Abstract
Objective
This study aimed to explore the associations of tobacco smoke exposure (TSE) and heavy metal exposure on sex hormones and the joint effects between them in adult males.
Methods
The study used data of 2244 adult males from the National Health and Nutrition Examination Survey (NHANES, 2013–2016). Weighted linear regression models were used to calculate their beta (β) coefficients and corresponding confidence interval (95% CI), which assessed the joint effects of TSE and heavy metals on sex hormones.
Results
Sex hormone-binding globulin (SHBG) showed a positive association with increased per standard deviation (SD) for cotinine (β=0.024 [0.004, 0.043]; P<0.001), lead (β=0.021 [0.002, 0.039]; P=0.028), and cadmium (β=0.034 [0.015, 0.053]; P<0.001). Manganese was positively associated with estradiol (E2) (β=0.025 [0.009, 0.042]; P=0.002). The subjects with higher cadmium levels were more likely to have higher total testosterone (TT) (β=0.042 [0.023, 0.062]; P<0.001). TSE and lead exerted synergistic effects on TT (p for interaction = 0.015) and E2 (p for interaction = 0.009), as also did TSE and cadmium on SHBG (p for interaction = 0.037). Compared with the reference group, TSE participants who were exposed to high concentrations of lead, cadmium, mercury, and manganese had significantly elevated TT levels, but these high levels presented no significant association with E2 levels. A significantly higher level of SHBG among TSE participants was detected in high concentrations for lead, cadmium, and mercury.
Conclusion
TSE exacerbated sex hormone imbalances when combined with high levels of metal exposure. Smoking cessation is crucial, especially in the case of high levels of occupational exposure to heavy metals.
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Data availability
The data used to support the findings of this study are available from the corresponding author upon request.
References
Tao C, Li Z, Fan Y, Li X, Qian H, Yu H, Xu QQ, Lu CC (2021) Independent and combined associations of urinary heavy metals exposure and serum sex hormones among adults in NHANES 2013–2016. Environ Pollut 281:117097
Gatzke-Kopp LM, Riis JL, Ahmadi H, Piccerillo HL, Granger DA, Blair CB, Thomas EA (2023) Environmental tobacco smoke exposure is associated with increased levels of metals in children’s saliva. J Expo Sci Environ Epidemiol 33(6):903–10
Gianatti EJ, Grossmann M (2020) Testosterone deficiency in men with Type 2 diabetes: pathophysiology and treatment. Diabet Med 37(2):174–86
Paller CJ, Shiels MS, Rohrmann S, Basaria S, Rifai N, Nelson W, Platz EA, Dobs A (2009) Relationship of sex steroid hormones with bone mineral density (BMD) in a nationally representative sample of men. Clin Endocrinol 70(1):26–34
Ruige JB, Mahmoud AM, De Bacquer D, Kaufman JM (2011) Endogenous testosterone and cardiovascular disease in healthy men: a meta-analysis. Heart 97(11):870–5
Boibessot C, Toren P (2018) Sex steroids in the tumor microenvironment and prostate cancer progression. Endocr Relat Cancer 25(3):R179-r96
Kresovich JK, Argos M, Turyk ME (2015) Associations of lead and cadmium with sex hormones in adult males. Environ Res 142:25–33
Bush D, Goniewicz ML (2015) A pilot study on nicotine residues in houses of electronic cigarette users, tobacco smokers, and non-users of nicotine-containing products. Int J Drug Policy 26(6):609–11
Ozgur K, Isikoglu M, Seleker M, Donmez L (2005) Semen quality of smoking and non-smoking men in infertile couples in a Turkish population. Arch Gynecol Obstet 271(2):109–12
Pasqualotto FF, Sobreiro BP, Hallak J, Pasqualotto EB, Lucon AM (2006) Cigarette smoking is related to a decrease in semen volume in a population of fertile men. BJU Int 97(2):324–6
Blanco-Muñoz J, Lacasaña M, Aguilar-Garduño C (2012) Effect of current tobacco consumption on the male reproductive hormone profile. Sci Total Environ 426:100–5
Ravnborg TL, Jensen TK, Andersson AM, Toppari J, Skakkebaek NE, Jørgensen N (2011) Prenatal and adult exposures to smoking are associated with adverse effects on reproductive hormones, semen quality, final height and body mass index. Hum Reprod 26(5):1000–11
Wang Y, Tang Y, Li Z, Hua Q, Wang L, Song X, Zou BB, Ding M, Zhao JS, Tang CL (2020) Joint toxicity of a multi-heavy metal mixture and chemoprevention in sprague dawley rats. Int J Environ Res Public Health 17(4):1451
Chen YW, Yang CY, Huang CF, Hung DZ, Leung YM, Liu SH (2009) Heavy metals, islet function and diabetes development. Islets 1(3):169–76
Zeng X, Jin T, Buchet JP, Jiang X, Kong Q, Ye T, Bernard A, Nordberg GF (2004) Impact of cadmium exposure on male sex hormones: a population-based study in China. Environ Res 96(3):338–44
Jurasović J, Cvitković P, Pizent A, Colak B, Telisman S (2004) Semen quality and reproductive endocrine function with regard to blood cadmium in Croatian male subjects. Biometals 17(6):735–43
Piascik MT, Champney RB, Kasarskis EJ, Forrester T (1985) A method for enriching the cadmium content of cigarette smoke and effect of exposure to this smoke on coronary vascular reactivity in the rat. Toxicol Appl Pharmacol 81(3 Pt 1):525–32
Lewis RC, Meeker JD (2015) Biomarkers of exposure to molybdenum and other metals in relation to testosterone among men from the United States National Health and Nutrition Examination Survey 2011–2012. Fertil Steril 103(1):172–8
Nagata C, Konishi K, Goto Y, Tamura T, Wada K, Hayashi M, Takeda N, Yasuda K (2016) Associations of urinary cadmium with circulating sex hormone levels in pre- and postmenopausal Japanese women. Environ Res 150:82–7
Pinto E, Cruz M, Ramos P, Santos A, Almeida A (2017) Metals transfer from tobacco to cigarette smoke: Evidences in smokers’ lung tissue. J Hazard Mater 325:31–5
Shakeri MT, Nezami H, Nakhaee S, Aaseth J, Mehrpour O (2021) Assessing heavy metal burden among cigarette smokers and non-smoking individuals in Iran: Cluster analysis and principal component analysis. Biol Trace Elem Res 199(11):4036–44
Dai H, Zhang H, Wang H, Niu J, Luo B, Yan J, Li X (2023) The effect of smoking habits on blood cadmium and lead levels in residents living near a mining and smelting area in Northwest China: a cross-sectional study. Biol Trace Elem Res 201(3):1101–11
Lee W, Lee S, Roh J, Won JU, Yoon JH (2017) The association between involuntary smoking exposure with urine cotinine level and blood cadmium level in general non-smoking populations. J Korean Med Sci 32(4):568–75
Matt GE, Quintana PJE, Hoh E, Dodder NG, Mahabee-Gittens EM, Padilla S, Markman L, Watanabe K (2021) Tobacco smoke is a likely source of lead and cadmium in settled house dust. J Trace Elem Med Biol 63:126656
Tian Y, Hou H, Zhu F, Wang A, Liu Y, Hu Q (2014) Simultaneous determination of chromium, cadmium, and lead and evaluation of the correlation between chromium and cotinine in Chinese smokers. Biol Trace Elem Res 158(1):9–14
Wang Y, Fang Y, Witting PK, Charchar FJ, Sobey CG, Drummond GR, Golledge J (2023) Dietary fatty acids and mortality risk from heart disease in US adults: an analysis based on NHANES. Sci Rep 13(1):1614
Li C, Wang Y, Wang S, Huang L (2023) Smoke exposure reduces the protective effect of physical activity on hypertension: Evidence from the national health and nutrition examination survey (NHANES) 2013–2018. Int J Environ Res Public Health 20(3):2532
Liu Q, Hu S, Fan F, Zheng Z, Zhou X, Zhang Y (2023) Association of blood metals with serum sex hormones in adults: A cross-sectional study. Environ Sci Pollut Res Int 30(26):69628–38
Willers S, Gerhardsson L, Lundh T (2005) Environmental tobacco smoke (ETS) exposure in children with asthma-relation between lead and cadmium, and cotinine concentrations in urine. Respir Med 99(12):1521–7
Afridi HI, Kazi TG, Talpur FN, Brabazon D, Naher S (2013) Estimation of toxic elements in the samples of different cigarettes and their impact on human health of Irish hypertensive consumers. Clin Chim Acta 426:51–7
Repić A, Bulat P, Antonijević B, Antunović M, Džudović J, Buha A, Bulat Z (2020) The influence of smoking habits on cadmium and lead blood levels in the Serbian adult people. Environ Sci Pollut Res Int 27(1):751–60
Samrat Y, Kim ND, Kimberly Y, Patrick JP, Kenneth MA, Erin NH (2015) Secondhand Tobacco Smoke Exposure and Neuromotor Function in Rural Children. J Pediatr 167(2):253–9.e1
Chen C, Wang NJ, Nie XM, Han B, Li Q, Chen Y, Zhai HL, Zhu CF, Chen YC, Xia FZ (2016) Blood cadmium level associates with lower testosterone and sex hormone-binding globulin in Chinese men: from SPECT-China study, 2014. Biol Trace Elem Res 171(1):71–8
Zhao J, Leung JYY, Lin SL, Mary Schooling C (2016) Cigarette smoking and testosterone in men and women: A systematic review and meta-analysis of observational studies. Prev Med 85:1–10
Schooling CM (2015) Smoking, sex, risk factors and abdominal aortic aneurysm: is it all down to testosterone? J Epidemiol Community Health 69(5):495
Järup L, Berglund M, Elinder CG, Nordberg G, Vahter M (1998) Health effects of cadmium exposure–a review of the literature and a risk estimate. Scand J Work Environ Health 24(Suppl 1):1–51
Ho KJ, Chen TH, Yang CC, Chuang YC, Chuang HY (2021) Interaction of smoking and lead exposure among carriers of genetic variants associated with a higher level of oxidative stress indicators. Int J Environ Res Public Health 18(16):8325
Acknowledgements
The authors thank the National Health and Nutrition Examination Survey for publicly available data.
Funding
This manuscript was supported by the Scientific Research Promotion Plan of Anhui Medical University (2021xkjT013), Project of Anhui Provincial Academic and Technical Leaders for Scientific Research Activities (2022D321), Projects of Anhui Provincial Key Laboratory of Population Health and Aristogenics (JKYS20225), and National Natural Science Foundation of China (No.72374005).
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Xiaoguo Hua performed the data analyses and wrote the manuscript. Rui Hu revised the final typescript. Cai Chen searched for and evaluated the retrieved articles. Xiqiu Feng and Jiangjie Sun contributed to the conception of the study. Xiujun Zhang were responsible for the communication of the paper.
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The application of every technique followed all applicable rules and regulations. The US National Center for Healthcare Statistics (NCHS) granted permission for the implementation of NHANES for 2013–2016.
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Hua, X., Hu, R., Chen, C. et al. Joint effects of tobacco smoke exposure and heavy metals on serum sex hormones in adult males. Hormones (2024). https://doi.org/10.1007/s42000-024-00600-8
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DOI: https://doi.org/10.1007/s42000-024-00600-8