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Ulrich Sure, Sandra Freman, Oliver Bozinov, Ludwig Benes, Adrian M. Siegel and Helmut Bertalanffy

Object. Cerebral cavernous malformations (CCMs) have previously been considered as congenital and biologically static malformations. On the other hand, the potential for growth and de novo generation of CCMs have also been reported. It is therefore important to study the proliferative and neoangiogenetic capacity of these lesions.

Methods. The authors studied the surgical specimens of 56 CCMs (23 deep and 33 superficial) obtained from adult patients. The proliferative activity of the endothelium and the neoangiogenetic capacity of these lesions were considered through immunohistochemical anaylsis of proliferating cell nuclear antigen (PCNA), MIB-1, Flk-1, vascular endothelial growth factor (VEGF), hypoxia-inducible factor (HIF)-1α, and endoglin antibodies.

Positive immunostaining of endothelial cells occurred in 86% of patients for PCNA and in 38% of the cases for MIB-1. The expression of Flk-1 was observed in the endothelium of 71% of the cases, for VEGF in 41%, for HIF-1α in 48.1%, and for endoglin in 63.6% of the cases. The correlation of immunohistochemical and clinical data indicated that VEGF was expressed in significantly less deep-seated lesions when compared with superficial CCMs. Neither the expression of the proliferative markers nor the expression of the angiogenetic antibodies correlated with patient age at surgery, sex, or the number of recent prior hemorrhagic episodes in the patients.

Conclusions. The CCMs from adult patients are active lesions exhibiting endothelial proliferation and neoangiogenesis. According to the data in this study, neoangiogenesis is more prominent in superficial CCMs than in deep-seated CCMs and is not associated with recent prior hemorrhages.

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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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Sophie S. Wang, Friederike Selge, Martina Sebök, Pierre Scheffler, Yang Yang, Giovanna Brandi, Sebastian Winklhofer and Oliver Bozinov

OBJECTIVE

Identifying tumor remnants in previously operated tumor lesions remains a challenge. Intraoperative MRI (ioMRI) helps the neurosurgeon to reorient and update image guidance during surgery. The purpose of this study was to analyze whether ioMRI is more efficient in detecting tumor remnants in the surgery of recurrent lesions compared with primary surgery.

METHODS

All consecutive patients undergoing elective intracranial tumor surgery between 2013 and 2018 at the authors’ institution were included in this retrospective cohort study. The cohort was divided into two groups: re-craniotomy and primary craniotomy. In contrast-enhancing tumors, tumor suspicion in ioMRI was defined as contrast enhancement in T1-weighted imaging. In non–contrast-enhancing tumors, tumor suspicion was defined as hypointensity in T1-weighted imaging and hyperintensity in T2-weighted imaging and FLAIR. In cases in which the ioMRI tumor suspicion was a false positive and not confirmed during in situ inspection by the neurosurgeon, the signal was defined as a tumor-imitating ioMRI signal (TIM). Descriptive statistics were performed.

RESULTS

A total of 214 tumor surgeries met the inclusion criteria. The re-craniotomy group included 89 surgeries, and the primary craniotomy group included 123 surgeries. Initial complete resection after ioMRI was less frequent in the re-craniotomy group than in the primary craniotomy group, but this was not a statistically significant difference. Radiological suspicion of tumor remnants in ioMRI was present in 78% of re-craniotomy surgeries and 69% of primary craniotomy surgeries. The incidence of false-positive TIMs was significantly higher in the re-craniotomy group (n = 11, 12%) compared with the primary craniotomy group (n = 5, 4%; p = 0.015), and in contrast-enhancing tumors was related to hemorrhages in situ (n = 9).

CONCLUSIONS

A history of previous surgery in contrast-enhancing tumors made correct identification of tumor remnants in ioMRI more difficult, with a higher rate of false-positive ioMRI signals in the re-craniotomy group. The majority of TIMs were associated with the inability to distinguish contrast enhancement from hyperacute hemorrhage. The addition of a specific sequence in ioMRI to further differentiate both should be investigated in future studies.

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Jan-Karl Burkhardt, Pascal O. Zinn, Muriel Graenicher, Alejandro Santillan, Oliver Bozinov, Ekkehard M. Kasper and Niklaus Krayenbühl

Object

Some patients develop communicating hydrocephalus after meningioma surgery, and this can develop into a serious clinical condition. However, this has rarely been addressed in the literature. Therefore, the authors sought to determine predictive patient variables for the occurrence of postoperative hydrocephalus following skull base meningioma surgery.

Methods

For this purpose, the authors retrospectively analyzed all patients who underwent resection of intracranial meningiomas between 1998 and 2009 at the Department of Neurosurgery, University Hospital Zurich, Switzerland. Of 594 patients with meningioma, 227 (38%) had a lesion located at the skull base, and thus were included for analysis. The following patient variables were examined: demographic data (age and sex); tumor number (solitary vs multiple); tumor side and localization within the skull base region (anterior, medial, posterior); infiltration of the cavernous sinus; compression of the optic channel/optic nerve; tumor volume; preoperative embolization (yes/no); duration of surgery; Simpson grade of resection; histopathological features (WHO grade); number of surgeries (single vs multiple); preoperative embolization; duration of hospital stay; tumor recurrence; use of an artificial dural substitute; postoperative infection rate; and clinical outcome (Glasgow Outcome Scale score at discharge and at 3 months, and vital status at last follow-up). Hierarchical clustering, factor analysis, and stepwise regression models revealed a ranking list for the top predictive variables for the occurrence of postoperative hydrocephalus.

Results

A total of 35 patients (5.9%) of the cohort of 594 developed communicating postoperative hydrocephalus, with no patient manifesting obstructive hydrocephalus. Of these 35 patients, 18 had a meningioma located at the skull base (18 [7.9%] of 227), in contrast to 17 patients with meningiomas in other locations (17 [4.6%] of 367). The following patient variables correlated with the occurrence of hydrocephalus, as defined by factor analysis: age, duration of surgery, duration of hospital stay, tumor volume, postoperative infection, and preoperative embolization. A stepwise regression analysis of the latter variables identified 2 variables as significantly predictive: age (p = 0.0012) and duration of surgery (p = 0.0013).

Conclusions

In this study, the incidence of communicating postoperative hydrocephalus was almost twice as high in patients with skull base lesions as in patients with meningiomas in other locations. Patient age, duration of surgery, duration of hospital stay, tumor volume, postoperative infection, and preoperative embolization were associated with the occurrence of hydrocephalus. In the statistical prediction model, patient age and duration of surgery were the most significant predictors of postoperative hydrocephalus after skull base meningioma surgery.

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Pascal O. Zinn, Oliver Bozinov, Jan-Karl Burkhardt, Robert Reisch, M. Gazi Yaşargil and Helmut Bertalanffy

Mechanical obstruction is a severe complication of ventricular catheter use. Its incidence was shown to be high in the 1960s and 1970s, with up to 41% of the catheters becoming obstructed within 10 years after surgery. The authors present what is to their knowledge the first reported case of a patient with failure of a Torkildsen shunt after 50 years of functioning. A 60-year-old woman presented with increasing gait ataxia, decline in cognitive functions (including short-term memory loss), and slight urinary incontinence. The diagnosis of hydrocephalus and thus malfunction of the Torkildsen shunt implanted 50 years previously was confirmed by MR images, which revealed a prominent triventricular hydrocephalus. The patient subsequently underwent endoscopic third ventriculostomy (ETV), the current surgical treatment of choice, resulting in total resolution of her neurological symptoms and amelioration of cerebral tissue distension. Decrease in ventricle dilation and success of the ETV were confirmed on postoperative follow-up MR images.

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Michel Roethlisberger, Lara Gut, Daniel Walter Zumofen, Urs Fisch, Oliver Boss, Nicolai Maldaner, Davide Marco Croci, Ethan Taub, Natascia Corti, Jan-Karl Burkhardt, Raphael Guzman, Oliver Bozinov and Luigi Mariani

OBJECTIVE

Women taking combined hormonal contraceptives (CHCs) are generally considered to be at low risk for cerebral venous thrombosis (CVT). When it does occur, however, intensive care and neurosurgical management may, in rare cases, be needed for the control of elevated intracranial pressure (ICP). The use of nonsurgical strategies such as barbiturate coma and induced hypothermia has never been reported in this context. The objective of this study is to determine predictive factors for invasive or surgical ICP treatment and the potential complications of nonsurgical strategies in this population.

METHODS

The authors conducted a 2-center, retrospective chart review of 168 cases of CVT in women between 2000 and 2012. Eligible patients were classified as having had a mild or a severe clinical course, the latter category including all patients who underwent invasive or surgical ICP treatment and all who had an unfavorable outcome (modified Rankin Scale score ≥ 3 or Glasgow Outcome Scale score ≤ 3). The Mann-Whitney U-test was used for continuous parameters and Fisher’s exact test for categorical parameters, and odds ratios were calculated with statistical significance set at p ≤ 0.05.

RESULTS

Of the 168 patients, 57 (age range 16–49 years) were determined to be eligible for the study. Six patients (10.5%) required invasive or surgical ICP treatment. Three patients (5.3%) developed refractory ICP > 30 mm Hg despite early surgical decompression; 2 of them (3.5%) were treated with barbiturate coma and induced hypothermia, with documented infectious, thromboembolic, and hemorrhagic complications. Coma on admission, thrombosis of the deep venous system with consecutive hydrocephalus, intraventricular hemorrhage, and hemorrhagic venous infarction were associated with a higher frequency of surgical intervention. Coma, quadriparesis on admission, and hydrocephalus were more commonly seen among women with unfavorable outcomes. Thrombosis of the transverse sinus was less common in patients with an unfavorable outcome, with similar distribution in patients needing invasive or surgical ICP treatment.

CONCLUSIONS

The need for invasive or surgical ICP treatment in women taking CHCs who have CVT is partly predictable on the basis of the clinical and radiological findings on admission. The use of nonsurgical treatments for refractory ICP, such as barbiturate coma and induced hypothermia, is associated with systemic infectious and hematological complications and may worsen morbidity in this patient population. The significance of these factors should be studied in larger multicenter cohorts.

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Julia Velz, Flavio Vasella, Kevin Akeret, Sandra F. Dias, Elisabeth Jehli, Oliver Bozinov, Luca Regli, Menno R. Germans and Martin N. Stienen

OBJECTIVE

Skin depressions may appear as undesired effects after burr-hole trepanation for the evacuation of chronic subdural hematomas (cSDH). Placement of burr-hole covers to reconstruct skull defects can prevent skin depressions, with the potential to improve the aesthetic result and patient satisfaction. The perception of the relevance of this practice, however, appears to vary substantially among neurosurgeons. The authors aimed to identify current practice variations with regard to the application of burr-hole covers after trepanation for cSDH.

METHODS

An electronic survey containing 12 questions was sent to resident and faculty neurosurgeons practicing in different parts of the world, as identified by an Internet search. All responses completed between September 2018 and December 2018 were considered. Descriptive statistics and logistic regression were used to analyze the data.

RESULTS

A total of 604 responses were obtained, of which 576 (95.4%) provided complete data. The respondents’ mean age was 42.4 years (SD 10.5), and 86.5% were male. The sample consisted of residents, fellows, junior/senior consultants, and department chairs from 79 countries (77.4% Europe, 11.8% Asia, 5.4% America, 3.5% Africa, and 1.9% Australasia). Skin depressions were considered a relevant issue by 31.6%, and 76.0% indicated that patients complain about skin depressions more or less frequently. Burr-hole covers are placed by 28.1% in the context of cSDH evacuation more or less frequently. The most frequent reasons for not placing a burr-hole cover were the lack of proven benefit (34.8%), followed by additional costs (21.9%), technical difficulty (19.9%), and fear of increased complications (4.9%). Most respondents (77.5%) stated that they would consider placing burr-hole covers in the future if there was evidence for superiority of the practice. The use of burr-hole covers varied substantially across countries, but a country’s gross domestic product per capita was not associated with their placement.

CONCLUSIONS

Only a minority of neurosurgeons place burr-hole covers after trepanation for cSDH on a regular basis, even though the majority of participants reported complaints from patients regarding postoperative skin depressions. There are significant differences in the patterns of care among countries. Class I evidence with regard to patient satisfaction and safety of burr-hole cover placement is likely to have an impact on future cSDH management.

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Giovanni Muscas, Christiaan Hendrik Bas van Niftrik, Jorn Fierstra, Marco Piccirelli, Martina Sebök, Jan-Karl Burkhardt, Antonios Valavanis, Athina Pangalu, Luca Regli and Oliver Bozinov

Blood oxygenation level–dependent functional MRI cerebrovascular reactivity (BOLD-CVR) is a contemporary technique to assess brain tissue hemodynamic changes after extracranial- intracranial (EC-IC) bypass flow augmentation surgery. The authors conducted a preliminary study to investigate the feasibility and safety of intraoperative 3-T MRI BOLD-CVR after EC-IC bypass flow augmentation surgery. Five consecutive patients selected for EC-IC bypass revascularization underwent an intraoperative BOLD-CVR examination to assess early hemodynamic changes after revascularization and to confirm the safety of this technique. All patients had a normal postoperative course, and none of the patients exhibited complications or radiological alterations related to prolonged anesthesia time. In addition to intraoperative flow measurements of the bypass graft, BOLD-CVR maps added information on the hemodynamic status and changes at the brain tissue level. Intraoperative BOLD-CVR is feasible and safe in patients undergoing EC-IC bypass revascularization. This technique can offer immediate hemodynamic feedback on brain tissue revascularization after bypass flow augmentation surgery.

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Jan-Karl Burkhardt, Dörthe Schmidt, Roman Schoenauer, Chad Brokopp, Irina Agarkova, Oliver Bozinov, Helmut Bertalanffy and Simon P. Hoerstrup

Object

Cerebral cavernous malformations (CCMs) are among the most prevalent cerebrovascular malformations, and endothelial cells seem to play a major role in the disease. However, the underlying mechanisms, including endothelial intercellular communication, have not yet been fully elucidated. In this article, the authors focus on the endothelial junction proteins CD31, VE-cadherin, and occludin as important factors for functional cell-cell contacts known as vascular adhesion molecules and adherence and tight junctions.

Methods

Thirteen human CCM specimens and 6 control tissue specimens were cryopreserved and examined for the presence of VE-cadherin, occludin, and CD31 by immunofluorescence staining. Protein quantification was performed by triplicate measurements using western blot analysis.

Results

Immunofluorescent analyses of the CCM sections revealed a discontinuous pattern of dilated microvessels and capillaries as well as increased expression of occludin, VE-cadherin, and CD31 in the intima and in the enclosed parenchymal tissue compared with controls. Protein quantification confirmed these findings by showing upregulation of the levels of these proteins up to 2–6 times.

Conclusions

A protocol enabling the molecular and morphological examination of the intercellular contact proteins in human CCM was validated. The abnormal and discontinuous pattern in these endothelial cell–contact proteins compared with control tissue explains the loose intercellular junctions that are considered to be one of the causes of CCM-associated bleeding or transendothelial oozing of erythrocytes. Despite the small number of specimens, this study demonstrates for the first time a quantitative analysis of endothelial junction proteins in human CCM.

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Victor E. Staartjes, Morgan Broggi, Costanza Maria Zattra, Flavio Vasella, Julia Velz, Silvia Schiavolin, Carlo Serra, Jiri Bartek Jr., Alexander Fletcher-Sandersjöö, Petter Förander, Darius Kalasauskas, Mirjam Renovanz, Florian Ringel, Konstantin R. Brawanski, Johannes Kerschbaumer, Christian F. Freyschlag, Asgeir S. Jakola, Kristin Sjåvik, Ole Solheim, Bawarjan Schatlo, Alexandra Sachkova, Hans Christoph Bock, Abdelhalim Hussein, Veit Rohde, Marike L. D. Broekman, Claudine O. Nogarede, Cynthia M. C. Lemmens, Julius M. Kernbach, Georg Neuloh, Oliver Bozinov, Niklaus Krayenbühl, Johannes Sarnthein, Paolo Ferroli, Luca Regli, Martin N. Stienen and FEBNS

OBJECTIVE

Decision-making for intracranial tumor surgery requires balancing the oncological benefit against the risk for resection-related impairment. Risk estimates are commonly based on subjective experience and generalized numbers from the literature, but even experienced surgeons overestimate functional outcome after surgery. Today, there is no reliable and objective way to preoperatively predict an individual patient’s risk of experiencing any functional impairment.

METHODS

The authors developed a prediction model for functional impairment at 3 to 6 months after microsurgical resection, defined as a decrease in Karnofsky Performance Status of ≥ 10 points. Two prospective registries in Switzerland and Italy were used for development. External validation was performed in 7 cohorts from Sweden, Norway, Germany, Austria, and the Netherlands. Age, sex, prior surgery, tumor histology and maximum diameter, expected major brain vessel or cranial nerve manipulation, resection in eloquent areas and the posterior fossa, and surgical approach were recorded. Discrimination and calibration metrics were evaluated.

RESULTS

In the development (2437 patients, 48.2% male; mean age ± SD: 55 ± 15 years) and external validation (2427 patients, 42.4% male; mean age ± SD: 58 ± 13 years) cohorts, functional impairment rates were 21.5% and 28.5%, respectively. In the development cohort, area under the curve (AUC) values of 0.72 (95% CI 0.69–0.74) were observed. In the pooled external validation cohort, the AUC was 0.72 (95% CI 0.69–0.74), confirming generalizability. Calibration plots indicated fair calibration in both cohorts. The tool has been incorporated into a web-based application available at https://neurosurgery.shinyapps.io/impairment/.

CONCLUSIONS

Functional impairment after intracranial tumor surgery remains extraordinarily difficult to predict, although machine learning can help quantify risk. This externally validated prediction tool can serve as the basis for case-by-case discussions and risk-to-benefit estimation of surgical treatment in the individual patient.