Functional Connectome Hierarchy Distortions in Female Nurses With Occupational Burnout and Its Gene Expression Signatures

Background Burnout has become a serious public health issue worldwide, particularly during the COVID‐19 pandemic. Functional connectome impairments associated with occupational burnout were widely distributed, involving both low‐level sensorimotor cortices and high‐level association cortices. Purpos...

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Veröffentlicht in:Journal of magnetic resonance imaging 2024-06, Vol.59 (6), p.2124-2136
Hauptverfasser: Shang, Yingying, Su, Qian, Ma, Rong, Chen, Miao, Zhao, Ziyang, Yao, Chaofan, Han, Lin, Yao, Zhijun, Hu, Bin
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container_end_page 2136
container_issue 6
container_start_page 2124
container_title Journal of magnetic resonance imaging
container_volume 59
creator Shang, Yingying
Su, Qian
Ma, Rong
Chen, Miao
Zhao, Ziyang
Yao, Chaofan
Han, Lin
Yao, Zhijun
Hu, Bin
description Background Burnout has become a serious public health issue worldwide, particularly during the COVID‐19 pandemic. Functional connectome impairments associated with occupational burnout were widely distributed, involving both low‐level sensorimotor cortices and high‐level association cortices. Purpose To investigate whether there are hierarchical perturbations in the functional connectomes and if these perturbations are potentially influenced by genetic factors in nurses who feel “burned out.” Study Type Prospective, case control. Population Thirty‐three female nurses with occupational burnout (aged 27–40, 32.42 ± 3.37) and 32 matched nurses who were not feeling burned out (aged 27–42, 32.50 ± 4.21). Field Strength/Sequence 3.0 T, gradient‐echo echo‐planar imaging sequence (GE‐EPI). Assessment Gradient‐based techniques were used to depict the perturbations in the multi‐dimensional hierarchical structure of the macroscale connectome. Gene expression data were acquired from the Allen Human Brain Atlas. Statistical Tests Cortex‐wide multivariate analyses were used for between‐group differences in gradients as well as association analyses between the hierarchy distortions and the MBI score (FDR corrected). Partial least squares, spin test and bootstrapping were utilized together to select the gene sets (FDR corrected). Gene enrichment analyses (GO, KEGG and cell‐type) were further performed. Significance level: P 
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Functional connectome impairments associated with occupational burnout were widely distributed, involving both low‐level sensorimotor cortices and high‐level association cortices. Purpose To investigate whether there are hierarchical perturbations in the functional connectomes and if these perturbations are potentially influenced by genetic factors in nurses who feel “burned out.” Study Type Prospective, case control. Population Thirty‐three female nurses with occupational burnout (aged 27–40, 32.42 ± 3.37) and 32 matched nurses who were not feeling burned out (aged 27–42, 32.50 ± 4.21). Field Strength/Sequence 3.0 T, gradient‐echo echo‐planar imaging sequence (GE‐EPI). Assessment Gradient‐based techniques were used to depict the perturbations in the multi‐dimensional hierarchical structure of the macroscale connectome. Gene expression data were acquired from the Allen Human Brain Atlas. Statistical Tests Cortex‐wide multivariate analyses were used for between‐group differences in gradients as well as association analyses between the hierarchy distortions and the MBI score (FDR corrected). Partial least squares, spin test and bootstrapping were utilized together to select the gene sets (FDR corrected). Gene enrichment analyses (GO, KEGG and cell‐type) were further performed. Significance level: P &lt; 0.05. Results There were significant gradient distortions, with strong between‐group effects in the somatosensory network and moderate effects in the higher‐order default‐mode network, which were significantly correlated with the gene expression profiles (r = 0.3171). The most related genes were broadly involved in the cellular response to minerals, neuronal plasticity, and the circadian rhythm pathway (q value &lt; 0.01). Significant enrichments were found in excitatory (r = 0.2588), inhibitory neurons (r = 0.2610), and astrocytes cells (r = 0.2633). Regions affected by burnout severity were mainly distributed in the association and visual cortices. Data Conclusion By connecting in vivo imaging to genes, cell classes, and clinical data, this study provides a framework to understand functional impairments in occupational burnout and how the microscopic genetic architecture drive macroscopic distortions. Evidence Level 1 Technical Efficacy Stage 2</description><identifier>ISSN: 1053-1807</identifier><identifier>ISSN: 1522-2586</identifier><identifier>EISSN: 1522-2586</identifier><identifier>DOI: 10.1002/jmri.28985</identifier><identifier>PMID: 37728385</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley &amp; Sons, Inc</publisher><subject>Adult ; Astrocytes ; Brain - diagnostic imaging ; Burnout ; Burnout, Professional ; Case-Control Studies ; Circadian rhythms ; Connectome ; COVID-19 ; Data acquisition ; Echo-Planar Imaging ; Female ; Females ; Field strength ; functional connectome gradient ; Gene Expression ; Genes ; Genetic factors ; Group effects ; Humans ; imaging‐transcriptomics analysis ; In vivo methods and tests ; Magnetic Resonance Imaging ; Neuroimaging ; Neuroplasticity ; Nurses ; occupational burnout ; Pandemics ; Perturbation ; Plastic foam ; Prospective Studies ; Public health ; resting‐state functional magnetic ; SARS-CoV-2 ; Sensorimotor system ; Somatosensory cortex ; Spin tests ; Statistical analysis ; Statistical tests</subject><ispartof>Journal of magnetic resonance imaging, 2024-06, Vol.59 (6), p.2124-2136</ispartof><rights>2023 International Society for Magnetic Resonance in Medicine.</rights><rights>2024 International Society for Magnetic Resonance in Medicine</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c3525-45f7977dd9b98bb4ca86e174c93d1c1b4d87c61612e285a29a57ea8b94a7e4693</cites><orcidid>0000-0003-3514-5413</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%2Fjmri.28985$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fjmri.28985$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,780,784,1416,27915,27916,45565,45566</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37728385$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Shang, Yingying</creatorcontrib><creatorcontrib>Su, Qian</creatorcontrib><creatorcontrib>Ma, Rong</creatorcontrib><creatorcontrib>Chen, Miao</creatorcontrib><creatorcontrib>Zhao, Ziyang</creatorcontrib><creatorcontrib>Yao, Chaofan</creatorcontrib><creatorcontrib>Han, Lin</creatorcontrib><creatorcontrib>Yao, Zhijun</creatorcontrib><creatorcontrib>Hu, Bin</creatorcontrib><title>Functional Connectome Hierarchy Distortions in Female Nurses With Occupational Burnout and Its Gene Expression Signatures</title><title>Journal of magnetic resonance imaging</title><addtitle>J Magn Reson Imaging</addtitle><description>Background Burnout has become a serious public health issue worldwide, particularly during the COVID‐19 pandemic. Functional connectome impairments associated with occupational burnout were widely distributed, involving both low‐level sensorimotor cortices and high‐level association cortices. Purpose To investigate whether there are hierarchical perturbations in the functional connectomes and if these perturbations are potentially influenced by genetic factors in nurses who feel “burned out.” Study Type Prospective, case control. Population Thirty‐three female nurses with occupational burnout (aged 27–40, 32.42 ± 3.37) and 32 matched nurses who were not feeling burned out (aged 27–42, 32.50 ± 4.21). Field Strength/Sequence 3.0 T, gradient‐echo echo‐planar imaging sequence (GE‐EPI). Assessment Gradient‐based techniques were used to depict the perturbations in the multi‐dimensional hierarchical structure of the macroscale connectome. Gene expression data were acquired from the Allen Human Brain Atlas. Statistical Tests Cortex‐wide multivariate analyses were used for between‐group differences in gradients as well as association analyses between the hierarchy distortions and the MBI score (FDR corrected). Partial least squares, spin test and bootstrapping were utilized together to select the gene sets (FDR corrected). Gene enrichment analyses (GO, KEGG and cell‐type) were further performed. Significance level: P &lt; 0.05. Results There were significant gradient distortions, with strong between‐group effects in the somatosensory network and moderate effects in the higher‐order default‐mode network, which were significantly correlated with the gene expression profiles (r = 0.3171). The most related genes were broadly involved in the cellular response to minerals, neuronal plasticity, and the circadian rhythm pathway (q value &lt; 0.01). Significant enrichments were found in excitatory (r = 0.2588), inhibitory neurons (r = 0.2610), and astrocytes cells (r = 0.2633). Regions affected by burnout severity were mainly distributed in the association and visual cortices. Data Conclusion By connecting in vivo imaging to genes, cell classes, and clinical data, this study provides a framework to understand functional impairments in occupational burnout and how the microscopic genetic architecture drive macroscopic distortions. 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Sons, Inc</general><general>Wiley Subscription Services, Inc</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>7QO</scope><scope>7TK</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>P64</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0003-3514-5413</orcidid></search><sort><creationdate>202406</creationdate><title>Functional Connectome Hierarchy Distortions in Female Nurses With Occupational Burnout and Its Gene Expression Signatures</title><author>Shang, Yingying ; Su, Qian ; Ma, Rong ; Chen, Miao ; Zhao, Ziyang ; Yao, Chaofan ; Han, Lin ; Yao, Zhijun ; Hu, Bin</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3525-45f7977dd9b98bb4ca86e174c93d1c1b4d87c61612e285a29a57ea8b94a7e4693</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Adult</topic><topic>Astrocytes</topic><topic>Brain - diagnostic imaging</topic><topic>Burnout</topic><topic>Burnout, Professional</topic><topic>Case-Control Studies</topic><topic>Circadian rhythms</topic><topic>Connectome</topic><topic>COVID-19</topic><topic>Data acquisition</topic><topic>Echo-Planar Imaging</topic><topic>Female</topic><topic>Females</topic><topic>Field strength</topic><topic>functional connectome gradient</topic><topic>Gene Expression</topic><topic>Genes</topic><topic>Genetic factors</topic><topic>Group effects</topic><topic>Humans</topic><topic>imaging‐transcriptomics analysis</topic><topic>In vivo methods and tests</topic><topic>Magnetic Resonance Imaging</topic><topic>Neuroimaging</topic><topic>Neuroplasticity</topic><topic>Nurses</topic><topic>occupational burnout</topic><topic>Pandemics</topic><topic>Perturbation</topic><topic>Plastic foam</topic><topic>Prospective Studies</topic><topic>Public health</topic><topic>resting‐state functional magnetic</topic><topic>SARS-CoV-2</topic><topic>Sensorimotor system</topic><topic>Somatosensory cortex</topic><topic>Spin tests</topic><topic>Statistical analysis</topic><topic>Statistical tests</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Shang, Yingying</creatorcontrib><creatorcontrib>Su, Qian</creatorcontrib><creatorcontrib>Ma, Rong</creatorcontrib><creatorcontrib>Chen, Miao</creatorcontrib><creatorcontrib>Zhao, Ziyang</creatorcontrib><creatorcontrib>Yao, Chaofan</creatorcontrib><creatorcontrib>Han, Lin</creatorcontrib><creatorcontrib>Yao, Zhijun</creatorcontrib><creatorcontrib>Hu, Bin</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Journal of magnetic resonance imaging</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Shang, Yingying</au><au>Su, Qian</au><au>Ma, Rong</au><au>Chen, Miao</au><au>Zhao, Ziyang</au><au>Yao, Chaofan</au><au>Han, Lin</au><au>Yao, Zhijun</au><au>Hu, Bin</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Functional Connectome Hierarchy Distortions in Female Nurses With Occupational Burnout and Its Gene Expression Signatures</atitle><jtitle>Journal of magnetic resonance imaging</jtitle><addtitle>J Magn Reson Imaging</addtitle><date>2024-06</date><risdate>2024</risdate><volume>59</volume><issue>6</issue><spage>2124</spage><epage>2136</epage><pages>2124-2136</pages><issn>1053-1807</issn><issn>1522-2586</issn><eissn>1522-2586</eissn><abstract>Background Burnout has become a serious public health issue worldwide, particularly during the COVID‐19 pandemic. Functional connectome impairments associated with occupational burnout were widely distributed, involving both low‐level sensorimotor cortices and high‐level association cortices. Purpose To investigate whether there are hierarchical perturbations in the functional connectomes and if these perturbations are potentially influenced by genetic factors in nurses who feel “burned out.” Study Type Prospective, case control. Population Thirty‐three female nurses with occupational burnout (aged 27–40, 32.42 ± 3.37) and 32 matched nurses who were not feeling burned out (aged 27–42, 32.50 ± 4.21). Field Strength/Sequence 3.0 T, gradient‐echo echo‐planar imaging sequence (GE‐EPI). Assessment Gradient‐based techniques were used to depict the perturbations in the multi‐dimensional hierarchical structure of the macroscale connectome. Gene expression data were acquired from the Allen Human Brain Atlas. Statistical Tests Cortex‐wide multivariate analyses were used for between‐group differences in gradients as well as association analyses between the hierarchy distortions and the MBI score (FDR corrected). Partial least squares, spin test and bootstrapping were utilized together to select the gene sets (FDR corrected). Gene enrichment analyses (GO, KEGG and cell‐type) were further performed. Significance level: P &lt; 0.05. Results There were significant gradient distortions, with strong between‐group effects in the somatosensory network and moderate effects in the higher‐order default‐mode network, which were significantly correlated with the gene expression profiles (r = 0.3171). The most related genes were broadly involved in the cellular response to minerals, neuronal plasticity, and the circadian rhythm pathway (q value &lt; 0.01). Significant enrichments were found in excitatory (r = 0.2588), inhibitory neurons (r = 0.2610), and astrocytes cells (r = 0.2633). Regions affected by burnout severity were mainly distributed in the association and visual cortices. Data Conclusion By connecting in vivo imaging to genes, cell classes, and clinical data, this study provides a framework to understand functional impairments in occupational burnout and how the microscopic genetic architecture drive macroscopic distortions. Evidence Level 1 Technical Efficacy Stage 2</abstract><cop>Hoboken, USA</cop><pub>John Wiley &amp; Sons, Inc</pub><pmid>37728385</pmid><doi>10.1002/jmri.28985</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0003-3514-5413</orcidid><oa>free_for_read</oa></addata></record>
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subjects Adult
Astrocytes
Brain - diagnostic imaging
Burnout
Burnout, Professional
Case-Control Studies
Circadian rhythms
Connectome
COVID-19
Data acquisition
Echo-Planar Imaging
Female
Females
Field strength
functional connectome gradient
Gene Expression
Genes
Genetic factors
Group effects
Humans
imaging‐transcriptomics analysis
In vivo methods and tests
Magnetic Resonance Imaging
Neuroimaging
Neuroplasticity
Nurses
occupational burnout
Pandemics
Perturbation
Plastic foam
Prospective Studies
Public health
resting‐state functional magnetic
SARS-CoV-2
Sensorimotor system
Somatosensory cortex
Spin tests
Statistical analysis
Statistical tests
title Functional Connectome Hierarchy Distortions in Female Nurses With Occupational Burnout and Its Gene Expression Signatures
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