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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| creator | 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 |
| description | 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 |
| doi_str_mv | 10.1002/mds.28654 |
| format | Article |
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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</description><identifier>ISSN: 0885-3185</identifier><identifier>EISSN: 1531-8257</identifier><identifier>DOI: 10.1002/mds.28654</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley & Sons, Inc</publisher><subject>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</subject><ispartof>Movement disorders, 2021-10, Vol.36 (10), p.2293-2302</ispartof><rights>2021 International Parkinson and Movement Disorder Society</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3304-b88d8c56fc914ad21bfaa844b22b2c62dba866da07b28f8205271192eda52f7d3</citedby><cites>FETCH-LOGICAL-c3304-b88d8c56fc914ad21bfaa844b22b2c62dba866da07b28f8205271192eda52f7d3</cites><orcidid>0000-0001-9983-7940 ; 0000-0001-6823-6069</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Fmds.28654$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fmds.28654$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27903,27904,45553,45554</link.rule.ids></links><search><creatorcontrib>Orso, Beatrice</creatorcontrib><creatorcontrib>Arnaldi, Dario</creatorcontrib><creatorcontrib>Girtler, Nicola</creatorcontrib><creatorcontrib>Brugnolo, Andrea</creatorcontrib><creatorcontrib>Doglione, Elisa</creatorcontrib><creatorcontrib>Mattioli, Pietro</creatorcontrib><creatorcontrib>Biassoni, Erica</creatorcontrib><creatorcontrib>Fancellu, Roberto</creatorcontrib><creatorcontrib>Massa, Federico</creatorcontrib><creatorcontrib>Bauckneht, Matteo</creatorcontrib><creatorcontrib>Chiola, Silvia</creatorcontrib><creatorcontrib>Morbelli, Silvia</creatorcontrib><creatorcontrib>Nobili, Flavio</creatorcontrib><creatorcontrib>Pardini, Matteo</creatorcontrib><title>Dopaminergic and Serotonergic Degeneration and Cortical [18F]Fluorodeoxyglucose Positron Emission Tomography in De Novo Parkinson's Disease</title><title>Movement disorders</title><description>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</description><subject>Computed tomography</subject><subject>cortical degeneration</subject><subject>Dopamine receptors</subject><subject>Drug metabolism</subject><subject>Glucose metabolism</subject><subject>Innervation</subject><subject>Metabolism</subject><subject>Movement disorders</subject><subject>Neostriatum</subject><subject>Neurodegeneration</subject><subject>Neurodegenerative diseases</subject><subject>Neuroimaging</subject><subject>nigrostriatal degeneration</subject><subject>Parkinson's disease</subject><subject>Positron emission tomography</subject><subject>Putamen</subject><subject>Single photon emission computed tomography</subject><subject>striatum</subject><subject>Substantia grisea</subject><subject>Thalamus</subject><subject>Tomography</subject><issn>0885-3185</issn><issn>1531-8257</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNp10c1KxDAQB_AgCq4fB9-g4EE9dE2mTTc9yq6rgh8L6kmkpEm6RtvOmrTqPoMvbXQ9CZ4Skt8Mw_wJ2WN0yCiF40b7IYiMp2tkwHjCYgF8tE4GVAgeJ0zwTbLl_TOljHGWDcjnBBeysa1xc6si2ero1jjs8PdhYuYmXGVnsf35HaPrrJJ19MDE9HFa9-hQG_xYzuteoTfRDL3tXNCnjfX-u-wOG5w7uXhaRrYNHaNrfMNoJt2LbT22Bz6aWG-kNztko5K1N7u_5za5n57ejc_jy5uzi_HJZayShKZxKYQWimeVylkqNbCyklKkaQlQgspAl1JkmZZ0VIKoBFAOI8ZyMFpyqEY62SaHq74Lh6-98V0RRlWmrmVrsPcFhL0B0DzPA93_Q5-xd22YLigBWc6DDOpopZRD752pioWzjXTLgtHiO5YixFL8xBLs8cq-29os_4fF1eR2VfEFtJKQrg</recordid><startdate>202110</startdate><enddate>202110</enddate><creator>Orso, Beatrice</creator><creator>Arnaldi, Dario</creator><creator>Girtler, Nicola</creator><creator>Brugnolo, Andrea</creator><creator>Doglione, Elisa</creator><creator>Mattioli, Pietro</creator><creator>Biassoni, Erica</creator><creator>Fancellu, Roberto</creator><creator>Massa, Federico</creator><creator>Bauckneht, Matteo</creator><creator>Chiola, Silvia</creator><creator>Morbelli, Silvia</creator><creator>Nobili, Flavio</creator><creator>Pardini, Matteo</creator><general>John Wiley & Sons, Inc</general><general>Wiley Subscription Services, Inc</general><scope>AAYXX</scope><scope>CITATION</scope><scope>7TK</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>NAPCQ</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-9983-7940</orcidid><orcidid>https://orcid.org/0000-0001-6823-6069</orcidid></search><sort><creationdate>202110</creationdate><title>Dopaminergic and Serotonergic Degeneration and Cortical [18F]Fluorodeoxyglucose Positron Emission Tomography in De Novo Parkinson's Disease</title><author>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</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3304-b88d8c56fc914ad21bfaa844b22b2c62dba866da07b28f8205271192eda52f7d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Computed tomography</topic><topic>cortical degeneration</topic><topic>Dopamine receptors</topic><topic>Drug metabolism</topic><topic>Glucose metabolism</topic><topic>Innervation</topic><topic>Metabolism</topic><topic>Movement disorders</topic><topic>Neostriatum</topic><topic>Neurodegeneration</topic><topic>Neurodegenerative diseases</topic><topic>Neuroimaging</topic><topic>nigrostriatal degeneration</topic><topic>Parkinson's disease</topic><topic>Positron emission tomography</topic><topic>Putamen</topic><topic>Single photon emission computed tomography</topic><topic>striatum</topic><topic>Substantia grisea</topic><topic>Thalamus</topic><topic>Tomography</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Orso, Beatrice</creatorcontrib><creatorcontrib>Arnaldi, Dario</creatorcontrib><creatorcontrib>Girtler, Nicola</creatorcontrib><creatorcontrib>Brugnolo, Andrea</creatorcontrib><creatorcontrib>Doglione, Elisa</creatorcontrib><creatorcontrib>Mattioli, Pietro</creatorcontrib><creatorcontrib>Biassoni, Erica</creatorcontrib><creatorcontrib>Fancellu, Roberto</creatorcontrib><creatorcontrib>Massa, Federico</creatorcontrib><creatorcontrib>Bauckneht, Matteo</creatorcontrib><creatorcontrib>Chiola, Silvia</creatorcontrib><creatorcontrib>Morbelli, Silvia</creatorcontrib><creatorcontrib>Nobili, Flavio</creatorcontrib><creatorcontrib>Pardini, Matteo</creatorcontrib><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Nursing & Allied Health Premium</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Movement disorders</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Orso, Beatrice</au><au>Arnaldi, Dario</au><au>Girtler, Nicola</au><au>Brugnolo, Andrea</au><au>Doglione, Elisa</au><au>Mattioli, Pietro</au><au>Biassoni, Erica</au><au>Fancellu, Roberto</au><au>Massa, Federico</au><au>Bauckneht, Matteo</au><au>Chiola, Silvia</au><au>Morbelli, Silvia</au><au>Nobili, Flavio</au><au>Pardini, Matteo</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Dopaminergic and Serotonergic Degeneration and Cortical [18F]Fluorodeoxyglucose Positron Emission Tomography in De Novo Parkinson's Disease</atitle><jtitle>Movement disorders</jtitle><date>2021-10</date><risdate>2021</risdate><volume>36</volume><issue>10</issue><spage>2293</spage><epage>2302</epage><pages>2293-2302</pages><issn>0885-3185</issn><eissn>1531-8257</eissn><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</abstract><cop>Hoboken, USA</cop><pub>John Wiley & Sons, Inc</pub><doi>10.1002/mds.28654</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0001-9983-7940</orcidid><orcidid>https://orcid.org/0000-0001-6823-6069</orcidid></addata></record> |
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| ispartof | Movement disorders, 2021-10, Vol.36 (10), p.2293-2302 |
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| source | Wiley Online Library Journals Frontfile Complete |
| 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 |
| title | Dopaminergic and Serotonergic Degeneration and Cortical [18F]Fluorodeoxyglucose Positron Emission Tomography in De Novo Parkinson's Disease |
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