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      Fecal microbiota transplantation in a rodent model of short bowel syndrome: A therapeutic approach?

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          Abstract

          Extensive intestinal resection leads to Short Bowel Syndrome (SBS), the main cause of chronic intestinal failure. Colon preservation is crucial for spontaneous adaptation, to improve absorption and reduce parenteral nutrition dependence. Fecal microbiota transplantation (FMT), a promising approach in pathologies with dysbiosis as the one observed in SBS patients, was assessed in SBS rats with jejuno‐colonic anastomosis. The evolution of weight and food intake, the lenght of intestinal villi and crypts and the composition of fecal microbiota of Sham and SBS rats, transplanted or not with high fat diet rat microbiota, were analyzed. All SBS rats lost weight, increased their food intake and exhibited jejunal and colonic hyperplasia. Microbiota composition of SBS rats, transplanted or not, was largely enriched with Lactobacillaceae, and α‐ and β‐diversity were significantly different from Sham. The FMT altered microbiota composition and α‐ and β‐diversity in Sham but not SBS rats. FMT from high fat diet rats was successfully engrafted in Sham, but failed to take hold in SBS rats, probably because of the specific luminal environment in colon of SBS subjects favoring aero‐tolerant over anaerobic bacteria. Finally, the level of food intake in SBS rats was positively correlated with their Lactobacillaceae abundance. Microbiota transfer must be optimized and adapted to this specific SBS environment.

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          Most cited references81

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          Metagenomic biomarker discovery and explanation

          This study describes and validates a new method for metagenomic biomarker discovery by way of class comparison, tests of biological consistency and effect size estimation. This addresses the challenge of finding organisms, genes, or pathways that consistently explain the differences between two or more microbial communities, which is a central problem to the study of metagenomics. We extensively validate our method on several microbiomes and a convenient online interface for the method is provided at http://huttenhower.sph.harvard.edu/lefse/.
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            An obesity-associated gut microbiome with increased capacity for energy harvest.

            The worldwide obesity epidemic is stimulating efforts to identify host and environmental factors that affect energy balance. Comparisons of the distal gut microbiota of genetically obese mice and their lean littermates, as well as those of obese and lean human volunteers have revealed that obesity is associated with changes in the relative abundance of the two dominant bacterial divisions, the Bacteroidetes and the Firmicutes. Here we demonstrate through metagenomic and biochemical analyses that these changes affect the metabolic potential of the mouse gut microbiota. Our results indicate that the obese microbiome has an increased capacity to harvest energy from the diet. Furthermore, this trait is transmissible: colonization of germ-free mice with an 'obese microbiota' results in a significantly greater increase in total body fat than colonization with a 'lean microbiota'. These results identify the gut microbiota as an additional contributing factor to the pathophysiology of obesity.
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              Formation of propionate and butyrate by the human colonic microbiota

              The human gut microbiota ferments dietary non-digestible carbohydrates into short-chain fatty acids (SCFA). These microbial products are utilized by the host and propionate and butyrate in particular exert a range of health-promoting functions. Here an overview of the metabolic pathways utilized by gut microbes to produce these two SCFA from dietary carbohydrates and from amino acids resulting from protein breakdown is provided. This overview emphasizes the important role played by cross-feeding of intermediary metabolites (in particular lactate, succinate and 1,2-propanediol) between different gut bacteria. The ecophysiology, including growth requirements and responses to environmental factors, of major propionate and butyrate producing bacteria are discussed in relation to dietary modulation of these metabolites. A detailed understanding of SCFA metabolism by the gut microbiota is necessary to underpin effective strategies to optimize SCFA supply to the host.
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                Author and article information

                Contributors
                Journal
                Front Cell Infect Microbiol
                Front Cell Infect Microbiol
                Front. Cell. Infect. Microbiol.
                Frontiers in Cellular and Infection Microbiology
                Frontiers Media S.A.
                2235-2988
                03 March 2023
                2023
                : 13
                : 1023441
                Affiliations
                [1] 1 UMR-S1149, Centre de recherche sur l’inflammation, INSERM, Universite Paris Cite , Paris, France
                [2] 2 Sorbonne Université, AP-HP, Hôpital de la Pitié‐Salpêtrière‐Charles Foix, Service de Biochimie Endocrinienne et Oncologique , Paris, France
                [3] 3 Paris Center for Microbiome Medicine, Federation Hospitalo-Universitaire , Paris, France
                [4] 4 AP-HP, Hôpital Bichat -Claude Bernard, Service de chirurgie Générale OEsogastrique et Bariatrique , Paris, France
                [5] 5 UMR1319 - Micalis Institute, Institut National de Recherche pour l’Agriculture, l’alimentation et l’environnement (INRAE), AgroParisTech, Université Paris-Saclay , Jouy-en-Josas, France
                [6] 6 UMR-S 1139, INSERM, Universite Paris Cite , Paris, France
                [7] 7 AP-HP, Hôpital de la Pitié‐Salpêtrière‐Charles Foix, Service de Coprologie fonctionnelle , Paris, France
                [8] 8 Department of gastroenterology, IBD and nutrition Support, AP‐HP, CRMR MarDi, Hôpital Beaujon , Clichy, France
                Author notes

                Edited by: Jaime Garcia-Mena, Instituto Politécnico Nacional de México (CINVESTAV), Mexico

                Reviewed by: Julie Tomas, UMR 7280 CNRS CIML, France; Selvasankar Murugesan, Sidra Medicine, Qatar

                This article was submitted to Intestinal Microbiome, a section of the journal Frontiers in Cellular and Infection Microbiology

                Article
                10.3389/fcimb.2023.1023441
                10020656
                36936775
                657873b7-383f-4df9-9a5e-141a50473aed
                Copyright © 2023 Fourati, Dumay, Roy, Willemetz, Ribeiro-Parenti, Mauras, Mayeur, Thomas, Kapel, Joly, Le Gall, Bado and Le Beyec

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 19 August 2022
                : 03 February 2023
                Page count
                Figures: 4, Tables: 0, Equations: 0, References: 81, Pages: 11, Words: 5548
                Funding
                This work was supported by the Institut National de la Santé et de la Recherche Médicale (INSERM) and the Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE).
                Categories
                Cellular and Infection Microbiology
                Brief Research Report

                Infectious disease & Microbiology
                short bowel syndrome,fecal microbiota transplantation,lactobiota,lactobacillaceae,hyperphagia,intestinal hyperplasia,short chain fatty acid

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