Changes in Faecal Short-Chain Fatty Acids after Weight-Loss Interventions in Subjects with Morbid Obesity

Per G Farup, Jørgen Valeur, Per G Farup, Jørgen Valeur

Abstract

The gut microbiota and their metabolites, e.g., short-chain fatty acids (SCFA), are associated with obesity. The primary aims were to study faecal SCFA levels and the changes in SCFA levels after weight-loss interventions in subjects with obesity, and secondarily, to study factors associated with the faecal SCFA levels. In total, 90 subjects (men / women: 15/75) with a mean age of 44.4 (SD 8.4) years, BMI 41.7 (SD 3.7) kg/m2 and morbid obesity (BMI > 40 or > 35 kg/m2 with obesity-related complications) were included. Faecal SCFA and other variables were measured at inclusion and after a six-month conservative weight-loss intervention followed by bariatric surgery (RouxenY gastric bypass or gastric sleeve). Six months after surgery, the total amount of SCFA was reduced, the total and relative amounts of the main straight SCFA (acetic-, propionic-, and butyric- acids) were reduced, and the total and relative amounts of branched SCFA (isobutyric-, isovaleric-, and isocaproic- acids) were increased. The changes indicate a shift toward a proteolytic fermentation pattern with unfavorable health effects. The amount of SCFA was associated with the diet but not with metabolic markers or makers of the faecal microbiota composition. Dietary interventions could counteract the unfavorable effects.

Keywords: bariatric surgery; faecal microbiota; obesity; short-chain fatty acids; weight-loss.

Conflict of interest statement

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

References

    1. Verbeke K.A., Boobis A.R., Chiodini A., Edwards C.A., Franck A., Kleerebezem M., Nauta A., Raes J., Van Tol E.A., Tuohy K.M. Towards microbial fermentation metabolites as markers for health benefits of prebiotics. Nutr. Res. Rev. 2015;28:42–66. doi: 10.1017/S0954422415000037.
    1. Korpela K. Diet, Microbiota, and Metabolic Health: Trade-Off Between Saccharolytic and Proteolytic Fermentation. Annu. Rev. Food Sci. Technol. 2018;9:65–84. doi: 10.1146/annurev-food-030117-012830.
    1. Bouter K.E., Van Raalte D.H., Groen A.K., Nieuwdorp M. Role of the Gut Microbiome in the Pathogenesis of Obesity and Obesity-Related Metabolic Dysfunction. Gastroenterology. 2017;152:1671–1678. doi: 10.1053/j.gastro.2016.12.048.
    1. Kim K.N., Yao Y., Ju S.Y. Short Chain Fatty Acids and Fecal Microbiota Abundance in Humans with Obesity: A Systematic Review and Meta-Analysis. Nutrients. 2019;11 doi: 10.3390/nu11102512.
    1. Wagner N.R.F., Zaparolli M.R., Cruz M.R.R., Schieferdecker M.E.M., Campos A.C.L. Postoperative Changes in Intestinal Microbiota and Use of Probiotics in Roux-En-Y Gastric Bypass and Sleeve Vertical Gastrectomy: An Integrative Review. Arq. Bras. Cir. Dig. 2018;31:e1400. doi: 10.1590/0102-672020180001e1400.
    1. De Vadder F., Kovatcheva-Datchary P., Goncalves D., Vinera J., Zitoun C., Duchampt A., Backhed F., Mithieux G. Microbiota-generated metabolites promote metabolic benefits via gut-brain neural circuits. Cell. 2014;156:84–96. doi: 10.1016/j.cell.2013.12.016.
    1. Vinolo M.A., Rodrigues H.G., Nachbar R.T., Curi R. Regulation of inflammation by short chain fatty acids. Nutrients. 2011;3:858–876. doi: 10.3390/nu3100858.
    1. Russell W.R., Gratz S.W., Duncan S.H., Holtrop G., Ince J., Scobbie L., Duncan G., Johnstone A.M., Lobley G.E., Wallace R.J., et al. High-protein, reduced-carbohydrate weight-loss diets promote metabolite profiles likely to be detrimental to colonic health. Am. J. Clin. Nutr. 2011;93:1062–1072. doi: 10.3945/ajcn.110.002188.
    1. Oliphant K., Allen-Vercoe E. Macronutrient metabolism by the human gut microbiome: Major fermentation by-products and their impact on host health. Microbiome. 2019;7:91. doi: 10.1186/s40168-019-0704-8.
    1. Damms-Machado A., Mitra S., Schollenberger A.E., Kramer K.M., Meile T., Konigsrainer A., Huson D.H., Bischoff S.C. Effects of surgical and dietary weight loss therapy for obesity on gut microbiota composition and nutrient absorption. Biomed. Res. Int. 2015;2015:806248. doi: 10.1155/2015/806248.
    1. Sowah S.A., Riedl L., Damms-Machado A., Johnson T.S., Schubel R., Graf M., Kartal E., Zeller G., Schwingshackl L., Stangl G.I., et al. Effects of Weight-Loss Interventions on Short-Chain Fatty Acid Concentrations in Blood and Feces of Adults: A Systematic Review. Adv. Nutr. 2019;10:673–684. doi: 10.1093/advances/nmy125.
    1. Tremaroli V., Karlsson F., Werling M., Stahlman M., Kovatcheva-Datchary P., Olbers T., Fandriks L., Le Roux C.W., Nielsen J., Backhed F. Roux-en-Y Gastric Bypass and Vertical Banded Gastroplasty Induce Long-Term Changes on the Human Gut Microbiome Contributing to Fat Mass Regulation. Cell Metab. 2015;22:228–238. doi: 10.1016/j.cmet.2015.07.009.
    1. Aron-Wisnewsky J., Prifti E., Belda E., Ichou F., Kayser B.D., Dao M.C., Verger E.O., Hedjazi L., Bouillot J.L., Chevallier J.M., et al. Major microbiota dysbiosis in severe obesity: Fate after bariatric surgery. Gut. 2019;68:70–82. doi: 10.1136/gutjnl-2018-316103.
    1. Paganelli F.L., Luyer M., Hazelbag C.M., Uh H.W., Rogers M.R.C., Adriaans D., Berbers R.M., Hendrickx A.P.A., Viveen M.C., Groot J.A., et al. Roux-Y Gastric Bypass and Sleeve Gastrectomy directly change gut microbiota composition independent of surgery type. Sci. Rep. 2019;9:10979. doi: 10.1038/s41598-019-47332-z.
    1. Aasbrenn M., Lydersen S., Farup P.G. A Conservative Weight Loss Intervention Relieves Bowel Symptoms in Morbidly Obese Subjects with Irritable Bowel Syndrome: A Prospective Cohort Study. J. Obes. 2018;2018:3732753. doi: 10.1155/2018/3732753.
    1. Schauer P.R., Ikramuddin S., Hamad G., Eid G.M., Mattar S., Cottam D., Ramanathan R., Gourash W. Laparoscopic gastric bypass surgery: Current technique. J. Laparoendosc. Adv. Surg. Tech. A. 2003;13:229–239. doi: 10.1089/109264203322333557.
    1. Roa P.E., Kaidar-Person O., Pinto D., Cho M., Szomstein S., Rosenthal R.J. Laparoscopic sleeve gastrectomy as treatment for morbid obesity: Technique and short-term outcome. Obes. Surg. 2006;16:1323–1326. doi: 10.1381/096089206778663869.
    1. Carlsen M.H., Lillegaard I.T., Karlsen A., Blomhoff R., Drevon C.A., Andersen L.F. Evaluation of energy and dietary intake estimates from a food frequency questionnaire using independent energy expenditure measurement and weighed food records. Nutr. J. 2010;9:37. doi: 10.1186/1475-2891-9-37.
    1. The Norwegian Food Composition Table. [(accessed on 25 February 2020)]; Available online: .
    1. Normobiosis or Dysbiosis? [(accessed on 25 February 2020)]; Available online: .
    1. Casen C., Vebo H.C., Sekelja M., Hegge F.T., Karlsson M.K., Ciemniejewska E., Dzankovic S., Froyland C., Nestestog R., Engstrand L., et al. Deviations in human gut microbiota: A novel diagnostic test for determining dysbiosis in patients with IBS or IBD. Aliment. Pharmacol. Ther. 2015;42:71–83. doi: 10.1111/apt.13236.
    1. Genetic Analysis AS. GAMap TM Dysbiosis Test. [(accessed on 25 February 2020)]; Available online: .
    1. Zijlstra J.B., Beukema J., Wolthers B.G., Byrne B.M., Groen A., Dankert J. Pretreatment methods prior to gaschromatographic analysis of volatile fatty acids from faecal samples. Clin. Chim. Acta. 1977;78:243–250. doi: 10.1016/0009-8981(77)90312-6.
    1. Hoverstad T., Bjorneklett A., Midtvedt T., Fausa O., Bohmer T. Short-chain fatty acids in the proximal gastrointestinal tract of healthy subjects. Scand. J. Gastroenterol. 1984;19:1053–1058.
    1. Patrone V., Vajana E., Minuti A., Callegari M.L., Federico A., Loguercio C., Dallio M., Tolone S., Docimo L., Morelli L. Postoperative Changes in Fecal Bacterial Communities and Fermentation Products in Obese Patients Undergoing Bilio-Intestinal Bypass. Front. Microbiol. 2016;7:200. doi: 10.3389/fmicb.2016.00200.
    1. Aasbrenn M., Farup P.G., Videm V. Changes in C-reactive protein, neopterin and lactoferrin differ after conservative and surgical weight loss in individuals with morbid obesity. Sci. Rep. 2019;9:17695. doi: 10.1038/s41598-019-54107-z.
    1. David L.A., Maurice C.F., Carmody R.N., Gootenberg D.B., Button J.E., Wolfe B.E., Ling A.V., Devlin A.S., Varma Y., Fischbach M.A., et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505:559–563. doi: 10.1038/nature12820.
    1. Hijova E. Gut bacterial metabolites of indigestible polysaccharides in intestinal fermentation as mediators of public health. Bratisl. Lek. Listy. 2019;120:807–812. doi: 10.4149/BLL_2019_134.
    1. Duncan S.H., Belenguer A., Holtrop G., Johnstone A.M., Flint H.J., Lobley G.E. Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces. Appl. Environ. Microbiol. 2007;73:1073–1078. doi: 10.1128/AEM.02340-06.
    1. Scott K.P., Duncan S.H., Flint H.J. Dietary fibre and the gut microbiota. Nutr. Bull. 2008;33:201–211. doi: 10.1111/j.1467-3010.2008.00706.x.
    1. Suez J., Korem T., Zilberman-Schapira G., Segal E., Elinav E. Non-caloric artificial sweeteners and the microbiome: Findings and challenges. Gut Microbes. 2015;6:149–155. doi: 10.1080/19490976.2015.1017700.
    1. Suez J., Korem T., Zeevi D., Zilberman-Schapira G., Thaiss C.A., Maza O., Israeli D., Zmora N., Gilad S., Weinberger A., et al. Artificial sweeteners induce glucose intolerance by altering the gut microbiota. Nature. 2014;514:181–186. doi: 10.1038/nature13793.
    1. Feehley T., Nagler C.R. Health: The weighty costs of non-caloric sweeteners. Nature. 2014;514:176–177. doi: 10.1038/nature13752.
    1. Farup P.G., Aasbrenn M., Valeur J. Separating “good” from “bad” faecal dysbiosis-evidence from two cross-sectional studies. BMC Obes. 2018;5:30. doi: 10.1186/s40608-018-0207-3.
    1. Cani P.D. Severe obesity and gut microbiota: Does bariatric surgery really reset the system? Gut. 2019;68:5–6. doi: 10.1136/gutjnl-2018-316815.
    1. Andoh A., Nishida A., Takahashi K., Inatomi O., Imaeda H., Bamba S., Kito K., Sugimoto M., Kobayashi T. Comparison of the gut microbial community between obese and lean peoples using 16S gene sequencing in a Japanese population. J. Clin. Biochem. Nutr. 2016;59:65–70. doi: 10.3164/jcbn.15-152.
    1. Koliada A., Syzenko G., Moseiko V., Budovska L., Puchkov K., Perederiy V., Gavalko Y., Dorofeyev A., Romanenko M., Tkach S., et al. Association between body mass index and Firmicutes/Bacteroidetes ratio in an adult Ukrainian population. BMC Microbiol. 2017;17:120. doi: 10.1186/s12866-017-1027-1.
    1. Rajilic-Stojanovic M., De Vos W.M. The first 1000 cultured species of the human gastrointestinal microbiota. FEMS Microbiol. Rev. 2014;38:996–1047. doi: 10.1111/1574-6976.12075.
    1. Mahawar K.K., Sharples A.J. Contribution of Malabsorption to Weight Loss After Roux-en-Y Gastric Bypass: A Systematic Review. Obes. Surg. 2017;27:2194–2206. doi: 10.1007/s11695-017-2762-y.
    1. Canfora E.E., Meex R.C.R., Venema K., Blaak E.E. Gut microbial metabolites in obesity, NAFLD and T2DM. Nat. Rev. Endocrinol. 2019;15:261–273. doi: 10.1038/s41574-019-0156-z.
    1. Arora T., Sharma R., Frost G. Propionate. Anti-obesity and satiety enhancing factor? Appetite. 2011;56:511–515. doi: 10.1016/j.appet.2011.01.016.
    1. Li Z., Yi C.X., Katiraei S., Kooijman S., Zhou E., Chung C.K., Gao Y., Van den Heuvel J.K., Meijer O.C., Berbee J.F.P., et al. Butyrate reduces appetite and activates brown adipose tissue via the gut-brain neural circuit. Gut. 2018;67:1269–1279. doi: 10.1136/gutjnl-2017-314050.
    1. Yao C.K., Muir J.G., Gibson P.R. Review article: Insights into colonic protein fermentation, its modulation and potential health implications. Aliment. Pharmacol. Ther. 2016;43:181–196. doi: 10.1111/apt.13456.
    1. Diether N.E., Willing B.P. Microbial Fermentation of Dietary Protein: An Important Factor in Diet-Microbe-Host Interaction. Microorganisms. 2019;7 doi: 10.3390/microorganisms7010019.

Source: PubMed

3
Abonnere