Current Pediatrics Reports

, Volume 5, Issue 3, pp 150–155 | Cite as

The Intestinal Microbiome and Childhood Obesity

  • Jessica McCann
  • John Rawls
  • Patrick Seed
  • Sarah Armstrong
Obesity (S Armstrong and A Patel, Section Editors)
Part of the following topical collections:
  1. Topical Collection on Obesity

Abstract

Purpose of Review

Pediatric obesity has reached epidemic proportions worldwide. The community of microbes inhabiting the human intestine affects differential nutrient absorption, metabolism, and weight status. However, the majority of our knowledge is derived from animal models and adults with obesity. This review discusses the role of the intestinal microbiome in the development and modification of pediatric obesity, with a focus on opportunities for modification of the microbiome through alteration of environmental factors.

Recent Findings

Recent evidence suggests that obesity is associated with phylogenetic changes in the gut microbiome, yet most of what we know about the role of the microbiome and obesity is from research on adults. A vast number of variables influence the gut microbial ecology early in life, including maternal weight status, breastfeeding, dietary manipulation, antibiotic exposure, and pre/probiotic use. Both in experimental animal and human studies, advances in genomic, proteomic, and metabolomics technologies have expanded our capacity to understand the composition and phenotype of the gut microbiome and mechanistic factors that modulate human health.

Summary

The human intestinal microbiome is associated with both the environment and child obesity. Understanding the mechanisms behind microbial regulation of human metabolism during infancy and childhood is key to developing effective prevention and treatment of obesity.

Keywords

Microbiome Pediatric obesity Dysbiosis Intestinal bacteria 

Notes

Compliance with Ethical Standards

Conflict of Interest

Jessica McCann, Patrick Seed, and Sarah Armstrong declare that they have no conflicts of interest.

John Rawls reports grants from National Institutes of Health during the conduct of the study. In addition, Dr. Rawls has a patent PCT/US16/22958 pending, and a patent US11/080,755 issued.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.
    Ogden CL, Carroll MD, Lawman HG, Fryar CD, Kruszon-Moran D, Kit BK, et al. Trends in obesity prevalence among children and adolescents in the United States, 1988-1994 through 2013-2014. JAMA. 2016;315:2292–9.CrossRefPubMedGoogle Scholar
  2. 2.
    Skinner AC, Perrin EM, Skelton JA. Prevalence of obesity and severe obesity in US children, 1999-2014. Obesity (Silver Spring). 2016;24:1116–23.CrossRefGoogle Scholar
  3. 3.
    Whitlock EP, O'Conner EA, Williams SB, Beil TL, Lutz KW. U.S. preventive services task force evidence syntheses, formerly systematic evidence reviews, effectiveness of primary care interventions for weight Management in Children and Adolescents: an updated, targeted systematic review for the USPSTF. Rockville (MD): Agency for Healthcare Research and Quality (US); 2010.Google Scholar
  4. 4.
    Kuchnia A, Huizenga R, Frankenfield D, Matthie JR, Earthman CP. Overstated metabolic adaptation after “the biggest loser” intervention. Obesity (Silver Spring). 2016;24:2025.CrossRefGoogle Scholar
  5. 5.
    •• Lynch SV, Pedersen O. The human intestinal microbiome in health and disease. N Engl J Med. 2016;375:2369–79. This review is the most up-to-date and detailed summary of evidence for what is known about the human intestinal microbiome and health.Google Scholar
  6. 6.
    Hollister EB, Riehle K, Luna RA, Weidler EM, Rubio-Gonzales M, Mistretta TA, et al. Structure and function of the healthy pre-adolescent pediatric gut microbiome. Microbiome. 2015;3:36.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    • Riva A, Borgo F, Lassandro C, Verduci E, Morace G, Borghi E, et al. Pediatric obesity is associated with an altered gut microbiota and discordant shifts in Firmicutes populations. Environ Microbiol. 2017;19:95–105. This paper is the first to demonstrate significant differences in the intestinal microbiome between obese and healthy weight pediatric individuals.Google Scholar
  8. 8.
    Valsecchi C, Carlotta Tagliacarne S, Castellazzi A. 2016. Gut microbiota and obesity. J Clin Gastroenterol 50 Suppl 2, Proceedings from the 8th Probiotics, Prebiotics & New Foods for Microbiota and Human Health meeting held in Rome, Italy on September 13–15, 2015:S157-S158.Google Scholar
  9. 9.
    Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A. 2005;102:11070–5.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature. 2006;444:1022–3.CrossRefPubMedGoogle Scholar
  11. 11.
    • Seganfredo FB, Blume CA, Moehlecke M, Giongo A, Casagrande DS, Spolidoro JVN, et al. Weight-loss interventions and gut microbiota changes in overweight and obese patients: a systematic review. Obes Rev. 2017; doi:10.1111/obr.12541. This paper provides evidence that changes in lifestyle correlate with changes in the intestinal microbiome.
  12. 12.
    Ursell LK, Haiser HJ, Van Treuren W, Garg N, Reddivari L, Vanamala J, et al. The intestinal metabolome: an intersection between microbiota and host. Gastroenterology. 2014;146:1470–6.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Wexler AG, Goodman AL. An insider’s perspective: bacteroides as a window into the microbiome. Nat Microbiol. 2017;2:17026.CrossRefPubMedGoogle Scholar
  14. 14.
    Gao X, Jia R, Xie L, Kuang L, Feng L, Wan C. Obesity in school-aged children and its correlation with gut E. coli and Bifidobacteria: a case-control study. BMC Pediatr. 2015;15:64.Google Scholar
  15. 15.
    Bergstrom A, Skov TH, Bahl MI, Roager HM, Christensen LB, Ejlerskov KT, et al. Establishment of intestinal microbiota during early life: a longitudinal, explorative study of a large cohort of Danish infants. Appl Environ Microbiol. 2014;80:2889–900.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Nicolucci AC, Hume MP, Martinez I, Mayengbam S, Walter J, Reimer RA. Prebiotic reduces body fat and alters intestinal microbiota in children with overweight or obesity. Gastroenterology. 2017; doi:10.1053/j.gastro.2017.05.055.
  17. 17.
    Pedersen HK, Gudmundsdottir V, Nielsen HB, Hyotylainen T, Nielsen T, Jensen BA, et al. Human gut microbes impact host serum metabolome and insulin sensitivity. Nature. 2016;535:376–81.CrossRefPubMedGoogle Scholar
  18. 18.
    Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE, Kau AL, et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science. 2013;341:1241214.CrossRefPubMedGoogle Scholar
  19. 19.
    Blanton LV, Charbonneau MR, Salih T, Barratt MJ, Venkatesh S, Ilkaveya O, et al. 2016. Gut bacteria that prevent growth impairments transmitted by microbiota from malnourished children. Science 351.Google Scholar
  20. 20.
    Koren O, Goodrich JK, Cullender TC, Spor A, Laitinen K, Backhed HK, et al. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell. 2012;150:470–80.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Williams JE, Price WJ, Shafii B, Yahvah KM, Bode L, McGuire MA, et al. Relationships among microbial communities, maternal cells, oligosaccharides, and macronutrients in human milk. J Hum Lact. 2017; doi:10.1177/0890334417709433:890334417709433.
  22. 22.
    Munthali RJ, Kagura J, Lombard Z, Norris SA. Early life growth predictors of childhood adiposity trajectories and future risk for obesity: birth to twenty cohort. Child Obes. 2017; doi:10.1089/chi.2016.0310.
  23. 23.
    Groer MW, Gregory KE, Louis-Jacques A, Thibeau S, Walker WA. The very low birth weight infant microbiome and childhood health. Birth Defects Res C Embryo Today. 2015;105:252–64.CrossRefPubMedGoogle Scholar
  24. 24.
    Smithers LG, Mol BW, Jamieson L, Lynch JW. Cesarean birth is not associated with early childhood body mass index. Pediatr Obes. 2016; doi:10.1111/ijpo.12180.
  25. 25.
    Rutayisire E, Wu X, Huang K, Tao S, Chen Y, Tao F. Cesarean section may increase the risk of both overweight and obesity in preschool children. BMC Pregnancy Childbirth. 2016;16:338.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Blustein J, Attina T, Liu M, Ryan AM, Cox LM, Blaser MJ, et al. Association of caesarean delivery with child adiposity from age 6 weeks to 15 years. Int J Obes. 2013;37:900–6.CrossRefGoogle Scholar
  27. 27.
    Bernardi JR, Pinheiro TV, Mueller NT, Goldani HA, Gutierrez MR, Bettiol H, et al. Cesarean delivery and metabolic risk factors in young adults: a Brazilian birth cohort study. Am J Clin Nutr. 2015;102:295–301.CrossRefPubMedGoogle Scholar
  28. 28.
    Mueller NT, Bakacs E, Combellick J, Grigoryan Z, Dominguez-Bello MG. The infant microbiome development: mom matters. Trends Mol Med. 2015;21:109–17.CrossRefPubMedGoogle Scholar
  29. 29.
    Chu DM, Ma J, Prince AL, Antony KM, Seferovic MD, Aagaard KM. Maturation of the infant microbiome community structure and function across multiple body sites and in relation to mode of delivery. Nat Med. 2017;23:314–26.CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Lefebvre CM, John RM. The effect of breastfeeding on childhood overweight and obesity: a systematic review of the literature. J Am Assoc Nurse Pract. 2014;26:386–401.PubMedGoogle Scholar
  31. 31.
    Bell KA, Wagner CL, Feldman HA, Shypailo RJ, Belfort MB. Associations of infant feeding with trajectories of body composition and growth. Am J Clin Nutr. 2017; doi:10.3945/ajcn.116.151126.
  32. 32.
    Piccolo BD, Mercer KE, Bhattacharya S, Bowlin AK, Saraf MK, Pack L, et al. Early postnatal diets affect the bioregional small intestine microbiome and ileal metabolome in neonatal pigs. J Nutr. 2017; doi:10.3945/jn.117.252767.
  33. 33.
    Pannaraj PS, Li F, Cerini C, Bender JM, Yang S, Rollie A, et al. Association between breast milk bacterial communities and establishment and development of the infant gut microbiome. JAMA Pediatr. 2017; doi:10.1001/jamapediatrics.2017.0378.
  34. 34.
    Scott FI, Mamtani R. Antibiotics and obesity—a burgeoning or thinning argument? JAMA Pediatr. 2017;171:118–20.CrossRefPubMedGoogle Scholar
  35. 35.
    Korpela K, Zijlmans MA, Kuitunen M, Kukkonen K, Savilahti E, Salonen A, et al. Childhood BMI in relation to microbiota in infancy and lifetime antibiotic use. Microbiome. 2017;5:26.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Cox LM, Blaser MJ. Antibiotics in early life and obesity. Nat Rev Endocrinol. 2015;11:182–90.CrossRefPubMedGoogle Scholar
  37. 37.
    Cox LM, Yamanishi S, Sohn J, Alekseyenko AV, Leung JM, Cho I, et al. Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences. Cell. 2014;158:705–21.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Reijnders D, Goossens GH, Hermes GD, Neis EP, van der Beek CM, Most J, 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;24:63–74.CrossRefPubMedGoogle Scholar
  39. 39.
    Gerber JS, Bryan M, Ross RK, Daymont C, Parks EP, Localio AR, et al. Antibiotic exposure during the first 6 months of life and weight gain during childhood. JAMA. 2016;315:1258–65.CrossRefGoogle Scholar
  40. 40.
    Ajslev TA, Andersen CS, Gamborg M, Sorensen TI, Jess T. Childhood overweight after establishment of the gut microbiota: the role of delivery mode, pre-pregnancy weight and early administration of antibiotics. Int J Obes. 2011;35:522–9.CrossRefGoogle Scholar
  41. 41.
    Howarth GS, Wang H. Role of endogenous microbiota, probiotics and their biological products in human health. Nutrients. 2013;5:58–81.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Rondanelli M, Faliva MA, Perna S, Giacosa A, Peroni G, Castellazzi AM. Using probiotics in clinical practice: where are we now? A review of existing meta-analyses. Gut Microbes. 2017; doi:10.1080/19490976.2017.1345414:0.
  43. 43.
    Sonnenburg JL, Backhed F. Diet-microbiota interactions as moderators of human metabolism. Nature. 2016;535:56–64.CrossRefPubMedGoogle Scholar
  44. 44.
    Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes. 2007;56:1761–72.CrossRefPubMedGoogle Scholar
  45. 45.
    Cani PD, Delzenne NM. The role of the gut microbiota in energy metabolism and metabolic disease. Curr Pharm Des. 2009;15:1546–58.CrossRefPubMedGoogle Scholar
  46. 46.
    Cani PD, Possemiers S, Van de Wiele T, Guiot Y, Everard A, Rottier O, et al. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut. 2009;58:1091–103.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Cani PD, Lecourt E, Dewulf EM, Sohet FM, Pachikian BD, Naslain D, 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;90:1236–43.CrossRefPubMedGoogle Scholar
  48. 48.
    Schele E, Grahnemo L, Anesten F, Hallen A, Backhed F, Jansson JO. The gut microbiota reduces leptin sensitivity and the expression of the obesity-suppressing neuropeptides proglucagon (Gcg) and brain-derived neurotrophic factor (Bdnf) in the central nervous system. Endocrinology. 2013;154:3643–51.CrossRefPubMedGoogle Scholar
  49. 49.
    Duca FA, Swartz TD, Sakar Y, Covasa M. Increased oral detection, but decreased intestinal signaling for fats in mice lacking gut microbiota. PLoS One. 2012;7:e39748.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Vijay-Kumar M, Aitken JD, Carvalho FA, Cullender TC, Mwangi S, et al. Metabolic syndrome and altered gut microbiota in mice lacking toll-like receptor 5. Science. 2010;328:228–31.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Jessica McCann
    • 1
  • John Rawls
    • 1
  • Patrick Seed
    • 2
    • 3
  • Sarah Armstrong
    • 4
  1. 1.Department of Molecular Genetics and Microbiology, Center for Genomics of Microbial SystemsDuke University Medical CenterDurhamUSA
  2. 2.Department of PediatricsNorthwestern Feinberg School of MedicineChicagoUSA
  3. 3.Ann and Robert H. Lurie Children’s Hospital, Stanley Manne Children’s Research InstituteChicagoUSA
  4. 4.Department of Pediatrics, Division of Primary CareDuke University Medical CenterDurhamUSA

Personalised recommendations