4,070
Views
25
CrossRef citations to date
0
Altmetric
Review

The intestinal microbiota, energy balance, and malnutrition: emphasis on the role of short-chain fatty acids

, , , , &
Pages 215-226 | Received 30 Jan 2017, Accepted 07 Apr 2017, Published online: 26 Apr 2017

References

  • Lochs H, Allison SP, Meier R, et al. Introductory to the ESPEN Guidelines on Enteral Nutrition: terminology, definitions and general topics. Clin Nutr. 2006;25(2):180–186.
  • What is malnutrition? Online Q&A. World Health Organisation, [cited 2017 Apr 18]. Available from: http://www.who.int/mediacentre/factsheets/fs311/en/.
  • Obesity and overweight: fact sheet. World Health Organisation, [cited 2017 Apr 18]. Available from: http://www.who.int/features/qa/malnutrition/en/.
  • Tremaroli V, Backhed F. Functional interactions between the gut microbiota and host metabolism. Nature. 2012;489(7415):242–249.
  • Ley RE, Turnbaugh PJ, Klein S, et al. Microbial ecology: human gut microbes associated with obesity. Nature. 2006;444(7122):1022–1023.
  • Monira S, Nakamura S, Gotoh K, et al. Gut microbiota of healthy and malnourished children in Bangladesh. Front Microbiol. 2011;2:228.
  • Smith MI, Yatsunenko T, Manary MJ, et al. Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science. 2013;339(6119):548–554.
  • Ridaura VK, Faith JJ, Rey FE, et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science. 2013;341(6150):1241214.
  • Canfora EE, Jocken JW, Blaak EE. Short-chain fatty acids in control of body weight and insulin sensitivity. Nat Rev Endocrinol. 2015;11(10):577–591.
  • Aagaard K, Ma J, Antony KM, et al. The placenta harbors a unique microbiome. Sci Transl Med. 2014;6(237):237ra265.
  • Lauder AP, Roche AM, Sherrill-Mix S, et al. Comparison of placenta samples with contamination controls does not provide evidence for a distinct placenta microbiota. Microbiome. 2016;4(1):29.
  • Bäckhed F, Roswall J, Peng Y, et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe. 2015;17(5):690–703.
  • Yatsunenko T, Rey FE, Manary MJ, et al. Human gut microbiome viewed across age and geography. Nature. 2012;486(7402):222–227.
  • Darmasseelane K, Hyde MJ, Santhakumaran S, et al. Mode of delivery and offspring body mass index, overweight and obesity in adult life: a systematic review and meta-analysis. PLoS One. 2014;9(2):e87896.
  • Ajslev TA, Andersen CS, Gamborg M, et al. Childhood overweight after establishment of the gut microbiota: the role of delivery mode, pre-pregnancy weight and early administration of antibiotics. Int J Obes (Lond). 2011;35(4):522–529.
  • Clausen TD, Bergholt T, Bouaziz O, et al. Broad-spectrum antibiotic treatment and subsequent childhood type 1 diabetes: a nationwide Danish cohort study. PLoS One. 2016;11(8):e0161654.
  • Qin J, Li R, Raes J, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010;464(7285):59–65.
  • Sender R, Fuchs S, Milo R. Are we really vastly outnumbered? revisiting the ratio of bacterial to host cells in humans. Cell. 2016;164(3):337–340.
  • David LA, Materna AC, Friedman J, et al. Host lifestyle affects human microbiota on daily timescales. Genome Biol. 2014;15(7):R89.
  • Consortium HMP. Structure, function and diversity of the healthy human microbiome. Nature. 2012;486(7402):207–214.
  • Goodrich JK, Waters JL, Poole AC, et al. Human genetics shape the gut microbiome. Cell. 2014;159(4):789–799.
  • de Filippo C, Cavalieri D, di Paola M, et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A. 2010;107(33):14691–14696.
  • Song SJ, Lauber C, Costello EK, et al. Cohabiting family members share microbiota with one another and with their dogs. Elife. 2013;2:e00458.
  • Claesson MJ, Jeffery IB, Conde S, et al. Gut microbiota composition correlates with diet and health in the elderly. Nature. 2012;488(7410):178–184.
  • Turnbaugh PJ, Hamady M, Yatsunenko T, et al. A core gut microbiome in obese and lean twins. Nature. 2009;457(7228):480–484.
  • David LA, Maurice CF, Carmody RN, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505(7484):559–563.
  • Zeevi D, Korem T, Zmora N, et al. Personalized nutrition by prediction of glycemic responses. Cell. 2015;163(5):1079–1094.
  • Aguirre M, Jonkers DM, Troost FJ, et al. In vitro characterization of the impact of different substrates on metabolite production, energy extraction and composition of gut microbiota from lean and obese subjects. Plos One. 2014;9(11):e113864.
  • Bäckhed F, Ding H, Wang T, et al. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A. 2004;101(44):15718–15723.
  • Cummings JH, Pomare EW, Branch WJ, et al. Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut. 1987;28(10):1221–1227.
  • Macfarlane S, Macfarlane GT. Regulation of short-chain fatty acid production. Proc Nutr Soc. 2003;62(1):67–72.
  • Turnbaugh PJ, Ley RE, Mahowald MA, et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444(7122):1027–1031.
  • den Besten G, Lange K, Havinga R, et al. Gut-derived short-chain fatty acids are vividly assimilated into host carbohydrates and lipids. Am J Physiol Gastrointest Liver Physiol. 2013;305(12):G900–910.
  • Bergman EN. Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiol Rev. 1990;70(2):567–590.
  • Donohoe DR, Garge N, Zhang X, et al. The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metab. 2011;13(5):517–526.
  • Hoverstad T, Midtvedt T. Short-chain fatty acids in germfree mice and rats. J Nutr. 1772-1776;116(9):1986.
  • Frankel WL, Zhang W, Singh A, et al. Mediation of the trophic effects of short-chain fatty acids on the rat jejunum and colon. Gastroenterology. 1994;106(2):375–380.
  • Clarke JM, Young GP, Topping DL, et al. Butyrate delivered by butyrylated starch increases distal colonic epithelial apoptosis in carcinogen-treated rats. Carcinogenesis. 2012;33(1):197–202.
  • Hamer HM, Jonkers DM, Bast A, et al. Butyrate modulates oxidative stress in the colonic mucosa of healthy humans. Clin Nutr. 2009;28(1):88–93.
  • De Vadder F, Kovatcheva-Datchary P, Goncalves D, et al. Microbiota-generated metabolites promote metabolic benefits via gut-brain neural circuits. Cell. 2014;156(1–2):84–96.
  • Bäckhed F, Manchester JK, Semenkovich CF, et al. Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc Natl Acad Sci U S A. 2007;104(3):979–984.
  • den Besten G, Bleeker A, Gerding A, et al. Short-chain fatty acids protect against high-fat diet-induced obesity via a PPARγ-dependent switch from lipogenesis to fat oxidation. Diabetes. 2015;64(7):2398–2408.
  • Li X, Chen H, Guan Y, et al. Acetic acid activates the AMP-activated protein kinase signaling pathway to regulate lipid metabolism in bovine hepatocytes. Plos One. 2013;8(7):e67880.
  • den Besten G, van Eunen K, Groen AK, et al. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J Lipid Res. 2013;54(9):2325–2340.
  • Gao Z, Yin J, Zhang J, et al. Butyrate improves insulin sensitivity and increases energy expenditure in mice. Diabetes. 2009;58(7):1509–1517.
  • Sakakibara S, Yamauchi T, Oshima Y, et al. Acetic acid activates hepatic AMPK and reduces hyperglycemia in diabetic KK-A(y) mice. Biochem Biophys Res Commun. 2006;344(2):597–604.
  • Tolhurst G, Heffron H, Lam YS, et al. Short-chain fatty acids stimulate glucagon-like peptide-1 secretion via the G-protein-coupled receptor FFAR2. Diabetes. 2012;61(2):364–371.
  • Psichas A, Sleeth ML, Murphy KG, et al. The short chain fatty acid propionate stimulates GLP-1 and PYY secretion via free fatty acid receptor 2 in rodents. Int J Obes (Lond). 2015;39(3):424–429.
  • Brown AJ, Goldsworthy SM, Barnes AA, et al. The Orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids. J Biol Chem. 2003;278(13):11312–11319.
  • van der Beek CM, Canfora EE, Lenaerts K, et al. Distal, not proximal, colonic acetate infusions promote fat oxidation and improve metabolic markers in overweight/obese men. Clin Sci (Lond). 2016;130(22):2073–2082.
  • Perry RJ, Peng L, Barry NA, et al. Acetate mediates a microbiome-brain-beta-cell axis to promote metabolic syndrome. Nature. 2016;534(7606):213–217.
  • Ostman E, Granfeldt Y, Persson L, et al. Vinegar supplementation lowers glucose and insulin responses and increases satiety after a bread meal in healthy subjects. Eur J Clin Nutr. 2005;59(9):983–988.
  • Kondo T, Kishi M, Fushimi T, et al. Vinegar intake reduces body weight, body fat mass, and serum triglyceride levels in obese Japanese subjects. Biosci Biotechnol Biochem. 1837-1843;73(8):2009.
  • Hong YH, Nishimura Y, Hishikawa D, et al. Acetate and propionate short chain fatty acids stimulate adipogenesis via GPCR43. Endocrinology. 2005;146(12):5092–5099.
  • Xiong Y, Miyamoto N, Shibata K, et al. Short-chain fatty acids stimulate leptin production in adipocytes through the G protein-coupled receptor GPR41. Proc Natl Acad Sci U S A. 2004;101(4):1045–1050.
  • Minokoshi Y, Kim YB, Peroni OD, et al. Leptin stimulates fatty-acid oxidation by activating AMP-activated protein kinase. Nature. 2002;415(6869):339–343.
  • Al-Lahham S, Roelofsen H, Rezaee F, et al. Propionic acid affects immune status and metabolism in adipose tissue from overweight subjects. Eur J Clin Invest. 2012;42(4):357–364.
  • Wahlstrom A, Sayin SI, Marschall HU, et al. Intestinal crosstalk between bile acids and microbiota and its impact on host metabolism. Cell Metab. 2016;24(1):41–50.
  • Sayin SI, Wahlstrom A, Felin J, et al. Gut microbiota regulates bile acid metabolism by reducing the levels of tauro-beta-muricholic acid, a naturally occurring FXR antagonist. Cell Metab. 2013;17(2):225–235.
  • Thomas C, Gioiello A, Noriega L, et al. TGR5-mediated bile acid sensing controls glucose homeostasis. Cell Metab. 2009;10(3):167–177.
  • Trabelsi MS, Daoudi M, Prawitt J, et al. Farnesoid X receptor inhibits glucagon-like peptide-1 production by enteroendocrine L cells. Nat Commun. 2015;6:7629.
  • Clercq N, Groen AK, Romijn JA, et al. Gut microbiota in obesity and undernutrition. Advances in Nutrition. 2016;7:1080–1089.
  • de Silva A, Bloom SR. Gut hormones and appetite control: a focus on PYY and GLP-1 as therapeutic targets in obesity. Gut Liver. 2012;6(1):10–20.
  • Anastasovska J, Arora T, Sanchez Canon GJ. et al. Fermentable carbohydrate alters hypothalamic neuronal activity and protects against the obesogenic environment. Obesity (Silver Spring). 2012;20(5):1016–1023.
  • Frost G, Sleeth ML, Sahuri-Arisoylu M, et al. The short-chain fatty acid acetate reduces appetite via a central homeostatic mechanism. Nat Commun. 2014;5:3611.
  • Round JL, Mazmanian SK. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol. 2009;9(5):313–323.
  • Cani PD, Amar J, Iglesias MA, et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes. 1761-1772;56(7):2007.
  • Genton L, Cani PD, Schrenzel J. Alterations of gut barrier and gut microbiota in food restriction, food deprivation and protein-energy wasting. Clin Nutr. 2015;34(3):341–349.
  • Peng L, Li ZR, Green RS, et al. Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP-activated protein kinase in Caco-2 cell monolayers. J Nutr. 2009;139(9):1619–1625.
  • Smith PM, Howitt MR, Panikov N, et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science. 2013;341(6145):569–573.
  • Le Chatelier E, Nielsen T, Qin J, et al. Richness of human gut microbiome correlates with metabolic markers. Nature. 2013;500(7464):541–546.
  • Ley RE, Bäckhed F, Turnbaugh P, et al. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A. 2005;102(31):11070–11075.
  • Fernandes J, Su W, Rahat-Rozenbloom S, et al. Adiposity, gut microbiota and faecal short chain fatty acids are linked in adult humans. Nutr Diabetes. 2014;4:e121.
  • Schwiertz A, Taras D, Schafer K, et al. Microbiota and SCFA in lean and overweight healthy subjects. Obesity (Silver Spring). 2010;18(1):190–195.
  • Furet JP, Kong LC, Tap J, et al. Differential adaptation of human gut microbiota to bariatric surgery-induced weight loss: links with metabolic and low-grade inflammation markers. Diabetes. 2010;59(12):3049–3057.
  • Schneeberger M, Everard A, Gomez-Valades AG, et al. Akkermansia muciniphila inversely correlates with the onset of inflammation, altered adipose tissue metabolism and metabolic disorders during obesity in mice. Sci Rep. 2015;5:16643.
  • Preidis GA, Ajami NJ, Wong MC, et al. Composition and function of the undernourished neonatal mouse intestinal microbiome. J Nutr Biochem. 2015;26(10):1050–1057.
  • Bindels LB, Beck R, Schakman O, et al. Restoring specific lactobacilli levels decreases inflammation and muscle atrophy markers in an acute leukemia mouse model. Plos One. 2012;7(6):e37971.
  • Subramanian S, Huq S, Yatsunenko T, et al. Persistent gut microbiota immaturity in malnourished Bangladeshi children. Nature. 2014;510(7505):417–421.
  • Blanton LV, Charbonneau MR, Salih T, et al. Gut bacteria that prevent growth impairments transmitted by microbiota from malnourished children. Science. 2016;351(6275):830.
  • Wysokinski A, Sobow T, Kloszewska I, et al. Mechanisms of the anorexia of aging-a review. Age (Dordr). 2015;37(4):9821.
  • Claesson MJ, Cusack S, O’Sullivan O, et al. Composition, variability, and temporal stability of the intestinal microbiota of the elderly. Proc Natl Acad Sci U S A. 2011;108(Suppl 1):4586–4591.
  • Mack I, Cuntz U, Gramer C, et al. Weight gain in anorexia nervosa does not ameliorate the faecal microbiota, branched chain fatty acid profiles, and gastrointestinal complaints. Sci Rep. 2016;6:26752.
  • Pandey KR, Naik SR, Vakil BV. Probiotics, prebiotics and synbiotics - a review. J Food Sci Technol. 2015;52(12):7577–7587.
  • Saulnier DM, Santos F, Roos S, et al. Exploring metabolic pathway reconstruction and genome-wide expression profiling in Lactobacillus reuteri to define functional probiotic features. Plos One. 2011;6(4):e18783.
  • Biesalski HK. Nutrition meets the microbiome: micronutrients and the microbiota. Ann N Y Acad Sci. 2016;1372(1):53–64.
  • Whisner CM, Martin BR, Schoterman MH, et al. Galacto-oligosaccharides increase calcium absorption and gut bifidobacteria in young girls: a double-blind cross-over trial. Br J Nutr. 2013;110(7):1292–1303.
  • Sazawal S, Dhingra U, Hiremath G, et al. Effects of Bifidobacterium lactis HN019 and prebiotic oligosaccharide added to milk on iron status, anemia, and growth among children 1 to 4 years old. J Pediatr Gastroenterol Nutr. 2010;51(3):341–346.
  • Scholz-Ahrens KE, Schaafsma G, van den Heuvel EG, et al. Effects of prebiotics on mineral metabolism. Am J Clin Nutr. 2001;73(2 Suppl):459S–464S.
  • Sheridan PO, Bindels LB, Saulnier DM, et al. Can prebiotics and probiotics improve therapeutic outcomes for undernourished individuals? Gut Microbes. 2014;5(1):74–82.
  • Onubi OJ, Poobalan AS, Dineen B, et al. Effects of probiotics on child growth: a systematic review. J Health Popul Nutr. 2015;34:8.
  • Parnell JA, Reimer RA. Weight loss during oligofructose supplementation is associated with decreased ghrelin and increased peptide YY in overweight and obese adults. Am J Clin Nutr. 1751-1759;89(6):2009.
  • Cani PD, Lecourt E, Dewulf EM, et al. Gut microbiota fermentation of prebiotics increases satietogenic and incretin gut peptide production with consequences for appetite sensation and glucose response after a meal. Am J Clin Nutr. 2009;90(5):1236–1243.
  • Razmpoosh E, Javadi M, Ejtahed HS, et al. Probiotics as beneficial agents in the management of diabetes mellitus: a systematic review. Diabetes Metab Res Rev. 2016;32(2):143–168.
  • Sun J, Buys N. Effects of probiotics consumption on lowering lipids and CVD risk factors: a systematic review and meta-analysis of randomized controlled trials. Ann Med. 2015;47(6):430–440.
  • Mobini R, Tremaroli V, Stahlman M, et al. Metabolic effects of Lactobacillus reuteri DSM 17938 in patients with type 2 diabetes: a randomized controlled trial. Diabetes Obes Metab. 2017;19:579–589.
  • Simon MC, Strassburger K, Nowotny B, et al. Intake of Lactobacillus reuteri improves incretin and insulin secretion in glucose-tolerant humans: a proof of concept. Diabetes Care. 1827-1834;38(10):2015.
  • Cani PD, Bibiloni R, Knauf C, et al. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes. 2008;57(6):1470–1481.
  • Membrez M, Blancher F, Jaquet M, et al. Gut microbiota modulation with norfloxacin and ampicillin enhances glucose tolerance in mice. Faseb J. 2008;22(7):2416–2426.
  • Vrieze A, Out C, Fuentes S, et al. Impact of oral vancomycin on gut microbiota, bile acid metabolism, and insulin sensitivity. J Hepatol. 2014;60(4):824–831.
  • Reijnders D, Goossens GH, Hermes GD, et al. Effects of gut microbiota manipulation by antibiotics on host metabolism in obese humans: a randomized double-blind placebo-controlled trial. Cell Metab. 2016;24(1):63–74.
  • Zhang F, Luo W, Shi Y, et al. Should we standardize the 1,700-year-old fecal microbiota transplantation? Am J Gastroenterol. 2012;107(11):1755; author reply p 1755-1756.
  • Nieuwdorp M. Faecal microbiota transplantation. Br J Surg. 2014;101(8):887–888.
  • Eiseman B, Silen W, Bascom GS, et al. Fecal enema as an adjunct in the treatment of pseudomembranous enterocolitis. Surgery. 1958;44(5):854–859.
  • van Nood E, Vrieze A, Nieuwdorp M, et al. Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med. 2013;368(5):407–415.
  • Baxter M, Colville A. Adverse events in faecal microbiota transplant: a review of the literature. J Hosp Infect. 2016;92(2):117–127.
  • Vrieze A, Van Nood E, Holleman F, et al. Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology. 2012;143(4):913–916e917.
  • Alang N, Kelly CR. Weight gain after fecal microbiota transplantation. Open Forum Infect Dis. 2015;2(1):ofv004.
  • Li SS, Zhu A, Benes V, et al. Durable coexistence of donor and recipient strains after fecal microbiota transplantation. Science. 2016;352(6285):586–589.
  • Eckburg PB, Bik EM, Bernstein CN, et al. Diversity of the human intestinal microbial flora. Science. 1635-1638;308(5728):2005.
  • Falony G, Joossens M, Vieira-Silva S, et al. Population-level analysis of gut microbiome variation. Science. 2016;352(6285):560–564.