Original Research

Ambient air pollution exposure and thyroid cancer incidence in Iran

Abstract

Introduction: Thyroid cancer is the most common endocrine malignant that is three times more prevalent in women than men. Fine particulate matter (PM2.5( has been indicated to affect Thyroid Hormone (TH) homeostasis. We sought to estimate the association between long-term exposure to ambient air pollution and the incidence of thyroid cancer in the Iranian female population.

Materials and methods: We extracted thyroid cancer incidence and ambient air pollution data from Iran from 2000 to 2019 for males and females for all age groups from the Global Burden of Disease (GBD) dataset. We entered the data into Joinpoint to present Annual Percent Change (APC) and Average Annual Percent Change (AAPC) and its confidence intervals. We entered the information into R3.5.0.

Results: Thyroid cancer in females had an upward trend [AAPC=4.9% (4.2-5.6)]. There was a correlation between ambient PM pollution (p≤0.001, r=0.84) and ambient ozone pollution (p≤0.001, r=0.94), and the incidence of thyroid cancer in females. The results of the analysis also showed a significant relationship between thyroid cancer incidence in females and secondhand smoke (p≤0.001, r=0.74).

Conclusion: This study indicated increasing trends in thyroid cancer incidence with exposure to ambient air pollution. Our novel findings provide additional insight into the potential associations between risk factors and thyroid cancer and warrant further investigation, specifically in areas with high levels of air pollution both nationally and internationally. However, causal relationships cannot be fully supported via ecological studies, and this article only focuses on Iran.

1. Franchini M, Mannucci PM. Air pollution and cardiovascular disease. Thromb Res. 2012;129(3):230–4.
2. Rappazzo KM, Daniels JL, Messer LC, Poole C, Lobdell DT. Exposure to fine particulate matter during pregnancy and risk of preterm birth among women in New Jersey, Ohio, and Pennsylvania, 2000–2005. Environ Health Perspect. 2014;122(9):992–7.
3. Cohen AJ, Brauer M, Burnett R, Anderson HR, Frostad J, Estep K, 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;389(10082):1907–18.
4. Crouse DL, Peters PA, van Donkelaar A, Goldberg MS, Villeneuve PJ, Brion O, et al. Risk of nonaccidental and cardiovascular mortality in relation to long-term exposure to low concentrations of fine particulate matter: a Canadian national-level cohort study. Environ Health Perspect. 2012;120(5):708–14.
5. Hart JE, Liao X, Hong B, Puett RC, Yanosky JD, Suh H, et al. The association of long-term exposure to PM 2.5 on all-cause mortality in the Nurses’ Health Study and the impact of measurement-error correction. Environ Heal. 2015;14(1):1–9.
6. Ji W, Zhao B. Estimating mortality derived from indoor exposure to particles of outdoor origin. PLoS One. 2015;10(4):e0124238.
7. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6):394–424.
8. Vaccarella S, Franceschi S, Bray F, Wild CP, Plummer M, Dal Maso L. Worldwide thyroid-cancer epidemic? The increasing impact of overdiagnosis. N engl j med. 2016;375(7):614–7.
9. Li M, Brito JP, Vaccarella S. Long-term declines of thyroid cancer mortality: an international age–period–cohort analysis. Thyroid. 2020;30(6):838–46.
10. Kitahara CM, Daltveit DS, Ekbom A, Engeland A, Gissler M, Glimelius I, et al. Maternal health, in-utero, and perinatal exposures and risk of thyroid cancer in offspring: a Nordic population-based nested case-control study. Lancet Diabetes Endocrinol. 2021;9(2):94–105.
11. Vaccarella S, Dal Maso L. Challenges in investigating risk factors for thyroid cancer. Lancet Diabetes Endocrinol [Internet]. 2021;9(2):57–9. Available from: http://dx.doi.org/10.1016/S2213-8587(20)30426-5.
12. Kim J, Gosnell JE, Roman SA. Geographic influences in the global rise of thyroid cancer. Nat Rev Endocrinol. 2020;16(1):17–29.
13. Fiore M, Oliveri Conti G, Caltabiano R, Buffone A, Zuccarello P, Cormaci L, et al. Role of emerging environmental risk factors in thyroid cancer: a brief review. Int J Environ Res Public Health. 2019;16(7):1185.
14. Abdelouahab N, Langlois M-F, Lavoie L, Corbin F, Pasquier J-C, Takser L. Maternal and cord-blood thyroid hormone levels and exposure to polybrominated diphenyl ethers and polychlorinated biphenyls during early pregnancy. Am J Epidemiol. 2013;178(5):701–13.
15. Baccarelli A, Giacomini SM, Corbetta C, Landi MT, Bonzini M, Consonni D, et al. Neonatal thyroid function in Seveso 25 years after maternal exposure to dioxin. PLoS Med. 2008;5(7):e161.
16. Janssen BG, Saenen ND, Roels HA, Madhloum N, Gyselaers W, Lefebvre W, et al. Fetal thyroid function, birth weight, and in utero exposure to fine particle air pollution: a birth cohort study. Environ Health Perspect. 2017;125(4):699–705.
17. Iijima K, Otake T, Yoshinaga J, Ikegami M, Suzuki E, Naruse H, et al. Cadmium, lead, and selenium in cord blood and thyroid hormone status of newborns. Biol Trace Elem Res. 2007;119(1):10–8.
18. Soldin OP, Goughenour BE, Gilbert SZ, Landy HJ, Soldin SJ. Thyroid hormone levels associated with active and passive cigarette smoking. Thyroid. 2009;19(8):817–23.
19. Lope V, Pérez-Gómez B, Aragonés N, López-Abente G, Gustavsson P, Plato N, et al. Occupational exposure to chemicals and risk of thyroid cancer in Sweden. Int Arch Occup Environ Health. 2009;82(2):267–74.
20. http://www.healthdata.org/.
21. Dicker D, Nguyen G, Abate D, Abate KH, Abay SM, Abbafati C, et al. Global, regional, and national age-sex-specific mortality and life expectancy, 1950–2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet. 2018;392(10159):1684–735.
22. Ensor KB, Raun LH, Persse D. A case-crossover analysis of out-of-hospital cardiac arrest and air pollution. Circulation. 2013;127(11):1192–9.
23. Miller DC, Salkind NJ. Handbook of research design and social measurement. Sage; 2002. 24. Levy D, Sheppard L, Checkoway H, Kaufman J, Lumley T, Koenig J, et al. A case-crossover analysis of particulate matter air pollution and out-of-hospital primary cardiac arrest. Epidemiology. 2001;12(2):193–9.
25. Silverman RA, Ito K, Freese J, Kaufman BJ, De Claro D, Braun J, et al. Association of ambient fine particles with out-of-hospital cardiac arrests in New York City. Am J Epidemiol. 2010;172(8):917–23.
26. Fitzmaurice C, Dicker D, Pain A, Hamavid H, Moradi-Lakeh M, MacIntyre MF, et al. The global burden of cancer 2013. JAMA Oncol. 2015;1(4):505–27.
27. Nasseri K, Mills PK, Allan M. Cancer incidence in the Middle Eastern population of California, 1988–2004. Asian Pacific J cancer Prev APJCP. 2007;8(3):405.
28. Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J cancer. 2015;136(5):E359–86.
29. Duedahl-Olesen L. Polycyclic aromatic hydrocarbons (PAHs) in foods [Internet]. Persistent Organic Pollutants and Toxic Metals in Foods. Woodhead Publishing Limited; 2013. 308–333 p. Available from: http://dx.doi.org/10.1533/9780857098917.2.308
30. Davies L, Welch HG. Increasing incidence of thyroid cancer in the United States, 1973-2002. Jama. 2006;295(18):2164–7.
31. Massey DD, Habil M, Taneja A. Particles in different indoor microenvironments-its implications on occupants. Build Environ. 2016;106:237–44.
32. O’Connor RJ, Schneller LM, Caruso R V, Stephens WE, Li Q, Yuan J, et al. Toxic metal and nicotine content of cigarettes sold in China, 2009 and 2012. Tob Control. 2015;24(Suppl 4):iv55–9.
33. Shen G, Tao S, Wei S, Chen Y, Zhang Y, Shen H, et al. Field measurement of emission factors of PM, EC, OC, parent, nitro-, and oxy-polycyclic aromatic hydrocarbons for residential briquette, coal cake, and wood in rural Shanxi, China. Environ Sci Technol. 2013;47(6):2998–3005.
34. Wang B, Li N, Deng F, Buglak N, Park G, Su S, et al. Human bronchial epithelial cell injuries induced by fine particulate matter from sandstorm and non-sandstorm periods: Association with particle constituents. J Environ Sci. 2016;47:201–10.
35. Wang B, Li K, Jin W, Lu Y, Zhang Y, Shen G, et al. Properties and inflammatory effects of various size fractions of ambient particulate matter from Beijing on A549 and J774A. 1 cells. Environ Sci Technol. 2013;47(18):10583–90.
36. Yang F, Tan J, Zhao Q, Du Z, He K, Ma Y, et al. Characteristics of PM 2.5 speciation in representative megacities and across China. Atmos Chem Phys. 2011;11(11):5207–19.
37. Wong MCS, Jiang JY, Liang M, Fang Y, Yeung MS, Sung JJY. Global temporal patterns of pancreatic cancer and association with socioeconomic development. Sci Rep. 2017;7(1):1–9.
38. Huang O, Wu W, Wang O, You J, Li Q, Huang D, et al. Sentinel lymph node biopsy is unsuitable for routine practice in younger female patients with unilateral low-risk papillary thyroid carcinoma. BMC Cancer. 2011;11(1):1–7.
39. Mehta S, Shin H, Burnett R, North T, Cohen AJ. Ambient particulate air pollution and acute lower respiratory infections: a systematic review and implications for estimating the global burden of disease. Air Qual Atmos Heal. 2013;6(1):69–83.
40. Kim K-H, Jahan SA, Kabir E. A review of diseases associated with household air pollution due to the use of biomass fuels. J Hazard Mater. 2011;192(2):425–31.
41. Zhang J, Smith KR. Household air pollution from coal and biomass fuels in China: measurements, health impacts, and interventions. Environ Health Perspect. 2007;115(6):848–55.
42. Zheng N, Liu J, Wang Q, Liang Z. Health risk assessment of heavy metal exposure to street dust in the zinc smelting district, Northeast of China. Sci Total Environ. 2010;408(4):726–33.
43. Chung H-K, Nam JS, Ahn CW, Lee YS, Kim KR. SomeElements in Thyroid Tissue are Associated with More Advanced Stage of Thyroid Cancer in Korean Women. Biol Trace Elem Res. 2016;171(1):54–62.
44. Malandrino P, Russo M, Ronchi A, Minoia C, Cataldo D, Regalbuto C, et al. Increased thyroid cancer incidence in a basaltic volcanic area is associated with non-anthropogenic pollution and biocontamination. Endocrine. 2016;53(2):471–9.
45. Liu Y, Su L, Xiao H. Review of factors related to the thyroid cancer epidemic. Int J Endocrinol. 2017;2017.
46. Jiang G, Duan W, Xu L, Song S, Zhu C, Wu L. Biphasic effect of cadmium on cell proliferation in human embryo lung fibroblast cells and its molecular mechanism. Toxicol Vitr. 2009;23(6):973–8.
47. Dhouib I, Jallouli M, Annabi A, Marzouki S, Gharbi N, Elfazaa S, et al. From immunotoxicity to carcinogenicity: the effects of carbamate pesticides on the immune system. Environ Sci Pollut Res. 2016;23(10):9448–58.
48. Birnbaum LS. State of the science of endocrine disruptors. National Institute of Environmental Health Sciences; 2013.
49. Dyer CA. Heavy metals as endocrine-disrupting chemicals. In: Endocrine-Disrupting Chemicals. Springer; 2007. p. 111–33.
50. Teil M-J, Moreau-Guigon E, Blanchard M, Alliot F, Gasperi J, Cladière M, et al. Endocrine disrupting compounds in gaseous and particulate outdoor air phases according to environmental factors. Chemosphere. 2016;146:94–104.
51. Rudel RA, Perovich LJ. Endocrine disrupting chemicals in indoor and outdoor air. Atmos Environ. 2009;43(1):170–81.
52. Darbre PD. Overview of air pollution and endocrine disorders. Int J Gen Med. 2018;11:191.
53. Rudel RA, Dodson RE, Perovich LJ, Morello-Frosch R, Camann DE, Zuniga MM, et al. Semivolatile endocrine-disrupting compounds in paired indoor and outdoor air in two northern California communities. Environ Sci Technol. 2010;44(17):6583–90.
54. Oziol L, Alliot F, Botton J, Bimbot M, Huteau V, Levi Y, et al. First characterization of the endocrine-disrupting potential of indoor gaseous and particulate contamination: comparison with urban outdoor air (France). Environ Sci Pollut Res. 2017;24(3):3142–52.
55. Oulhote Y, Chevrier J, Bouchard MF. Exposure to polybrominated diphenyl ethers (PBDEs) and hypothyroidism in Canadian women. J Clin Endocrinol Metab. 2016;101(2):590–8.
56. Rosen DH, Flanders WD, Friede A, Humphrey HE, Sinks TH. Half-life of polybrominated biphenyl in human sera. Environ Health Perspect. 1995;103(3):272–4.
57. Liu S, Zhao G, Li J, Zhao H, Wang Y, Chen J, et al. Association of polybrominated diphenylethers (PBDEs) and hydroxylated metabolites (OH-PBDEs) serum levels with thyroid function in thyroid cancer patients. Environ Res. 2017;159:1–8.
58. Allen JG, Gale S, Zoeller RT, Spengler JD, Birnbaum L, McNeely E. PBDE flame retardants, thyroid disease, and menopausal status in US women. Environ Heal. 2016;15(1):1–9.
59. Lin H, Chin Y, Yang YSH, Lai H, Whang‐Peng J, Liu LF, et al. Thyroid hormone, cancer, and apoptosis. Compr Physiol. 2011;6(3):1221–37.
60. (IARC) IA for R on C. Agents Classified by the IARC Monographs, Volumes 1-123 CAS No. Agent 0 B 0 B 0 B Group Volume Year. 2017;(026148):1–37. Available from: https://monographs.iarc.fr/wp-content/uploads/2018/09/ClassificationsAlphaOrder.pdf
61. Kitahara CM, Sosa JA. Understanding the ever-changing incidence of thyroid cancer. Nat Rev Endocrinol. 2020;16(11):617–8.
62. Goyal N, Camacho F, Mangano J, Goldenberg D. Evaluating for a geospatial relationship between radon levels and thyroid cancer in Pennsylvania. Laryngoscope. 2015;125(1):E45–9.
63. Oakland C, Meliker JR. County-level radon and incidence of female thyroid cancer in Iowa, New Jersey, and Wisconsin, USA. Toxics. 2018;6(1):17.
64. Kristbjornsdottir A, Rafnsson V. Incidence of cancer among residents of high temperature geothermal areas in Iceland: a census based study 1981 to 2010. Environ Heal. 2012;11(1):1–12.
65. Henson MC, Chedrese PJ. Endocrine disruption by cadmium, a common environmental toxicant with paradoxical effects on reproduction. Exp Biol Med. 2004;229(5):383–92.
66. Hajizadeh N, Pourhoseingholi MA, Baghestani A. Incidence rate of thyroid cancer in Iranian population, trend analysis from 2003 to 2009. Int J Epidemiol Res. 2015;2(1):12–7.
67. Vali M, Hassanzadeh J, Mirahmadizadeh A, Hoseini M, Dehghani S, Maleki Z, et al. Effect of meteorological factors and Air Quality Index on the COVID-19 epidemiological characteristics: an ecological study among 210 countries. Environ Sci Pollut Res. 2021;1–11.
68. Allen SI, Foulds J, Wasserman E, Veldheer S, Hrabovsky S, Yingst J, et al. Peer Reviewed: Tobacco Use Among Middle and High School Students in Pennsylvania. Prev Chronic Dis. 2018;15.
69. Rudatsikira E, Muula AS, Siziya S. Current cigarette smoking among in-school American youth: results from the 2004 National Youth Tobacco Survey. Int J Equity Health. 2009;8(1):1–9.
70. Pieraccini G, Furlanetto S, Orlandini S, Bartolucci G, Giannini I, Pinzauti S, et al. Identification and determination of mainstream and sidestream smoke components in different brands and types of cigarettes by means of solid-phase microextraction–gas chromatography–mass spectrometry. J Chromatogr A. 2008;1180(1–2):138–50.
71. Group IW. IARC monographs on the evaluation of carcinogenic risks to humans. Lyon Int Agency Res Cancer. 2012.
72. Burguet A, Kaminski M, Truffert P, Menget A, Marpeau L, Voyer M, et al. Does smoking in pregnancy modify the impact of antenatal steroids on neonatal respiratory distress syndrome? Results of the Epipage study. Arch Dis Childhood-Fetal Neonatal Ed. 2005;90(1):F41–5.
73. Pontikides N, Krassas GE. Influence of cigarette smoking on thyroid function, goiter formation and autoimmune thyroid disorders. HORMONES-ATHENS-. 2002;1:91–8.
74. Lim SS, Vos T, Flaxman AD, Danaei G, Shibuya K, Adair-Rohani H, et al. A comparative risk assessment of burden of disease and injury attributable to 67 risk factors and risk factor clusters in 21 regions, 1990–2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet. 2012;380(9859):2224–60.
75. Benedetti M, Zona A, Contiero P, Armiento ED, Iavarone I. Incidence of Thyroid Cancer in Italian Contaminated Sites. 2021;
76. Organization WH. WHO air quality guidelines for particulate matter, ozone, nitrose dioxide and sulfur dioxide. VOC volatile Org Compd. 2005.
Files
IssueVol 6 No 1 (2021): Winter 2021 QRcode
SectionOriginal Research
DOI https://doi.org/10.18502/japh.v6i1.7603
Keywords
Particulate matter 2.5 (PM2.5); Thyroid cancer; Air pollution; Cancer

Rights and permissions
Creative Commons License This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
How to Cite
1.
Dehghani S, Vali M, Abedinzade A. Ambient air pollution exposure and thyroid cancer incidence in Iran. japh. 2021;6(1):30-41.