Abstract
Background
The evidence linking ambient air pollution to bladder cancer is limited and mixed.
Methods
We assessed the associations of bladder cancer incidence with residential exposure to fine particles (PM2.5), nitrogen dioxide (NO2), black carbon (BC), warm season ozone (O3) and eight PM2.5 elemental components (copper, iron, potassium, nickel, sulfur, silicon, vanadium, and zinc) in a pooled cohort (N = 302,493). Exposures were primarily assessed based on 2010 measurements and back-extrapolated to the baseline years. We applied Cox proportional hazard models adjusting for individual- and area-level potential confounders.
Results
During an average of 18.2 years follow-up, 967 bladder cancer cases occurred. We observed a positive though statistically non-significant association between PM2.5 and bladder cancer incidence. Hazard Ratios (HR) were 1.09 (95% confidence interval (CI): 0.93–1.27) per 5 µg/m3 for 2010 exposure and 1.06 (95% CI: 0.99–1.14) for baseline exposure. Effect estimates for NO2, BC and O3 were close to unity. A positive association was observed with PM2.5 zinc (HR 1.08; 95% CI: 1.00–1.16 per 10 ng/m3).
Conclusions
We found suggestive evidence of an association between long-term PM2.5 mass exposure and bladder cancer, strengthening the evidence from the few previous studies. The association with zinc in PM2.5 suggests the importance of industrial emissions.
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Data availability
The exposure maps are available on request from Dr Kees de Hoogh (c.dehoogh@swisstph.ch). The cohort data could only be pooled for the ELAPSE framework but is not available for sharing due to strict national data protection regulations and the General Data Protection Regulation of the European Union. The ELAPSE study protocol is available at http://www.elapseproject.eu/. A detailed statistical analysis plan is available on reasonable request from the corresponding author (j.chen1@uu.nl).
References
Loomis D, Grosse Y, Lauby-Secretan B, Ghissassi FE, Bouvard V, Benbrahim-Tallaa L, et al. The carcinogenicity of outdoor air pollution. Lancet Oncol. 2013;14:1262–3.
Collaborators GDaI, Vos T, Lim SS, Abbafati C, Abbas KM, Abbasi M, et al. Global burden of 369 diseases and injuries in 204 countries and territories, 1990–2019: a systematic analysis for the Global Burden of Disease Study 2019. Lancet. 2020;396:1204–22.
Boffetta P, Jourenkova N, Gustavsson P. Cancer risk from occupational and environmental exposure to polycyclic aromatic hydrocarbons. Cancer Causes Control. 1997;8:444–72.
Boffetta P, Silverman DT. A meta-analysis of bladder cancer and diesel exhaust exposure. Epidemiology. 2001;12:125–30.
Kogevinas M, Mannetje AT, Cordier S, Ranft U, González CA, Vineis P, et al. Occupation and bladder cancer among men in Western Europe. Cancer Causes Control. 2003;14:907–14.
Silverman DT, Hoover RN, Mason TJ, Swanson GM. Motor exhaust-related occupations and bladder cancer. Cancer Res. 1986;46:2113–6.
Turner MC, Krewski D, Diver WR, Pope CA 3rd, Burnett RT, Jerrett M, et al. Ambient Air Pollution and Cancer Mortality in the Cancer Prevention Study II. Environ Health Perspect. 2017;125:087013.
Coleman NC, Burnett RT, Higbee JD, Lefler JS, Merrill RM, Ezzati M, et al. Cancer mortality risk, fine particulate air pollution, and smoking in a large, representative cohort of US adults. Cancer Causes Control. 2020;31:767–76.
Turner MC, Gracia-Lavedan E, Cirac M, Castano-Vinyals G, Malats N, Tardon A, et al. Ambient air pollution and incident bladder cancer risk: Updated analysis of the Spanish Bladder Cancer Study. Int J Cancer. 2019;145:894–900.
Pedersen M, Stafoggia M, Weinmayr G, Andersen ZJ, Galassi C, Sommar J, et al. Is There an Association Between Ambient Air Pollution and Bladder Cancer Incidence? Analysis of 15 European Cohorts. Eur Urol Focus. 2018;4:113–20.
Raaschou-Nielsen O, Andersen ZJ, Hvidberg M, Jensen SS, Ketzel M, Sørensen M, et al. Air pollution from traffic and cancer incidence: a Danish cohort study. Environ Health. 2011;10:67.
Cohen G, Levy I, Yuval, Kark JD, Levin N, Witberg G, et al. Chronic exposure to traffic-related air pollution and cancer incidence among 10,000 patients undergoing percutaneous coronary interventions: a historical prospective study. Eur J Prev Cardiol. 2018;25:659–70.
Visser O, van Wijnen JH, van Leeuwen FE. Residential traffic density and cancer incidence in Amsterdam, 1989-97. Cancer Causes Control. 2004;15:331–9.
Castano-Vinyals G, Cantor KP, Malats N, Tardon A, Garcia-Closas R, Serra C, et al. Air pollution and risk of urinary bladder cancer in a case-control study in Spain. Occup Environ Med. 2008;65:56–60.
Ancona C, Badaloni C, Mataloni F, Bolignano A, Bucci S, Cesaroni G, et al. Mortality and morbidity in a population exposed to multiple sources of air pollution: A retrospective cohort study using air dispersion models. Environ Res. 2015;137:467–74.
Brunekreef B, Strak M, Chen J, Andersen ZJ, Atkinson R, Bauwelinck M, et al. Mortality and Morbidity Effects of Long-Term Exposure To Low-Level PM2.5, Black Carbon, NO2 and O3: an analysis of European Cohorts. Research Report (Health Effects Institute). 2021.
Chen J, Rodopoulou S, de Hoogh K, Strak M, Andersen ZJ, Atkinson R, et al. Long-term exposure to fine particle elemental components and natural and cause-specific mortality-a pooled analysis of eight European Cohorts within the ELAPSE Project. Environ Health Perspect. 2021;129:47009.
Hvidtfeldt UA, Chen J, Andersen ZJ, Atkinson R, Bauwelinck M, Bellander T, et al. Long-term exposure to fine particle elemental components and lung cancer incidence in the ELAPSE pooled cohort. Environ Res. 2021;193:110568.
Eriksson AK, Ekbom A, Granath F, Hilding A, Efendic S, Östenson CG. Psychological distress and risk of pre‐diabetes and Type 2 diabetes in a prospective study of Swedish middle‐aged men and women. Diabet Med. 2008;25:834–42.
Lagergren M, Fratiglioni L, Hallberg IR, Berglund J, Elmståhl S, Hagberg B, et al. A longitudinal study integrating population, care and social services data. The Swedish National study on Aging and Care (SNAC). Aging Clin Exp Res. 2004;16:158–68.
Magnusson PK, Almqvist C, Rahman I, Ganna A, Viktorin A, Walum H, et al. The Swedish Twin Registry: establishment of a biobank and other recent developments. Twin Res Hum Genet. 2013;16:317–29.
Wändell P-E, Wajngot A, De Faire U, Hellénius M-L. Increased prevalence of diabetes among immigrants from non-European countries in 60-year-old men and women in Sweden. Diabetes Metab. 2007;33:30–6.
Tjønneland A, Olsen A, Boll K, Stripp C, Christensen J, Engholm G, et al. Study design, exposure variables, and socioeconomic determinants of participation in diet, cancer and health: a population-based prospective cohort study of 57,053 men and women in Denmark. Scand J Public Health. 2007;35:432–41.
Hundrup YA, Simonsen MK, Jørgensen T, Obel EB. Cohort profile: the Danish nurse cohort. Int J Epidemiol. 2012;41:1241–7.
Beulens JW, Monninkhof EM, Verschuren WM, Schouw YTVD, Smit J, Ocke MC, et al. Cohort profile: the EPIC-NL study. Int J Epidemiol. 2010;39:1170–8.
Clavel-Chapelon F. Group ENS. Cohort profile: the French E3N cohort study. Int J Epidemiol. 2015;44:801–9.
Ulmer H, Kelleher C, Fitz‐Simon N, Diem G, Concin H. Secular trends in cardiovascular risk factors: an age‐period cohort analysis of 6 98 954 health examinations in 1 81 350 Austrian men and women. J Intern Med. 2007;261:566–76.
de Hoogh K, Wang M, Adam M, Badaloni C, Beelen R, Birk M, et al. Development of land use regression models for particle composition in twenty study areas in Europe. Environ Sci Technol. 2013;47:5778–86.
Tsai MY, Hoek G, Eeftens M, de Hoogh K, Beelen R, Beregszaszi T, et al. Spatial variation of PM elemental composition between and within 20 European study areas-Results of the ESCAPE project. Environ Int. 2015;84:181–92.
De Hoogh K, Chen J, Gulliver J, Hoffmann B, Hertel O, Ketzel M, et al. Spatial PM2. 5, NO2, O3 and BC models for Western Europe–Evaluation of spatiotemporal stability. Environ Int. 2018;120:81–92.
Chen J, de Hoogh K, Gulliver J, Hoffmann B, Hertel O, Ketzel M, et al. Development of Europe-Wide models for particle elemental composition using supervised linear regression and random forest. Environ Sci Technol. 2020;54:15698–709.
Brandt J, Silver JD, Frohn LM, Geels C, Gross A, Hansen AB, et al. An integrated model study for Europe and North America using the Danish Eulerian Hemispheric Model with focus on intercontinental transport of air pollution. Atmos Environ. 2012;53:156–76.
Samoli E, Rodopoulou S, Hvidtfeldt UA, Wolf K, Stafoggia M, Brunekreef B, et al. Modeling multi-level survival data in multi-center epidemiological cohort studies: Applications from the ELAPSE project. Environ Int. 2021;147:106371.
Hvidtfeldt UA, Severi G, Andersen ZJ, Atkinson R, Bauwelinck M, Bellander T, et al. Long-term low-level ambient air pollution exposure and risk of lung cancer—a pooled analysis of 7 European cohorts. Environ Int. 2021;146:106249.
Beelen R, Hoek G, Raaschou-Nielsen O, Stafoggia M, Andersen ZJ, Weinmayr G, et al. Natural-cause mortality and long-term exposure to particle components: an analysis of 19 European cohorts within the multi-center ESCAPE project. Environ Health Perspect. 2015;123:525–33.
Strak M, Weinmayr G, Rodopoulou S, Chen J, de Hoogh K, Andersen ZJ, et al. Long term exposure to low level air pollution and mortality in eight European cohorts within the ELAPSE project: pooled analysis. BMJ. 2021;374:n1904.
Andersen ZJ, Stafoggia M, Weinmayr G, Pedersen M, Galassi C, Jorgensen JT, et al. Long-term exposure to ambient air pollution and incidence of postmenopausal breast cancer in 15 European Cohorts within the ESCAPE Project. Environ Health Perspect. 2017;125:107005.
Chen J, de Hoogh K, Gulliver J, Hoffmann B, Hertel O, Ketzel M, et al. A comparison of linear regression, regularization, and machine learning algorithms to develop Europe-wide spatial models of fine particles and nitrogen dioxide. Environ Int. 2019;130:104934.
Siegel RL, Miller KD, Fuchs HE, Jemal A. Cancer statistics, 2021. CA Cancer J Clin. 2021;71:7–33.
Wong CM, Tsang H, Lai HK, Thomas GN, Lam KB, Chan KP, et al. Cancer mortality risks from long-term exposure to ambient fine particle. Cancer Epidemiol Biomark Prev. 2016;25:839–45.
Brown T, Slack R, Rushton L.British Occupational Cancer Burden Study Group Occupational cancer in Britain. Urinary tract cancers: bladder and kidney. Br J Cancer. 2012;107:S76–84.
Moorthy B, Chu C, Carlin DJ. Polycyclic aromatic hydrocarbons: from metabolism to lung cancer. Toxicological Sci. 2015;145:5–15.
Turner MC, Andersen ZJ, Baccarelli A, Diver WR, Gapstur SM, Pope CA, 3rd, et al. Outdoor air pollution and cancer: An overview of the current evidence and public health recommendations. CA Cancer J Clin. 2020;70:460–79.
Latifovic L, Villeneuve PJ, Parent ME, Johnson KC, Kachuri L, Canadian Cancer Registries Epidemiology G, et al. Bladder cancer and occupational exposure to diesel and gasoline engine emissions among Canadian men. Cancer Med. 2015;4:1948–62.
Benbrahim-Tallaa L, Baan RA, Grosse Y, Lauby-Secretan B, El Ghissassi F, Bouvard V, et al. Carcinogenicity of diesel-engine and gasoline-engine exhausts and some nitroarenes. Lancet Oncol. 2012;13:663–4.
Viana M, Kuhlbusch TAJ, Querol X, Alastuey A, Harrison RM, Hopke PK, et al. Source apportionment of particulate matter in Europe: A review of methods and results. J Aerosol Sci. 2008;39:827–49.
Thurston GD, Burnett RT, Turner MC, Shi Y, Krewski D, Lall R, et al. Ischemic heart disease mortality and long-term exposure to source-related components of U.S. Fine particle air pollution. Environ Health Perspect. 2016;124:785–94.
Collarile P, Bidoli E, Barbone F, Zanier L, Del Zotto S, Fuser S, et al. Residence in proximity of a coal-oil-fired thermal power plant and risk of lung and bladder cancer in North-Eastern Italy. A Population-Based Study: 1995-2009. Int J Environ Res Public Health. 2017;14:860.
de Hoogh K, Gulliver J, Donkelaar AV, Martin RV, Marshall JD, Bechle MJ, et al. Development of West-European PM2.5 and NO2 land use regression models incorporating satellite-derived and chemical transport modelling data. Environ Res. 2016;151:1–10.
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;68:765–70.
Cesaroni G, Porta D, Badaloni C, Stafoggia M, Eeftens M, Meliefste K, 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.
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;47:7804–11.
Acknowledgements
We thank Marjan Tewis for the data management tasks in creating the pooled cohort database.
Funding
The research described in this article was conducted under contract to the Health Effects Institute (HEI), an organisation jointly funded by the United States Environmental Protection Agency (EPA) (Assistance Award No. R-82811201) and certain motor vehicle and engine manufacturers. The contents of this article do not necessarily reflect the views of HEI, or its sponsors, nor do they necessarily reflect the views and policies of the EPA or motor vehicle and engine manufacturers.
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GH, ORN and JC: study conceptualisation and design; GH and BB: principal investigators of the ELAPSE project; JC: statistical analysis and manuscript writing; GH, ORN and BB: supervision, manuscript review and editing; GH, BB, JC and MS: ELAPSE project coordination, preparing pooled data for analyses, and providing support with the access to pooled cohort data; SR, ES and KK: contribution of statistical analyses strategy and scripts for the statistical analyses; KdH, JC and GH: exposure assessment. All authors contributed to the interpretation of the results. All authors read and revised the manuscript for the important intellectual content and approved the final draft of the manuscript.
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This study involved no contact with members of the study population and the published results does not allow identification of individuals. The analyses were undertaken in a secure IT environment where no individual level data can be retrieved. All included cohort studies were approved by the medical ethics committees in their respective countries.
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Chen, J., Rodopoulou, S., Strak, M. et al. Long-term exposure to ambient air pollution and bladder cancer incidence in a pooled European cohort: the ELAPSE project. Br J Cancer 126, 1499–1507 (2022). https://doi.org/10.1038/s41416-022-01735-4
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DOI: https://doi.org/10.1038/s41416-022-01735-4
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