Obesity is associated with a distinct brain-gut microbiome signature that connects Prevotella and Bacteroides to the brain’s reward center
The prevalence of obesity has risen to its highest values over the last two decades. While many studies have either shown brain or microbiome connections to obesity, few have attempted to analyze the brain-gut-microbiome relationship in a large cohort adjusting for cofounders. Therefore, we aim to e...
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| Language: | English |
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Taylor & Francis Group
2022-12-01
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| Series: | Gut Microbes |
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| Online Access: | https://www.tandfonline.com/doi/10.1080/19490976.2022.2051999 |
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| author | Tien S. Dong Michelle Guan Emeran A. Mayer Jean Stains Cathy Liu Priten Vora Jonathan P. Jacobs Venu Lagishetty Lin Chang Robert L. Barry Arpana Gupta |
| author_facet | Tien S. Dong Michelle Guan Emeran A. Mayer Jean Stains Cathy Liu Priten Vora Jonathan P. Jacobs Venu Lagishetty Lin Chang Robert L. Barry Arpana Gupta |
| author_sort | Tien S. Dong |
| collection | DOAJ |
| description | The prevalence of obesity has risen to its highest values over the last two decades. While many studies have either shown brain or microbiome connections to obesity, few have attempted to analyze the brain-gut-microbiome relationship in a large cohort adjusting for cofounders. Therefore, we aim to explore the connection of the brain-gut-microbiome axis to obesity controlling for such cofounders as sex, race, and diet. Whole brain resting state functional MRI was acquired, and connectivity and brain network properties were calculated. Fecal samples were obtained from 287 obese and non-obese participants (males n = 99, females n = 198) for 16s rRNA profiling and fecal metabolites, along with a validated dietary questionnaire. Obesity was associated with alterations in the brain’s reward network (nucleus accumbens, brainstem). Microbial diversity (p = .03) and composition (p = .03) differed by obesity independent of sex, race, or diet. Obesity was associated with an increase in Prevotella/Bacteroides (P/B) ratio and a decrease in fecal tryptophan (p = .02). P/B ratio was positively correlated to nucleus accumbens centrality (p = .03) and negatively correlated to fecal tryptophan (p = .004). Being Hispanic, eating a standard American diet, having a high Prevotella/Bacteroides ratio, and a high nucleus accumbens centrality were all independent risk factors for obesity. There are obesity-related signatures in the BGM-axis independent of sex, race, and diet. Race, diet, P/B ratio and increased nucleus accumbens centrality were independent risk factors for obesity. P/B ratio was inversely related to fecal tryptophan, a metabolite related to serotonin biosynthesis, and positively related to nucleus accumbens centrality, a region central to the brain’s reward center. These findings may expand the field of therapies for obesity through novel pathways directed at the BGM axis. |
| format | Article |
| id | doaj-art-84f43b27e4f74e38872672f004a0992a |
| institution | DOAJ |
| issn | 1949-0976 1949-0984 |
| language | English |
| publishDate | 2022-12-01 |
| publisher | Taylor & Francis Group |
| record_format | Article |
| series | Gut Microbes |
| spelling | doaj-art-84f43b27e4f74e38872672f004a0992a2025-08-20T03:22:16ZengTaylor & Francis GroupGut Microbes1949-09761949-09842022-12-0114110.1080/19490976.2022.2051999Obesity is associated with a distinct brain-gut microbiome signature that connects Prevotella and Bacteroides to the brain’s reward centerTien S. Dong0Michelle Guan1Emeran A. Mayer2Jean Stains3Cathy Liu4Priten Vora5Jonathan P. Jacobs6Venu Lagishetty7Lin Chang8Robert L. Barry9Arpana Gupta10Department of Medicine, Vatche and Tamar Manoukian Division of Digestive Diseases Los Angeles, USADepartment of Medicine, David Geffen School of Medicine Los Angeles, USADepartment of Medicine, Vatche and Tamar Manoukian Division of Digestive Diseases Los Angeles, USADepartment of Medicine, Vatche and Tamar Manoukian Division of Digestive Diseases Los Angeles, USADepartment of Medicine, Vatche and Tamar Manoukian Division of Digestive Diseases Los Angeles, USADepartment of Medicine, Vatche and Tamar Manoukian Division of Digestive Diseases Los Angeles, USADepartment of Medicine, Vatche and Tamar Manoukian Division of Digestive Diseases Los Angeles, USADepartment of Medicine, UCLA Microbiome Center, David Geffen School of Medicine at UCLA Los Angeles, USADepartment of Medicine, Vatche and Tamar Manoukian Division of Digestive Diseases Los Angeles, USADepartment of Radiology, Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Charlestown, MA, USADepartment of Medicine, Vatche and Tamar Manoukian Division of Digestive Diseases Los Angeles, USAThe prevalence of obesity has risen to its highest values over the last two decades. While many studies have either shown brain or microbiome connections to obesity, few have attempted to analyze the brain-gut-microbiome relationship in a large cohort adjusting for cofounders. Therefore, we aim to explore the connection of the brain-gut-microbiome axis to obesity controlling for such cofounders as sex, race, and diet. Whole brain resting state functional MRI was acquired, and connectivity and brain network properties were calculated. Fecal samples were obtained from 287 obese and non-obese participants (males n = 99, females n = 198) for 16s rRNA profiling and fecal metabolites, along with a validated dietary questionnaire. Obesity was associated with alterations in the brain’s reward network (nucleus accumbens, brainstem). Microbial diversity (p = .03) and composition (p = .03) differed by obesity independent of sex, race, or diet. Obesity was associated with an increase in Prevotella/Bacteroides (P/B) ratio and a decrease in fecal tryptophan (p = .02). P/B ratio was positively correlated to nucleus accumbens centrality (p = .03) and negatively correlated to fecal tryptophan (p = .004). Being Hispanic, eating a standard American diet, having a high Prevotella/Bacteroides ratio, and a high nucleus accumbens centrality were all independent risk factors for obesity. There are obesity-related signatures in the BGM-axis independent of sex, race, and diet. Race, diet, P/B ratio and increased nucleus accumbens centrality were independent risk factors for obesity. P/B ratio was inversely related to fecal tryptophan, a metabolite related to serotonin biosynthesis, and positively related to nucleus accumbens centrality, a region central to the brain’s reward center. These findings may expand the field of therapies for obesity through novel pathways directed at the BGM axis.https://www.tandfonline.com/doi/10.1080/19490976.2022.2051999Brain-Gut-MicrobiomePrevotellaBacteroidesObesitynucleus accumbens |
| spellingShingle | Tien S. Dong Michelle Guan Emeran A. Mayer Jean Stains Cathy Liu Priten Vora Jonathan P. Jacobs Venu Lagishetty Lin Chang Robert L. Barry Arpana Gupta Obesity is associated with a distinct brain-gut microbiome signature that connects Prevotella and Bacteroides to the brain’s reward center Gut Microbes Brain-Gut-Microbiome Prevotella Bacteroides Obesity nucleus accumbens |
| title | Obesity is associated with a distinct brain-gut microbiome signature that connects Prevotella and Bacteroides to the brain’s reward center |
| title_full | Obesity is associated with a distinct brain-gut microbiome signature that connects Prevotella and Bacteroides to the brain’s reward center |
| title_fullStr | Obesity is associated with a distinct brain-gut microbiome signature that connects Prevotella and Bacteroides to the brain’s reward center |
| title_full_unstemmed | Obesity is associated with a distinct brain-gut microbiome signature that connects Prevotella and Bacteroides to the brain’s reward center |
| title_short | Obesity is associated with a distinct brain-gut microbiome signature that connects Prevotella and Bacteroides to the brain’s reward center |
| title_sort | obesity is associated with a distinct brain gut microbiome signature that connects prevotella and bacteroides to the brain s reward center |
| topic | Brain-Gut-Microbiome Prevotella Bacteroides Obesity nucleus accumbens |
| url | https://www.tandfonline.com/doi/10.1080/19490976.2022.2051999 |
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