Skip to main content

Advertisement

Log in

Ambient Air Pollution and Pediatric Inflammatory Bowel Diseases: An Updated Scoping Review

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

Abstract

To review and discuss recent findings on the associations between pediatric/early-life exposures to ambient air pollution and the risk of pediatric-onset inflammatory bowel diseases (IBD). A scoping review was conducted using the Peters Micah et al. framework. We searched, selected, extracted, and reviewed information from published peer-reviewed papers from three bibliographic databases, chosen to cover a broad range of disciplines. Limits on date (last decade), language, and subject were placed on the database search. The search identified 109 papers from 2010 to June 2021. After screening, we identified nine articles with data on air pollution as a risk factor for IBD, but only four epidemiologic studies directly investigated the association between air pollution and IBD development in children and young adults. These four papers show that air pollution components have different associations with pediatric IBD (pIBD) incidence. Consequently, sulfur dioxide (SO2), nitrogen dioxide (NO2), and the oxidant capacity of air pollution (Ox) were positively associated with pIBD incidence, whereas the association effects of particulate matter (PM) and ozone (O3) exposures were not clear. Despite good scientific rationale and some studies, the evidence on the role that air pollution has in IBD development is limited, highlighting the need for further investigation. Future studies should include the epidemiology of air pollutants and its sources, identifying and understanding mechanisms linking air pollution and pIBD, and identifying signatures of biological responses to air pollutants.

Graphical Abstract

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.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Ng SC, Shi HY, Hamidi N et al. Worldwide incidence and prevalence of inflammatory bowel disease in the 21st century: a systematic review of population-based studies. Lancet. 2017;390:2769–2778.

    Article  PubMed  Google Scholar 

  2. Coward S, Clement F, Benchimol EI et al. Past and future burden of inflammatory bowel diseases based on modeling of population-based data. Gastroenterology. 2019;156:1345–1353.

    Article  PubMed  Google Scholar 

  3. Kuenzig ME, Fung SG, Marderfeld L et al. Twenty-first century trends in the global epidemiology of pediatric-onset inflammatory bowel disease: systematic review. Gastroenterology. 2022;162:1147–1159.

    Article  PubMed  Google Scholar 

  4. Benchimol EI, Bernstein CN, Bitton A et al. Trends in epidemiology of pediatric inflammatory bowel disease in Canada: distributed network analysis of multiple population-based provincial health administrative databases. Am J Gastroenterol. 2017;112:1120–1134.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Rosen MJ, Dhawan A, Saeed SA. Inflammatory bowel disease in children and adolescents. JAMA Pediatr. 2015;169:1053–1060.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Aujnarain A, Mack DR, Benchimol EI. The role of the environment in the development of pediatric inflammatory bowel disease. Curr Gastroenterol Rep. 2013;15:326.

    Article  PubMed  Google Scholar 

  7. Strisciuglio C, Giugliano F, Martinelli M et al. Impact of environmental and familial factors in a cohort of pediatric patients with inflammatory bowel disease. J Pediatr Gastroenterol Nutr. 2017;64:569–574.

    Article  PubMed  Google Scholar 

  8. Kugathasan S, Judd RH, Hoffmann RG et al. Epidemiologic and clinical characteristics of children with newly diagnosed inflammatory bowel disease in Wisconsin: a statewide population-based study. J Pediatr. 2003;143:525–531.

    Article  PubMed  Google Scholar 

  9. Molodecky NA, Soon IS, Rabi DM et al. Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology. 2012;142:46–54.

    Article  PubMed  Google Scholar 

  10. Rogler G, Vavricka S. Exposome in IBD: recent insights in environmental factors that influence the onset and course of IBD. Inflamm Bowel Dis. 2015;21:400–408.

    Article  PubMed  Google Scholar 

  11. Renz H, Holt PG, Inouye M, Logan AC, Prescott SL, Sly PD. An exposome perspective: Early-life events and immune development in a changing world. J Allergy Clin Immunol. 2017;140:24–40.

    Article  PubMed  Google Scholar 

  12. Ritz SA. Air pollution as a potential contributor to the ‘epidemic’ of autoimmune disease. Med Hypotheses. 2010;74:110–117.

    Article  CAS  PubMed  Google Scholar 

  13. Kish L, Hotte N, Kaplan GG et al. Environmental particulate matter induces murine intestinal inflammatory responses and alters the gut microbiome. PLoS ONE. 2013;8:e62220.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Ananthakrishnan AN, Bernstein CN, Iliopoulos D et al. Environmental triggers in IBD: a review of progress and evidence. Nat Rev Gastroenterol Hepatol. 2018;15:39–49.

    Article  PubMed  Google Scholar 

  15. Örtqvist AK, Lundholm C, Halfvarson J, Ludvigsson JF, Almqvist C. Fetal and early life antibiotics exposure and very early onset inflammatory bowel disease: a population-based study. Gut. 2019;68:218–225.

    Article  PubMed  CAS  Google Scholar 

  16. Chua HH, Chou HC, Tung YL et al. Intestinal dysbiosis featuring abundance of Ruminococcus gnavus associates with allergic diseases in infants. Gastroenterology. 2018;154:154–167.

    Article  PubMed  Google Scholar 

  17. Yassour M, Jason E, Hogstrom LJ et al. Strain-level analysis of mother-to-child bacterial transmission during the first few months of life. Cell Host Microbe. 2018;24:146–154.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Tamburini S, Shen N, Wu HC, Clemente JC. The microbiome in early life: implications for health outcomes. Nat Med. 2016;22:713–722.

    Article  CAS  PubMed  Google Scholar 

  19. Arrieta MC, Stiemsma LT, Amenyogbe N, Brown EM, Finlay B. The intestinal microbiome in early life: health and disease. Front Immunol. 2014;5:427.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Korpela K, Helve O, Kolho KL et al. Maternal fecal microbiota transplantation in cesarean-born infants rapidly restores normal gut microbial development: a proof-of-concept study. Cell. 2020;183:324–334.

    Article  CAS  PubMed  Google Scholar 

  21. Shouval DS, Rufo PA. The role of environmental factors in the pathogenesis of inflammatory bowel diseases. JAMA Pediatr. 2017;171:999–1005.

    Article  PubMed  Google Scholar 

  22. Baron S, Turck D, Leplat C et al. Environmental risk factors in paediatric inflammatory bowel diseases: a population based case control study. Gut. 2005;54:357–363.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Bager P, Simonsen J, Nielsen NM, Frisch M. Cesarean section and offspringʼs risk of inflammatory bowel disease: a national cohort study. Inflamm Bowel Dis. 2012;18:857–862.

    Article  PubMed  Google Scholar 

  24. Sonntag B, Stolze B, Heinecke A et al. Preterm birth but not mode of delivery is associated with an increased risk of developing inflammatory bowel disease later in life. Inflamm Bowel Dis. 2007;13:1385–1390.

    Article  PubMed  Google Scholar 

  25. Barclay AR, Russell RK, Wilson ML, Gilmour WH, Satsangi J, Wilson DC. Systematic review: the role of breastfeeding in the development of pediatric inflammatory bowel disease. J Pediatr. 2009;155:421–426.

    Article  PubMed  Google Scholar 

  26. Bernstein CN, Rawsthorne P, Cheang M, Blanchard JF. A population-based case control study of potential risk factors for IBD. Am J Gastroenterol. 2006;101:993–1002.

    Article  PubMed  Google Scholar 

  27. Wurzelmann JI, Lyles CM, Sandler RS. Childhood infections and the risk of inflammatory bowel disease. Dig Dis Sci. 1994;39:555–560.

    Article  CAS  PubMed  Google Scholar 

  28. Jakobsen C, Paerregaard A, Munkholm P, Wewer V. Environmental factors and risk of developing paediatric inflammatory bowel disease—a population based study 2007–2009. J Crohns Colitis. 2013;7:79–88.

    Article  PubMed  Google Scholar 

  29. Rodríguez LAG, Ruigómez A, Panés J. Acute gastroenteritis is followed by an increased risk of inflammatory bowel disease. Gastroenterology. 2006;130:1588–1594.

    Article  Google Scholar 

  30. Koutroubakis IE, Vlachonikolis IG. Appendectomy and the development of ulcerative colitis: results of a metaanalysis of published case-control studies. Am J Gastroenterol. 2000;95:171–176.

    Article  CAS  PubMed  Google Scholar 

  31. Carroll MW, Kuenzig ME, Mack DR et al. The impact of inflammatory bowel disease in Canada 2018: children and adolescents with IBD. J Can Assoc Gastroenterol. 2019;2:S49–S67.

    Article  PubMed  Google Scholar 

  32. Andersen V, Olsen A, Carbonnel F, Tjønneland A, Vogel U. Diet and risk of inflammatory bowel disease. Dig Liv Dis. 2012;44:185–194.

    Article  CAS  Google Scholar 

  33. El Amrousy D, El Ashry H, Hodeib H, Hassan S. Vitamin D in children with inflammatory bowel disease. J Clin Gastroenterol. 2021;55:815–820.

    PubMed  Google Scholar 

  34. Hasosah M, Alhashmi W, Abualsaud R et al. Environmental risk factors for childhood inflammatory bowel diseases: a multicenter case-control study. Children (Basel). 2022;9:4–12.

    Google Scholar 

  35. Du L, Ha C. Epidemiology and pathogenesis of ulcerative colitis. Gastroenterol Clin North Am. 2020;49:643–654.

    Article  PubMed  Google Scholar 

  36. Levine A, Sigall Boneh R, Wine E. Evolving role of diet in the pathogenesis and treatment of inflammatory bowel diseases. Gut. 2018;67:1726–1738.

    Article  CAS  PubMed  Google Scholar 

  37. Karban A. Effect of smoking on inflammatory bowel disease: Is it disease or organ specific. World J Gastroenterol. 2007;13:2150–2152.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Cohen AJ, Brauer M, Burnett R et al. Estimates and 25-year trends of the global burden of disease attributable to ambient air pollution: an analysis of data from the Global Burden of Diseases Study 2015. Lancet. 2017;389:1907–1918.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Mukherjee A, Agrawal M. A global perspective of fine particulate matter pollution and its health effects. Rev Environ Contam Toxicol. 2018;244:5–51.

    PubMed  Google Scholar 

  40. Bazyar J, Pourvakhshoori N, Khankeh H, Farrokhi M, Delshad V, Rajabi E. A comprehensive evaluation of the association between ambient air pollution and adverse health outcomes of major organ systems: a systematic review with a worldwide approach. Environ Sci Pollut Res. 2019;26:12648–12661.

    Article  CAS  Google Scholar 

  41. Jacquemin B, Siroux V, Sanchez M et al. Ambient air pollution and adult asthma incidence in six European cohorts (ESCAPE). Environ Health Perspect. 2015;123:613–621.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Heydarpour P, Amini H, Khoshkish S, Seidkhani H, Sahraian MA, Yunesian M. Potential impact of air pollution on multiple sclerosis in Tehran, Iran. Neuroepidemiology. 2014;43:233–238.

    Article  PubMed  Google Scholar 

  43. Beamish LA, Osornio-Vargas AR, Wine E. Air pollution: an environmental factor contributing to intestinal disease. J Crohns Colitis. 2011;5:279–286.

    Article  PubMed  Google Scholar 

  44. Vignal C, Guilloteau E, Gower C, Body M. Review article: epidemiological and animal evidence for the role of air pollution in intestinal diseases. Sci Total Environ. 2021;757:143718.

    Article  CAS  PubMed  Google Scholar 

  45. Ran Z, An Y, Zhou J et al. Subchronic exposure to concentrated ambient PM2.5 perturbs gut and lung microbiota as well as metabolic profiles in mice. Environmen Pollution. 2021;272:115987.

    Article  CAS  Google Scholar 

  46. Ribière C, Peyret P, Parisot N et al. Oral exposure to environmental pollutant benzo[a]pyrene impacts the intestinal epithelium and induces gut microbial shifts in murine model. Sci Rep. 2016;6:31027.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Chen L, Zhang W, Hua J et al. Dysregulation of intestinal health by environmental pollutants: involvement of the estrogen receptor and aryl hydrocarbon receptor. Environmen Sci Technol. 2018;52:2323–2330.

    Article  CAS  Google Scholar 

  48. Lavigne É, Bélair A, Rodriguez D et al. Effect modification of perinatal exposure to air pollution and childhood asthma incidence. Euro Respir J. 2018;51:1701884.

    Article  CAS  Google Scholar 

  49. Peters M, Godfrey C, McInerney P, Munn Z, Trico A, Khalil H. Chapter 11: Scoping Reviews. In: JBI Manual for evidence synthesis. JBI; 2020.

  50. Mudway IS, Kelly FJ, Holgate ST. Oxidative stress in air pollution research. Free Radic Biol Med. 2020;151:2–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Gawda A, Majka G, Nowak B, Marcinkiewicz J. Air pollution, oxidative stress, and exacerbation of autoimmune diseases. Centr Eur J Immunol. 2017;3:305–312.

    Article  CAS  Google Scholar 

  52. Gruzieva O, Merid SK, Gref A et al. Exposure to traffic-related air pollution and serum inflammatory cytokines in children. Environmen Health Perspect. 2017;125:067007.

    Article  Google Scholar 

  53. Wilson DC, Russell RK. Overview of paediatric IBD. Semin Pediatr Surg. 2017;26:344–348.

    Article  PubMed  Google Scholar 

  54. Kaplan GG, Hubbard J, Korzenik J et al. The inflammatory bowel diseases and ambient air pollution: a novel association. Am J Gastroenterology. 2010;105:2412–2419.

    Article  CAS  Google Scholar 

  55. Opstelten JL, Beelen RMJ, Leenders M et al. Exposure to ambient air pollution and the risk of inflammatory bowel disease: a European nested case-control study. Dig Dis Sci. 2016;61:2963–2971.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Alderete TL, Jones RB, Chen Z, Kim JS et al. Exposure to traffic-related air pollution and the composition of the gut microbiota in overweight and obese adolescents. Environ Res. 2018;161:472–478.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Liu T, Chen X, Xu Y et al. Gut microbiota partially mediates the effects of fine particulate matter on type 2 diabetes: evidence from a population-based epidemiological study. Environ Intern. 2019;130:104882.

    Article  CAS  Google Scholar 

  58. Lehtinen P, Pasanen K, Kolho L, Auvinen A. Incidence of pediatric inflammatory bowel disease in finland: an environmental study. J Pediatr Gastroenterol Nut. 2016;63:1778–1783.

    Article  Google Scholar 

  59. Elten M, Benchimol EI, Fell DB et al. Ambient air pollution and the risk of pediatric-onset inflammatory bowel disease: a population-based cohort study. Environ Int. 2020;138:105676.

    Article  CAS  PubMed  Google Scholar 

  60. Elten M, Benchimol EI, Fell DB et al. Residential greenspace in childhood reduces risk of pediatric inflammatory bowel disease: a population-based cohort study. Am J Gastroenterol. 2021;116:347–353.

    Article  PubMed  Google Scholar 

  61. Benchimol EI, Manuel DG, To T et al. Asthma, type 1 and type 2 diabetes mellitus, and inflammatory bowel disease amongst South Asian immigrants to Canada and their children: a population-based cohort study. PLoS ONE. 2015;10:e0123599.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Landrigan PJ, Sly JL, Ruchirawat M et al. Health consequences of environmental exposures: changing global patterns of exposure and disease. Ann Global Health. 2016;82:10–19.

    Article  Google Scholar 

  63. Björkstén B. Environment and infant immunity. Proc Nutr Soc. 1999;58:729–732.

    Article  PubMed  Google Scholar 

  64. Noverr MC, Huffnagle GB. The “microflora hypothesis” of allergic diseases. Clin Exp Allergy. 2005;35:1511–1520.

    Article  CAS  PubMed  Google Scholar 

  65. Vallès Y, Francino MP. Air pollution, early life microbiome, and development. Curr Environ Health Rep. 2018;5:512–521.

    Article  PubMed  PubMed Central  Google Scholar 

  66. Georgountzou A, Papadopoulos NG. Postnatal innate immune development: from birth to adulthood. Front Immunol. 2017;8:957.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  67. Alam MT, Amos GCA, Murphy ARJ, Murch S, Wellington EMH, Arasaradnam RP. Microbial imbalance in inflammatory bowel disease patients at different taxonomic levels. Gut Pathog. 2020;12:1.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Mutlu EA, Engen PA, Soberanes S et al. Particulate matter air pollution causes oxidant-mediated increase in gut permeability in mice. Part Fibre Toxicol. 2011;8:8–19.

    Article  CAS  Google Scholar 

  69. Li X, Cui J, Yang H et al. Colonic injuries induced by inhalational exposure to particulate-matter air pollution. Advanced Sci. 2019;6:1900180.

    Article  CAS  Google Scholar 

  70. Mutlu EA, Comba IY, Cho T et al. Inhalational exposure to particulate matter air pollution alters the composition of the gut microbiome. Environ Pollut. 2018;240:817–830.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Fu P, Bai L, Cai Z, Li R, Yung KKL. Fine particulate matter aggravates intestinal and brain injury and affects bacterial community structure of intestine and feces in Alzheimer’s disease transgenic mice. Ecotoxicol Environ Saf. 2020;192:110325.

    Article  CAS  PubMed  Google Scholar 

  72. Salim SY, Jovel J, Wine E et al. Exposure to ingested airborne pollutant particulate matter increases mucosal exposure to bacteria and induces early onset of inflammation in neonatal IL-10-deficient mice. Inflamm Bowel Dis. 2014;20:1129–1138.

    Article  PubMed  Google Scholar 

  73. Reiss R, Anderson EL, Cross CE et al. Evidence of health impacts of sulfate-and nitrate-containing particles in ambient air. Inhal Toxicol. 2007;19:419–449.

    Article  CAS  PubMed  Google Scholar 

  74. Imathiu S. Street vended foods: potential for improving food and nutrition security or a risk factor for food borne diseases in developing countries? Current Research in Nutrition and Food Science Journal. 2017;5:55–65.

    Article  Google Scholar 

  75. Alimi BA. Risk factors in street food practices in developing countries: a review. Food Sci. Hum. Wellness. 2016;5:141–148.

    Article  Google Scholar 

  76. Mazzeo N. Chemistry, emission control, radioactive pollution and indoor air quality [Internet]. London: IntechOpen; 2011.

    Book  Google Scholar 

  77. Ruiz T, Acuña JJ, Fujiyoshi S et al. Airborne bacterial communities of outdoor environments and their associated influencing factors. Environ Intern. 2020;145:106156.

    Article  Google Scholar 

  78. Vester MK, Mirsepasi HC, Prosberg MV et al. Increased abundance of proteobacteria in aggressive Crohn’s disease seven years after diagnosis. Sci Rep. 2019;9:13473.

    Article  CAS  Google Scholar 

  79. Fujimura KE, Demoor T, Rauch M et al. House dust exposure mediates gut microbiome Lactobacillus enrichment and airway immune defense against allergens and virus infection. Proc Natl Acad Sci U S A. 2014;111:805–810.

    Article  CAS  PubMed  Google Scholar 

  80. Cholapranee A, Ananthakrishnan AN. Environmental hygiene and risk of inflammatory bowel diseases. Inflamm Bowel Dis. 2016;22:2191–2199.

    Article  PubMed  Google Scholar 

  81. Vedamurthy A, Ananthakrishnan AN. Influence of environmental factors in the development and outcomes of inflammatory bowel disease. Gastroenterol Hepatol (N Y). 2019;2:72–82.

    Google Scholar 

  82. Almaraz M, Bai E, Wang C et al. Agriculture is a major source of NOx pollution in California. Sci Adv. 2018;4:eaao3477.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  83. Ahuja V, Tandon RK. Inflammatory bowel disease in the Asia-Pacific area: a comparison with developed countries and regional differences. J Dig Dis. 2010;11:134–147.

    Article  PubMed  Google Scholar 

  84. Mannucci P, Franchini M. Health effects of ambient air pollution in developing countries. Int J Environ Res Public Health. 2017;14:1048.

    Article  PubMed Central  CAS  Google Scholar 

  85. Thia KT, Loftus EV, Sandborn WJ, Yang SK. An update on the epidemiology of inflammatory bowel disease in Asia. Am J Gastroenterol. 2008;103:3167–3182.

    Article  PubMed  Google Scholar 

  86. Gancarczyk M. Enterprise- and industry-level drivers of cluster evolution and their outcomes for clusters from developed and less-developed countries. Eur Plan Stud. 2015;23:1–21.

    Article  Google Scholar 

  87. Williams ML. Patterns of air pollution in developed countries. London: Academic Press; 1999.

    Book  Google Scholar 

  88. Ryan FJ, Ahern AM, Fitzgerald RS et al. Colonic microbiota is associated with inflammation and host epigenomic alterations in inflammatory bowel disease. Nat Commun. 2020;11:15342.

    Google Scholar 

  89. Fouladi F, Bailey MJ, Patterson WB et al. Air pollution exposure is associated with the gut microbiome as revealed by shotgun metagenomic sequencing. Environ Inter. 2020;138:1937–1943.

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by the IMAGINE Chronic Disease Network, which is supported by a grant from the Canadian Institute of Health Research (Funding Reference Number: 1715-000-001) with funding from several partners.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Eytan Wine.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest and no relevant financial disclosures related to this work.

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

Suarez, R.G., Osornio-Vargas, A.R. & Wine, E. Ambient Air Pollution and Pediatric Inflammatory Bowel Diseases: An Updated Scoping Review. Dig Dis Sci 67, 4342–4354 (2022). https://doi.org/10.1007/s10620-022-07597-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10620-022-07597-3

Keywords

Navigation