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Analysis of the relationship between the blood concentration of several metals, macro- and micronutrients and endocrine disorders associated with male aging

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Abstract

Beyond 30 years of age, men experience a decline in the production of testosterone, yet only a few develop late-onset hypogonadism. This study was designed to determine the relationship between blood concentrations of metals, macro- and micronutrients and age-related testosterone deficiency and associated hormonal changes in aging men. The research involved 313 men aged 50–75 years. We used ELISA to determine the concentrations of total testosterone (TT), free testosterone (FT), estradiol (E2), dehydroepiandrosterone sulfate (DHEAS) and sex hormone-binding globulin (SHBG). We calculated free androgen index (FAI). With the use of emission spectrometry in inductively coupled argon plasma, we determined the whole-blood concentrations of lead (Pb), cadmium (Cd), mercury (Hg), arsenic (As) and tungsten (W), as well as serum concentrations of magnesium (Mg), iron (Fe), calcium (Ca), copper (Cu), zinc (Zn), selenium (Se), chromium (Cr), manganese (Mn) and molybdenum (Mo). The study showed no relationship between TT and FT and the concentrations of metals. Men with TT deficiency had significantly lower concentrations of Mg and Fe and increased Mn. Men with FT deficiency had higher W and Cr levels and lower Fe. Assessing the correlation between the concentrations of hormones, SHBG and FAI, and the concentration of metals and macro- and microelements in the blood of the men, we found positive correlations between the concentrations of TT-Mg, TT-Fe, TT-Mo, FT-Fe, E2-As, SHBG-Mn, FAI-W, FAI-As, FAI-Zn and FAI-Ca, and negative correlations between the concentrations of TT-Mn, FT-Cd, FT-Cr, E2-Hg, E2-Cr, SHBG-W, SHBG-As, SHBG-Zn, SHBG-Ca, FAI-Pb and FAI-Mn. Positive correlations between As and E2 and between As and FAI may suggest a lack of association between this metal and hypogonadism in people not exposed to excess As levels. Our research indicates a positive relationship between the concentrations of Mg, Fe and Zn and endocrine system in aging men, in contrast to Mn and Cr. Toxic metals (Cd, Pb) seemed to negatively affect the level of bioavailable testosterone. In persons not exposed to As, As does not contribute late-onset hypogonadism. Heavy metals (Pb, Cd, Hg and W) may contribute to a lower concentration of DHEAS. The role of W in men with LOH was found to be ambiguous, as on the one hand its concentration was higher in men with FT deficiency, and on the other hand it positively correlated with FAI, which in turn indirectly indicates testosterone availability. Copper and selenium do not seem to play any significant role in the occurrence of TT deficiency in aging men.

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Abbreviations

PADAM:

Partial androgen deficiency in an aging male

LOH:

Late-onset hypogonadism

T:

Testosterone

TT:

Total testosterone

FT:

Free testosterone

DHEAS:

Dehydroepiandrosterone sulfate

SHBG:

Sex hormone-binding globulin

E2 :

Estradiol

FAI:

Free androgen index

NOS:

Nitric oxide synthase

References

  • Ayaz, O., & Howlett, S. E. (2015). Testosterone modulates cardiac contraction and calcium homeostasis: Cellular and molecular mechanisms. Biology of Sex Differences, 6, 9.

    Article  Google Scholar 

  • Bachman, E., Feng, R., Travison, T., Li, M., Olbina, G., Ostland, V., et al. (2010). Testosterone suppressed hepcidin in men: A potential mechanism for testosterone-inducted erythrocitosis. Journal of Clinical Endocrinology and Metabolism, 95, 4743–4747.

    Article  CAS  Google Scholar 

  • Ballester, J., Dominguez, J., Munoz, M. C., Sensat, M., Rigau, T., Guinovart, J. J., & Rodriguez-Gil, J. E. (2005). Tungstate treatment improves Leydig cell function in streptozotocin-diabetic rats. Journal of Andrology, 26, 706–715.

    Article  CAS  Google Scholar 

  • Barbagallo, M., Belvedere, M., & Dominguez, L. J. (2009). Magnesium homeostasis and aging. Magnesium Research, 22, 235–246.

    CAS  Google Scholar 

  • Barbagallo, M., & Dominguez, L. J. (2010). Magnesium and aging. Current Pharmaceutical Design, 16, 832–839.

    Article  CAS  Google Scholar 

  • Baulieu, E. E., Thomas, G., Legrain, S., Lahlou, N., Roger, M., Debuire, B., et al. (2000). Dehydroepiandrosterone (DHEA), DHEA sulfate, and aging: Contribution of the DHEAge Study to a sociobiomedical issue. Proceedings of the national academy of sciences of the United States of America, 97, 4279–4284.

    Article  CAS  Google Scholar 

  • Benoff, S., Millan, C., Hurley, I. R., Napolitano, B., & Marmar, J. L. (2004). Bilateral increased apoptosis and bilateral accumulation of cadmium in infertile men with left varicocele. Human Reproduction, 19, 616–627.

    Article  CAS  Google Scholar 

  • Boudou, F., Aldi, D. E. H., Slimani, M., & Berroukche, A. (2014). The impact of chronic exposure to manganese on testiculaire tissue and sperm parameters in rat Wistar. International Journal of Natural Sciences Research, 3, 12–19.

    Google Scholar 

  • Byrne, J. V., Hope, J. K., Hubbard, N., & Morris, J. H. (1997). The nature of thrombosis induced by platinum and tungsten coils in saccular aneurysms. American Journal of Neuroradiology, 18, 29–33.

    CAS  Google Scholar 

  • Castanho, T. C., Moreira, P. S., Portugal-Nunes, C., Novais, A., Costa, P. S., Palha, J. A., et al. (2014). The role of sex and sex-related hormones in cognition, mood and well-being in older men and women. Biological Psychology, 103, 158–166.

    Article  Google Scholar 

  • Chang, S. C., Choi, J. B., Kim, H. J., & Park, S. B. (2011). Correlation between serum testosterone level and concentrations of copper and zinc in hair tissue. Biological Trace Element Research, 144, 264–271.

    Article  CAS  Google Scholar 

  • Christensen, M. (2014). Selenium and prostate cancer prevention: What next—if anything? Cancer prevention research, 7, 781–785. (Philadelphia, Pa.).

    Article  CAS  Google Scholar 

  • Chung, A. S., & Mains, P. D. (1987). Differential effect of cadmium on GSH—peroxides activity in the leydig and the sertoli cells of rats testis. Biochemical Pharmacology, 36, 1367–1372.

    Article  CAS  Google Scholar 

  • Cinar, V., Polat, Y., Baltaci, A. K., & Mogulkoc, R. (2011). Effects of magnesium supplementation on testosterone level of athletes and sedentary subjects et rest and after exhaustion. Biological Trace Element Research, 149, 18–23.

    Article  Google Scholar 

  • Costa, M., & Klein, C. B. (2006). Toxicity and carcinogenicity of chromium compounds in humans. Critical Reviews in Toxicology, 36, 155–163.

    Article  CAS  Google Scholar 

  • Croxford, T. P., McCormick, N. H., & Kelleher, S. L. (2011). Moderate zinc deficiency reduces testicular Zip6 and Zip10 abundance and impairs spermatogenesis in mice. Journal of Nutrition, 141, 359–365.

    Article  CAS  Google Scholar 

  • Czeczot, H., & Majewska, M. (2010). Cadmium—exposure and its effects health. Farmacja Polska, 66, 243–250. (in Polish).

    Google Scholar 

  • Deslypere, J. P., & Vermeulen, A. (1984). Leydig cell function in normal men: Effect of age, life-style, residence, diet and activity. Journal of Clinical Endocrinology and Metabolism, 59, 955–962.

    Article  CAS  Google Scholar 

  • Dharia, S., & Parker, C. R, Jr. (2004). Adrenal androgens and aging. Seminars in Reproductive Medicine, 22, 361–368.

    Article  CAS  Google Scholar 

  • El Husseiny, N. M., Said, E. S., El Shahat Mohamed, N., & Othman, A. I. (2011). Impact of trace element changes on dehydroepiandrosterone sulfate in healthy and diabetic states among middle-age and elderly Egyptians. Biological Trace Element Research, 143, 1451–1460.

    Article  CAS  Google Scholar 

  • El-Desoky, G. E., Bashandy, S. A., Alhazza, I. M., Al-Othman, Z. A., Aboul-Soud, M. A. M., & Yusuf, K. (2013). Improvement od mercuric chloride-inducted testis injuries and sperm quality deteriorations by Spirulina platensis in rats. PLoS ONE, 8, e59177.

    Article  CAS  Google Scholar 

  • Eroglu, M., Sahin, S., Durukan, B., Ozakpinar, O. B., Erdinc, N., Turkgeldi, L., et al. (2014). Blood serum and seminal plasma selenium, total antioxidant capacity and coenzyme Q10 levels in relation to semen parameters in men with idiopathic infertility. Biological Trace Element Research, 2014(159), 46–51.

    Article  Google Scholar 

  • Fahim, M. S., Wang, M., Sutcu, M. F., & Fahim, Z. (1993). Zinc arginine, a 5 alpha-reductase inhibitor, reduces rat ventral prostate weight and DNA without affecting testicular function. Andrology, 25, 369–775.

    Article  CAS  Google Scholar 

  • Gomuła, A., & Rabijewski, M. (2010). Testosterone deficiency syndrome—diagnosis and treatment—based on age-related testosterone referent levels. Seksuologia Polska, 8, 1–16.

    Google Scholar 

  • Gorbel, F., Boujelbene, M., Makni-Ayadi, F., Guermazi, F., Croute, F., Soleilhavoup, J. P., & el Feki, A. (2002). Cytotoxic effect of lead on the endocrine and exocrine sexual function of pubescent male and female rats. Demonstration of apoptotic activity. Comptes Rendus Biologies, 325, 927–940.

    Article  CAS  Google Scholar 

  • Goyer, R. A., Liu, J., & Waalkes, M. P. (2004). Cadmium and cancer of prostate and testis. BioMetals, 2004(17), 555–558.

    Article  Google Scholar 

  • Guo, W., Bachman, E., Li, M., Roy, C. N., Blusztajn, J., Wong, S., et al. (2013). Testosterone administration inhibits hepcidin transcription and is associated with increased iron incorporation into red blood cells. Aging Cell, 12, 280–291.

    Article  CAS  Google Scholar 

  • Herrera, A., Lobo-Escolar, A., Mateo, J., Gil, J., Ibarz, E., & Gracia, L. (2012). Male osteoporosis: A review. World Journal of Orthopedics, 3, 223–234.

    Article  Google Scholar 

  • Hsieh, F. I., Hwang, T. S., Hsieh, Y. C., Lo, H. C., Su, C. T., Hsu, H. S., et al. (2008). Risk of erectile dysfunction inducted by arsenic exposure through well water consumption in Taiwan. Environmental Health Perspectives, 116, 532–536.

    Article  CAS  Google Scholar 

  • Huang, J. H., Lu, Y. F., Cheng, F. C., Lee, J. N., & Tsai, L. C. (2012). Correlation of magnesium intake with metabolic parameters, depression and physical activity in elderly type 2 diabetes patients: A cross-sectional study. Nutrition Journal, 11, 41.

    Article  Google Scholar 

  • Jalali, G. R., Roozbeh, J., Mohammadzadeh, A., Sharifian, M., Sagheb, M. M., Hamidian Jahromi, A., et al. (2010). Impact of oral zinc therapy on the level of sex hormones in male patients on hemodialysis. Renal Failure, 32, 417–419.

    Article  CAS  Google Scholar 

  • Jurczak, A., Brodowski, J., Grochans, E., Karakiewicz, B., Szkup-Jabłońska, M., Wieder-Huszla, S., et al. (2013). Effect of menopausal hormone therapy on the levels of magnesium, zinc, lead and cadmium in post-menopausal women. Annals of Agricultural and Environmental Medicine, 20, 147–151.

    CAS  Google Scholar 

  • Kaufman, J. M., & Vermeulen, A. (2005). The decline of androgen levels in elderly men and its clinical and therapeutic implications. Endocrine Reviews, 26, 833–876.

    Article  CAS  Google Scholar 

  • Killilea, D. W., & Maier, J. A. (2008). A connection between magnesium deficiency and aging: New insights from cellular studies. Magnesium Research, 21, 77–82.

    CAS  Google Scholar 

  • Kim, S. W., Hwang, J. H., Cheon, J. M., Park, N. S., Park, S. E., Park, S. J., et al. (2005). Direct and indirect effects of androgens on survival of hematopoietic progenitor cells in vitro. Journal of Korean Medical Science, 20, 409–416.

    Article  Google Scholar 

  • Koehler, K., Parr, M. K., Geyer, H., Mester, J., & Schanzer, W. (2009). Serum testosterone and urinary excretion of steroid hormone metabolites after administration of a high-dose zinc supplement. European Journal of Clinical Nutrition, 63, 63–70.

    Article  Google Scholar 

  • Koshla, S. (2004). Role of hormonal changes in the pathogenesis of osteoporosis in men. Calcified Tissue International, 75, 110–113.

    Google Scholar 

  • Kula, K., & Słowikowska-Hilczer, J. (2012). Late onset hypogonadism in men. Polish Journal of Endocrinology, 63, 15–19.

    CAS  Google Scholar 

  • Kumari, D., Nair, N., & Bedwal, R. S. (2011). Testicular apoptosis after dietary zinc deficiency: Ultrastructural and TUNEL studies. Systems Biology in Reproductive Medicine, 57, 233–243.

    Article  CAS  Google Scholar 

  • Langard, S., Andersen, A., & Ravnestad, J. (1990). Incidence of cancer among ferrochromium and ferrosilicon workers: An extended observation period. British Journal of Industrial Medicine, 47, 14–19.

    CAS  Google Scholar 

  • Leder, B. Z., LeBlanc, K. M., Schoenefeld, D. A., Eastell, R., & Finkelstein, J. S. (2003). Differential effects of androgens and estrogens on bone turnover in normal men. Journal of Clinical Endocrinology and Metabolism, 88, 204–210.

    Article  CAS  Google Scholar 

  • Maggio, M., Ceda, C. P., Lauretani, F., Cattabiani, C., Avantaggiato, E., Morganti, S., et al. (2011). Magnesium and anabolic hormones in older men. International Journal of Andrology, 34, e594–e600.

    Article  CAS  Google Scholar 

  • Maggio, M., De Vita, F., Lauretani, F., Nouvenne, A., Meschi, T., Ticinesi, A., et al. (2014). The interplay between magnesium and testosterone in modulating physical function in men. International Journal of Endocrinology, 2014, 525249.

    Article  Google Scholar 

  • Majewska, D., Małgorzata Jakubowska, M., Ligocki, M., Tarasewicz, Z., Szczerbińska, D., Karamucki, T., & Sales, J. (2009). Physicochemical characteristics, proximate analysis and mineral composition of ostrich meat as influenced by muscle. Food Chemistry, 117, 207–211.

    Article  CAS  Google Scholar 

  • Martin, M. B., Voeller, H. J., Gelmann, E. P., Lu, J., Stoica, E. G., Herbert, E. J., et al. (2002). Role of cadmium in the regulation of AR gene expression and activity. Endocrinology, 143, 263–275.

    Article  CAS  Google Scholar 

  • Martynowicz, H., Andrzejak, R., & Mędraś, M. (2005). The influence of lead on testis function). Medycyna Pracy, 56, 495–500.

    CAS  Google Scholar 

  • McVey, M. J., Cooke, G. M., Curran, I. H., Chan, H. M., Kubow, S., Lok, E., & Mehta, R. (2008). An investigation of the effects of methylmercury in rats fed different dietary fats and proteins: Testicular steroidogenic enzymes and serum testosterone levels. Food and Chemical Toxicology, 46, 270–279.

    Article  CAS  Google Scholar 

  • Meeker, J. D., Rossano, M. G., Protas, B., Padmanahban, V., Diamond, M. P., Puscheck, E., et al. (2010). Environmental exposure to metals and male reproductive hormones: Circulating testosterone is inversely, associated with blood molybdenum. Fertility and Sterility, 93, 130–140.

    Article  CAS  Google Scholar 

  • Mendiola, J., Moreno, J. M., Roca, M., Vergara-Juarez, N., Martinez-Garcia, M., Garcia-Sanchez, A., et al. (2011). Relationships between heavy metal concentration in three different body fluids and male reproductive parameters: A pilot study. Environmental Health, 10, 6.

    Article  CAS  Google Scholar 

  • Menke, A., Guallar, E., Shiels, M., Rohrmann, S., Basaria, S., Rifai, N., et al. (2008). The association of urinary cadmium with sex steroid hormone concentrations in a general population sample of US adult men. BMC Public Health, 8, 72.

    Article  Google Scholar 

  • Mocevic, E., Specht, I. O., Marrot, J. L., Giwercman, A., Jonsson, B. A., Toft, G., et al. (2013). Environmental mercury exposure, semen quality and reproductive hormones in Greenlandic Inuit and European men: A cross-sectional study. Asian Journal of Andrology, 15, 97–104.

    Article  CAS  Google Scholar 

  • Morley, J. E., Charlton, E., Patrick, P., Kaiser, F. E., Cadeau, P., McCready, D., & Perry, H. M, 3rd. (2000). Validation of a screening questionnaire for androgen deficiency in aging males. Metabolism, 49, 1239–1242.

    Article  CAS  Google Scholar 

  • Neff, M. S., Goldberg, J., Slifkin, R. F., Eiser, A. F., Calamia, V., Kaplan, M., et al. (1981). A comparison of androgens for anemia in patients on hemodialysis. New England Journal of Medicine, 304, 871–875.

    Article  CAS  Google Scholar 

  • Ng, T. P., Goh, H. H., Ng, Y. L., Ong, H. Y., Ong, C. N., Chia, H. S., et al. (1991). Male endocrine functions in workers with moderate exposure to lead. British Journal of Industrial Medicine, 48, 485–491.

    CAS  Google Scholar 

  • Pandya, C., Pillai, P., Nampoothiri, L. P., Bhatt, N., Gupta, S., & Gupta, S. (2012). Effect of lead and cadmium co-exposure on testicular steroid metabolism and antioxidant system of adult male rats. Andrology, Supp, 1, 813–822.

    Article  Google Scholar 

  • Pant, N., Kumar, R., Murthy, R. C., & Srivastava, S. P. (2001). Male reproductive effect of arsenic in mice. BioMetals, 14, 113–117.

    Article  CAS  Google Scholar 

  • Pizent, A., Tariba, B., & Živković, T. (2012). Reproductive toxicity of metals in men. Archives of Industria Hygiene and Toxicology, 63, 35–46.

    Article  Google Scholar 

  • Potula, V., & Kaye, W. (2006). The impact of menopause and lifestyle factors on blood and bone lead levels among female former smelter workers: The Bunker Hill Study. American Journal of Industrial Medicine, 49, 143–152.

    Article  CAS  Google Scholar 

  • Prasad, A. S. (2008). Zinc in human health: Effect of zinc on immune cells. Molecular Medicine, 14, 353–357.

    Article  CAS  Google Scholar 

  • Rabijewski, M., & Zgliczyński, W. (2009). Pathogenesis, evaluation and treatment of hypogonadism in men. Polish Journal of Endocrinology, 3, 222–233.

    Google Scholar 

  • Rambouskova, J., Krskova, A., Slavíkova, M., Cejchanova, M., & Cerna, M. (2014). Blood levels of lead, cadmium and mercury in the elderly living in institutionalized care in Czech Republic. Experimental Gerontology, 9, 8–13.

    Article  Google Scholar 

  • Rutkowski, K., Sowa, P., Rutkowska-Talipska, J., Kuryliszyn-Moskal, A., & Rutkowski, R. (2014). Dehydroepiandrosterone (DHEA): Hypes and Hopes. Drugs, 74, 1195–1207.

    Article  CAS  Google Scholar 

  • Sanghamitra, S., Hazra, J., Upadhyay, S. N., Singh, S. K., & Amal, R. C. (2008). Arsenic inducted toxicity on testicular tissue of mice. Indian Journal of Physiology and Pharmacology, 52, 84–90.

    Google Scholar 

  • Satarug, S., Baker, J. R., Urbenjapol, S., Haswell-Elkins, M., Reilly, P. E., Williams, D. J., & Moore, M. R. (2003). A global perspective on cadmium pollutionand toxicity in non-occupationally exposed population. Toxicology Letters, 137, 65–83.

    Article  CAS  Google Scholar 

  • Shinohara, A., & Watanabe, H. (1996). Role of essential trace elements on sexual function and its disorder. Nihon Rinsho, 54, 155–161. (in Japanese).

    CAS  Google Scholar 

  • Siu, E. R., Mruk, D. D., Porto, C. S., & Cheng, C. J. (2009). Cadmium-induced testicular injury. Toxicology and Applied Pharmacology, 238, 240–249.

    Article  CAS  Google Scholar 

  • Snyder, P. (2001). Effects of age on testicular function and consequences of testosterone treatment. Journal of Clinical Endocrinology and Metabolism, 86, 2369–2372.

    CAS  Google Scholar 

  • Stojek, E., & Skoczyńska, A. (2003). The effect of lead on vascular endothelium. Medycyna Pracy, 54, 87–93.

    CAS  Google Scholar 

  • Svartberg, J., Midtby, M., Bonaa, K. H., Sundsfjord, J., Joakimsen, R. M., & Jorde, R. (2003). The associations of age, lifestyle factors and chronic disease with testosterone in men: The Tromso Study. European Journal of Endocrinology, 149, 145–152.

    Article  CAS  Google Scholar 

  • Swaminathan, R. (2003). Magnesium metabolism and its disorders. Clinical Biochemist Reviews, 24, 47–66.

    CAS  Google Scholar 

  • Symanski, E., & Hertz, P. I. (1995). Blood lead levels in relation to menopause smoking and pregnancy history. American Journal of Epidemiology, 141, 1047–1058.

    CAS  Google Scholar 

  • Tilghman, S. L., Nierth-Simpson, E. N., Wallace, R., Burow, M. E., & McLachlan, J. A. (2008). Environmental hormones: Multiple pathways for response may lead to multiple disease out-comes. Steroids, 75, 520–523.

    Article  Google Scholar 

  • Turk, S., Mandar, R., Mahlapuu, R., Viitak, A., Punab, M., & Kullissar, T. (2014). Male infertility: Decreased level of selenium, zinc and antioxidants. Journal of Trace Elements in Medicine and Biology, 28, 179–185.

    Article  CAS  Google Scholar 

  • Wang, T. C., Jia, G., Song, Y. S., Zhang, J., Ma, Y. H., Feng, W. Y., et al. (2012). Effects of chronic chromate exposure on human serum prostate specific antigen: A cross sectional study. Industrial Health, 50, 95–102.

    Article  CAS  Google Scholar 

  • Wirth, J. J., & Mijal, R. S. (2010). Adverse effects of low level heavy metal exposure on male reproductive function. Systems Biology in Reproductive Medicine, 56, 147–167.

    Article  CAS  Google Scholar 

  • Wirth, J. J., Rossano, M. G., Daly, D. C., Paneth, N., Puscheck, E., Potter, R. C., & Diamond, M. P. (2007). Ambient manganese exposure is negatively associated with human sperm motility and concentration. Epidemiology, 18, 270–273.

    Article  Google Scholar 

  • Wlazlo, N., Peters, W., & Bravenboer, B. (2012). Hypogonadism in a patient with mild hereditary haemochromatosis. Netherlands Journal of Medicine, 70, 318–320.

    CAS  Google Scholar 

  • Wong, W. Y., Flik, G., Groenen, P. M., Swinkels, D. W., Thomas, C. M., Copius-Peereboom, J. H., et al. (2001). The impact of calcium, magnesium, zinc, and copper in blood and seminal plasma on semen parameters in men. Reproductive Toxicology, 15, 131–136.

    Article  CAS  Google Scholar 

  • World Medical Association. (2013). World Medical Association Declaration of Helsinki ethical principles for medical research involving human subjects. JAMA, 310, 2191–2194.

    Article  Google Scholar 

  • Wu, F. C., Tajar, A., Pye, S. R., Silman, A. J., Finn, J. D., O’Neill, T. W., et al. (2008). European Male Aging Study Group: Hypothalmic-pituitary-testicular axis disruptions in older men are differentially linked to age and modifiable risk factors: The European Male Aging Study. Journal of Clinical Endocrinology and Metabolism, 93, 2737–2745.

    Article  CAS  Google Scholar 

  • Yamaguchi, S., Miura, C., Kikuchi, K., Celino, F. T., Agusa, T., Tanabe, S., & Miura, T. (2009). Zinc is an essential trace element for spermatogenesis. Proceedings of the National Academy of Sciences of the United States of America, 106, 10859–10864.

    Article  CAS  Google Scholar 

  • Yousofvand, N., Zarei, F., & Ghanbari, A. (2013). Exogenous testosterone, finasteride and castration effects on testosterone, insulin, zinc and chromium in adult male rats. Iranian Biomedical Journal, 17, 49–53.

    CAS  Google Scholar 

  • Zeng, X., Jin, T., Jiang, X., Kong, Q., Ye, T., & Nordberg, G. F. (2004). Effects on the prostate of environmental cadmium exposure–a cross-sectional population study in China. BioMetals, 17, 559–565.

    Article  CAS  Google Scholar 

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Acknowledgments

The study was financed as research Project No. FSN (stimulation fund research) WNoZ 321-10/13 by Pomeranian Medical University in Szczecin.

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Rotter, I., Kosik-Bogacka, D.I., Dołęgowska, B. et al. Analysis of the relationship between the blood concentration of several metals, macro- and micronutrients and endocrine disorders associated with male aging. Environ Geochem Health 38, 749–761 (2016). https://doi.org/10.1007/s10653-015-9758-0

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