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Influence of Intestinal Microbiota on Body Weight Gain: a Narrative Review of the Literature

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Abstract

In recent decades, experimental and clinical studies have associated the development of obesity with the composition of the gut microbiota. Mechanisms potentially involved in the contribution of gut microbiota to body weight gain include changes in energy extraction from the diet and the modulation of lipid metabolism, endocrine functions, and the immune system. The host’s specific genetic heritage, the type and amount of food intake, chronic inflammation, reduced body energy expenditure, and exposure to obesogenic pollutants are also potential contributing factors. The pathophysiological processes involved in the relationship between gut microbiota and obesity are not fully understood, and further studies are needed to establish whether differences in gut bacterial diversity between obese and normal body weight individuals are the cause or a consequence of obesity.

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References

  1. Gill SR, Pop M, DeBoy RT, Eckburg PB, Turnbaugh PJ, Samuel BS, et al. Metagenomic analysis of the human distal gut microbiome. Science. 2006;312(5778):1355–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  2. Gong J, Yang C. Advances in the methods for studying gut microbiota and their relevance to the research of dietary fiber functions. Food Res Int. 2012;489(2):916–29.

    Article  Google Scholar 

  3. Andersson AF, Lindberg M, Jakobsson H, Bäckhed F, Nyrén P, Engstrand L. Comparative analysis of human gut microbiota by barcoded pyrosequencing. PLoS One. 2008;3(7):e2836.

    Article  PubMed Central  PubMed  Google Scholar 

  4. Angelakis E, Armougom F, Million M, Raoult D. The relationship between gut microbiota and weight gain in humans. Future Microbiol. 2012;7(1):91–109.

    Article  PubMed  Google Scholar 

  5. Turnbaugh PJ, Bäckhed F, Fulton L, Gordon JI. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe. 2008;3(4):213–23.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  6. Vrieze A, Holleman F, Zoetendal EG, De Vos WM, Hoekstra JBL, Nieuwdorp M. The environment within: how gut microbiota may influence metabolism and body composition. Diabetologia. 2010;53(4):606–13.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  7. Diamant M, Blaak EE, De Vos WM. Do nutrient–gut–microbiota interactions play a role in human obesity, insulin resistance and type 2 diabetes? Obes Rev. 2011;12(4):272–81.

    Article  CAS  PubMed  Google Scholar 

  8. Krajmalnik-Brown R, Ilhan ZE, Kang DW, DiBaise JK. Effects of gut microbes on nutrient absorption and energy regulation. NutrClinPract. 2012;27(2):201–14.

    Google Scholar 

  9. Kovatcheva-Datchary P, Arora T. Nutrition, the gut microbiome and the metabolic syndrome. Best Pract Res Clin Gastroenterol. 2013;27(1):59–72.

    Article  CAS  PubMed  Google Scholar 

  10. Tsukumo DM, Carvalho BM, Carvalho-Filho MA, Saad MJ. Translational research into gut microbiota: new horizons in obesity treatment. Arq Bras Endocrinol Metabol. 2009;53(2):139–44.

    Article  PubMed  Google Scholar 

  11. Nyangale EP, Mottram DS, Gibson GR. Gut microbial activity, implications for health and disease: the potential role of metabolite analysis. J Proteome Res. 2012;11(2):5573–85.

    CAS  PubMed  Google Scholar 

  12. Kaiyala KJ, Schwartz MW. Toward a more complete (and less controversial) understanding of energy expenditure and its role in obesity pathogenesis. Diabetes. 2011;60(1):17–23.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  13. Tilg H, Kaser A. Gut microbiome, obesity, and metabolic dysfunction. J Clin Invest. 2011;121(6):2126.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  14. Russell WR, Duncan SH, Flint HJ. The gut microbial metabolome: modulation of cancer risk in obese individuals. Proc Nutr Soc. 2013;1(1):1–11.

    Google Scholar 

  15. Requena T, Cotter P, Shahar DR, Kleiveland CR, Martínez-Cuesta MC, Peláez C, et al. Interactions between gut microbiota, food and the obese host. Trends Food Sci Technol. 2013;34(1):44–53.

    Article  CAS  Google Scholar 

  16. Le Chatelier E, Nielsen T, Qin J, Prifti E, Hildebrand F, Falony G, et al. Richness of human gut microbiome correlates with metabolic markers. Nature. 2013;500:541–6.

    Article  PubMed  Google Scholar 

  17. Armougom F, Henry M, Vialettes B, Raccah D, Raoult D. Monitoring bacterial community of human gut microbiota reveals an increase in Lactobacillus in obese patients and Methanogens in anorexic patients. PLoS One. 2009;4(9):e7125.

    Article  PubMed Central  PubMed  Google Scholar 

  18. Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A. 2005;102(31):11070–5.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  19. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature. 2006;444(7122):1022–3.

    Article  CAS  PubMed  Google Scholar 

  20. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444(7122):1027–131.

    Article  PubMed  Google Scholar 

  21. Greiner T, Bäckhed F. Effects of the gut microbiota on obesity and glucose homeostasis. Trends Endocrinol Metab. 2011;22(4):117–23.

    Article  CAS  PubMed  Google Scholar 

  22. Frazier TH, DiBaise JK, McClain CJ. Gut microbiota, intestinal permeability, obesity-induced inflammation, and liver injury. JPEN J Parenter Enteral Nutr. 2011;35(5 Suppl):14S–20S.

    Article  CAS  PubMed  Google Scholar 

  23. Zuo HJ, Xie ZM, Zhang WW, Li YR, Wang W, Ding XB, et al. Gut bacteria alteration in obese people and its relationship with gene polymorphism. World J Gastroenterol: WJG. 2011;17(8):1076.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  24. Spor A, Koren O, Ley R. Unravelling the effects of the environment and host genotype on the gut microbiome. Nat Rev Microbiol. 2011;9(4):279–90.

    Article  CAS  PubMed  Google Scholar 

  25. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA, et al. Linking long-term dietary patterns with gut microbial enterotypes. Science. 2011;334(6052):105–8.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. Hildebrandt MA, Hoffmann C, Sherrill–Mix SA, Keilbaugh SA, Hamady M, Chen YY, et al. High-fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterology. 2009;137(5):1716–24,e2.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  27. Ravussin Y, Koren O, Spor A, LeDuc C, Gutman R, Stombaugh J, et al. Responses of gut microbiota to diet composition and weight loss in lean and obese mice. Obesity. 2012;20(4):738–47.

    Article  CAS  PubMed  Google Scholar 

  28. Snedeker SM, Hay AG. Do interactions between gut ecology and environmental chemicals contribute to obesity and diabetes? Environ Health Perspect. 2012;120(3):332.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  29. Tims S, Zoetendal EG, de Vos WM & Kleerebezem M. In: Metagenomics of the human body (ed. Nelson, KE.) 15–41; Springer, Berlin, 2011.

  30. Stewart JA, Chadwick VS, Murray A. Investigations into the influence of host genetics on the predominant eubacteria in the faecal microflora of children. J Med Microbiol. 2005;54:1239–42.

    Article  CAS  PubMed  Google Scholar 

  31. Zoetendal EG, Akkermans AD, Akkermans-van Vliet WM, de Visser JA, de Vos WM. The host genotype affects the bacterial community in the human gastronintestinal tract. Microb Ecol Health Dis. 2001;13:129–34.

    Article  Google Scholar 

  32. Jumpertz R, Le DS, Turnbaugh PJ, Trinidad C, Bogardus C, Gordon JI, et al. Energy-balance studies reveal associations between gut microbes, caloric load, and nutrient absorption in humans. The American J Clin Nut. 2011;94(1):8–65.

    Article  Google Scholar 

  33. Murphy EF, Cotter PD, Healy S, Marques TM, O’Sullivan O, Fouhy F, et al. Composition and energy harvesting capacity of the gut microbiota: relationship to diet, obesity and time in mouse models. Gut. 2010;59:1635–42.

    Article  CAS  PubMed  Google Scholar 

  34. Armougom F, Henry M, Vialettes B, Raccah D, Raoult D. Monitoring bacterial community of human gut microbiota reveals an increase in lactobacillus in obese patients and methanogens in anorexic patients. PLoS One. 2009;4(9):e7125.

    Article  PubMed Central  PubMed  Google Scholar 

  35. Zhang H, DiBaise JK, Zuccolo A, et al. Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci U S A. 2009;106(7):2365–70.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  36. Samuel BS, Gordon JI. A humanized gnotobiotic mouse model of host–archaeal–bacterial mutualism. Proc Natl Acad Sci. 2006;103(26):10011–6.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  37. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, et al. Diversity of the human intestinal microbial flora. Science. 2005;308:1635–8.

    Article  PubMed Central  PubMed  Google Scholar 

  38. DiBaise JK, Zhang H, Crowell MD, Krajmalnik-Brown R, Decker GA, Rittmann BE. Gut microbiota and its possible relationship with obesity. In: Mayo Clinic Proceedings. Elsevier. 2008;460–469.

  39. Dridi B, Raoult D, Drancourt M. Archaea as emerging organisms in complex human microbiomes. Anaerobe. 2011;17(2):56–63.

    Article  PubMed  Google Scholar 

  40. Bergman EN. Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiol Rev. 1990;70(2):567–90.

    CAS  PubMed  Google Scholar 

  41. Bron PA, Van Baarlen P, Kleerebezem M. Emerging molecular insights into the interaction between probiotics and the host intestinal mucosa. Nat Rev Microbiol. 2011;10(1):66–78.

    PubMed  Google Scholar 

  42. Shi X, Leng L, Wang T, Wang W, Du X, Li J, et al. CD44 is the signaling component of the macrophage migration inhibitory factor-CD74 receptor complex. Immunity. 2006;25(4):595–606.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  43. Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes. 2007;56(7):1761–72.

    Article  CAS  PubMed  Google Scholar 

  44. Musso G, Gambino R, Cassader M. Interactions between gut microbiota and host metabolism predisposing to obesity and diabetes. Annu Rev Med. 2011;62:361–80.

    Article  CAS  PubMed  Google Scholar 

  45. Bäckhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, et al. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A. 2004;101(44):15718–23.

    Article  PubMed Central  PubMed  Google Scholar 

  46. Bäckhed F, Manchester JK, Semenkovich CF, Gordon JI. Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc Natl Acad Sci. 2007;104(3):979–84.

    Article  PubMed Central  PubMed  Google Scholar 

  47. Musso G, Gambino R, Cassader M. Obesity, diabetes, and gut microbiota: the hygiene hypothesis expanded? Diabetes Care. 2010;33(10):2277–84.

    Article  PubMed Central  PubMed  Google Scholar 

  48. Ley RE. Obesity and the human microbiome. Curr Opin Gastroenterol. 2010;26(1):5–11.

    Article  PubMed  Google Scholar 

  49. Dutton S, Trayhurn P. Regulation of angiopoietin-like protein 4/fasting-induced adipose factor (Angptl4/FIAF) expression in mouse white adipose tissue and 3 T3-L1 adipocytes. Br J Nutr. 2008;100(1):18–26.

    Article  CAS  PubMed  Google Scholar 

  50. Kersten S. Regulation of lipid metabolism via angiopoietin-like proteins. Biochem Soc Trans. 2005;33(5):1059–62.

    Article  CAS  PubMed  Google Scholar 

  51. Zocco MA, Ainora ME, Gasbarrini G, Gasbarrini A. Bacteroides thetaiotaomicron in the gut: molecular aspects of their interaction. Dig Liver Dis. 2007;39(8):707–12.

    Article  CAS  PubMed  Google Scholar 

  52. Parker DS, Mcmillan RT. The determination of volatile fatty acids in the caecum of the conscious rabbit. Br J Nutr. 1976;35(3):365–71.

    Article  CAS  PubMed  Google Scholar 

  53. Cani PD, Delzenne NM, Amar J, Burcelin R. Role of gut microflora in the development of obesity and insulin resistance following high-fat diet feeding. Pathol Biol. 2008;56(5):305–9.

    Article  CAS  PubMed  Google Scholar 

  54. Delzenne NM, Cani PD, Neyrinck AM. Modulation of glucagon-like peptide 1 and energy metabolism by inulin and oligofructose: experimental data. J Nutr. 2007;137(11 Suppl):2547S–51S.

    CAS  PubMed  Google Scholar 

  55. Darzi J, Frost GS, Robertson MD. Do SCFA have a role in appetite regulation? Proc Nutr Soc. 2011;70(1):119–28.

    Article  CAS  PubMed  Google Scholar 

  56. Kellermayer R, Dowd SE, Harris RA, Balasa A, Schaible TD, Wolcott RD, et al. Colonic mucosal DNA methylation, immune response, and microbiome patterns in Toll-like receptor 2-knockout mice. FASEB J. 2011;25(5):1449–60.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  57. Ehses JA, Meier DT, Wueest S, Rytka J, Boller S, Wielinga PY, et al. Toll-like receptor 2-deficient mice are protected from insulin resistance and beta cell dysfunction induced by a high-fat diet. Diabetologia. 2010;53(8):1795–806.

    Article  CAS  PubMed  Google Scholar 

  58. Santaolalla R, Sussman DA, Abreu MT. TLR signaling: a link between gut microflora, colorectal inflammation and tumorigenesis. Drug Discov Today: Dis Mech. 2012;8(3):e57–62.

    Google Scholar 

  59. Bron PA, Van Baarlen P, Kleerebezem M. Emerging molecular insights into the interaction between probiotics and the host intestinal mucosa. Nat Rev Microbiol. 2011;10(1):66–78.

    PubMed  Google Scholar 

  60. Jacobs DM, Gaudier E, Duynhoven JV, Vaughan EE, et al. Non-digestible food ingredients, colonic microbiota and the impact on gut health and immunity: a role for metabolomics. Curr Drug Metab. 2009;10(1):41–54.

    Article  CAS  PubMed  Google Scholar 

  61. Varavallo MA, Thomé JN, Teshima E. Aplicação de bactérias probióticas para profilaxia e tratamento de doenças gastrointestinais. Semina cienc biol saúde. 2008;29(1):83–104.

    Article  Google Scholar 

  62. Benjdia A et al. Sulfatases and a radical S-adenosyl-L-methionine (AdoMet) enzyme are key for mucosal foraging and fitness of the prominent human gut symbiont, Bacteroides thetaiotaomicron. J Biol Chem. 2011;286(29):25973–82.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  63. Turnbaugh PJ, Gordon J. The core gut microbiome, energy balance and obesity. J Physiol. 2009;587(17):4153–8.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  64. Sachidanandam R, Weissman D, Schmidt SC, Kakol JM, Stein LD, Marth G, et al. A map of human genome sequence variation containing 1.42 million single nucleotide polymorphisms. Nature. 2001;409(6822):928–33.

    Article  CAS  PubMed  Google Scholar 

  65. Geurts L, Lazarevic V, Derrien M, Everard A, Van Roye M, Knauf C, et al. Altered gut microbiota and endocannabinoid system tone in obese and diabetic leptin-resistant mice: impact on apelin regulation in adipose tissue. Front Microbiol. 2011;2:149.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  66. Turnbaugh PJ, Ridaura VK, Faith JJ, Rey FE, Knight R, Gordon JI. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med. 2009;1(6):6ra14.

  67. Zhang C et al. Interactions between gut microbiota, host genetics and diet relevant to development of metabolic syndromes in mice. ISME J. 2009;4(2):232–41.

    Article  PubMed  Google Scholar 

  68. Fleissner CK, Huebel N, Abd El-Bary MM, Loh G, Klaus S, Blaut M. Absence of intestinal microbiota does not protect mice from diet-induced obesity. Br J Nutr. 2010;104(6):919.

    Article  CAS  PubMed  Google Scholar 

  69. Nadal I, Santacruz A, Marcos A, Warnberg J, Garagorri M, Moreno LA, et al. Shifts in clostridia, bacteroides and immunoglobulin-coating fecal bacteria associated with weight loss in obese adolescents. Int J Obes. 2009;33(7):758–67.

    Article  CAS  Google Scholar 

  70. Brinkworth GD, Noakes M, Clifton PM, Bird AR. Comparative effects of very low-carbohydrate, high-fat and high-carbohydrate, low-fat weight-loss diets on bowel habit and faecal short-chain fatty acids and bacterial populations. Br J Nutr. 2009;101(10):1493–502.

    Article  CAS  PubMed  Google Scholar 

  71. Russell WR, Gratz SW, Duncan SH, Holtrop G, Ince J, Scobbie L, 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(5):1062–72.

    Article  CAS  PubMed  Google Scholar 

  72. Li JV, Ashrafian H, Bueter M, Kinross J, Sands C, le Roux CW, et al. Metabolic surgery profoundly influences gut microbial–host metabolic cross-talk. Gut. 2011;60(9):1214–23.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  73. Li JV, Reshat R, Wu Q, Ashrafian H, Bueter M, le Roux CW, et al. Experimental bariatric surgery in rats generates a cytotoxic chemical environment in the gut contents. Front Microbiol. 2011;2:183.

    PubMed Central  PubMed  Google Scholar 

  74. Furet JP, Kong LC, Tap J, Poitou C, Basdevant A, Bouillot JL, 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):3049–57.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  75. Graessler J, Qin Y, Zhong H, Zhang J, Licinio J, Wong ML, et al. Metagenomic sequencing of the human gut microbiome before and after bariatric surgery in obese patients with type 2 diabetes: correlation with inflammatory and metabolic parameters. Pharmacogenomics J. 2013;13(6):514–22.

    Article  CAS  PubMed  Google Scholar 

  76. Kong LC, Tap J, Aron-Wisnewsky J, Pelloux V, Basdevant A, Bouillot JL, et al. Gut microbiota after gastric bypass in human obesity: increased richness and associations of bacterial genera with adipose tissue genes. Am J Clin Nutr. 2013;98(1):16–24.

    Article  CAS  PubMed  Google Scholar 

  77. Liou AP, Paziuk M, Luevano JM Jr, Machineni S, Turnbaugh PJ, Kaplan LM. Conserved shifts in the gut microbiota due to gastric bypass reduce host weight and adiposity. Sci Transl Med. 2013;5(178):178ra41.

  78. Collins SM, Surette M, Bercik P. The interplay between the intestinal microbiota and the brain. Nat Rev Microbiol. 2012;10(11):735–42.

    Article  CAS  PubMed  Google Scholar 

  79. Alcock J, Maley CC, Aktipis CA. Is eating behavior manipulated by the gastrointestinal microbiota? Evolutionary pressures and potential mechanisms. Bioessays. 2014;36(10):940–9.

    Article  PubMed Central  PubMed  Google Scholar 

  80. Zoetendal EG, Rajilic-Stojanovic M, de Vos WM. High-throughput diversity and functionality analysis of the gastrointestinal tract microbiota. Gut. 2008;57:1605–15.

    Article  CAS  PubMed  Google Scholar 

  81. Woodard GA, Encarnacion B, Downey JR, et al. Probiotics improve outcomes after Roux-en-Y gastric bypass surgery: a prospective randomized trial. J Gastrointest Surg. 2009;13(7):1198–204.

    Article  PubMed  Google Scholar 

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Acknowledgments

This review is linked to a project supported by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP 2011/09612-3).

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The authors have declared no conflict of interests.

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Authors and Affiliations

  1. Gastroenterology Department, School of Medicine, University of São Paulo, Avenida Doutor Arnaldo, 455, Cerqueira César, São Paulo, SP, CEP 01246-903, Brazil

    Camila S. Cardinelli, Priscila C. Sala, Raquel S. Torrinhas & Dan L. Waitzberg

  2. Biosciences Department, Federal University of São Paulo, Santos, São Paulo, Brazil

    Claudia C. Alves

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  1. Camila S. Cardinelli
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  2. Priscila C. Sala
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  3. Claudia C. Alves
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Cardinelli, C.S., Sala, P.C., Alves, C.C. et al. Influence of Intestinal Microbiota on Body Weight Gain: a Narrative Review of the Literature. OBES SURG 25, 346–353 (2015). https://doi.org/10.1007/s11695-014-1525-2

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