Urbanization and the gut microbiota in health and inflammatory bowel disease

Nature Reviews Gastroenterology and Hepatology

Volumn 15, Issue 7, 2018, Pages 440-452

  Zuo, Tao ^a   Kamm, Michael A ^b   Colombel, Jean Frédéric ^c   Ng, Siew C ^a,d  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^b ST VINCENT S HOSPITAL   (Australia)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^d and Hong Kong Branch of CAS Center for Excellence in Animal Evolution and Genetics   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

RNA 16S; ANTIINFECTIVE AGENT;

16SRRNA GENE; ACIDAMINOCOCCACEAE; ACREMONIUM; ACTINOMYCES; AFRICAN AMERICAN; ALISTIPES; ALTERNARIA; ASPERGILLUS; BACTEROIDES FRAGILIS; BIFIDOBACTERIUM; BILOPHILA; BLAUTIA; BOTRYTIS; CAUCASIAN; CHRYSOSPORIUM; CLADOSPORIUM; CROHN DISEASE; CXCL16 GENE; DISEASE PREDISPOSITION; DISEASE TRANSMISSION; ERYSIPELOTRICHACEAE; ESCHERICHIA COLI; FAECALIBACTERIUM; GENE SEQUENCE; GENETIC VARIABILITY; HELIGMOSOMOIDES; HELIGMOSOMOIDES POLYGYRUS; HOST PATHOGEN INTERACTION; HUMAN; IMMUNE RESPONSE; INTESTINE FLORA; KLEBSIELLA; LACHNOSPIRACEAE; LACTOBACILLACEAE; LACTOBACILLUS; LACTOBACILLUS HELVETICUS; MICROBIAL COLONIZATION; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MICROVIRIDAE; NATURAL KILLER T CELL; NONHUMAN; PATHOGENESIS; PENICILLIUM; PHASCOLARCTOBACTERIUM; POPULATION RESEARCH; PREVOTELLA; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; RUMINOCOCCUS; SCHISTOSOMA MANSONI; TRICHURIS MURIS; TRICHURIS SUIS; ULCERATIVE COLITIS; URBANIZATION; WESTERN DIET; DRUG EFFECT; INFLAMMATORY BOWEL DISEASE; MICROBIOLOGY; PHYSIOLOGY;

ANTI-BACTERIAL AGENTS; GASTROINTESTINAL MICROBIOME; HUMANS; INFLAMMATORY BOWEL DISEASES; URBANIZATION;

EID: 85045653616     PISSN: 17595045     EISSN: 17595053     Source Type: Journal    
DOI: 10.1038/s41575-018-0003-z     Document Type: Review

References (245)

1. Swinburn, B. A. et al. The global obesity pandemic: shaped by global drivers and local environments. Lancet 378, 804-814 (2011).
2. Kaplan, G. G. & Ng, S. C. Globalisation of inflammatory bowel disease: perspectives from the evolution of inflammatory bowel disease in the UK and China. Lancet Gastroenterol. Hepatol. 1, 307-316 (2016).
3. Cheema, A., Adeloye, D., Sidhu, S., Sridhar, D. & Chan, K. Y. Urbanization and prevalence of type 2 diabetes in Southern Asia: a systematic analysis. J. Glob. Health 4, 010404 (2014).
4. Allender, S., Foster, C., Hutchinson, L. & Arambepola, C. Quantification of urbanization in relation to chronic diseases in developing countries: a systematic review. J. Urban Health-Bull. New York Acad. Med. 85, 938-951 (2008).
5. Seto, K. C., Parnell, S. & Elmqvist, T. In Urbanization, Biodiversity and Ecosystem Services: Challenges and Opportunities: A Global Assessment (T. Elmqvist et al. eds.) 1-12 (Springer Netherlands, Dordrecht, 2013).
6. Manichanh, C., Borruel, N., Casellas, F. & Guarner, F. The gut microbiota in IBD. Nat. Rev. Gastroenterol. Hepatol. 9, 599-608 (2012).
7. Shreiner, A. B., Kao, J. Y. & Young, V. B. The gut microbiome in health and in disease. Curr. Opin. Gastroenterol. 31, 69 (2015).
8. Cho, I. & Blaser, M. J. The human microbiome: at the interface of health and disease. Nat. Rev. Genet. 13, 260-270 (2012).
9. Podolsky, D. K. Inflammatory bowel-disease. N. Engl. J. Med. 325, 928-937 (1991).
10. Love, J. R., Irvine, E. J. & Fedorak, R. N. Quality-of-life in inflammatory bowel-disease. J. Clin. Gastroenterol. 14, 15-19 (1992).
11. Sands, B. E. Therapy of inflammatory bowel disease. Gastroenterology 118, S68-S82 (2000).
12. Molodecky, N. A. et al. Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology 142, 46-54 (2012).
13. Rocchi, A. et al. Inflammatory bowel disease: a Canadian burden of illness review. Can. J. Gastroenterol. 26, 811-817 (2012).
14. Hammer, T., Nielsen, K. R., Munkholm, P., Burisch, J. & Lynge, E. The Faroese IBD study: incidence of inflammatory bowel diseases across 54 years of population-based data. J. Crohns Colitis 10, 934-942 (2016).
15. Benchimol, E. I. et al. Changing age demographics of inflammatory bowel disease in Ontario, Canada: a population-based cohort study of epidemiology trends. Inflamm. Bowel Dis. 20, (1761-1769 (2014).
16. Kaplan, G. G. The global burden of IBD: from 2015 to 2025. Nat. Rev. Gastroenterol. Hepatol. 12, 720-727 (2015).
17. Benchimol, E. I. et al. Increasing incidence of paediatric inflammatory bowel disease in Ontario, Canada: evidence from health administrative data. Gut 58, (1490-1497 (2009).
18. Ng, S. C. et al. Worldwide incidence and prevalence of inflammatory bowel disease in the 21st century: a systematic review of population-based studies. Lancet 390, 2769-2778 (2017).
19. Ng, S. C. et al. Incidence and phenotype of inflammatory bowel disease based on results from the Asia-Pacific Crohn's and colitis epidemiology study. Gastroenterology 145, 158-165.e2 (2013).
20. Ng, S. C. et al. Geographical variability and environmental risk factors in inflammatory bowel disease. Gut 62, 630-649 (2013).
21. Park, S. J., Kim, W. H. & Cheon, J. H. Clinical characteristics and treatment of inflammatory bowel disease: a comparison of Eastern and Western perspectives. World J. Gastroenterol. 20, 11525-11537 (2014).
22. Ng, S. C. Emerging leadership lecture: inflammatory bowel disease in Asia: emergence of a "Western" disease. J. Gastroenterol. Hepatol. 30, 440-445 (2015).
23. Tozun, N. et al. Clinical characteristics of inflammatory bowel disease in Turkey a multicenter epidemiologic survey. J. Clin. Gastroenterol. 43, 51-57 (2009).
24. Kirsner, J. B. Historical origins of current IBD concepts. World J. Gastroenterol. 7, 175-184 (2001).
25. McGranahan, G. & Satterthwaite, D. Urbanisation: Concepts and Trends (IIED, 2014).
26. Soon, S. et al. The relationship between urban environment and the inflammatory bowel diseases: a systematic review and meta-analysis. BMC Gastroenterol. 12, 51 (2012).
27. Benchimol, E. I. et al. Inflammatory bowel disease in immigrants to Canada and their children: a population-based cohort study. Am. J. Gastroenterol. 110, 553-563 (2015).
28. Ghione, S. et al. Dramatic increase in incidence of ulcerative colitis and Crohn's disease (1988-2011): a population-based study of French adolescents. Am. J. Gastroenterol. 113, 265-272 (2018).
29. Ng, W. K., Wong, S. H. & Ng, S. C. Changing epidemiological trends of inflammatory bowel disease in Asia. Intestinal Res. 14, 111-119 (2016).
30. Ng, S. C. et al. Environmental risk factors in inflammatory bowel disease: a population-based case-control study in Asia-Pacific. Gut 64, 1063-1071 (2015).
31. Sartor, R. B. & Wu, G. D. Roles for intestinal bacteria, viruses, and fungi in pathogenesis of inflammatory bowel diseases and therapeutic approaches. Gastroenterology 152, 327-339.e4 (2017).
32. Jostins, L. et al. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature 491, 119-124 (2012).
33. Liu, J. Z. & Anderson, C. A. Genetic studies of Crohn's disease: past, present and future. Best Pract. Res. Clin. Gastroenterol. 28, 373-386 (2014).
34. Liu, J. Z. et al. Association analyses identify 38 susceptibility loci for inflammatory bowel disease and highlight shared genetic risk across populations. Nat. Genet. 47, 979-986 (2015).
35. Kaplan, G. G. & Jess, T. The changing landscape of inflammatory bowel disease: East meets West. Gastroenterology 150, 24-26 (2016).
36. Ng, S. C. et al. Genetics of inflammatory bowel disease in Asia: systematic review and meta-analysis. Inflamm. Bowel Dis. 18, 1164-1176 (2012).
37. Kostic, A. D., Xavier, R. J. & Gevers, D. The microbiome in inflammatory bowel disease: current status and the future ahead. Gastroenterology 146, 1489-1499 (2014).
38. Paun, A. & Danska, J. S. Immuno-ecology: how the microbiome regulates tolerance and autoimmunity. Curr. Opin. Immunol. 37, 34-39 (2015).
39. Belkaid, Y. & Hand, T. W. Role of the microbiota in immunity and inflammation. Cell 157, 121-141 (2014).
40. Gensollen, T., Iyer, S. S., Kasper, D. L. & Blumberg, R. S. How colonization by microbiota in early life shapes the immune system. Science 352, 539-544 (2016).
41. Barreiro-de Acosta, M. et al. Emigration to western industrialized countries: a risk factor for developing inflammatory bowel disease. J. Crohns Colitis 5, 566-569 (2011).
42. Probert, C. S. J., Jayanthi, V., Pinder, D., Wicks, A. C. & Mayberry, J. F. Epidemiologic-study of ulcerative proctocolitis in Indian migrants and the indigenous population of Leicestershire. Gut 33, 687-693 (1992).
43. De Filippo, C. 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 107, 14691-14696 (2010).
44. Schnorr, S. L. et al. Gut microbiome of the Hadza hunter-gatherers. Nat. Commun. 5, 3654 (2014).
45. Yatsunenko, T. et al. Human gut microbiome viewed across age and geography. Nature 486, 222-227 (2012).
46. Martinez, I. et al. The gut microbiota of rural Papua New Guineans: composition, diversity patterns, and ecological processes. Cell Rep. 11, 527-538 (2015).
47. Zoetendal, E. G. et al. Distinct microbiotas are present in urban and rural native South Africans, and in African Americans. Gastroenterology 144, S347-S347 (2013).
48. Benno, Y. et al. Comparison of faecal microflora of elderly persons in rural and urban areas of Japan. Appl. Environ. Microbiol. 55, 1100-1105 (1989).
49. Zhang, J. et al. The diversity of intestinal microbiota of Mongolians living in Inner Mongolia, China. Benef. Microbes 4, 319-328 (2013).
50. Tyakht, A. V. et al. Human gut microbiota community structures in urban and rural populations in Russia. Nat. Commun. 4, 2469 (2013).
51. Arumugam, M. et al. Enterotypes of the human gut microbiome. Nature 473, 174-180 (2011).
52. Jahns, L., Baturin, A. & Popkin, B. M. Obesity, diet, and poverty: trends in the Russian transition to market economy. Eur. J. Clin. Nutr. 57, 1295-1302 (2003).
53. Tyakht, A. V., Alexeev, D. G., Popenko, A. S., Kostryukova, E. S. & Govorun, V. M. Rural and urban microbiota: to be or not to be? Gut Microbes 5, 351-356 (2014).
54. Blaser, M. J. The theory of disappearing microbiota and the epidemics of chronic diseases. Nat. Rev. Immunol. 17, 461-463 (2017).
55. Costello, E. K., Stagaman, K., Dethlefsen, L., Bohannan, B. J. M. & Relman, D. A. The application of ecological theory toward an understanding of the human microbiome. Science 336, 1255-1262 (2012).
56. Dethlefsen, L., McFall-Ngai, M. & Relman, D. A. An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature 449, 811-818 (2007).
57. Leach, J. Please pass the microbes. Nature 504, 33-33 (2013).
58. Mihaljevic, J. R. Linking metacommunity theory and symbiont evolutionary ecology. Trends Ecol. Evol. 27, 323-329 (2012).
59. Nemergut, D. R. et al. Patterns and processes of microbial community assembly. Microbiol. Mol. Biol. Rev. 77, 342-356 (2013).
60. Chase, J. M., Kraft, N. J. B., Smith, K. G., Vellend, M. & Inouye, B. D. Using null models to disentangle variation in community dissimilarity from variation in alpha-diversity. Ecosphere 2, 24 (2011).
61. Stegen, J. C., Lin, X. J., Konopka, A. E. & Fredrickson, J. K. Stochastic and deterministic assembly processes in subsurface microbial communities. ISME J. 6, 1653-1664 (2012).
62. Browne, H. P., Neville, B. A., Forster, S. C. & Lawley, T. D. Transmission of the gut microbiota: spreading of health. Nat. Rev. Microbiol. 15, 531-543 (2017).
63. Clemente, J. C. et al. The microbiome of uncontacted Amerindians. Sci. Adv. 1, e1500183 (2015).
64. Bager, P., Simonsen, J., Nielsen, N. M. & Frisch, M. Cesarean section and offspring's risk of inflammatory bowel disease: a national cohort study. Inflamm. Bowel Dis. 18, 857-862 (2012).
65. Li, Y. et al. Cesarean delivery and risk of inflammatory bowel disease: a systematic review and meta-analysis. Scand. J. Gastroenterol. 49, 834-844 (2014).
66. Klement, E., Cohen, R. V., Boxman, J., Joseph, A. & Reif, S. Breastfeeding and risk of inflammatory bowel disease: a systematic review with meta-analysis(1-3). Am. J. Clin. Nutr. 80, 1342-1352 (2004).
67. Abegunde, A. T., Muhammad, B. H., Bhatti, O. & Ali, T. Environmental risk factors for inflammatory bowel diseases: evidence based literature review. World J. Gastroenterol. 22, 6296-6317 (2016).
68. Malekzadeh, F. et al. Crohn's disease and early exposure to domestic refrigeration. PLoS ONE 4, e4288 (2009).
69. Forbes, A. & Kalantzis, T. Crohn's disease: the cold chain hypothesis. Int. J. Colorectal Dis. 21, 399-401 (2006).
70. Korzenik, J. R. Past and current theories of etiology of IBD - toothpaste, worms, and refrigerators. J. Clin. Gastroenterol. 39, S59-S65 (2005).
71. Yin, W. Y. et al. Inverse association between poor oral health and inflammatory bowel diseases. Clin. Gastroenterol. Hepatol. 15, 525-531 (2017).
72. Atarashi, K. et al. Ectopic colonization of oral bacteria in the intestine drives TH1 cell induction and inflammation. Science 358, 359-365 (2017).
73. Sullivan, S. N. Hypothesis revisited: toothpaste and the cause of Crohn's disease. Lancet 336, 1096-1097 (1990).
74. Albenberg, L. G. & Wu, G. D. Diet and the intestinal microbiome: associations, functions, and implications for health and disease. Gastroenterology 146, 1564-1572 (2014).
75. Ley, R. E. et al. Evolution of mammals and their gut microbes. Science 320, 1647-1651 (2008).
76. Carrillo-Larco, R. M. et al. Obesity risk in rural, urban and rural-to-urban migrants: prospective results of the PERU MIGRANT study. Int. J. Obes. 40, 181-185 (2016).
77. Conlon, M. A. & Bird, A. R. The impact of diet and lifestyle on gut microbiota and human health. Nutrients 7, 17-44 (2015).
78. Agus, A. et al. Western diet induces a shift in microbiota composition enhancing susceptibility to Adherent-Invasive E. coli infection and intestinal inflammation. Sci. Rep. 6, 19032 (2016).
79. Turnbaugh, P. J., Baeckhed, F., Fulton, L. & Gordon, J. I. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 3, 213-223 (2008).
80. Christ, A. et al. Western diet triggers NLRP3-dependent innate immune reprogramming. Cell 172, 162-175.e14 (2018).
81. Statovci, D., Aguilera, M., MacSharry, J. & Melgar, S. The impact of Western diet and nutrients on the microbiota and immune response at mucosal interfaces. Front. Immunol. 8, 838 (2017).
82. Wu, G. D. et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 334, 105-108 (2011).
83. Muegge, B. D. et al. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332, 970-974 (2011).
84. David, L. A. et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505, 559-563 (2014).
85. Obregon-Tito, A. J. et al. Subsistence strategies in traditional societies distinguish gut microbiomes. Nat. Commun. 6, 6505 (2015).
86. Rigoni, R. et al. Intestinal microbiota sustains inflammation and autoimmunity induced by hypomorphic RAG defects. J. Exp. Med. 213, 355-375 (2016).
87. Negroni, A. et al. Characterization of adherent-invasive Escherichia coli isolated from pediatric patients with inflammatory bowel disease. Inflamm. Bowel Dis. 18, 913-924 (2012).
88. Munyaka, P. M., Sepehri, S., Ghia, J. E. & Khafipour, E. Carrageenan gum and Adherent Invasive Escherichia coli in a piglet model of inflammatory bowel disease: impact on intestinal mucosa-associated microbiota. Front. Microbiol 7, 462 (2016).
89. Rolhion, N. & Darfeuille-Michaud, A. Adherent-invasive Escherichia coli in inflammatory bowel disease. Inflamm. Bowel Dis. 13, 1277-1283 (2007).
90. Simpson, K., Dogan, B., Bitar, P. P., Schukken, Y. & Stanhope, M. Comparative genomics of adherent-invasive Escherichia coli (AIEC) associated with Crohn's disease. Inflamm. Bowel Dis. 17, S1 (2011).
91. Shivashankar, R., Beauvais, J. C. & Lewis, J. D. The relationship of regional diets with global incidence rates of inflammatory bowel disease. Gastroenterology 152, S975-S976 (2017).
92. El Kaoutari, A., Armougom, F., Gordon, J. I., Raoult, D. & Henrissat, B. The abundance and variety of carbohydrate-active enzymes in the human gut microbiota. Nat. Rev. Microbiol. 11, 497-504 (2013).
93. Sonnenburg, E. D. et al. Diet-induced extinctions in the gut microbiota compound over generations. Nature 529, 212-U208 (2016).
94. Griffin, N. W. et al. Prior dietary practices and connections to a human gut microbial metacommunity alter responses to diet interventions. Cell Host Microbe 21, 84-96 (2017).
95. Desai, M. S. et al. A dietary fiber-deprived gut microbiota degrades the colonic mucus barrier and enhances pathogen susceptibility. Cell 167, 1339-1353.e21 (2016).
96. Schroeder, B. O. et al. Bifidobacteria or fiber protects against diet-induced microbiota-mediated colonic mucus deterioration. Cell Host Microbe 23, 27-40.e7 (2017).
97. Zou, J. et al. Fiber-mediated nourishment of gut microbiota protects against diet-induced obesity by restoring IL-22-mediated colonic health. Cell Host Microbe 23, 41-53.e4 (2017).
98. Cani, P. D. Dietary emulsifiers-sweepers of the gut lining? Nat. Rev. Endocrinol. 11, 319-320 (2015).
99. Chassaing, B. et al. Dietary emulsifiers impact the mouse gut microbiota promoting colitis and metabolic syndrome. Nature 519, 92-96 (2015).
100. Chassaing, B., Van de Wiele, T., De Bodt, J., Marzorati, M. & Gewirtz, A. T. Dietary emulsifiers directly alter human microbiota composition and gene expression ex vivo potentiating intestinal inflammation. Gut 66, 1414-1427 (2017).
101. Suez, J. et al. Artificial sweeteners induce glucose intolerance by altering the gut microbiota. Nature 514, 181-186 (2014).
102. Ruiz, P. A. et al. Titanium dioxide nanoparticles exacerbate DSS-induced colitis: role of the NLRP3 inflammasome. Gut 66, 1216-1224 (2017).
103. Sonnenburg, E. D. & Sonnenburg, J. L. Starving our microbial self: the deleterious consequences of a diet deficient in microbiota-accessible carbohydrates. Cell. Metab. 20, 779-786 (2014).
104. Galvez, J., Rodriguez-Cabezas, M. E. & Zarzuelo, A. Effects of dietary fiber on inflammatory bowel disease. Mol. Nutr. Food Res. 49, 601-608 (2005).
105. Pituch-Zdanowska, A., Banaszkiewicz, A. & Albrecht, P. The role of dietary fibre in inflammatory bowel disease. Przeglad Gastroenterol. 10, 135 (2015).
106. Chiba, M., Tsuji, T., Nakane, K. & Komatsu, M. High amount of dietary fiber not harmful but favorable for Crohn disease. Perm. J. 19, 58 (2015).
107. Gong, P. et al. Urbanisation and health in China. Lancet 379, 843-852 (2012).
108. Wang, H. X. et al. Antibiotics detected in urines and adipogenesis in school children. Environ. Int. 89-90, 204-211 (2016).
109. Jernberg, C., Lofmark, S., Edlund, C. & Jansson, J. K. Long-term impacts of antibiotic exposure on the human intestinal microbiota. Microbiology 156, 3216-3223 (2010).
110. Blaser, M. J. Antibiotic use and its consequences for the normal microbiome. Science 352, 544-545 (2016).
111. Dethlefsen, L., Huse, S., Sogin, M. L. & Relman, D. A. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol. 6, 2383-2400 (2008).
112. Dethlefsen, L. & Relman, D. A. Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proc. Natl Acad. Sci. USA 108, 4554-4561 (2011).
113. De La Cochetiere, M. F. et al. Resilience of the dominant human fecal microbiota upon short-course antibiotic challenge. J. Clin. Microbiol. 43, 5588-5592 (2005).
114. Jernberg, C., Lofmark, S., Edlund, C. & Jansson, J. K. Long-term ecological impacts of antibiotic administration on the human intestinal microbiota. ISME J. 7, 456-456 (2013).
115. Molodecky, N. A. & Kaplan, G. G. Environmental risk factors for inflammatory bowel disease. Gastroenterol. Hepatol. 6, 339 (2010).
116. Ko, Y. et al. Inflammatory bowel disease environmental risk factors: a population-based case-control study of Middle Eastern migration to Australia. Clin. Gastroenterol. Hepatol. 13, 1453-1463.e1 (2015).
117. Leong, R. W., Mitrev, N. & Ko, Y. N. Hygiene hypothesis: is the evidence the same all over the world? Dig. Dis. 34, 35-42 (2016).
118. Francino, M. P. Early development of the gut microbiota and immune health. Pathogens 3, 769-790 (2014).
119. Bokulich, N. A. et al. Antibiotics, birth mode, and diet shape microbiome maturation during early life. Sci. Transl Med. 8, 343ra82 (2016).
120. Cox, L. M. et al. Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences. Cell 158, 705-721 (2014).
121. Turta, O. & Rautava, S. Antibiotics, obesity and the link to microbes - what are we doing to our children? BMC Med. 14, 57 (2016).
122. Pihl, A. F. et al. The role of the gut microbiota in childhood obesity. Childhood Obes. 12, 292-299 (2016).
123. Candon, S. et al. Antibiotics in early life alter the gut microbiome and increase disease incidence in a spontaneous mouse model of autoimmune insulin-dependent diabetes. PLoS ONE 10, e0125448 (2015).
124. + T cells during intestinal inflammation. J. Leukoc. Biol. 101, 893-900 (2017).
125. Schulfer, A. & Blaser, M. J. Risks of antibiotic exposures early in life on the developing microbiome. PLoS Pathog. 11, e1004903 (2015).
126. Yamamoto-Hanada, K., Yang, L. M., Narita, M., Saito, H. & Ohya, Y. Influence of antibiotic use in early childhood on asthma and allergic diseases at age 5. Ann. Allergy Asthma Immunol. 119, 54-58 (2017).
127. Ramakrishna, B. S. et al. Hygiene factors in India and the US in early childhood influence the subsequent development of Crohn's disease but not ulcerative colitis: a large case controlled study in two countries. Gastroenterology 142, S789 (2012).
128. Card, T., Logan, R. F. A., Rodrigues, L. C. & Wheeler, J. G. Antibiotic use and the development of Crohn's disease. Gut 53, 246-250 (2004).
129. Hildebrand, H., Malmborg, P., Askling, J., Ekbom, A. & Montgomery, S. M. Early-life exposures associated with antibiotic use and risk of subsequent Crohn's disease. Scand. J. Gastroenterol. 43, 961-966 (2008).
130. Mai, V. et al. Distortions in development of intestinal microbiota associated with late onset sepsis in preterm infants. PLoS ONE 8, e52876 (2013).
131. Mai, V. et al. Fecal microbiota in premature infants prior to necrotizing enterocolitis. PLoS ONE 6, e20647 (2011).
132. Deshpande, G., Rao, S., Patole, S. & Bulsara, M. Updated meta-analysis of probiotics for preventing necrotizing enterocolitis in preterm neonates. Pediatrics 125, 921-930 (2010).
133. Kenyon, S. L., Taylor, D. J., Tarnow-Mordi, W. & Grp, O. C. Broad-spectrum antibiotics for preterm, prelabour rupture of fetal membranes: the ORACLE I randomised trial. Lancet 357, 979-988 (2001).
134. Bisgaard, H. 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. 128, 646-U318 (2011).
135. Abrahamsson, T. R. et al. Low diversity of the gut microbiota in infants with atopic eczema. J. Allergy Clin. Immunol. 129, 434-U244 (2012).
136. McKeever, T. M. et al. Early exposure to infections and antibiotics and the incidence of allergic disease: A birth cohort study with the West Midlands General Practice Research Database. J. Allergy Clin. Immunol. 109, 43-50 (2002).
137. Kozyrskyj, A. L., Ernst, P. & Becker, A. B. Increased risk of childhood asthma from antibiotic use in early life. Chest 131, 1753-1759 (2007).
138. Risnes, K. R., Belanger, K., Murk, W. & Bracken, M. B. Antibiotic exposure by 6 months and asthma and allergy at 6 years: findings in a cohort of 1,401 US children. Am. J. Epidemiol. 173, 310-318 (2011).
139. Samet, J. M. & Gruskin, S. Air pollution, health, and human rights. Lancet. Respir. Med. 3, 98 (2015).
140. Franklin, B. A., Brook, R. & Pope, C. A. Air pollution and cardiovascular disease. Curr. Problems Cardiol. 40, 207-238 (2015).
141. Kaplan, G. G. et al. The inflammatory bowel diseases and ambient air pollution: a novel association. Am. J. Gastroenterol. 105, 2412-2419 (2010).
142. Ananthakrishnan, A. N., McGinley, E. L., Binion, D. G. & Saeian, K. Ambient air pollution correlates with hospitalizations for inflammatory bowel disease: an ecologic analysis. Inflamm. Bowel Dis. 17, 1138-1145 (2011).
143. To, N., Gracie, D. J. & Ford, A. C. The importance of smoking cessation in improving disease course in Crohn's disease. Am. J. Gastroenterol. 111, 1198-1198 (2016).
144. Nunes, T. et al. Impact of smoking cessation on the clinical course of Crohn's disease under current therapeutic algorithms: a multicenter prospective study. Am. J. Gastroenterol. 111, 411-419 (2016).
145. Johnson, G. J., Cosnes, J. & Mansfield, J. C. Review article: Smoking cessation as primary therapy to modify the course of Crohn's disease. Aliment. Pharmacol. Ther. 21, 921-931 (2005).
146. Benjamin, J. L. et al. Smokers with active Crohn's disease have a clinically relevant dysbiosis of the gastrointestinal microbiota. Inflamm. Bowel Dis. 18, 1092-1100 (2012).
147. Van de Wiele, T. et al. Arsenic metabolism by human gut microbiota upon in vitro digestion of contaminated soils. Environ. Health Persp. 118, 1004 (2010).
148. Van de Wiele, T. et al. Human colon microbiota transform polycyclic aromatic hydrocarbons to estrogenic metabolites. Environ. Health Persp. 113, 6-10 (2005).
149. Sawyer, K., Mundandhara, S., Ghio, A. J. & Madden, M. C. The effects of ambient particulate matter on human alveolar macrophage oxidative and inflammatory responses. J. Toxicol. Environ. Health A 73, 41-57 (2010).
150. van Eeden, S. F. et al. Cytokines involved in the systemic inflammatory response induced by exposure to particulate Matter air pollutants (PM10). Am. J. Respir. Crit. Care Med. 164, 826-830 (2001).
151. Rickert, D. E., Butterworth, B. E. & Popp, J. A. Dinitrotoluene - acute toxicity, oncogenicity, genotoxicity, and metabolism. CRC Crit. Rev. Toxicol. 13, 217-234 (1984).
152. Rickert, D. E., Long, R. M., Krakowka, S. & Dent, J. G. Metabolism and excretion of 2,4-dinitrotoluene-C-14 in conventional and axenic Fischer-344 rats. Toxicol. Appl. Pharmacol. 59, 574-579 (1981).
153. Yim, Y. J., Seo, J., Kang, S. I., Ahn, J. H. & Hur, H. G. Reductive dechlorination of methoxychlor and DDT by human intestinal bacterium Eubacterium limosum under anaerobic conditions. Arch. Environ. Contamin. Toxicol. 54, 406-411 (2008).
154. Joly, C. et al. Impact of chronic exposure to low doses of chlorpyrifos on the intestinal microbiota in the Simulator of the Human Intestinal Microbial Ecosystem (SHIME (R)) and in the rat. Environ. Sci. Poll. Res. 20, 2726-2734 (2013).
155. Fazeli, M., Hassanzadeh, P. & Alaei, S. Cadmium chloride exhibits a profound toxic effect on bacterial microflora of the mice gastrointestinal tract. Hum. Exp. Toxicol. 30, 152-159 (2011).
156. Breton, J. et al. Ecotoxicology inside the gut: impact of heavy metals on the mouse microbiome. BMC Pharmacol. Toxicol. 14, 62 (2013).
157. Lu, K. et al. Arsenic exposure perturbs the gut microbiome and its metabolic profile in mice: an integrated metagenomics and metabolomics analysis. Environ. Health Persp. 122, 284-291 (2014).
158. Xu, H. Y., Heinze, T. M., Chen, S. W., Cerniglia, C. E. & Chen, H. Z. Anaerobic metabolism of 1-amino-2-naphthol-based azo dyes (Sudan dyes) by human intestinal microflora. Appl. Environ. Microbiol. 73, 7759-7762 (2007).
159. Zheng, X. et al. Melamine-induced renal toxicity is mediated by the gut microbiota. Sci. Transl Med. 5, 172ra22 (2013).
160. Kish, L. et al. Environmental particulate matter induces murine intestinal inflammatory responses and alters the gut microbiome. PLoS ONE 8, e62220 (2013).
161. Nicholson, J. K. et al. Host-gut microbiota metabolic interactions. Science 336, 1262-1267 (2012).
162. Choi, J. J. et al. Exercise attenuates PCB-induced changes in the mouse gut microbiome. Environ. Health Persp. 121, 725-730 (2013).
163. Lepage, P. et al. Twin study indicates loss of interaction between microbiota and mucosa of patients with ulcerative colitis. Gastroenterology 141, 227-236 (2011).
164. Russell, S. L. & Finlay, B. B. The impact of gut microbes in allergic diseases. Curr. Opin. Gastroenterol. 28, 563-569 (2012).
165. Gascon, M., Morales, E., Sunyer, J. & Vrijheid, M. Effects of persistent organic pollutants on the developing respiratory and immune systems: a systematic review. Environ. Int. 52, 51-65 (2013).
166. Menard, S. et al. Food intolerance at adulthood after perinatal exposure to the endocrine disruptor bisphenol A. FASEB J. 28, 4893-4900 (2014).
167. Belles-Isles, M., Ayotte, P., Dewailly, E., Weber, J. P. & Roy, R. Cord blood lymphocyte functions in newborns from a remote maritime population exposed to organochlorines and methylmercury. J. Toxicol. Environ. Health A 65, 165-182 (2002).
168. MacGillivray, D. M. & Kollmann, T. R. The role of environmental factors in modulating immune responses in early life. Front. Immunol. 5, 434 (2014).
169. de Chambrun, G. P. et al. Aluminum enhances inflammation and decreases mucosal healing in experimental colitis in mice. Mucosal Immunol. 7, 589-601 (2014).
170. Benchimol, E. I. et al. Rural and urban residence during early life is associated with a lower risk of inflammatory bowel disease: a population-based inception and birth cohort study. Am. J. Gastroenterol. 112, 1412-1422 (2017).
171. Geuking, M. B. et al. Intestinal bacterial colonization induces mutualistic regulatory T cell responses. Immunity 34, 794-806 (2011).
172. Rakoff-Nahoum, S. & Medzhitov, R. Innate immune recognition of the indigenous microbial flora. Mucosal Immunol. 1, S10-S14 (2008).
173. Crabbe, P. A., Nash, D. R., Bazin, H., Eyssen, H. & Heremans, J. F. Immunohistochemical observations on lymphoid tissues from conventional and germ-free mice. Lab. Invest. 22, 448-457 (1970).
174. El Aidy, S., Hooiveld, G., Tremaroli, V., Bäckhed, F. & Kleerebezem, M. The gut microbiota and mucosal homeostasis: colonized at birth or at adulthood, does it matter? Gut Microbes 4, 118-124 (2013).
175. Markle, J. G. M. et al. Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science 339, 1084-1088 (2013).
176. Stefka, A. T. et al. Commensal bacteria protect against food allergen sensitization. Proc. Natl Acad. Sci. USA 111, 13145-13150 (2014).
177. Tumwine, J. K. et al. Sanitation and hygiene in urban and rural households in East Africa. Int. J. Environ. Health Res. 13, 107-115 (2003).
178. Chaudhuri, S. & Roy, M. Rural-urban spatial inequality in water and sanitation facilities in India: a cross-sectional study from household to national level. Appl. Geogr. 85, 27-38 (2017).
179. Vatanen, T. et al. Variation in microbiome LPS immunogenicity contributes to autoimmunity in humans. Cell 165, 842-853 (2016).
180. Bach, J. F. Mechanisms of disease: The effect of infections on susceptibility to autoimmune and allergic diseases. N. Engl. J. Med. 347, 911-920 (2002).
181. von Mutius, E. & Vercelli, D. Farm living: effects on childhood asthma and allergy. Nat. Rev. Immunol. 10, 861-868 (2010).
182. de Aguero, M. G. et al. The maternal microbiota drives early postnatal innate immune development. Science 351, 1296-1301 (2016).
183. Macpherson, A. J., de Agüero, M. G. & Ganal-Vonarburg, S. C. How nutrition and the maternal microbiota shape the neonatal immune system. Nat. Rev. Immunol. 17, 508-517 (2017).
184. Grindstaff, J. L., Brodie, E. D. & Ketterson, E. D. Immune function across generations: integrating mechanism and evolutionary process in maternal antibody transmission. Proc. R. Soc. B Biol Sci. 270, 2309-2319 (2003).
185. van de Pavert, S. A. et al. Maternal retinoids control type 3 innate lymphoid cells and set the offspring immunity. Nature 508, 123-127 (2014).
186. Hu, J. et al. Infants born to mothers with inflammatory bowel disease exhibit distinct microbiome features that persist up to 3 months of life. Gastroenterology 152, S193 (2017).
187. Zeissig, S. & Blumberg, R. S. Commensal microbial regulation of natural killer T cells at the frontiers of the mucosal immune system. FEBS Lett. 588, 4188-4194 (2014).
188. Olszak, T. et al. Microbial exposure during early life has persistent effects on natural killer T cell function. Science 336, 489-493 (2012).
189. An, D. D. et al. Sphingolipids from a symbiotic microbe regulate homeostasis of host intestinal natural killer T cells. Cell 156, 123-133 (2014).
190. Chassin, C. et al. miR-146a mediates protective innate immune tolerance in the neonate intestine. Cell Host Microbe 8, 358-368 (2010).
191. Stockinger, S., Hornef, M. W. & Chassin, C. Establishment of intestinal homeostasis during the neonatal period. Cell. Mol. Life Sci. 68, 3699-3712 (2011).
192. Fendrick, A. M., Monto, A. S., Nightengale, B. & Sarnes, M. The economic burden of non-influenza-related viral respiratory tract infection in the United States. Arch. Intern. Med. 163, 487-494 (2003).
193. Kosek, M., Bern, C. & Guerrant, R. L. The global burden of diarrhoeal disease, as estimated from studies published between 1992 and 2000. Bull. World Health Organiz. 81, 197-204 (2003).
194. Vernacchio, L. et al. Diarrhea in American infants and young children in the community setting: incidence, clinical presentation and microbiology. Pediatr. Infect. Dis. J. 25, 2-7 (2006).
195. da Fonseca, D. M. et al. Microbiota-dependent sequelae of acute infection compromise tissue-specific immunity. Cell 163, 354-366 (2015).
196. Randolph, G. J. et al. Lymphoid aggregates remodel lymphatic collecting vessels that serve mesenteric lymph nodes in Crohn disease. Am. J. Pathol. 186, 3066-3073 (2016).
197. Virgin, H. W. The virome in mammalian physiology and disease. Cell 157, 142-150 (2014).
198. Ogilvie, L. A. & Jones, B. V. The human gut virome: a multifaceted majority. Front. Microbiol. 6, 918 (2015).
199. Lecuit, M. & Eloit, M. The human virome: new tools and concepts. Trends Microbiol. 21, 510-515 (2013).
200. Minot, S. et al. Rapid evolution of the human gut virome. Proc. Natl Acad. Sci. USA 110, 12450-12455 (2013).
201. Minot, S., Grunberg, S., Wu, G. D., Lewis, J. D. & Bushman, F. D. Hypervariable loci in the human gut virome. Proc. Natl Acad. Sci. USA 109, 3962-3966 (2012).
202. Reyes, A. et al. Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature 466, 334-338 (2010).
203. Waller, A. S. et al. Classification and quantification of bacteriophage taxa in human gut metagenomes. ISME J. 8, 1391-1402 (2014).
204. Norman, J. M. et al. Disease-specific alterations in the enteric virome in inflammatory bowel disease. Cell 160, 447-460 (2015).
205. Perez-Brocal, V. et al. Study of the viral and microbial communities associated with Crohn's disease: a metagenomic approach. Clin. Transl Gastroenterol. 4, e36 (2013).
206. Wagner, J. et al. Bacteriophages in gut samples from pediatric Crohn's disease patients: metagenomic analysis using 454 Pyrosequencing. Inflamm. Bowel Dis. 19, 1598-1608 (2013).
207. Lepage, P. et al. Dysbiosis in inflammatory bowel disease: a role for bacteriophages? Gut 57, 424-425 (2008).
208. Kim, M. S. & Bae, J. W. Spatial disturbances in altered mucosal and luminal gut viromes of diet-induced obese mice. Environ. Microbiol. 18, 1498-1510 (2016).
209. Kernbauer, E., Ding, Y. & Cadwell, K. An enteric virus can replace the beneficial function of commensal bacteria. Nature 516, 94-U223 (2014).
210. Barr, J. J. et al. Bacteriophage adhering to mucus provide a non-host-derived immunity. Proc. Natl Acad. Sci. USA 110, 10771-10776 (2013).
211. Barr, J. et al. Bacteriophage adhered to mucus provide a novel mucosal immune system [abstract]. J. Immunol. 190 (Suppl), P3166 (2013).
212. Sokol, H. et al. Fungal microbiota dysbiosis in IBD. Gut 66, 1039-1048 (2017).
213. Richard, M. L., Lamas, B., Liguori, G., Hoffmann, T. W. & Sokol, H. Gut fungal microbiota: the yin and yang of inflammatory bowel disease. Inflamm. Bowel Dis. 21, 656-665 (2015).
214. Jawhara, S. et al. Colonization of mice by Candida albicans is promoted by chemically induced colitis and augments inflammatory responses through galectin-3. J. Infect. Dis. 197, 972-980 (2008).
215. Chen, X. H. et al. Probiotic yeast inhibits VEGFR signaling and angiogenesis in intestinal inflammation. PLoS ONE 8, e64227 (2013).
216. Jawhara, S. & Poulain, D. Saccharomyces boulardii decreases inflammation and intestinal colonization by Candida albicans in a mouse model of chemically-induced colitis. Med. Mycol. 45, 691-700 (2007).
217. Zwolinska-Wcislo, M. et al. Effect of Candida colonization on human ulcerative colitis and the healing of inflammatory changes of the colon in the experimental model of colitis ulcerosa. J. Physiol. Pharmacol. 60, 107-118 (2009).
218. Wheeler, M. L. et al. Immunological consequences of intestinal fungal dysbiosis. Cell Host Microbe 19, 865-873 (2016).
219. Iliev, I. D. et al. Interactions between commensal fungi and the C-type lectin receptor Dectin-1 influence colitis. Science 336, 1314-1317 (2012).
220. Sokol, H. et al. Card9 mediates intestinal epithelial cell restitution, T-helper 17 responses, and control of bacterial infection in mice. Gastroenterology 145, 591-601 (2013).
221. Cao, Z. F. et al. Ubiquitin ligase TRIM62 regulates CARD9-mediated anti-fungal immunity and intestinal inflammation. Immunity 43, 715-726 (2015).
222. Angebault, C. et al. Candida albicans is not always the preferential yeast colonizing humans: a study in Wayampi Amerindians. J. Infect. Dis. 208, 1705-1716 (2013).
223. Newbound, M., Mccarthy, M. A. & Lebel, T. Fungi and the urban environment: a review. Landscape Urban Plann. 96, 138-145 (2010).
224. Arnolds, E. Decline of ectomycorrhizal fungi in europe. Agric. Ecosyst. Environ. 35, 209-244 (1991).
225. O'gorman, C. M. & Fuller, H. T. Prevalence of culturable airborne spores of selected allergenic and pathogenic fungi in outdoor air. Atmospher. Environ. 42, 4355-4368 (2008).
226. Kurup, V. P., Shen, H. D. & Banerjee, B. Respiratory fungal allergy. Microbes Infect. 2, 1101-1110 (2000).
227. Conti, M. E. & Cecchetti, G. Biological monitoring: lichens as bioindicators of air pollution assessment - a review. Environ. Poll. 114, 471-492 (2001).
228. Joshi, S. R. Influence of roadside pollution on the phylloplane microbial community of Alnus nepalensis (Betulaceae). Revista De Biol. Trop. 56, 1521-1529 (2008).
229. Pasanen, A. L., Kalliokoski, P., Pasanen, P., Salmi, T. & Tossavainen, A. Fungi carried from farmers work into farm homes. Am. Industrial Hyg. Assoc. J. 50, 631-633 (1989).
230. Oliveira, M. et al. Outdoor allergenic fungal spores: comparison between an urban and a rural area in northern Portugal. J. Invest. Allergol. Clin. Immunol. 20, 117-128 (2010).
231. Kasprzyk, I. & Worek, M. Airborne fungal spores in urban and rural environments in Poland. Aerobiologia 22, 169-176 (2006).
232. Weinstock, J. V. & Elliott, D. E. Helminths and the IBD Hygiene Hypothesis. Inflamm. Bowel Dis. 15, 128-133 (2009).
233. Weinstock, J. V. et al. The possible link between de-worming and the emergence of immunological disease. J. Lab. Clin. Med. 139, 334-338 (2002).
234. Ramanan, D. et al. Helminth infection promotes colonization resistance via type 2 immunity. Science 352, 608-612 (2016).
235. Yang, X. D. et al. Excretory/secretory products from Trichinella spiralis adult worms ameliorate DSS-induced colitis in mice. PLoS One 9, e96454 (2014).
236. Motomura, Y. et al. Helminth antigen-based strategy to ameliorate inflammation in an experimental model of colitis. Clin. Exp. Immunol. 155, 88-95 (2009).
237. Ruyssers, N. E. et al. Therapeutic potential of helminth soluble proteins in TNBS-induced colitis in mice. Inflamm. Bowel Dis. 15, 491-500 (2009).
238. + T cells are associated with therapeutic Trichuris trichiura infection in an ulcerative colitis patient. Sci. Transl Med. 2, 60ra88 (2010).
239. Elliott, D. E. et al. Colonization with Heligmosomoides polygyrus suppresses mucosal IL-17 production. J. Immunol. 181, 2414-2419 (2008).
240. + T cells enhancing their capacity to prevent colitis. J. Immunol. 191, 1927-1934 (2013).
241. Lee, S. C. et al. Helminth colonization is associated with increased diversity of the gut microbiota. PLoS Negl. Trop. Dis. 8, e2880 (2014).
242. Stepek, G. et al. Expression of the filarial nematode phosphorylcholine-containing glycoprotein, ES62, is stage specific. Parasitology 125, 155-164 (2002).
243. Harnett, W. & Harnett, M. M. Filarial nematode secreted product ES-62 is an anti-inflammatory agent: therapeutic potential of small molecule derivatives and ES-62 peptide mimetics. Clin. Exp. Pharmacol. Physiol. 33, 511-518 (2006).
244. Helmby, H. Human helminth therapy to treat inflammatory disorders- where do we stand? BMC Immunol. 16, 12 (2015).
245. Summers, R. W., Elliott, D. E., Urban, J. F., Thompson, R. A. & Weinstock, J. V. Trichuris suis therapy for active ulcerative colitis: a randomized controlled trial. Gastroenterology 128, 825-832 (2005).