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Bauke M. de Jong

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YNICL Journal 2023 Journal Article

Altered brain connectivity in hyperkinetic movement disorders: A review of resting-state fMRI

  • Ramesh S. Marapin
  • Harm J. van der Horn
  • A.M. Madelein van der Stouwe
  • Jelle R. Dalenberg
  • Bauke M. de Jong
  • Marina A.J. Tijssen

BACKGROUND: Hyperkinetic movement disorders (HMD) manifest as abnormal and uncontrollable movements. Despite reported involvement of several neural circuits, exact connectivity profiles remain elusive. OBJECTIVES: Providing a comprehensive literature review of resting-state brain connectivity alterations using resting-state fMRI (rs-fMRI). We additionally discuss alterations from the perspective of brain networks, as well as correlations between connectivity and clinical measures. METHODS: A systematic review was performed according to PRISMA guidelines and searching PubMed until October 2022. Rs-fMRI studies addressing ataxia, chorea, dystonia, myoclonus, tics, tremor, and functional movement disorders (FMD) were included. The standardized mean difference was used to summarize findings per region in the Automated Anatomical Labeling atlas for each phenotype. Furthermore, the activation likelihood estimation meta-analytic method was used to analyze convergence of significant between-group differences per phenotype. Finally, we conducted hierarchical cluster analysis to provide additional insights into commonalities and differences across HMD phenotypes. RESULTS: Most articles concerned tremor (51), followed by dystonia (46), tics (19), chorea (12), myoclonus (11), FMD (11), and ataxia (8). Altered resting-state connectivity was found in several brain regions: in ataxia mainly cerebellar areas; for chorea, the caudate nucleus; for dystonia, sensorimotor and basal ganglia regions; for myoclonus, the thalamus and cingulate cortex; in tics, the basal ganglia, cerebellum, insula, and frontal cortex; for tremor, the cerebello-thalamo-cortical circuit; finally, in FMD, frontal, parietal, and cerebellar regions. Both decreased and increased connectivity were found for all HMD. Significant spatial convergence was found for dystonia, FMD, myoclonus, and tremor. Correlations between clinical measures and resting-state connectivity were frequently described. CONCLUSION: Key brain regions contributing to functional connectivity changes across HMD often overlap. Possible increases and decreases of functional connections of a specific region emphasize that HMD should be viewed as a network disorder. Despite the complex interplay of physiological and methodological factors, this review serves to gain insight in brain connectivity profiles across HMD phenotypes.

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YNICL Journal 2023 Journal Article

Comparison of univariate and multivariate analyses for brain [18F]FDG PET data in α-synucleinopathies

  • Giulia Carli
  • Sanne K. Meles
  • Fransje E. Reesink
  • Bauke M. de Jong
  • Andrea Pilotto
  • Alessandro Padovani
  • Andrea Galbiati
  • Luigi Ferini-Strambi

BACKGROUND: Brain imaging with [18F]FDG-PET can support the diagnostic work-up of patients with α-synucleinopathies. Validated data analysis approaches are necessary to evaluate disease-specific brain metabolism patterns in neurodegenerative disorders. This study compared the univariate Statistical Parametric Mapping (SPM) single-subject procedure and the multivariate Scaled Subprofile Model/Principal Component Analysis (SSM/PCA) in a cohort of patients with α-synucleinopathies. METHODS: We included [18F]FDG-PET scans of 122 subjects within the α-synucleinopathy spectrum: Parkinson's Disease (PD) normal cognition on long-term follow-up (PD - low risk to dementia (LDR); n = 28), PD who developed dementia on clinical follow-up (PD - high risk of dementia (HDR); n = 16), Dementia with Lewy Bodies (DLB; n = 67), and Multiple System Atrophy (MSA; n = 11). We also included [18F]FDG-PET scans of isolated REM sleep behaviour disorder (iRBD; n = 51) subjects with a high risk of developing a manifest α-synucleinopathy. Each [18F]FDG-PET scan was compared with 112 healthy controls using SPM procedures. In the SSM/PCA approach, we computed the individual scores of previously identified patterns for PD, DLB, and MSA: PD-related patterns (PDRP), DLBRP, and MSARP. We used ROC curves to compare the diagnostic performances of SPM t-maps (visual rating) and SSM/PCA individual pattern scores in identifying each clinical condition across the spectrum. Specifically, we used the clinical diagnoses ("gold standard") as our reference in ROC curves to evaluate the accuracy of the two methods. Experts in movement disorders and dementia made all the diagnoses according to the current clinical criteria of each disease (PD, DLB and MSA). RESULTS: The visual rating of SPM t-maps showed higher performance (AUC: 0.995, specificity: 0.989, sensitivity 1.000) than PDRP z-scores (AUC: 0.818, specificity: 0.734, sensitivity 1.000) in differentiating PD-LDR from other α-synucleinopathies (PD-HDR, DLB and MSA). This result was mainly driven by the ability of SPM t-maps to reveal the limited or absent brain hypometabolism characteristics of PD-LDR. Both SPM t-maps visual rating and SSM/PCA z-scores showed high performance in identifying DLB (DLBRP = AUC: 0.909, specificity: 0.873, sensitivity 0.866; SPM t-maps = AUC: 0.892, specificity: 0.872, sensitivity 0.910) and MSA (MSARP: AUC: 0.921, specificity: 0.811, sensitivity 1.000; SPM t-maps: AUC: 1.000, specificity: 1.000, sensitivity 1.000) from other α-synucleinopathies. PD-HDR and DLB were comparable for the brain hypo and hypermetabolism patterns, thus not allowing differentiation by SPM t-maps or SSM/PCA. Of note, we found a gradual increase of PDRP and DLBRP expression in the continuum from iRBD to PD-HDR and DLB, where the DLB patients had the highest scores. SSM/PCA could differentiate iRBD from DLB, reflecting specifically the differences in disease staging and severity (AUC: 0.938, specificity: 0.821, sensitivity 0.941). CONCLUSIONS: SPM-single subject maps and SSM/PCA are both valid methods in supporting diagnosis within the α-synucleinopathy spectrum, with different strengths and pitfalls. The former reveals dysfunctional brain topographies at the individual level with high accuracy for all the specific subtype patterns, and particularly also the normal maps; the latter provides a reliable quantification, independent from the rater experience, particularly in tracking the disease severity and staging. Thus, our findings suggest that differences in data analysis approaches exist and should be considered in clinical settings. However, combining both methods might offer the best diagnostic performance.

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YNICL Journal 2022 Journal Article

A resting-state fMRI pattern of spinocerebellar ataxia type 3 and comparison with 18F-FDG PET

  • Harm J. van der Horn
  • Sanne K. Meles
  • Jelmer G. Kok
  • Victor M. Vergara
  • Shile Qi
  • Vince D. Calhoun
  • Jelle R. Dalenberg
  • Jeroen C.W. Siero

F-FDG PET methodology. Altogether, our findings shed new light on the neural substrate of SCA3, and encourage further validation of the fSCA3-RP to assess its potential contribution as imaging biomarker for future research and clinical use.

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YNICL Journal 2021 Journal Article

Feasibility of pharmacokinetic parametric PET images in scaled subprofile modelling using principal component analysis

  • Débora E. Peretti
  • Remco J. Renken
  • Fransje E. Reesink
  • Bauke M. de Jong
  • Peter P. De Deyn
  • Rudi A.J.O. Dierckx
  • Janine Doorduin
  • Ronald Boellaard

Scaled subprofile model using principal component analysis (SSM/PCA) is a multivariate analysis technique used, mainly in [18F]-2-fluoro-2-deoxy-d-glucose (FDG) PET studies, for the generation of disease-specific metabolic patterns (DP) that may aid with the classification of subjects with neurological disorders, like Alzheimer’s disease (AD). The aim of this study was to explore the feasibility of using quantitative parametric images for this type of analysis, with dynamic [11C]-labelled Pittsburgh Compound B (PIB) PET data as an example. Therefore, 15 AD patients and 15 healthy control subjects were included in an SSM/PCA analysis to generate four AD-DPs using relative cerebral blood flow (R 1), binding potential (BP ND) and SUVR images derived from dynamic PIB and static FDG-PET studies. Furthermore, 49 new subjects with a variety of neurodegenerative cognitive disorders were tested against these DPs. The AD-DP was characterized by a reduction in the frontal, parietal, and temporal lobes voxel values for R 1 and SUVR-FDG DPs; and by a general increase of values in cortical areas for BP ND and SUVR-PIB DPs. In conclusion, the results suggest that the combination of parametric images derived from a single dynamic scan might be a good alternative for subject classification instead of using 2 independent PET studies.

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YNICL Journal 2020 Journal Article

Intrastriatal gradient analyses of 18F-FDOPA PET scans for differentiation of Parkinsonian disorders

  • Gilles N. Stormezand
  • Lumi T. Chaves
  • David Vállez García
  • Janine Doorduin
  • Bauke M. de Jong
  • Klaus L. Leenders
  • Berry P.H. Kremer
  • Rudi A.J.O. Dierckx

AIM: L -3,4-dihydroxy-6-18F-fluorophenylalanine (18F-DOPA PET may be used to distinguish subjects with Parkinsonism from those with symptoms not originating from impaired dopaminergic transmission. However, it is not routinely utilized to discriminate Idiopathic Parkinson's disease (IPD) from Atypical Parkinsonian Disorders (APD). We investigated the potential of FDOPA PET to discriminate between IPD and APD, with a focus on the anterior-to-posterior decline in het striatum, considered to be more specific for IPD. MATERIALS AND METHODS: 18F-DOPA PET data from a total of 58 subjects were retrospectively analyzed. 28 subjects had idiopathic Parkinson's disease (14 male, 14 female; age at scan 61 +- 11,5), 13 atypical Parkinsonian disease (7 male, 6 females; age at scan: 69,6 +- 6,4) and 17 were controls (6 male, 11 female; age at scan 65,3 +-8,6). Regional striatal-to-occipital ratio's (RSOR's) were calculated, as well as multiple in-line VOI's from the caudate nucleus to the posterior part of the putamen. The linearity of anteroposterior decline was determined by a linear regression fit and associated R squared values. ROC curves were calculated to assess the diagnostic performance of these measurements. Data contralateral to the clinically most affected side were used for analysis. RESULTS: ROC curve analysis for differentiation between controls and Parkinsonism patients showed the highest AUC for the caudate nucleus-to-posterior putamen ratio (AUC = 0.930; p < 0.00) and for the R squared value for the linear regression fit (AUC = 0.948; p = 0.006). For discrimating IPD from APD, the highest AUC was found for the caudate nucleus-to-anterior putamen ratio (0.824; p < 0.001) CONCLUSIONS: Subregional analysis of the striatum in F-DOPA PET scans may provide additional diagnostic information in patients screened for a presynaptic dopaminergic deficit. A more linear decrease from the head of the caudate nucleus to the posterior putamen was present in patients with IPD, although this feature did not have additional diagnostic value over the RSOR analysis.

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YNICL Journal 2020 Journal Article

The chronnectome as a model for Charcot’s ‘dynamic lesion’ in functional movement disorders

  • Ramesh S. Marapin
  • A.M. Madelein van der Stouwe
  • Bauke M. de Jong
  • Jeannette M. Gelauff
  • Victor M. Vergara
  • Vince D. Calhoun
  • Jelle R. Dalenberg
  • Yasmine E.M. Dreissen

This exploratory study set out to investigate dynamic functional connectivity (dFC) in patients with jerky and tremulous functional movement disorders (JT-FMD). The focus in this work is on dynamic brain states, which represent distinct dFC patterns that reoccur in time and across subjects. Resting-state fMRI data were collected from 17 patients with JT-FMD and 17 healthy controls (HC). Symptom severity was measured using the Clinical Global Impression-Severity scale. Depression and anxiety were measured using the Beck Depression Inventory (BDI) and Beck Anxiety Inventory (BAI), respectively. Independent component analysis was used to extract functional brain components. After computing dFC, dynamic brain states were determined for every subject using k-means clustering. Compared to HC, patients with JT-FMD spent more time in a state that was characterized predominantly by increasing medial prefrontal, and decreasing posterior midline connectivity over time. They also tended to visit this state more frequently. In addition, patients with JT-FMD transitioned significantly more often between different states compared to HC, and incorporated a state with decreasing medial prefrontal, and increasing posterior midline connectivity in their attractor, i.e., the cyclic patterns of state transitions. Altogether, this is the first study that demonstrates altered functional brain network dynamics in JT-FMD that may support concepts of increased self-reflective processes and impaired sense of agency as driving factors in FMD.

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YNICL Journal 2018 Journal Article

The cerebral metabolic topography of spinocerebellar ataxia type 3

  • Sanne K. Meles
  • Jelmer G. Kok
  • Bauke M. de Jong
  • Remco J. Renken
  • Jeroen J. de Vries
  • Jacoba M. Spikman
  • Aaltje L. Ziengs
  • Antoon T.M. Willemsen

Introduction: We aimed to uncover the pattern of network-level changes in neuronal function in Spinocerebellar ataxia type 3 (SCA3). Methods: F]‑Fluoro‑deoxyglucose Positron Emission Tomography (FDG-PET) imaging. A SCA3-related pattern (SCA3-RP) was identified using a multivariate method (scaled subprofile model and principal component analysis (SSM PCA)). Participants were evaluated with the Scale for Assessment and Rating of Ataxia (SARA) and with neuropsychological examination including tests for language, executive dysfunction, memory, and information processing speed. The relationships between SCA3-RP expression and clinical scores were explored. Voxel based morphology (VBM) was applied on MRI-T1 images to assess possible correlations between FDG reduction and grey matter atrophy. Results: = 0.04, uncorrected for multiple comparisons). Conclusion: The SCA3 metabolic profile reflects network-level alterations which are primarily associated with the motor features of the disease. Striatum decreases additional to cerebellar hypometabolism underscores an intrinsic extrapyramidal involvement in SCA3. Cerebellar-posterior parietal hypometabolism together with anterior parietal (sensory) cortex hypermetabolism may reflect a shift from impaired feedforward to compensatory feedback processing in higher-order motor control. The demonstrated SCA3-RP provides basic insight in cerebral network changes in this disease.

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YNICL Journal 2016 Journal Article

Bilateral cerebellar activation in unilaterally challenged essential tremor

  • Marja Broersma
  • Anna M.M. van der Stouwe
  • Arthur W.G. Buijink
  • Bauke M. de Jong
  • Paul F.C. Groot
  • Johannes D. Speelman
  • Marina A.J. Tijssen
  • Anne-Fleur van Rootselaar

BACKGROUND: Essential tremor (ET) is one of the most common hyperkinetic movement disorders. Previous research into the pathophysiology of ET suggested underlying cerebellar abnormalities. OBJECTIVE: In this study, we added electromyography as an index of tremor intensity to functional Magnetic Resonance Imaging (EMG-fMRI) to study a group of ET patients selected according to strict criteria to achieve maximal homogeneity. With this approach we expected to improve upon the localization of the bilateral cerebellar abnormalities found in earlier fMRI studies. METHODS: We included 21 propranolol sensitive patients, who were not using other tremor medication, with a definite diagnosis of ET defined by the Tremor Investigation Group. Simultaneous EMG-fMRI recordings were performed while patients were off tremor medication. Patients performed unilateral right hand and arm extension, inducing tremor, alternated with relaxation (rest). Twenty-one healthy, age- and sex-matched participants mimicked tremor during right arm extension. EMG power variability at the individual tremor frequency as a measure of tremor intensity variability was used as a regressor, mathematically independent of the block regressor, in the general linear model used for fMRI analysis, to find specific tremor-related activations. RESULTS: Block-related activations were found in the classical upper-limb motor network, both for ET patients and healthy participants in motor, premotor and supplementary motor areas. In ET patients, we found tremor-related activations bilaterally in the cerebellum: in left lobules V, VI, VIIb and IX and in right lobules V, VI, VIIIa and b, and in the brainstem. In healthy controls we found simulated tremor-related activations in right cerebellar lobule V. CONCLUSIONS: Our results expand on previous findings of bilateral cerebellar involvement in ET. We have identified specific areas in the bilateral somatomotor regions of the cerebellum: lobules V, VI and VIII.

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YNICL Journal 2016 Journal Article

Relation of 18-F-Dopa PET with hypokinesia-rigidity, tremor and freezing in Parkinson’s disease

  • Angelina R.A. Pikstra
  • Anouk van der Hoorn
  • Klaus L. Leenders
  • Bauke M. de Jong

INTRODUCTION: In this retrospective study concerning patients with Parkinson's disease (PD) scanned with 18-F-Dopa PET (N = 129), we looked for an association between reduced 18-F-Dopa uptake and the key PD symptoms tremor and hypokinesia-rigidity. We hypothesized to find a stronger correlation between dopaminergic depletion in the striatum and hypokinesia-rigidity compared to tremor. METHODS: The onset side of symptoms (documented for 102 patients) as well as the first registered UPDRS (available for 79 patients) was used to correlate with F-Dopa uptake values in the caudate nucleus and putamen in this large retrospective sample. RESULTS: Reduced F-Dopa uptake was contralateral to hypokinesia-rigidity symptoms and correlated with its severity (quantified by UPDRS). For tremor severity, no correlation was seen with F-Dopa reduction. Furthermore, freezing of gait correlated with reduced F-Dopa uptake in the putamen of the right hemisphere. CONCLUSION AND DISCUSSION: Our results, obtained in a large patient group, provides support for the concept that tremor in PD is not only based on a dopamine related pathway but may rely on a different pathway.

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YNICL Journal 2014 Journal Article

Parkinson's disease-related perfusion and glucose metabolic brain patterns identified with PCASL-MRI and FDG-PET imaging

  • Laura K. Teune
  • Remco J. Renken
  • Bauke M. de Jong
  • Antoon T. Willemsen
  • Matthias J. van Osch
  • Jos B.T.M. Roerdink
  • Rudi A. Dierckx
  • Klaus L. Leenders

INTRODUCTION: Under normal conditions, the spatial distribution of resting cerebral blood flow and cerebral metabolic rate of glucose are closely related. A relatively new magnetic resonance (MR) technique, pseudo-continuous arterial spin labeling (PCASL), can be used to measure regional brain perfusion. We identified a Parkinson's disease (PD)-related perfusion and metabolic covariance pattern in the same patients using PCASL and FDG-PET imaging and assessed (dis)similarities in the disease-related pattern between perfusion and metabolism in PD patients. METHODS: Nineteen PD patients and seventeen healthy controls underwent [(18)F]-fluorodeoxyglucose positron emission tomography (FDG-PET) imaging. Of 14 PD patients and all healthy controls PCASL-MRI could be obtained. Data were analyzed using scaled subprofile model/principal component analysis (SSM/PCA). RESULTS: Unique Parkinson's disease-related perfusion and metabolic covariance patterns were identified using PCASL and FDG-PET in the same patients. The PD-related metabolic covariance brain pattern is in high accordance with previously reports. Also our disease-related perfusion pattern is comparable to the earlier described perfusion pattern. The most marked difference between our perfusion and metabolic patterns is the larger perfusion decrease in cortical regions including the insula. CONCLUSION: We identified PD-related perfusion and metabolic brain patterns using PCASL and FDG-PET in the same patients which were comparable with results of existing research. In this respect, PCASL appears to be a promising addition in the early diagnosis of individual parkinsonian patients.

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