Skip to main content

Advertisement

Log in

Diet and the Human Gut Microbiome: An International Review

  • Review
  • Published:
Digestive Diseases and Sciences Aims and scope Submit manuscript

Abstract

This review summarizes the key results of recently published studies on the effects of dietary change and nutritional intervention on the human microbiome from around the world, focusing on the USA, Canada, Europe, Asia, and Africa. It first explores mechanisms that might explain the ability of fiber-rich foods to suppress the incidence and mortality from westernized diseases, notably cancers of the colon, breast, liver, cardiovascular, infectious, and respiratory diseases, diabetes, and obesity (O’Keefe in Lancet Gastroenterol Hepatol 4(12):984–996, 2019; Am J Clin Nutr 110:265–266, 2019). It summarizes studies from Africa which suggest that disturbance of the colonic microbiome may exacerbate chronic malnutrition and growth failure in impoverished communities and highlights the importance of breast feeding. The American section discusses the role of the microbiome in the swelling population of patients with obesity and type 2 diabetes and examines the effects of race, ethnicity, geography, and climate on microbial diversity and metabolism. The studies from Europe and Asia extoll the benefits of whole foods and plant-based diets. The Asian studies examine the worrying changes from low-fat, high-carbohydrate diets to high-fat, low-carbohydrate ones and the increasing appearance of westernized diseases as in Africa and documents the ability of high-fiber traditional Chinese diets to reverse type 2 diabetes and control weight loss. In conclusion, most of the studies reviewed demonstrate clear changes in microbe abundances and in the production of fermentation products, such as short-chain fatty acids and phytochemicals following dietary change, but the significance of the microbiota changes to human health, with the possible exception of the stimulation of butyrogenic taxa by fiber-rich foods, is generally implied and not measured. Further studies are needed to determine how these changes in microbiota composition and metabolism can improve our health and be used to prevent and treat disease.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Sender R, Fuchs S, Milo R. Revised estimates for the number of human and bacteria cells in the body. PLoS Biol. 2016;14(8):e1002533.

    PubMed  PubMed Central  Google Scholar 

  2. Subramanian S, Huq S, Yatsunenko T, et al. Persistent gut microbiota immaturity in malnourished Bangladeshi children. Nature. 2014;510(7505):417–421.

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Arnold JW, Roach J, Azcarate-Peril MA. Emerging technologies for gut microbiome research. Trends Microbiol. 2016;24(11):887–901.

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Reid G, Nduti N, Sybesma W, et al. Harnessing microbiome and probiotic research in sub-Saharan Africa: recommendations from an African workshop. Microbiome. 2014;16(2):12.

    Google Scholar 

  5. Graf D, Di Cagno R, Fåk F, et al. Contribution of diet to the composition of the human gut microbiota. Microb Ecol Health Dis. 2015;4(26):26164.

    Google Scholar 

  6. Walker AW, Ince J, Duncan SH, et al. Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME J. 2011;5(2):220–230.

    CAS  PubMed  Google Scholar 

  7. Bäckhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI. Host-bacterial mutualism in the human intestine. Science. 2005;307(5717):1915–1920.

    PubMed  Google Scholar 

  8. Topping DL, Clifton PM. Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiol Rev. 2001;81(3):1031–1064.

    CAS  PubMed  Google Scholar 

  9. O’Keefe SJD. Diet, microorganisms and their metabolites, and colon cancer. Nat Rev Gastroenterol Hepatol. 2016;13(12):691–706.

    PubMed  PubMed Central  Google Scholar 

  10. O’Keefe SJ. The association between dietary fibre deficiency and high-income lifestyle-associated diseases: Burkitt’s hypothesis revisited. Lancet Gastroenterol Hepatol. 2019;4(12):984–996.

    PubMed  PubMed Central  Google Scholar 

  11. O’Keefe SJD. Plant-based foods and the microbiome in the preservation of health and prevention of disease. Am J Clin Nutr. 2019;110:265–266.

    PubMed  Google Scholar 

  12. Kim Y, Je Y. Dietary fibre intake and mortality from cardiovascular disease and all cancers: a meta-analysis of prospective cohort studies. Arch Cardiovasc Dis. 2016;109(1):39–54.

    PubMed  Google Scholar 

  13. Park Y, Subar AF, Hollenbeck A, Schatzkin A. Dietary fiber intake and mortality in the NIH-AARP diet and health study. Arch Intern Med. 2011;171(12):1061–1068.

    PubMed  PubMed Central  Google Scholar 

  14. Aune D, Chan DSM, Lau R, et al. Dietary fibre, whole grains, and risk of colorectal cancer: systematic review and dose-response meta-analysis of prospective studies. BMJ. 2011;10(343):d6617.

    Google Scholar 

  15. Blanton LV, Barratt MJ, Charbonneau MR, Ahmed T, Gordon JI. Childhood undernutrition, the gut microbiota, and microbiota-directed therapeutics. Science. 2016;352(6293):1533.

    CAS  PubMed  Google Scholar 

  16. Black RE, Victora CG, Walker SP, et al. Maternal and child undernutrition and overweight in low-income and middle-income countries. Lancet. 2013;382(9890):427–451.

    PubMed  Google Scholar 

  17. Nel E. Severe acute malnutrition. Curr Opin Clin Nutr Metab Care. 2018;21(3):195–199.

    CAS  PubMed  Google Scholar 

  18. Jones KD, Thitiri J, Ngari M, Berkley JA. Childhood malnutrition: toward an understanding of infections, inflammation, and antimicrobials. Food Nutr Bull. 2014;35(2 Suppl):S64–S70.

    PubMed  PubMed Central  Google Scholar 

  19. Kau AL, Ahern PP, Griffin NW, Goodman AL, Gordon JI. Human nutrition, the gut microbiome and the immune system. Nature. 2011;474(7351):327–336.

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Smith MI, Yatsunenko T, Manary MJ, et al. Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science. 2013;339(6119):548–554.

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Oldenburg CE, Sié A, Coulibaly B, et al. Effect of commonly used pediatric antibiotics on gut microbial diversity in preschool children in burkina faso: a randomized clinical trial. Open Forum Infect Dis. 2018;5(11):ofy289.

    PubMed  PubMed Central  Google Scholar 

  22. Atukunda P, Muhoozi GKM, van den Broek TJ, et al. Child development, growth and microbiota: follow-up of a randomized education trial in Uganda. J Glob Health. 2019;9(1):010431.

    PubMed  PubMed Central  Google Scholar 

  23. Paganini D, Uyoga MA, Kortman GAM, et al. Iron-containing micronutrient powders modify the effect of oral antibiotics on the infant gut microbiome and increase post-antibiotic diarrhoea risk: a controlled study in Kenya. Gut. 2019;68(4):645–653.

    CAS  PubMed  Google Scholar 

  24. Jaeggi T, Kortman GAM, Moretti D, et al. Iron fortification adversely affects the gut microbiome, increases pathogen abundance and induces intestinal inflammation in Kenyan infants. Gut. 2015;64(5):731–742.

    CAS  PubMed  Google Scholar 

  25. Tang M, Frank DN, Hendricks AE, et al. Iron in micronutrient powder promotes an unfavorable gut microbiota in Kenyan infants. Nutrients. 2017;9(7):776.

    PubMed Central  Google Scholar 

  26. Davis JCC, Lewis ZT, Krishnan S, et al. Growth and morbidity of Gambian infants are influenced by maternal milk oligosaccharides and infant gut microbiota. Sci Rep. 2017;12(7):40466.

    Google Scholar 

  27. Ordiz MI, Stephenson K, Agapova S, et al. Environmental enteric dysfunction and the fecal microbiota in Malawian children. Am J Trop Med Hyg. 2017;96(2):473–476.

    PubMed  PubMed Central  Google Scholar 

  28. Million M, Tidjani Alou M, Khelaifia S, et al. Increased gut redox and depletion of anaerobic and methanogenic prokaryotes in severe acute malnutrition. Sci Rep. 2016;17(6):26051.

    Google Scholar 

  29. Charbonneau MR, O’Donnell D, Blanton LV, et al. Sialylated milk oligosaccharides promote microbiota-dependent growth in models of infant undernutrition. Cell. 2016;164(5):859–871.

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Kristensen KHS, Wiese M, Rytter MJH, et al. Gut microbiota in children hospitalized with oedematous and non-oedematous severe acute malnutrition in Uganda. PLoS Negl Trop Dis. 2016;10(1):e0004369.

    PubMed  PubMed Central  Google Scholar 

  31. Reyes A, Blanton LV, Cao S, et al. Gut DNA viromes of Malawian twins discordant for severe acute malnutrition. Proc Natl Acad Sci USA. 2015;112(38):11941–11946.

    CAS  PubMed  Google Scholar 

  32. Kau AL, Planer JD, Liu J, et al. Functional characterization of IgA-targeted bacterial taxa from undernourished Malawian children that produce diet-dependent enteropathy. Sci Transl Med. 2015;7(276):276ra24.

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Bwakura-Dangarembizi M, Amadi B, Bourke CD, et al. Health outcomes, pathogenesis and epidemiology of severe acute malnutrition (HOPE-SAM): rationale and methods of a longitudinal observational study. BMJ Open. 2019;9(1):e023077.

    PubMed  PubMed Central  Google Scholar 

  34. Vray M, Hedible BG, Adam P, et al. A multicenter, randomized controlled comparison of three renutrition strategies for the management of moderate acute malnutrition among children aged from 6 to 24 months (the MALINEA project). Trials. 2018;19(1):666.

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Kane AV, Dinh DM, Ward HD. Childhood malnutrition and the intestinal microbiome. Pediatr Res. 2015;77(1–2):256–262.

    PubMed  Google Scholar 

  36. Gordon JI, Dewey KG, Mills DA, Medzhitov RM. The human gut microbiota and undernutrition. Sci Transl Med. 2012;4(137):137ps12.

    PubMed  Google Scholar 

  37. Williams JE, Price WJ, Shafii B, et al. Relationships among microbial communities, maternal cells, oligosaccharides, and macronutrients in human milk. J Hum Lact. 2017;33(3):540–551.

    PubMed  Google Scholar 

  38. Gough EK, Stephens DA, Moodie EEM, et al. Linear growth faltering in infants is associated with Acidaminococcus sp. and community-level changes in the gut microbiota. Microbiome. 2015;3:24.

    PubMed  PubMed Central  Google Scholar 

  39. Sonnenburg ED, Sonnenburg JL. Starving our microbial self: the deleterious consequences of a diet deficient in microbiota-accessible carbohydrates. Cell Metab. 2014;20(5):779–786.

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Ferlay J, Shin H-R, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer. 2010;127(12):2893–2917.

    CAS  PubMed  Google Scholar 

  41. Katsidzira L, Ocvirk S, Wilson A, et al. Differences in fecal gut microbiota, short-chain fatty acids and bile acids link colorectal cancer risk to dietary changes associated with urbanization among Zimbabweans. Nutr Cancer. 2019;71(8):1313–1324.

    CAS  PubMed  Google Scholar 

  42. O’Keefe SJD, Li JV, Lahti L, et al. Fat, fibre and cancer risk in African Americans and rural Africans. Nat Commun. 2015;28(6):6342.

    Google Scholar 

  43. Rampelli S, Schnorr SL, Consolandi C, et al. Metagenome sequencing of the Hadza A. Curr Biol. 2015;25(13):1682–1693.

    CAS  PubMed  Google Scholar 

  44. Turroni S, Fiori J, Rampelli S, et al. Fecal metabolome of the Hadza hunter-gatherers: a host-microbiome integrative view. Sci Rep. 2016;14(6):32826.

    Google Scholar 

  45. de Vrieze J. Gut instinct. Science. 2014;343(6168):241–243.

    PubMed  Google Scholar 

  46. Reimer RA, Willis HJ, Tunnicliffe JM, Park H, Madsen KL, Soto-Vaca A. Inulin-type fructans and whey protein both modulate appetite but only fructans alter gut microbiota in adults with overweight/obesity: a randomized controlled trial. Mol Nutr Food Res. 2017;61(11):1700484.

    Google Scholar 

  47. Nicolucci AC, Hume MP, Martínez I, Mayengbam S, Walter J, Reimer RA. Prebiotics reduce body fat and alter intestinal microbiota in children who are overweight or with obesity. Gastroenterology. 2017;153(3):711–722.

    PubMed  Google Scholar 

  48. Lambert JE, Parnell JA, Tunnicliffe JM, Han J, Sturzenegger T, Reimer RA. Consuming yellow pea fiber reduces voluntary energy intake and body fat in overweight/obese adults in a 12-week randomized controlled trial. Clin Nutr. 2017;36(1):126–133.

    CAS  PubMed  Google Scholar 

  49. Maldonado-Gómez MX, Martínez I, Bottacini F, et al. Stable engraftment of bifidobacterium longum AH1206 in the human gut depends on individualized features of the resident microbiome. Cell Host Microbe. 2016;20(4):515–526.

    PubMed  Google Scholar 

  50. Krumbeck JA, Maldonado-Gomez MX, Martínez I, et al. In vivo selection to identify bacterial strains with enhanced ecological performance in synbiotic applications. Appl Environ Microbiol. 2015;81(7):2455–2465.

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Krumbeck JA, Rasmussen HE, Hutkins RW, et al. Probiotic bifidobacterium strains and galactooligosaccharides improve intestinal barrier function in obese adults but show no synergism when used together as synbiotics. Microbiome. 2018;6(1):121.

    PubMed  PubMed Central  Google Scholar 

  52. Dubois G, Girard C, Lapointe F-J, Shapiro BJ. The inuit gut microbiome is dynamic over time and shaped by traditional foods. Microbiome. 2017;5(1):151.

    PubMed  PubMed Central  Google Scholar 

  53. Falk PG, Hooper LV, Midtvedt T, Gordon JI. Creating and maintaining the gastrointestinal ecosystem: what we know and need to know from gnotobiology. Microbiol Mol Biol Rev. 1998;62(4):1157–1170.

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Guarner F, Malagelada J-R. Gut flora in health and disease. Lancet. 2003;361(9356):512–519.

    PubMed  Google Scholar 

  55. Bokulich NA, Chung J, Battaglia T, et al. Antibiotics, birth mode, and diet shape microbiome maturation during early life. Sci Transl Med. 2016;8(343):343ra82.

    PubMed  PubMed Central  Google Scholar 

  56. Yatsunenko T, Rey FE, Manary MJ, et al. Human gut microbiome viewed across age and geography. Nature. 2012;486(7402):222–227.

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Schnorr SL. The diverse microbiome of the hunter-gatherer. Nature. 2015;518(7540):S14–S15.

    CAS  PubMed  Google Scholar 

  58. Stearns JC, Zulyniak MA, de Souza RJ, et al. Ethnic and diet-related differences in the healthy infant microbiome. Genome Med. 2017;9(1):32.

    PubMed  PubMed Central  Google Scholar 

  59. Duncan SH, Louis P, Flint HJ. Lactate-utilizing bacteria, isolated from human feces, that produce butyrate as a major fermentation product. Appl Environ Microbiol. 2004;70(10):5810–5817.

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Martínez I, Lattimer JM, Hubach KL, et al. Gut microbiome composition is linked to whole grain-induced immunological improvements. ISME J. 2013;7(2):269–280.

    PubMed  Google Scholar 

  61. Wu GD, Chen J, Hoffmann C, et al. Linking long-term dietary patterns with gut microbial enterotypes. Science. 2011;334(6052):105–108.

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Bamberger C, Rossmeier A, Lechner K, et al. A walnut-enriched diet reduces lipids in healthy caucasian subjects, independent of recommended macronutrient replacement and time point of consumption: a prospective, randomized, controlled trial. Nutrients. 2017;9(10):1097.

    PubMed Central  Google Scholar 

  63. Bamberger C, Rossmeier A, Lechner K, et al. A walnut-enriched diet affects gut microbiome in healthy Caucasian subjects: a randomized, controlled trial. Nutrients. 2018;10(2):244.

    PubMed Central  Google Scholar 

  64. Tanaka T, Kouda K, Kotani M, et al. Vegetarian diet ameliorates symptoms of atopic dermatitis through reduction of the number of peripheral eosinophils and of PGE2 synthesis by monocytes. J Physiol Anthropol Appl Human Sci. 2001;20(6):353–361.

    CAS  PubMed  Google Scholar 

  65. Zhang C, Björkman A, Cai K, et al. Impact of a 3-months vegetarian diet on the gut microbiota and immune repertoire. Front Immunol. 2018;27(9):908.

    Google Scholar 

  66. Rivière A, Selak M, Lantin D, Leroy F, De Vuyst L. Bifidobacteria and butyrate-producing colon bacteria: importance and strategies for their stimulation in the human gut. Front Microbiol. 2016;28(7):979.

    Google Scholar 

  67. Volokh O, Klimenko N, Berezhnaya Y, et al. Human gut microbiome response induced by fermented dairy product intake in healthy volunteers. Nutrients. 2019;11(3):547.

    CAS  PubMed Central  Google Scholar 

  68. Adatorwovor R, Roggenkamp K, Anderson JJB. Intakes of calcium and phosphorus and calculated calcium-to-phosphorus ratios of older adults: NHANES 2005–2006 data. Nutrients. 2015;7(11):9633–9639.

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Ritz E, Hahn K, Ketteler M, Kuhlmann MK, Mann J. Phosphate additives in food–a health risk. Dtsch Arztebl Int. 2012;109(4):49–55.

    PubMed  PubMed Central  Google Scholar 

  70. Trautvetter U, Camarinha-Silva A, Jahreis G, Lorkowski S, Glei M. High phosphorus intake and gut-related parameters—results of a randomized placebo-controlled human intervention study. Nutr J. 2018;17(1):23.

    PubMed  PubMed Central  Google Scholar 

  71. Du SF, Wang HJ, Zhang B, Zhai FY, Popkin BM. China in the period of transition from scarcity and extensive undernutrition to emerging nutrition-related non-communicable diseases, 1949–1992. Obes Rev. 2014;15(Suppl 1):8–15.

    CAS  PubMed  Google Scholar 

  72. 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 USA. 2010;107(33):14691–14696.

    PubMed  Google Scholar 

  73. Ou J, Carbonero F, Zoetendal EG, et al. Diet, microbiota, and microbial metabolites in colon cancer risk in rural Africans and African Americans. Am J Clin Nutr. 2013;98(1):111–120.

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Wan Y, Wang F, Yuan J, et al. Effects of dietary fat on gut microbiota and faecal metabolites, and their relationship with cardiometabolic risk factors: a 6-month randomised controlled-feeding trial. Gut. 2019;68(8):1417–1429.

    CAS  PubMed  Google Scholar 

  75. Zackular JP, Rogers MAM, Ruffin MT, Schloss PD. The human gut microbiome as a screening tool for colorectal cancer. Cancer Prev Res (Phila Pa). 2014;7(11):1112–1121.

    CAS  Google Scholar 

  76. Zhao L, Zhang F, Ding X, et al. Gut bacteria selectively promoted by dietary fibers alleviate type 2 diabetes. Science. 2018;359(6380):1151–1156.

    CAS  PubMed  Google Scholar 

  77. Zhang C, Yin A, Li H, et al. Dietary modulation of gut microbiota contributes to alleviation of both genetic and simple obesity in children. EBioMedicine. 2015;2(8):968–984.

    PubMed  PubMed Central  Google Scholar 

  78. Xu J, Lian F, Zhao L, et al. Structural modulation of gut microbiota during alleviation of type 2 diabetes with a Chinese herbal formula. ISME J. 2015;9(3):552–562.

    PubMed  Google Scholar 

  79. Li T, Lu X, Yang X. Stachyose-enriched α-galacto-oligosaccharides regulate gut microbiota and relieve constipation in mice. J Agric Food Chem. 2013;61(48):11825–11831.

    CAS  PubMed  Google Scholar 

  80. Li T, Lu X, Yang X. Evaluation of clinical safety and beneficial effects of stachyose-enriched α-galacto-oligosaccharides on gut microbiota and bowel function in humans. Food Funct. 2017;8(1):262–269.

    CAS  PubMed  Google Scholar 

  81. Stoner GD, Mukhtar H. Polyphenols as cancer chemopreventive agents. J Cell Biochem Suppl. 1995;22:169–180.

    CAS  PubMed  Google Scholar 

  82. Yuan X, Long Y, Ji Z, et al. Green tea liquid consumption alters the human intestinal and oral microbiome. Mol Nutr Food Res. 2018;62(12):e1800178.

    PubMed  Google Scholar 

  83. Xie G, Zhou Q, Qiu C-Z, et al. Ketogenic diet poses a significant effect on imbalanced gut microbiota in infants with refractory epilepsy. World J Gastroenterol. 2017;23(33):6164–6171.

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stephen J. D. O’Keefe.

Ethics declarations

Conflict of interest

ASW, CC, and SJO report research support from the NIH. KRK, CAF, and ZTM report research support from the NIH and Mayo Clinic outside of this work. FRS reports research support from the NIH outside of this work. All other authors have no conflict of interest to disclose.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wilson, A.S., Koller, K.R., Ramaboli, M.C. et al. Diet and the Human Gut Microbiome: An International Review. Dig Dis Sci 65, 723–740 (2020). https://doi.org/10.1007/s10620-020-06112-w

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10620-020-06112-w

Keywords

Navigation