Gut Microbiota-Induced Changes in β-Hydroxybutyrate Metabolism Are Linked to Altered Sociability and Depression in Alcohol Use Disorder

Leclercq, Sophie; Roy, Tiphaine Le; Furgiuele, Sonia; Coste, Valentin; Bindels, Laure B.; Leyrolle, Quentin; Neyrinck, Audrey M.; Quoilin, Caroline; Amadieu, Camille; Petit, Géraldine; Dricot, Laurence; Tagliatti, Vanessa; Cani, Patrice D.; Verbeke, Kristin; Colet, Jean‐Marie; Stärkel, Peter; Timary, Philippe de

doi:10.1016/j.celrep.2020.108238

Cited by 124 publications

(117 citation statements)

References 97 publications

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“…However, these associations do not persist when taking into account potential confounding factors like sociodemographic characteristics, BMI, energy intake and tobacco use. The observation of a relationship between lipid metabolism dysregulation and the importance of symptoms of AUD as well as changes in myelin synthesis has recently been highlighted by a translational study from our research group [62]. Together, these data stress the importance of lipid intake and metabolism in the development of AUD.…”

Section: Discussionmentioning

confidence: 86%

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Dietary fiber deficiency as a component of malnutrition associated with psychological alterations in alcohol use disorder

et al. 2021

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Background & aims: Chronic alcohol consumption can cause malnutrition that may contribute to alcoholinduced organ injury and psychological disorders. We evaluated the link between nutrient intake, especially dietary fibers (DF) and different parameters reflecting mental health and well being, namely anxiety, depression, alcohol craving, sociability, fatigue and intestinal comfort in alcohol use disorder (AUD) patients. Methods: Cross-sectional data from 50 AUD patients, hospitalized for a 3-week detoxification program were used. Three 24-h recalls allowed to calculate dietary habits and nutrient intakes, that was also assessed in healthy subjects (HS). Diet quality was measured using the NOVA score. Psychological factors and intestinal discomfort were evaluated using validated self-administered questionnaires. Results: Energy intake (excluding alcoholic beverage), total fat, monounsaturated and polyunsaturated fatty acids, protein and DF intakes were lower in AUD subjects compared to HS. Ninety percent of patients had a DF intake below the recommendation. AUD patients consumed more than twice as much ultra-processed food than HS. Fructan intake was negatively associated with anxiety (p ¼ 0.04) adjusted for main confounders. Total DF, insoluble, soluble DF and galacto-oligosaccharide intakes were associated with higher sociability score. Soluble DF intake was associated with better satisfaction of bowel function (p ¼ 0.02) and a lower intestinal discomfort (p ¼ 0.04). Conclusions: This study reveals that insufficient DF intake is part of AUD-related malnutrition syndrome, and is associated with higher anxiety, lower sociability score and intestinal discomfort. Our results suggest that an adequate intake of DF might be beneficial for recovery from AUD. Trial registration: NCT03803709, https://clinicaltrials.gov/ct2/show/NCT03803709.

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Section: Discussionmentioning

confidence: 86%

“…We have already shown that the gut microbiota of alcoholic patients is altered [2]. It has been shown in animal studies that gut microbiota could influence anxiety and social behaviour [62,70,71]. In humans, microbial changes caused by fermented foods induce changes in mood [20,72].…”

Section: Discussionmentioning

confidence: 98%

Dietary fiber deficiency as a component of malnutrition associated with psychological alterations in alcohol use disorder

et al. 2021

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“…For instance, we have described two different behavioral profiles in mice that had intermittent or continuous access to HFD during adolescence [ 56 ]. In addition, a recent study has described a unique gut microbial profile in BED patients compared to obese individuals [ 71 ].…”

Section: Discussionmentioning

confidence: 99%

Pairing Binge Drinking and a High-Fat Diet in Adolescence Modulates the Inflammatory Effects of Subsequent Alcohol Consumption in Mice

González-Portilla

Montagud‐Romero

Navarrete

et al. 2021

IJMS

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Alcohol binge drinking (BD) and poor nutritional habits are two frequent behaviors among many adolescents that alter gut microbiota in a pro-inflammatory direction. Dysbiotic changes in the gut microbiome are observed after alcohol and high-fat diet (HFD) consumption, even before obesity onset. In this study, we investigate the neuroinflammatory response of adolescent BD when combined with a continuous or intermittent HFD and its effects on adult ethanol consumption by using a self-administration (SA) paradigm in mice. The inflammatory biomarkers IL-6 and CX3CL1 were measured in the striatum 24 h after BD, 3 weeks later and after the ethanol (EtOH) SA. Adolescent BD increased alcohol consumption in the oral SA and caused a greater motivation to seek the substance. Likewise, mice with intermittent access to HFD exhibited higher EtOH consumption, while the opposite effect was found in mice with continuous HFD access. Biochemical analyses showed that after BD and three weeks later, striatal levels of IL-6 and CX3CL1 were increased. In addition, in saline-treated mice, CX3CL1 was increased after continuous access to HFD. After oral SA procedure, striatal IL-6 was increased only in animals exposed to BD and HFD. In addition, striatal CX3CL1 levels were increased in all BD- and HFD-exposed groups. Overall, our findings show that adolescent BD and intermittent HFD increase adult alcohol intake and point to neuroinflammation as an important mechanism modulating this interaction.

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“…Leclercq and collaborators demonstrated that alterations in gut permeability and microbiome composition (principally decreases in genera from Ruminococcaceae family) were associated with craving, a hallmark of addiction (Leclercq et al, 2012(Leclercq et al, , 2014. More recently these authors have shown that gut microbiota induce changes in metabolism linked to alterations in sociability and depression in AUD (Leclercq et al, 2020). Recently, we have proposed a framework of how emotional dysregulation and alcohol-related microbiome dysbiosis could contribute to accelerate the addiction cycle in AUD (Carbia et al, 2020), highlighting the importance of integrating disparate aspects such as microbiota for advancing in the understanding of addiction.…”

Section: Implication For Substance Use Disordersmentioning

confidence: 99%

Microbiota‐gut‐brain axis as a regulator of reward processes

García-Cabrerizo

Carbia

Riordan

et al. 2021

Journal of Neurochemistry

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The reward system is a set of neuronal structures responsible for the processing of a number of psychological components, such as 'wanting', 'liking' and associative learning (Berridge & Robinson, 2003).These three processes occur together, 'wanting' dominates the initial appetitive phase, 'liking' dominates the consummatory phase, and learning occurs through the reward-behavioural cycle (Berridge et al., 2016). Both phenomena are underpinned by different brain circuits and neurotransmitter systems. The 'wanting' component is largely controlled by the dopaminergic system, whereas the 'liking' component is thought to be more mediated by opioid and GABAergic systems (Berridge & Robinson, 2003). The neural circuitry constituting the anatomical and neurochemical substrate for reward and pleasure was described several decades ago by Olds and Milner, who, after implanting electrodes in certain areas of the central nervous system (CNS) and administering electrical microstimuli, demonstrated a pleasure response in the animals (Olds and Milner 1954).Following this, it was proposed that the monoaminergic activity could underlie the neurochemical basis of pleasure, with the monoaminergic system playing an important role in drug reinforcement

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Gut Microbiota-Induced Changes in β-Hydroxybutyrate Metabolism Are Linked to Altered Sociability and Depression in Alcohol Use Disorder

Cited by 124 publications

References 97 publications

Dietary fiber deficiency as a component of malnutrition associated with psychological alterations in alcohol use disorder

Dietary fiber deficiency as a component of malnutrition associated with psychological alterations in alcohol use disorder

Pairing Binge Drinking and a High-Fat Diet in Adolescence Modulates the Inflammatory Effects of Subsequent Alcohol Consumption in Mice

Microbiota‐gut‐brain axis as a regulator of reward processes

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