Consequences of repeated blood-brain barrier disruption in football players
The acknowledgement of risks for traumatic brain injury in American football players has prompted studies for sideline concussion diagnosis and testing for neurological deficits. While concussions are recognized etiological factors for a spectrum of neurological sequelae, the consequences of sub-con...
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| creator | Marchi, Nicola Bazarian, Jeffrey J Puvenna, Vikram Janigro, Mattia Ghosh, Chaitali Zhong, Jianhui Zhu, Tong Blackman, Eric Stewart, Desiree Ellis, Jasmina Butler, Robert Janigro, Damir |
| description | The acknowledgement of risks for traumatic brain injury in American football players has prompted studies for sideline concussion diagnosis and testing for neurological deficits. While concussions are recognized etiological factors for a spectrum of neurological sequelae, the consequences of sub-concussive events are unclear. We tested the hypothesis that blood-brain barrier disruption (BBBD) and the accompanying surge of the astrocytic protein S100B in blood may cause an immune response associated with production of auto-antibodies. We also wished to determine whether these events result in disrupted white matter on diffusion tensor imaging (DT) scans. Players from three college football teams were enrolled (total of 67 volunteers). None of the players experienced a concussion. Blood samples were collected before and after games (n = 57); the number of head hits in all players was monitored by movie review and post-game interviews. S100B serum levels and auto-antibodies against S100B were measured and correlated by direct and reverse immunoassays (n = 15 players; 5 games). A subset of players underwent DTI scans pre- and post-season and after a 6-month interval (n = 10). Cognitive and functional assessments were also performed. After a game, transient BBB damage measured by serum S100B was detected only in players experiencing the greatest number of sub-concussive head hits. Elevated levels of auto-antibodies against S100B were elevated only after repeated sub-concussive events characterized by BBBD. Serum levels of S100B auto-antibodies also predicted persistence of MRI-DTI abnormalities which in turn correlated with cognitive changes. Even in the absence of concussion, football players may experience repeated BBBD and serum surges of the potential auto-antigen S100B. The correlation of serum S100B, auto-antibodies and DTI changes support a link between repeated BBBD and future risk for cognitive changes. |
| doi_str_mv | 10.1371/journal.pone.0056805 |
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While concussions are recognized etiological factors for a spectrum of neurological sequelae, the consequences of sub-concussive events are unclear. We tested the hypothesis that blood-brain barrier disruption (BBBD) and the accompanying surge of the astrocytic protein S100B in blood may cause an immune response associated with production of auto-antibodies. We also wished to determine whether these events result in disrupted white matter on diffusion tensor imaging (DT) scans. Players from three college football teams were enrolled (total of 67 volunteers). None of the players experienced a concussion. Blood samples were collected before and after games (n = 57); the number of head hits in all players was monitored by movie review and post-game interviews. S100B serum levels and auto-antibodies against S100B were measured and correlated by direct and reverse immunoassays (n = 15 players; 5 games). A subset of players underwent DTI scans pre- and post-season and after a 6-month interval (n = 10). Cognitive and functional assessments were also performed. After a game, transient BBB damage measured by serum S100B was detected only in players experiencing the greatest number of sub-concussive head hits. Elevated levels of auto-antibodies against S100B were elevated only after repeated sub-concussive events characterized by BBBD. Serum levels of S100B auto-antibodies also predicted persistence of MRI-DTI abnormalities which in turn correlated with cognitive changes. Even in the absence of concussion, football players may experience repeated BBBD and serum surges of the potential auto-antigen S100B. The correlation of serum S100B, auto-antibodies and DTI changes support a link between repeated BBBD and future risk for cognitive changes.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0056805</identifier><identifier>PMID: 23483891</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Abnormalities ; Adolescent ; Alzheimer's disease ; Antibodies ; Athletes ; Autoantibodies ; Autoantibodies - blood ; Blood-brain barrier ; Blood-Brain Barrier - pathology ; Blotting, Western ; Brain ; Brain research ; Chromatography, High Pressure Liquid ; Cognitive ability ; Concussion ; Correlation analysis ; Damage assessment ; Damage detection ; Diffusion Tensor Imaging ; Etiology ; Football ; Football (College) ; Football teams ; Games ; Head ; Head injuries ; Health risks ; Humans ; Hypotheses ; Immune response ; Immune system ; Immunoassays ; Immunoglobulin G - blood ; Immunohistochemistry ; Magnetic resonance imaging ; Male ; Mass Spectrometry ; Medicine ; Nerve Growth Factors - blood ; Nerve Growth Factors - immunology ; Neuroimaging ; Neurological complications ; Neurological diseases ; Neurological disorders ; Neurosurgery ; Permeability ; Players ; Proteins ; S100 Calcium Binding Protein beta Subunit ; S100 Proteins - blood ; S100 Proteins - immunology ; S100b protein ; Serum levels ; Sports injuries ; Substantia alba ; Surges ; Tomography ; Trauma ; Traumatic brain injury ; Young Adult</subject><ispartof>PloS one, 2013-03, Vol.8 (3), p.e56805-e56805</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013 Marchi et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2013 Marchi et al 2013 Marchi et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-f4d12ac13595faa062f4d9c60983150cd7726e61efc0e1715acaab891cd225e43</citedby><cites>FETCH-LOGICAL-c692t-f4d12ac13595faa062f4d9c60983150cd7726e61efc0e1715acaab891cd225e43</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3590196/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3590196/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,724,777,781,861,882,2096,2915,23847,27905,27906,53772,53774,79349,79350</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23483891$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Dhandapani, Krishnan M.</contributor><creatorcontrib>Marchi, Nicola</creatorcontrib><creatorcontrib>Bazarian, Jeffrey J</creatorcontrib><creatorcontrib>Puvenna, Vikram</creatorcontrib><creatorcontrib>Janigro, Mattia</creatorcontrib><creatorcontrib>Ghosh, Chaitali</creatorcontrib><creatorcontrib>Zhong, Jianhui</creatorcontrib><creatorcontrib>Zhu, Tong</creatorcontrib><creatorcontrib>Blackman, Eric</creatorcontrib><creatorcontrib>Stewart, Desiree</creatorcontrib><creatorcontrib>Ellis, Jasmina</creatorcontrib><creatorcontrib>Butler, Robert</creatorcontrib><creatorcontrib>Janigro, Damir</creatorcontrib><title>Consequences of repeated blood-brain barrier disruption in football players</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>The acknowledgement of risks for traumatic brain injury in American football players has prompted studies for sideline concussion diagnosis and testing for neurological deficits. While concussions are recognized etiological factors for a spectrum of neurological sequelae, the consequences of sub-concussive events are unclear. We tested the hypothesis that blood-brain barrier disruption (BBBD) and the accompanying surge of the astrocytic protein S100B in blood may cause an immune response associated with production of auto-antibodies. We also wished to determine whether these events result in disrupted white matter on diffusion tensor imaging (DT) scans. Players from three college football teams were enrolled (total of 67 volunteers). None of the players experienced a concussion. Blood samples were collected before and after games (n = 57); the number of head hits in all players was monitored by movie review and post-game interviews. S100B serum levels and auto-antibodies against S100B were measured and correlated by direct and reverse immunoassays (n = 15 players; 5 games). A subset of players underwent DTI scans pre- and post-season and after a 6-month interval (n = 10). Cognitive and functional assessments were also performed. After a game, transient BBB damage measured by serum S100B was detected only in players experiencing the greatest number of sub-concussive head hits. Elevated levels of auto-antibodies against S100B were elevated only after repeated sub-concussive events characterized by BBBD. Serum levels of S100B auto-antibodies also predicted persistence of MRI-DTI abnormalities which in turn correlated with cognitive changes. Even in the absence of concussion, football players may experience repeated BBBD and serum surges of the potential auto-antigen S100B. The correlation of serum S100B, auto-antibodies and DTI changes support a link between repeated BBBD and future risk for cognitive changes.</description><subject>Abnormalities</subject><subject>Adolescent</subject><subject>Alzheimer's disease</subject><subject>Antibodies</subject><subject>Athletes</subject><subject>Autoantibodies</subject><subject>Autoantibodies - blood</subject><subject>Blood-brain barrier</subject><subject>Blood-Brain Barrier - pathology</subject><subject>Blotting, Western</subject><subject>Brain</subject><subject>Brain research</subject><subject>Chromatography, High Pressure Liquid</subject><subject>Cognitive ability</subject><subject>Concussion</subject><subject>Correlation analysis</subject><subject>Damage assessment</subject><subject>Damage detection</subject><subject>Diffusion Tensor Imaging</subject><subject>Etiology</subject><subject>Football</subject><subject>Football (College)</subject><subject>Football teams</subject><subject>Games</subject><subject>Head</subject><subject>Head injuries</subject><subject>Health risks</subject><subject>Humans</subject><subject>Hypotheses</subject><subject>Immune response</subject><subject>Immune system</subject><subject>Immunoassays</subject><subject>Immunoglobulin G - blood</subject><subject>Immunohistochemistry</subject><subject>Magnetic resonance imaging</subject><subject>Male</subject><subject>Mass Spectrometry</subject><subject>Medicine</subject><subject>Nerve Growth Factors - blood</subject><subject>Nerve Growth Factors - immunology</subject><subject>Neuroimaging</subject><subject>Neurological complications</subject><subject>Neurological diseases</subject><subject>Neurological disorders</subject><subject>Neurosurgery</subject><subject>Permeability</subject><subject>Players</subject><subject>Proteins</subject><subject>S100 Calcium Binding Protein beta Subunit</subject><subject>S100 Proteins - blood</subject><subject>S100 Proteins - immunology</subject><subject>S100b protein</subject><subject>Serum levels</subject><subject>Sports injuries</subject><subject>Substantia alba</subject><subject>Surges</subject><subject>Tomography</subject><subject>Trauma</subject><subject>Traumatic brain injury</subject><subject>Young Adult</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNkl2L1DAUhoso7rr6D0QLgujFjEmTps2NsAx-DC4s-HUbTpPTmSyZppu04v57M053mcpeSC9STp7zJufNm2XPKVlSVtF3V34MHbhl7ztcElKKmpQPslMqWbEQBWEPj_5PsicxXiWI1UI8zk4KxmtWS3qafVn5LuL1iJ3GmPs2D9gjDGjyxnlvFk0A2-UNhGAx5MbGMPaD9V2eqq33QwPO5b2DGwzxafaoBRfx2bSeZT8-fvi--ry4uPy0Xp1fLLSQxbBouaEFaMpKWbYARBSpIrUgsma0JNpUVSFQUGw1QVrREjRAk26rTVGUyNlZ9vKg2zsf1eRDVJQxUteUM5mI9YEwHq5UH-wOwo3yYNXfgg8bBWGw2qHCigCTtC6ZYdxwAazitERiknc1a5qk9X46bWx2aDR2QwA3E53vdHarNv6XSvMRKkUSeDMJBJ-MjoPa2ajROejQj_t704qTNBpJ6Kt_0Punm6gNpAFs1_p0rt6LqnNe1ZwSKctELe-h0mdwZ3UKTWtTfdbwdtaQmAF_DxsYY1Trb1__n738OWdfH7FbBDdso3fjPkZxDvIDqIOPMWB7ZzIlap_5WzfUPvNqynxqe3H8QHdNtyFnfwBtX_tH</recordid><startdate>20130306</startdate><enddate>20130306</enddate><creator>Marchi, Nicola</creator><creator>Bazarian, Jeffrey J</creator><creator>Puvenna, Vikram</creator><creator>Janigro, Mattia</creator><creator>Ghosh, Chaitali</creator><creator>Zhong, Jianhui</creator><creator>Zhu, Tong</creator><creator>Blackman, Eric</creator><creator>Stewart, Desiree</creator><creator>Ellis, Jasmina</creator><creator>Butler, Robert</creator><creator>Janigro, Damir</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20130306</creationdate><title>Consequences of repeated blood-brain barrier disruption in football players</title><author>Marchi, Nicola ; Bazarian, Jeffrey J ; Puvenna, Vikram ; Janigro, Mattia ; Ghosh, Chaitali ; Zhong, Jianhui ; Zhu, Tong ; Blackman, Eric ; Stewart, Desiree ; Ellis, Jasmina ; Butler, Robert ; Janigro, Damir</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-f4d12ac13595faa062f4d9c60983150cd7726e61efc0e1715acaab891cd225e43</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Abnormalities</topic><topic>Adolescent</topic><topic>Alzheimer's disease</topic><topic>Antibodies</topic><topic>Athletes</topic><topic>Autoantibodies</topic><topic>Autoantibodies - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Marchi, Nicola</au><au>Bazarian, Jeffrey J</au><au>Puvenna, Vikram</au><au>Janigro, Mattia</au><au>Ghosh, Chaitali</au><au>Zhong, Jianhui</au><au>Zhu, Tong</au><au>Blackman, Eric</au><au>Stewart, Desiree</au><au>Ellis, Jasmina</au><au>Butler, Robert</au><au>Janigro, Damir</au><au>Dhandapani, Krishnan M.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Consequences of repeated blood-brain barrier disruption in football players</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2013-03-06</date><risdate>2013</risdate><volume>8</volume><issue>3</issue><spage>e56805</spage><epage>e56805</epage><pages>e56805-e56805</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>The acknowledgement of risks for traumatic brain injury in American football players has prompted studies for sideline concussion diagnosis and testing for neurological deficits. While concussions are recognized etiological factors for a spectrum of neurological sequelae, the consequences of sub-concussive events are unclear. We tested the hypothesis that blood-brain barrier disruption (BBBD) and the accompanying surge of the astrocytic protein S100B in blood may cause an immune response associated with production of auto-antibodies. We also wished to determine whether these events result in disrupted white matter on diffusion tensor imaging (DT) scans. Players from three college football teams were enrolled (total of 67 volunteers). None of the players experienced a concussion. Blood samples were collected before and after games (n = 57); the number of head hits in all players was monitored by movie review and post-game interviews. S100B serum levels and auto-antibodies against S100B were measured and correlated by direct and reverse immunoassays (n = 15 players; 5 games). A subset of players underwent DTI scans pre- and post-season and after a 6-month interval (n = 10). Cognitive and functional assessments were also performed. After a game, transient BBB damage measured by serum S100B was detected only in players experiencing the greatest number of sub-concussive head hits. Elevated levels of auto-antibodies against S100B were elevated only after repeated sub-concussive events characterized by BBBD. Serum levels of S100B auto-antibodies also predicted persistence of MRI-DTI abnormalities which in turn correlated with cognitive changes. Even in the absence of concussion, football players may experience repeated BBBD and serum surges of the potential auto-antigen S100B. The correlation of serum S100B, auto-antibodies and DTI changes support a link between repeated BBBD and future risk for cognitive changes.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>23483891</pmid><doi>10.1371/journal.pone.0056805</doi><tpages>e56805</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2013-03, Vol.8 (3), p.e56805-e56805 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1330881439 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS); EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Abnormalities Adolescent Alzheimer's disease Antibodies Athletes Autoantibodies Autoantibodies - blood Blood-brain barrier Blood-Brain Barrier - pathology Blotting, Western Brain Brain research Chromatography, High Pressure Liquid Cognitive ability Concussion Correlation analysis Damage assessment Damage detection Diffusion Tensor Imaging Etiology Football Football (College) Football teams Games Head Head injuries Health risks Humans Hypotheses Immune response Immune system Immunoassays Immunoglobulin G - blood Immunohistochemistry Magnetic resonance imaging Male Mass Spectrometry Medicine Nerve Growth Factors - blood Nerve Growth Factors - immunology Neuroimaging Neurological complications Neurological diseases Neurological disorders Neurosurgery Permeability Players Proteins S100 Calcium Binding Protein beta Subunit S100 Proteins - blood S100 Proteins - immunology S100b protein Serum levels Sports injuries Substantia alba Surges Tomography Trauma Traumatic brain injury Young Adult |
| title | Consequences of repeated blood-brain barrier disruption in football players |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-20T00%3A24%3A41IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Consequences%20of%20repeated%20blood-brain%20barrier%20disruption%20in%20football%20players&rft.jtitle=PloS%20one&rft.au=Marchi,%20Nicola&rft.date=2013-03-06&rft.volume=8&rft.issue=3&rft.spage=e56805&rft.epage=e56805&rft.pages=e56805-e56805&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0056805&rft_dat=%3Cgale_plos_%3EA478410995%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1330881439&rft_id=info:pmid/23483891&rft_galeid=A478410995&rft_doaj_id=oai_doaj_org_article_e70a391853d34d46a37415e0d93283bb&rfr_iscdi=true |