Does Fluoride Affect Serum Testosterone and Androgen Binding Protein with Age-Specificity? A Population-Based Cross-Sectional Study in Chinese Male Farmers

Abstract

Many studies have demonstrated that exposure to excess fluoride was associated with a variety of diseases. Little is known about the variation of testosterone (T) levels caused by fluoride exposure. The aim of this study is to explore the association of fluoride exposure and age with serum T and androgen-binding protein (ABP) levels in male farmers. A cross-sectional study was conducted in a county of Henan Province, China, including high fluoride exposure from drinking water villages and control villages. Male farmers aged 18–55 years old who lived in these villages were recruited by cluster sampling and divided into a higher fluoride exposure group (HFG) and a lower fluoride exposure group (LFG) according to the level of urinary fluoride. Levels of T and ABP in serum were measured using chemiluminescence immunoassay (CLIA) and enzyme-linked immunosorbent assay (ELISA) respectively. Markedly lower T levels were observed in male farmers from the HFG than in those from the LFG (t = 2.496, P < 0.05). Furthermore, younger farmers, 18–29 and 30–39 years old, may be the most likely to have lower T levels when exposed to fluoride (P < 0.05). No significant differences were observed in serum ABP levels in all male farmers between the two groups with different fluoride exposure. These results supported that excess fluoride exposure decreased serum T levels of male farmers with age-specificity.

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References

  1. 1.

    Choi AL, Guifan S, Ying Z, Philippe G (2012) Developmental fluoride neurotoxicity: a systematic review and meta-analysis. Environ Health Perspect 120(6):1362–1368

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  2. 2.

    Vitoria I, Maraver F, Almerichsilla JM (2014) Fluoride content in tap water in Spain and prevention of dental caries. Gac Sanit 28(3):255–256

    Article  PubMed  Google Scholar 

  3. 3.

    Moimaz SAS, Saliba O, Marques LB, Garbin CAS, Saliba NA (2015;) Dental fluorosis and its influence on children’s life. Brazilian oral research 29 (1):1–7

  4. 4.

    Jin H, Ji Z, Yuan J, Li J, Liu M, Xu C, Dong J, Hou P, Hou S (2015) Research on removal of fluoride in aqueous solution by alumina-modified expanded graphite composite. J Alloys Compd 620:361–367

    CAS  Article  Google Scholar 

  5. 5.

    Jiang Y, Guo X, Sun Q, Shan Z, Teng W (2015) Effects of excess fluoride and iodide on thyroid function and morphology. Biol Trace Elem Res 170(2):382–389

  6. 6.

    Sprando R, Collins T, Black T, Olejnik N, Rorie J (1998) Testing the potential of sodium fluoride to affect spermatogenesis: a morphometric study. Food Chem Toxicol 36(12):1117–1124

    CAS  Article  PubMed  Google Scholar 

  7. 7.

    Gupta R, Khan T, Agrawal D, Kachhawa J (2007) The toxic effects of sodium fluoride on the reproductive system of male rats. Toxicol Ind Health 23(9):507–513

    CAS  Article  PubMed  Google Scholar 

  8. 8.

    Sun Z, Niu R, Wang B, Jiao Z, Wang J, Zhang J, Wang S, Wang J (2011) Fluoride-induced apoptosis and gene expression profiling in mice sperm in vivo. Arch Toxicol 85(11):1441–1452

    CAS  Article  PubMed  Google Scholar 

  9. 9.

    Sengupta P (2013) Environmental and occupational exposure of metals and their role in male reproductive functions. Drug Chem Toxicol 36(3):353–368

    CAS  Article  PubMed  Google Scholar 

  10. 10.

    Yang Y, Huang H, Ba Y, Cheng XM, Cui LX (2015) Effect of oxidative stress on fluoride-induced apoptosis in primary cultured Sertoli cells of rats. Int J Environ Health Res 25(1):1–9

    Article  PubMed  Google Scholar 

  11. 11.

    Niu R, Wang J, Sun Z, Xue X, Yan X, Wang J, Zhang J, Wang J (2015) Transcriptional regulatory dynamics of the hypothalamic-pituitary-testicular axis in male mice exposed to fluoride. Environ Toxicol Pharmacol 40(2):557–562

    CAS  Article  PubMed  Google Scholar 

  12. 12.

    Hao P, Ma X, Cheng X, Ba Y, Zhu J, Cui L (2010) Effect of fluoride on human hypothalamus-hypophysis-testis axis hormones. Journal of hygiene research 39(1):53–55

    CAS  PubMed  Google Scholar 

  13. 13.

    Susheela AK, Jethanandani P (1996) Circulating testosterone levels in skeletal fluorosis patients. Journal of Toxicology: Clinical Toxicology 34(34):183–189

    CAS  PubMed  Google Scholar 

  14. 14.

    Han H, Sun Z, Luo G, Wang C, Wei R, Wang J (2015) Fluoride exposure changed the structure and the expressions of reproductive related genes in the hypothalamus–pituitary–testicular axis of male mice. Chemosphere 135:297–303

    CAS  Article  PubMed  Google Scholar 

  15. 15.

    Zhu JY, Ba Y, Li EW, Cheng XM, Liu S, Gao LH, Cui LX (2007) Effects of high fluoride in drinking water on serum hormonal level. Journal of Zhengzhou university (Medical Sciences) 42(1):58–60

    CAS  Google Scholar 

  16. 16.

    Ma Y, Yang HZ, Xu LM, Huang YR, Dai HL, Kang XN (2015) Testosterone regulates the autophagic clearance of androgen binding protein in rat Sertoli cells. Sci Rep 5:1–8

  17. 17.

    Vermeulen A (2000) Andropause. Maturitas 34(1):5–15

    CAS  Article  PubMed  Google Scholar 

  18. 18.

    Prasad AS, Mantzoros CS, Beck FWJ, Hess JW, Brewer GJ (1996) Zinc status and serum testosterone levels of healthy adults. Nutrition 12(5):344–348

    CAS  Article  PubMed  Google Scholar 

  19. 19.

    Zhao WM, Wang JT, Ding L, Hao JX, Gao ES, Yuan W (2011) Effect of bisphenol-a Exporsure on sex hormone level of men. Journal of Environment & Health 28(1):36–40

    CAS  Google Scholar 

  20. 20.

    Zhou T, Duan L, Ding Z, Yang R, Li S, Xi Y, Cheng XM, Hou JX, Wen SB, Chen J (2012) Environmental fluoride exposure and reproductive hormones in male living in endemic fluorosis villages in China. Life Science Journal 9(4):1–7

  21. 21.

    Sun DJ, Gu L, W W (2012) Exploration of urinary fluoride results of 798 normal adult in Dalian area. China Medical Herald 9:113–114

  22. 22.

    Cui RR, Ding Z, Cui LX, Yang RP, Xi Y, Cheng XM, Ren LJ, Duan LJ, Hou JX, Ba Y (2013) Influences of fluoride exposure in drinking water on serum androgen binding protein and testosterone of adult males. Journal of Zhengzhou university (Medical Sciences) 48(6):750–753

    CAS  Google Scholar 

  23. 23.

    Liang S, Zhao MH, Ock S A, Kim NH, Cui XS (2015) Fluoride impairs oocyte maturation and subsequent embryonic development in mice. Environ Toxicol. doi:10.1002/tox.22153

  24. 24.

    Wang J, Zhang H, Xu F, Xu F, Zhang K, Zhang Y (2014) The antagonism of aluminum against fluoride-induced oxidative stress and c-Fos overexpression in rat testes. Toxicol Mech Methods 24(2):136–141

    Article  PubMed  Google Scholar 

  25. 25.

    Argoud T, Boutroy S, Claustrat B, Chapurlat R, Szulc P (2014) Association between sex steroid levels and bone microarchitecture in men: the STRAMBO study. The Journal of Clinical Endocrinology & Metabolism 99(4):1400–1410

    CAS  Article  Google Scholar 

  26. 26.

    Tesarik J, Greco E, Rienzi L, Ubaldi F, Guido M, Cohen-Bacrie P, Mendoza C (1998) Differentiation of spermatogenic cells during in-vitro culture of testicular biopsy samples from patients with obstructive azoospermia: effect of recombinant follicle stimulating hormone. Hum Reprod 13(10):2772–2781

    CAS  Article  PubMed  Google Scholar 

  27. 27.

    Sofikitis N, Pappas E, Kawatani A, Baltogiannis D, Loutradis D, Kanakas N, Giannakis D, Dimitriadis F, Tsoukanelis K, Georgiou I (2005) Efforts to create an artificial testis: culture systems of male germ cells under biochemical conditions resembling the seminiferous tubular biochemical environment. Hum Reprod Update 11(3):229–259

    CAS  Article  PubMed  Google Scholar 

  28. 28.

    Zhou T, Yang R, Li S, Zheng G, Xi Y, Cheng X, Hou J, Cui L, Ba Y (2013) Influence of water fluoride exposure on sex hormone binding globulin and testosterone in adult male. Journal of hygiene research 42(2):241–244

    CAS  PubMed  Google Scholar 

  29. 29.

    Zhang, Liang, Ma, Niu, Wang, Zhang J, Liang C, Ma J, Niu R, Wang J (2006) Effects of sodium fluoride and sulfur dioxide on sperm motility and serum testosterone in male rats. Fluoride 39 (2):126–131

  30. 30.

    Chen P, Meng X, He J (1997) Effects of Hyperfluoride on reproduction-endocrine of male adults. Endemic Diseases Bulletin 12(2):57–58

  31. 31.

    Kelsey TW, Li LQ, Mitchell RT, Ashley W, Anderson RA, Wallace WHB (2014) A validated age-related normative model for male total testosterone shows increasing variance but no decline after age 40 years. PLoS One 9(10):e109346–e109346

    Article  PubMed  PubMed Central  Google Scholar 

  32. 32.

    Gideon S, Sasa S, Amanda I, Leo T, Elise F, Anna Z, Allan CA, Ly LP, Conway AJ, Mclachlan RI (2012) Serum testosterone, dihydrotestosterone and estradiol concentrations in older men self-reporting very good health: the healthy man study. Clin Endocrinol 77(5):755–763

    Article  Google Scholar 

  33. 33.

    Schiavi RC, Stimmel BB, Mandeli J, White D (1995) Chronic alcoholism and male sexual function. Am J Psychiatr 152(7):1045–1051

    CAS  Article  PubMed  Google Scholar 

  34. 34.

    Orpana AK, Harkonen M, Eriksson CJ (1990) Ethanol-induced inhibition of testosterone biosynthesis in rat Leydig cells: role of mitochondrial substrate shuttles and citrate. Alcohol Alcohol 25(5):499–507

    CAS  PubMed  Google Scholar 

  35. 35.

    Gerard K, Franck O (2014) Regulation of male fertility by the bone-derived hormone osteocalcin. Molecular & Cellular Endocrinology 382(1):521–526

    Article  Google Scholar 

  36. 36.

    Oury F, Sumara G, Sumara O, Ferron M, Chang H, Smith C, Hermo L, Suarez S, Roth B, Ducy P (2011) Endocrine regulation of male fertility by the skeleton. Cell 144(5):796–809

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  37. 37.

    Joseph DR (1994) Structure, function, and regulation of androgen-binding protein/sex hormone-binding globulin. Vitamins & Hormones 49(1):197–280

    CAS  Article  Google Scholar 

  38. 38.

    Caneguim BH, Beltrame FL, Da LJ, Valentini SR, Cerri PS, Sasso-Cerri E (2012) Primordial germ cells (Spermatogonial stem cells) of bullfrogs express sex hormone-binding globulin and steroid receptors during seasonal spermatogenesis. Cells Tissues Organs 197(2):136–144

    Article  PubMed  Google Scholar 

  39. 39.

    Pogach L, Giglio W, Nathan E, Huang HF (1993) Maintenance of spermiogenesis by exogenous testosterone in rats treated with a GnRH antagonist: relationship with androgen-binding protein status. J Reprod Fertil 98(2):415–422

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgments

We express our sincere thanks to all individuals who volunteered to participate in this study and the numerous doctors and nurses of the Tongxu Center for Disease Prevention and Control. The study was supported by the grant 81072247 from the National Natural Science Foundation of China and grant 13 A330653 from the Education Department of Henan Province, China.

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Correspondence to Yue Ba.

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All procedures were performed in accordance to protocols approved by the Human Investigation Committees at Zhengzhou University.

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The authors declare that they have no conflict of interest.

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Duan, L., Zhu, J., Wang, K. et al. Does Fluoride Affect Serum Testosterone and Androgen Binding Protein with Age-Specificity? A Population-Based Cross-Sectional Study in Chinese Male Farmers. Biol Trace Elem Res 174, 294–299 (2016). https://doi.org/10.1007/s12011-016-0726-z

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Keywords

  • Fluorine
  • Male
  • Androgen binding protein
  • Testosterone
  • Age