Christiaan Hendrik Bas van Niftrik

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Hemodynamic Evaluation of Paradoxical Blood Oxygenation Level-Dependent Cerebrovascular Reactivity with Transcranial Doppler and MR Perfusion in Patients with Symptomatic Cerebrovascular Steno-occlusive Disease

Neuromethods (2021)

Christiaan Hendrik Bas van Niftrik Martina Sebök Giovanni Muscas Aimée Hiller Matthias Halter

Background and Purpose: In patients with steno-occlusive disease, paradoxical blood oxygenation level-dependent fMRI cerebrovascular reactivity (BOLD-CVR) is a feasible surrogate marker for hemodynamic impairment. BOLD-CVR, however, does not measure hemodynamic changes directly; hence, we study complementary hemodynamic features in brain areas exhibiting paradoxical BOLD-CVR using perfusion-weighted MRI (PW-MRI) and transcranial Doppler (TCD). Methods: Twenty participants with unilateral symptomatic chronic cerebrovascular steno-occlusive disease and ipsilateral paradoxical BOLD-CVR were studied. The region with paradoxical BOLD-CVR was used as a region of interest for the PW-MRI-weighted images. As a comparison, a contralateral analysis was done. Ipsilateral and contralateral TCDTranscranial doppler (TCD) flow velocities of the posterior circulation were compared as an indicator of collateral supply. Results: Brain tissue exhibiting paradoxical BOLD-CVR showed prolonged mean transit time and time-to-peak with increased cerebral blood volume. CBFCerebral blood flow (CBF) followed a post-stroke time evolution. The ipsilateral posterior cerebral artery (PCA)-P2 segment flow velocity was significantly increased compared to the contralateral side, correlating strongly with the paradoxical BOLD-CVR brain tissue volume. Conclusions: In symptomatic steno-occlusive patients, brain areas with ipsilateral paradoxical BOLD-CVR show clear hemodynamicHemodynamics changes, i.e., prolonged mean transit time and time-to-peak and increased cerebral blood volume. Moreover, increased flow velocities in the ipsilateral PCA-P2 segment indicate increased hemodynamicHemodynamics efforts due to increased need for collateral supply from the posterior circulation. This further supports the premise that paradoxical BOLD-CVR within the symptomatic hemisphere is a reliable surrogate for exhausted perfusion reservePerfusion reserve and should be studied in an independent study cohort to determine its value for predicting strokeStrokes risk.

Transcranial Doppler

Posterior cerebral artery

Collateral circulation

10.1007/978-1-0716-1763-2_6

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Citations (1)

The voxel-wise analysis of false negative fMRI activation in regions of provoked impaired cerebrovascular reactivity

PLoS ONE (2019)

Christiaan Hendrik Bas van Niftrik Marco Piccirelli Giovanni Muscas Martina Sebök Joseph A. Fisher

Task-evoked Blood-oxygenation-level-dependent (BOLD-fMRI) signal activation is widely used to interrogate eloquence of brain areas. However, data interpretation can be improved, especially in regions with absent BOLD-fMRI signal activation. Absent BOLD-fMRI signal activation may actually represent false-negative activation due to impaired cerebrovascular reactivity (BOLD-CVR) of the vascular bed. The relationship between impaired BOLD-CVR and BOLD-fMRI signal activation may be better studied in healthy subjects where neurovascular coupling is known to be intact. Using a model-based prospective end-tidal carbon dioxide (CO2) targeting algorithm, we performed two controlled 3 tesla BOLD-CVR studies on 17 healthy subjects: 1: at the subjects' individual resting end-tidal CO2 baseline. 2: Around +6.0 mmHg CO2 above the subjects' individual resting baseline. Two BOLD-fMRI finger-tapping experiments were performed at similar normo- and hypercapnic levels. Relative BOLD fMRI signal activation and t-values were calculated for BOLD-CVR and BOLD-fMRI data. For each component of the cerebral motor-network (precentral gyrus, postcentral gyrus, supplementary motor area, cerebellum und fronto-operculum), the correlation between BOLD-CVR and BOLD-fMRI signal changes and t-values was investigated. Finally, a voxel-wise quantitative analysis of the impact of BOLD-CVR on BOLD-fMRI was performed. For the motor-network, the linear correlation coefficient between BOLD-CVR and BOLD-fMRI t-values were significant (p<0.01) and in the range 0.33–0.55, similar to the correlations between the CVR and fMRI Δ%signal (p<0.05; range 0.34–0.60). The linear relationship between CVR and fMRI is challenged by our voxel-wise analysis of Δ%signal and t-value change between normo- and hypercapnia. Our main finding is that BOLD fMRI signal activation maps are markedly dampened in the presence of impaired BOLD-CVR and highlights the importance of a complementary BOLD-CVR assessment in addition to a task-evoked BOLD fMRI to identify brain areas at risk for false-negative BOLD-fMRI signal activation.

Postcentral gyrus

Blood-oxygen-level dependent

Precentral gyrus

Brain mapping

EEG-fMRI

Supplementary motor area

Blood oxygenation

10.1371/journal.pone.0215294

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Citations (9)

Machine Learning Algorithms in Neuroimaging: An Overview

Acta neurochirurgica. Supplementum (2021)

Vittorio Stumpo Julius M. Kernbach Christiaan Hendrik Bas van Niftrik Martina Sebök Jorn Fierstra

Neuroradiology

Interventional radiology

10.1007/978-3-030-85292-4_17

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Neural network–based identification of patients at high risk for intraoperative cerebrospinal fluid leaks in endoscopic pituitary surgery

Journal of neurosurgery (2019)

Victor E. Staartjes Costanza Maria Zattra Kevin Akeret Nicolai Maldaner Giovanni Muscas

OBJECTIVE Although rates of postoperative morbidity and mortality have become relatively low in patients undergoing transnasal transsphenoidal surgery (TSS) for pituitary adenoma, cerebrospinal fluid (CSF) fistulas remain a major driver of postoperative morbidity. Persistent CSF fistulas harbor the potential for headache and meningitis. The aim of this study was to investigate whether neural network–based models can reliably identify patients at high risk for intraoperative CSF leakage. METHODS From a prospective registry, patients who underwent endoscopic TSS for pituitary adenoma were identified. Risk factors for intraoperative CSF leaks were identified using conventional statistical methods. Subsequently, the authors built a prediction model for intraoperative CSF leaks based on deep learning. RESULTS Intraoperative CSF leaks occurred in 45 (29%) of 154 patients. No risk factors for CSF leaks were identified using conventional statistical methods. The deep neural network–based prediction model classified 88% of patients in the test set correctly, with an area under the curve of 0.84. Sensitivity (83%) and specificity (89%) were high. The positive predictive value was 71%, negative predictive value was 94%, and F1 score was 0.77. High suprasellar Hardy grade, prior surgery, and older age contributed most to the predictions. CONCLUSIONS The authors trained and internally validated a robust deep neural network–based prediction model that identifies patients at high risk for intraoperative CSF. Machine learning algorithms may predict outcomes and adverse events that were previously nearly unpredictable, thus enabling safer and improved patient care and better patient counseling.

Transsphenoidal surgery

10.3171/2019.4.jns19477

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Citations (46)

Blood oxygen‐level dependent functional assessment of cerebrovascular reactivity: Feasibility for intraoperative 3 Tesla MRI

Magnetic Resonance in Medicine (2016)

Jorn Fierstra Jan‐Karl Burkhardt Christiaan Hendrik Bas van Niftrik Marco Piccirelli Athina Pangalu

To assess the feasibility of functional blood oxygen-level dependent (BOLD) MRI to evaluate intraoperative cerebrovascular reactivity (CVR) at 3 Tesla field strength.Ten consecutive neurosurgical subjects scheduled for a clinical intraoperative MRI examination were enrolled in this study. In addition to the clinical protocol a BOLD sequence was implemented with three cycles of 44 s apnea to calculate CVR values on a voxel-by-voxel basis throughout the brain. The CVR range was then color-coded and superimposed on an anatomical volume to create high spatial resolution CVR maps.Ten subjects (mean age 34.8 ± 13.4; 2 females) uneventfully underwent the intraoperative BOLD protocol, with no complications occurring. Whole-brain CVR for all subjects was (mean ± SD) 0.69 ± 0.42, whereas CVR was markedly higher for tumor subjects as compared to vascular subjects, 0.81 ± 0.44 versus 0.33 ± 0.10, respectively. Furthermore, color-coded functional maps could be robustly interpreted for a whole-brain assessment of CVR.We demonstrate that intraoperative BOLD MRI is feasible in creating functional maps to assess cerebrovascular reactivity throughout the brain in subjects undergoing a neurosurgical procedure. Magn Reson Med 77:806-813, 2017. © 2016 International Society for Magnetic Resonance in Medicine.

Blood-oxygen-level dependent

10.1002/mrm.26135

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Citations (12)

Distinct Cerebrovascular Reactivity Patterns for Brain Radiation Necrosis

Cancers (2021)

Giovanni Muscas Christiaan Hendrik Bas van Niftrik Martina Sebök Alessandro Della Puppa Katharina Seystahl

Background: Current imaging-based discrimination between radiation necrosis versus recurrent glioblastoma contrast-enhancing lesions remains imprecise but is paramount for prognostic and therapeutic evaluation. We examined whether patients with radiation necrosis exhibit distinct patterns of blood oxygenation-level dependent fMRI cerebrovascular reactivity (BOLD-CVR) as the first step to better distinguishing patients with radiation necrosis from recurrent glioblastoma compared with patients with newly diagnosed glioblastoma before surgery and radiotherapy. Methods: Eight consecutive patients with primary and secondary brain tumors and a multidisciplinary clinical and radiological diagnosis of radiation necrosis, and fourteen patients with a first diagnosis of glioblastoma underwent BOLD-CVR mapping. For all these patients, the contrast-enhancing lesion was derived from high-resolution T1-weighted MRI and rendered the volume-of-interest (VOI). From this primary VOI, additional 3 mm concentric expanding VOIs up to 30 mm were created for a detailed perilesional BOLD-CVR tissue analysis between the two groups. Receiver operating characteristic curves assessed the discriminative properties of BOLD-CVR for both groups. Results: Mean intralesional BOLD-CVR values were markedly lower in radiation necrosis than in glioblastoma contrast-enhancing lesions (0.001 ± 0.06 vs. 0.057 ± 0.05; p = 0.04). Perilesionally, a characteristic BOLD-CVR pattern was observed for radiation necrosis and glioblastoma patients, with an improvement of BOLD-CVR values in the radiation necrosis group and persisting lower perilesional BOLD-CVR values in glioblastoma patients. The ROC analysis discriminated against both groups when these two parameters were analyzed together (area under the curve: 0.85, 95% CI: 0.65–1.00). Conclusions: In this preliminary analysis, distinctive intralesional and perilesional BOLD-cerebrovascular reactivity patterns are found for radiation necrosis.

10.3390/cancers13081840

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Citations (4)

Hemodynamic investigation of peritumoral impaired blood oxygenation-level dependent cerebrovascular reactivity in patients with diffuse glioma

Magnetic Resonance Imaging (2020)

Giovanni Muscas Christiaan Hendrik Bas van Niftrik Martina Sebök Katharina Seystahl Marco Piccirelli

The presence of peritumorally impaired blood oxygenation-level dependent cerebrovascular reactivity (BOLD-CVR) has been unequivocally demonstrated in patients with diffuse glioma, and may have value to better identify tumor infiltration zone. Since BOLD-CVR does not measure hemodynamic changes directly, we performed additional MR perfusion studies to better characterize the peritumoral hemodynamic environment.Seventeen patients with WHO grade III and IV diffuse glioma underwent high resolution advanced hemodynamic MR imaging including BOLD-CVR and MR perfusion. The obtained multiparametric hemodynamic factors (i.e., regional cerebral blood flow (rCBF), relative cerebral blood volume (rCBV), mean transit time (MTT), time-to-peak (TTP) and BOLD-CVR, were analyzed within 10 concentric expanding 3 mm volumes of interest (VOIs) up to 30 mm from the tumor tissue mask.BOLD-CVR impairment was found within the tumor tissue mask and the peritumoral VOIs up to 21 mm as compared to the contralateral flipped CVR analysis (p<0.05). In the affected hemisphere, we observed positive spatial correlations including all VOIs between BOLD-CVR and rCBV values (r=0.27; p<0.001), rCBF (r=0.42; p<0.001) and a negative correlation between BOLD-CVR and TTP (r=-0.47; p<0.001).Peritumorally impaired BOLD-CVR is associated with concomitant hemodynamic alterations with severity correlating to tumor volume. The distribution of these multiparametric hemodynamic MRI patterns may be considered for future studies characterizing the hemodynamic peritumoral environment, thereby better identifying the extent of tumor infiltration.

10.1016/j.mri.2020.03.012

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Citations (7)

Delayed cerebral atrophy after cerebellar stroke: topographical relation and clinical impact

Brain Communications (2021)

Christiaan Hendrik Bas van Niftrik Thomas Visser Martina Sebök Giovanni Muscas Mohamad El Amki

Remote dysconnectivity following cerebellar ischaemic stroke may have a negative impact on supratentorial brain tissue. Since the cerebellum is connected to the individual cerebral lobes via contralateral tracts, cerebellar lesion topography might determine the distribution of contralateral supratentorial brain tissue changes. We investigated (i) the occurrence of delayed cerebral atrophy after cerebellar ischaemic stroke and its relationship to infarct volume; (ii) whether cerebellar stroke topography determines supratentorial atrophy location; and (iii) how cortical atrophy after cerebellar stroke impacts clinical outcome. We performed longitudinal volumetric MRI analysis of patients with isolated cerebellar stroke from the Swiss Stroke Registry database. Stroke location and volume were determined at baseline MRI. Delayed cerebral atrophy was measured as supratentorial cortical volumetric change at follow-up, in contralateral target as compared to ipsilateral reference-areas. In patients with bilateral stroke, both hemispheres were analysed separately. We obtained maps of how cerebellar lesion topography, determines the probability of delayed atrophy per distinct cerebral lobe. Clinical performance was measured with the National Institutes of Health Stroke Scale and modified Rankin Scale. In 29 patients (age 58 ± 18; 9 females; median follow-up: 6.2 months), with 36 datasets (7 patients with bilateral cerebellar stroke), delayed cerebral atrophy occurred in 28 (78%) datasets. A multivariable generalized linear model for a Poisson distribution showed that infarct volume (milliliter) in bilateral stroke patients was positively associated with the number of atrophic target areas (Rate ratio = 1.08; P = 0.01). Lobe-specific cerebral atrophy related to distinct topographical cerebellar stroke patterns. By ordinal logistic regression (shift analysis), more atrophic areas predicted higher 3-month mRS scores in patients with low baseline scores (baseline score 3-5: Odds ratio = 1.34; P = 0.02; baseline score 0-2: OR = 0.71; P = 0.19). Our results indicate that (i) isolated cerebellar ischaemic stroke commonly results in delayed cerebral atrophy and stroke volume determines the severity of cerebral atrophy in patients with bilateral stroke; (ii) cerebellar stroke topography affects the location of delayed cerebral atrophy; and (iii) delayed cerebral atrophy negatively impacts clinical outcome.

Stroke

Frontal lobe

10.1093/braincomms/fcab279

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Citations (6)

Crossed Cerebellar Diaschisis Indicates Hemodynamic Compromise in Ischemic Stroke Patients

Translational Stroke Research (2020)

Lita von Bieberstein Christiaan Hendrik Bas van Niftrik Martina Sebök Mohamad El Amki Marco Piccirelli

Abstract Crossed cerebellar diaschisis (CCD) in internal carotid artery (ICA) stroke refers to attenuated blood flow and energy metabolism in the contralateral cerebellar hemisphere. CCD is associated with an interruption of cerebro-cerebellar tracts, but the precise mechanism is unknown. We hypothesized that in patients with ICA occlusions, CCD might indicate severe hemodynamic impairment in addition to tissue damage. Duplex sonography and clinical data from stroke patients with unilateral ICAO who underwent blood oxygen-level-dependent MRI cerebrovascular reserve (BOLD-CVR) assessment were analysed. The presence of CCD (either CCD+ or CCD−) was inferred from BOLD-CVR. We considered regions with negative BOLD-CVR signal as areas suffering from hemodynamic steal. Twenty-five patients were included (11 CCD+ and 14 CCD−). Stroke deficits on admission and at 3 months were more severe in the CCD+ group. While infarct volumes were similar, CCD+ patients had markedly larger BOLD steal volumes than CCD− patients (median [IQR] 122.2 [111] vs. 11.6 [50.6] ml; p < 0.001). Furthermore, duplex revealed higher peak-systolic flow velocities in the intracranial collateral pathways. Strikingly, posterior cerebral artery (PCA)-P2 velocities strongly correlated with the National Institute of Health Stroke Scale on admission and BOLD-CVR steal volume. In patients with strokes due to ICAO, the presence of CCD indicated hemodynamic impairment with larger BOLD-defined steal volume and higher flow in the ACA/PCA collateral system. Our data support the concept of a vascular component of CCD as an indicator of hemodynamic failure in patients with ICAO.

Diaschisis

Stroke

10.1007/s12975-020-00821-0

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Citations (21)

Transient deoxyhemoglobin formation as a contrast for perfusion MRI studies in patients with brain tumors: a feasibility study

Frontiers in Physiology (2024)

Vittorio Stumpo Ece Su Sayin Jacopo Bellomo Olivia Sobczyk Christiaan Hendrik Bas van Niftrik

Background: Transient hypoxia-induced deoxyhemoglobin (dOHb) has recently been shown to represent a comparable contrast to gadolinium-based contrast agents for generating resting perfusion measures in healthy subjects. Here, we investigate the feasibility of translating this non-invasive approach to patients with brain tumors. Methods: A computer-controlled gas blender was used to induce transient precise isocapnic lung hypoxia and thereby transient arterial dOHb during echo-planar-imaging acquisition in a cohort of patients with different types of brain tumors (n = 9). We calculated relative cerebral blood volume (rCBV), cerebral blood flow (rCBF), and mean transit time (MTT) using a standard model-based analysis. The transient hypoxia induced-dOHb MRI perfusion maps were compared to available clinical DSC-MRI. Results: Transient hypoxia induced-dOHb based maps of resting perfusion displayed perfusion patterns consistent with underlying tumor histology and showed high spatial coherence to gadolinium-based DSC MR perfusion maps. Conclusion: Non-invasive transient hypoxia induced-dOHb was well-tolerated in patients with different types of brain tumors, and the generated rCBV, rCBF and MTT maps appear in good agreement with perfusion maps generated with gadolinium-based DSC MR perfusion.

10.3389/fphys.2024.1238533

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Citations (1)