Reduced Verbal Fluency following Subthalamic Deep Brain Stimulation: A Frontal-Related Cognitive Deficit?
Identifieur interne : 000086 ( Pmc/Curation ); précédent : 000085; suivant : 000087Reduced Verbal Fluency following Subthalamic Deep Brain Stimulation: A Frontal-Related Cognitive Deficit?
Auteurs : Jean-François Houvenaghel [France] ; Florence Le Jeune [France] ; Thibaut Dondaine [France] ; Aurore Esquevin [France] ; Gabriel Hadrien Robert [France] ; Julie Péron [France, Suisse] ; Claire Haegelen [France] ; Sophie Drapier [France] ; Pierre Jannin [France] ; Clément Lozachmeur [France] ; Soizic Argaud [France, Suisse] ; Joan Duprez [France] ; Dominique Drapier [France] ; Marc Vérin [France] ; Paul Sauleau [France]Source :
- PLoS ONE [ 1932-6203 ] ; 2015.
Abstract
The decrease in verbal fluency in patients with Parkinson’s disease (PD) undergoing subthalamic nucleus deep brain stimulation (STN-DBS) is usually assumed to reflect a frontal lobe-related cognitive dysfunction, although evidence for this is lacking.
To explore its underlying mechanisms, we combined neuropsychological, psychiatric and motor assessments with an examination of brain metabolism using F-18 fluorodeoxyglucose positron emission tomography, in 26 patients with PD, 3 months before and after surgery. We divided these patients into two groups, depending on whether or not they exhibited a postoperative deterioration in either phonemic (10 patients) or semantic (8 patients) fluency. We then compared the STN-DBS groups with and without verbal deterioration on changes in clinical measures and brain metabolism.
We did not find any neuropsychological change supporting the presence of an executive dysfunction in patients with a deficit in either phonemic or semantic fluency. Similarly, a comparison of patients with or without impaired fluency on brain metabolism failed to highlight any frontal areas involved in cognitive functions. However, greater changes in cognitive slowdown and apathy were observed in patients with a postoperative decrease in verbal fluency.
These results suggest that frontal lobe-related cognitive dysfunction could play only a minor role in the postoperative impairment of phonemic or semantic fluency, and that cognitive slowdown and apathy could have a more decisive influence. Furthermore, the phonemic and semantic impairments appeared to result from the disturbance of distinct mechanisms.
Url:
DOI: 10.1371/journal.pone.0140083
PubMed: 26448131
PubMed Central: 4598145
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Reduced Verbal Fluency following Subthalamic Deep Brain Stimulation: A Frontal-Related Cognitive Deficit?</title>
<author><name sortKey="Houvenaghel, Jean Francois" sort="Houvenaghel, Jean Francois" uniqKey="Houvenaghel J" first="Jean-François" last="Houvenaghel">Jean-François Houvenaghel</name>
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<affiliation wicri:level="1"><nlm:aff id="aff002"><addr-line>Department of Neurology, Rennes University Hospital, Rennes, France</addr-line>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Department of Neurology, Rennes University Hospital, Rennes</wicri:regionArea>
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<author><name sortKey="Le Jeune, Florence" sort="Le Jeune, Florence" uniqKey="Le Jeune F" first="Florence" last="Le Jeune">Florence Le Jeune</name>
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<country xml:lang="fr">France</country>
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</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Department of Nuclear Medicine, Eugène Marquis Hospital, Rennes</wicri:regionArea>
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<author><name sortKey="Dondaine, Thibaut" sort="Dondaine, Thibaut" uniqKey="Dondaine T" first="Thibaut" last="Dondaine">Thibaut Dondaine</name>
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<author><name sortKey="Robert, Gabriel Hadrien" sort="Robert, Gabriel Hadrien" uniqKey="Robert G" first="Gabriel Hadrien" last="Robert">Gabriel Hadrien Robert</name>
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<author><name sortKey="Peron, Julie" sort="Peron, Julie" uniqKey="Peron J" first="Julie" last="Péron">Julie Péron</name>
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</nlm:aff>
<country xml:lang="fr">Suisse</country>
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<author><name sortKey="Haegelen, Claire" sort="Haegelen, Claire" uniqKey="Haegelen C" first="Claire" last="Haegelen">Claire Haegelen</name>
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<author><name sortKey="Drapier, Sophie" sort="Drapier, Sophie" uniqKey="Drapier S" first="Sophie" last="Drapier">Sophie Drapier</name>
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</nlm:aff>
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</nlm:aff>
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<author><name sortKey="Jannin, Pierre" sort="Jannin, Pierre" uniqKey="Jannin P" first="Pierre" last="Jannin">Pierre Jannin</name>
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</nlm:aff>
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<author><name sortKey="Lozachmeur, Clement" sort="Lozachmeur, Clement" uniqKey="Lozachmeur C" first="Clément" last="Lozachmeur">Clément Lozachmeur</name>
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</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>“Behaviour and Basal Ganglia” research unit (EA 4712), University of Rennes, Rennes</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff005"><addr-line>Department of Psychiatry, Rennes University Hospital, Rennes, France</addr-line>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Department of Psychiatry, Rennes University Hospital, Rennes</wicri:regionArea>
</affiliation>
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<author><name sortKey="Argaud, Soizic" sort="Argaud, Soizic" uniqKey="Argaud S" first="Soizic" last="Argaud">Soizic Argaud</name>
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</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>“Behaviour and Basal Ganglia” research unit (EA 4712), University of Rennes, Rennes</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff006"><addr-line>‘Neuroscience of Emotion and Affective Dynamics’ laboratory, Department of Psychology, and Swiss Center for Affective Sciences, University of Geneva, Geneva, Switzerland</addr-line>
</nlm:aff>
<country xml:lang="fr">Suisse</country>
<wicri:regionArea>‘Neuroscience of Emotion and Affective Dynamics’ laboratory, Department of Psychology, and Swiss Center for Affective Sciences, University of Geneva, Geneva</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Duprez, Joan" sort="Duprez, Joan" uniqKey="Duprez J" first="Joan" last="Duprez">Joan Duprez</name>
<affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>“Behaviour and Basal Ganglia” research unit (EA 4712), University of Rennes, Rennes, France</addr-line>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>“Behaviour and Basal Ganglia” research unit (EA 4712), University of Rennes, Rennes</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Drapier, Dominique" sort="Drapier, Dominique" uniqKey="Drapier D" first="Dominique" last="Drapier">Dominique Drapier</name>
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</nlm:aff>
<country xml:lang="fr">France</country>
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</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff005"><addr-line>Department of Psychiatry, Rennes University Hospital, Rennes, France</addr-line>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Department of Psychiatry, Rennes University Hospital, Rennes</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Verin, Marc" sort="Verin, Marc" uniqKey="Verin M" first="Marc" last="Vérin">Marc Vérin</name>
<affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>“Behaviour and Basal Ganglia” research unit (EA 4712), University of Rennes, Rennes, France</addr-line>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>“Behaviour and Basal Ganglia” research unit (EA 4712), University of Rennes, Rennes</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff002"><addr-line>Department of Neurology, Rennes University Hospital, Rennes, France</addr-line>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Department of Neurology, Rennes University Hospital, Rennes</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Sauleau, Paul" sort="Sauleau, Paul" uniqKey="Sauleau P" first="Paul" last="Sauleau">Paul Sauleau</name>
<affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>“Behaviour and Basal Ganglia” research unit (EA 4712), University of Rennes, Rennes, France</addr-line>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>“Behaviour and Basal Ganglia” research unit (EA 4712), University of Rennes, Rennes</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff009"><addr-line>Department of Neurophysiology, Rennes University Hospital, Rennes, France</addr-line>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Department of Neurophysiology, Rennes University Hospital, Rennes</wicri:regionArea>
</affiliation>
</author>
</analytic>
<series><title level="j">PLoS ONE</title>
<idno type="eISSN">1932-6203</idno>
<imprint><date when="2015">2015</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc><textClass></textClass>
</profileDesc>
</teiHeader>
<front><div type="abstract" xml:lang="en"><sec id="sec001"><title>Objective</title>
<p>The decrease in verbal fluency in patients with Parkinson’s disease (PD) undergoing subthalamic nucleus deep brain stimulation (STN-DBS) is usually assumed to reflect a frontal lobe-related cognitive dysfunction, although evidence for this is lacking.</p>
</sec>
<sec id="sec002"><title>Methods</title>
<p>To explore its underlying mechanisms, we combined neuropsychological, psychiatric and motor assessments with an examination of brain metabolism using F-18 fluorodeoxyglucose positron emission tomography, in 26 patients with PD, 3 months before and after surgery. We divided these patients into two groups, depending on whether or not they exhibited a postoperative deterioration in either phonemic (10 patients) or semantic (8 patients) fluency. We then compared the STN-DBS groups with and without verbal deterioration on changes in clinical measures and brain metabolism.</p>
</sec>
<sec id="sec003"><title>Results</title>
<p>We did not find any neuropsychological change supporting the presence of an executive dysfunction in patients with a deficit in either phonemic or semantic fluency. Similarly, a comparison of patients with or without impaired fluency on brain metabolism failed to highlight any frontal areas involved in cognitive functions. However, greater changes in cognitive slowdown and apathy were observed in patients with a postoperative decrease in verbal fluency.</p>
</sec>
<sec id="sec004"><title>Conclusions</title>
<p>These results suggest that frontal lobe-related cognitive dysfunction could play only a minor role in the postoperative impairment of phonemic or semantic fluency, and that cognitive slowdown and apathy could have a more decisive influence. Furthermore, the phonemic and semantic impairments appeared to result from the disturbance of distinct mechanisms.</p>
</sec>
</div>
</front>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id>
<journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id>
<journal-id journal-id-type="publisher-id">plos</journal-id>
<journal-id journal-id-type="pmc">plosone</journal-id>
<journal-title-group><journal-title>PLoS ONE</journal-title>
</journal-title-group>
<issn pub-type="epub">1932-6203</issn>
<publisher><publisher-name>Public Library of Science</publisher-name>
<publisher-loc>San Francisco, CA USA</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">26448131</article-id>
<article-id pub-id-type="pmc">4598145</article-id>
<article-id pub-id-type="doi">10.1371/journal.pone.0140083</article-id>
<article-id pub-id-type="publisher-id">PONE-D-15-33790</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>Reduced Verbal Fluency following Subthalamic Deep Brain Stimulation: A Frontal-Related Cognitive Deficit?</article-title>
<alt-title alt-title-type="running-head">Verbal Fluency Deficit following STN-DBS in PD</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Houvenaghel</surname>
<given-names>Jean-François</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff002"><sup>2</sup>
</xref>
<xref rid="cor001" ref-type="corresp">*</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Le Jeune</surname>
<given-names>Florence</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff003"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Dondaine</surname>
<given-names>Thibaut</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Esquevin</surname>
<given-names>Aurore</given-names>
</name>
<xref ref-type="aff" rid="aff004"><sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Robert</surname>
<given-names>Gabriel Hadrien</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff005"><sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Péron</surname>
<given-names>Julie</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff006"><sup>6</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Haegelen</surname>
<given-names>Claire</given-names>
</name>
<xref ref-type="aff" rid="aff007"><sup>7</sup>
</xref>
<xref ref-type="aff" rid="aff008"><sup>8</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Drapier</surname>
<given-names>Sophie</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff002"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Jannin</surname>
<given-names>Pierre</given-names>
</name>
<xref ref-type="aff" rid="aff008"><sup>8</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lozachmeur</surname>
<given-names>Clément</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff005"><sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Argaud</surname>
<given-names>Soizic</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff006"><sup>6</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Duprez</surname>
<given-names>Joan</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Drapier</surname>
<given-names>Dominique</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff005"><sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Vérin</surname>
<given-names>Marc</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff002"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Sauleau</surname>
<given-names>Paul</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff009"><sup>9</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff001"><label>1</label>
<addr-line>“Behaviour and Basal Ganglia” research unit (EA 4712), University of Rennes, Rennes, France</addr-line>
</aff>
<aff id="aff002"><label>2</label>
<addr-line>Department of Neurology, Rennes University Hospital, Rennes, France</addr-line>
</aff>
<aff id="aff003"><label>3</label>
<addr-line>Department of Nuclear Medicine, Eugène Marquis Hospital, Rennes, France</addr-line>
</aff>
<aff id="aff004"><label>4</label>
<addr-line>Department of Neuroradiology, Rennes University Hospital, Rennes, France</addr-line>
</aff>
<aff id="aff005"><label>5</label>
<addr-line>Department of Psychiatry, Rennes University Hospital, Rennes, France</addr-line>
</aff>
<aff id="aff006"><label>6</label>
<addr-line>‘Neuroscience of Emotion and Affective Dynamics’ laboratory, Department of Psychology, and Swiss Center for Affective Sciences, University of Geneva, Geneva, Switzerland</addr-line>
</aff>
<aff id="aff007"><label>7</label>
<addr-line>Department of Neurosurgery, Rennes University Hospital, Rennes, France</addr-line>
</aff>
<aff id="aff008"><label>8</label>
<addr-line>“MediCIS” laboratory (UMR 1099 LTSI), Inserm/University of Rennes, Rennes, France</addr-line>
</aff>
<aff id="aff009"><label>9</label>
<addr-line>Department of Neurophysiology, Rennes University Hospital, Rennes, France</addr-line>
</aff>
<contrib-group><contrib contrib-type="editor"><name><surname>Toft</surname>
<given-names>Mathias</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1"><addr-line>Oslo University Hospital, NORWAY</addr-line>
</aff>
<author-notes><fn fn-type="conflict" id="coi001"><p><bold>Competing Interests: </bold>
Dr Sophie Drapier received speech honorarium from Teva and Medtronic and served on scientific advisory boards for Aguettant and Britannia.</p>
</fn>
<fn fn-type="con" id="contrib001"><p>Conceived and designed the experiments: JFH MV PS. Performed the experiments: JFH TD JP CH GR SD PJ CL DD MV. Analyzed the data: JFH FLJ AE. Contributed reagents/materials/analysis tools: JFH FLJ AE. Wrote the paper: JFH FLJ TD AE GR JP CH SD PJ CL SA JD DD MV PS.</p>
</fn>
<corresp id="cor001">* E-mail: <email>Jeanfrancois.Houvenaghel@chu-rennes.fr</email>
</corresp>
</author-notes>
<pub-date pub-type="epub"><day>8</day>
<month>10</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="collection"><year>2015</year>
</pub-date>
<volume>10</volume>
<issue>10</issue>
<elocation-id>e0140083</elocation-id>
<history><date date-type="received"><day>1</day>
<month>8</month>
<year>2015</year>
</date>
<date date-type="accepted"><day>21</day>
<month>9</month>
<year>2015</year>
</date>
</history>
<permissions><copyright-year>2015</copyright-year>
<copyright-holder>Houvenaghel et al</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>
, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited</license-p>
</license>
</permissions>
<self-uri content-type="pdf" xlink:type="simple" xlink:href="pone.0140083.pdf"></self-uri>
<abstract><sec id="sec001"><title>Objective</title>
<p>The decrease in verbal fluency in patients with Parkinson’s disease (PD) undergoing subthalamic nucleus deep brain stimulation (STN-DBS) is usually assumed to reflect a frontal lobe-related cognitive dysfunction, although evidence for this is lacking.</p>
</sec>
<sec id="sec002"><title>Methods</title>
<p>To explore its underlying mechanisms, we combined neuropsychological, psychiatric and motor assessments with an examination of brain metabolism using F-18 fluorodeoxyglucose positron emission tomography, in 26 patients with PD, 3 months before and after surgery. We divided these patients into two groups, depending on whether or not they exhibited a postoperative deterioration in either phonemic (10 patients) or semantic (8 patients) fluency. We then compared the STN-DBS groups with and without verbal deterioration on changes in clinical measures and brain metabolism.</p>
</sec>
<sec id="sec003"><title>Results</title>
<p>We did not find any neuropsychological change supporting the presence of an executive dysfunction in patients with a deficit in either phonemic or semantic fluency. Similarly, a comparison of patients with or without impaired fluency on brain metabolism failed to highlight any frontal areas involved in cognitive functions. However, greater changes in cognitive slowdown and apathy were observed in patients with a postoperative decrease in verbal fluency.</p>
</sec>
<sec id="sec004"><title>Conclusions</title>
<p>These results suggest that frontal lobe-related cognitive dysfunction could play only a minor role in the postoperative impairment of phonemic or semantic fluency, and that cognitive slowdown and apathy could have a more decisive influence. Furthermore, the phonemic and semantic impairments appeared to result from the disturbance of distinct mechanisms.</p>
</sec>
</abstract>
<funding-group><funding-statement>The study was funded by University of Rennes 1.</funding-statement>
</funding-group>
<counts><fig-count count="1"></fig-count>
<table-count count="4"></table-count>
<page-count count="14"></page-count>
</counts>
<custom-meta-group><custom-meta id="data-availability"><meta-name>Data Availability</meta-name>
<meta-value>All relevant data are within the paper and its Supporting Information files.</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
<notes><title>Data Availability</title>
<p>All relevant data are within the paper and its Supporting Information files.</p>
</notes>
</front>
</pmc>
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