Endocrine-disrupting chemicals and male reproductive health: a review

  • Damjan Balabanič Faculty of Industrial Engineering Novo mesto, Novo mesto, Slovenia
  • Aleksandra Krivograd Klemenčič Institute for Sanitary Engineering, Faculty of Civil and Geodetic Engineering, University of ljubljana, ljubljana, Slovenia
Keywords: endocrine-disrupting chemicals, endogenous hormones, environment, human male reproductive health

Abstract

Balanced functioning of the endocrine system is essential for preservation of human species by providing normal growth and development, reproduction, and normal functioning of all other organ systems. In the last decades, emerging area of interest is the impact of environmental exposures to human health. Important environmental pollutants are endocrine-disrupting che- micals (EDCs), which can have adverse e ects on the living organism due to their interference with the endocrine system. The group of known EDCs embraces ubiquitous synthetic substan- ces used as industrial lubricants and solvents, with their by-products, incomplete combustion remains, pharmaceuticals and personal care products, pesticides and plasticizers. Natural com- pounds such as genistein, a phytoestrogen, and heavy metals can also have endocrine e ects. Endocrine disruption is a serious public health problem. EDCs among other health problems ge- nerate reproductive disorders in males, such as decreases in sperm count and quality, increases in testicular germ cell numbers, prostate and breast cancers, cryptorchidism and hypospadias, impaired fertility, and infertility. This paper critically reviews the current knowledge of the impa- ct of EDCs on reproductive disorders in human males.

Downloads

Download data is not yet available.

Author Biographies

Damjan Balabanič, Faculty of Industrial Engineering Novo mesto, Novo mesto, Slovenia

/

Aleksandra Krivograd Klemenčič, Institute for Sanitary Engineering, Faculty of Civil and Geodetic Engineering, University of ljubljana, ljubljana, Slovenia
/

References

Colborn T, vom Saal FS, Soto AM. Developmental effects of endocrine-disrupting chemicals in wildlife and humans. Environmental Health Perspectives. 1993;101(5):378–84.

Safe SH. Endocrine Disruptors and Human Health–Is There a Problem? An Update. Environmental Health Perspectives. 2000;108(6):487–93.

Baskin LS, Himes K, Colborn T. Hypospadias and Endocrine Disruption: Is There a Connection? Environmental Health Perspectives. 2001;109(11):1175–83.

Balabanič D, Rupnik M, Krivograd Klemenčič A. Negative impacts of endocrine-disrupting compounds on human reproductive health. Reprod Fertil Dev. 2011;23(3):403–416.

Coster S, Larebeke N. Endocrine-Disrupting Chemicals: Associated Disorders and Mechanisms of Action. J. Environ. Public Health. 2012;2012:713696.

(EDSTAC)USEPA EDSaTAC. Endocrine disrupter screening and testing advisory committee final report. Available from: http://www.epa.gov/scipoly/oscpendo/history/finalrpt.htm.

Al-Saleh I, Coskun S, Mashhour A, Shinwari N, El-Doush I, Billedo G, et al. Exposure to heavy metals (lead, cadmium and mercury) and its effect on the outcome of in-vitro fertilization treatment. International Journal of Hygiene and Environmental Health. 2008;211(5–6):560–79.

Villeneuve S, Cyr D, Lynge E, Orsi L, Sabroe S, Merletti F, et al. Occupation and occupational exposure to endocrine disrupting chemicals in male breast cancer: a case-control study in Europe. Occupational and Environmental Medicine. 2010;67(12):837–44.

Birkett JW. Scope of the Problem. In: Birkett JW, Lester JN, eds. Endocrine Disrupters Wastewater and Sludge Treatment Processes. London: Lewis Publishers; 2003.

Fasano E, Bono-Blay F, Cirillo T, Montuori P, Lacorte S. Migration of phthalates, alkylphenols, bisphenol A and di(2-ethylhexyl)adipate from food packaging. Food Control. 2012;27(1):132–8.

McNeal TP, Biles JE, Begley TH, Craun JC, Hopper ML, Sack CA. Determination of Suspected Endocrine Disruptors in Foods and Food Packaging. ACS Symposium Series: American Chemical Society; 1999. p. 33–52.

Fernandes AR, Rose M, Charlton C. 4-Nonylphenol (NP) in food-contact materials: Analytical methodology and occurrence. Food Additives & Contaminants: Part A. 2008;25(3):364–72.

Toyo’Oka T, Oshige Y. Determination of Alkylphenols in Mineral Water Contained in PET Bottles by Liquid Chromatography with Coulometric Detection. Analytical Sciences. 2000;16(10):1071–6.

Casajuana N, Lacorte S. New Methodology for the Determination of Phthalate Esters, Bisphenol A, Bisphenol A Diglycidyl Ether, and Nonylphenol in Commercial Whole Milk Samples. Journal of Agricultural and Food Chemistry. 2004;52(12):3702–7.

Fierens T, Servaes K, Van Holderbeke M, Geerts L, De Henauw S, Sioen I, et al. Analysis of phthalates in food products and packaging materials sold on the Belgian market. Food and Chemical Toxicology. 2012;50(7):2575–83.

Self RL, Wu W-H. Rapid qualitative analysis of phthalates added to food and nutraceutical products by direct analysis in real time/orbitrap mass spectrometry. Food Control. 2012;25(1):13–6.

Nasreddine L, Parent-Massin D. Food contamination by metals and pesticides in the European Union. Should we worry? Toxicology Letters. 2002;127(1–3):29–41.

Mukherjee A, Sengupta MK, Hossain MA, Ahamed S, Das B, Nayak B, et al. Arsenic contamination in groundwater: a global perspective with emphasis on the Asian scenario. Journal of health, population, and nutrition. 2006;24(2):142–63.

Alam MGM, Snow ET, Tanaka A. Arsenic and heavy metal contamination of vegetables grown in Samta village, Bangladesh. Science of The Total Environment. 2003;308(1–3):83–96.

Sirot V, Guérin T, Volatier JL, Leblanc JC. Dietary exposure and biomarkers of arsenic in consumers of fish and shellfish from France. Science of The Total Environment. 2009;407(6):1875–85.

Clarkson TW. The Three Modern Faces of Mercury. Environmental Health Perspectives. 2002;110(s1):11–23.

Nasreddine L, Parent-Massin D. Food contamination by metals and pesticides in the European Union. Should we worry? Toxicology Letters. 2002;127(1–3):29–41.

Campion S, Catlin N, Heger N, McDonnell EV, Pacheco SE, Saffarini C, et al. Male Reprotoxicity and Endocrine Disruption. Experientia Supplementum: Springer Basel; 2012. p. 315–60.

Diamanti-Kandarakis E, Bourguignon J-P, Giudice LC, Hauser R, Prins GS, Soto AM, et al. Endocrine-Disrupting Chemicals: An Endocrine Society Scientific Statement. Endocrine Reviews. 2009;30(4):293–342.

Sharpe RM, Skakkebaek NE. Are oestrogens involved in falling sperm counts and disorders of the male reproductive tract? The Lancet. 1993;341(8857):1392–6.

Skakkebæk NE, Rajpert-De Meyts E, Main KM. Testicular dysgenesis syndrome: an increasingly common developmental disorder with environmental aspects: Opinion. Human Reproduction. 2001;16(5):972–8.

Schug TT, Janesick A, Blumberg B, Heindel JJ. Endocrine disrupting chemicals and disease susceptibility. The Journal of Steroid Biochemistry and Molecular Biology. 2011;127(3–5):204–15.

Foster PMD. Mode of Action: Impaired Fetal Leydig Cell Function—Effects on Male Reproductive Development Produced by Certain Phthalate Esters. Critical Reviews in Toxicology. 2005;35(8–9):713–9.

Foster PMD. Disruption of reproductive development in male rat offspring following in utero exposure to phthalate esters. International Journal of Andrology. 2006;29(1):140–7.

Sharpe RM. Environmental/lifestyle effects on spermatogenesis. Philosophical Transactions of the Royal Society B: Biological Sciences. 2010;365(1546):1697–712.

Mocarelli P, Gerthoux PM, Patterson DG, Milani S, Limonta G, Bertona M, et al. Dioxin Exposure, from Infancy through Puberty, Produces Endocrine Disruption and Affects Human Semen Quality. Environmental Health Perspectives. 2007;116(1):70–7.

Summary of DES effects Stillman R: In utero exposure to diethylstilbestrol: Adverse effects on the reproductive tract and reproductive performance in male and female offspring. Am J Obstet Gynecol 142:905, 1982. Journal of Nurse-Midwifery. 1982;27(6):39.

Weidner IS, Møller H, Jensen TK, Skakkebaek NE. Cryptorchidism and hypospadias in sons of gardeners and farmers. Environmental Health Perspectives. 1998;106(12):793–6.

Hosie S, Loff S, Witt K, Niessen K, Waag K. Is There a Correlation Between Organochlorine Compounds and Undescended Testes? European Journal of Pediatric Surgery. 2000;10(05):304–9.

Toppari J, Kaleva M, Virtanen HE. Trends in the incidence of cryptorchidism and hypospadias, and methodological limitations of registry-based data. APMIS. 2001;109(S103):S37-S42.

Boisen KA, Kaleva M, Main KM, Virtanen HE, Haavisto AM, Schmidt IM, et al. Difference in prevalence of congenital cryptorchidism in infants between two Nordic countries. The Lancet. 2004;363(9417):1264–9.

Carlsen E, Giwercman A, Keiding N, Skakkebaek NE. Evidence for decreasing quality of semen during past 50 years. BMJ. 1992;305(6854):609–13.

Dallinga JW, Moonen EJ, Dumoulin JC, Evers JL, Geraedts JP, Kleinjans JC. Decreased human semen quality and organochlorine compounds in blood. Human reproduction (Oxford, England). 2002;17(8):1973–9.

Guo YL, Hsu P-C, Hsu C-C, Lambert GH. Semen quality after prenatal exposure to polychlorinated biphenyls and dibenzofurans. The Lancet. 2000;356(9237):1240–1.

Skakkebaek NE, Rajpert-De Meyts E, Jorgensen N, Main KM, Leffers H, Andersson AM, et al. Testicular cancer trends as 'whistle blowers' of testicular developmental problems in populations. Int J Androl. 2007;30(4):198–204; discussion -5.

Lacerda HM, Akre O, Merletti F, Richiardi L. Time Trends in the Incidence of Testicular Cancer in Childhood and Young Adulthood. Cancer Epidemiology Biomarkers & Prevention. 2009;18(7):2042–5.

Kumar V, Yadav CS, Singh S, Goel S, Ahmed RS, Gupta S, et al. CYP 1A1 polymorphism and organochlorine pesticides levels in the etiology of prostate cancer. Chemosphere. 2010;81(4):464–8.

Hileman B. Environmental Estrogens linked to Reproductive Abnormalities, Cancer. Chemical & Engineering News. 1994;72(5):19–23.

Yu M-H, Tsunoda H, Tsunoda M. Environmental toxicology: biological and health effects of pollutants: CRC Press; 2011. p. 281–295.

Marques-Pinto A, Carvalho D. Human infertility: are endocrine disruptors to blame? Endocrine Connections. 2013;2(3):R15-R29.

Jeng HA. Exposure to Endocrine Disrupting Chemicals and Male Reproductive Health. Frontiers in Public Health. 2014;2.

Dearnaley D. Regular review: Managing testicular cancer. BMJ. 2001;322(7302):1583–8.

Sharpe RM. The 'oestrogen hypothesis'- where do we stand now?1. International Journal of Andrology. 2003;26(1):2–15.

Aitken RJ, Skakkebaek NE, Roman SD. Male reproductive health and the environment. The Medical journal of Australia. 2006;185(8):414–5.

Curado M-P, Edwards B, Shin HR, Storm H, Ferlay J, Heanue M, et al. Cancer incidence in five continents, Volume IX: IARC Press, International Agency for Research on Cancer; 2007.

Virtanen HE, Rajpert-De Meyts E, Main KM, Skakkebaek NE, Toppari J. Testicular dysgenesis syndrome and the development and occurrence of male reproductive disorders. Toxicology and applied pharmacology. 2005;207(2 Suppl):501–5.

Rajpert-De Meyts E. Developmental model for the pathogenesis of testicular carcinoma in situ: genetic and environmental aspects. Human reproduction update. 2006;12(3):303–23.

Mylchreest E, Sar M, Wallace DG, Foster PM. Fetal testosterone insufficiency and abnormal proliferation of Leydig cells and gonocytes in rats exposed to di(n-butyl) phthalate. Reproductive toxicology (Elmsford, NY). 2002;16(1):19–28.

Ferrara D, Hallmark N, Scott H, Brown R, McKinnell C, Mahood IK, et al. Acute and long-term effects of in utero exposure of rats to di(n-butyl) phthalate on testicular germ cell development and proliferation. Endocrinology. 2006;147(11):5352–62.

Olesen IA, Sonne SB, Hoei-Hansen CE, Rajpert-De Meyts E, Skakkebaek NE. Environment, testicular dysgenesis and carcinoma in situ testis. Best practice & research Clinical endocrinology & metabolism. 2007;21(3):462–78.

Haas GP, Delongchamps N, Brawley OW, Wang CY, de la Roza G. The worldwide epidemiology of prostate cancer: perspectives from autopsy studies. The Canadian journal of urology. 2008;15(1):3866–71.

Hsing AW, Tsao L, Devesa SS. International trends and patterns of prostate cancer incidence and mortality. International journal of cancer. 2000;85(1):60–7.

Greenlee RT, Hill-Harmon MB, Murray T, Thun M. Cancer statistics, 2001. CA: a cancer journal for clinicians. 2001;51(1):15–36.

CDC. Centers for Disease Control and prevention. United States Cancer Statistics, 2012. Top Ten Cancers[20.10.2015]. Availabe from. https://nccd.cdc.gov/uscs/toptencancers.aspx.

Prins GS, Tang W-Y, Belmonte J, Ho S-M. Perinatal Exposure to Oestradiol and Bisphenol A Alters the Prostate Epigenome and Increases Susceptibility to Carcinogenesis. Basic & Clinical Pharmacology & Toxicology. 2008;102(2):134–8.

Maffini MV, Rubin BS, Sonnenschein C, Soto AM. Endocrine disruptors and reproductive health: The case of bisphenol-A. Molecular and Cellular Endocrinology. 2006;254–255:179–86.

Schlumpf M, Durrer S, Faass O, Ehnes C, Fuetsch M, Gaille C, et al. Developmental toxicity of UV filters and environmental exposure: a review. International Journal of Andrology. 2008;31(2):144–51.

Hofkamp L, Bradley S, Tresguerres J, Lichtensteiger W, Schlumpf M, Timms B. Region-Specific Growth Effects in the Developing Rat Prostate Following Fetal Exposure to Estrogenic Ultraviolet Filters. Environmental Health Perspectives. 2008;116(7):867–72.

Schlumpf M, Schmid P, Durrer S, Conscience M, Maerkel K, Henseler M, et al. Endocrine activity and developmental toxicity of cosmetic UV filters—an update. Toxicology. 2004;205(1–2):113–22.

Fechner P, Damdimopoulou P, Gauglitz G. Biosensors Paving the Way to Understanding the Interaction between Cadmium and the Estrogen Receptor Alpha. PloS one. 2011;6(8):e23048.

Waalkes MP. Cadmium carcinogenesis in review. Journal of Inorganic Biochemistry. 2000;79(1–4):241–4.

Benbrahim-Tallaa L, Waterland RA, Dill AL, Webber MM, Waalkes MP. Tumor Suppressor Gene Inactivation during Cadmium-Induced Malignant Transformation of Human Prostate Cells Correlates with Overexpression ofde NovoDNA Methyltransferase. Environmental Health Perspectives. 2007.

Benbrahim-Tallaa L, Waalkes MP. Inorganic Arsenic and Human Prostate Cancer. Environmental Health Perspectives. 2007;116(2):158–64.

García MA, Peña D, Álvarez L, Cocca C, Pontillo C, Bergoc R, et al. Hexachlorobenzene induces cell proliferation and IGF-I signaling pathway in an estrogen receptor α-dependent manner in MCF-7 breast cancer cell line. Toxicology Letters. 2010;192(2):195–205.

Valerón PF, Pestano JJ, Luzardo OP, Zumbado ML, Almeida M, Boada LD. Differential effects exerted on human mammary epithelial cells by environmentally relevant organochlorine pesticides either individually or in combination. Chemico-Biological Interactions. 2009;180(3):485–91

Calaf G, Roy D. Cancer genes induced by malathion and parathion in the presence of estrogen in breast cells. International Journal of Molecular Medicine. 2008.

Ptak A, Ludewig G, Rak A, Nadolna W, Bochenek M, Gregoraszczuk EL. Induction of cytochrome P450 1A1 in MCF-7 human breast cancer cells by 4-chlorobiphenyl (PCB3) and the effects of its hydroxylated metabolites on cellular apoptosis. Environment International. 2010;36(8):935–41.

Weng Y-I, Hsu P-Y, Liyanarachchi S, Liu J, Deatherage DE, Huang Y-W, et al. Epigenetic influences of low-dose bisphenol A in primary human breast epithelial cells. Toxicology and applied pharmacology. 2010;248(2):111–21.

Fernandez SV, Russo J. Estrogen and Xenoestrogens in Breast Cancer. Toxicologic Pathology. 2009;38(1):110–22.

Charles AK, Darbre PD. Oestrogenic activity of benzyl salicylate, benzyl benzoate and butylphenylmethylpropional (Lilial) in MCF7 human breast cancer cellsin vitro. Journal of Applied Toxicology. 2009;29(5):422–34.

Siewit CL, Gengler B, Vegas E, Puckett R, Louie MC. Cadmium Promotes Breast Cancer Cell Proliferation by Potentiating the Interaction between ERα and c-Jun. Molecular Endocrinology. 2010;24(5):981–92.

Yu X, Filardo EJ, Shaikh ZA. The membrane estrogen receptor GPR30 mediates cadmium-induced proliferation of breast cancer cells. Toxicology and applied pharmacology. 2010;245(1):83–90.

Jenkins S, Rowell C, Wang J, Lamartiniere C. Prenatal TCDD exposure predisposes for mammary cancer in rats. Reproductive Toxicology. 2007;23(3):391–6.

Murray T, Maffini M, Ucci A, Sonnenschein C, Soto A. Induction of mammary gland ductal hyperplasias and carcinoma in situ following fetal bisphenol A exposure. Reproductive Toxicology. 2007;23(3):383–90.

Vandenberg LN, Maffini MV, Schaeberle CM, Ucci AA, Sonnenschein C, Rubin BS, et al. Perinatal exposure to the xenoestrogen bisphenol-A induces mammary intraductal hyperplasias in adult CD-1 mice. Reproductive Toxicology. 2008;26(3–4):210–9.

Durando M, Kass L, Piva J, Sonnenschein C, Soto AM, Luque EH, et al. Prenatal Bisphenol A Exposure Induces Preneoplastic Lesions in the Mammary Gland in Wistar Rats. Environmental Health Perspectives. 2006;115(1):80–6.

Jenkins S, Raghuraman N, Eltoum I, Carpenter M, Russo J, Lamartiniere CA. Oral Exposure to Bisphenol A Increases Dimethylbenzanthracene-Induced Mammary Cancer in Rats. Environmental Health Perspectives. 2009;117(6):910–5.

Markey CM, Luque EH, Munoz de Toro M, Sonnenschein C, Soto AM. In Utero Exposure to Bisphenol A Alters the Development and Tissue Organization of the Mouse Mammary Gland1. Biology of Reproduction. 2001;65(4):1215–23.

Russo J, Russo IH. DNA labeling index and structure of the rat mammary gland as determinants of its susceptibility to carcinogenesis. Journal of the National Cancer Institute. 1978;61(6):1451–9.

Toppari J, Skakkebæk NE. Endocrine disruption in male human reproduction. Environmental Endocrine Disruptors: An Evolutionary Perspective. 2000. p. 269–290.

Swan SH. Semen quality in fertile US men in relation to geographical area and pesticide exposure. International Journal of Andrology. 2006;29(1):62–8.

Serrano M, Gonzalvo MC, Sanchez-Pozo MC, Clavero A, Fernandez MF, Lopez-Regalado ML, et al. Adherence to reporting guidelines in observational studies concerning exposure to persistent organic pollutants and effects on semen parameters. Human Reproduction. 2014;29(6):1122–33.

De Celis R, Feria-Velasco A, González-Unzaga M, Torres-Calleja J, Pedrón-Nuevo N. Semen quality of workers occupationally exposed to hydrocarbons. Fertility and Sterility. 2000;73(2):221–8.

Danadevi K, Rozati R, Reddy PP, Grover P. Semen quality of Indian welders occupationally exposed to nickel and chromium. Reproductive Toxicology. 2003;17(4):451–6.

Woodruff TJ, Zota AR, Schwartz JM. Environmental Chemicals in Pregnant Women in the United States: NHANES 2003–2004. Environmental Health Perspectives. 2011;119(6):878–85.

Published
2018-03-02
How to Cite
1.
Balabanič D, Krivograd Klemenčič A. Endocrine-disrupting chemicals and male reproductive health: a review. TEST ZdravVestn [Internet]. 2Mar.2018 [cited 26Apr.2024];87(1-2):69-0. Available from: http://vestnik-dev.szd.si/index.php/ZdravVest/article/view/2456
Section
Professional Article