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The Microbiome-Gut-Brain axis regulates social cognition & craving in young binge drinkers

BACKGROUND: Binge drinking is the consumption of an excessive amount of alcohol in a short period of time. This pattern of consumption is highly prevalent during the crucial developmental period of adolescence. Recently, the severity of alcohol use disorders (AUDs) has been linked with microbiome al...

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Autores principales: Carbia, Carina, Bastiaanssen, Thomaz F.S., Iannone, Luigi Francesco, García-Cabrerizo, Rubén, Boscaini, Serena, Berding, Kirsten, Strain, Conall R., Clarke, Gerard, Stanton, Catherine, Dinan, Timothy G., Cryan, John F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Elsevier 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10025767/
https://www.ncbi.nlm.nih.gov/pubmed/36739238
http://dx.doi.org/10.1016/j.ebiom.2023.104442
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author Carbia, Carina
Bastiaanssen, Thomaz F.S.
Iannone, Luigi Francesco
García-Cabrerizo, Rubén
Boscaini, Serena
Berding, Kirsten
Strain, Conall R.
Clarke, Gerard
Stanton, Catherine
Dinan, Timothy G.
Cryan, John F.
author_facet Carbia, Carina
Bastiaanssen, Thomaz F.S.
Iannone, Luigi Francesco
García-Cabrerizo, Rubén
Boscaini, Serena
Berding, Kirsten
Strain, Conall R.
Clarke, Gerard
Stanton, Catherine
Dinan, Timothy G.
Cryan, John F.
author_sort Carbia, Carina
collection PubMed
description BACKGROUND: Binge drinking is the consumption of an excessive amount of alcohol in a short period of time. This pattern of consumption is highly prevalent during the crucial developmental period of adolescence. Recently, the severity of alcohol use disorders (AUDs) has been linked with microbiome alterations suggesting a role for the gut microbiome in its development. Furthermore, a strong link has emerged too between microbiome composition and socio-emotional functioning across different disorders including AUD. The aim of this study was to investigate the potential link (and its predictive value) between alcohol-related altered microbial profile, social cognition, impulsivity and craving. METHODS: Young people (N = 71) aged 18–25 reported their alcohol use and underwent a neuropsychological evaluation. Craving was measured at baseline and three months later. Diet was controlled for. Blood, saliva and hair samples were taken for inflammatory, kynurenine and cortisol analysis. Stool samples were provided for shotgun metagenomic sequencing and short-chain fatty acids (SCFAs) were measured. FINDINGS: Binge drinking was associated with distinct microbiome alterations and emotional recognition difficulties. Associations were found for several microbiome species with emotional processing and impulsivity. Craving showed a strong link with alterations in microbiome composition and neuroactive potential over time. INTERPRETATION: In conclusion, this research demonstrates alterations in the gut microbiome of young binge drinkers (BDs) and identifies early biomarkers of craving. Associations between emotional processing and microbiome composition further support the growing literature on the gut microbiome as a regulator of social cognition. These findings are of relevance for new gut-derived interventions directed at improving early alcohol-related alterations during the vulnerability period of adolescence. FUNDING: C.C. and R.G-C. received funding from the European Union's Horizon 2020 research and innovation programme under the Marie Sklodowska-Curie grant agreement No. 754535. APC Microbiome Ireland is a research centre funded by 10.13039/501100001602Science Foundation Ireland (SFI), through the Irish Government’s National Development Plan [grant no. SFI/12/RC/2273_P2]. J.F.C has research support from Cremo, 10.13039/100007082Pharmavite, 10.13039/100004352DuPont and Nutricia. He has spoken at meetings sponsored by food and pharmaceutical companies. G.C. has received honoraria from Janssen, Probi, and Apsen as an invited speaker; is in receipt of research funding from 10.13039/100007082Pharmavite, 10.13039/501100003144Fonterra, Nestle and Reckitt; and is a paid consultant for 10.13039/501100012030Yakult, Zentiva and Heel pharmaceuticals. All the authors declare no competing interests.
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spelling pubmed-100257672023-03-21 The Microbiome-Gut-Brain axis regulates social cognition & craving in young binge drinkers Carbia, Carina Bastiaanssen, Thomaz F.S. Iannone, Luigi Francesco García-Cabrerizo, Rubén Boscaini, Serena Berding, Kirsten Strain, Conall R. Clarke, Gerard Stanton, Catherine Dinan, Timothy G. Cryan, John F. eBioMedicine Articles BACKGROUND: Binge drinking is the consumption of an excessive amount of alcohol in a short period of time. This pattern of consumption is highly prevalent during the crucial developmental period of adolescence. Recently, the severity of alcohol use disorders (AUDs) has been linked with microbiome alterations suggesting a role for the gut microbiome in its development. Furthermore, a strong link has emerged too between microbiome composition and socio-emotional functioning across different disorders including AUD. The aim of this study was to investigate the potential link (and its predictive value) between alcohol-related altered microbial profile, social cognition, impulsivity and craving. METHODS: Young people (N = 71) aged 18–25 reported their alcohol use and underwent a neuropsychological evaluation. Craving was measured at baseline and three months later. Diet was controlled for. Blood, saliva and hair samples were taken for inflammatory, kynurenine and cortisol analysis. Stool samples were provided for shotgun metagenomic sequencing and short-chain fatty acids (SCFAs) were measured. FINDINGS: Binge drinking was associated with distinct microbiome alterations and emotional recognition difficulties. Associations were found for several microbiome species with emotional processing and impulsivity. Craving showed a strong link with alterations in microbiome composition and neuroactive potential over time. INTERPRETATION: In conclusion, this research demonstrates alterations in the gut microbiome of young binge drinkers (BDs) and identifies early biomarkers of craving. Associations between emotional processing and microbiome composition further support the growing literature on the gut microbiome as a regulator of social cognition. These findings are of relevance for new gut-derived interventions directed at improving early alcohol-related alterations during the vulnerability period of adolescence. FUNDING: C.C. and R.G-C. received funding from the European Union's Horizon 2020 research and innovation programme under the Marie Sklodowska-Curie grant agreement No. 754535. APC Microbiome Ireland is a research centre funded by 10.13039/501100001602Science Foundation Ireland (SFI), through the Irish Government’s National Development Plan [grant no. SFI/12/RC/2273_P2]. J.F.C has research support from Cremo, 10.13039/100007082Pharmavite, 10.13039/100004352DuPont and Nutricia. He has spoken at meetings sponsored by food and pharmaceutical companies. G.C. has received honoraria from Janssen, Probi, and Apsen as an invited speaker; is in receipt of research funding from 10.13039/100007082Pharmavite, 10.13039/501100003144Fonterra, Nestle and Reckitt; and is a paid consultant for 10.13039/501100012030Yakult, Zentiva and Heel pharmaceuticals. All the authors declare no competing interests. Elsevier 2023-02-02 /pmc/articles/PMC10025767/ /pubmed/36739238 http://dx.doi.org/10.1016/j.ebiom.2023.104442 Text en © 2023 The Author(s) https://creativecommons.org/licenses/by/4.0/This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Articles
Carbia, Carina
Bastiaanssen, Thomaz F.S.
Iannone, Luigi Francesco
García-Cabrerizo, Rubén
Boscaini, Serena
Berding, Kirsten
Strain, Conall R.
Clarke, Gerard
Stanton, Catherine
Dinan, Timothy G.
Cryan, John F.
The Microbiome-Gut-Brain axis regulates social cognition & craving in young binge drinkers
title The Microbiome-Gut-Brain axis regulates social cognition & craving in young binge drinkers
title_full The Microbiome-Gut-Brain axis regulates social cognition & craving in young binge drinkers
title_fullStr The Microbiome-Gut-Brain axis regulates social cognition & craving in young binge drinkers
title_full_unstemmed The Microbiome-Gut-Brain axis regulates social cognition & craving in young binge drinkers
title_short The Microbiome-Gut-Brain axis regulates social cognition & craving in young binge drinkers
title_sort microbiome-gut-brain axis regulates social cognition & craving in young binge drinkers
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10025767/
https://www.ncbi.nlm.nih.gov/pubmed/36739238
http://dx.doi.org/10.1016/j.ebiom.2023.104442
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