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Review: Short Chain Fatty Acids in Human Gut and Metabolic Health

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Review: Short Chain Fatty Acids in Human Gut and Metabolic Health Wageningen Academic Beneficial Microbes, 2020; 11(5): 411-455 Publishers Short chain fatty acids in human gut and metabolic health E.E. Blaak1*, E.E. Canfora1, S. Theis2, G. Frost3, A.K. Groen4,5, G. Mithieux6, A. Nauta7, K. Scott8, B. Stahl9,10, J. van Harsselaar2, R. van Tol11, E.E. Vaughan12 and K. Verbeke13 1Department of Human Biology, NUTRIM School of Nutrition and Translational Research in Metabolism, Maastricht University, Universiteitssingel 50, 6229 ER Maastricht, The Netherlands.; 2Südzucker Group – Beneo, Wormser Str. 11, Mannheim, 67283, Germany; 3Faculty of Medicine, Department of Metabolism, Digestion and Reproduction, Imperial College London, SW7 2AZ London, United Kingdom; 4Diabetes Center, Department of Internal and Vascular Medicine, Amsterdam University Medical Centers, location AMC, Amsterdam, the Netherlands; 5Quantitative Systems Biology, Department of Pediatrics, Centre for Liver, Digestive and Metabolic Diseases, University Medical Centre Groningen (UMCG), University of Groningen, P.O. Box 30.001, 9700 RB Groningen, the Netherlands; 6INSERM U1213, Faculté de Médecine Laennec, University of Lyon, 7-11 Rue Guillaume Paradin, 69372 Lyon, France; 7FrieslandCampina, P.O. Box 1551, 3800 BN Amersfoort, the Netherlands; 8The Rowett Institute, University of Aberdeen, Aberdeen, AB25 2ZD, United Kingdom; 9Danone Nutricia Research, Uppsalalaan 12, 3584 CT, Utrecht, the Netherlands; 10Department of Chemical Biology & Drug Discovery, Utrecht Institute for Pharmaceutical Sciences, Utrecht University, Universiteitsweg 99, 3584 CG Utrecht, the Netherlands; 11Reckitt Benckiser/Mead Johnson Nutrition, Middenkampweg 2, 6545 CJ Nijmegen, the Netherlands; 12Sensus (Royal Cosun), Borchwerf 3, 4704 RG Roosendaal, the Netherlands; 13Translational Research Center for Gastrointestinal Disorders (TARGID), KU Leuven, Herestraat 49, 3000 Leuven, Belgium; [email protected] Received: 31 March 2020 / Accepted: 1 July 2020 © 2020 Wageningen Academic Publishers OPEN ACCESS REVIEW ARTICLE Abstract Evidence is accumulating that short chain fatty acids (SCFA) play an important role in the maintenance of gut and metabolic health. The SCFA acetate, propionate and butyrate are produced from the microbial fermentation of indigestible carbohydrates and appear to be key mediators of the beneficial effects elicited by the gut microbiome. Microbial SCFA production is essential for gut integrity by regulating the luminal pH, mucus production, providing fuel for epithelial cells and effects on mucosal immune function. SCFA also directly modulate host metabolic health through a range of tissue-specific mechanisms related to appetite regulation, energy expenditure, glucose homeostasis and immunomodulation. Therefore, an increased microbial SCFA production can be considered as a health benefit, but data are mainly based on animal studies, whereas well-controlled human studies are limited. In this review an expert group by ILSI Europe’s Prebiotics Task Force discussed the current scientific knowledge on SCFA to consider the relationship between SCFA and gut and metabolic health with a particular focus on human evidence. Overall, the available mechanistic data and limited human data on the metabolic consequences of elevated gut-derived SCFA production strongly suggest that increasing SCFA production could be a valuable strategy in the preventing gastro-intestinal dysfunction, obesity and type 2 diabetes mellitus. Nevertheless, there is an urgent need for well controlled longer term human SCFA intervention studies, including measurement of SCFA fluxes and kinetics, the heterogeneity in response based on metabolic phenotype, the type of dietary fibre and fermentation site in fibre intervention studies and the control for factors that could shape the microbiome like diet, physical activity and use of medication. Keywords: prebiotics, SCFA, dietary fibre, gut health, metabolic health ISSN 1876-2883 print, ISSN 1876-2891 online, DOI 10.3920/BM2020.0057 411 E.E. Blaak et al. 1. Introduction is followed by an overview of SCFA in relation to gastro- intestinal health. Subsequently, effects on metabolic health There is accumulating evidence that the gut microbiome are addressed, including effects on energy balance, substrate is of importance in mucosal immunity, barrier integrity metabolism and low-grade inflammation. and gut health as well in the regulation of host metabolic health. The gut microbiota is able to ferment indigestible 2. Method section food components such as prebiotics and soluble dietary fibres. Prebiotic consumption can result in the microbial The search strategy conducted was developed through production of short-chain fatty acids (SCFA), including internal discussion within the research team, and deployed acetate, butyrate and propionate, as major end products. within the PubMed and/or SCOPUS bibliographic database. These metabolites emerge as one of the key mechanism by The search used a combination of terms targeting title which prebiotics exert their beneficial health effects (Gibson headings, keywords or free-text words, with specific filters et al., 2017; Koh et al., 2016). These include health effects finally applied. that are attributed to increased microbial SCFA formation including an improved gut barrier function and reduced With respect to all topics on physiological effects the intestinal inflammation. In addition, the SCFA butyrate is following search terms for SCFA was used: (short chain fatty an important fuel for the colonocytes and impairment in acid*[TI] OR SCFA[TI] OR butyrate[TI] OR butanoate[TI] fuel supply may play a role in a reduced gastro-intestinal OR butyric acid[TI] OR butanoic acid[TI] OR acetate[TI] functioning. Additionally, SCFA may affect gastro-intestinal OR ethanoate[TI] OR acetic acid[TI] OR ethanoic acid[TI] transit and motility. Besides effects on gastro-intestinal OR propionate[TI] OR propanoate[TI] OR propanoic health, SCFA may play a role in the pathophysiology of acid[TI] OR propionic acid[TI]). obesity and related diseases such as type 2 diabetes mellitus (T2DM) by affecting body weight control through effects This search string was combined with other specific search on energy intake and energy expenditure, as well as insulin terms as detailed in the supplementary data. References sensitivity and systemic low-grade (Canfora et al., 2015; cited in this review include primarily English language Chambers et al., 2018c; Rios-Covian et al., 2016). original research and some specific reviews by experts in the field. Increasing SCFA production and a more saccharolytic fermentation may in that context be considered as a health The focus was on studies in humans, but important benefit, but data are mostly based on animal studies and mechanistic insights from animal or ‘in vitro’ studies human studies are limited. Additionally, the majority of were included. For the parts on body weight control and mechanistic evidence from animal studies used different metabolic health a systematic narrative approach was used. routes to administer SCFA (e.g. oral vs intragastric infusions No protocol for this review has been published. Detailed vs colonic infusions vs gut microbial fermentation), which information on the applied search can be found in the may not all directly translate to the human situation. supplementary data. Consequently, a thorough review of the available evidence is required, with a particular focus on human clinical 3. Short chain fatty acid metabolism interventions or on human ex vivo studies such as human gut microbiota colonic models. Human gut microbiota generate short chain fatty acids Therefore, an expert group has been set up by ILSI Europe’s The human large intestine is home to a large and diverse Prebiotics Task Force, investigating and reviewing the population of microbial species, with particularly large current scientific knowledge on SCFA to consider the numbers of bacteria. The phylogenetic core, dynamics and relationship between SCFA and human health as well as stability of this ecosystem have been intensively studied by whether an increased gut-derived SCFA production can high throughput 16S ribosomal RNA gene sequencing- be regarded as a biomarker of gut and metabolic health. based technologies (see recent reviews (Almeida et al., The manuscript and its conclusions have been refined in a 2019; Falony et al., 2016; Hornung et al., 2018; Shetty workshop with scientific experts, industrial representatives et al., 2017). Briefly, the dominant bacterial phyla are and policy makers. Bacteroidetes and Firmicutes, while minor phyla include Actinobacteria, Proteobacteria and Verrucomicrobia, and In the review, we present current scientific evidence on methanogens are dominant amongst the Archaea. Notably health effects of gut-derived SCFA with a focus on evidence eight abundant genera, namely Bacteroides, Eubacterium, from human studies and interventions and only from in Faecalibacterium, Alistipes, Ruminococcus, Clostridium, vitro or animal research where almost no human research Roseburia and Blautia, were identified in more than 1000 is available. We first provide an overview of intestinal SCFA humans (Shetty et al., 2017). These microbes utilise a production, metabolism as well as rate of absorption, which diverse range of dietary substrates to produce an array of 412 Beneficial Microbes 11(5) Short-chain fatty acids in human gut and metabolic health metabolites, many of which are important for the health of only in the presence of acetate (Louis et al., 2004). Butyrate
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