management of GBM in elderly patients remains controversial. The aim of this study was to assess the role of surgery in the elderly (≥ 65 years old) based on clinical, molecular, and imaging data routinely available in neurosurgical departments and to assess a prognostic survival score that could be helpful in stratifying the prognosis for elderly GBM patients.

METHODS

Clinical, radiological, surgical, and molecular data were retrospectively analyzed in 322 patients with GBM from 9 neurosurgical centers. Univariate and multivariate analyses were performed to identify predictors of survival. A random forest approach (classification and regression tree [CART] analysis) was utilized to create the prognostic survival score.

RESULTS

Survival analysis showed that overall survival (OS) was influenced by age as a continuous variable (p = 0.018), MGMT (p = 0.012), extent of resection (EOR; p = 0.002), and preoperative tumor growth pattern (evaluated with the preoperative T1/T2 MRI index; p = 0.002). CART analysis was used to create the prognostic survival score, forming six different survival groups on the basis of tumor volumetric, surgical, and molecular features. Terminal nodes with similar hazard ratios were grouped together to form a final diagram composed of five classes with different OSs (p < 0.0001). EOR was the most robust influencing factor in the algorithm hierarchy, while age appeared at the third node of the CART algorithm. The ability of the prognostic survival score to predict death was determined by a Harrell’s c-index of 0.75 (95% CI 0.76–0.81).

CONCLUSIONS

The CART algorithm provided a promising, thorough, and new clinical prognostic survival score for elderly surgical patients with GBM. The prognostic survival score can be useful to stratify survival risk in elderly GBM patients with different surgical, radiological, and molecular profiles, thus assisting physicians in daily clinical management. The preliminary model, however, requires validation with future prospective investigations. Practical recommendations for clinicians/surgeons would strengthen the quality of the study; e.g., surgery can be considered as a first therapeutic option in the workflow of elderly patients with GBM, especially when the preoperative estimated EOR is greater than 80%.

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Successful weaning versus permanent cerebrospinal fluid diversion after aneurysmal subarachnoid hemorrhage: post hoc analysis of a Swiss multicenter study

Ahmed El-Garci, Olivia Zindel-Geisseler, Noemi Dannecker, Yannick Rothacher, Ladina Schlosser, Anna Zeitlberger, Julia Velz, Martina Sebök, Noemi Eggenberger, Adrien May, Philippe Bijlenga, Ursula Guerra-Lopez, Rodolfo Maduri, Valérie Beaud, Daniele Starnoni, Alessio Chiappini, Stefania Rossi, Thomas Robert, Sara Bonasia, Johannes Goldberg, Christian Fung, David Bervini, Klemens Gutbrod, Nicolai Maldaner, Severin Früh, Marc Schwind, Oliver Bozinov, Marian C. Neidert, Peter Brugger, Emanuela Keller, Menno R. Germans, Luca Regli, Isabel C. Hostettler, Martin N. Stienen, and on behalf of the MoCA-DCI Study Group

OBJECTIVE

Acute hydrocephalus is a frequent complication after aneurysmal subarachnoid hemorrhage (aSAH). Among patients needing CSF diversion, some cannot be weaned. Little is known about the comparative neurological, neuropsychological, and health-related quality-of-life (HRQOL) outcomes in patients with successful and unsuccessful CSF weaning. The authors aimed to assess outcomes of patients by comparing those with successful and unsuccessful CSF weaning; the latter was defined as occurring in patients with permanent CSF diversion at 3 months post-aSAH.

METHODS

The authors included prospectively recruited alert (i.e., Glasgow Coma Scale score 13–15) patients with aSAH in this retrospective study from six Swiss neurovascular centers. Patients underwent serial neurological (National Institutes of Health Stroke Scale), neuropsychological (Montreal Cognitive Assessment), disability (modified Rankin Scale), and HRQOL (EuroQol-5D) examinations at < 72 hours, 14–28 days, and 3 months post-aSAH.

RESULTS

Of 126 included patients, 54 (42.9%) developed acute hydrocephalus needing CSF diversion, of whom 37 (68.5%) could be successfully weaned and 17 (31.5%) required permanent CSF diversion. Patients with unsuccessful weaning were older (64.5 vs 50.8 years, p = 0.003) and had a higher rate of intraventricular hemorrhage (52.9% vs 24.3%, p = 0.04). Patients who succeed in restoration of physiological CSF dynamics improve on average by 2 points on the Montreal Cognitive Assessment between 48–72 hours and 14–28 days, whereas those in whom weaning fails worsen by 4 points (adjusted coefficient 6.80, 95% CI 1.57–12.04, p = 0.01). They show better neuropsychological recovery between 48–72 hours and 3 months, compared to patients in whom weaning fails (adjusted coefficient 7.60, 95% CI 3.09–12.11, p = 0.02). Patients who receive permanent CSF diversion (ventriculoperitoneal shunt) show significant neuropsychological improvement thereafter, catching up the delay in neuropsychological improvement between 14–28 days and 3 months post-aSAH. Neurological, disability, and HRQOL outcomes at 3 months were similar.

CONCLUSIONS

These results show a temporary but clinically meaningful cognitive benefit in the first weeks after aSAH in successfully weaned patients. The resolution of this difference over time may be due to the positive effects of permanent CSF diversion and underlines its importance. Patients who do not show progressive neuropsychological improvement after weaning should be considered for repeat CT imaging to rule out chronic (untreated) hydrocephalus.

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Longitudinal neuropsychological assessment after aneurysmal subarachnoid hemorrhage and its relationship with delayed cerebral ischemia: a prospective Swiss multicenter study

Martin N. Stienen, Menno R. Germans, Olivia Zindel-Geisseler, Noemi Dannecker, Yannick Rothacher, Ladina Schlosser, Julia Velz, Martina Sebök, Noemi Eggenberger, Adrien May, Julien Haemmerli, Philippe Bijlenga, Karl Schaller, Ursula Guerra-Lopez, Rodolfo Maduri, Valérie Beaud, Khalid Al-Taha, Roy Thomas Daniel, Alessio Chiappini, Stefania Rossi, Thomas Robert, Sara Bonasia, Johannes Goldberg, Christian Fung, David Bervini, Marie Elise Maradan-Gachet, Klemens Gutbrod, Nicolai Maldaner, Marian C. Neidert, Severin Früh, Marc Schwind, Oliver Bozinov, Peter Brugger, Emanuela Keller, Angelina Marr, Sébastien Roux, Luca Regli, and on behalf of the MoCA-DCI Study Group

OBJECTIVE

While prior retrospective studies have suggested that delayed cerebral ischemia (DCI) is a predictor of neuropsychological deficits after aneurysmal subarachnoid hemorrhage (aSAH), all studies to date have shown a high risk of bias. This study was designed to determine the impact of DCI on the longitudinal neuropsychological outcome after aSAH, and importantly, it includes a baseline examination after aSAH but before DCI onset to reduce the risk of bias.

METHODS

In a prospective, multicenter study (8 Swiss centers), 112 consecutive alert patients underwent serial neuropsychological assessments (Montreal Cognitive Assessment [MoCA]) before and after the DCI period (first assessment, < 72 hours after aSAH; second, 14 days after aSAH; third, 3 months after aSAH). The authors compared standardized MoCA scores and determined the likelihood for a clinically meaningful decline of ≥ 2 points from baseline in patients with DCI versus those without.

RESULTS

The authors screened 519 patients, enrolled 128, and obtained complete data in 112 (87.5%; mean [± SD] age 53.9 ± 13.9 years; 66.1% female; 73% World Federation of Neurosurgical Societies [WFNS] grade I, 17% WFNS grade II, 10% WFNS grades III–V), of whom 30 (26.8%) developed DCI. MoCA z-scores were worse in the DCI group at baseline (−2.6 vs −1.4, p = 0.013) and 14 days (−3.4 vs −0.9, p < 0.001), and 3 months (−0.8 vs 0.0, p = 0.037) after aSAH. Patients with DCI were more likely to experience a decline of ≥ 2 points in MoCA score at 14 days after aSAH (adjusted OR [aOR] 3.02, 95% CI 1.07–8.54; p = 0.037), but the likelihood was similar to that in patients without DCI at 3 months after aSAH (aOR 1.58, 95% CI 0.28–8.89; p = 0.606).

CONCLUSIONS

Aneurysmal SAH patients experiencing DCI have worse neuropsychological function before and until 3 months after the DCI period. DCI itself is responsible for a temporary and clinically meaningful decline in neuropsychological function, but its effect on the MoCA score could not be measured at the time of the 3-month follow-up in patients with low-grade aSAH with little or no impairment of consciousness. Whether these findings can be extrapolated to patients with high-grade aSAH remains unclear.

Clinical trial registration no.: NCT03032471 (ClinicalTrials.gov)