Navigating the Pediatric Microbiome: Emerging Evidence and Clinical Implications

Current Pediatrics Reports

Volumn 2, Issue 2, 2014, Pages 93-101

  Kassam, Zain ^a   Murray, Thomas S ^b  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b New York   (United States)

Author keywords

Atopic dermatitis; Fecal transplant; Inflammatory bowel disease; Microbiome; Obesity; Probiotics

Indexed keywords

EID: 84923926083     PISSN: None     EISSN: 21674841     Source Type: Journal    
DOI: 10.1007/s40124-014-0040-1     Document Type: Article

References (68)

1. Eckburg PB, Bik EM, Bernstein CN, et al. Diversity of the human intestinal microbial flora. Science. 2005;308:1635–8. DOI: 10.1126/science.1110591
2. Lozupone CA, Stombaugh JI, Gordon JI, et al. Diversity, stability and resilience of the human gut microbiota. Nature. 2012;489:220–30. doi:10.1038/nature11550. DOI: 10.1038/nature11550
3. Kim BS, Jeon YS, Chun J. Current status and future promise of the human microbiome. Pediatr Gastroenterol Hepatol Nutr. 2013;16:71–9. DOI: 10.5223/pghn.2013.16.2.71
4. Collins SM, Kassam Z, Bercik P. The adoptive transfer of behavioral phenotype via the intestinal microbiota: experimental evidence and clinical implications. Curr Opin Microbiol. 2013;16:240–5. DOI: 10.1016/j.mib.2013.06.004
5. Benson AK, Kelly SA, Legge R, et al. Individuality in gut microbiota composition in a complex polygenic trait shaped by multiple environmental and host genetic factors. Proc Natl Acad Sci USA. 2010;107:18933–8. DOI: 10.1073/pnas.1007028107
6. Spor A, Koren O, Ley R. Unravelling the effects of the environment and host genotype on the gut microbiome. Nat Rev Microbiol. 2011;9:279–90. DOI: 10.1038/nrmicro2540
7. Nauta AJ, Ben-Amor K, Knol J, et al. Relevance of pre- and postnatal nutrition to development and interplay between the microbiota and metabolic and immune systems. Am J Clin Nutr. 2013;98(Suppl):586–93. DOI: 10.3945/ajcn.112.039644
8. Kuo CH, Kuo HF, Huang CH, et al. Early life exposure to antibiotics and the risk of childhood allergic diseases: an update from the perspective of the hygiene hypothesis. J Microbiol Immunol Infect. 2013;46(5):320–9. DOI: 10.1016/j.jmii.2013.04.005
9. Turngaugh PJ, Ley RE, Hamady M, et al. The human microbiome project. Nature. 2007;449:804–10. DOI: 10.1038/nature06244
10. Arumugam M, Raes J, Pelletier E, et al.; MetaHIT Consortium. Enterotypes of the human gut microbiome. Nature. 2011;473(7346):174–80.
11. •• Fraher MH, O’Toole PW, Quigley EMM. Techniques used to characterize the gut microbiota: a guide for the clinician. Nat Rev Gastroenterol Hepatol. 2012;9:312–22. This is an excellent detailed review and critique of the many techniques currently available to extract and analyze data regarding microbiota in the gut.
12. Arumugam M, Raes J M, Pelletier E, et al. Enterotypes of the human gut microbiome. Nature. 2011;473:174–80. DOI: 10.1038/nature09944
13. Azad MB, Konya T, Maughan H, et al. Gut microbiota of healthy Canadian infants: profiles by mode of delivery and infant diet at 4 months. CMAJ. 2013;185:385–94. DOI: 10.1503/cmaj.121189
14. Johnson CL, Versalovic J. The human microbiome and its potential importance to pediatrics. Pediatrics. 2012;125(5):950–60. DOI: 10.1542/peds.2011-2736
15. Clemente JC, Ursell LK, Parfrey LW, Knight R. The impact of the gut microbiota on human health: an integrative view. Cell. 2013;148:1258–70. DOI: 10.1016/j.cell.2012.01.035
16. Chang JY, Antonopoulos DA, Kalra A, et al. Decreased diversity of the fecal microbiome in recurrent Clostridium difficile-associated diarrhea. J Infect Dis. 2008;197(3):435–8. DOI: 10.1086/525047
17. Elinav E, Strowig T, Kau AL, et al. NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell. 2011;145:745–57. DOI: 10.1016/j.cell.2011.04.022
18. de Vos WM, de Vos EA. Role of the intestinal microbiome in health and disease: from correlation to causation. Nutr Rev. 2012;70(Suppl 1):S45–56. DOI: 10.1111/j.1753-4887.2012.00505.x
19. Turnbaugh PJ, Hamady M, Yatsunenko T, et al. A core gut microbiome in obese and lean twins. Nature. 2009;457:480–4. DOI: 10.1038/nature07540
20. Vaahtovuo J, Munukka E, Korkeamaki M, et al. Fecal microbiota in early rheumatoid arthritis. J Rheumatol. 2008;35(8):1500–5.
21. Gosalbes MJ, Llop S, Valles Y, et al. Meconium microbiota types dominated by lactic acid or enteric bacteria are differentially associated with maternal eczema and respiratory problems in infants. Clin Exp Allergy. 2013;43:198–211. DOI: 10.1111/cea.12063
22. Hu J, Nomura Y, Bashir A, et al. Diversified microbiota of meconium is affected by maternal diabetes status. PLoS ONE. 2013;8(11):e78257. doi:10.1371/journal.pone.0078257. DOI: 10.1371/journal.pone.0078257
23. Dominguez-Bello MG, Costello EK, Contreras M, et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci USA. 2010;107(26):11971–5. DOI: 10.1073/pnas.1002601107
24. Breitbart B, Haynes M, Kelley S, et al. Viral diversity and dynamics in an infant gut. Res Microbiol. 2008;159:367–73. DOI: 10.1016/j.resmic.2008.04.006
25. Vaishampayan PA, Kuehl JV, Froula JL, et al. Comparative metagenomics and population dynamics of he gut microbiota in mothers and infants. Genome Biol Evol. 2010;2:53–66. DOI: 10.1093/gbe/evp057
26. Thum C, Cookson AL, Otter D, et al. Can nutritional modulation of maternal intestinal microbiota influence the development of the infant gastrointestinal tract? J Nutr. 2012;142(11):1921–8. DOI: 10.3945/jn.112.166231
27. Collado MC, Cernada M, Bäuerl C, et al. Microbial ecology and host–microbiota interactions during early life. Gut Microbes. 2012;3(4):352–65. DOI: 10.4161/gmic.21215
28. Fallini M, Amarri S, Uusijarvi A, et al. Determinants of the human intestinal microbiota after the introduction of first complementary foods in infant samples from European centres. Microbiology. 2011;157:1385–92. DOI: 10.1099/mic.0.042143-0
29. Koenig JE, Spor A, Scalfone N, et al. Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci USA. 2011;108(Supp1):4578–85. DOI: 10.1073/pnas.1000081107
30. Sartor RB, Muehlbauer M. Microbial host interaction in IBD: implications for pathogenesis and therapy. Curr Gastroenterol Rep. 2007;9(6):497–507. DOI: 10.1007/s11894-007-0066-4
31. Fava F, Danese S. Intestinal microbiota in inflammatory bowel disease: friend of foe. World J Gastroenterol. 2011;17(5):557–66. DOI: 10.3748/wjg.v17.i5.557
32. Vanderploeg R, Panaccione R, Ghosh S, Rioux K. Influences of intestinal bacteria in human inflammatory bowel disease. Infect Dis Clin N Am. 2010;24(4):977–93. DOI: 10.1016/j.idc.2010.07.008
33. Frank DN, Robertson CE, Hamm CM, et al. Disease phenotype and genotype are associated with shifts in intestinal-associated microbiota in inflammatory bowel disease. Inflamm Bowel Dis. 2011;1:179–84. DOI: 10.1002/ibd.21339
34. Sha S, Xu B, Wang X, et al. The biodiversity and composition of the dominant fecal microbiota in patients with inflammatory bowel disease. Diagn Microbiol Infect Dis. 2013;75:245–51. DOI: 10.1016/j.diagmicrobio.2012.11.022
35. Qin J, Li R, Raes J, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010;464:59–65. DOI: 10.1038/nature08821
36. Michail S, Durbin M, Turner D, et al. Alterations in the gut microbiome of children with severe ulcerative colitis. Inflamm Bowel Dis. 2012;18(10):1799–808. DOI: 10.1002/ibd.22860
37. • Kronman MP, Zaoutis TE, Haynes K, et al. Antibiotic exposure and IBD development among children: a population-based cohort study. Pediatrics. 2012;130:e794–803. This is an important observational study linking antibiotic exposure and IBD highlighting the need for appropriate antibiotic stewardship.
38. Ley RE, Turnbaugh PJ, Klein S, et al. Microbial ecology: human gut microbes associated with obesity. Nature. 2006;444:1022–3. DOI: 10.1038/4441022a
39. 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. DOI: 10.1146/annurev-med-012510-175505
40. •• Ridaura VK, Faith JJ, Rey FE, et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science. 2013;341. doi: 10.1126/science.1241214. This human–mouse model study is important as it elegantly illustrates the causal effect of the microbiome on obesity.
41. Backhed F, Ding H, Wang T, et al. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA. 2004;101:15718–23. DOI: 10.1073/pnas.0407076101
42. Reinhardt C, Reigstad CS, Backhed F. Intestinal microbiota during infancy and its implications for obesity. JPGN. 2009;48:249–56.
43. Turnbaugh PJ, Ley RE, Mahowald MA, et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444:1027–31. DOI: 10.1038/nature05414
44. Kalliomaki M, Collado MC, Salminen S, Isolauri E. Early differences in fecal microbiota composition in children may predict overweight. Am J Clin Nutr. 2008;87:534–8.
45. Xu P, Li M, Zhang J, Zhang T. Correlation of intestinal microbiota with overweight and obesity in Kazakh school children. BMC Microbiol. 2012;12:283. doi:10.1186/1471-2180-12-283. DOI: 10.1186/1471-2180-12-283
46. Ismail IH, Oppedisano F, Joseph SJ, et al. Reduced gut microbial diversity in early life is associated with later development of eczema but not atopy in high-risk infants. Pediatr Allergy Immunol. 2012;23:674–81. DOI: 10.1111/j.1399-3038.2012.01328.x
47. Bisgaard H, Li N, Bonnelykke K, et al. Reduced diversity of the intestinal microbiota during infancy is associated with increased risk of allergic disease at school age. J Allergy Clin Immunol. 2011;128(3):646–52. DOI: 10.1016/j.jaci.2011.04.060
48. Abrahamsson TR, Jakobsson HE, Andersson AF, et al. Low gut microbiota diversity in early infancy precedes asthma at school age. Clin Exp Allergy. 2013. doi: 10.1111/cea.12253 (Epub ahead of print).
49. Stensballe LG, Simonsen J, Jensen SM, et al. Use of antibiotics during pregnancy increases the risk of asthma in early childhood. J Pediatr. 2013;162:832–8. DOI: 10.1016/j.jpeds.2012.09.049
50. •• Hoskin-Parr L, Teyhan A, Blocker A, Henderson AJW. Antibiotic exposure in the first two years of life and development of asthma and other allergic diseases by 7.5 yr: a dose-dependent relationship. Pediatr Allergy Immunol. 2013;24:762–71. The dose dependent relationship between antibiotic exposure and asthma and allergic disease is striking in this cohort study of 4952 children.
51. FAO/WHO. Guidelines for the evaluation of probiotics in food. Joint FAO/WHO Working Group Report on Drafting for the Evaluation of Probiotics in Food. 2002. www.who.int/foodsafety/publications/fs_management/probiotics2. Accessed 14 Dec 2013.
52. Ismail IH, Oppedisano F, Joseph SJ, et al. Prenatal administration of Lactobacillus rhamnosus has no effect on the diversity of the early infant gut microbiota. Pediatr Allergy Immunol. 2012;23:255–8. DOI: 10.1111/j.1399-3038.2011.01239.x
53. Elazab N, Mendy A, Gasana J, et al. Probiotic administration in early life, atopy, and asthma: a meta-analysis of clinical trials. Pediatrics. 2013;132(3):e666–76. DOI: 10.1542/peds.2013-0246
54. Pelucchi C, Chatenoud L, Turati F, et al. Probiotics supplementation during pregnancy or infancy for the prevention of atopic dermatitis: a meta-analysis. Epidemiology. 2012;23(3):402–14. DOI: 10.1097/EDE.0b013e31824d5da2
55. •• Bertelsen R, Brantsæter J, Magnus AL, et al. Probiotic milk consumption in pregnancy and infancy and subsequent childhood allergic diseases. J Allergy Clin Immunol. 2013. doi: 10.1016/j.jaci.2013.07.032 (Epub ahead of print). This is a large cohort study of over 40,000 maternal-child pairs providing evidence for early probiotic use and protection against later allergic disease.
56. Arora T, Singh S, Sharma RK. Probiotics: interaction with gut microbiome and anti-obesity potential. Nutrition. 2013;29(4):591–6. DOI: 10.1016/j.nut.2012.07.017
57. Luoto R, Kalliomäki M, Laitinen K, et al. Initial dietary and microbiological environments deviate in normal-weight compared to overweight children at 10 years of age. J Pediatr Gastroenterol Nutr. 2011;52(1):90–5. DOI: 10.1097/MPG.0b013e3181f3457f
58. Luoto R, Kalliomäki M, Laitinen K, Isolauri E. The impact of perinatal probiotic intervention on the development of overweight and obesity: follow-up study from birth to 10 years. Int J Obes. 2010;34(10):531–7. DOI: 10.1038/ijo.2010.50
59. Million M, Angelakis E, Paul M, et al. Comparative meta-analysis of the effect of Lactobacillus species on weight gain in humans and animals. Microb Pathog. 2012;53(2):100–8. DOI: 10.1016/j.micpath.2012.05.007
60. Million M, Lagier JC, Yahav D, Paul M. Gut bacterial microbiota and obesity. Clin Microbiol Infect. 2013;19(4):305–13. DOI: 10.1111/1469-0691.12172
61. • Kassam Z, Lee CH, Yuan Y, Hunt RH. Fecal microbiota transplantation for Clostridium difficile infection: systematic review and meta-analysis. Am J Gastroenterol. 2013;108:500–8. This is an important meta-analysis that robustly summarizes the impact of fecal microbiota transplantation in Clostridium difficile infection and explores areas of concern, including safety in this field.
62. Kassam Z, Hundal R, Marshall JK, Lee CH. Fecal transplant via retention enema for refractory or recurrent Clostridium difficile infection. Arch Intern Med. 2010;172:191–3. DOI: 10.1001/archinte.172.2.191
63. •• Van Nood E, Vrieze A, Nieuwdorp M, et al. Duodenal infusion of donor feces for recurrent Clostridium difficile infection. N Engl J Med. 2013;368:407–15. This is the first randomized controlled trial for fecal microbiota transplant for Clostridium difficile, and it was stopped early for benefit highlighting the potential of this emerging therapy.
64. Vreize A, Van Nood E, Holleman F, et al. Transfer of intestinal microbiota from lean donor increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology. 2012;143:913–6. DOI: 10.1053/j.gastro.2012.06.031
65. Palmer C, Bik EM, Digiulio DB, et al. Development of human infant intestinal microbiota. PLoS Biol. 2007;5(e177):1556–73.
66. Tiihonen K, Ouwehand AC, Rautonen N. Human intestinal microbiota and healthy ageing. Ageing Res Rev. 2010;9(2):107–16. DOI: 10.1016/j.arr.2009.10.004
67. Allen-Vercoe E, Reid G, Viner N, et al. Canadian Working Group report on fecal microbiota therapy: microbial ecosystem therapeutics. Can J Gastroenterol. 2012;26(7):457–62.
68. Bakken JS, Borody T, Brandt LJ, et al. Treating Clostridium difficile infection with fecal microbiota transplantation. Clin Gastroenterol Hepatol. 2011;9(12):1044–9. DOI: 10.1016/j.cgh.2011.08.014