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Impaired frontal‐parietal control network in chronic prostatitis/chronic pelvic pain syndrome revealed by graph theoretical analysis: A DTI study
Chronic prostatitis/chronic pelvic pain syndrome (CP/CPPS) is characterized by chronic pain in pelvic area and lower urinary tract symptoms (LUTS). Previous neuroimaging studies demonstrated that chronic pain was associated with the altered brain activity. However, the pathological mechanisms associ...
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Published in: | The European journal of neuroscience 2021-02, Vol.53 (4), p.1060-1071 |
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description | Chronic prostatitis/chronic pelvic pain syndrome (CP/CPPS) is characterized by chronic pain in pelvic area and lower urinary tract symptoms (LUTS). Previous neuroimaging studies demonstrated that chronic pain was associated with the altered brain activity. However, the pathological mechanisms associated with altered brain control of CP/CPPS are not well‐understood. Therefore, we sought to investigate the topological properties of white matter brain networks in patients with CP/CPPS and whether the topological configuration of frontal‐parietal control network was disrupted. We collected 19 patients with CP/CPPS and 32 matched healthy controls (HCs). Diffusion tensor imaging data of all participates were used to map the white matter structural networks. Graph theoretical method was applied to investigate the alterations of topological properties of brain network in patients. Moreover, we also investigated whether the alerted brain regions might be correlated with any clinical features of patients by the method of Pearson correlation analysis. Both CP/CPPS patients and HCs exhibited a ‘small‐world’ behavior or economical small‐world architecture of the white matter brain networks. In addition, CP/CPPS had a lower global efficiency in the right middle frontal gyrus (orbital part) and a higher global efficiency in the left middle cingulate and paracingulate gyri. CP/CPPS also showed increased local efficiency in the left middle cingulate and paracingulate gyri and paracentral lobule. Moreover, the local efficiency of the left middle cingulate gyrus was positively correlated with the scores of the influence of symptoms on the quality of life. The local efficiency of the left precuneus and right supplementary motor area were positively correlated with the total scores of NIH‐CPSI and the scores of pain and discomfort symptoms, respectively. Together, we found that patients with CP/CPPS had alterations of connections within the frontal‐parietal control network, which suggested that the altered connectivity involved in the executive control processing procedures might contribute to the pathogenesis of the pelvic pain and LUTS in CP/CPPS. Thus these results provided new insights into the understanding of CP/CPPS.
Regional nodal efficiency of the WM brain networks in CP/CPPS. (a) brain regions with abnormal global efficiency in CP/CPPS; (b) brain regions with abnormal local efficiency in CP/CPPS. L: left; R: right; ORBmid: middle frontal gyrus (orbital part); SMA: su |
doi_str_mv | 10.1111/ejn.14962 |
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Regional nodal efficiency of the WM brain networks in CP/CPPS. (a) brain regions with abnormal global efficiency in CP/CPPS; (b) brain regions with abnormal local efficiency in CP/CPPS. L: left; R: right; ORBmid: middle frontal gyrus (orbital part); SMA: supplementary motor area; DCG: middle cingulate and paracingulate gyri; PoCG: postcentral gyrus; PCL: paracentral lobule; PreCG: precental gyrus; SMA: supplementary motor area; PCG: posterior cingulate gyrus; PHG: parahippocampal gyrus; SPG: superior parietal gyrus; SMG: supramarginal gyrus; PCUN: precuneus; STG: superior temporal gyrus.</description><identifier>ISSN: 0953-816X</identifier><identifier>EISSN: 1460-9568</identifier><identifier>DOI: 10.1111/ejn.14962</identifier><identifier>PMID: 32896914</identifier><language>eng</language><publisher>France: Wiley Subscription Services, Inc</publisher><subject>Chronic pain ; chronic prostatitis/chronic pelvic pain syndrome ; Correlation analysis ; Cortex (parietal) ; diffusion tensor imaging ; Efficiency ; Executive function ; Frontal gyrus ; graph theory ; Magnetic resonance imaging ; Neural networks ; Neuroimaging ; Pain ; Pelvis ; Prostatitis ; Quality of life ; small‐world ; Substantia alba ; Supplementary motor area ; Urinary tract ; white matter</subject><ispartof>The European journal of neuroscience, 2021-02, Vol.53 (4), p.1060-1071</ispartof><rights>2020 Federation of European Neuroscience Societies and John Wiley & Sons Ltd</rights><rights>2020 Federation of European Neuroscience Societies and John Wiley & Sons Ltd.</rights><rights>Copyright © 2021 Federation of European Neuroscience Societies and John Wiley & Sons Ltd</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3882-d3fdad6a9d762353209c6c4db40c1100e8e79df685429205a3c22cf54e58ce0a3</citedby><cites>FETCH-LOGICAL-c3882-d3fdad6a9d762353209c6c4db40c1100e8e79df685429205a3c22cf54e58ce0a3</cites><orcidid>0000-0003-0389-4049</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32896914$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Huang, Xinfei</creatorcontrib><creatorcontrib>Chen, Jianhuai</creatorcontrib><creatorcontrib>Liu, Shaowei</creatorcontrib><creatorcontrib>Gong, Qingkuo</creatorcontrib><creatorcontrib>Liu, Tao</creatorcontrib><creatorcontrib>Lu, Chao</creatorcontrib><creatorcontrib>Qin, Zhan</creatorcontrib><creatorcontrib>Cui, Hongliang</creatorcontrib><creatorcontrib>Chen, Yun</creatorcontrib><creatorcontrib>Zhu, Yongkang</creatorcontrib><title>Impaired frontal‐parietal control network in chronic prostatitis/chronic pelvic pain syndrome revealed by graph theoretical analysis: A DTI study</title><title>The European journal of neuroscience</title><addtitle>Eur J Neurosci</addtitle><description>Chronic prostatitis/chronic pelvic pain syndrome (CP/CPPS) is characterized by chronic pain in pelvic area and lower urinary tract symptoms (LUTS). Previous neuroimaging studies demonstrated that chronic pain was associated with the altered brain activity. However, the pathological mechanisms associated with altered brain control of CP/CPPS are not well‐understood. Therefore, we sought to investigate the topological properties of white matter brain networks in patients with CP/CPPS and whether the topological configuration of frontal‐parietal control network was disrupted. We collected 19 patients with CP/CPPS and 32 matched healthy controls (HCs). Diffusion tensor imaging data of all participates were used to map the white matter structural networks. Graph theoretical method was applied to investigate the alterations of topological properties of brain network in patients. Moreover, we also investigated whether the alerted brain regions might be correlated with any clinical features of patients by the method of Pearson correlation analysis. Both CP/CPPS patients and HCs exhibited a ‘small‐world’ behavior or economical small‐world architecture of the white matter brain networks. In addition, CP/CPPS had a lower global efficiency in the right middle frontal gyrus (orbital part) and a higher global efficiency in the left middle cingulate and paracingulate gyri. CP/CPPS also showed increased local efficiency in the left middle cingulate and paracingulate gyri and paracentral lobule. Moreover, the local efficiency of the left middle cingulate gyrus was positively correlated with the scores of the influence of symptoms on the quality of life. The local efficiency of the left precuneus and right supplementary motor area were positively correlated with the total scores of NIH‐CPSI and the scores of pain and discomfort symptoms, respectively. Together, we found that patients with CP/CPPS had alterations of connections within the frontal‐parietal control network, which suggested that the altered connectivity involved in the executive control processing procedures might contribute to the pathogenesis of the pelvic pain and LUTS in CP/CPPS. Thus these results provided new insights into the understanding of CP/CPPS.
Regional nodal efficiency of the WM brain networks in CP/CPPS. (a) brain regions with abnormal global efficiency in CP/CPPS; (b) brain regions with abnormal local efficiency in CP/CPPS. L: left; R: right; ORBmid: middle frontal gyrus (orbital part); SMA: supplementary motor area; DCG: middle cingulate and paracingulate gyri; PoCG: postcentral gyrus; PCL: paracentral lobule; PreCG: precental gyrus; SMA: supplementary motor area; PCG: posterior cingulate gyrus; PHG: parahippocampal gyrus; SPG: superior parietal gyrus; SMG: supramarginal gyrus; PCUN: precuneus; STG: superior temporal gyrus.</description><subject>Chronic pain</subject><subject>chronic prostatitis/chronic pelvic pain syndrome</subject><subject>Correlation analysis</subject><subject>Cortex (parietal)</subject><subject>diffusion tensor imaging</subject><subject>Efficiency</subject><subject>Executive function</subject><subject>Frontal gyrus</subject><subject>graph theory</subject><subject>Magnetic resonance imaging</subject><subject>Neural networks</subject><subject>Neuroimaging</subject><subject>Pain</subject><subject>Pelvis</subject><subject>Prostatitis</subject><subject>Quality of life</subject><subject>small‐world</subject><subject>Substantia alba</subject><subject>Supplementary motor area</subject><subject>Urinary tract</subject><subject>white matter</subject><issn>0953-816X</issn><issn>1460-9568</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNp1kUtuFDEQhi0EIkNgwQWQJTaw6Ixf7djsohDIoAg2QWLX8tjVjAf3A9udqHccASk3zEnwZEIWSHhTVunT5yr_CL2k5IiWs4Rtf0SFluwRWlAhSaVrqR6jBdE1rxSV3w7Qs5S2hBAlRf0UHXCmtNRULNDNqhuNj-BwG4c-m3D76_dooodyxbZ04hBwD_l6iD-w77HdFMxbPMYhZZN99mn50INwtSumcGnuXRw6wBGuwITiX8_4ezTjBucNDBGyt-UF05swJ5_e4RP8_nKFU57c_Bw9aU1I8OK-HqKvH84uT8-riy8fV6cnF5XlSrHK8dYZJ412x5LxmjOirbTCrQWxlBICCo61a6WqBdOM1IZbxmxbC6iVBWL4IXqz95Zlfk6QctP5ZCEE08MwpYYJQZTWWtGCvv4H3Q5TLMPvKE0lF5KRQr3dU7b8TorQNmP0nYlzQ0mzS6opSTV3SRX21b1xWnfgHsi_0RRguQeufYD5_6bm7NPnvfIPJ9SgqA</recordid><startdate>202102</startdate><enddate>202102</enddate><creator>Huang, Xinfei</creator><creator>Chen, Jianhuai</creator><creator>Liu, Shaowei</creator><creator>Gong, Qingkuo</creator><creator>Liu, Tao</creator><creator>Lu, Chao</creator><creator>Qin, Zhan</creator><creator>Cui, Hongliang</creator><creator>Chen, Yun</creator><creator>Zhu, Yongkang</creator><general>Wiley Subscription Services, Inc</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0003-0389-4049</orcidid></search><sort><creationdate>202102</creationdate><title>Impaired frontal‐parietal control network in chronic prostatitis/chronic pelvic pain syndrome revealed by graph theoretical analysis: A DTI study</title><author>Huang, Xinfei ; Chen, Jianhuai ; Liu, Shaowei ; Gong, Qingkuo ; Liu, Tao ; Lu, Chao ; Qin, Zhan ; Cui, Hongliang ; Chen, Yun ; Zhu, Yongkang</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3882-d3fdad6a9d762353209c6c4db40c1100e8e79df685429205a3c22cf54e58ce0a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Chronic pain</topic><topic>chronic prostatitis/chronic pelvic pain syndrome</topic><topic>Correlation analysis</topic><topic>Cortex (parietal)</topic><topic>diffusion tensor imaging</topic><topic>Efficiency</topic><topic>Executive function</topic><topic>Frontal gyrus</topic><topic>graph theory</topic><topic>Magnetic resonance imaging</topic><topic>Neural networks</topic><topic>Neuroimaging</topic><topic>Pain</topic><topic>Pelvis</topic><topic>Prostatitis</topic><topic>Quality of life</topic><topic>small‐world</topic><topic>Substantia alba</topic><topic>Supplementary motor area</topic><topic>Urinary tract</topic><topic>white matter</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Huang, Xinfei</creatorcontrib><creatorcontrib>Chen, Jianhuai</creatorcontrib><creatorcontrib>Liu, Shaowei</creatorcontrib><creatorcontrib>Gong, Qingkuo</creatorcontrib><creatorcontrib>Liu, Tao</creatorcontrib><creatorcontrib>Lu, Chao</creatorcontrib><creatorcontrib>Qin, Zhan</creatorcontrib><creatorcontrib>Cui, Hongliang</creatorcontrib><creatorcontrib>Chen, Yun</creatorcontrib><creatorcontrib>Zhu, Yongkang</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>The European journal of neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Huang, Xinfei</au><au>Chen, Jianhuai</au><au>Liu, Shaowei</au><au>Gong, Qingkuo</au><au>Liu, Tao</au><au>Lu, Chao</au><au>Qin, Zhan</au><au>Cui, Hongliang</au><au>Chen, Yun</au><au>Zhu, Yongkang</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Impaired frontal‐parietal control network in chronic prostatitis/chronic pelvic pain syndrome revealed by graph theoretical analysis: A DTI study</atitle><jtitle>The European journal of neuroscience</jtitle><addtitle>Eur J Neurosci</addtitle><date>2021-02</date><risdate>2021</risdate><volume>53</volume><issue>4</issue><spage>1060</spage><epage>1071</epage><pages>1060-1071</pages><issn>0953-816X</issn><eissn>1460-9568</eissn><abstract>Chronic prostatitis/chronic pelvic pain syndrome (CP/CPPS) is characterized by chronic pain in pelvic area and lower urinary tract symptoms (LUTS). Previous neuroimaging studies demonstrated that chronic pain was associated with the altered brain activity. However, the pathological mechanisms associated with altered brain control of CP/CPPS are not well‐understood. Therefore, we sought to investigate the topological properties of white matter brain networks in patients with CP/CPPS and whether the topological configuration of frontal‐parietal control network was disrupted. We collected 19 patients with CP/CPPS and 32 matched healthy controls (HCs). Diffusion tensor imaging data of all participates were used to map the white matter structural networks. Graph theoretical method was applied to investigate the alterations of topological properties of brain network in patients. Moreover, we also investigated whether the alerted brain regions might be correlated with any clinical features of patients by the method of Pearson correlation analysis. Both CP/CPPS patients and HCs exhibited a ‘small‐world’ behavior or economical small‐world architecture of the white matter brain networks. In addition, CP/CPPS had a lower global efficiency in the right middle frontal gyrus (orbital part) and a higher global efficiency in the left middle cingulate and paracingulate gyri. CP/CPPS also showed increased local efficiency in the left middle cingulate and paracingulate gyri and paracentral lobule. Moreover, the local efficiency of the left middle cingulate gyrus was positively correlated with the scores of the influence of symptoms on the quality of life. The local efficiency of the left precuneus and right supplementary motor area were positively correlated with the total scores of NIH‐CPSI and the scores of pain and discomfort symptoms, respectively. Together, we found that patients with CP/CPPS had alterations of connections within the frontal‐parietal control network, which suggested that the altered connectivity involved in the executive control processing procedures might contribute to the pathogenesis of the pelvic pain and LUTS in CP/CPPS. Thus these results provided new insights into the understanding of CP/CPPS.
Regional nodal efficiency of the WM brain networks in CP/CPPS. (a) brain regions with abnormal global efficiency in CP/CPPS; (b) brain regions with abnormal local efficiency in CP/CPPS. L: left; R: right; ORBmid: middle frontal gyrus (orbital part); SMA: supplementary motor area; DCG: middle cingulate and paracingulate gyri; PoCG: postcentral gyrus; PCL: paracentral lobule; PreCG: precental gyrus; SMA: supplementary motor area; PCG: posterior cingulate gyrus; PHG: parahippocampal gyrus; SPG: superior parietal gyrus; SMG: supramarginal gyrus; PCUN: precuneus; STG: superior temporal gyrus.</abstract><cop>France</cop><pub>Wiley Subscription Services, Inc</pub><pmid>32896914</pmid><doi>10.1111/ejn.14962</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0003-0389-4049</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Chronic pain chronic prostatitis/chronic pelvic pain syndrome Correlation analysis Cortex (parietal) diffusion tensor imaging Efficiency Executive function Frontal gyrus graph theory Magnetic resonance imaging Neural networks Neuroimaging Pain Pelvis Prostatitis Quality of life small‐world Substantia alba Supplementary motor area Urinary tract white matter |
title | Impaired frontal‐parietal control network in chronic prostatitis/chronic pelvic pain syndrome revealed by graph theoretical analysis: A DTI study |
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