Association of concussion history with psychiatric symptoms, limbic system structure, and kynurenine pathway metabolites in healthy, collegiate-aged athletes
•Healthy athletes with more prior concussions report worse psychiatric symptoms.•More concussions are associated with limbic system structural abnormalities.•Worse prior concussion-related psychiatric outcomes observed in female athletes.•Kynurenine metabolites may underlie concussion-related limbic...
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| Veröffentlicht in: | Brain, behavior, and immunity behavior, and immunity, 2025-01, Vol.123, p.619-630 |
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| creator | Meier, Timothy B. Savitz, Jonathan España, Lezlie Y. Goeckner, Bryna D. Kent Teague, T. van der Horn, Harm Jan Tugan Muftuler, L. Mayer, Andrew R. Brett, Benjamin L. |
| description | •Healthy athletes with more prior concussions report worse psychiatric symptoms.•More concussions are associated with limbic system structural abnormalities.•Worse prior concussion-related psychiatric outcomes observed in female athletes.•Kynurenine metabolites may underlie concussion-related limbic abnormalities.
Psychiatric outcomes are commonly observed in individuals with repeated concussions, though their underlying mechanism is unknown. One potential mechanism linking concussion with psychiatric symptoms is inflammation-induced activation of the kynurenine pathway, which is thought to play a role in the pathogenesis of mood disorders. Here, we investigated the association of prior concussion with multiple psychiatric-related outcomes in otherwise healthy male and female collegiate-aged athletes (N = 212) with varying histories of concussion recruited from the community. Specially, we tested the hypotheses that concussion history is associated with worse psychiatric symptoms, limbic system structural abnormalities (hippocampal volume, white matter microstructure assessed using neurite orientation dispersion and density imaging; NODDI), and elevations in kynurenine pathway (KP) metabolites (e.g., Quinolinic acid; QuinA). Given known sex-effects on concussion risk and recovery, psychiatric outcomes, and the kynurenine pathway, the moderating effect of sex was considered for all analyses. More concussions were associated with greater depression, anxiety, and anhedonia symptoms in female athletes (ps ≤ 0.005) and greater depression symptoms in male athletes (p = 0.011). More concussions were associated with smaller bilateral hippocampal tail (ps |
| doi_str_mv | 10.1016/j.bbi.2024.10.015 |
| format | Article |
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Psychiatric outcomes are commonly observed in individuals with repeated concussions, though their underlying mechanism is unknown. One potential mechanism linking concussion with psychiatric symptoms is inflammation-induced activation of the kynurenine pathway, which is thought to play a role in the pathogenesis of mood disorders. Here, we investigated the association of prior concussion with multiple psychiatric-related outcomes in otherwise healthy male and female collegiate-aged athletes (N = 212) with varying histories of concussion recruited from the community. Specially, we tested the hypotheses that concussion history is associated with worse psychiatric symptoms, limbic system structural abnormalities (hippocampal volume, white matter microstructure assessed using neurite orientation dispersion and density imaging; NODDI), and elevations in kynurenine pathway (KP) metabolites (e.g., Quinolinic acid; QuinA). Given known sex-effects on concussion risk and recovery, psychiatric outcomes, and the kynurenine pathway, the moderating effect of sex was considered for all analyses. More concussions were associated with greater depression, anxiety, and anhedonia symptoms in female athletes (ps ≤ 0.005) and greater depression symptoms in male athletes (p = 0.011). More concussions were associated with smaller bilateral hippocampal tail (ps < 0.010) and left hippocampal body (p < 0.001) volumes across male and female athletes. Prior concussion was also associated with elevations in the orientation dispersion index (ODI) and lower intracellular volume fraction in several white matter tracts including the in uncinate fasciculus, cingulum-gyrus, and forceps major and minor, with evidence of female-specific associations in select regions. Regarding serum KP metabolites, more concussions were associated with elevated QuinA in females and lower tryptophan in males (ps ≤ 0.010). Finally, serum levels of QuinA were associated with elevated ODI (male and female athletes) and worse anxiety symptoms (females only), while higher ODI in female athletes and smaller hippocampal volumes in male athletes were associated with more severe anxiety and depression symptoms (ps ≤ 0.05). These data suggest that cumulative concussion is associated with psychiatric symptoms and limbic system structure in healthy athletes, with increased susceptibility to these effects in female athletes. Moreover, the associations of outcomes with serum KP metabolites highlight the KP as one potential molecular pathway underlying these observations.</description><identifier>ISSN: 0889-1591</identifier><identifier>ISSN: 1090-2139</identifier><identifier>EISSN: 1090-2139</identifier><identifier>DOI: 10.1016/j.bbi.2024.10.015</identifier><identifier>PMID: 39414174</identifier><language>eng</language><publisher>Netherlands: Elsevier Inc</publisher><subject>Adolescent ; Adult ; Anhedonia - physiology ; Anxiety - metabolism ; Athletes ; Athletic Injuries - complications ; Athletic Injuries - metabolism ; Brain Concussion - complications ; Brain Concussion - metabolism ; Depression ; Depression - metabolism ; diffusion MRI ; Female ; Hippocampus ; Hippocampus - metabolism ; Humans ; Kynurenine - metabolism ; Limbic System - metabolism ; Magnetic Resonance Imaging ; Male ; Mild traumatic brain injury ; Quinolinic acid ; Quinolinic Acid - blood ; Quinolinic Acid - metabolism ; Sport ; White Matter - metabolism ; White Matter - pathology ; Young Adult</subject><ispartof>Brain, behavior, and immunity, 2025-01, Vol.123, p.619-630</ispartof><rights>2024 Elsevier Inc.</rights><rights>Copyright © 2024 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c235t-ca0a008ceb2538adfe4b831b1bb29a67efabc9490a98f8de9e3cf8d77a7033c93</cites><orcidid>0000-0002-4495-2754</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.bbi.2024.10.015$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39414174$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Meier, Timothy B.</creatorcontrib><creatorcontrib>Savitz, Jonathan</creatorcontrib><creatorcontrib>España, Lezlie Y.</creatorcontrib><creatorcontrib>Goeckner, Bryna D.</creatorcontrib><creatorcontrib>Kent Teague, T.</creatorcontrib><creatorcontrib>van der Horn, Harm Jan</creatorcontrib><creatorcontrib>Tugan Muftuler, L.</creatorcontrib><creatorcontrib>Mayer, Andrew R.</creatorcontrib><creatorcontrib>Brett, Benjamin L.</creatorcontrib><title>Association of concussion history with psychiatric symptoms, limbic system structure, and kynurenine pathway metabolites in healthy, collegiate-aged athletes</title><title>Brain, behavior, and immunity</title><addtitle>Brain Behav Immun</addtitle><description>•Healthy athletes with more prior concussions report worse psychiatric symptoms.•More concussions are associated with limbic system structural abnormalities.•Worse prior concussion-related psychiatric outcomes observed in female athletes.•Kynurenine metabolites may underlie concussion-related limbic abnormalities.
Psychiatric outcomes are commonly observed in individuals with repeated concussions, though their underlying mechanism is unknown. One potential mechanism linking concussion with psychiatric symptoms is inflammation-induced activation of the kynurenine pathway, which is thought to play a role in the pathogenesis of mood disorders. Here, we investigated the association of prior concussion with multiple psychiatric-related outcomes in otherwise healthy male and female collegiate-aged athletes (N = 212) with varying histories of concussion recruited from the community. Specially, we tested the hypotheses that concussion history is associated with worse psychiatric symptoms, limbic system structural abnormalities (hippocampal volume, white matter microstructure assessed using neurite orientation dispersion and density imaging; NODDI), and elevations in kynurenine pathway (KP) metabolites (e.g., Quinolinic acid; QuinA). Given known sex-effects on concussion risk and recovery, psychiatric outcomes, and the kynurenine pathway, the moderating effect of sex was considered for all analyses. More concussions were associated with greater depression, anxiety, and anhedonia symptoms in female athletes (ps ≤ 0.005) and greater depression symptoms in male athletes (p = 0.011). More concussions were associated with smaller bilateral hippocampal tail (ps < 0.010) and left hippocampal body (p < 0.001) volumes across male and female athletes. Prior concussion was also associated with elevations in the orientation dispersion index (ODI) and lower intracellular volume fraction in several white matter tracts including the in uncinate fasciculus, cingulum-gyrus, and forceps major and minor, with evidence of female-specific associations in select regions. Regarding serum KP metabolites, more concussions were associated with elevated QuinA in females and lower tryptophan in males (ps ≤ 0.010). Finally, serum levels of QuinA were associated with elevated ODI (male and female athletes) and worse anxiety symptoms (females only), while higher ODI in female athletes and smaller hippocampal volumes in male athletes were associated with more severe anxiety and depression symptoms (ps ≤ 0.05). These data suggest that cumulative concussion is associated with psychiatric symptoms and limbic system structure in healthy athletes, with increased susceptibility to these effects in female athletes. Moreover, the associations of outcomes with serum KP metabolites highlight the KP as one potential molecular pathway underlying these observations.</description><subject>Adolescent</subject><subject>Adult</subject><subject>Anhedonia - physiology</subject><subject>Anxiety - metabolism</subject><subject>Athletes</subject><subject>Athletic Injuries - complications</subject><subject>Athletic Injuries - metabolism</subject><subject>Brain Concussion - complications</subject><subject>Brain Concussion - metabolism</subject><subject>Depression</subject><subject>Depression - metabolism</subject><subject>diffusion MRI</subject><subject>Female</subject><subject>Hippocampus</subject><subject>Hippocampus - metabolism</subject><subject>Humans</subject><subject>Kynurenine - metabolism</subject><subject>Limbic System - metabolism</subject><subject>Magnetic Resonance Imaging</subject><subject>Male</subject><subject>Mild traumatic brain injury</subject><subject>Quinolinic acid</subject><subject>Quinolinic Acid - blood</subject><subject>Quinolinic Acid - metabolism</subject><subject>Sport</subject><subject>White Matter - metabolism</subject><subject>White Matter - pathology</subject><subject>Young Adult</subject><issn>0889-1591</issn><issn>1090-2139</issn><issn>1090-2139</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2025</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kcFu1DAQhi1ERZfCA3BBPnLYbO042cTiVFUUkCr1AmfLdiaNFycOHqdVHoZ3rbdbOHIaz-ibf2R9hHzgbMcZ318edsa4XcnKKvc7xutXZMOZZEXJhXxNNqxtZcFryc_JW8QDY6wWvH1DzoWseMWbakP-XCEG63RyYaKhpzZMdkE8doPDFOJKH10a6IyrHTIWnaW4jnMKI26pd6N5HmCCkWKKi01LhC3VU0d_rVN-T24COus0POqVjpC0Cd4lQOryBdA-Des2X_Ue7nM8FPoeOppxDxl6R8567RHev9QL8vPmy4_rb8Xt3dfv11e3hS1FnQqrmWastWDKWrS666EyreCGG1NKvW-g18bKSjIt277tQIKwuTaNbpgQVooL8umUO8fwewFManRowXs9QVhQCc6bPZdV3WSUn1AbA2KEXs3RjTquijN1tKIOKltRRyvHUbaSdz6-xC9mhO7fxl8NGfh8AiB_8sFBVGgdTBY6F8Em1QX3n_gnHDii4g</recordid><startdate>202501</startdate><enddate>202501</enddate><creator>Meier, Timothy B.</creator><creator>Savitz, Jonathan</creator><creator>España, Lezlie Y.</creator><creator>Goeckner, Bryna D.</creator><creator>Kent Teague, T.</creator><creator>van der Horn, Harm Jan</creator><creator>Tugan Muftuler, L.</creator><creator>Mayer, Andrew R.</creator><creator>Brett, Benjamin L.</creator><general>Elsevier 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>7X8</scope><orcidid>https://orcid.org/0000-0002-4495-2754</orcidid></search><sort><creationdate>202501</creationdate><title>Association of concussion history with psychiatric symptoms, limbic system structure, and kynurenine pathway metabolites in healthy, collegiate-aged athletes</title><author>Meier, Timothy B. ; Savitz, Jonathan ; España, Lezlie Y. ; Goeckner, Bryna D. ; Kent Teague, T. ; van der Horn, Harm Jan ; Tugan Muftuler, L. ; Mayer, Andrew R. ; Brett, Benjamin L.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c235t-ca0a008ceb2538adfe4b831b1bb29a67efabc9490a98f8de9e3cf8d77a7033c93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2025</creationdate><topic>Adolescent</topic><topic>Adult</topic><topic>Anhedonia - physiology</topic><topic>Anxiety - metabolism</topic><topic>Athletes</topic><topic>Athletic Injuries - complications</topic><topic>Athletic Injuries - metabolism</topic><topic>Brain Concussion - complications</topic><topic>Brain Concussion - metabolism</topic><topic>Depression</topic><topic>Depression - metabolism</topic><topic>diffusion MRI</topic><topic>Female</topic><topic>Hippocampus</topic><topic>Hippocampus - metabolism</topic><topic>Humans</topic><topic>Kynurenine - metabolism</topic><topic>Limbic System - metabolism</topic><topic>Magnetic Resonance Imaging</topic><topic>Male</topic><topic>Mild traumatic brain injury</topic><topic>Quinolinic acid</topic><topic>Quinolinic Acid - blood</topic><topic>Quinolinic Acid - metabolism</topic><topic>Sport</topic><topic>White Matter - metabolism</topic><topic>White Matter - pathology</topic><topic>Young Adult</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Meier, Timothy B.</creatorcontrib><creatorcontrib>Savitz, Jonathan</creatorcontrib><creatorcontrib>España, Lezlie Y.</creatorcontrib><creatorcontrib>Goeckner, Bryna D.</creatorcontrib><creatorcontrib>Kent Teague, T.</creatorcontrib><creatorcontrib>van der Horn, Harm Jan</creatorcontrib><creatorcontrib>Tugan Muftuler, L.</creatorcontrib><creatorcontrib>Mayer, Andrew R.</creatorcontrib><creatorcontrib>Brett, Benjamin L.</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>Brain, behavior, and immunity</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Meier, Timothy B.</au><au>Savitz, Jonathan</au><au>España, Lezlie Y.</au><au>Goeckner, Bryna D.</au><au>Kent Teague, T.</au><au>van der Horn, Harm Jan</au><au>Tugan Muftuler, L.</au><au>Mayer, Andrew R.</au><au>Brett, Benjamin L.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Association of concussion history with psychiatric symptoms, limbic system structure, and kynurenine pathway metabolites in healthy, collegiate-aged athletes</atitle><jtitle>Brain, behavior, and immunity</jtitle><addtitle>Brain Behav Immun</addtitle><date>2025-01</date><risdate>2025</risdate><volume>123</volume><spage>619</spage><epage>630</epage><pages>619-630</pages><issn>0889-1591</issn><issn>1090-2139</issn><eissn>1090-2139</eissn><abstract>•Healthy athletes with more prior concussions report worse psychiatric symptoms.•More concussions are associated with limbic system structural abnormalities.•Worse prior concussion-related psychiatric outcomes observed in female athletes.•Kynurenine metabolites may underlie concussion-related limbic abnormalities.
Psychiatric outcomes are commonly observed in individuals with repeated concussions, though their underlying mechanism is unknown. One potential mechanism linking concussion with psychiatric symptoms is inflammation-induced activation of the kynurenine pathway, which is thought to play a role in the pathogenesis of mood disorders. Here, we investigated the association of prior concussion with multiple psychiatric-related outcomes in otherwise healthy male and female collegiate-aged athletes (N = 212) with varying histories of concussion recruited from the community. Specially, we tested the hypotheses that concussion history is associated with worse psychiatric symptoms, limbic system structural abnormalities (hippocampal volume, white matter microstructure assessed using neurite orientation dispersion and density imaging; NODDI), and elevations in kynurenine pathway (KP) metabolites (e.g., Quinolinic acid; QuinA). Given known sex-effects on concussion risk and recovery, psychiatric outcomes, and the kynurenine pathway, the moderating effect of sex was considered for all analyses. More concussions were associated with greater depression, anxiety, and anhedonia symptoms in female athletes (ps ≤ 0.005) and greater depression symptoms in male athletes (p = 0.011). More concussions were associated with smaller bilateral hippocampal tail (ps < 0.010) and left hippocampal body (p < 0.001) volumes across male and female athletes. Prior concussion was also associated with elevations in the orientation dispersion index (ODI) and lower intracellular volume fraction in several white matter tracts including the in uncinate fasciculus, cingulum-gyrus, and forceps major and minor, with evidence of female-specific associations in select regions. Regarding serum KP metabolites, more concussions were associated with elevated QuinA in females and lower tryptophan in males (ps ≤ 0.010). Finally, serum levels of QuinA were associated with elevated ODI (male and female athletes) and worse anxiety symptoms (females only), while higher ODI in female athletes and smaller hippocampal volumes in male athletes were associated with more severe anxiety and depression symptoms (ps ≤ 0.05). These data suggest that cumulative concussion is associated with psychiatric symptoms and limbic system structure in healthy athletes, with increased susceptibility to these effects in female athletes. Moreover, the associations of outcomes with serum KP metabolites highlight the KP as one potential molecular pathway underlying these observations.</abstract><cop>Netherlands</cop><pub>Elsevier Inc</pub><pmid>39414174</pmid><doi>10.1016/j.bbi.2024.10.015</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0002-4495-2754</orcidid></addata></record> |
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| ispartof | Brain, behavior, and immunity, 2025-01, Vol.123, p.619-630 |
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| subjects | Adolescent Adult Anhedonia - physiology Anxiety - metabolism Athletes Athletic Injuries - complications Athletic Injuries - metabolism Brain Concussion - complications Brain Concussion - metabolism Depression Depression - metabolism diffusion MRI Female Hippocampus Hippocampus - metabolism Humans Kynurenine - metabolism Limbic System - metabolism Magnetic Resonance Imaging Male Mild traumatic brain injury Quinolinic acid Quinolinic Acid - blood Quinolinic Acid - metabolism Sport White Matter - metabolism White Matter - pathology Young Adult |
| title | Association of concussion history with psychiatric symptoms, limbic system structure, and kynurenine pathway metabolites in healthy, collegiate-aged athletes |
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