Predictors of Lung Cancer Risk: An Ecological Study Using Mortality and Environmental Data by Municipalities in Italy
Abstract
:1. Introduction
2. Materials and Methods
2.1. The Study Design
2.2. Mortality and Occupational Data
2.3. Environmental Data
2.4. Geographical Data
2.5. Statistical Analysis
3. Results
3.1. Environmental Exposure
3.2. Statistical Results and Model Estimates
3.3. Estimates for the Attributable Fraction
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Acknowledgments
Conflicts of Interest
References
- IARC. Lung Fact Sheet. 2018. Available online: https://gco.iarc.fr/today/data/factsheets/cancers/15-Lung-fact-sheet.pdf (accessed on 15 February 2021).
- Malhotra, J.; Malvezzi, M.; Negri, E.; la Vecchia, C.; Boffetta, P. Risk factors for lung cancer worldwide. Eur. Respir. J. 2016. [Google Scholar] [CrossRef] [Green Version]
- Driscoll, T. GBD 2016 Occupational Carcinogens Collaborators. Global and regional burden of cancer in 2016 arising from occupational exposure to selected carcinogens: A systematic analysis for the Global Burden of Disease Study 2016. Occup. Environ. Med. 2020, 77, 151–159. [Google Scholar] [CrossRef]
- IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. A Review of Human Carcinogens. Part F: Chemical Agents and Related Occupations; International Agency for Research on Cancer: Lyon, France, 2009. [Google Scholar]
- Albin, M.; Magnani, C.; Krstev, S.; Rapiti, E.; Shefer, I. Asbestos and cancer: An overview of current trends in Europe. Environ. Health Perspect. 1999. [Google Scholar] [CrossRef]
- Darnton, A.J.; McElvenny, D.M.; Hodgson, J.T. Estimating the number of asbestos-related lung cancer deaths in Great Britain from 1980 to 2000. Ann. Occup. Hyg. 2006. [Google Scholar] [CrossRef]
- Marinaccio, A.; Binazzi, A.; Di Marzio, D.; Scarselli, A.; Verardo, M.; Mirabelli, D.; Gennaro, V.; Mensi, C.; Riboldi, L.; Merler, E.; et al. Pleural malignant mesothelioma epidemic: Incidence, modalities of asbestos exposure and occupations involved from the Italian National Register. Int. J. Cancer 2012. [Google Scholar] [CrossRef]
- Mirabelli, D.; Kauppinen, T. Occupational exposures to carcinogens in Italy: An update of CAREX database. Int. J. Occup. Environ. Health 2005. [Google Scholar] [CrossRef] [PubMed]
- Martuzzi, M.; Comba, P.; De Santis, M.; Iavarone, I.; Di Paola, M.; Mastrantonio, M.; Pirastu, R. Asbestos-related lung cancer mortality in Piedmont, Italy. Am. J. Ind. Med. 1998. [Google Scholar] [CrossRef]
- Marinaccio, A.; Scarselli, A.; Binazzi, A.; Mastrantonio, M.; Ferrante, P.; Iavicoli, S. Magnitude of asbestos-related lung cancer mortality in Italy. Br. J. Cancer 2008. [Google Scholar] [CrossRef]
- WHO. Report of the 2nd Meeting of the WHO International Radon Project. Geneve. 2006. Available online: https://www.who.int/ionizing_radiation/env/radon/Mar06MeetingReport.pdf (accessed on 15 February 2021).
- Gaskin, J.; Coyle, D.; Whyte, J.; Krewksi, D. Global estimate of lung cancer mortality attributable to residential radon. Environ. Health Perspect. 2018. [Google Scholar] [CrossRef]
- Carr, L.L.; Jacobson, S.; Lynch, D.A.; Foreman, M.G.; Flenaugh, E.L.; Hersh, C.P.; Sciurba, F.C.; Wilson, D.O.; Sieren, J.C.; Mulhall, P.; et al. Features of COPD as Predictors of Lung Cancer. Chest 2018. [Google Scholar] [CrossRef]
- Doḿnguez-Berjón, M.F.; Gandarillas, A.; Soto, M.J. Lung cancer and urbanization level in a region of Southern Europe: Influence of socio-economic and environmental factors. J. Public Health 2016. [Google Scholar] [CrossRef]
- O’Neil, M.E.; Henley, S.J.; Rohan, E.A.; Ellington, T.D.; Gallaway, M.S. Lung Cancer Incidence in Nonmetropolitan and Metropolitan Counties—United States, 2007–2016. MMWR. Morb. Mortal. Wkly. Rep. 2019. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Loomis, D.; Grosse, Y.; Lauby-Secretan, B.; El Ghissassi, F.; Bouvard, V.; Benbrahim-Tallaa, L.; Guha, N.; Baan, R.; Mattock, H.; Straif, K. The carcinogenicity of outdoor air pollution. Lancet Oncol. 2013. [Google Scholar] [CrossRef]
- Wang, N.; Mengersen, K.; Kimlin, M.; Zhou, M.; Tong, S.; Fang, L.; Wang, B.; Hu, W. Lung cancer and particulate pollution: A critical review of spatial and temporal analysis evidence. Environ. Res. 2018. [Google Scholar] [CrossRef]
- Chen, J.; Hoek, G. Long-term exposure to PM and all-cause and cause-specific mortality: A systematic review and meta-analysis. Environ. Int. 2020. [Google Scholar] [CrossRef]
- Global Burden of Disease Cancer Collaboration; Fitzmaurice, C.; Allen, C.; Barber, R.M.; Barregard, L.; Bhutta, Z.A.; Brenner, H.; Dicker, D.J.; Chimed-Orchir, O.; Dandona, R.; et al. Global, regional, and national cancer incidence, mortality, years of life lost, years lived with disability, and disability-adjusted life-years for 32 cancer groups, 1990 to 2015: A Systematic Analysis for the Global Burden of Disease Study Global Burden. JAMA Oncol. 2017. [Google Scholar] [CrossRef]
- Bochicchio, F.; Campos-Venuti, G.; Piermattei, S.; Nuccetelli, C.; Risica, S.; Tommasino, L.; Torri, G.; Magnoni, M.; Agnesod, G.; Sgorbati, G.; et al. Annual average and seasonal variations of residential radon concentration for all the Italian Regions. Radiat. Meas. 2005. [Google Scholar] [CrossRef]
- Stafoggia, M.; Renzi, M.; Forastiere, F.; Ljungman, P.; Davoli, M.; de’Donato, F.; Gariazzo, C.; Michelozzi, P.; Scortichini, M.; Solimini, A.; et al. Short-term effects of particulate matter on cardiovascular morbidity in Italy. A national analysis. Eur. J. Prev. Cardiol. 2021, in press. [Google Scholar]
- Caranci, N.; Biggeri, A.; Grisotto, L.; Pacelli, B.; Spadea, T.; Costa, G. L’indice di deprivazione italiano a livello di sezione di censimento: Definizione, descrizione e associazione con la mortalità. Epidemiol. Prev. 2010, 34, 167–176. [Google Scholar]
- He, Y.; Gao, Z.; Guo, T.; Qu, F.; Liang, D.; Li, D.; Shi, J.; Shan, B. Fine particulate matter associated mortality burden of lung cancer in Hebei Province, China. Thorac. Cancer 2018. [Google Scholar] [CrossRef]
- López-Abente, G.; Núñez, O.; Fernández-Navarro, P.; Barros-Dios, J.M.; Martín-Méndez, I.; Bel-Lan, A.; Locutura, J.; Quindós, L.; Sainz, C.; Ruano-Ravina, A. Residential radon and cancer mortality in Galicia, Spain. Sci. Total Environ. 2018. [Google Scholar] [CrossRef]
- Stafoggia, M.; Schwartz, J.; Badaloni, C.; Bellander, T.; Alessandrini, E.; Cattani, G.; de’ Donato, F.; Gaeta, A.; Leone, G.; Lyapustin, A.; et al. Estimation of daily PM10 concentrations in Italy (2006–2012) using finely resolved satellite data, land use variables and meteorology. Environ. Int. 2017. [Google Scholar] [CrossRef]
- Stafoggia, M.; Bellander, T.; Bucci, S.; Davoli, M.; De Hoogh, K.; de’ Donato, F.; Gariazzo, C.; Lyapustin, A.; Michelozzi, P.; Renzi, M.; et al. Estimation of daily PM10 and PM2.5 concentrations in Italy, 2013–2015, using a spatiotemporal land-use random-forest model. Environ. Int. 2019, 124, 170–179. [Google Scholar] [CrossRef]
- Hsiao, C. Analysis of Panel Data, 3rd ed.; Cambridge University Press: Cambridge, UK, 2014. [Google Scholar]
- Cohen, A.J.; Brauer, M.; Burnett, R.; Anderson, H.R.; Frostad, J.; Estep, K.; Balakrishnan, K.; Brunekreef, B.; Dandona, L.; Dandona, 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. [Google Scholar] [CrossRef] [Green Version]
- Naghavi, M.; Abajobir, A.A.; Abbafati, C.; Abbas, K.M.; Abd-Allah, F.; Abera, S.F.; Aboyans, V.; Adetokunboh, O.; Afshin, A.; Agrawal, A.; et al. Global, regional, and national age-sex specifc mortality for 264 causes of death, 1980-2016: A systematic analysis for the Global Burden of Disease Study 2016. Lancet 2017. [Google Scholar] [CrossRef] [Green Version]
- Lee, P.N.; Forey, B.A.; Thornton, A.J.; Coombs, K.J. The relationship of cigarette smoking in Japan to lung cancer, copd, ischemic heart disease and stroke: A systematic review [version 1; referees: 2 approved]. F1000 Res. 2018. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Houghton, A.M.G. Mechanistic links between COPD and lung cancer. Nat. Rev. Cancer 2013. [Google Scholar] [CrossRef]
- Young, R.P.; Hopkins, R.J.; Christmas, T.; Black, P.N.; Metcalf, P.; Gamble, G.D. COPD prevalence is increased in lung cancer, independent of age, sex and smoking history. Eur. Respir. J. 2008. [Google Scholar] [CrossRef] [Green Version]
- de Matteis, S.; Consonni, D.; Bertazzi, P.A. Exposure to occupational carcinogens and lung cancer risk. Evolution of epidemiological estimates of attributable fraction. Acta Biomed. l’Ateneo Parm. 2008, 79, 34–42. [Google Scholar]
- Rushton, L.; Hutchings, S.J.; Fortunato, L.; Young, C.; Evans, G.S.; Brown, T.; Bevan, R.; Slack, R.; Holmes, P.; Bagga, S.; et al. Occupational cancer burden in Great Britain. Br. J. Cancer 2012. [Google Scholar] [CrossRef] [PubMed]
- Boffetta, P.; Autier, P.; Boniol, M.; Boyle, P.; Hill, C.; Aurengo, A.; Masse, R.; De Thé, G.; Valleron, A.-J.; Monier, R.; et al. An estimate of cancers attributable to occupational exposures in France. J. Occup. Environ. Med. 2010. [Google Scholar] [CrossRef] [PubMed]
- Pasetto, R.; Terracini, B.; Marsili, D.; Comba, P. Occupational burden of asbestos-related cancer in argentina, Brazil, Colombia, and Mexico. Ann. Glob. Health 2014. [Google Scholar] [CrossRef] [PubMed]
- Virta, R.L. Worldwide asbestos supply and consumption trends from1900 through 2003. US Geol. Surv. Circ. 2006, 1298, 80. [Google Scholar]
- Amin, W.; Linkov, F.; Landsittel, D.P.; Silverstein, J.C.; Bashara, W.; Gaudioso, C.; Feldman, M.D.; Pass, H.I.; Melamed, J.; Friedberg, J.S.; et al. Factors influencing malignant mesothelioma survival: A retrospective review of the national mesothelioma virtual bank cohort [version 3; peer review: 2 approved, 1 approved with reservations]. F1000 Res. 2018, 7. [Google Scholar] [CrossRef]
- Barone-adesi, F.; Mirabelli, D.; Magnani, C.; Orientale, P.; Orientale, P. Rischio di tumore del polmone negli ex-esposti ad amianto Risk of lung cancer in individuals with previous exposure to asbestos. Epidemiol. Prev. 2016, 40, 20–25. [Google Scholar]
- Uguen, M.; Dewitte, J.; Marcorelles, P.; Loddé, B.; Pougnet, R.; Saliou, P.; De Braekeleer, M.; Uguen, A. Asbestos-related lung cancers: A retrospective clinical and pathological study. Mol. Clin. Oncol. 2017. [Google Scholar] [CrossRef] [Green Version]
- Marinaccio, A.; Binazzi, A.; Cauzillo, G.; Cavone, D.; De Zotti, R.; Ferrante, P.; Gennaro, V.; Gorini, G.; Menegozzo, M.; Mensi, C.; et al. Analysis of latency time and its determinants in asbestos related malignant mesothelioma cases of the Italian register. Eur. J. Cancer 2007. [Google Scholar] [CrossRef] [PubMed]
- Li, X.; Sundquist, J.; Zöller, B.; Sundquist, K. Neighborhood deprivation and lung cancer incidence and mortality: A multilevel analysis from Sweden. J. Thorac. Oncol. 2015. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kuznetsov, L.; Maier, W.; Hunger, M.; Meyer, M.; Mielck, A. Associations between regional socioeconomic deprivation and cancer risk: Analysis of Population-based Cancer Registry data from Bavaria, Germany. Prev. Med. 2011. [Google Scholar] [CrossRef]
- Hamra, G.B.; Guha, N.; Cohen, A.; Laden, F.; Raaschou-Nielsen, O.; Samet, J.M.; Vineis, P.; Forastiere, F.; Saldiva, P.; Yorifuji, T.; et al. Outdoor particulate matter exposure and lung cancer: A systematic review and meta-analysis. Environ. Health Perspect. 2014. [Google Scholar] [CrossRef]
- National Research Council. Health Effects of Exposure to Radon: BEIR VI; National Research Council: Washington, DC, USA, 1999.
- WHO. WHO Handbook on Indoor Radon: A public Health Perspective; WHO: Geneve, Swizerland, 2009. [Google Scholar]
- Boffetta, P. Human cancer from environmental pollutants: The epidemiological evidence. Mutat. Res. Genet. Toxicol. Environ. Mutagen. 2006. [Google Scholar] [CrossRef] [PubMed]
- Lantz, P.M.; Mendez, D.; Philbert, M.A. Radon, smoking, and lung cancer: The need to refocus radon control policy. Am. J. Public Health 2013. [Google Scholar] [CrossRef] [PubMed]
- Guo, Y.; Zeng, H.; Zheng, R.; Li, S.; Barnett, A.G.; Zhang, S.; Zou, X.; Huxley, R.; Chen, W.; Williams, G. The association between lung cancer incidence and ambient air pollution in China: A spatiotemporal analysis. Environ. Res. 2016. [Google Scholar] [CrossRef] [PubMed]
Variable | Description | Source | Temporal Resolution | Spatial Resolution |
---|---|---|---|---|
Lung cancer mortality | Malignant neoplasm trachea, bronchus, and lung (ICD-10 codes: C33-C34) | ISTAT | daily | Municipality |
Mesothelioma mortality | Malignant mesothelioma (ICD-10 codes: C45) | ISTAT | daily | Municipality |
Ischemic heart mortality | Ischemic heart diseases (ICD-10 codes: I20-I25) | ISTAT | daily | Municipality |
COPD mortality | Chronic obstructive pulmonary disease and other respiratory conditions (ICD-10 codes: J40-J44) | ISTAT | daily | Municipality |
Occupational respiratory diseases | Compensated cases for occupational respiratory diseases (ICD-10 codes: J40-J47, J60-J67) | INAIL | daily | Municipality |
PM2.5 | Concentration of PM2.5 | BEEP project | daily | 1 × 1 km |
Radon | Concentration of Radon | Local Environmental Authorities data and [20] | constant | Municipality |
Urbanization level | Index of urbanization levels | [21] | constant | Municipality |
Deprivation level | Index of deprivation levels | [22] | constant | Municipality |
Population | Amount of population | ISTAT | Annual | Municipality |
Min | Max | Mean | SD | Percentiles | ||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
5th | 25th | 50th | 75th | 95th | ||||||||
PM2.5 (µg/m3) | 5.85 | 36.28 | 15.88 | 6.35 | 8.20 | 10.75 | 13.92 | 20.90 | 27.83 | |||
Radon (Bq/m3) | 9 | 1008 | 80.33 | 58.59 | 18 | 44 | 69 | 102 | 181 | |||
Radon levels (Bq/m3) | Municipalities | |||||||||||
N. | % | |||||||||||
0–50 | 2569 | 31.7 | ||||||||||
51–100 | 3459 | 42.7 | ||||||||||
101–150 | 1455 | 18.0 | ||||||||||
151–300 | 537 | 6.6 | ||||||||||
>300 | 72 | 0.9 |
Predictor | Lung Cancer | |
---|---|---|
Cases | Crude Mortality RATE (per 100,000) | |
Total | 329,101 | 55.4 |
Gender | ||
Male | 246,555 | 85.6 |
Female | 82,546 | 26.9 |
Mesothelioma (death counts) | ||
0 | 192,421 | 47.0 |
1–20 | 117,170 | 66.4 |
21–40 | 16,209 | 93.8 |
41–60 | 2623 | 118.9 |
>60 | 678 | 121.9 |
PM2.5 (µg/m3) | ||
5–10 | 15,536 | 47.0 |
11–15 | 109,296 | 51.0 |
15–20 | 85,884 | 60.2 |
20–25 | 58,487 | 57.0 |
>25 | 59,898 | 58.9 |
COPD (death counts) | ||
0 | 51,551 | 45.3 |
1–5 | 121,109 | 51.6 |
6–10 | 37,113 | 58.1 |
10–15 | 18,701 | 64.5 |
>15 | 100,627 | 68.6 |
Ischemic heart disease (death counts) | ||
0 | 14,689 | 50.8 |
1–20 | 168,570 | 51.3 |
21–40 | 35,791 | 56.5 |
41–60 | 16,537 | 60.8 |
>60 | 93,514 | 66.9 |
Occupational Resp. disease (claims) | ||
0 | 269,673 | 51.6 |
1–2 | 40,362 | 78.1 |
3–4 | 10,265 | 87.8 |
5–6 | 1504 | 105.0 |
>6 | 7297 | 100.6 |
Radon (Bq/m3) | ||
0–50 | 139,633 | 54.2 |
51–100 | 126,914 | 56.9 |
101–150 | 49,264 | 55.4 |
151–300 | 11,950 | 55.2 |
>300 | 1340 | 43.0 |
Urbanization level | ||
low | 13,622 | 51.2 |
low-medium | 21,848 | 50.4 |
medium | 35,891 | 51.1 |
medium-high | 61,165 | 51.8 |
high | 196,575 | 58.4 |
Deprivation level | ||
very rich | 64,321 | 52.4 |
rich | 64,321 | 52.4 |
medium | 71,489 | 60.9 |
deprived | 67,997 | 58.0 |
very deprived | 55,494 | 48.5 |
Predictor | Incr | Unit | IR% (95% CI) | Exp. LC Cases(95% CI) | LC Fraction (%) (95% CI) |
---|---|---|---|---|---|
Mesothelioma | |||||
Male | 1 | Death per 1000 pers. | 33.59 (21.98, 46.30) | 2719 (2018, 3419) | 1.10 (0.82, 1.39) |
Female | 46.74 (17.86, 82.70) | 436 (182, 689) | 0.53 (0.22, 0.83) | ||
PM2.5 | |||||
Male | 10 | µg/m3 | 12.33 (10.04, 14.33) | 34,641 (30,738, 38,657) | 14.05 (12.47, 15.68) |
Female | 14.96 (11.54, 18.49) | 13,424 (13,402, 13,447) | 16.26 (16.24, 16.29) | ||
Occupational respiratory disease | |||||
Male | 1 | Disease per 1000 pers. | ns | n.a. | n.a. |
Female | ns | n.a. | n.a. | ||
Radon (Bq/m3) | |||||
Male | 9669 (8605, 10,346) | 3.92 (3.49, 4.20) | |||
0–50 | 0.00 | ||||
51–100 | 4.12 (2.38, 5.89) | ||||
101–150 | 17.98 (15.26, 20.76) | ||||
151–300 | 2.44 (−0.78, 5.77) | ||||
300+ | −8.20 (−18.17, −2.99) | ||||
Female | 1277 (1174, 1368) | 1.56 (1.42, 1.66) | |||
0–50 | 0.00 | ||||
51–100 | −0.27 (−3.72, 3.31) | ||||
101–150 | 10.23 (5.52, 15.15) | ||||
151–300 | 10.50 (4.44, 16.90) | ||||
300+ | 16.76 (−3.30, 40.98) |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Gariazzo, C.; Binazzi, A.; Alfò, M.; Massari, S.; Stafoggia, M.; Marinaccio, A. Predictors of Lung Cancer Risk: An Ecological Study Using Mortality and Environmental Data by Municipalities in Italy. Int. J. Environ. Res. Public Health 2021, 18, 1896. https://doi.org/10.3390/ijerph18041896
Gariazzo C, Binazzi A, Alfò M, Massari S, Stafoggia M, Marinaccio A. Predictors of Lung Cancer Risk: An Ecological Study Using Mortality and Environmental Data by Municipalities in Italy. International Journal of Environmental Research and Public Health. 2021; 18(4):1896. https://doi.org/10.3390/ijerph18041896
Chicago/Turabian StyleGariazzo, Claudio, Alessandra Binazzi, Marco Alfò, Stefania Massari, Massimo Stafoggia, and Alessandro Marinaccio. 2021. "Predictors of Lung Cancer Risk: An Ecological Study Using Mortality and Environmental Data by Municipalities in Italy" International Journal of Environmental Research and Public Health 18, no. 4: 1896. https://doi.org/10.3390/ijerph18041896