BMC Womens Health. 2022 Jan 08;22(1):3. doi: 10.1186/s12905-021-01586-w.

Joint effect of particulate matter and cigarette smoke on women's sex hormones.

BMC women's health

Anna Merklinger-Gruchala, Grazyna Jasienska, Inger Thune, Maria Kapiszewska

PMID: 34996432 DOI: 10.1186/s12905-021-01586-w

Abstract

BACKGROUND: Although relationships between exposure to air pollution and reproductive health are broadly studied, mechanisms behind these phenomena are still unknown. The aim of the study was to assess whether exposure to particulate matter (PM10) and tobacco smoking have an impact on menstrual profiles of 17β-estradiol (E2) and progesterone (P) and the E2/P ratio.

METHODS: Levels of sex hormones were measured daily in saliva during the entire menstrual cycle among 132 healthy, urban women. Exposure to smoking (active or passive) was assessed by questionnaire, whilst exposure to PM10 with municipal monitoring data.

RESULTS: During the early luteal phase, profiles of E2 were elevated among women with higher versus lower exposure to PM10 (p = 0.02, post-hoc tests). Among those who were exposed versus unexposed to tobacco smoking, the levels of mean E2 measured during the entire cycle were higher (p = 0.02). The difference in mean E2 levels between the group of joint exposure (i.e. to high PM10 and passive or active smoking) versus the reference group (low PM10, no smoking) was statistically significant at p = 0.03 (18.4 vs. 12.4 pmol/l, respectively). The E2/P ratios were higher among women with higher versus lower exposure to PM10 and this difference was seen only in the early luteal phase (p = 0.01, exploratory post-hoc tests).

CONCLUSIONS: We found that PM10 and tobacco smoking affect ovarian hormones independently and do not interact with each other. Both exposures appear to have estrogenic effects even though women's susceptibility to these effects differs across the menstrual cycle. We propose that the hormonal mechanisms are involved in observed relationships between air pollution and smoking with women's reproductive health.

© 2022. The Author(s).

Keywords: Air pollution; Cigarette smoke; Estradiol; Estrogens; Gonadal Steroid Hormones; Luteal phase; Menstrual cycle; PAH; PM10; Particulate matter; Polycyclic aromatic hydrocarbons; Progesterone; Reproductive health

References

1. Lelieveld J, Pozzer A, Poschl U, Fnais M, Haines A, Munzel T. Loss of life expectancy from air pollution compared to other risk factors: a worldwide perspective. Cardiovasc Res. 2020;116(11):1910–7. - PubMed
2. Reitsma MB, Kendrick PJ, Ababneh E, Abbafati C, Abbasi-Kangevari M, Abdoli A, Abedi A, Abhilash ES, Abila DB, Aboyans V, Abu-Rmeileh NM. Spatial, temporal, and demographic patterns in prevalence of smoking tobacco use and attributable disease burden in 204 countries and territories, 1990–2019: a systematic analysis from the Global Burden of Disease Study 2019. Lancet. 2021;397(10292):2337–60. - PubMed
3. Jedrychowski WA, Majewska R, Spengler JD, Camann D, Roen EL, Perera FP. Prenatal exposure to fine particles and polycyclic aromatic hydrocarbons and birth outcomes: a two-pollutant approach. Int Arch Occup Environ Health. 2017;90(3):255–64. - PubMed
4. Merklinger-Gruchala A, Jasienska G, Kapiszewska M. Effect of air pollution on menstrual cycle length-a prognostic factor of women’s reproductive health. Int J Environ Res Public Health. 2017;14(7):816. - PubMed
5. Bolden AL, Rochester JR, Schultz K, Kwiatkowski CF. Polycyclic aromatic hydrocarbons and female reproductive health: a scoping review. Reprod Toxicol. 2017;73:61–74. - PubMed
6. Gouveia N, Bremner SA, Novaes HM. Association between ambient air pollution and birth weight in Sao Paulo, Brazil. J Epidemiol Community Health. 2004;58(1):11–7. - PubMed
7. Dechanet C, Brunet C, Anahory T, Hamamah S, Hedon B, Dechaud H. Effects of cigarette smoking on female reproduction: from oocyte to embryo (part I). Gynecol Obstet Fertil. 2011;39(10):559–66. - PubMed
8. Prior JC. Women’s reproductive system as balanced estradiol and progesterone actions—a revolutionary, paradigm-shifting concept in women’s health. Drug Discov Today Disease Models. 2020;32:31–4. - PubMed
9. Shalom-Paz E, Aslih N, Samara N, Michaeli M, Ellenbogen A. Late follicular progesterone to estradiol ratio is not influenced by protocols or gonadotropins used. Reprod Biol Endocrinol. 2015;13:119. - PubMed
10. Mascarenhas M, Kamath MS, Chandy A, Kunjummen AT. Progesterone/estradiol ratio as a predictor in the ART cycles with premature progesterone elevation on the day of hCG trigger. J Reprod Infertil. 2015;16(3):155–61. - PubMed
11. Band PR, Le ND, Fang R, Deschamps M. Carcinogenic and endocrine disrupting effects of cigarette smoke and risk of breast cancer. Lancet. 2002;360(9339):1044–9. - PubMed
12. Hecht SS. Tobacco smoke carcinogens and breast cancer. Environ Mol Mutagen. 2002;39(2–3):119–26. - PubMed
13. Jasienska G, Thune I. Lifestyle, hormones, and risk of breast cancer. BMJ. 2001;322(7286):586–7. - PubMed
14. Rosenberg CR, Pasternack BS, Shore RE, Koenig KL, Toniolo PG. Premenopausal estradiol levels and the risk of breast cancer: a new method of controlling for day of the menstrual cycle. Am J Epidemiol. 1994;140(6):518–25. - PubMed
15. Tansavatdi K, McClain B, Herrington DM. The effects of smoking on estradiol metabolism. Minerva Ginecol. 2004;56(1):105–14. - PubMed
16. Windham GC, Mitchell P, Anderson M, Lasley BL. Cigarette smoking and effects on hormone function in premenopausal women. Environ Health Perspect. 2005;113(10):1285–90. - PubMed
17. Teil MJ, Moreau-Guigon E, Blanchard M, Alliot F, Gasperi J, Cladiere M, Mandin C, Moukhtar S, Chevreuil M. Endocrine disrupting compounds in gaseous and particulate outdoor air phases according to environmental factors. Chemosphere. 2016;146:94–104. - PubMed
18. Wenger D, Gerecke AC, Heeb NV, Schmid P, Hueglin C, Naegeli H, Zenobi R. In vitro estrogenicity of ambient particulate matter: contribution of hydroxylated polycyclic aromatic hydrocarbons. J Appl Toxicol. 2009;29(3):223–32. - PubMed
19. Ravindra K, Mittal AK, Van Grieken R. Health risk assessment of urban suspended particulate matter with special reference to polycyclic aromatic hydrocarbons: a review. Rev Environ Health. 2001;16(3):169–89. - PubMed
20. Bonner MR, Han D, Nie J, Rogerson P, Vena JE, Muti P, Trevisan M, Edge SB, Freudenheim JL. Breast cancer risk and exposure in early life to polycyclic aromatic hydrocarbons using total suspended particulates as a proxy measure. Cancer Epidemiol Biomark Prev. 2005;14(1):53–60. - PubMed
21. Bostrom CE, Gerde P, Hanberg A, Jernstrom B, Johansson C, Kyrklund T, Rannug A, Tornqvist M, Victorin K, Westerholm R. Cancer risk assessment, indicators, and guidelines for polycyclic aromatic hydrocarbons in the ambient air. Environ Health Perspect. 2002;110(Suppl 3):451–88. - PubMed
22. Akyuz M, Cabuk H. Meteorological variations of PM2.5/PM10 concentrations and particle-associated polycyclic aromatic hydrocarbons in the atmospheric environment of Zonguldak, Turkey. J Hazard Mater. 2009;170(1):13–21. - PubMed
23. Bekki K, Toriba A, Tang N, Kameda T, Hayakawa K. Biological effects of polycyclic aromatic hydrocarbon derivatives. J Uoeh. 2013;35(1):17–24. - PubMed
24. Santodonato J. Review of the estrogenic and antiestrogenic activity of polycyclic aromatic hydrocarbons: relationship to carcinogenicity. Chemosphere. 1997;34(4):835–48. - PubMed
25. White AJ, Bradshaw PT, Hamra GB. Air pollution and breast cancer: a review. Curr Epidemiol Rep. 2018;5(2):92–100. - PubMed
26. Akhmedkhanov A, Zeleniuch-Jacquotte A, Toniolo P. Role of exogenous and endogenous hormones in endometrial cancer: review of the evidence and research perspectives. Ann N Y Acad Sci. 2001;943:296–315. - PubMed
27. Schindler AE. Progestogen deficiency and endometrial cancer risk. Maturitas. 2009;62(4):334–7. - PubMed
28. Lipson SF, Ellison PT. Comparison of salivary steroid profiles in naturally occurring conception and non-conception cycles. Hum Reprod. 1996;11(10):2090–6. - PubMed
29. Jasienska G, Ziomkiewicz A, Thune I, Lipson SF, Ellison PT. Habitual physical activity and estradiol levels in women of reproductive age. Eur J Cancer Prev. 2006;15(5):439–45. - PubMed
30. Jasienska G, Ellison PT. Energetic factors and seasonal changes in ovarian function in women from rural Poland. Am J Hum Biol. 2004;16(5):563–80. - PubMed
31. Vandenbroucke JP, von Elm E, Altman DG, Gotzsche PC, Mulrow CD, Pocock SJ, Poole C, Schlesselman JJ, Egger M. Strengthening the Reporting of Observational Studies in Epidemiology (STROBE): explanation and elaboration. Epidemiology. 2007;18(6):805–35. - PubMed
32. Cohen J. A power primer. Psychol Bull. 1992;112(1):155–9. - PubMed
33. Aleksandropoulou V, Eleftheriadis K, Diapouli E, Torseth K, Lazaridis M. Assessing PM10 source reduction in urban agglomerations for air quality compliance. J Environ Monit. 2012;14(1):266–78. - PubMed
34. Amarillo AC, Tavera Busso I, Carreras H. Exposure to polycyclic aromatic hydrocarbons in urban environments: health risk assessment by age groups. Environ Pollut. 2014;195:157–62. - PubMed
35. Bostrom CE, Almen J, Steen B, Westerholm R. Human exposure to urban air pollution. Environ Health Perspect. 1994;102(Suppl 4):39–47. - PubMed
36. Wu J, Laurent O, Li L, Hu J, Kleeman M. Adverse reproductive health outcomes and exposure to gaseous and particulate-matter air pollution in pregnant women. Res Rep Health Eff Inst. 2016;188:1–58. - PubMed
37. Conforti A, Mascia M, Cioffi G, De Angelis C, Coppola G, De Rosa P, Pivonello R, Alviggi C, De Placido G. Air pollution and female fertility: a systematic review of literature. Reprod Biol Endocrinol. 2018;16(1):117. - PubMed
38. Sram R. Impact of air pollution on reproductive health. Environ Health Perspect. 1999;107(11):A542-543. - PubMed
39. Zhang Y, Yang J, Ma L. The influence of ambient air pollution on reproductive health: current situation and prospects. Zhonghua Yu Fang Yi Xue Za Zhi. 2017;51(3):193–6. - PubMed
40. Shimada T, Murajama N, Tanaka K, Takenaka S, Imai Y, Hopkins NE, Foroozesh MK, Alworth WL, Yamazaki H, Guengerich FP, et al. Interaction of polycyclic aromatic hydrocarbons with human cytochrome P450 1B1 in inhibiting catalytic activity. Chem Res Toxicol. 2008;21(12):2313–23. - PubMed
41. Tarnow P, Tralau T, Luch A. Chemical activation of estrogen and aryl hydrocarbon receptor signalling pathways and their interaction in toxicology and metabolism. Expert Opin Drug Metab Toxicol. 2019;15(3):219–29. - PubMed
42. Najmeddin A, Keshavarzi B. Health risk assessment and source apportionment of polycyclic aromatic hydrocarbons associated with PM10 and road deposited dust in Ahvaz metropolis of Iran. Environ Geochem Health. 2019;41(3):1267–90. - PubMed
43. Wiriya W, Prapamontol T, Chantara S. PM10-bound polycyclic aromatic hydrocarbons in Chiang Mai (Thailand): seasonal variations, source identification, health risk assessment and their relationship to air-mass movement. Atmos Res. 2013;124:109–22. - PubMed
44. Matthews J, Gustafsson JA. Estrogen receptor and aryl hydrocarbon receptor signaling pathways. Nucl Recept Signal. 2006;4:e016. - PubMed
45. Gozgit JM, Nestor KM, Fasco MJ, Pentecost BT, Arcaro KF. Differential action of polycyclic aromatic hydrocarbons on endogenous estrogen-responsive genes and on a transfected estrogen-responsive reporter in MCF-7 cells. Toxicol Appl Pharmacol. 2004;196(1):58–67. - PubMed
46. Kamiya M, Toriba A, Onoda Y, Kizu R, Hayakawa K. Evaluation of estrogenic activities of hydroxylated polycyclic aromatic hydrocarbons in cigarette smoke condensate. Food Chem Toxicol. 2005;43(7):1017–27. - PubMed
47. Shimada T, Guengerich FP. Inhibition of human cytochrome P450 1A1-, 1A2-, and 1B1-mediated activation of procarcinogens to genotoxic metabolites by polycyclic aromatic hydrocarbons. Chem Res Toxicol. 2006;19(2):288–94. - PubMed
48. Shoham Z, Schachter M. Estrogen biosynthesis—regulation, action, remote effects, and value of monitoring in ovarian stimulation cycles. Fertil Steril. 1996;65(4):687–701. - PubMed
49. Payne AH, Hales DB. Overview of steroidogenic enzymes in the pathway from cholesterol to active steroid hormones. Endocr Rev. 2004;25(6):947–70. - PubMed
50. Christou M, Savas U, Schroeder S, Shen X, Thompson T, Gould MN, Jefcoate CR. Cytochromes CYP1A1 and CYP1B1 in the rat mammary gland: cell-specific expression and regulation by polycyclic aromatic hydrocarbons and hormones. Mol Cell Endocrinol. 1995;115(1):41–50. - PubMed
51. Son DS, Roby KF, Rozman KK, Terranova PF. Estradiol enhances and estriol inhibits the expression of CYP1A1 induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin in a mouse ovarian cancer cell line. Toxicology. 2002;176(3):229–43. - PubMed
52. Ricci MS, Toscano DG, Mattingly CJ, Toscano WA Jr. Estrogen receptor reduces CYP1A1 induction in cultured human endometrial cells. J Biol Chem. 1999;274(6):3430–8. - PubMed
53. Thomas MP, Potter BV. The structural biology of oestrogen metabolism. J Steroid Biochem Mol Biol. 2013;137:27–49. - PubMed
54. Williams GP, Darbre PD. Low-dose environmental endocrine disruptors, increase aromatase activity, estradiol biosynthesis and cell proliferation in human breast cells. Mol Cell Endocrinol. 2019;486:55–64. - PubMed
55. Saito R, Miki Y, Hata S, Ishida T, Suzuki T, Ohuchi N, Sasano H. Aryl hydrocarbon receptor induced intratumoral aromatase in breast cancer. Breast Cancer Res Treat. 2017;161(3):399–407. - PubMed
56. Johansson HKL, Damdimopoulou P, van Duursen MBM, Boberg J, Franssen D, de Cock M, Jaager K, Wagner M, Velthut-Meikas A, Xie Y, et al. Putative adverse outcome pathways for female reproductive disorders to improve testing and regulation of chemicals. Arch Toxicol. 2020;94:3359–79. - PubMed
57. Hernandez-Ochoa I, Karman BN, Flaws JA. The role of the aryl hydrocarbon receptor in the female reproductive system. Biochem Pharmacol. 2009;77(4):547–59. - PubMed
58. Perin PM, Maluf M, Czeresnia CE, Januario DA, Saldiva PH. Impact of short-term preconceptional exposure to particulate air pollution on treatment outcome in couples undergoing in vitro fertilization and embryo transfer (IVF/ET). J Assist Reprod Genet. 2010;27(7):371–82. - PubMed
59. Enkhmaa D, Warburton N, Javzandulam B, Uyanga J, Khishigsuren Y, Lodoysamba S, Enkhtur S, Warburton D. Seasonal ambient air pollution correlates strongly with spontaneous abortion in Mongolia. BMC Pregnancy Childbirth. 2014;14:146. - PubMed
60. Merklinger-Gruchala A, Kapiszewska M. Association between PM10 air pollution and birth weight after full-term pregnancy in Krakow city 1995–2009—trimester specificity. Ann Agric Environ Med. 2015;22(2):265–70. - PubMed
61. Ma WG, Song H, Das SK, Paria BC, Dey SK. Estrogen is a critical determinant that specifies the duration of the window of uterine receptivity for implantation. Proc Natl Acad Sci U S A. 2003;100(5):2963–8. - PubMed
62. Reizer M, Juda-Rezler K. Explaining the high PM10 concentrations observed in Polish urban areas. Air Qual Atmos Health. 2016;9:517–31. - PubMed
63. Gini M, Lianou M, Chalbot MC, Kotronarou A, Kavouras IG, Helmis CG. Quantification of environmental tobacco smoke contribution on outdoor particulate aliphatic and polycyclic aromatic hydrocarbons. Arch Environ Contam Toxicol. 2013;64(3):347–56. - PubMed
64. National Research Council. Environmental tobacco smoke: measuring exposures and assessing health effects. Washington, DC: National Research Council; 1986. - PubMed
65. Soldin OP, Makambi KH, Soldin SJ, O’Mara DM. Steroid hormone levels associated with passive and active smoking. Steroids. 2011;76(7):653–9. - PubMed
66. Thomas EJ, Edridge W, Weddell A, McGill A, McGarrigle HH. The impact of cigarette smoking on the plasma concentrations of gonadotrophins, ovarian steroids and androgens and upon the metabolism of oestrogens in the human female. Hum Reprod. 1993;8(8):1187–93. - PubMed
67. Whitcomb BW, Bodach SD, Mumford SL, Perkins NJ, Trevisan M, Wactawski-Wende J, Liu A, Schisterman EF. Ovarian function and cigarette smoking. Paediatr Perinat Epidemiol. 2010;24(5):433–40. - PubMed
68. Sterzik K, Strehler E, De Santo M, Trumpp N, Abt M, Rosenbusch B, Schneider A. Influence of smoking on fertility in women attending an in vitro fertilization program. Fertil Steril. 1996;65(4):810–4. - PubMed
69. Berta L, Frairia R, Fortunati N, Fazzari A, Gaidano G. Smoking effects on the hormonal balance of fertile women. Horm Res. 1992;37(1–2):45–8. - PubMed
70. Key TJ, Pike MC, Baron JA, Moore JW, Wang DY, Thomas BS, Bulbrook RD. Cigarette smoking and steroid hormones in women. J Steroid Biochem Mol Biol. 1991;39(4A):529–34. - PubMed
71. Kant N, Müller R, Braun M, Gerber A, Groneberg D. Particulate matter in second-hand smoke emitted from different cigarette sizes and types of the brand vogue mainly smoked by women. Int J Environ Res Public Health. 2016;13:799–809. - PubMed
72. Rebagliato M. Validation of self reported smoking. J Epidemiol Community Health. 2002;56(3):163–4. - PubMed
73. Zumoff B, Miller L, Levit CD, Miller EH, Heinz U, Kalin M, Denman H, Jandorek R, Rosenfeld RS. The effect of smoking on serum progesterone, estradiol, and luteinizing hormone levels over a menstrual cycle in normal women. Steroids. 1990;55(11):507–11. - PubMed
74. Brand JS, Chan MF, Dowsett M, Folkerd E, Wareham NJ, Luben RN, van der Schouw YT, Khaw KT. Cigarette smoking and endogenous sex hormones in postmenopausal women. J Clin Endocrinol Metab. 2011;96(10):3184–92. - PubMed
75. Benowitz NL. Cotinine as a biomarker of environmental tobacco smoke exposure. Epidemiol Rev. 1996;18(2):188–204. - PubMed
76. Wray JM, Gass JC, Miller EI, Wilkins DG, Rollins DE, Tiffany ST. A comparative evaluation of self-report and biological measures of cigarette use in nondaily smokers. Psychol Assess. 2016;28(9):1043–50. - PubMed
77. Vartiainen E, Seppala T, Lillsunde P, Puska P. Validation of self reported smoking by serum cotinine measurement in a community-based study. J Epidemiol Community Health. 2002;56(3):167–70. - PubMed
78. Jedrychowski W, Bendkowska I, Flak E, Penar A, Jacek R, Kaim I, Spengler JD, Camann D, Perera FP. Estimated risk for altered fetal growth resulting from exposure to fine particles during pregnancy: an epidemiologic prospective cohort study in Poland. Environ Health Perspect. 2004;112(14):1398–402. - PubMed
79. Scibor M, Galbarczyk A, Jasienska G. Living well with pollution? The impact of the concentration of PM2.5 on the quality of life of patients with asthma. Int J Environ Res Public Health. 2019;16(14):2502. - PubMed
80. Rosner W. Free estradiol and sex hormone-binding globulin. Steroids. 2015;99(Pt A):113–6. - PubMed
81. Gandara BK, Leresche L, Mancl L. Patterns of salivary estradiol and progesterone across the menstrual cycle. Ann N Y Acad Sci. 2007;1098:446–50. - PubMed
82. Jasienska G, Jasienski M. Interpopulation, interindividual, intercycle, and intracycle natural variation in progesterone levels: a quantitative assessment and implications for population studies. Am J Hum Biol. 2008;20(1):35–42. - PubMed
83. Chatterton RT Jr, Mateo ET, Hou N, Rademaker AW, Acharya S, Jordan VC, Morrow M. Characteristics of salivary profiles of oestradiol and progesterone in premenopausal women. J Endocrinol. 2005;186(1):77–84. - PubMed
84. Celec P, Ostanikova D, Skoknova M, Hodosy J, Putz Z, Kudela M. Salivary sex hormones during the menstrual cycle. Endocr J. 2009;56(3):521–3. - PubMed
85. Dechaud H, Ravard C, Claustrat F, de la Perriere AB, Pugeat M. Xenoestrogen interaction with human sex hormone-binding globulin (hSHBG). Steroids. 1999;64(5):328–34. - PubMed

Publication Types

• Journal Article

Grant support

• UMO-2017/25/B/NZ7/01509/the national science centre (poland)
• 213997/H10/the norwegian research council
• N N404 055 136/ministry of science and higher education
• WZiNM/DS/3/2016/ministry of science and higher education
• TP 49257 - 05087/the norwegian cancer society
• 59010/the foundation for the norwegian health and rehabilitation organizations