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IL-6, but not TNF-α, response to alcohol cues and acute consumption associated with neural cue reactivity, craving, and future drinking in binge drinkers

OBJECTIVE AND DESIGN: Preclinical studies suggest learned immune system responses to alcohol cues and consumption may contribute to alcohol's pharmacodynamic properties and/or Alcohol Use Disorder (AUD) pathogenesis. Mechanistically, these immune alterations may be associated with increased cra...

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Autores principales: Blaine, Sara K., Ridner, Clayton M., Campbell, Benjamin R., Crone, Lily, Claus, Eric D., Wilson, Juliet R., West, Summer N., McClanahan, Austin J., Siddiq, Anna S., Layman, Isaak M.P., Macatee, Richard, Ansell, Emily B., Robinson, Jennifer L., Beck, Darren T.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Elsevier 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10362517/
https://www.ncbi.nlm.nih.gov/pubmed/37484196
http://dx.doi.org/10.1016/j.bbih.2023.100645
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author Blaine, Sara K.
Ridner, Clayton M.
Campbell, Benjamin R.
Crone, Lily
Claus, Eric D.
Wilson, Juliet R.
West, Summer N.
McClanahan, Austin J.
Siddiq, Anna S.
Layman, Isaak M.P.
Macatee, Richard
Ansell, Emily B.
Robinson, Jennifer L.
Beck, Darren T.
author_facet Blaine, Sara K.
Ridner, Clayton M.
Campbell, Benjamin R.
Crone, Lily
Claus, Eric D.
Wilson, Juliet R.
West, Summer N.
McClanahan, Austin J.
Siddiq, Anna S.
Layman, Isaak M.P.
Macatee, Richard
Ansell, Emily B.
Robinson, Jennifer L.
Beck, Darren T.
author_sort Blaine, Sara K.
collection PubMed
description OBJECTIVE AND DESIGN: Preclinical studies suggest learned immune system responses to alcohol cues and consumption may contribute to alcohol's pharmacodynamic properties and/or Alcohol Use Disorder (AUD) pathogenesis. Mechanistically, these immune alterations may be associated with increased craving and alcohol consumption, both acutely and over time. We sought to characterize this relationship in a randomized, counter-balanced, crossover neuroimaging experiment which took place between June 2020–November 2021. METHODS: Thirty-three binge drinkers (BD) and 31 non-binge, social drinkers (SD), matched for demographic and psychological variables, were exposed to alcohol cues and water cues in two separate 7 T functional magnetic resonance imaging (fMRI) scans. Each scan was followed by the Alcohol Taste Test (ATT) of implicit motivation for acute alcohol. Craving measures and blood cytokine levels were collected repeatedly during and after scanning to examine the effects of alcohol cues and alcohol consumption on craving levels, Tumor necrosis factor alpha (TNF-α), and Interleukin 6 (IL-6) levels. A post-experiment one-month prospective measurement of participants’ “real world” drinking behavior was performed to approximate chronic effects. RESULTS: BD demonstrated significantly higher peak craving and IL-6 levels than SD in response to alcohol cues and relative to water cues. Ventromedial Prefrontal Cortex (VmPFC) signal change in the alcohol-water contrast positively related to alcohol cue condition craving and IL-6 levels, relative to water cue condition craving and IL-6 levels, in BD only. Additionally, peak craving and IL-6 levels were each independently related to ATT alcohol consumption and the number of drinks consumed in the next month for BD, again after controlling for craving and IL-6 repones to water cues. However, TNF-α release in the alcohol cue condition was not related to craving, neural activation, IL-6 levels, immediate and future alcohol consumption in either group after controlling for water cue condition responses. CONCLUSIONS: In sum, BD show greater craving and IL-6 release in the alcohol cue condition than SD, both of which were associated with prefrontal cue reactivity, immediate alcohol consumption, and future alcohol consumption over the subsequent 30 days. Alcohol associated immune changes and craving effects on drinking behavior may be independent of one another or may be indicative of a common pathway by which immune changes in BD could influence motivation to consume alcohol. TRIAL REGISTRATION: Clinical Trials NCT04412824.
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spelling pubmed-103625172023-07-23 IL-6, but not TNF-α, response to alcohol cues and acute consumption associated with neural cue reactivity, craving, and future drinking in binge drinkers Blaine, Sara K. Ridner, Clayton M. Campbell, Benjamin R. Crone, Lily Claus, Eric D. Wilson, Juliet R. West, Summer N. McClanahan, Austin J. Siddiq, Anna S. Layman, Isaak M.P. Macatee, Richard Ansell, Emily B. Robinson, Jennifer L. Beck, Darren T. Brain Behav Immun Health Full Length Article OBJECTIVE AND DESIGN: Preclinical studies suggest learned immune system responses to alcohol cues and consumption may contribute to alcohol's pharmacodynamic properties and/or Alcohol Use Disorder (AUD) pathogenesis. Mechanistically, these immune alterations may be associated with increased craving and alcohol consumption, both acutely and over time. We sought to characterize this relationship in a randomized, counter-balanced, crossover neuroimaging experiment which took place between June 2020–November 2021. METHODS: Thirty-three binge drinkers (BD) and 31 non-binge, social drinkers (SD), matched for demographic and psychological variables, were exposed to alcohol cues and water cues in two separate 7 T functional magnetic resonance imaging (fMRI) scans. Each scan was followed by the Alcohol Taste Test (ATT) of implicit motivation for acute alcohol. Craving measures and blood cytokine levels were collected repeatedly during and after scanning to examine the effects of alcohol cues and alcohol consumption on craving levels, Tumor necrosis factor alpha (TNF-α), and Interleukin 6 (IL-6) levels. A post-experiment one-month prospective measurement of participants’ “real world” drinking behavior was performed to approximate chronic effects. RESULTS: BD demonstrated significantly higher peak craving and IL-6 levels than SD in response to alcohol cues and relative to water cues. Ventromedial Prefrontal Cortex (VmPFC) signal change in the alcohol-water contrast positively related to alcohol cue condition craving and IL-6 levels, relative to water cue condition craving and IL-6 levels, in BD only. Additionally, peak craving and IL-6 levels were each independently related to ATT alcohol consumption and the number of drinks consumed in the next month for BD, again after controlling for craving and IL-6 repones to water cues. However, TNF-α release in the alcohol cue condition was not related to craving, neural activation, IL-6 levels, immediate and future alcohol consumption in either group after controlling for water cue condition responses. CONCLUSIONS: In sum, BD show greater craving and IL-6 release in the alcohol cue condition than SD, both of which were associated with prefrontal cue reactivity, immediate alcohol consumption, and future alcohol consumption over the subsequent 30 days. Alcohol associated immune changes and craving effects on drinking behavior may be independent of one another or may be indicative of a common pathway by which immune changes in BD could influence motivation to consume alcohol. TRIAL REGISTRATION: Clinical Trials NCT04412824. Elsevier 2023-06-11 /pmc/articles/PMC10362517/ /pubmed/37484196 http://dx.doi.org/10.1016/j.bbih.2023.100645 Text en © 2023 The Authors https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Full Length Article
Blaine, Sara K.
Ridner, Clayton M.
Campbell, Benjamin R.
Crone, Lily
Claus, Eric D.
Wilson, Juliet R.
West, Summer N.
McClanahan, Austin J.
Siddiq, Anna S.
Layman, Isaak M.P.
Macatee, Richard
Ansell, Emily B.
Robinson, Jennifer L.
Beck, Darren T.
IL-6, but not TNF-α, response to alcohol cues and acute consumption associated with neural cue reactivity, craving, and future drinking in binge drinkers
title IL-6, but not TNF-α, response to alcohol cues and acute consumption associated with neural cue reactivity, craving, and future drinking in binge drinkers
title_full IL-6, but not TNF-α, response to alcohol cues and acute consumption associated with neural cue reactivity, craving, and future drinking in binge drinkers
title_fullStr IL-6, but not TNF-α, response to alcohol cues and acute consumption associated with neural cue reactivity, craving, and future drinking in binge drinkers
title_full_unstemmed IL-6, but not TNF-α, response to alcohol cues and acute consumption associated with neural cue reactivity, craving, and future drinking in binge drinkers
title_short IL-6, but not TNF-α, response to alcohol cues and acute consumption associated with neural cue reactivity, craving, and future drinking in binge drinkers
title_sort il-6, but not tnf-α, response to alcohol cues and acute consumption associated with neural cue reactivity, craving, and future drinking in binge drinkers
topic Full Length Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10362517/
https://www.ncbi.nlm.nih.gov/pubmed/37484196
http://dx.doi.org/10.1016/j.bbih.2023.100645
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