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Interactive effect of orthostatic hypotension on gray matter atrophy associated with hyposmia and RBD in de novo Parkinson’s disease
Background Orthostatic hypotension (OH) is a potential modifiable risk factor for cognitive impairment in patients with Parkinson’s disease (PD). Although other risk factors for dementia, hyposmia and REM sleep behavior disorder (RBD), are closely associated with autonomic dysfunction in PD, little...
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| Published in: | Journal of neurology 2023-12, Vol.270 (12), p.5924-5934 |
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| container_end_page | 5934 |
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| container_title | Journal of neurology |
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| creator | Shiraishi, Tomotaka Yoshimaru, Daisuke Umehara, Tadashi Ozawa, Masakazu Omoto, Shusaku Okumura, Motohiro Kokubu, Tatsushi Takahashi, Junichiro Sato, Takeo Onda, Asako Komatsu, Teppei Sakai, Kenichiro Mitsumura, Hidetaka Murakami, Hidetomo Okano, Hirotaka James Iguchi, Yasuyuki |
| description | Background
Orthostatic hypotension (OH) is a potential modifiable risk factor for cognitive impairment in patients with Parkinson’s disease (PD). Although other risk factors for dementia, hyposmia and REM sleep behavior disorder (RBD), are closely associated with autonomic dysfunction in PD, little is known about how these risk factors influence cognitive function and cerebral pathology.
Objective
We investigated how these three factors contribute to gray matter atrophy by considering the interaction of OH with hyposmia and RBD.
Methods
We analyzed cortical thickness, subcortical gray matter volume, and cognitive measures from 78 patients with de novo PD who underwent the head-up tilt test for the diagnosis of OH.
Results
Whole-brain analyses with Monte Carlo corrections revealed that hyposmia was associated with decreased cortical thickness in a marginal branch of the cingulate sulcus among patients with OH, and cortical thickness in this area correlated with cognitive functioning only in patients with OH. Subcortical gray matter volume analysis indicated that severe RBD was associated with decreased volume in the left hippocampus and bilateral amygdala among patients with OH.
Conclusion
Even in early PD, OH exerts effects on gray matter atrophy and cognitive dysfunction by interacting with RBD and hyposmia. OH might exacerbate cerebral pathology induced by hyposmia or RBD. |
| doi_str_mv | 10.1007/s00415-023-11934-5 |
| format | article |
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Orthostatic hypotension (OH) is a potential modifiable risk factor for cognitive impairment in patients with Parkinson’s disease (PD). Although other risk factors for dementia, hyposmia and REM sleep behavior disorder (RBD), are closely associated with autonomic dysfunction in PD, little is known about how these risk factors influence cognitive function and cerebral pathology.
Objective
We investigated how these three factors contribute to gray matter atrophy by considering the interaction of OH with hyposmia and RBD.
Methods
We analyzed cortical thickness, subcortical gray matter volume, and cognitive measures from 78 patients with de novo PD who underwent the head-up tilt test for the diagnosis of OH.
Results
Whole-brain analyses with Monte Carlo corrections revealed that hyposmia was associated with decreased cortical thickness in a marginal branch of the cingulate sulcus among patients with OH, and cortical thickness in this area correlated with cognitive functioning only in patients with OH. Subcortical gray matter volume analysis indicated that severe RBD was associated with decreased volume in the left hippocampus and bilateral amygdala among patients with OH.
Conclusion
Even in early PD, OH exerts effects on gray matter atrophy and cognitive dysfunction by interacting with RBD and hyposmia. OH might exacerbate cerebral pathology induced by hyposmia or RBD.</description><identifier>ISSN: 0340-5354</identifier><identifier>EISSN: 1432-1459</identifier><identifier>DOI: 10.1007/s00415-023-11934-5</identifier><identifier>PMID: 37626243</identifier><language>eng</language><publisher>Berlin/Heidelberg: Springer Berlin Heidelberg</publisher><subject>Amygdala ; Anosmia - complications ; Anosmia - pathology ; Atrophy ; Atrophy - pathology ; Cognitive ability ; Dementia disorders ; Gray Matter - pathology ; Humans ; Hypotension ; Hypotension, Orthostatic - complications ; Hypotension, Orthostatic - diagnostic imaging ; Medicine ; Medicine & Public Health ; Movement disorders ; Neurodegenerative diseases ; Neurology ; Neuroradiology ; Neurosciences ; Olfaction disorders ; Original Communication ; Orthostatic hypotension ; Parkinson Disease - complications ; Parkinson Disease - diagnostic imaging ; Parkinson Disease - pathology ; Parkinson's disease ; Pathology ; REM sleep ; REM Sleep Behavior Disorder - complications ; Risk factors ; Sleep disorders ; Substantia grisea</subject><ispartof>Journal of neurology, 2023-12, Vol.270 (12), p.5924-5934</ispartof><rights>The Author(s), under exclusive licence to Springer-Verlag GmbH Germany 2023. Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.</rights><rights>2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c326t-32b761bb91923d192bad61714d799ffa6f750aeb6084c134a6aad070d439e1f43</cites><orcidid>0000-0002-0916-5800</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,777,781,27905,27906</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37626243$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Shiraishi, Tomotaka</creatorcontrib><creatorcontrib>Yoshimaru, Daisuke</creatorcontrib><creatorcontrib>Umehara, Tadashi</creatorcontrib><creatorcontrib>Ozawa, Masakazu</creatorcontrib><creatorcontrib>Omoto, Shusaku</creatorcontrib><creatorcontrib>Okumura, Motohiro</creatorcontrib><creatorcontrib>Kokubu, Tatsushi</creatorcontrib><creatorcontrib>Takahashi, Junichiro</creatorcontrib><creatorcontrib>Sato, Takeo</creatorcontrib><creatorcontrib>Onda, Asako</creatorcontrib><creatorcontrib>Komatsu, Teppei</creatorcontrib><creatorcontrib>Sakai, Kenichiro</creatorcontrib><creatorcontrib>Mitsumura, Hidetaka</creatorcontrib><creatorcontrib>Murakami, Hidetomo</creatorcontrib><creatorcontrib>Okano, Hirotaka James</creatorcontrib><creatorcontrib>Iguchi, Yasuyuki</creatorcontrib><title>Interactive effect of orthostatic hypotension on gray matter atrophy associated with hyposmia and RBD in de novo Parkinson’s disease</title><title>Journal of neurology</title><addtitle>J Neurol</addtitle><addtitle>J Neurol</addtitle><description>Background
Orthostatic hypotension (OH) is a potential modifiable risk factor for cognitive impairment in patients with Parkinson’s disease (PD). Although other risk factors for dementia, hyposmia and REM sleep behavior disorder (RBD), are closely associated with autonomic dysfunction in PD, little is known about how these risk factors influence cognitive function and cerebral pathology.
Objective
We investigated how these three factors contribute to gray matter atrophy by considering the interaction of OH with hyposmia and RBD.
Methods
We analyzed cortical thickness, subcortical gray matter volume, and cognitive measures from 78 patients with de novo PD who underwent the head-up tilt test for the diagnosis of OH.
Results
Whole-brain analyses with Monte Carlo corrections revealed that hyposmia was associated with decreased cortical thickness in a marginal branch of the cingulate sulcus among patients with OH, and cortical thickness in this area correlated with cognitive functioning only in patients with OH. Subcortical gray matter volume analysis indicated that severe RBD was associated with decreased volume in the left hippocampus and bilateral amygdala among patients with OH.
Conclusion
Even in early PD, OH exerts effects on gray matter atrophy and cognitive dysfunction by interacting with RBD and hyposmia. OH might exacerbate cerebral pathology induced by hyposmia or RBD.</description><subject>Amygdala</subject><subject>Anosmia - complications</subject><subject>Anosmia - pathology</subject><subject>Atrophy</subject><subject>Atrophy - pathology</subject><subject>Cognitive ability</subject><subject>Dementia disorders</subject><subject>Gray Matter - pathology</subject><subject>Humans</subject><subject>Hypotension</subject><subject>Hypotension, Orthostatic - complications</subject><subject>Hypotension, Orthostatic - diagnostic imaging</subject><subject>Medicine</subject><subject>Medicine & Public Health</subject><subject>Movement disorders</subject><subject>Neurodegenerative diseases</subject><subject>Neurology</subject><subject>Neuroradiology</subject><subject>Neurosciences</subject><subject>Olfaction disorders</subject><subject>Original Communication</subject><subject>Orthostatic hypotension</subject><subject>Parkinson Disease - complications</subject><subject>Parkinson Disease - diagnostic imaging</subject><subject>Parkinson Disease - pathology</subject><subject>Parkinson's disease</subject><subject>Pathology</subject><subject>REM sleep</subject><subject>REM Sleep Behavior Disorder - complications</subject><subject>Risk factors</subject><subject>Sleep disorders</subject><subject>Substantia grisea</subject><issn>0340-5354</issn><issn>1432-1459</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><recordid>eNp9kU1uFDEQhS1ERIbABVggS2zYNPi_p5eQ8BMpUhCCtVXdtjMO0_bg8gTNjhV3yPVyEkwmgMQCySov6nuvqvQIecLZC85Y_xIZU1x3TMiO80GqTt8jC66k6LjSw32yYFKxTkutDslDxEvG2LI1HpBD2RthhJIL8uM0VV9gqvHKUx-CnyrNgeZSVxkr1DjR1W6Tq08Yc6LtXRTY0Rlqk1GoJW9WOwqIeYpQvaPfYl3dSnCOQCE5-vH1CY2JOk9Tvsr0A5QvMWFON9-vkbqIHtA_IgcB1ugf3_1H5PPbN5-O33dn5-9Oj1-ddZMUpnZSjL3h4zjwQUjXygjO8J4r1w9DCGBCrxn40bRDJy4VGADHeuaUHDwPSh6R53vfTclftx6rnSNOfr2G5PMWrVjqfqmM1rKhz_5BL_O2pLZdo5ZtpjaKN0rsqalkxOKD3ZQ4Q9lZzuyvlOw-JdtSsrcpWd1ET--st-Ps3R_J71gaIPcAtla68OXv7P_Y_gTRip9q</recordid><startdate>20231201</startdate><enddate>20231201</enddate><creator>Shiraishi, Tomotaka</creator><creator>Yoshimaru, Daisuke</creator><creator>Umehara, Tadashi</creator><creator>Ozawa, Masakazu</creator><creator>Omoto, Shusaku</creator><creator>Okumura, Motohiro</creator><creator>Kokubu, Tatsushi</creator><creator>Takahashi, Junichiro</creator><creator>Sato, Takeo</creator><creator>Onda, Asako</creator><creator>Komatsu, Teppei</creator><creator>Sakai, Kenichiro</creator><creator>Mitsumura, Hidetaka</creator><creator>Murakami, Hidetomo</creator><creator>Okano, Hirotaka James</creator><creator>Iguchi, Yasuyuki</creator><general>Springer Berlin Heidelberg</general><general>Springer Nature B.V</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7TK</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>BENPR</scope><scope>CCPQU</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>K9.</scope><scope>M0S</scope><scope>M1P</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-0916-5800</orcidid></search><sort><creationdate>20231201</creationdate><title>Interactive effect of orthostatic hypotension on gray matter atrophy associated with hyposmia and RBD in de novo Parkinson’s disease</title><author>Shiraishi, Tomotaka ; Yoshimaru, Daisuke ; Umehara, Tadashi ; Ozawa, Masakazu ; Omoto, Shusaku ; Okumura, Motohiro ; Kokubu, Tatsushi ; Takahashi, Junichiro ; Sato, Takeo ; Onda, Asako ; Komatsu, Teppei ; Sakai, Kenichiro ; Mitsumura, Hidetaka ; Murakami, Hidetomo ; Okano, Hirotaka James ; Iguchi, Yasuyuki</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c326t-32b761bb91923d192bad61714d799ffa6f750aeb6084c134a6aad070d439e1f43</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Amygdala</topic><topic>Anosmia - complications</topic><topic>Anosmia - pathology</topic><topic>Atrophy</topic><topic>Atrophy - pathology</topic><topic>Cognitive ability</topic><topic>Dementia disorders</topic><topic>Gray Matter - pathology</topic><topic>Humans</topic><topic>Hypotension</topic><topic>Hypotension, Orthostatic - complications</topic><topic>Hypotension, Orthostatic - diagnostic imaging</topic><topic>Medicine</topic><topic>Medicine & Public Health</topic><topic>Movement disorders</topic><topic>Neurodegenerative diseases</topic><topic>Neurology</topic><topic>Neuroradiology</topic><topic>Neurosciences</topic><topic>Olfaction disorders</topic><topic>Original Communication</topic><topic>Orthostatic hypotension</topic><topic>Parkinson Disease - complications</topic><topic>Parkinson Disease - diagnostic imaging</topic><topic>Parkinson Disease - pathology</topic><topic>Parkinson's disease</topic><topic>Pathology</topic><topic>REM sleep</topic><topic>REM Sleep Behavior Disorder - complications</topic><topic>Risk factors</topic><topic>Sleep disorders</topic><topic>Substantia grisea</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Shiraishi, Tomotaka</creatorcontrib><creatorcontrib>Yoshimaru, Daisuke</creatorcontrib><creatorcontrib>Umehara, Tadashi</creatorcontrib><creatorcontrib>Ozawa, Masakazu</creatorcontrib><creatorcontrib>Omoto, Shusaku</creatorcontrib><creatorcontrib>Okumura, Motohiro</creatorcontrib><creatorcontrib>Kokubu, Tatsushi</creatorcontrib><creatorcontrib>Takahashi, Junichiro</creatorcontrib><creatorcontrib>Sato, Takeo</creatorcontrib><creatorcontrib>Onda, Asako</creatorcontrib><creatorcontrib>Komatsu, Teppei</creatorcontrib><creatorcontrib>Sakai, Kenichiro</creatorcontrib><creatorcontrib>Mitsumura, Hidetaka</creatorcontrib><creatorcontrib>Murakami, Hidetomo</creatorcontrib><creatorcontrib>Okano, Hirotaka James</creatorcontrib><creatorcontrib>Iguchi, Yasuyuki</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Neurosciences Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>ProQuest Central</collection><collection>ProQuest One Community College</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>PML(ProQuest Medical Library)</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>MEDLINE - Academic</collection><jtitle>Journal of neurology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Shiraishi, Tomotaka</au><au>Yoshimaru, Daisuke</au><au>Umehara, Tadashi</au><au>Ozawa, Masakazu</au><au>Omoto, Shusaku</au><au>Okumura, Motohiro</au><au>Kokubu, Tatsushi</au><au>Takahashi, Junichiro</au><au>Sato, Takeo</au><au>Onda, Asako</au><au>Komatsu, Teppei</au><au>Sakai, Kenichiro</au><au>Mitsumura, Hidetaka</au><au>Murakami, Hidetomo</au><au>Okano, Hirotaka James</au><au>Iguchi, Yasuyuki</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Interactive effect of orthostatic hypotension on gray matter atrophy associated with hyposmia and RBD in de novo Parkinson’s disease</atitle><jtitle>Journal of neurology</jtitle><stitle>J Neurol</stitle><addtitle>J Neurol</addtitle><date>2023-12-01</date><risdate>2023</risdate><volume>270</volume><issue>12</issue><spage>5924</spage><epage>5934</epage><pages>5924-5934</pages><issn>0340-5354</issn><eissn>1432-1459</eissn><abstract>Background
Orthostatic hypotension (OH) is a potential modifiable risk factor for cognitive impairment in patients with Parkinson’s disease (PD). Although other risk factors for dementia, hyposmia and REM sleep behavior disorder (RBD), are closely associated with autonomic dysfunction in PD, little is known about how these risk factors influence cognitive function and cerebral pathology.
Objective
We investigated how these three factors contribute to gray matter atrophy by considering the interaction of OH with hyposmia and RBD.
Methods
We analyzed cortical thickness, subcortical gray matter volume, and cognitive measures from 78 patients with de novo PD who underwent the head-up tilt test for the diagnosis of OH.
Results
Whole-brain analyses with Monte Carlo corrections revealed that hyposmia was associated with decreased cortical thickness in a marginal branch of the cingulate sulcus among patients with OH, and cortical thickness in this area correlated with cognitive functioning only in patients with OH. Subcortical gray matter volume analysis indicated that severe RBD was associated with decreased volume in the left hippocampus and bilateral amygdala among patients with OH.
Conclusion
Even in early PD, OH exerts effects on gray matter atrophy and cognitive dysfunction by interacting with RBD and hyposmia. OH might exacerbate cerebral pathology induced by hyposmia or RBD.</abstract><cop>Berlin/Heidelberg</cop><pub>Springer Berlin Heidelberg</pub><pmid>37626243</pmid><doi>10.1007/s00415-023-11934-5</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0002-0916-5800</orcidid></addata></record> |
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| ispartof | Journal of neurology, 2023-12, Vol.270 (12), p.5924-5934 |
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| source | Springer Nature |
| subjects | Amygdala Anosmia - complications Anosmia - pathology Atrophy Atrophy - pathology Cognitive ability Dementia disorders Gray Matter - pathology Humans Hypotension Hypotension, Orthostatic - complications Hypotension, Orthostatic - diagnostic imaging Medicine Medicine & Public Health Movement disorders Neurodegenerative diseases Neurology Neuroradiology Neurosciences Olfaction disorders Original Communication Orthostatic hypotension Parkinson Disease - complications Parkinson Disease - diagnostic imaging Parkinson Disease - pathology Parkinson's disease Pathology REM sleep REM Sleep Behavior Disorder - complications Risk factors Sleep disorders Substantia grisea |
| title | Interactive effect of orthostatic hypotension on gray matter atrophy associated with hyposmia and RBD in de novo Parkinson’s disease |
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