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Published in: Digestive Diseases and Sciences 10/2016

Open Access 01-10-2016 | Original Article

Exposure to Ambient Air Pollution and the Risk of Inflammatory Bowel Disease: A European Nested Case–Control Study

Authors: Jorrit L. Opstelten, Rob M. J. Beelen, Max Leenders, Gerard Hoek, Bert Brunekreef, Fiona D. M. van Schaik, Peter D. Siersema, Kirsten T. Eriksen, Ole Raaschou-Nielsen, Anne Tjønneland, Kim Overvad, Marie-Christine Boutron-Ruault, Franck Carbonnel, Kees de Hoogh, Timothy J. Key, Robert Luben, Simon S. M. Chan, Andrew R. Hart, H. Bas Bueno-de-Mesquita, Bas Oldenburg

Published in: Digestive Diseases and Sciences | Issue 10/2016

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Abstract

Background

Industrialization has been linked to the etiology of inflammatory bowel disease (IBD).

Aim

We investigated the association between air pollution exposure and IBD.

Methods

The European Prospective Investigation into Cancer and Nutrition cohort was used to identify cases with Crohn’s disease (CD) (n = 38) and ulcerative colitis (UC) (n = 104) and controls (n = 568) from Denmark, France, the Netherlands, and the UK, matched for center, gender, age, and date of recruitment. Air pollution data were obtained from the European Study of Cohorts for Air Pollution Effects. Residential exposure was assessed with land-use regression models for particulate matter with diameters of <10 μm (PM10), <2.5 μm (PM2.5), and between 2.5 and 10 μm (PMcoarse), soot (PM2.5 absorbance), nitrogen oxides, and two traffic indicators. Conditional logistic regression analyses were performed to calculate odds ratios (ORs) with 95 % confidence intervals (CIs).

Results

Although air pollution was not significantly associated with CD or UC separately, the associations were mostly similar. Individuals with IBD were less likely to have higher exposure levels of PM2.5 and PM10, with ORs of 0.24 (95 % CI 0.07–0.81) per 5 μg/m3 and 0.25 (95 % CI 0.08–0.78) per 10 μg/m3, respectively. There was an inverse but nonsignificant association for PMcoarse. A higher nearby traffic load was positively associated with IBD [OR 1.60 (95 % CI 1.04–2.46) per 4,000,000 motor vehicles × m per day]. Other air pollutants were positively but not significantly associated with IBD.

Conclusion

Exposure to air pollution was not found to be consistently associated with IBD.
Appendix
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Literature
1.
go back to reference Burisch J, Jess T, Martinato M, Lakatos PL. The burden of inflammatory bowel disease in Europe. J Crohns Colitis. 2013;7:322–337.CrossRefPubMed Burisch J, Jess T, Martinato M, Lakatos PL. The burden of inflammatory bowel disease in Europe. J Crohns Colitis. 2013;7:322–337.CrossRefPubMed
2.
go back to reference Scharl M, Rogler G. Inflammatory bowel disease pathogenesis: what is new? Curr Opin Gastroenterol. 2012;28:301–309.CrossRefPubMed Scharl M, Rogler G. Inflammatory bowel disease pathogenesis: what is new? Curr Opin Gastroenterol. 2012;28:301–309.CrossRefPubMed
3.
go back to reference Ng SC, Bernstein CN, Vatn MH, et al. Geographical variability and environmental risk factors in inflammatory bowel disease. Gut. 2013;62:630–649.CrossRefPubMed Ng SC, Bernstein CN, Vatn MH, et al. Geographical variability and environmental risk factors in inflammatory bowel disease. Gut. 2013;62:630–649.CrossRefPubMed
4.
go back to reference Thia KT, Loftus EV Jr, Sandborn WJ, Yang SK. An update on the epidemiology of inflammatory bowel disease in Asia. Am J Gastroenterol. 2008;103:3167–3182.CrossRefPubMed Thia KT, Loftus EV Jr, Sandborn WJ, Yang SK. An update on the epidemiology of inflammatory bowel disease in Asia. Am J Gastroenterol. 2008;103:3167–3182.CrossRefPubMed
5.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
6.
go back to reference Bernstein CN, Shanahan F. Disorders of a modern lifestyle: reconciling the epidemiology of inflammatory bowel diseases. Gut. 2008;57:1185–1191.CrossRefPubMed Bernstein CN, Shanahan F. Disorders of a modern lifestyle: reconciling the epidemiology of inflammatory bowel diseases. Gut. 2008;57:1185–1191.CrossRefPubMed
7.
go back to reference Soon IS, Molodecky NA, Rabi DM, Ghali WA, Barkema HW, Kaplan GG. The relationship between urban environment and the inflammatory bowel diseases: a systematic review and meta-analysis. BMC Gastroenterol. 2012;12:51.CrossRefPubMedPubMedCentral Soon IS, Molodecky NA, Rabi DM, Ghali WA, Barkema HW, Kaplan GG. The relationship between urban environment and the inflammatory bowel diseases: a systematic review and meta-analysis. BMC Gastroenterol. 2012;12:51.CrossRefPubMedPubMedCentral
8.
go back to reference Hou JK, Abraham B, El-Serag H. Dietary intake and risk of developing inflammatory bowel disease: a systematic review of the literature. Am J Gastroenterol. 2011;106:563–573.CrossRefPubMed Hou JK, Abraham B, El-Serag H. Dietary intake and risk of developing inflammatory bowel disease: a systematic review of the literature. Am J Gastroenterol. 2011;106:563–573.CrossRefPubMed
9.
go back to reference Ananthakrishnan AN. Environmental risk factors for inflammatory bowel diseases: a review. Dig Dis Sci. 2015;60:290–298.CrossRefPubMed Ananthakrishnan AN. Environmental risk factors for inflammatory bowel diseases: a review. Dig Dis Sci. 2015;60:290–298.CrossRefPubMed
11.
go back to reference Beamish LA, Osornio-Vargas AR, Wine E. Air pollution: an environmental factor contributing to intestinal disease. J Crohns Colitis. 2011;5:279–286.CrossRefPubMed Beamish LA, Osornio-Vargas AR, Wine E. Air pollution: an environmental factor contributing to intestinal disease. J Crohns Colitis. 2011;5:279–286.CrossRefPubMed
12.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
13.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
14.
go back to reference Salim SY, Kaplan GG, Madsen KL. Air pollution effects on the gut microbiota: a link between exposure and inflammatory disease. Gut Microbes. 2014;5:215–219.CrossRefPubMed Salim SY, Kaplan GG, Madsen KL. Air pollution effects on the gut microbiota: a link between exposure and inflammatory disease. Gut Microbes. 2014;5:215–219.CrossRefPubMed
15.
go back to reference Kaplan GG, Hubbard J, Korzenik J, et al. The inflammatory bowel diseases and ambient air pollution: a novel association. Am J Gastroenterol. 2010;105:2412–2419.CrossRefPubMedPubMedCentral Kaplan GG, Hubbard J, Korzenik J, et al. The inflammatory bowel diseases and ambient air pollution: a novel association. Am J Gastroenterol. 2010;105:2412–2419.CrossRefPubMedPubMedCentral
16.
go back to reference Riboli E, Hunt KJ, Slimani N, et al. European Prospective Investigation into Cancer and Nutrition (EPIC): study populations and data collection. Public Health Nutr. 2002;5:1113–1124.CrossRefPubMed Riboli E, Hunt KJ, Slimani N, et al. European Prospective Investigation into Cancer and Nutrition (EPIC): study populations and data collection. Public Health Nutr. 2002;5:1113–1124.CrossRefPubMed
17.
go back to reference Beelen R, Raaschou-Nielsen O, Stafoggia M, et al. Effects of long-term exposure to air pollution on natural-cause mortality: an analysis of 22 European cohorts within the multicentre ESCAPE project. Lancet. 2014;383:785–795.CrossRefPubMed Beelen R, Raaschou-Nielsen O, Stafoggia M, et al. Effects of long-term exposure to air pollution on natural-cause mortality: an analysis of 22 European cohorts within the multicentre ESCAPE project. Lancet. 2014;383:785–795.CrossRefPubMed
18.
go back to reference Eeftens M, Beelen R, de Hoogh K, et al. Development of land use regression models for PM2.5, PM2.5 absorbance, PM10 and PMcoarse in 20 European study areas; results of the ESCAPE project. Environ Sci Technol. 2012;46:11195–11205.CrossRefPubMed Eeftens M, Beelen R, de Hoogh K, et al. Development of land use regression models for PM2.5, PM2.5 absorbance, PM10 and PMcoarse in 20 European study areas; results of the ESCAPE project. Environ Sci Technol. 2012;46:11195–11205.CrossRefPubMed
19.
go back to reference Beelen R, Hoek G, Vienneau D, et al. Development of NO2 and NO x land use regression models for estimating air pollution exposure in 36 study areas in Europe—the ESCAPE project. Atmos Environ. 2013;72:10–23.CrossRef Beelen R, Hoek G, Vienneau D, et al. Development of NO2 and NO x land use regression models for estimating air pollution exposure in 36 study areas in Europe—the ESCAPE project. Atmos Environ. 2013;72:10–23.CrossRef
20.
go back to reference Cyrys J, Eeftens M, Heinrich J, et al. Variation of NO2 and NO x concentrations between and within 36 European study areas: results from the ESCAPE study. Atmos Environ. 2012;62:374–390.CrossRef Cyrys J, Eeftens M, Heinrich J, et al. Variation of NO2 and NO x concentrations between and within 36 European study areas: results from the ESCAPE study. Atmos Environ. 2012;62:374–390.CrossRef
21.
go back to reference Eeftens M, Tsai M-Y, Ampe C, et al. Spatial variation of PM2.5, PM10, PM2.5 absorbance and PMcoarse concentrations between and within 20 European study areas and the relationship with NO2—results of the ESCAPE project. Atmos Environ. 2012;62:303–317.CrossRef Eeftens M, Tsai M-Y, Ampe C, et al. Spatial variation of PM2.5, PM10, PM2.5 absorbance and PMcoarse concentrations between and within 20 European study areas and the relationship with NO2—results of the ESCAPE project. Atmos Environ. 2012;62:303–317.CrossRef
22.
go back to reference Mahid SS, Minor KS, Soto RE, Hornung CA, Galandiuk S. Smoking and inflammatory bowel disease: a meta-analysis. Mayo Clin Proc. 2006;81:1462–1471.CrossRefPubMed Mahid SS, Minor KS, Soto RE, Hornung CA, Galandiuk S. Smoking and inflammatory bowel disease: a meta-analysis. Mayo Clin Proc. 2006;81:1462–1471.CrossRefPubMed
23.
go back to reference Aamodt G, Jahnsen J, Bengtson MB, Moum B, Vatn MH. Geographic distribution and ecological studies of inflammatory bowel disease in southeastern Norway in 1990–1993. Inflamm Bowel Dis. 2008;14:984–991.CrossRefPubMed Aamodt G, Jahnsen J, Bengtson MB, Moum B, Vatn MH. Geographic distribution and ecological studies of inflammatory bowel disease in southeastern Norway in 1990–1993. Inflamm Bowel Dis. 2008;14:984–991.CrossRefPubMed
24.
go back to reference Mills NL, Donaldson K, Hadoke PW, et al. Adverse cardiovascular effects of air pollution. Nat Clin Pract Cardiovasc Med. 2009;6:36–44.CrossRefPubMed Mills NL, Donaldson K, Hadoke PW, et al. Adverse cardiovascular effects of air pollution. Nat Clin Pract Cardiovasc Med. 2009;6:36–44.CrossRefPubMed
25.
go back to reference Langrish JP, Bosson J, Unosson J, et al. Cardiovascular effects of particulate air pollution exposure: time course and underlying mechanisms. J Intern Med. 2012;272:224–239.CrossRefPubMed Langrish JP, Bosson J, Unosson J, et al. Cardiovascular effects of particulate air pollution exposure: time course and underlying mechanisms. J Intern Med. 2012;272:224–239.CrossRefPubMed
26.
go back to reference Calvert GM, Ward E, Schnorr TM, Fine LJ. Cancer risks among workers exposed to metalworking fluids: a systematic review. Am J Ind Med. 1998;33:282–292.CrossRefPubMed Calvert GM, Ward E, Schnorr TM, Fine LJ. Cancer risks among workers exposed to metalworking fluids: a systematic review. Am J Ind Med. 1998;33:282–292.CrossRefPubMed
27.
go back to reference García-Pérez J, López-Cima MF, Pérez-Gómez B, et al. Mortality due to tumours of the digestive system in towns lying in the vicinity of metal production and processing installations. Sci Total Environ. 2010;408:3102–3112.CrossRefPubMed García-Pérez J, López-Cima MF, Pérez-Gómez B, et al. Mortality due to tumours of the digestive system in towns lying in the vicinity of metal production and processing installations. Sci Total Environ. 2010;408:3102–3112.CrossRefPubMed
29.
go back to reference Orazzo F, Nespoli L, Ito K, et al. Air pollution, aeroallergens, and emergency room visits for acute respiratory diseases and gastroenteric disorders among young children in six Italian cities. Environ Health Perspect. 2009;117:1780–1785.PubMedPubMedCentral Orazzo F, Nespoli L, Ito K, et al. Air pollution, aeroallergens, and emergency room visits for acute respiratory diseases and gastroenteric disorders among young children in six Italian cities. Environ Health Perspect. 2009;117:1780–1785.PubMedPubMedCentral
31.
go back to reference Silverstein MD, Lashner BA, Hanauer SB, Evans AA, Kirsner JB. Cigarette smoking in Crohn’s disease. Am J Gastroenterol. 1989;84:31–33.PubMed Silverstein MD, Lashner BA, Hanauer SB, Evans AA, Kirsner JB. Cigarette smoking in Crohn’s disease. Am J Gastroenterol. 1989;84:31–33.PubMed
32.
go back to reference Botteri E, Iodice S, Bagnardi V, Raimondi S, Lowenfels AB, Maisonneuve P. Smoking and colorectal cancer: a meta-analysis. JAMA. 2008;300:2765–2778.CrossRefPubMed Botteri E, Iodice S, Bagnardi V, Raimondi S, Lowenfels AB, Maisonneuve P. Smoking and colorectal cancer: a meta-analysis. JAMA. 2008;300:2765–2778.CrossRefPubMed
33.
go back to reference van Eeden SF, Tan WC, Suwa T, et al. Cytokines involved in the systemic inflammatory response induced by exposure to particulate matter air pollutants (PM(10)). Am J Respir Crit Care Med. 2001;164:826–830.CrossRefPubMed van Eeden SF, Tan WC, Suwa T, et al. Cytokines involved in the systemic inflammatory response induced by exposure to particulate matter air pollutants (PM(10)). Am J Respir Crit Care Med. 2001;164:826–830.CrossRefPubMed
34.
go back to reference Cohen R, Robinson D Jr, Paramore C, Fraeman K, Renahan K, Bala M. Autoimmune disease concomitance among inflammatory bowel disease patients in the United States, 2001–2002. Inflamm Bowel Dis. 2008;14:738–743.CrossRefPubMed Cohen R, Robinson D Jr, Paramore C, Fraeman K, Renahan K, Bala M. Autoimmune disease concomitance among inflammatory bowel disease patients in the United States, 2001–2002. Inflamm Bowel Dis. 2008;14:738–743.CrossRefPubMed
35.
go back to reference Oikonen M, Laaksonen M, Laippala P, et al. Ambient air quality and occurrence of multiple sclerosis relapse. Neuroepidemiology. 2003;22:95–99.CrossRefPubMed Oikonen M, Laaksonen M, Laippala P, et al. Ambient air quality and occurrence of multiple sclerosis relapse. Neuroepidemiology. 2003;22:95–99.CrossRefPubMed
36.
go back to reference Hart JE, Laden F, Puett RC, Costenbader KH, Karlson EW. Exposure to traffic pollution and increased risk of rheumatoid arthritis. Environ Health Perspect. 2009;117:1065–1069.CrossRefPubMedPubMedCentral Hart JE, Laden F, Puett RC, Costenbader KH, Karlson EW. Exposure to traffic pollution and increased risk of rheumatoid arthritis. Environ Health Perspect. 2009;117:1065–1069.CrossRefPubMedPubMedCentral
37.
go back to reference Ananthakrishnan AN, McGinley EL, Binion DG, Saeian K. Ambient air pollution correlates with hospitalizations for inflammatory bowel disease: an ecologic analysis. Inflamm Bowel Dis. 2011;17:1138–1145.CrossRefPubMed Ananthakrishnan AN, McGinley EL, Binion DG, Saeian K. Ambient air pollution correlates with hospitalizations for inflammatory bowel disease: an ecologic analysis. Inflamm Bowel Dis. 2011;17:1138–1145.CrossRefPubMed
38.
go back to reference Shivananda S, Lennard-Jones J, Logan R, et al. Incidence of inflammatory bowel disease across Europe: is there a difference between north and south? Results of the European Collaborative Study on Inflammatory Bowel Disease (EC-IBD). Gut. 1996;39:690–697.CrossRefPubMedPubMedCentral Shivananda S, Lennard-Jones J, Logan R, et al. Incidence of inflammatory bowel disease across Europe: is there a difference between north and south? Results of the European Collaborative Study on Inflammatory Bowel Disease (EC-IBD). Gut. 1996;39:690–697.CrossRefPubMedPubMedCentral
39.
go back to reference Beelen R, Hoek G, Fischer P, van den Brandt PA, Brunekreef B. Estimated long-term outdoor air pollution concentrations in a cohort study. Atmos Environ. 2007;41:1343–1358.CrossRef Beelen R, Hoek G, Fischer P, van den Brandt PA, Brunekreef B. Estimated long-term outdoor air pollution concentrations in a cohort study. Atmos Environ. 2007;41:1343–1358.CrossRef
40.
go back to reference Eeftens M, Beelen R, Fischer P, Brunekreef B, Meliefste K, Hoek G. Stability of measured and modelled spatial contrasts in NO2 over time. Occup Environ Med. 2011;68:765–770.CrossRefPubMed Eeftens M, Beelen R, Fischer P, Brunekreef B, Meliefste K, Hoek G. Stability of measured and modelled spatial contrasts in NO2 over time. Occup Environ Med. 2011;68:765–770.CrossRefPubMed
41.
go back to reference Cesaroni G, Porta D, Badaloni C, et al. Nitrogen dioxide levels estimated from land use regression models several years apart and association with mortality in a large cohort study. Environ Health. 2012;11:48.CrossRefPubMedPubMedCentral Cesaroni G, Porta D, Badaloni C, et al. Nitrogen dioxide levels estimated from land use regression models several years apart and association with mortality in a large cohort study. Environ Health. 2012;11:48.CrossRefPubMedPubMedCentral
42.
go back to reference Wang R, Henderson SB, Sbihi H, Allen RW, Brauer M. Temporal stability of land use regression models for traffic-related air pollution. Atmos Environ. 2013;64:312–319.CrossRef Wang R, Henderson SB, Sbihi H, Allen RW, Brauer M. Temporal stability of land use regression models for traffic-related air pollution. Atmos Environ. 2013;64:312–319.CrossRef
43.
go back to reference Gulliver J, de Hoogh K, Hansell A, Vienneau D. Development and back-extrapolation of NO2 land use regression models for historic exposure assessment in Great Britain. Environ Sci Technol. 2013;47:7804–7811.CrossRefPubMed Gulliver J, de Hoogh K, Hansell A, Vienneau D. Development and back-extrapolation of NO2 land use regression models for historic exposure assessment in Great Britain. Environ Sci Technol. 2013;47:7804–7811.CrossRefPubMed
Metadata
Title
Exposure to Ambient Air Pollution and the Risk of Inflammatory Bowel Disease: A European Nested Case–Control Study
Authors
Jorrit L. Opstelten
Rob M. J. Beelen
Max Leenders
Gerard Hoek
Bert Brunekreef
Fiona D. M. van Schaik
Peter D. Siersema
Kirsten T. Eriksen
Ole Raaschou-Nielsen
Anne Tjønneland
Kim Overvad
Marie-Christine Boutron-Ruault
Franck Carbonnel
Kees de Hoogh
Timothy J. Key
Robert Luben
Simon S. M. Chan
Andrew R. Hart
H. Bas Bueno-de-Mesquita
Bas Oldenburg
Publication date
01-10-2016
Publisher
Springer US
Published in
Digestive Diseases and Sciences / Issue 10/2016
Print ISSN: 0163-2116
Electronic ISSN: 1573-2568
DOI
https://doi.org/10.1007/s10620-016-4249-4

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