Puzzling relationship between levels of toxic metals in blood and serum levels of reproductive hormones: Benchmark dose approach in cross-sectional study

References

• Adelakun SA, Ukwenya VO, Akingbade GT, Omotoso OD, Aniah JA. 2020. Interventions of aqueous extract of Solanum melongena fruits (garden eggs) on mercury chloride induced testicular toxicity in adult male Wistar rats. Biomed J. 43:174–182. doi:10.1016/j.bj.2019.07.004.
   PubMed Web of Science ®Google Scholar
• Agarwal A, Mulgund A, Hamada A, Chyatte MR. 2015. A unique view on male infertility around the globe. Reprod Biol Endocrinol. 13:1–9. doi:10.1186/s12958-015-0032-1.
   PubMed Web of Science ®Google Scholar
• Anđelković M, Djordjevic AB, Miljaković EA, Javorac D, Čolaković N, Oprić S, Petričević S, Granić M, Kotur-Stevuljević J, Antonijević B, Bulat Z. 2021. Cadmium tissue level in women diagnosed with breast cancer – a case control study. Environ Res. 199. doi:10.1016/j.envres.2021.111300.
   PubMed Web of Science ®Google Scholar
• Anlar HG, Bacanli M, Başaran N. 2021. Endocrine disrupting mechanisms and effects of pesticides. Arch Farm. 71(6):480–490. doi:10.5937/arhfarm71-34291.
   Google Scholar
• Aruldhas MM, Subramanian S, Sekar P, Vengatesh G, Chandrahasan G, Govindarajulu P, Akbarsha MA. 2005. Chronic chromium exposure-induced changes in testicular histoarchitecture are associated with oxidative stress: study in a non-human primate (Macaca radiata Geoffroy). Hum Reprod. 20:2801–2813. doi:10.1093/humrep/dei148.
   PubMed Web of Science ®Google Scholar
• Bala R, Singh V, Rajender S, Singh K. 2021. Environment, lifestyle, and female infertility. Reprod Sci. 28:617–638. doi:10.1007/s43032-020-00279-3.
   PubMed Web of Science ®Google Scholar
• Baralić K, Javorac D, Marić Đ, Đukić-Ćosić D, Bulat Z, Antonijević Miljaković E, Anđelković M, Antonijević B, Aschner M, Buha Djordjevic A. 2022. Benchmark dose approach in investigating the relationship between blood metal levels and reproductive hormones: data set from human study. Environ Int. 165:107313. doi:10.1016/j.envint.2022.107313.
   PubMed Web of Science ®Google Scholar
• Boulila I, Ounassa A. 2020. Protective effects of selenium and zinc on nickel chloride induced reproductive toxicity in wistar albinos preimplanted rats. Stud Univ Vasile Goldis Arad Ser Stiint Vietii. 30:126–135.
   Google Scholar
• Buha-Đorđević A, Anđelković M, Kačavenda E, Javorac D, Antonijević-Miljaković E, Marić Đ, Baralić K, Đukić-Ćosić D, Ćurčić M, Antonijević B, Bulat Z. 2021. Cadmium levels in human breast tissue and estradiol serum levels: is there a connection? Arh Farm. 71:581–595. doi:10.5937/arhfarm71-34280.
   Google Scholar
• Castellanos CG, Sørvik IB, Tanum MB, Verhaegen S, Brandt I, Ropstad E. 2013. Differential effects of the persistent DDT metabolite methylsulfonyl-DDE in nonstimulated and LH-stimulated neonatal porcine Leydig cells. Toxicol Appl Pharmacol. 267:247–255. doi:10.1016/j.taap.2012.12.022.
   PubMed Web of Science ®Google Scholar
• Chen YW, Yang CY, Huang CF, Hung DZ, Leung YM, Liu S. 2009. Heavy metals, islet function and diabetes development. Islets. 1:169–176. doi:10.4161/isl.1.3.9262.
   PubMed Web of Science ®Google Scholar
• Chowdhury A. 2009. Recent advances in heavy metals induced effect on male reproductive function – a retrospective. Al Ameen J Med Sci. 2:37–42.
   Google Scholar
• Choy CMY, Lam CWK, Cheung LTF, Briton-Jones CM, Cheung LP, Haines CJ. 2002. Infertility, blood mercury concentrations and dietary seafood consumption: a case-control study. BJOG Int J Obstet Gynaecol. 109:1121–1125. doi:10.1016/S1470-0328(02)02984-1.
   PubMed Web of Science ®Google Scholar
• Chung MK, Buck Louis GM, Kannan K, Patel CJ. 2019. Exposome-wide association study of semen quality: systematic discovery of endocrine disrupting chemical biomarkers in fertility require large sample sizes. Environ Int. 125:505–514. doi:10.1016/j.envint.2018.11.037.
   PubMed Web of Science ®Google Scholar
• Davis BJ, Price HC, O’Connor RW, Fernando R, Rowland AS, Morgan DL. 2001. Mercury vapor and female reproductive toxicity. Toxicol Sci. 59:291–296. doi:10.1093/toxsci/59.2.291.
   PubMed Web of Science ®Google Scholar
• Diamanti-Kandarakis E, Palioura E, Kandarakis SA, Koutsilieris M. 2010. The impact of endocrine disruptors on endocrine targets. Horm Metab Res. 42:543–552. doi:10.1055/s-0030-1252034.
   PubMed Web of Science ®Google Scholar
• El-Demerdash FM, Jebur AB, Nasr HM, Hamid HM. 2019. Modulatory effect of Turnera diffusa against testicular toxicity induced by fenitrothion and/or hexavalent chromium in rats. Environ Toxicol. 34:330–339. doi:10.1002/tox.22688.
   PubMed Web of Science ®Google Scholar
• Feng Y, Zhang P, Zhang Z, Shi J, Jiao Z, Shao B. 2016. Endocrine disrupting effects of triclosan on the placenta in pregnant rats. PLoS One. 11:1–14. doi:10.1371/journal.pone.0154758.
   Web of Science ®Google Scholar
• Gan X, Zhang X, Qiannan E, Zhang Q, Ye Y, Cai Y, Han A, Tian M, Wang C, Su Z, et al. 2019. Nano-selenium attenuates nickel-induced testosterone synthesis disturbance through inhibition of MAPK pathways in Sprague-Dawley rats. Environ Toxicol. 34:968–978. doi:10.1002/tox.22768.
   PubMed Web of Science ®Google Scholar
• González-Villalva A, Colín-Barenque L, Bizarro-Nevares P, Rojas-Lemus M, Rodríguez-Lara V, García-Pelaez I, Ustarroz-Cano M, López-Valdez N, Albarrán-Alonso JC, Fortoul TI. 2016. Pollution by metals: is there a relationship in glycemic control? Environ Toxicol Pharmacol. 46:337–343. doi:10.1016/j.etap.2016.06.023.
   PubMed Web of Science ®Google Scholar
• Goumenou M, Djordjevic AB, Vassilopoulou L, Tsatsakis AM. 2021. Endocrine disruption and human health risk assessment in the light of real-life risk simulation. In: Toxicological risk assessment and multi-system health impacts from exposure. Elsevier; p. 147–162. doi:10.1016/B978-0-323-85215-9.00041-6.
   Google Scholar
• Guvvala PR, Sellappan S, Parameswaraiah RJ. 2016. Impact of arsenic(V) on testicular oxidative stress and sperm functional attributes in Swiss albino mice. Environ Sci Pollut Res. 23:18200–18210. doi:10.1007/s11356-016-6870-3.
   PubMed Web of Science ®Google Scholar
• Hardy A, Benford D, Halldorsson T, Jeger MJ, Knutsen KH, More S, Mortensen A, Naegeli H, Noteborn H, Ockleford C, et al. 2017. Update: use of the Benchmark dose approach in risk assessment. EFSA J. 15:1–41. doi:10.2903/j.efsa.2017.4658.
   Web of Science ®Google Scholar
• Hayes AW, Li R, Hoeng J, Iskandar A, Peistch MC, Dourson ML. 2019. New approaches to risk assessment of chemical mixtures. Toxicol Res Applic. 3. doi:10.1177/2397847318820768.
   Google Scholar
• He K, Xun P, Liu K, Morris S, Reis J, Guallar E. 2013. Mercury exposure in young adulthood and incidence of diabetes later in life: the CARDIA trace element study. Diabetes Care. 36:1584–1589. doi:10.2337/dc12-1842.
   PubMed Web of Science ®Google Scholar
• Henriques MC, Loureiro S, Fardilha M, Herdeiro MT. 2019. Exposure to mercury and human reproductive health: a systematic review. Reprod Toxicol. 85:93–103. doi:10.1016/j.reprotox.2019.02.012.
   PubMed Web of Science ®Google Scholar
• Hernandez AF, Buha A, Constantin C, Wallace DR, Sarigiannis D, Neagu M, Antonijevic B, Hayes AW, Wilks MF, Tsatsakis A. 2019. Critical assessment and integration of separate lines of evidence for risk assessment of chemical mixtures. Arch Toxicol. 93:2741–2757. doi:10.1007/s00204-019-02547-x.
   PubMed Web of Science ®Google Scholar
• Jana K, Jana S, Samanta PK. 2006. Effects of chronic exposure to sodium arsenite on hypothalamo-pituitary-testicular activities in adult rats: possible an estrogenic mode of action. Reprod Biol Endocrinol. 4:1–13. doi:10.1186/1477-7827-4-9.
   PubMed Web of Science ®Google Scholar
• Jia X, Zhang L, Zhao J, Ren M, Zewu L, Wang J, Wang S, Liu Y, An H, Li Y, et al. 2021. Associations between endocrine-disrupting heavy metals in maternal hair and gestational diabetes mellitus: a nested case-control study in China. Environ Int. 157:106770. doi:10.1016/j.envint.2021.106770.
   PubMed Web of Science ®Google Scholar
• Kalender S, Uzun FG, Demir F, Uzunhisarcikli M, Aslanturk A. 2013. Mercuric chloride-induced testicular toxicity in rats and the protective role of sodium selenite and vitamin E. Food Chem Toxicol. 55:456–462. doi:10.1016/j.fct.2013.01.024.
   PubMed Web of Science ®Google Scholar
• Kong L, Tang M, Zhang T, Wang D, Hu K, Lu W, Wei C, Liang G, Pu Y. 2014. Nickel nanoparticles exposure and reproductive toxicity in healthy adult rats. Int J Mol Sci. 15:21253–21269. doi:10.3390/ijms151121253.
   PubMed Web of Science ®Google Scholar
• Kresovich JK, Argos M, Turyk ME. 2015. Associations of lead and cadmium with sex hormones in adult males. Environ Res. 142:25–33. doi:10.1016/j.envres.2015.05.026.
   PubMed Web of Science ®Google Scholar
• Lin T, Xiao-Ting L, Ai G, Qiu-Ying L, Tai-Yi J. 2008. Application of Benchmark dose for occupational epidemiology in lead exposure. Toxicol Mech Methods. 18:363–367. doi:10.1080/15376510701623888.
   PubMed Web of Science ®Google Scholar
• Ma Y, He X, Qi K, Wang T, Qi Y, Cui L, Wang F, Song M. 2019. Effects of environmental contaminants on fertility and reproductive health. J Environ Sci (China). 77:210–217. doi:10.1016/j.jes.2018.07.015.
   PubMedGoogle Scholar
• Mouro VGS, Siman VA, da Silva J, Dias FCR, Damasceno EM, Cupertino MDC, de Melo FCSA, da Matta SLP. 2020. Cadmium-induced testicular toxicity in mice: subacute and subchronic route-dependent effects. Biol Trace Elem Res. 193:466–482. doi:10.1007/s12011-019-01731-5.
   PubMed Web of Science ®Google Scholar
• Nagata C, Nagao Y, Shibuya C, Kashiki Y, Shimizu H. 2005. Urinary cadmium and serum levels of estrogens and androgens in postmenopausal Japanese women. Cancer Epidemiol Biomark Prev. 14:705–708. doi:10.1158/1055-9965.EPI-04-0619.
   PubMed Web of Science ®Google Scholar
• Nagels HE, Rishworth JR, Siristatidis CS, Kroon B. 2015. Androgens (dehydroepiandrosterone or testosterone) for women undergoing assisted reproduction. Cochrane Database Syst Rev. doi:10.1002/14651858.CD009749.pub2.
   PubMed Web of Science ®Google Scholar
• Nelms MD, Simmons JE, Edwards SW. 2018. Adverse outcome pathways to support the assessment of chemical mixtures. In: Chemical mixtures and combined chemical and nonchemical stressors: exposure, toxicity, analysis, and risk. Cham: Springer; p. 177–201. doi:10.1007/978-3-319-56234-6_7.
   Google Scholar
• Oettel M, Mukhopadhyay AK. 2004. Progesterone: the forgotten hormone in men? Aging Male. 7:236–257. doi:10.1080/13685530400004199.
   PubMedGoogle Scholar
• Pan W, Ye X, Zhu Z, Li C, Zhou J, Liu J. 2020. A case-control study of arsenic exposure with the risk of primary ovarian insufficiency in women. Environ Sci Pollut Res. 27:25220–25229. doi:10.1007/s11356-020-08806-0.
   PubMed Web of Science ®Google Scholar
• Pizent A, Tariba B, Živković T. 2012. Reproductive toxicity of metals in men. Arh Hig Rada Toksikol. 63:35–46. doi:10.2478/10004-1254-63-2012-2151.
   PubMed Web of Science ®Google Scholar
• Rana SVS. 2014. Perspectives in endocrine toxicity of heavy metals – a review. Biol Trace Elem Res. 160:1–14. doi:10.1007/s12011-014-0023-7.
   PubMed Web of Science ®Google Scholar
• Russell N, Grossmann M. 2019. Estradiol as a male hormone. Eur J Endocrinol. 181:R23–R43. doi:10.1530/EJE-18-1000.
   PubMed Web of Science ®Google Scholar
• Sengupta P, Banerjee R, Nath S, Das S, Banerjee S. 2015. Metals and female reproductive toxicity. Hum Exp Toxicol. 34:679–697. doi:10.1177/0960327114559611.
   PubMed Web of Science ®Google Scholar
• Silva N, Peiris-John R, Wickremasinghe R, Senanayake H, Sathiakumar N. 2012. Cadmium a metalloestrogen: are we convinced? J Appl Toxicol. 32:318–332. doi:10.1002/jat.1771.
   PubMed Web of Science ®Google Scholar
• Sparks DL. 2005. Toxic metals in the environment: the role of surfaces. Elements. 1(4):193–197.
   Web of Science ®Google Scholar
• Tariba Lovaković B. 2020. Cadmium, arsenic, and lead: elements affecting male reproductive health. Curr Opin Toxicol. 19:7–14. doi:10.1016/j.cotox.2019.09.005.
   Web of Science ®Google Scholar
• Tomei G, Ciarrocca M, Fiore P, Rosati MV, Pimpinella B, Anzani MF, Giubilati R, Cangemi C, Tomao E, Tomei F. 2008. Exposure to urban stressor and effects on free testosterone in female workers. Sci Total Environ. 392:198–202. doi:10.1016/j.scitotenv.2007.12.007.
   PubMed Web of Science ®Google Scholar
• Tyagi V, Scordo M, Yoon RS, Liporace FA, Greene LW. 2017. Revisiting the role of testosterone: are we missing something? Rev Urol. 19:16–24. doi:10.3909/riu0716.
   PubMedGoogle Scholar
• Vieira Silva A, Chu I, Feeley M, Bergman Å, Håkansson H, Öberg M. 2022. Dose-dependent toxicological effects in rats following a 90-day dietary exposure to PCB-156 include retinoid disruption. Reprod Toxicol. 107:123–139. doi:10.1016/j.reprotox.2021.09.012.
   PubMed Web of Science ®Google Scholar
• Wang YX, Sun Y, Feng W, Wang P, Yang P, Li J, Huang Z, Chen YJ, Liu C, Sun L, et al. 2016. Association of urinary metal levels with human semen quality: a cross-sectional study in China. Environ Int. 91:51–59. doi:10.1016/j.envint.2016.02.019.
   PubMed Web of Science ®Google Scholar
• WHO (World Health Organisation), UNEP (United Nations Environment Programme). 2013. State-of-the-science of endocrine disrupting chemicals, 2012. Geneva: United Nations Environment Programme and the World Health Organization.
   Google Scholar
• Xiong YW, Zhu HL, Nan Y, Cao XL, Shi XT, Yi SJ, Feng YJ, Zhang C, Gao L, Chen YH, et al. 2020. Maternal cadmium exposure during late pregnancy causes fetal growth restriction via inhibiting placental progesterone synthesis. Ecotoxicol Environ Saf. 187:109879. doi:10.1016/j.ecoenv.2019.109879.
   PubMed Web of Science ®Google Scholar
• Yao Q, Zhou G, Xu M, Dai J, Qian Z, Cai Z, Zhang L, Tan Y, Hu R. 2019. Blood metal levels and serum testosterone concentrations in male and female children and adolescents: NHANES 2011–2012. PLoS One. 14:1–14. doi:10.1371/journal.pone.0224892.
   Google Scholar
• Yilmaz B, Terekeci H, Sandal S, Kelestimur F. 2020. Endocrine disrupting chemicals: exposure, effects on human health, mechanism of action, models for testing and strategies for prevention. Rev Endocr Metab Disord. 21:127–147. doi:10.1007/s11154-019-09521-z.
   PubMed Web of Science ®Google Scholar
• Zheng W, Ge F, Wu K, Chen X, Li X, Chen Y, Lv Y, Lian Q, Ge RS. 2018. In utero exposure to hexavalent chromium disrupts rat fetal testis development. Toxicol Lett. 299:201–209. doi:10.1016/j.toxlet.2018.10.010s.
   PubMed Web of Science ®Google Scholar