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Association between exposure to air pollutants and the risk of inflammatory bowel diseases visits

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Abstract

The topic of inflammatory bowel disease (IBD) has attracted more and more attention. Accumulating evidence suggests that exposure to air pollutants is associated with IBD, yet the results are inconsistent and study about daily exposure is few. This study evaluated the association between daily air pollution and IBD in Hefei, China. Daily IBD admission data were obtained from two hospitals in Hefei from January 1, 2019, to December 31, 2019. Daily concentrations of major air pollutants were provided by the Hefei Environmental Protection Bureau. Meteorological data were collected from China Meteorological Data Network. Distributed lag nonlinear model (DLNM) considering both the lag effects of exposure factors and nonlinear relationship of exposure-reaction was used to assess the effect of daily air pollutants exposure on IBD admission. During the study period, totally 886 cases of IBD were recruited, including 313 cases of ulcerative colitis (UC) and 573 cases of Crohn’s disease (CD). The findings showed PM2.5, O3, and CO exposure significantly increased the risk of IBD. Mean concentrations of PM2.5, O3, and CO in Hefei were 43.85ug/m3, 100.78ug/m3, and 0.76 mg/m3, respectively. Each increase of 10 mg/m3 in PM2.5/O3 and 0.1 mg/m3 in CO increased the risk of IBD. The strongest effects of these three pollutants on IBD were observed in lag2-lag3 (RR = 1.037, 95% CI: 1.005–1.070%), lag3 (RR = 1.020, 95% CI: 1.002–1.038%), and lag2 (RR = 1.036, 95% CI: 1.003–1.071%), respectively. In warm seasons, PM2.5, O3, and CO had a stronger effect increased the risk of IBD, which were observed in lag2 (RR = 1.104, 95% CI: 1.032–1.181%), lag2 and lag5 (RR = 1.023, 95% CI: 1.002–1.044%; RR = 1.036, 95% CI: 1.004–1.069%), and lag2 (RR = 1.071, 95% CI: 1.012–1.133%), respectively. Air pollutant (PM2.5, O3, and CO) exposure could increase the risk of IBD, while the most susceptibility seasons for the exposure were mainly in warm seasons. The results of this study suggest that air pollutants increase the risk of IBD patients in Hefei, China, providing a basis for developing countries to improve effective prevention of IBD, and a potential opportunity to avoid part of the risk of the onset or recurrence of IBD. This study contributes to the knowledge of the association between air pollution and IBD, but the associations need to be verified by further studies.

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Data availability

Data sharing is not applicable to this article as no datasets were generated or analyzed during the current study.

Abbreviations

IBD:

Inflammatory bowel disease

DLNM:

Distributed lag nonlinear model

UC:

Ulcerative colitis

CD:

Crohn’s disease

CO:

Carbon monoxide

NO2 :

Nitrogen dioxide

SO2 :

Sulfur dioxide

PM2.5 :

Particulate matter with aerodynamic equivalent diameter < 2.5 μm

PM:

Particulate matter

O3 :

Ozone

PM10 :

Particulate matter with aerodynamic equivalent diameter < 10 μm

RR:

Relative risk

CI:

Confidence interval

ROS:

Reactive oxygen species

References

  • Ananthakrishnan AN, Bernstein CN, Iliopoulos D, Macpherson A, Neurath MF, Ali R, Vavricka SR, Fiocchi C (2018) Environmental triggers in IBD: a review of progress and evidence. Nat Rev Gastroenterol Hepatol 15(1):39–49

    Article  Google Scholar 

  • Ananthakrishnan AN, McGinley EL, Binion DG, Saeian K (2011) Ambient air pollution correlates with hospitalizations for inflammatory bowel disease: an ecologic analysis. Inflamm Bowel Dis 17(5):1138–1145

    Article  Google Scholar 

  • Bernal JL, Cummins S, Gasparrini A (2017) Interrupted time series regression for the evaluation of public health interventions: a tutorial. Int J Epidemiol 46(1):348–355

    Google Scholar 

  • Bernstein CN, Burchill C, Targownik LE, Singh H, Roos LL (2019) Events within the first year of life, but not the neonatal period, affect risk for later development of inflammatory bowel diseases. Gastroenterol 156(8):2190-2197.e10

    Article  Google Scholar 

  • Bhaskaran K, Gasparrini A, Hajat S, Smeeth L, Armstrong B (2013) Time series regression studies in environmental epidemiology. Int J Epidemiol 42(4):1187–1195

    Article  Google Scholar 

  • Bocci V, Borrelli E, Travagli V, Zanardi I (2009) The ozone paradox: ozone is a strong oxidant as well as a medical drug. Med Res Rev 29(4):646–682

    Article  CAS  Google Scholar 

  • Breuer-Katschinski BD, Holländer N, Goebell H (1996) Effect of cigarette smoking on the course of Crohn’s disease. Eur J Gastroenterol Hepatol 8(3):225–228

    Article  CAS  Google Scholar 

  • Brugha R, Grigg J (2014) Urban air pollution and respiratory infections. Paediatr Respir Rev 15(2):194–199

    Google Scholar 

  • Chen P, Zhou G, Lin J, Li L, Zeng Z, Chen M, Zhang S (2020) Serum biomarkers for inflammatory bowel disease. Front Med (lausanne) 7:123

    Article  Google Scholar 

  • Cheng H, Zhu F, Lei R, Shen C, Liu J, Yang M, Ding R, Cao J (2019) Associations of ambient PM(2.5) and O(3) with cardiovascular mortality a time-series study in Hefei, China. Int J Biometeorol 63(10):1437–1447

    Article  Google Scholar 

  • Chun H, Leung C, Wen SW, McDonald J, Shin HH (2020) Maternal exposure to air pollution and risk of autism in children: a systematic review and meta-analysis. Environmental Pollution 256:113307

    Article  CAS  Google Scholar 

  • Flynn S, Eisenstein S (2019) Inflammatory bowel disease presentation and diagnosis. Surg Clin North Am 99(6):1051–1062

    Article  Google Scholar 

  • Gasparrini A (2014) Modeling exposure-lag-response associations with distributed lag non-linear models. Stat Med 33(5):881–899

    Article  Google Scholar 

  • Gordon CJ (2003) Role of environmental stress in the physiological response to chemical toxicants. Environ Res 92(1):1–7

    Article  CAS  Google Scholar 

  • Goyette P, Labbé C, Trinh TT, Xavier RJ, Rioux JD (2007) Molecular pathogenesis of inflammatory bowel disease: genotypes, phenotypes and personalized medicine. Ann Med 39(3):177–199

    Article  CAS  Google Scholar 

  • Gu J, Shi Y, Zhu Y, Chen N, Wang H, Zhang Z, Chen T (2020) Ambient air pollution and cause-specific risk of hospital admission in China: a nationwide time-series study. Plos Medicine 17(8):e1003188

    Article  Google Scholar 

  • Guven A, Gundogdu G, Vurucu S, Uysal B, Oztas E, Ozturk H, Korkmaz A (2009) Medical ozone therapy reduces oxidative stress and intestinal damage in an experimental model of necrotizing enterocolitis in neonatal rats. J Pediatr Surg 44(9):1730–1735

    Article  Google Scholar 

  • Himuro H (2018) The effect of ozone on colonic epithelial cells. Kurume Med J 64(4):75–81

    Article  Google Scholar 

  • Huang K, Ding K, Yang XJ, Hu CY, Jiang W, Hua XG, Liu J, Cao JY, Zhang T, Kan XH, Zhang XJ (2020) Association between short-term exposure to ambient air pollutants and the risk of tuberculosis outpatient visits: a time-series study in Hefei China. Environ Res 184:109343

    Article  CAS  Google Scholar 

  • Kaplan GG (2015) The global burden of IBD: from 2015 to 2025. Nat Rev Gastroenterol Hepatol 12(12):720–727

    Article  Google Scholar 

  • Kaplan GG, Hubbard J, Korzenik J, Sands BE, Panaccione R, Ghosh S, Wheeler AJ, Villeneuve PJ (2010) The inflammatory bowel diseases and ambient air pollution: a novel association. Am J Gastroenterol 105(11):2412–2419

    Article  CAS  Google Scholar 

  • Kaplan GG, Szyszkowicz M, Fichna J, Rowe BH, Porada E, Vincent R, Madsen K, Ghosh S, Storr M (2012) Non-specific abdominal pain and air pollution: a novel association. PLoS One 7(10):e47669

    Article  CAS  Google Scholar 

  • Karczewski J, Poniedziałek B, Rzymski P, Rychlewska-Hańczewska A, Adamski Z, Wiktorowicz K (2014) The effect of cigarette smoking on the clinical course of inflammatory bowel disease. Prz Gastroenterol 9(3):153–159

    Google Scholar 

  • Katada K, Takagi T, Uchiyama K, Naito Y (2015) Therapeutic roles of carbon monoxide in intestinal ischemia-reperfusion injury. J Gastroenterol Hepatol 30(Suppl 1):46–52

    Article  CAS  Google Scholar 

  • Khreis H, Kelly C, Tate J, Parslow R, Lucas K, Nieuwenhuijsen M (2017) Exposure to traffic-related air pollution and risk of development of childhood asthma: a systematic review and meta-analysis. Environ Int 100:1–31

    Article  CAS  Google Scholar 

  • Kim H, Lee JT (2019) On inferences about lag effects using lag models in air pollution time-series studies. Environ Res 171:134–144

    Article  CAS  Google Scholar 

  • Kish L, Hotte N, Kaplan GG, Vincent R, Tso R, Gänzle M, Rioux KP, Thiesen A, Barkema HW, Wine E, Madsen KL (2013) Environmental particulate matter induces murine intestinal inflammatory responses and alters the gut microbiome. PLoS One 8(4):e62220

    Article  CAS  Google Scholar 

  • Mutlu EA, Comba IY, Cho T, Engen PA, Yazıcı C, Soberanes S, Hamanaka RB, Niğdelioğlu R, Meliton AY, Ghio AJ, Budinger G, Mutlu GM (2018) Inhalational exposure to particulate matter air pollution alters the composition of the gut microbiome. Environ Pollut 240:817–830

    Article  CAS  Google Scholar 

  • Mutlu EA, Engen PA, Soberanes S, Urich D, Forsyth CB, Nigdelioglu R, Chiarella SE, Radigan KA, Gonzalez A, Jakate S, Keshavarzian A, Budinger GR, Mutlu GM (2011) Particulate matter air pollution causes oxidant-mediated increase in gut permeability in mice. Part Fibre Toxicol 8:19

    Article  CAS  Google Scholar 

  • Onyiah JC, Sheikh SZ, Maharshak N, Otterbein LE, Plevy SE (2014) Heme oxygenase-1 and carbon monoxide regulate intestinal homeostasis and mucosal immune responses to the enteric microbiota. Gut Microbes 5(2):220–224

    Article  Google Scholar 

  • Papa A, Scaldaferri F, Danese S, Guglielmo S, Roberto I, Bonizzi M, Mocci G, Felice C, Ricci C, Andrisani G, Fedeli G, Gasbarrini G, Gasbarrini A (2008) Vascular involvement in inflammatory bowel disease: pathogenesis and clinical aspects. Dig Dis 26(2):149–155

    Article  Google Scholar 

  • Ran Z, An Y, Zhou J, Yang J, Zhang Y, Yang J, Wang L, Li X, Lu D, Zhong J, Song H, Qin X, Li R (2021) Subchronic exposure to concentrated ambient PM2.5 perturbs gut and lung microbiota as well as metabolic profiles in mice. Environ Pollution 272:115987

    Article  CAS  Google Scholar 

  • Rich DQ, Balmes JR, Frampton MW, Zareba W, Stark P, Arjomandi M, Hazucha MJ, Costantini MG, Ganz P, Hollenbeck-Pringle D, Dagincourt N, Bromberg PA (2018) Cardiovascular function and ozone exposure: the Multicenter Ozone Study in oldEr Subjects (MOSES). Environ Int 119:193–202

    Article  CAS  Google Scholar 

  • Sairenji T, Collins KL, Evans DV (2017) An update on inflammatory bowel disease. Prim Care 44(4):673–692

    Article  Google Scholar 

  • Salim SY, Kaplan GG, Madsen KL (2014) Air pollution effects on the gut microbiota: a link between exposure and inflammatory disease. Gut Microbes 5(2):215–219

    Article  Google Scholar 

  • Sies H (1997) Oxidative stress: oxidants and antioxidants. Exp Physiol 82(2):291–295

    Article  CAS  Google Scholar 

  • Smith GS, Van Den Eeden SK, Garcia C, Shan J, Baxter R, Herring AH, Richardson DB, Van Rie A, Emch M, Gammon MD (2016) Air pollution and pulmonary tuberculosis: a nested case-control study among members of a northern California health plan. Environ Health Perspect 124(6):761–768

    Article  CAS  Google Scholar 

  • Tan F, Wang W, Qi S, Kan H, Yu X, Liu Y, Wu D, Xu B, Meng F, Liu S (2019) Air pollutants and outpatient visits for cardiovascular disease in a severe haze-fog city: Shijiazhuang. China Bmc Public Health 19(1):1366

    Article  Google Scholar 

  • Tian T, Wang Z, Zhang J (2017) Pathomechanisms of oxidative stress in inflammatory bowel disease and potential antioxidant therapies. Oxid Med Cell Longev 2017:4535194

    Article  Google Scholar 

  • Valavanidis A, Vlachogianni T, Fiotakis K, Loridas S (2013) Pulmonary oxidative stress, inflammation and cancer: respirable particulate matter, fibrous dusts and ozone as major causes of lung carcinogenesis through reactive oxygen species mechanisms. Int J Environ Res Public Health 10(9):3886–3907

    Article  Google Scholar 

  • Wiegman CH, Li F, Ryffel B, Togbe D, Chung KF (2020) Oxidative stress in Ozone-Induced chronic lung inflammation and emphysema: a facet of chronic obstructive pulmonary disease. Front Immunol 11:1957

    Article  CAS  Google Scholar 

  • Xu MX, Ge CX, Qin YT, Gu TT, Lou DS, Li Q, Hu LF, Feng J, Huang P, Tan J (2019) Prolonged PM2.5 exposure elevates risk of oxidative stress-driven nonalcoholic fatty liver disease by triggering increase of dyslipidemia. Free Radic Biol Med 130:542–556

    Article  CAS  Google Scholar 

  • Zhang S, Zheng S, Wang X, Shi Q, Wang X, Yuan S, Wang G, Ji Z (2015) Carbon monoxide-releasing molecule-2 reduces intestinal epithelial tight-junction damage and mortality in septic rats. PLoS One 10(12):e0145988

    Article  Google Scholar 

  • Zhang X, Staimer N, Tjoa T, Gillen DL, Schauer JJ, Shafer MM, Hasheminassab S, Pakbin P, Longhurst J, Sioutas C, Delfino RJ (2016) Associations between microvascular function and short-term exposure to traffic-related air pollution and particulate matter oxidative potential. Environ Health 15(1):81

    Article  Google Scholar 

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Funding

This work was supported by the Research Foundation of Anhui Medical University (No. 2019xkj133).

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Contributions

All authors contributed to the study’s conception and design. Material preparation, data collection, and analysis were performed by Siwen Ding and Shu Sun. The first draft of the manuscript was written by Siwen Ding. The manuscript was reviewed and edited by Rui Ding, Shasha Song, and Yi Cao. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript. Lijiu Zhang is the corresponding author and acts on behalf of all authors to ensure the accuracy or completeness of any part of the work.

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Correspondence to Lijiu Zhang.

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Ding, S., Sun, S., Ding, R. et al. Association between exposure to air pollutants and the risk of inflammatory bowel diseases visits. Environ Sci Pollut Res 29, 17645–17654 (2022). https://doi.org/10.1007/s11356-021-17009-0

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