Evaluation of the Glymphatic System in Schizophrenia Spectrum Disorder Using Proton Magnetic Resonance Spectroscopy Measurement of Brain Macromolecule and Diffusion Tensor Image Analysis Along the Perivascular Space Index
Abstract Background and Hypothesis The glymphatic system (GS), a brain waste clearance pathway, is disrupted in various neurodegenerative and vascular diseases. As schizophrenia shares clinical characteristics with these conditions, we hypothesized GS disruptions in patients with schizophrenia spect...
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| Veröffentlicht in: | Schizophrenia bulletin 2024-11, Vol.50 (6), p.1396-1410 |
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| creator | Abdolizadeh, Ali Torres-Carmona, Edgardo Kambari, Yasaman Amaev, Aron Song, Jianmeng Ueno, Fumihiko Koizumi, Teruki Nakajima, Shinichiro Agarwal, Sri Mahavir De Luca, Vincenzo Gerretsen, Philip Graff-Guerrero, Ariel |
| description | Abstract
Background and Hypothesis
The glymphatic system (GS), a brain waste clearance pathway, is disrupted in various neurodegenerative and vascular diseases. As schizophrenia shares clinical characteristics with these conditions, we hypothesized GS disruptions in patients with schizophrenia spectrum disorder (SCZ-SD), reflected in increased brain macromolecule (MM) and decreased diffusion-tensor-image-analysis along the perivascular space (DTI-ALPS) index.
Study Design
Forty-seven healthy controls (HCs) and 103 patients with SCZ-SD were studied. Data included 135 proton magnetic resonance spectroscopy (1H-MRS) sets, 96 DTI sets, with 79 participants contributing both. MM levels were quantified in the dorsal-anterior cingulate cortex (dACC), dorsolateral prefrontal cortex, and dorsal caudate (point resolved spectroscopy, echo-time = 35ms). Diffusivities in the projection and association fibers near the lateral ventricle were measured to calculate DTI-ALPS indices. General linear models were performed, adjusting for age, sex, and smoking. Correlation analyses examined relationships with age, illness duration, and symptoms severity.
Study Results
MM levels were not different between patients and HCs. However, left, right, and bilateral DTI-ALPS indices were lower in patients compared with HCs (P |
| doi_str_mv | 10.1093/schbul/sbae060 |
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Background and Hypothesis
The glymphatic system (GS), a brain waste clearance pathway, is disrupted in various neurodegenerative and vascular diseases. As schizophrenia shares clinical characteristics with these conditions, we hypothesized GS disruptions in patients with schizophrenia spectrum disorder (SCZ-SD), reflected in increased brain macromolecule (MM) and decreased diffusion-tensor-image-analysis along the perivascular space (DTI-ALPS) index.
Study Design
Forty-seven healthy controls (HCs) and 103 patients with SCZ-SD were studied. Data included 135 proton magnetic resonance spectroscopy (1H-MRS) sets, 96 DTI sets, with 79 participants contributing both. MM levels were quantified in the dorsal-anterior cingulate cortex (dACC), dorsolateral prefrontal cortex, and dorsal caudate (point resolved spectroscopy, echo-time = 35ms). Diffusivities in the projection and association fibers near the lateral ventricle were measured to calculate DTI-ALPS indices. General linear models were performed, adjusting for age, sex, and smoking. Correlation analyses examined relationships with age, illness duration, and symptoms severity.
Study Results
MM levels were not different between patients and HCs. However, left, right, and bilateral DTI-ALPS indices were lower in patients compared with HCs (P < .001). In HCs, age was positively correlated with dACC MM and negatively correlated with left, right, and bilateral DTI-ALPS indices (P < .001). In patients, illness duration was positively correlated with dACC MM and negatively correlated with the right DTI-ALPS index (P < .05). In the entire population, dACC MM and DTI-ALPS indices showed an inverse correlation (P < .01).
Conclusions
Our results suggest potential disruptions in the GS of patients with SCZ-SD. Improving brain’s waste clearance may offer a potential therapeutic approach for patients with SCZ-SD.</description><identifier>ISSN: 0586-7614</identifier><identifier>ISSN: 1745-1701</identifier><identifier>EISSN: 1745-1701</identifier><identifier>DOI: 10.1093/schbul/sbae060</identifier><identifier>PMID: 38748498</identifier><language>eng</language><publisher>US: Oxford University Press</publisher><subject>Adult ; Caudate Nucleus - diagnostic imaging ; Caudate Nucleus - metabolism ; Diffusion Tensor Imaging ; Dorsolateral Prefrontal Cortex - diagnostic imaging ; Dorsolateral Prefrontal Cortex - metabolism ; Female ; Glymphatic System - diagnostic imaging ; Glymphatic System - metabolism ; Glymphatic System - physiopathology ; Gyrus Cinguli - diagnostic imaging ; Gyrus Cinguli - metabolism ; Humans ; Male ; Middle Aged ; Proton Magnetic Resonance Spectroscopy ; Psychotic Disorders - diagnostic imaging ; Psychotic Disorders - metabolism ; Psychotic Disorders - physiopathology ; Schizophrenia - diagnostic imaging ; Schizophrenia - metabolism ; Schizophrenia - physiopathology ; Young Adult</subject><ispartof>Schizophrenia bulletin, 2024-11, Vol.50 (6), p.1396-1410</ispartof><rights>The Author(s) 2024. Published by Oxford University Press on behalf of the Maryland Psychiatric Research Center. All rights reserved. For commercial re-use, please contact reprints@oup.com for reprints and translation rights for reprints. All other permissions can be obtained through our RightsLink service via the Permissions link on the article page on our site—for further information please contact journals.permissions@oup.com. 2024</rights><rights>The Author(s) 2024. Published by Oxford University Press on behalf of the Maryland Psychiatric Research Center. All rights reserved. For commercial re-use, please contact reprints@oup.com for reprints and translation rights for reprints. All other permissions can be obtained through our RightsLink service via the Permissions link on the article page on our site—for further information please contact journals.permissions@oup.com.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c214t-25dfc4aa0b97234a16a177ffe56f13feaee500955c2961f1203712e406a06d3f3</cites><orcidid>0000-0003-3463-5672 ; 0000-0002-0984-4141</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,1584,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38748498$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Abdolizadeh, Ali</creatorcontrib><creatorcontrib>Torres-Carmona, Edgardo</creatorcontrib><creatorcontrib>Kambari, Yasaman</creatorcontrib><creatorcontrib>Amaev, Aron</creatorcontrib><creatorcontrib>Song, Jianmeng</creatorcontrib><creatorcontrib>Ueno, Fumihiko</creatorcontrib><creatorcontrib>Koizumi, Teruki</creatorcontrib><creatorcontrib>Nakajima, Shinichiro</creatorcontrib><creatorcontrib>Agarwal, Sri Mahavir</creatorcontrib><creatorcontrib>De Luca, Vincenzo</creatorcontrib><creatorcontrib>Gerretsen, Philip</creatorcontrib><creatorcontrib>Graff-Guerrero, Ariel</creatorcontrib><title>Evaluation of the Glymphatic System in Schizophrenia Spectrum Disorder Using Proton Magnetic Resonance Spectroscopy Measurement of Brain Macromolecule and Diffusion Tensor Image Analysis Along the Perivascular Space Index</title><title>Schizophrenia bulletin</title><addtitle>Schizophr Bull</addtitle><description>Abstract
Background and Hypothesis
The glymphatic system (GS), a brain waste clearance pathway, is disrupted in various neurodegenerative and vascular diseases. As schizophrenia shares clinical characteristics with these conditions, we hypothesized GS disruptions in patients with schizophrenia spectrum disorder (SCZ-SD), reflected in increased brain macromolecule (MM) and decreased diffusion-tensor-image-analysis along the perivascular space (DTI-ALPS) index.
Study Design
Forty-seven healthy controls (HCs) and 103 patients with SCZ-SD were studied. Data included 135 proton magnetic resonance spectroscopy (1H-MRS) sets, 96 DTI sets, with 79 participants contributing both. MM levels were quantified in the dorsal-anterior cingulate cortex (dACC), dorsolateral prefrontal cortex, and dorsal caudate (point resolved spectroscopy, echo-time = 35ms). Diffusivities in the projection and association fibers near the lateral ventricle were measured to calculate DTI-ALPS indices. General linear models were performed, adjusting for age, sex, and smoking. Correlation analyses examined relationships with age, illness duration, and symptoms severity.
Study Results
MM levels were not different between patients and HCs. However, left, right, and bilateral DTI-ALPS indices were lower in patients compared with HCs (P < .001). In HCs, age was positively correlated with dACC MM and negatively correlated with left, right, and bilateral DTI-ALPS indices (P < .001). In patients, illness duration was positively correlated with dACC MM and negatively correlated with the right DTI-ALPS index (P < .05). In the entire population, dACC MM and DTI-ALPS indices showed an inverse correlation (P < .01).
Conclusions
Our results suggest potential disruptions in the GS of patients with SCZ-SD. Improving brain’s waste clearance may offer a potential therapeutic approach for patients with SCZ-SD.</description><subject>Adult</subject><subject>Caudate Nucleus - diagnostic imaging</subject><subject>Caudate Nucleus - metabolism</subject><subject>Diffusion Tensor Imaging</subject><subject>Dorsolateral Prefrontal Cortex - diagnostic imaging</subject><subject>Dorsolateral Prefrontal Cortex - metabolism</subject><subject>Female</subject><subject>Glymphatic System - diagnostic imaging</subject><subject>Glymphatic System - metabolism</subject><subject>Glymphatic System - physiopathology</subject><subject>Gyrus Cinguli - diagnostic imaging</subject><subject>Gyrus Cinguli - metabolism</subject><subject>Humans</subject><subject>Male</subject><subject>Middle Aged</subject><subject>Proton Magnetic Resonance Spectroscopy</subject><subject>Psychotic Disorders - diagnostic imaging</subject><subject>Psychotic Disorders - metabolism</subject><subject>Psychotic Disorders - physiopathology</subject><subject>Schizophrenia - diagnostic imaging</subject><subject>Schizophrenia - metabolism</subject><subject>Schizophrenia - physiopathology</subject><subject>Young Adult</subject><issn>0586-7614</issn><issn>1745-1701</issn><issn>1745-1701</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkUFv1DAQhS0EokvhyhH5CIe0duI4yXEppazUioptz9GsM941cuxgJxXhv_JfcLQLV04jjb733oweIW85u-CsKS6jOuwmexl3gEyyZ2TFK1FmvGL8OVmxspZZJbk4I69i_M4YF43MX5Kzoq5ELZp6RX5fP4GdYDTeUa_peEB6Y-d-OKSVots5jthT4-hWHcwvPxwCOgN0O6Aaw9TTTyb60GGgj9G4Pb0PfkxGd7B3uOi_YfQOnMKTwkflh5neIcQpYI9uXEI_BjCLSAXfe4tqskjBdclc6ykulz2gSzl008Me6dqBnaOJdG19ylxOvsdgniAmJYQUBSlw4zr8-Zq80GAjvjnNc_L4-frh6kt2-_Vmc7W-zVTOxZjlZaeVAGC7psoLAVwCryqtsZSaFxoBsWSsKUuVN5JrnrOi4jkKJoHJrtDFOXl_9B2C_zFhHNveRIXWgkM_xbZgZVk3omYyoRdHNH0bY0DdDsH0EOaWs3aptD1W2p4qTYJ3J-9p12P3D__bYQI-HAE_Df8z-wPb1LM6</recordid><startdate>20241108</startdate><enddate>20241108</enddate><creator>Abdolizadeh, Ali</creator><creator>Torres-Carmona, Edgardo</creator><creator>Kambari, Yasaman</creator><creator>Amaev, Aron</creator><creator>Song, Jianmeng</creator><creator>Ueno, Fumihiko</creator><creator>Koizumi, Teruki</creator><creator>Nakajima, Shinichiro</creator><creator>Agarwal, Sri Mahavir</creator><creator>De Luca, Vincenzo</creator><creator>Gerretsen, Philip</creator><creator>Graff-Guerrero, Ariel</creator><general>Oxford University Press</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>7X8</scope><orcidid>https://orcid.org/0000-0003-3463-5672</orcidid><orcidid>https://orcid.org/0000-0002-0984-4141</orcidid></search><sort><creationdate>20241108</creationdate><title>Evaluation of the Glymphatic System in Schizophrenia Spectrum Disorder Using Proton Magnetic Resonance Spectroscopy Measurement of Brain Macromolecule and Diffusion Tensor Image Analysis Along the Perivascular Space Index</title><author>Abdolizadeh, Ali ; Torres-Carmona, Edgardo ; Kambari, Yasaman ; Amaev, Aron ; Song, Jianmeng ; Ueno, Fumihiko ; Koizumi, Teruki ; Nakajima, Shinichiro ; Agarwal, Sri Mahavir ; De Luca, Vincenzo ; Gerretsen, Philip ; Graff-Guerrero, Ariel</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c214t-25dfc4aa0b97234a16a177ffe56f13feaee500955c2961f1203712e406a06d3f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Adult</topic><topic>Caudate Nucleus - diagnostic imaging</topic><topic>Caudate Nucleus - metabolism</topic><topic>Diffusion Tensor Imaging</topic><topic>Dorsolateral Prefrontal Cortex - diagnostic imaging</topic><topic>Dorsolateral Prefrontal Cortex - metabolism</topic><topic>Female</topic><topic>Glymphatic System - diagnostic imaging</topic><topic>Glymphatic System - metabolism</topic><topic>Glymphatic System - physiopathology</topic><topic>Gyrus Cinguli - diagnostic imaging</topic><topic>Gyrus Cinguli - metabolism</topic><topic>Humans</topic><topic>Male</topic><topic>Middle Aged</topic><topic>Proton Magnetic Resonance Spectroscopy</topic><topic>Psychotic Disorders - diagnostic imaging</topic><topic>Psychotic Disorders - metabolism</topic><topic>Psychotic Disorders - physiopathology</topic><topic>Schizophrenia - diagnostic imaging</topic><topic>Schizophrenia - metabolism</topic><topic>Schizophrenia - physiopathology</topic><topic>Young Adult</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Abdolizadeh, Ali</creatorcontrib><creatorcontrib>Torres-Carmona, Edgardo</creatorcontrib><creatorcontrib>Kambari, Yasaman</creatorcontrib><creatorcontrib>Amaev, Aron</creatorcontrib><creatorcontrib>Song, Jianmeng</creatorcontrib><creatorcontrib>Ueno, Fumihiko</creatorcontrib><creatorcontrib>Koizumi, Teruki</creatorcontrib><creatorcontrib>Nakajima, Shinichiro</creatorcontrib><creatorcontrib>Agarwal, Sri Mahavir</creatorcontrib><creatorcontrib>De Luca, Vincenzo</creatorcontrib><creatorcontrib>Gerretsen, Philip</creatorcontrib><creatorcontrib>Graff-Guerrero, Ariel</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Schizophrenia bulletin</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Abdolizadeh, Ali</au><au>Torres-Carmona, Edgardo</au><au>Kambari, Yasaman</au><au>Amaev, Aron</au><au>Song, Jianmeng</au><au>Ueno, Fumihiko</au><au>Koizumi, Teruki</au><au>Nakajima, Shinichiro</au><au>Agarwal, Sri Mahavir</au><au>De Luca, Vincenzo</au><au>Gerretsen, Philip</au><au>Graff-Guerrero, Ariel</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Evaluation of the Glymphatic System in Schizophrenia Spectrum Disorder Using Proton Magnetic Resonance Spectroscopy Measurement of Brain Macromolecule and Diffusion Tensor Image Analysis Along the Perivascular Space Index</atitle><jtitle>Schizophrenia bulletin</jtitle><addtitle>Schizophr Bull</addtitle><date>2024-11-08</date><risdate>2024</risdate><volume>50</volume><issue>6</issue><spage>1396</spage><epage>1410</epage><pages>1396-1410</pages><issn>0586-7614</issn><issn>1745-1701</issn><eissn>1745-1701</eissn><abstract>Abstract
Background and Hypothesis
The glymphatic system (GS), a brain waste clearance pathway, is disrupted in various neurodegenerative and vascular diseases. As schizophrenia shares clinical characteristics with these conditions, we hypothesized GS disruptions in patients with schizophrenia spectrum disorder (SCZ-SD), reflected in increased brain macromolecule (MM) and decreased diffusion-tensor-image-analysis along the perivascular space (DTI-ALPS) index.
Study Design
Forty-seven healthy controls (HCs) and 103 patients with SCZ-SD were studied. Data included 135 proton magnetic resonance spectroscopy (1H-MRS) sets, 96 DTI sets, with 79 participants contributing both. MM levels were quantified in the dorsal-anterior cingulate cortex (dACC), dorsolateral prefrontal cortex, and dorsal caudate (point resolved spectroscopy, echo-time = 35ms). Diffusivities in the projection and association fibers near the lateral ventricle were measured to calculate DTI-ALPS indices. General linear models were performed, adjusting for age, sex, and smoking. Correlation analyses examined relationships with age, illness duration, and symptoms severity.
Study Results
MM levels were not different between patients and HCs. However, left, right, and bilateral DTI-ALPS indices were lower in patients compared with HCs (P < .001). In HCs, age was positively correlated with dACC MM and negatively correlated with left, right, and bilateral DTI-ALPS indices (P < .001). In patients, illness duration was positively correlated with dACC MM and negatively correlated with the right DTI-ALPS index (P < .05). In the entire population, dACC MM and DTI-ALPS indices showed an inverse correlation (P < .01).
Conclusions
Our results suggest potential disruptions in the GS of patients with SCZ-SD. Improving brain’s waste clearance may offer a potential therapeutic approach for patients with SCZ-SD.</abstract><cop>US</cop><pub>Oxford University Press</pub><pmid>38748498</pmid><doi>10.1093/schbul/sbae060</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0003-3463-5672</orcidid><orcidid>https://orcid.org/0000-0002-0984-4141</orcidid></addata></record> |
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| subjects | Adult Caudate Nucleus - diagnostic imaging Caudate Nucleus - metabolism Diffusion Tensor Imaging Dorsolateral Prefrontal Cortex - diagnostic imaging Dorsolateral Prefrontal Cortex - metabolism Female Glymphatic System - diagnostic imaging Glymphatic System - metabolism Glymphatic System - physiopathology Gyrus Cinguli - diagnostic imaging Gyrus Cinguli - metabolism Humans Male Middle Aged Proton Magnetic Resonance Spectroscopy Psychotic Disorders - diagnostic imaging Psychotic Disorders - metabolism Psychotic Disorders - physiopathology Schizophrenia - diagnostic imaging Schizophrenia - metabolism Schizophrenia - physiopathology Young Adult |
| title | Evaluation of the Glymphatic System in Schizophrenia Spectrum Disorder Using Proton Magnetic Resonance Spectroscopy Measurement of Brain Macromolecule and Diffusion Tensor Image Analysis Along the Perivascular Space Index |
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