Cortical atrophy accelerates as cognitive decline worsens in multiple sclerosis

OBJECTIVETo determine which pathologic process could be responsible for the acceleration of cognitive decline during the course of multiple sclerosis (MS), using longitudinal structural MRI, which was related to cognitive decline in relapsing-remitting MS (RRMS) and progressive MS (PMS). METHODSA pr...

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Veröffentlicht in:Neurology 2019-10, Vol.93 (14), p.e1348-e1359
Hauptverfasser: Eijlers, Anand J.C, Dekker, Iris, Steenwijk, Martijn D, Meijer, Kim A, Hulst, Hanneke E, Pouwels, Petra J.W, Uitdehaag, Bernard M.J, Barkhof, Frederik, Vrenken, Hugo, Schoonheim, Menno M, Geurts, Jeroen J.G
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container_end_page e1359
container_issue 14
container_start_page e1348
container_title Neurology
container_volume 93
creator Eijlers, Anand J.C
Dekker, Iris
Steenwijk, Martijn D
Meijer, Kim A
Hulst, Hanneke E
Pouwels, Petra J.W
Uitdehaag, Bernard M.J
Barkhof, Frederik
Vrenken, Hugo
Schoonheim, Menno M
Geurts, Jeroen J.G
description OBJECTIVETo determine which pathologic process could be responsible for the acceleration of cognitive decline during the course of multiple sclerosis (MS), using longitudinal structural MRI, which was related to cognitive decline in relapsing-remitting MS (RRMS) and progressive MS (PMS). METHODSA prospective cohort of 230 patients with MS (179 RRMS and 51 PMS) and 59 healthy controls was evaluated twice with 5-year (mean 4.9, SD 0.94) interval during which 22 patients with RRMS converted to PMS. Annual rates of cortical and deep gray matter atrophy as well as lesion volume increase were computed on longitudinal (3T) MRI data and correlated to the annual rate of cognitive decline as measured using an extensive cognitive evaluation at both time points. RESULTSThe deep gray matter atrophy rate did not differ between PMS and RRMS (−0.82%/year vs −0.71%/year, p = 0.11), while faster cortical atrophy was observed in PMS (−0.87%/year vs −0.48%/year, p < 0.01). Similarly, faster cognitive decline was observed in PMS compared to RRMS (p < 0.01). Annual cognitive decline was related to the rate of annual lesion volume increase in stable RRMS (r = −0.17, p = 0.03) to the rate of annual deep gray matter atrophy in converting RRMS (r = 0.50, p = 0.02) and annual cortical atrophy in PMS (r = 0.35, p = 0.01). CONCLUSIONSThese results indicate that cortical atrophy and cognitive decline accelerate together during the course of MS. Substrates of cognitive decline shifted from worsening lesional pathology in stable RRMS to deep gray matter atrophy in converting RRMS and to accelerated cortical atrophy in PMS only.
doi_str_mv 10.1212/WNL.0000000000008198
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METHODSA prospective cohort of 230 patients with MS (179 RRMS and 51 PMS) and 59 healthy controls was evaluated twice with 5-year (mean 4.9, SD 0.94) interval during which 22 patients with RRMS converted to PMS. Annual rates of cortical and deep gray matter atrophy as well as lesion volume increase were computed on longitudinal (3T) MRI data and correlated to the annual rate of cognitive decline as measured using an extensive cognitive evaluation at both time points. RESULTSThe deep gray matter atrophy rate did not differ between PMS and RRMS (−0.82%/year vs −0.71%/year, p = 0.11), while faster cortical atrophy was observed in PMS (−0.87%/year vs −0.48%/year, p &lt; 0.01). Similarly, faster cognitive decline was observed in PMS compared to RRMS (p &lt; 0.01). Annual cognitive decline was related to the rate of annual lesion volume increase in stable RRMS (r = −0.17, p = 0.03) to the rate of annual deep gray matter atrophy in converting RRMS (r = 0.50, p = 0.02) and annual cortical atrophy in PMS (r = 0.35, p = 0.01). CONCLUSIONSThese results indicate that cortical atrophy and cognitive decline accelerate together during the course of MS. Substrates of cognitive decline shifted from worsening lesional pathology in stable RRMS to deep gray matter atrophy in converting RRMS and to accelerated cortical atrophy in PMS only.</description><identifier>ISSN: 0028-3878</identifier><identifier>EISSN: 1526-632X</identifier><identifier>DOI: 10.1212/WNL.0000000000008198</identifier><identifier>PMID: 31484713</identifier><language>eng</language><publisher>United States: American Academy of Neurology</publisher><subject>Adult ; Aged ; Atrophy - diagnostic imaging ; Atrophy - epidemiology ; Atrophy - psychology ; Cerebral Cortex - diagnostic imaging ; Cognitive Dysfunction - diagnostic imaging ; Cognitive Dysfunction - epidemiology ; Cognitive Dysfunction - psychology ; Cohort Studies ; Female ; Follow-Up Studies ; Humans ; Longitudinal Studies ; Magnetic Resonance Imaging - trends ; Male ; Middle Aged ; Multiple Sclerosis - diagnostic imaging ; Multiple Sclerosis - epidemiology ; Multiple Sclerosis - psychology ; Prospective Studies</subject><ispartof>Neurology, 2019-10, Vol.93 (14), p.e1348-e1359</ispartof><rights>2019 American Academy of Neurology</rights><rights>2019 American Academy of Neurology.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4078-b8e5bf3942a0bcd2bd565ce22a2f945dca16795a266860bc6cafdd5c82bbd7ef3</citedby><cites>FETCH-LOGICAL-c4078-b8e5bf3942a0bcd2bd565ce22a2f945dca16795a266860bc6cafdd5c82bbd7ef3</cites><orcidid>0000-0002-2504-6959 ; 0000-0002-6651-574X</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/31484713$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Eijlers, Anand J.C</creatorcontrib><creatorcontrib>Dekker, Iris</creatorcontrib><creatorcontrib>Steenwijk, Martijn D</creatorcontrib><creatorcontrib>Meijer, Kim A</creatorcontrib><creatorcontrib>Hulst, Hanneke E</creatorcontrib><creatorcontrib>Pouwels, Petra J.W</creatorcontrib><creatorcontrib>Uitdehaag, Bernard M.J</creatorcontrib><creatorcontrib>Barkhof, Frederik</creatorcontrib><creatorcontrib>Vrenken, Hugo</creatorcontrib><creatorcontrib>Schoonheim, Menno M</creatorcontrib><creatorcontrib>Geurts, Jeroen J.G</creatorcontrib><title>Cortical atrophy accelerates as cognitive decline worsens in multiple sclerosis</title><title>Neurology</title><addtitle>Neurology</addtitle><description>OBJECTIVETo determine which pathologic process could be responsible for the acceleration of cognitive decline during the course of multiple sclerosis (MS), using longitudinal structural MRI, which was related to cognitive decline in relapsing-remitting MS (RRMS) and progressive MS (PMS). METHODSA prospective cohort of 230 patients with MS (179 RRMS and 51 PMS) and 59 healthy controls was evaluated twice with 5-year (mean 4.9, SD 0.94) interval during which 22 patients with RRMS converted to PMS. Annual rates of cortical and deep gray matter atrophy as well as lesion volume increase were computed on longitudinal (3T) MRI data and correlated to the annual rate of cognitive decline as measured using an extensive cognitive evaluation at both time points. RESULTSThe deep gray matter atrophy rate did not differ between PMS and RRMS (−0.82%/year vs −0.71%/year, p = 0.11), while faster cortical atrophy was observed in PMS (−0.87%/year vs −0.48%/year, p &lt; 0.01). Similarly, faster cognitive decline was observed in PMS compared to RRMS (p &lt; 0.01). Annual cognitive decline was related to the rate of annual lesion volume increase in stable RRMS (r = −0.17, p = 0.03) to the rate of annual deep gray matter atrophy in converting RRMS (r = 0.50, p = 0.02) and annual cortical atrophy in PMS (r = 0.35, p = 0.01). CONCLUSIONSThese results indicate that cortical atrophy and cognitive decline accelerate together during the course of MS. Substrates of cognitive decline shifted from worsening lesional pathology in stable RRMS to deep gray matter atrophy in converting RRMS and to accelerated cortical atrophy in PMS only.</description><subject>Adult</subject><subject>Aged</subject><subject>Atrophy - diagnostic imaging</subject><subject>Atrophy - epidemiology</subject><subject>Atrophy - psychology</subject><subject>Cerebral Cortex - diagnostic imaging</subject><subject>Cognitive Dysfunction - diagnostic imaging</subject><subject>Cognitive Dysfunction - epidemiology</subject><subject>Cognitive Dysfunction - psychology</subject><subject>Cohort Studies</subject><subject>Female</subject><subject>Follow-Up Studies</subject><subject>Humans</subject><subject>Longitudinal Studies</subject><subject>Magnetic Resonance Imaging - trends</subject><subject>Male</subject><subject>Middle Aged</subject><subject>Multiple Sclerosis - diagnostic imaging</subject><subject>Multiple Sclerosis - epidemiology</subject><subject>Multiple Sclerosis - psychology</subject><subject>Prospective Studies</subject><issn>0028-3878</issn><issn>1526-632X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kM1OwzAQhC0EoqXwBgj5yCXFdmLHOaKKP6miFxDcIsfZUIOTFNuh6ttj1IIQB_ayh_1mdjQInVIypYyyi6f7-ZT8GkkLuYfGlDORiJQ976MxIUwmqczlCB15_0pIPObFIRqlNJNZTtMxWsx6F4xWFqvg-tVyg5XWYMGpAB4rj3X_0plgPgDXoK3pAK9756Hz2HS4HWwwKwvY6yjpvfHH6KBR1sPJbk_Q4_XVw-w2mS9u7maX80RnJJdJJYFXTVpkTJFK16yqueAaGFOsKTJea0VFXnDFhJAiEkKrpq65lqyq6hyadILOt74r178P4EPZGh-DW9VBP_iSMckpSSnlEc22qI4JvYOmXDnTKrcpKSm_qixjleXfKqPsbPdhqFqof0Tf3UVAboF1bwM4_2aHNbhyCcqG5f_en7Czgek</recordid><startdate>20191001</startdate><enddate>20191001</enddate><creator>Eijlers, Anand J.C</creator><creator>Dekker, Iris</creator><creator>Steenwijk, Martijn D</creator><creator>Meijer, Kim A</creator><creator>Hulst, Hanneke E</creator><creator>Pouwels, Petra J.W</creator><creator>Uitdehaag, Bernard M.J</creator><creator>Barkhof, Frederik</creator><creator>Vrenken, Hugo</creator><creator>Schoonheim, Menno M</creator><creator>Geurts, Jeroen J.G</creator><general>American Academy of Neurology</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/0000-0002-2504-6959</orcidid><orcidid>https://orcid.org/0000-0002-6651-574X</orcidid></search><sort><creationdate>20191001</creationdate><title>Cortical atrophy accelerates as cognitive decline worsens in multiple sclerosis</title><author>Eijlers, Anand J.C ; Dekker, Iris ; Steenwijk, Martijn D ; Meijer, Kim A ; Hulst, Hanneke E ; Pouwels, Petra J.W ; Uitdehaag, Bernard M.J ; Barkhof, Frederik ; Vrenken, Hugo ; Schoonheim, Menno M ; Geurts, Jeroen J.G</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4078-b8e5bf3942a0bcd2bd565ce22a2f945dca16795a266860bc6cafdd5c82bbd7ef3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Adult</topic><topic>Aged</topic><topic>Atrophy - diagnostic imaging</topic><topic>Atrophy - epidemiology</topic><topic>Atrophy - psychology</topic><topic>Cerebral Cortex - diagnostic imaging</topic><topic>Cognitive Dysfunction - diagnostic imaging</topic><topic>Cognitive Dysfunction - epidemiology</topic><topic>Cognitive Dysfunction - psychology</topic><topic>Cohort Studies</topic><topic>Female</topic><topic>Follow-Up Studies</topic><topic>Humans</topic><topic>Longitudinal Studies</topic><topic>Magnetic Resonance Imaging - trends</topic><topic>Male</topic><topic>Middle Aged</topic><topic>Multiple Sclerosis - diagnostic imaging</topic><topic>Multiple Sclerosis - epidemiology</topic><topic>Multiple Sclerosis - psychology</topic><topic>Prospective Studies</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Eijlers, Anand J.C</creatorcontrib><creatorcontrib>Dekker, Iris</creatorcontrib><creatorcontrib>Steenwijk, Martijn D</creatorcontrib><creatorcontrib>Meijer, Kim A</creatorcontrib><creatorcontrib>Hulst, Hanneke E</creatorcontrib><creatorcontrib>Pouwels, Petra J.W</creatorcontrib><creatorcontrib>Uitdehaag, Bernard M.J</creatorcontrib><creatorcontrib>Barkhof, Frederik</creatorcontrib><creatorcontrib>Vrenken, Hugo</creatorcontrib><creatorcontrib>Schoonheim, Menno M</creatorcontrib><creatorcontrib>Geurts, Jeroen J.G</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>Neurology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Eijlers, Anand J.C</au><au>Dekker, Iris</au><au>Steenwijk, Martijn D</au><au>Meijer, Kim A</au><au>Hulst, Hanneke E</au><au>Pouwels, Petra J.W</au><au>Uitdehaag, Bernard M.J</au><au>Barkhof, Frederik</au><au>Vrenken, Hugo</au><au>Schoonheim, Menno M</au><au>Geurts, Jeroen J.G</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Cortical atrophy accelerates as cognitive decline worsens in multiple sclerosis</atitle><jtitle>Neurology</jtitle><addtitle>Neurology</addtitle><date>2019-10-01</date><risdate>2019</risdate><volume>93</volume><issue>14</issue><spage>e1348</spage><epage>e1359</epage><pages>e1348-e1359</pages><issn>0028-3878</issn><eissn>1526-632X</eissn><abstract>OBJECTIVETo determine which pathologic process could be responsible for the acceleration of cognitive decline during the course of multiple sclerosis (MS), using longitudinal structural MRI, which was related to cognitive decline in relapsing-remitting MS (RRMS) and progressive MS (PMS). METHODSA prospective cohort of 230 patients with MS (179 RRMS and 51 PMS) and 59 healthy controls was evaluated twice with 5-year (mean 4.9, SD 0.94) interval during which 22 patients with RRMS converted to PMS. Annual rates of cortical and deep gray matter atrophy as well as lesion volume increase were computed on longitudinal (3T) MRI data and correlated to the annual rate of cognitive decline as measured using an extensive cognitive evaluation at both time points. RESULTSThe deep gray matter atrophy rate did not differ between PMS and RRMS (−0.82%/year vs −0.71%/year, p = 0.11), while faster cortical atrophy was observed in PMS (−0.87%/year vs −0.48%/year, p &lt; 0.01). Similarly, faster cognitive decline was observed in PMS compared to RRMS (p &lt; 0.01). Annual cognitive decline was related to the rate of annual lesion volume increase in stable RRMS (r = −0.17, p = 0.03) to the rate of annual deep gray matter atrophy in converting RRMS (r = 0.50, p = 0.02) and annual cortical atrophy in PMS (r = 0.35, p = 0.01). CONCLUSIONSThese results indicate that cortical atrophy and cognitive decline accelerate together during the course of MS. Substrates of cognitive decline shifted from worsening lesional pathology in stable RRMS to deep gray matter atrophy in converting RRMS and to accelerated cortical atrophy in PMS only.</abstract><cop>United States</cop><pub>American Academy of Neurology</pub><pmid>31484713</pmid><doi>10.1212/WNL.0000000000008198</doi><orcidid>https://orcid.org/0000-0002-2504-6959</orcidid><orcidid>https://orcid.org/0000-0002-6651-574X</orcidid></addata></record>
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subjects Adult
Aged
Atrophy - diagnostic imaging
Atrophy - epidemiology
Atrophy - psychology
Cerebral Cortex - diagnostic imaging
Cognitive Dysfunction - diagnostic imaging
Cognitive Dysfunction - epidemiology
Cognitive Dysfunction - psychology
Cohort Studies
Female
Follow-Up Studies
Humans
Longitudinal Studies
Magnetic Resonance Imaging - trends
Male
Middle Aged
Multiple Sclerosis - diagnostic imaging
Multiple Sclerosis - epidemiology
Multiple Sclerosis - psychology
Prospective Studies
title Cortical atrophy accelerates as cognitive decline worsens in multiple sclerosis
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