. 2017 Oct 13;125(10):107005.

doi: 10.1289/EHP1742.

Long-Term Exposure to Ambient Air Pollution and Incidence of Postmenopausal Breast Cancer in 15 European Cohorts within the ESCAPE Project

Zorana J Andersen¹, Massimo Stafoggia^{2

3}, Gudrun Weinmayr⁴, Marie Pedersen^{1

5}, Claudia Galassi⁶, Jeanette T Jørgensen¹, Anna Oudin⁷, Bertil Forsberg⁷, David Olsson⁷, Bente Oftedal⁸, Gunn Marit Aasvang⁸, Geir Aamodt⁸, Andrei Pyko³, Göran Pershagen³, Michal Korek³, Ulf De Faire³, Nancy L Pedersen⁹, Claes-Göran Östenson¹⁰, Laura Fratiglioni¹¹, Kirsten T Eriksen⁵, Anne Tjønneland⁵, Petra H Peeters^{12

13}, Bas Bueno-de-Mesquita^{13

14

15}, Michelle Plusquin¹³, Timothy J Key¹⁶, Andrea Jaensch⁴, Gabriele Nagel^{4

17}, Alois Lang¹⁸, Meng Wang¹⁹, Ming-Yi Tsai^{19

20

21}, Agnes Fournier^{22

23}, Marie-Christine Boutron-Ruault^{22

23}, Laura Baglietto^{22

23}, Sara Grioni²⁴, Alessandro Marcon²⁵, Vittorio Krogh²⁴, Fulvio Ricceri^{6

26}, Carlotta Sacerdote⁶, Enrica Migliore⁶, Ibon Tamayo-Uria^{27

28

29}, Pilar Amiano^{28

30}, Miren Dorronsoro^{28

30}, Roel Vermeulen^{12

13

31}, Ranjeet Sokhi³², Menno Keuken³³, Kees de Hoogh^{20

21}, Rob Beelen^{31

34}, Paolo Vineis^{13

35}, Giulia Cesaroni², Bert Brunekreef^{12

28}, Gerard Hoek^{12

31}, Ole Raaschou-Nielsen^{5

36}

Affiliations

¹ Centre for Epidemiology and Screening, Department of Public Health, University of Copenhagen, Copenhagen, Denmark.
² Department of Epidemiology, Lazio Regional Health Service, Local Health Unit Azienda Sanitaria Locale Roma 1 (ASL RM1), Rome, Italy.
³ Institute of Environmental Medicine, Karolinska Institute, Stockholm, Sweden.
⁴ Institute of Epidemiology and Medical Biometry, Ulm University, Ulm, Germany.
⁵ The Danish Cancer Society Research Center, Copenhagen, Denmark.
⁶ Unit of Cancer Epidemiology, Città della Salute e della Scienza University-Hospital and Center for Cancer Prevention (CPO), Turin, Italy.
⁷ Occupational and Environmental Medicine, Department of Public Health and Clinical Medicine, Umeå University, Umeå, Sweden.
⁸ Norwegian Institute of Public Health, Oslo, Norway.
⁹ Department of Medical Epidemiology and Biostatistics, Karolinska Institute, Stockholm, Sweden.
¹⁰ Department of Molecular Medicine and Surgery, Karolinska Institute, Stockholm, Sweden.
¹¹ Aging Research Center, Department of Neurobiology Care Science and Society, Karolinska Institute, Stockholm, Sweden.
¹² Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Utrecht, Netherlands.
¹³ MRC-PHE Centre for Environment and Health, Department of Epidemiology and Biostatistics, School of Public Health, Imperial College, London, UK.
¹⁴ Department for Determinants of Chronic Diseases (DCD), National Institute for Public Health and the Environment (RIVM), Bilthoven, Netherlands.
¹⁵ Department of Social and Preventive Medicine, Faculty of Medicine, University of Malaya, Kuala Lumpur, Malaysia.
¹⁶ Cancer Epidemiology Unit, Nuffield Department of Population Health, University of Oxford, Oxford, UK.
¹⁷ Agency for Preventive and Social Medicine, Bregenz, Austria.
¹⁸ Vorarlberg Cancer Registry, Agency for Preventive and Social Medicine (aks, Bregenz, Austria.
¹⁹ Department of Environmental and Occupational Health Sciences, University of Washington, Seattle, Washington, USA.
²⁰ Swiss Tropical and Public Health Institute, Basel, Switzerland.
²¹ University of Basel, Basel, Switzerland.
²² Centre de recherche en Épidémiologie et Santé des Populations (CESP) "Health across Generations", Institut national de la santé et de la recherche médicale (Inserm), Université Paris-Saclay, Villejuif, France.
²³ Institut Gustave Roussy, Villejuif, France.
²⁴ Epidemiology and Prevention Unit, Department of Preventive and Predictive Medicine, Fondazione Istituto di ricovero e cura a carattere scientifico (IRCCS) Istituto Nazionale dei Tumori, Milan, Italy.
²⁵ Unit of Epidemiology and Medical Statistics, Department of Diagnostics and Public Health, University of Verona, Verona, Italy.
²⁶ Unit of Epidemiology, Regional Health Service Azienda Sanitaria Locale Torino 3 (ASL TO3), Grugliasco, Italy.
²⁷ ISGlobal Institute de Salut Global Barcelona, Barcelona, Spain.
²⁸ Consortium for Biomedical Research in Epidemiology and Public Health (CIBER en Epidemiología y Salud Pública-CIBERESP), Madrid, Spain.
²⁹ Universitat Pompeu Fabra, Barcelona, Spain.
³⁰ Public Health Department of Gipuzkoa, BioDonostia Research Institute, San Sebastian, Spain.
³¹ Institute for Risk Assessment Sciences, Utrecht University, Utrecht, Netherlands.
³² Centre for Atmospheric and Instrumentation Research, University of Hertfordshire, Hatfield, UK.
³³ Netherlands Organization for Applied Scientific Research, Utrecht, Netherlands.
³⁴ National Institute for Public Health and the Environment (RIVM), Bilthoven, Netherlands.
³⁵ Molecular and Epidemiology Unit, Human Genetics Foundation (HuGeF), Torino, Italy.
³⁶ Department of Environmental Science, Aarhus University, Roskilde, Denmark.

PMID: 29033383
PMCID: PMC5933325
DOI: 10.1289/EHP1742

Long-Term Exposure to Ambient Air Pollution and Incidence of Postmenopausal Breast Cancer in 15 European Cohorts within the ESCAPE Project

Zorana J Andersen et al. Environ Health Perspect. 2017.

. 2017 Oct 13;125(10):107005.

doi: 10.1289/EHP1742.

Authors

Affiliations

¹ Centre for Epidemiology and Screening, Department of Public Health, University of Copenhagen, Copenhagen, Denmark.
² Department of Epidemiology, Lazio Regional Health Service, Local Health Unit Azienda Sanitaria Locale Roma 1 (ASL RM1), Rome, Italy.
³ Institute of Environmental Medicine, Karolinska Institute, Stockholm, Sweden.
⁴ Institute of Epidemiology and Medical Biometry, Ulm University, Ulm, Germany.
⁵ The Danish Cancer Society Research Center, Copenhagen, Denmark.
⁶ Unit of Cancer Epidemiology, Città della Salute e della Scienza University-Hospital and Center for Cancer Prevention (CPO), Turin, Italy.
⁷ Occupational and Environmental Medicine, Department of Public Health and Clinical Medicine, Umeå University, Umeå, Sweden.
⁸ Norwegian Institute of Public Health, Oslo, Norway.
⁹ Department of Medical Epidemiology and Biostatistics, Karolinska Institute, Stockholm, Sweden.
¹⁰ Department of Molecular Medicine and Surgery, Karolinska Institute, Stockholm, Sweden.
¹¹ Aging Research Center, Department of Neurobiology Care Science and Society, Karolinska Institute, Stockholm, Sweden.
¹² Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Utrecht, Netherlands.
¹³ MRC-PHE Centre for Environment and Health, Department of Epidemiology and Biostatistics, School of Public Health, Imperial College, London, UK.
¹⁴ Department for Determinants of Chronic Diseases (DCD), National Institute for Public Health and the Environment (RIVM), Bilthoven, Netherlands.
¹⁵ Department of Social and Preventive Medicine, Faculty of Medicine, University of Malaya, Kuala Lumpur, Malaysia.
¹⁶ Cancer Epidemiology Unit, Nuffield Department of Population Health, University of Oxford, Oxford, UK.
¹⁷ Agency for Preventive and Social Medicine, Bregenz, Austria.
¹⁸ Vorarlberg Cancer Registry, Agency for Preventive and Social Medicine (aks, Bregenz, Austria.
¹⁹ Department of Environmental and Occupational Health Sciences, University of Washington, Seattle, Washington, USA.
²⁰ Swiss Tropical and Public Health Institute, Basel, Switzerland.
²¹ University of Basel, Basel, Switzerland.
²² Centre de recherche en Épidémiologie et Santé des Populations (CESP) "Health across Generations", Institut national de la santé et de la recherche médicale (Inserm), Université Paris-Saclay, Villejuif, France.
²³ Institut Gustave Roussy, Villejuif, France.
²⁴ Epidemiology and Prevention Unit, Department of Preventive and Predictive Medicine, Fondazione Istituto di ricovero e cura a carattere scientifico (IRCCS) Istituto Nazionale dei Tumori, Milan, Italy.
²⁵ Unit of Epidemiology and Medical Statistics, Department of Diagnostics and Public Health, University of Verona, Verona, Italy.
²⁶ Unit of Epidemiology, Regional Health Service Azienda Sanitaria Locale Torino 3 (ASL TO3), Grugliasco, Italy.
²⁷ ISGlobal Institute de Salut Global Barcelona, Barcelona, Spain.
²⁸ Consortium for Biomedical Research in Epidemiology and Public Health (CIBER en Epidemiología y Salud Pública-CIBERESP), Madrid, Spain.
²⁹ Universitat Pompeu Fabra, Barcelona, Spain.
³⁰ Public Health Department of Gipuzkoa, BioDonostia Research Institute, San Sebastian, Spain.
³¹ Institute for Risk Assessment Sciences, Utrecht University, Utrecht, Netherlands.
³² Centre for Atmospheric and Instrumentation Research, University of Hertfordshire, Hatfield, UK.
³³ Netherlands Organization for Applied Scientific Research, Utrecht, Netherlands.
³⁴ National Institute for Public Health and the Environment (RIVM), Bilthoven, Netherlands.
³⁵ Molecular and Epidemiology Unit, Human Genetics Foundation (HuGeF), Torino, Italy.
³⁶ Department of Environmental Science, Aarhus University, Roskilde, Denmark.

PMID: 29033383
PMCID: PMC5933325
DOI: 10.1289/EHP1742

Abstract

Background: Epidemiological evidence on the association between ambient air pollution and breast cancer risk is inconsistent.

Objective: We examined the association between long-term exposure to ambient air pollution and incidence of postmenopausal breast cancer in European women.

Methods: In 15 cohorts from nine European countries, individual estimates of air pollution levels at the residence were estimated by standardized land-use regression models developed within the European Study of Cohorts for Air Pollution Effects (ESCAPE) and Transport related Air Pollution and Health impacts – Integrated Methodologies for Assessing Particulate Matter (TRANSPHORM) projects: particulate matter (PM) ≤2.5μm, ≤10μm, and 2.5–10μm in diameter (PM_2.5, PM₁₀, and PM_coarse, respectively); PM_2.5 absorbance; nitrogen oxides (NO₂ and NO_x); traffic intensity; and elemental composition of PM. We estimated cohort-specific associations between breast cancer and air pollutants using Cox regression models, adjusting for major lifestyle risk factors, and pooled cohort-specific estimates using random-effects meta-analyses.

Results: Of 74,750 postmenopausal women included in the study, 3,612 developed breast cancer during 991,353 person-years of follow-up. We found positive and statistically insignificant associations between breast cancer and PM_2.5 {hazard ratio (HR)=1.08 [95% confidence interval (CI): 0.77, 1.51] per 5 μg/m³}, PM₁₀ [1.07 (95% CI: 0.89, 1.30) per 10 μg/m³], PM_coarse[1.20 (95% CI: 0.96, 1.49 per 5 μg/m³], and NO₂ [1.02 (95% CI: 0.98, 1.07 per 10 μg/m³], and a statistically significant association with NO_x [1.04 (95% CI: 1.00, 1.08) per 20 μg/m³, p=0.04].

Conclusions: We found suggestive evidence of an association between ambient air pollution and incidence of postmenopausal breast cancer in European women. https://doi.org/10.1289/EHP1742.

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Figures

Map marking the following study sites: Umea, Oslo, Stockholm, Copenhagen, Netherlands, London virgule Oxford, France, Voralberg, Varese, Turin, and San Sebastian. — **Figure 1.**
Map of the study sites in the breast cancer analyses.

Two forest plots indicate adjusted associations between breast cancer and N O sub 2 [overall I squared value (0.0 percent) and p value (0.720)] and N O sub x [overall I squared value (0.0 percent) and p value (0.775)] in 15 cohorts separately. HR with 95 percent confidence intervals and weight percentage are presented. — **Figure 2.**
Adjusted associations (Model 3) between breast cancer and nitrogen dioxide ( ${NO}_{2}$ ) (per $10 {μ g / m}^{3}$ ) and nitrogen oxides ( ${NO}_{x}$ ) (per $20 {μ g / m}^{3}$ ) in 15 European cohorts [Cardiovascular Effects of Air pollution and Noise in Stockholm (CEANS)-Stockholm consists of four Stockholm, Sweden, cohorts: Study on Aging and Care in Kungsholmen (SNAC-K), Screening Across the Lifespan Twin study (SALT)/TwinGene, 60 Years Old (60YO)/IMPROVE, and Stockholm Diabetes Prevention Program (SDPP); European Prospective Investigation into Cancer and Nutrition (EPIC)-Netherlands consists of two Dutch cohorts: EPIC-MORGEN and EPIC-Prospect]: Results from cohort-specific analyses and random-effects analyses.

Four forest plots indicate adjusted associations between breast cancer and PM sub 2.5 [overall I squared value (56.7 percent) and p value (0.031)], PM sub 2.5 absorbance [overall I squared value (23.6 percent) and p value (0.249)], PM sub 10 [overall I squared value (16.6 percent) and p value (0.303)], and PM sub coarse [overall I squared value (40.2 percent) and p value (0.123)] in 11 cohorts separately. HR with 95 percent confidence intervals and weight percentage are presented. — **Figure 3.**
Adjusted associations (Model 3) between breast cancer and particulate matter $< 2.5 μ m$ ( ${PM}_{2.5}$ ), (per $5 {μ g / m}^{3}$ ), ${PM}_{2.5}$ absorbance (per $10^{- 5} / m$ ), particulate matter $< 10 μ m$ ( ${PM}_{10}$ ) (per $10 {μ g / m}^{3}$ ), and particulate matter $2.5 - 10 μ m$ ( ${PM}_{coarse}$ ) (per $5 {μ g / m}^{3}$ ) in 11 European cohorts [Cardiovascular Effects of Air pollution and Noise in Stockholm (CEANS)-Stockholm consists of four Stockholm, Sweden, cohorts: Study on Aging and Care in Kungsholmen (SNAC-K), Screening Across the Lifespan Twin study (SALT)/TwinGene), 60 Years Old (60YO)/IMPROVE, and Stockholm Diabetes Prevention Program (SDPP); European Prospective Investigation into Cancer and Nutrition (EPIC)-Netherlands consists of two Dutch cohorts: EPIC-MORGEN and EPIC-Prospect]: Results from cohort-specific analyses and random-effects analyses.

Forest plot indicates adjusted associations between breast cancer and nickel component of PM sub 10 [overall I squared value (36.3 percent) and p value (0.194)] in 5 cohorts. HR with 95 percent confidence intervals and weight percentage are presented. — **Figure 4.**
Adjusted associations (Model 3) between breast cancer and the nickel component of particulate matter $< 10 μ m$ ( ${PM}_{10}$ ) in 5 European cohorts [European Prospective Investigation into Cancer and Nutrition (EPIC)-Netherlands consists of two Dutch cohorts: EPIC-MORGEN and EPIC-Prospect]: Results from cohort-specific analyses and random-effects analyses.

See this image and copyright information in PMC

Comment in

Air Pollution and Breast Cancer in Postmenopausal Women: Evidence across Cohorts.
Schmidt CW. Schmidt CW. Environ Health Perspect. 2018 Mar 27;126(3):034001. doi: 10.1289/EHP3200. Environ Health Perspect. 2018. PMID: 29589879 Free PMC article. No abstract available.

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Long-Term Exposure to Ambient Air Pollution and Incidence of Postmenopausal Breast Cancer in 15 European Cohorts within the ESCAPE Project

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Long-Term Exposure to Ambient Air Pollution and Incidence of Postmenopausal Breast Cancer in 15 European Cohorts within the ESCAPE Project

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