Dopaminergic and Serotonergic Degeneration and Cortical [18F]Fluorodeoxyglucose Positron Emission Tomography in De Novo Parkinson's Disease

Background Degeneration of the nigrostriatal dopaminergic (DA) and the raphe‐thalamic serotonergic (SE) systems is among the earliest changes observed in Parkinson's disease (PD). The consequences of those changes on brain metabolism, especially regarding their impact on the cortex, are poorly...

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Published inMovement disorders Vol. 36; no. 10; pp. 2293 - 2302
Main Authors Orso, Beatrice, Arnaldi, Dario, Girtler, Nicola, Brugnolo, Andrea, Doglione, Elisa, Mattioli, Pietro, Biassoni, Erica, Fancellu, Roberto, Massa, Federico, Bauckneht, Matteo, Chiola, Silvia, Morbelli, Silvia, Nobili, Flavio, Pardini, Matteo
Format Journal Article
LanguageEnglish
Published Hoboken, USA John Wiley & Sons, Inc 01.10.2021
Wiley Subscription Services, Inc
Subjects
Computed tomography
cortical degeneration
Dopamine receptors
Drug metabolism
Glucose metabolism
Innervation
Metabolism
Movement disorders
Neostriatum
Neurodegeneration
Neurodegenerative diseases
Neuroimaging
nigrostriatal degeneration
Parkinson's disease
Positron emission tomography
Putamen
Single photon emission computed tomography
striatum
Substantia grisea
Thalamus
Tomography
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Abstract Background Degeneration of the nigrostriatal dopaminergic (DA) and the raphe‐thalamic serotonergic (SE) systems is among the earliest changes observed in Parkinson's disease (PD). The consequences of those changes on brain metabolism, especially regarding their impact on the cortex, are poorly understood. Objectives Using multi‐tracer molecular imaging, we assessed in a cohort of drug‐naive PD patients the association between cortical metabolism and DA and SE system deafferentation of either striatum or thalamus, and we explored whether this association was mediated by either striatum or thalamus metabolism. Methods We recruited 96 drug‐naive PD patients (aged 71.9 ± 7.5 years) who underwent [123I]ioflupane single‐photon emission computed tomography ([123I]FP‐CIT‐SPECT) and brain [18F]fluorodeoxyglucose positron emission tomography ([18F]FDG‐PET). We used a voxel‐wise analysis of [18F]FDG‐PET images to correlate regional metabolism with striatal DA and thalamic SE innervation as assessed using [123I]FP‐CIT‐SPECT. Results We found that [123I]FP‐CIT specific to nondisplaceable binding ratio (SBR) and glucose metabolism positively correlated with one another in the deep gray matter (thalamus: P = 0.001, r = 0.541; caudate P = 0.001, r = 0.331; putamen P = 0.001, r = 0.423). We then observed a direct correlation between temporoparietal metabolism and caudate DA innervation, as well as a direct correlation between prefrontal metabolism and thalamus SE innervation. The effect of caudate [123I]FP‐CIT SBR values on temporoparietal metabolism was mediated by caudate metabolic values (percentage mediated: 89%, P‐value = 0.008), and the effect of thalamus [123I]FP‐CIT SBR values on prefrontal metabolism was fully mediated by thalamus metabolic values (P < 0.001). Conclusions These data suggest that the impact of deep gray matter monoaminergic deafferentation on cortical function is mediated by striatal and thalamic metabolism in drug‐naive PD. © 2021 International Parkinson and Movement Disorder Society
AbstractList BACKGROUNDDegeneration of the nigrostriatal dopaminergic (DA) and the raphe-thalamic serotonergic (SE) systems is among the earliest changes observed in Parkinson's disease (PD). The consequences of those changes on brain metabolism, especially regarding their impact on the cortex, are poorly understood. OBJECTIVESUsing multi-tracer molecular imaging, we assessed in a cohort of drug-naive PD patients the association between cortical metabolism and DA and SE system deafferentation of either striatum or thalamus, and we explored whether this association was mediated by either striatum or thalamus metabolism. METHODSWe recruited 96 drug-naive PD patients (aged 71.9 ± 7.5 years) who underwent [123 I]ioflupane single-photon emission computed tomography ([123 I]FP-CIT-SPECT) and brain [18 F]fluorodeoxyglucose positron emission tomography ([18 F]FDG-PET). We used a voxel-wise analysis of [18 F]FDG-PET images to correlate regional metabolism with striatal DA and thalamic SE innervation as assessed using [123 I]FP-CIT-SPECT. RESULTSWe found that [123 I]FP-CIT specific to nondisplaceable binding ratio (SBR) and glucose metabolism positively correlated with one another in the deep gray matter (thalamus: P = 0.001, r = 0.541; caudate P = 0.001, r = 0.331; putamen P = 0.001, r = 0.423). We then observed a direct correlation between temporoparietal metabolism and caudate DA innervation, as well as a direct correlation between prefrontal metabolism and thalamus SE innervation. The effect of caudate [123 I]FP-CIT SBR values on temporoparietal metabolism was mediated by caudate metabolic values (percentage mediated: 89%, P-value = 0.008), and the effect of thalamus [123 I]FP-CIT SBR values on prefrontal metabolism was fully mediated by thalamus metabolic values (P < 0.001). CONCLUSIONSThese data suggest that the impact of deep gray matter monoaminergic deafferentation on cortical function is mediated by striatal and thalamic metabolism in drug-naive PD. © 2021 International Parkinson and Movement Disorder Society.
BackgroundDegeneration of the nigrostriatal dopaminergic (DA) and the raphe‐thalamic serotonergic (SE) systems is among the earliest changes observed in Parkinson's disease (PD). The consequences of those changes on brain metabolism, especially regarding their impact on the cortex, are poorly understood.ObjectivesUsing multi‐tracer molecular imaging, we assessed in a cohort of drug‐naive PD patients the association between cortical metabolism and DA and SE system deafferentation of either striatum or thalamus, and we explored whether this association was mediated by either striatum or thalamus metabolism.MethodsWe recruited 96 drug‐naive PD patients (aged 71.9 ± 7.5 years) who underwent [123I]ioflupane single‐photon emission computed tomography ([123I]FP‐CIT‐SPECT) and brain [18F]fluorodeoxyglucose positron emission tomography ([18F]FDG‐PET). We used a voxel‐wise analysis of [18F]FDG‐PET images to correlate regional metabolism with striatal DA and thalamic SE innervation as assessed using [123I]FP‐CIT‐SPECT.ResultsWe found that [123I]FP‐CIT specific to nondisplaceable binding ratio (SBR) and glucose metabolism positively correlated with one another in the deep gray matter (thalamus: P = 0.001, r = 0.541; caudate P = 0.001, r = 0.331; putamen P = 0.001, r = 0.423). We then observed a direct correlation between temporoparietal metabolism and caudate DA innervation, as well as a direct correlation between prefrontal metabolism and thalamus SE innervation. The effect of caudate [123I]FP‐CIT SBR values on temporoparietal metabolism was mediated by caudate metabolic values (percentage mediated: 89%, P‐value = 0.008), and the effect of thalamus [123I]FP‐CIT SBR values on prefrontal metabolism was fully mediated by thalamus metabolic values (P < 0.001).ConclusionsThese data suggest that the impact of deep gray matter monoaminergic deafferentation on cortical function is mediated by striatal and thalamic metabolism in drug‐naive PD. © 2021 International Parkinson and Movement Disorder Society
Background Degeneration of the nigrostriatal dopaminergic (DA) and the raphe‐thalamic serotonergic (SE) systems is among the earliest changes observed in Parkinson's disease (PD). The consequences of those changes on brain metabolism, especially regarding their impact on the cortex, are poorly understood. Objectives Using multi‐tracer molecular imaging, we assessed in a cohort of drug‐naive PD patients the association between cortical metabolism and DA and SE system deafferentation of either striatum or thalamus, and we explored whether this association was mediated by either striatum or thalamus metabolism. Methods We recruited 96 drug‐naive PD patients (aged 71.9 ± 7.5 years) who underwent [123I]ioflupane single‐photon emission computed tomography ([123I]FP‐CIT‐SPECT) and brain [18F]fluorodeoxyglucose positron emission tomography ([18F]FDG‐PET). We used a voxel‐wise analysis of [18F]FDG‐PET images to correlate regional metabolism with striatal DA and thalamic SE innervation as assessed using [123I]FP‐CIT‐SPECT. Results We found that [123I]FP‐CIT specific to nondisplaceable binding ratio (SBR) and glucose metabolism positively correlated with one another in the deep gray matter (thalamus: P = 0.001, r = 0.541; caudate P = 0.001, r = 0.331; putamen P = 0.001, r = 0.423). We then observed a direct correlation between temporoparietal metabolism and caudate DA innervation, as well as a direct correlation between prefrontal metabolism and thalamus SE innervation. The effect of caudate [123I]FP‐CIT SBR values on temporoparietal metabolism was mediated by caudate metabolic values (percentage mediated: 89%, P‐value = 0.008), and the effect of thalamus [123I]FP‐CIT SBR values on prefrontal metabolism was fully mediated by thalamus metabolic values (P < 0.001). Conclusions These data suggest that the impact of deep gray matter monoaminergic deafferentation on cortical function is mediated by striatal and thalamic metabolism in drug‐naive PD. © 2021 International Parkinson and Movement Disorder Society
Abstract Background Degeneration of the nigrostriatal dopaminergic (DA) and the raphe‐thalamic serotonergic (SE) systems is among the earliest changes observed in Parkinson's disease (PD). The consequences of those changes on brain metabolism, especially regarding their impact on the cortex, are poorly understood. Objectives Using multi‐tracer molecular imaging, we assessed in a cohort of drug‐naive PD patients the association between cortical metabolism and DA and SE system deafferentation of either striatum or thalamus, and we explored whether this association was mediated by either striatum or thalamus metabolism. Methods We recruited 96 drug‐naive PD patients (aged 71.9 ± 7.5 years) who underwent [ 123 I]ioflupane single‐photon emission computed tomography ([ 123 I]FP‐CIT‐SPECT) and brain [ 18 F]fluorodeoxyglucose positron emission tomography ([ 18 F]FDG‐PET). We used a voxel‐wise analysis of [ 18 F]FDG‐PET images to correlate regional metabolism with striatal DA and thalamic SE innervation as assessed using [ 123 I]FP‐CIT‐SPECT. Results We found that [ 123 I]FP‐CIT specific to nondisplaceable binding ratio (SBR) and glucose metabolism positively correlated with one another in the deep gray matter (thalamus: P  = 0.001, r = 0.541; caudate P  = 0.001, r = 0.331; putamen P  = 0.001, r = 0.423). We then observed a direct correlation between temporoparietal metabolism and caudate DA innervation, as well as a direct correlation between prefrontal metabolism and thalamus SE innervation. The effect of caudate [ 123 I]FP‐CIT SBR values on temporoparietal metabolism was mediated by caudate metabolic values (percentage mediated: 89%, P ‐value = 0.008), and the effect of thalamus [ 123 I]FP‐CIT SBR values on prefrontal metabolism was fully mediated by thalamus metabolic values ( P  < 0.001). Conclusions These data suggest that the impact of deep gray matter monoaminergic deafferentation on cortical function is mediated by striatal and thalamic metabolism in drug‐naive PD. © 2021 International Parkinson and Movement Disorder Society
Author Pardini, Matteo
Chiola, Silvia
Doglione, Elisa
Fancellu, Roberto
Bauckneht, Matteo
Girtler, Nicola
Morbelli, Silvia
Arnaldi, Dario
Orso, Beatrice
Massa, Federico
Biassoni, Erica
Nobili, Flavio
Mattioli, Pietro
Brugnolo, Andrea
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Notes Funding agency
The study was partly supported by a grant from the Italian Ministry of Health to IRCCS Ospedale Policlinico San Martino (Fondi per la Ricerca Corrente 2019/2020).
Relevant conflicts of interest/financial disclosures
Matteo Pardini received fees from Novartis, Merck, and Biogen. Dario Arnaldi received fees from Fidia. Silvia Morbelli received speaker honoraria from GE Healthcare. Flavio Nobili received fees from Roche Bial and GE Healthcare. All other authors report no conflicts of interest.
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Snippet Background Degeneration of the nigrostriatal dopaminergic (DA) and the raphe‐thalamic serotonergic (SE) systems is among the earliest changes observed in...
Abstract Background Degeneration of the nigrostriatal dopaminergic (DA) and the raphe‐thalamic serotonergic (SE) systems is among the earliest changes observed...
BackgroundDegeneration of the nigrostriatal dopaminergic (DA) and the raphe‐thalamic serotonergic (SE) systems is among the earliest changes observed in...
BACKGROUNDDegeneration of the nigrostriatal dopaminergic (DA) and the raphe-thalamic serotonergic (SE) systems is among the earliest changes observed in...
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SubjectTerms Computed tomography
cortical degeneration
Dopamine receptors
Drug metabolism
Glucose metabolism
Innervation
Metabolism
Movement disorders
Neostriatum
Neurodegeneration
Neurodegenerative diseases
Neuroimaging
nigrostriatal degeneration
Parkinson's disease
Positron emission tomography
Putamen
Single photon emission computed tomography
striatum
Substantia grisea
Thalamus
Tomography
Title Dopaminergic and Serotonergic Degeneration and Cortical [18F]Fluorodeoxyglucose Positron Emission Tomography in De Novo Parkinson's Disease
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