Prebiotic diet changes neural correlates of food decision-making in overweight adults: a randomised controlled within-subject cross-over trial.

Evelyn Medawar, Frauke Beyer, Ronja Thieleking, Sven-Bastiaan Haange, Ulrike Rolle-Kampczyk, Madlen Reinicke, Rima Chakaroun, Martin von Bergen, Michael Stumvoll, Arno Villringer, A Veronica Witte

Journal: Gut 2024;73(2):298-310

PMID: 37793780

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Plain Language Summary

It is thought that there is a connection between the gut microbiota and the brain and that prebiotics which fuel these gut microbiota may be able to affect mood and decision making. This randomised control trial of 59 individuals with overweight aimed to determine if supplementation of prebiotic fibre in the form of inulin could affect the desire for food. The results showed that compared to placebo individuals given inulin had a lower desire towards high caloric foods in conjunction with a change in the composition of the gut microbiota, especially Bifidobacteriaceae. It was concluded that prebiotics may be able to alter food-related decision making and alter the composition of the gut microbiota. This study could be used by healthcare professionals to understand that individuals who are overweight may choose unhealthy foods due to an imbalance in their gut microbiota. These individuals may benefit from prebiotic fibre to help aid microbiota changes and empowerment over food choices.

Abstract

OBJECTIVE

Animal studies suggest that prebiotic, plant-derived nutrients could improve homoeostatic and hedonic brain functions through improvements in microbiome-gut-brain communication. However, little is known if these results are applicable to humans. Therefore, we tested the effects of high-dosed prebiotic fibre on reward-related food decision-making in a randomised controlled within-subject cross-over study and assayed potential microbial and metabolic markers.

DESIGN

59 overweight young adults (19 females, 18-42 years, body mass index 25-30 kg/m) underwent functional task MRI before and after 14 days of supplementary intake of 30 g/day of inulin (prebiotics) and equicaloric placebo, respectively. Short chain fatty acids (SCFA), gastrointestinal hormones, glucose/lipid and inflammatory markers were assayed in fasting blood. Gut microbiota and SCFA were measured in stool.

RESULTS

Compared with placebo, participants showed decreased brain activation towards high-caloric wanted food stimuli in the ventral tegmental area and right orbitofrontal cortex after prebiotics (preregistered, family wise error-corrected p <0.05). While fasting blood levels remained largely unchanged, 16S-rRNA sequencing showed significant shifts in the microbiome towards increased occurrence of, among others, SCFA-producing , and changes in >60 predicted functional signalling pathways after prebiotic intake. Changes in brain activation correlated with changes in microbial abundance and associated activity previously linked with SCFA production, such as ABC transporter metabolism.

CONCLUSIONS

In this proof-of-concept study, a prebiotic intervention attenuated reward-related brain activation during food decision-making, paralleled by shifts in gut microbiota.

TRIAL REGISTRATION NUMBER

NCT03829189.

Address: Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany.; Berlin School of Mind and Brain, Humboldt-Universität zu Berlin, Berlin, Germany.; Charité Universitätsmedizin Berlin, Berlin, Germany.; Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany.; Cognitive Neurology, University of Leipzig Medical Center, Leipzig, Germany.; Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany.; Department of Molecular Systems Biology, Helmholtz-Centre for Environmental Research - UFZ, Leipzig, Germany.; Institute for Laboratory Medicine, Clinical Chemistry and Molecular Diagnostics, University of Leipzig Medical Center, Leipzig, Germany.; Department of Molecular and Clinical Medicine, University of Gothenburg, Goteborg, Sweden.; Medical Department III Endocrinology Nephrology Rheumatology, University of Leipzig Medical Center, Leipzig, Germany.; Medical Department III Endocrinology Nephrology Rheumatology, University of Leipzig Medical Center, Leipzig, Germany.; Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany [email protected].; Cognitive Neurology, University of Leipzig Medical Center, Leipzig, Germany.

DOI: 10.1136/gutjnl-2023-330365