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Agreement of novel hemodynamic imaging parameters for the acute and chronic stages of ischemic stroke: a matched-pair cohort study

Martina Sebök, Christiaan Hendrik Bas van Niftrik, Susanne Wegener, Andreas Luft, Luca Regli, and Jorn Fierstra

OBJECTIVE

In symptomatic patients with cerebrovascular steno-occlusive disease, impaired blood oxygenation level–dependent cerebrovascular reactivity (BOLD-CVR) and increased flow velocity of the P2 segment of the posterior cerebral artery (PCA-P2) on transcranial Doppler (TCD) ultrasonography have been introduced as emerging clinical imaging parameters to identify patients at high risk for recurrent ischemic events. Since hemodynamic physiology differs between the acute and chronic stages of ischemic stroke, the authors sought to investigate whether those parameters have merit for both the acute and chronic stages of ischemic stroke.

METHODS

From a prospective database, patients who underwent BOLD-CVR and TCD examinations in the acute stroke stage (< 10 days) were matched to patients in the chronic stroke stage (> 3 months). A linear regression analysis for both groups was performed between ipsilateral PCA-P2 systolic flow velocity and BOLD-CVR of the ipsilateral (affected) hemisphere, the ipsilateral middle cerebral artery (MCA) territory, and the ipsilateral steal volume (i.e., paradoxical BOLD-CVR response). The resulting slopes and intercepts were statistically compared to evaluate differences between groups.

RESULTS

Forty matched patient pairs were included. Regression analysis showed no significant difference for either the intercept (p = 0.84) or the slope (p = 0.85) between PCA-P2 flow velocity and BOLD-CVR as measured for the ipsilateral (affected) hemisphere. Similarly, no significant difference was seen between PCA-P2 flow velocity and BOLD-CVR of the ipsilateral MCA territory (intercept, p = 0.72; slope, p = 0.36) or between PCA-P2 flow velocity and steal volume (intercept, p = 0.59; slope, p = 0.34).

CONCLUSIONS

The study results indicated that the relationship between ipsilateral PCA-P2 systolic flow velocity and BOLD-CVR remains the same during the acute and chronic stages of ischemic stroke. This provides further support that these novel hemodynamic imaging parameters may have merit to assess the risk for recurrent ischemic events for a wide ischemic stroke population. PCA-P2 systolic flow velocity, in particular, may be a highly practical screening tool, independent of ischemic stroke stage.

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More pronounced hemodynamic alterations in patients with brain arteriovenous malformation–associated epilepsy

Martina Sebök, Menno Robbert Germans, Christiaan Hendrik Bas van Niftrik, Zsolt Kulcsár, Luca Regli, and Jorn Fierstra

OBJECTIVE

Epileptic seizures in patients with brain arteriovenous malformations (bAVMs) may be caused by hemodynamic alterations due to the complex angioarchitecture of bAVMs. In particular, an arterial steal phenomenon and venous outflow disruption may play an etiological role in seizure development but remain challenging to demonstrate quantitatively. Blood oxygenation level–dependent (BOLD) cerebrovascular reactivity (CVR) imaging is an emerging technique that can measure both arterial steal phenomenon (as a paradoxical BOLD signal decrease during a vasodilatory stimulus) and impaired perinidal BOLD-CVR (which has been found in the presence of venous congestion on conventional angiography in bAVM patients with epilepsy). By applying this innovative BOLD-CVR technique, the aim is to better study CVR patterns and their correlation with morphological features on conventional angiography in patients with bAVM with and without epilepsy.

METHODS

Twenty-two patients with unruptured and previously untreated bAVMs (8 with and 14 without epilepsy) were included in this case-control study. Quantitative CVR measurements were derived from BOLD functional MRI volumes using a novel standardized and precise hypercapnic stimulus (i.e., % BOLD/mm Hg CO2). In addition, 22 matched healthy controls underwent an identical BOLD-CVR study. Evaluation of venous congestion was performed on conventional angiography for all patients with bAVM.

RESULTS

Patients with bAVM-associated epilepsy showed impaired whole-brain BOLD-CVR compared to those in the nonepilepsy group, even after correction for AVM volume and AVM grade (epilepsy vs nonepilepsy group: 0.17 ± 0.07 vs 0.25 ± 0.07, p = 0.04). A BOLD-CVR–derived arterial steal phenomenon was observed in 2 patients with epilepsy (25%). Venous congestion was noted in 3 patients with epilepsy (38%) and in 1 patient without epilepsy (7%; p = 0.08).

CONCLUSIONS

These data suggest that whole-brain CVR impairment, and more pronounced hemodynamic alterations (i.e., arterial steal phenomenon and venous outflow restriction), may be more present in patients with bAVM-associated epilepsy. The association of impaired BOLD-CVR and bAVM-associated epilepsy will need further investigation in a larger patient cohort.

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Thrombocyte transfusion and rebleeding rate in patients using antiplatelet agents before aneurysmal subarachnoid hemorrhage

Martina Sebök, Natalie Zaugg, Emanuela Keller, Jan Willms, Luca Regli, and Menno Germans

OBJECTIVE

The reason for a rebleed after an initial hemorrhage in patients with aneurysmal subarachnoid hemorrhage (aSAH) is considered multifactorial. Antiplatelet use is one of the factors that has been related to early rebleed and worse outcome after aSAH. Thrombocyte transfusion overcomes the inhibitory effects of antiplatelet agents by increasing the number of functional thrombocytes, but its impact on the rebleed rate and clinical outcome remains unknown. The aim of this study was to assess the effect of thrombocyte transfusion on rebleeding and clinical outcome in patients with aSAH and prehemorrhage antiplatelet use, considering confounding factors.

METHODS

Data were prospectively collected at a single tertiary reference center for aSAH in Zurich, Switzerland. Patients with aSAH and prehemorrhage antiplatelet use were divided into "thrombocyte transfusion" and "nontransfusion" groups based on whether they did or did not receive any thrombocyte transfusion in the acute stage of aSAH after hospital admission and before the exclusion of the bleeding source. Using multivariate logistic regression analysis, the impact of thrombocyte transfusion on the rebleed rate and on clinical outcome (defined as Glasgow Outcome Scale score 1–3) was calculated.

RESULTS

One hundred fifty-seven patients were included, 87 (55.4%) of whom received thrombocyte transfusion. Eighteen (11.5%) of 157 patients had a rebleed during the hospital stay. The rebleed risk was 6.9% in the thrombocyte transfusion group and 17.1% in the nontransfusion group. After adjusting for confounders, thrombocyte transfusion showed evidence for a reduction in the rebleed rate (adjusted OR [aOR] 0.29, 95% CI 0.10–0.87). Fifty-seven patients (36.3%) achieved a poor outcome at 6 months’ follow-up. Among those 57 patients, 31 (54.4%) underwent at least one thrombocyte transfusion. Thrombocyte transfusion was not associated with poor clinical outcome at 6 months’ follow-up (aOR 0.91, 95% CI 0.39–2.15).

CONCLUSIONS

Thrombocyte transfusion in patients with aSAH and prehemorrhage antiplatelet use is independently associated with a reduction in rebleeds but shows no impact on clinical outcome at 6 months’ follow-up. Larger and randomized studies are needed to investigate the impact of thrombocyte transfusion on rebleed and outcome.

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The value of intraoperative MRI in recurrent intracranial tumor surgery

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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The value of intraoperative MRI in recurrent intracranial tumor surgery

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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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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Feasibility and safety of intraoperative BOLD functional MRI cerebrovascular reactivity to evaluate extracranial-to-intracranial bypass efficacy

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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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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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)