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Association between aldehyde exposure and sex steroid hormones among adults

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Abstract

Exogenous and endogenous exposure to aldehydes is seen worldwide. Aldehydes are closely associated with human diseases, especially reproductive toxicity. However, the effect of aldehyde exposure on sex steroid hormones among adults remains uninvestigated. A total of 851 participants aged over 18 years were included in this cross-sectional analysis based on data from National Health and Nutrition Examination Survey (NHANES) 2013–2014. Serum aldehyde concentrations were quantified following an automated analytical method. Sex steroid hormones including total testosterone, estradiol, and sex hormone binding globulin (SHBG) were detected. Multivariate linear regression models, forest plots, generalized additive model (GAM), and smooth curve fitting analysis were used to assess the associations between quartiles of aldehydes and sex steroid hormones levels after adjusting for potential confounders. Butyraldehyde and propanaldehyde were found to be negatively associated with estradiol and SHBG in females and males, respectively. β values with 95% confidence intervals (95% CIs) were − 20.59 (− 38.30 to − 2.88) for Q2 vs. Q1 of butyraldehyde and − 8.13 (− 14.92 to − 1.33) and − 7.79 (− 14.91 to − 0.67) for Q2 vs. Q1 and Q4 vs. Q1 of propanaldehyde. No significant associations were observed between other aldehydes and sex hormones. In premenopausal women, isopentanaldehyde was inversely associated with serum total testosterone levels (Q4 vs. Q1: OR =  − 7.95, 95% CI: − 15.62 to − 0.27), whereas propanaldehyde was positively associated with serum estradiol concentration (Q3 vs. Q1: β = 28.88, 95% CI: 0.83 to 56.94). Compared with Q1, Q3 of isopentanaldehyde was associated with 3.53 pg/mL higher concentration of estradiol in postmenopausal women (β = 3.53, 95% CI: 0.08 to 6.97). Moreover, in males under 40 years, butyraldehyde and heptanaldehyde were inversely proportional to total testosterone levels and heptanaldehyde and butyraldehyde were negatively associated with estradiol and SHBG. Decreased total testosterone, elevated estradiol, and decreased SHBG levels were found in higher quartiles of benzaldehyde, hexanaldehyde and isopentanaldehyde, and propanaldehyde, respectively, in males aged over 60 years. In male participants aged 40–60 years, only hexanaldehyde was observed to be correlated with higher serum estradiol levels. In conclusion, our current research presented the association between six serum aldehydes and sex hormones. Of note, stratification analyses were conducted in participants with different menopausal statuses and age among males and females. Sex- and age-specific effect of aldehyde exposure on alterations in sex hormone levels were observed. Further studies are warranted to confirm the causal relationship and explore the underlying mechanisms.

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Data availability

Publicly available datasets were analyzed in this study. This data can be found at: https://www.cdc.gov/nchs/nhanes/index.htm.

References

  • Abarikwu SO, Pant AB, Farombi EO (2012) 4-Hydroxynonenal induces mitochondrial-mediated apoptosis and oxidative stress in SH-SY5Y human neuronal cells. Basic Clin Pharmacol Toxicol 110(5):441–448

    CAS  Google Scholar 

  • Alam F, Khan TA, Amjad S et al (2019) Association of oxidative stress with female infertility - a case control study. JPMA J Pakistan Med Assoc 69(5):627–631

    Google Scholar 

  • Buczyńska A, Sidorkiewicz I, Rogucki M et al (2021) Oxidative stress and radioiodine treatment of differentiated thyroid cancer. Sci Rep 11(1):17126

    Google Scholar 

  • Caldwell GS, Lewis C, Pickavance G et al (2011) Exposure to copper and a cytotoxic polyunsaturated aldehyde induces reproductive failure in the marine polychaete Nereis virens (Sars). Aquat Toxicol (amsterdam, Netherlands) 104(1–2):126–134

    CAS  Google Scholar 

  • Cao Y, Li B, Ismail N, et al (2021) Neurotoxicity and underlying mechanisms of endogenous neurotoxins. Int J Mol Sci 22(23):12805

  • Casin KM, Kohr MJ (2020) An emerging perspective on sex differences: Intersecting S-nitrosothiol and aldehyde signaling in the heart. Redox Biol 31:101441

    CAS  Google Scholar 

  • Chen N, Su P, Wang M et al (2018) Ascorbic acid inhibits cadmium-induced disruption of the blood-testis barrier by regulating oxidative stress-mediated p38 MAPK pathways. Environ Sci Pollut Res Int 25(22):21713–21720

    CAS  Google Scholar 

  • Chen PW, Kuo TC, Liu ZS et al (2021) Assessment of the mutagenicity of two common indoor air pollutants, formaldehyde and toluene. Indoor Air 31(5):1353–1363

    CAS  Google Scholar 

  • Destaillats H, Spaulding RS, Charles MJ (2002) Ambient air measurement of acrolein and other carbonyls at the Oakland-San Francisco Bay Bridge toll plaza. Environ Sci Technol 36(10):2227–2235

    CAS  Google Scholar 

  • Dong JJ, Ruan MC, Hang JG et al (2020) The relationship between perinatal exposure to dioxins and serum steroid hormone levels in preschool-aged children at an e-waste region in China. Int J Hyg Environ Health 229:113580

    CAS  Google Scholar 

  • Dost FN (1991) Acute toxicology of components of vegetation smoke. Rev Environ Contam Toxicol 119:1–46

    CAS  Google Scholar 

  • Duong A, Steinmaus C, McHale CM et al (2011) Reproductive and developmental toxicity of formaldehyde: a systematic review. Mutat Res 728(3):118–138

    CAS  Google Scholar 

  • Gibb Z, Lambourne SR, Curry BJ et al (2016) Aldehyde dehydrogenase plays a pivotal role in the maintenance of stallion sperm motility. Biol Reprod 94(6):133

    Google Scholar 

  • Group IMV (2021) Carcinogenicity of acrolein, crotonaldehyde, and arecoline. Lancet Oncol 22(1):19–20

    Google Scholar 

  • Gunness P, Aleksa K, Bend J et al (2011) Acyclovir-induced nephrotoxicity: the role of the acyclovir aldehyde metabolite. Trans Res: J Lab Clin Med 158(5):290–301

    CAS  Google Scholar 

  • Hardt U, Larsson A, Gunnarsson I et al (2018) Autoimmune reactivity to malondialdehyde adducts in systemic lupus erythematosus is associated with disease activity and nephritis. Arthritis Res Ther 20(1):36

    Google Scholar 

  • Hilali N, Vural M, Camuzcuoglu H et al (2013) Increased prolidase activity and oxidative stress in PCOS. Clin Endocrinol 79(1):105–110

    CAS  Google Scholar 

  • Hoque SAM, Umehara T, Kawai T et al (2021) Adverse effect of superoxide-induced mitochondrial damage in granulosa cells on follicular development in mouse ovaries. Free Radical Biol Med 163:344–355

    CAS  Google Scholar 

  • Huang T, Du J, Yu D et al (2022) Oxidative degradation of p-chlorophenol by the persulfate-doped Fe-Mn bimetallic hydroxide, the parametrical significance, and systematical optimization. Environ Sci Pollut Res Int 29(1):1289–1300

    CAS  Google Scholar 

  • Huang T, Liu L, Tao J et al (2018) Microbial fuel cells coupling with the three-dimensional electro-Fenton technique enhances the degradation of methyl orange in the wastewater. Environ Sci Pollut Res Int 25(18):17989–18000

    CAS  Google Scholar 

  • Jarboe LR (2011) YqhD: a broad-substrate range aldehyde reductase with various applications in production of biorenewable fuels and chemicals. Appl Microbiol Biotechnol 89(2):249–257

    CAS  Google Scholar 

  • Kawano T, Matsuse H, Fukahori S et al (2012) Acetaldehyde at a low concentration synergistically exacerbates allergic airway inflammation as an endocrine-disrupting chemical and as a volatile organic compound. Resp Int Rev Thoracic Diseases 84(2):135–141

    CAS  Google Scholar 

  • Khlystov A, Samburova V (2016) Flavoring compounds dominate toxic aldehyde production during e-cigarette vaping. Environ Sci Technol 50(23):13080–13085

    CAS  Google Scholar 

  • Kou Y, Zhao H, Cui D et al (2022) Formaldehyde toxicity in age-related neurological dementia. Ageing Res Rev 73:101512

    CAS  Google Scholar 

  • Lagranha CJ, Deschamps A, Aponte A et al (2010) Sex differences in the phosphorylation of mitochondrial proteins result in reduced production of reactive oxygen species and cardioprotection in females. Circ Res 106(11):1681–1691

    CAS  Google Scholar 

  • Leflaive J, Ten-Hage L (2009) Chemical interactions in diatoms: role of polyunsaturated aldehydes and precursors. New Phytol 184(4):794–805

    CAS  Google Scholar 

  • Leifke E, Gorenoi V, Wichers C et al (2000) Age-related changes of serum sex hormones, insulin-like growth factor-1 and sex-hormone binding globulin levels in men: cross-sectional data from a healthy male cohort. Clin Endocrinol 53(6):689–695

    CAS  Google Scholar 

  • Li D, Gu Z, Zhang J et al (2019) Protective effect of inducible aldo-keto reductases on 4-hydroxynonenal- induced hepatotoxicity. Chem Biol Interact 304:124–130

    CAS  Google Scholar 

  • Liao S, Zhang J, Shi S et al (2020) Association of aldehyde exposure with cardiovascular disease. Ecotoxicol Environ Saf 206:111385

    CAS  Google Scholar 

  • Mayes JS, Watson GH (2004) Direct effects of sex steroid hormones on adipose tissues and obesity. Obes Rev: Official J Int Assoc Study Obes 5(4):197–216

    CAS  Google Scholar 

  • Mezzullo M, Gambineri A, Di Dalmazi G et al (2021) Steroid reference intervals in women: influence of menopause, age and metabolism. Eur J Endocrinol 184(3):395–407

    Google Scholar 

  • Moghe A, Ghare S, Lamoreau B et al (2015) Molecular mechanisms of acrolein toxicity: relevance to human disease. Toxicol Sci: Official J Soc Toxicol 143(2):242–255

    CAS  Google Scholar 

  • Montoya-Estrada A,Velázquez-Yescas KG,Veruete-Bedolla DB et al (2020) Parameters of oxidative stress in reproductive and postmenopausal Mexican women. Int J Environ Res Public Health 17(5):1492

  • Moraga-Amaro R,van Waarde A,Doorduin J, et al (2018) Sex steroid hormones and brain function: PET imaging as a tool for research. J Neuroendocrinol 30(2)

  • Mouro VGS, Martins ALP, Silva J et al (2019) Subacute Testicular toxicity to cadmium exposure intraperitoneally and orally. Oxid Med Cell Longev 2019:3429635

    Google Scholar 

  • Murawski A, Fiedler N, Schmied-Tobies MIH et al (2020) Metabolites of the fragrance 2-(4-tert-butylbenzyl)propionaldehyde (lysmeral) in urine of children and adolescents in Germany - Human biomonitoring results of the German Environmental Survey 2014–2017 (GerES V). Int J Hyg Environ Health 229:113594

    CAS  Google Scholar 

  • O’Brien PJ, Siraki AG, Shangari N (2005) Aldehyde sources, metabolism, molecular toxicity mechanisms, and possible effects on human health. Crit Rev Toxicol 35(7):609–662

    CAS  Google Scholar 

  • Phipps AI, Ichikawa L, Bowles EJ et al (2010) Defining menopausal status in epidemiologic studies: a comparison of multiple approaches and their effects on breast cancer rates. Maturitas 67(1):60–66

    Google Scholar 

  • Salem JE, Alexandre J, Bachelot A et al (2016) Influence of steroid hormones on ventricular repolarization. Pharmacol Ther 167:38–47

    CAS  Google Scholar 

  • Salerni S, Di Francescomarino S, Cadeddu C et al (2015) The different role of sex hormones on female cardiovascular physiology and function: not only oestrogens. Eur J Clin Invest 45(6):634–645

    CAS  Google Scholar 

  • Simó R, Sáez-López C, Barbosa-Desongles A et al (2015) Novel insights in SHBG regulation and clinical implications. Trends Endocrinol Metab 26(7):376–383

    Google Scholar 

  • Sohal RS, Orr WC (2012) The redox stress hypothesis of aging. Free Radical Biol Med 52(3):539–555

    CAS  Google Scholar 

  • Soyman Z, Uzun H, Bayindir N et al (2018) Can ebselen prevent cisplatin-induced ovarian damage? Arch Gynecol Obstet 297(6):1549–1555

    CAS  Google Scholar 

  • Spickett CM (2013) The lipid peroxidation product 4-hydroxy-2-nonenal: Advances in chemistry and analysis. Redox Biol 1(1):145–152

    CAS  Google Scholar 

  • Taneja V (2018) Sex hormones determine immune response. Front Immunol 9:1931

    Google Scholar 

  • Tian M, Wang YX, Wang X et al (2021) Environmental doses of arsenic exposure are associated with increased reproductive-age male urinary hormone excretion and in vitro Leydig cell steroidogenesis. J Hazard Mater 408:124904

    CAS  Google Scholar 

  • Unfer TC, Figueiredo CG, Zanchi MM et al (2015) Estrogen plus progestin increase superoxide dismutase and total antioxidant capacity in postmenopausal women. Clim: J Int Menopause Soc 18(3):379–388

    CAS  Google Scholar 

  • Wang HX, Zhou DX, Zheng LR et al (2012) Effects of paternal occupation exposure to formaldehyde on reproductive outcomes. J Occup Environ Med 54(5):518–524

    CAS  Google Scholar 

  • Wang Y, Aimuzi R, Nian M et al (2021) Perfluoroalkyl substances and sex hormones in postmenopausal women: NHANES 2013–2016. Environ Int 149:106408

    CAS  Google Scholar 

  • Warembourg C, Debost-Legrand A, Bonvallot N et al (2016) Exposure of pregnant women to persistent organic pollutants and cord sex hormone levels. Human Reprod (oxford, England) 31(1):190–198

    CAS  Google Scholar 

  • Xu L, Yuan Y, Che Z et al (2022) The hepatoprotective and hepatotoxic roles of sex and sex-related hormones. Front Immunol 13:939631

    CAS  Google Scholar 

  • Yuan S,Wang L,Sun J, et al (2022) Genetically predicted sex hormone levels and health outcomes: phenome-wide Mendelian randomization investigation. Int J Epidemiol

  • Zhang H, Morgan TE, Forman HJ (2021) Age-related alteration in HNE elimination enzymes. Arch Biochem Biophys 699:108749

    CAS  Google Scholar 

  • Zhou H, Wang Y, Gatcombe M et al (2017) Simultaneous measurement of total estradiol and testosterone in human serum by isotope dilution liquid chromatography tandem mass spectrometry. Anal Bioanal Chem 409(25):5943–5954

    CAS  Google Scholar 

  • Zhu R, Liu H, Liu C et al (2017) Cinnamaldehyde in diabetes: a review of pharmacology, pharmacokinetics and safety. Pharmacol Res 122:78–89

    CAS  Google Scholar 

  • Zirkin BR, Papadopoulos V (2018) Leydig cells: formation, function, and regulation. Biol Reprod 99(1):101–111

    Google Scholar 

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Acknowledgements

We thank the research staff of the National Center for Health Statistics of the Centers for Disease Control (CDC) and Prevention for their time and effort and the participants who enrolled in the NHANES project; we also appreciate CDC for publicizing the HNANES database.

Funding

The study was supported by the grants from Central Scientific Research Projects for Public Welfare Research Institutes (ZX2022QT020) and the Doctoral Program of Entrepreneurship and Innovation in Jiangsu Province (JSSCBS20211323).

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Authors and Affiliations

  1. Laboratory of Pesticide Environmental Assessment and Pollution Control, Nanjing Institute of Environmental Sciences, Ministry of Ecology and Environment (MEE), Nanjing, 210042, People’s Republic of China

    Weilong Xing, Wen Gu, Mengyuan Liang, Zhen Wang, Deling Fan, Bing Zhang & Lei Wang

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  1. Weilong Xing
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Contributions

Study conception and design, Weilong Xing, Lei Wang; data collection, Weilong Xing, Lei Wang, Wen Gu; data analysis and interpretation, Weilong Xing, Lei Wang, Wen Gu, Mengyuan Liang, Zhen Wang, Deling Fan, Bing Zhang; manuscript writing and reviewing, Weilong Xing; study supervision, Weilong Xing. All authors read and approved the final manuscript.

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Correspondence to Weilong Xing.

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The program was approved by the National Center for Health Statistics Ethics Review Board. All of the participants provided written informed consent.

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Responsible Editor: Lotfi Aleya

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Supplementary Information

ESM 1

Association between aldehydes and sex steroid hormones, stratified by gender. (PNG 91 kb)

High resolution image (TIF 2966 kb)

ESM 2

Association between aldehydes and sex steroid hormones in pre-menopause and post-menopause. (PNG 117 kb)

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ESM 3

Association between aldehydes and sex steroid hormones in males, stratified by age. (PNG 381 kb)

High resolution image (TIF 8928 kb)

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Xing, W., Gu, W., Liang, M. et al. Association between aldehyde exposure and sex steroid hormones among adults. Environ Sci Pollut Res 30, 30444–30461 (2023). https://doi.org/10.1007/s11356-022-24362-1

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