Environmental Geochemistry and Health

, Volume 38, Issue 3, pp 749–761 | Cite as

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

  • Iwona Rotter
  • Danuta I. Kosik-Bogacka
  • Barbara Dołęgowska
  • Krzysztof Safranow
  • Magdalena Kuczyńska
  • Maria Laszczyńska
Original Paper

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.

Keywords

Blood levels of metals Macroelements Microelements Androgen deficiency 

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

  1. Ayaz, O., & Howlett, S. E. (2015). Testosterone modulates cardiac contraction and calcium homeostasis: Cellular and molecular mechanisms. Biology of Sex Differences, 6, 9.CrossRefGoogle Scholar
  2. 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.CrossRefGoogle Scholar
  3. 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.CrossRefGoogle Scholar
  4. Barbagallo, M., Belvedere, M., & Dominguez, L. J. (2009). Magnesium homeostasis and aging. Magnesium Research, 22, 235–246.Google Scholar
  5. Barbagallo, M., & Dominguez, L. J. (2010). Magnesium and aging. Current Pharmaceutical Design, 16, 832–839.CrossRefGoogle Scholar
  6. 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.CrossRefGoogle Scholar
  7. 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.CrossRefGoogle Scholar
  8. 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
  9. 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.Google Scholar
  10. 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.CrossRefGoogle Scholar
  11. 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.CrossRefGoogle Scholar
  12. Christensen, M. (2014). Selenium and prostate cancer prevention: What next—if anything? Cancer prevention research, 7, 781–785. (Philadelphia, Pa.).CrossRefGoogle Scholar
  13. 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.CrossRefGoogle Scholar
  14. 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.CrossRefGoogle Scholar
  15. Costa, M., & Klein, C. B. (2006). Toxicity and carcinogenicity of chromium compounds in humans. Critical Reviews in Toxicology, 36, 155–163.CrossRefGoogle Scholar
  16. 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.CrossRefGoogle Scholar
  17. Czeczot, H., & Majewska, M. (2010). Cadmium—exposure and its effects health. Farmacja Polska, 66, 243–250. (in Polish).Google Scholar
  18. 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.CrossRefGoogle Scholar
  19. Dharia, S., & Parker, C. R, Jr. (2004). Adrenal androgens and aging. Seminars in Reproductive Medicine, 22, 361–368.CrossRefGoogle Scholar
  20. 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.CrossRefGoogle Scholar
  21. 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.CrossRefGoogle Scholar
  22. 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.CrossRefGoogle Scholar
  23. 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.CrossRefGoogle Scholar
  24. 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
  25. 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.CrossRefGoogle Scholar
  26. Goyer, R. A., Liu, J., & Waalkes, M. P. (2004). Cadmium and cancer of prostate and testis. BioMetals, 2004(17), 555–558.CrossRefGoogle Scholar
  27. 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.CrossRefGoogle Scholar
  28. 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.CrossRefGoogle Scholar
  29. 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.CrossRefGoogle Scholar
  30. 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.CrossRefGoogle Scholar
  31. 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.CrossRefGoogle Scholar
  32. 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.Google Scholar
  33. 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.CrossRefGoogle Scholar
  34. Killilea, D. W., & Maier, J. A. (2008). A connection between magnesium deficiency and aging: New insights from cellular studies. Magnesium Research, 21, 77–82.Google Scholar
  35. 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.CrossRefGoogle Scholar
  36. 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.CrossRefGoogle Scholar
  37. Koshla, S. (2004). Role of hormonal changes in the pathogenesis of osteoporosis in men. Calcified Tissue International, 75, 110–113.Google Scholar
  38. Kula, K., & Słowikowska-Hilczer, J. (2012). Late onset hypogonadism in men. Polish Journal of Endocrinology, 63, 15–19.Google Scholar
  39. 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.CrossRefGoogle Scholar
  40. 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.Google Scholar
  41. 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.CrossRefGoogle Scholar
  42. 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.CrossRefGoogle Scholar
  43. 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.CrossRefGoogle Scholar
  44. 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.CrossRefGoogle Scholar
  45. 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.CrossRefGoogle Scholar
  46. Martynowicz, H., Andrzejak, R., & Mędraś, M. (2005). The influence of lead on testis function). Medycyna Pracy, 56, 495–500.Google Scholar
  47. 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.CrossRefGoogle Scholar
  48. 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.CrossRefGoogle Scholar
  49. 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.CrossRefGoogle Scholar
  50. 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.CrossRefGoogle Scholar
  51. 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.CrossRefGoogle Scholar
  52. 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.CrossRefGoogle Scholar
  53. 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.CrossRefGoogle Scholar
  54. 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.Google Scholar
  55. 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.CrossRefGoogle Scholar
  56. Pant, N., Kumar, R., Murthy, R. C., & Srivastava, S. P. (2001). Male reproductive effect of arsenic in mice. BioMetals, 14, 113–117.CrossRefGoogle Scholar
  57. Pizent, A., Tariba, B., & Živković, T. (2012). Reproductive toxicity of metals in men. Archives of Industria Hygiene and Toxicology, 63, 35–46.CrossRefGoogle Scholar
  58. 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.CrossRefGoogle Scholar
  59. Prasad, A. S. (2008). Zinc in human health: Effect of zinc on immune cells. Molecular Medicine, 14, 353–357.CrossRefGoogle Scholar
  60. Rabijewski, M., & Zgliczyński, W. (2009). Pathogenesis, evaluation and treatment of hypogonadism in men. Polish Journal of Endocrinology, 3, 222–233.Google Scholar
  61. 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.CrossRefGoogle Scholar
  62. Rutkowski, K., Sowa, P., Rutkowska-Talipska, J., Kuryliszyn-Moskal, A., & Rutkowski, R. (2014). Dehydroepiandrosterone (DHEA): Hypes and Hopes. Drugs, 74, 1195–1207.CrossRefGoogle Scholar
  63. 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
  64. 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.CrossRefGoogle Scholar
  65. Shinohara, A., & Watanabe, H. (1996). Role of essential trace elements on sexual function and its disorder. Nihon Rinsho, 54, 155–161. (in Japanese).Google Scholar
  66. Siu, E. R., Mruk, D. D., Porto, C. S., & Cheng, C. J. (2009). Cadmium-induced testicular injury. Toxicology and Applied Pharmacology, 238, 240–249.CrossRefGoogle Scholar
  67. Snyder, P. (2001). Effects of age on testicular function and consequences of testosterone treatment. Journal of Clinical Endocrinology and Metabolism, 86, 2369–2372.Google Scholar
  68. Stojek, E., & Skoczyńska, A. (2003). The effect of lead on vascular endothelium. Medycyna Pracy, 54, 87–93.Google Scholar
  69. 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.CrossRefGoogle Scholar
  70. Swaminathan, R. (2003). Magnesium metabolism and its disorders. Clinical Biochemist Reviews, 24, 47–66.Google Scholar
  71. Symanski, E., & Hertz, P. I. (1995). Blood lead levels in relation to menopause smoking and pregnancy history. American Journal of Epidemiology, 141, 1047–1058.Google Scholar
  72. 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.CrossRefGoogle Scholar
  73. 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.CrossRefGoogle Scholar
  74. 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.CrossRefGoogle Scholar
  75. 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.CrossRefGoogle Scholar
  76. 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.CrossRefGoogle Scholar
  77. Wlazlo, N., Peters, W., & Bravenboer, B. (2012). Hypogonadism in a patient with mild hereditary haemochromatosis. Netherlands Journal of Medicine, 70, 318–320.Google Scholar
  78. 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.CrossRefGoogle Scholar
  79. World Medical Association. (2013). World Medical Association Declaration of Helsinki ethical principles for medical research involving human subjects. JAMA, 310, 2191–2194.CrossRefGoogle Scholar
  80. 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.CrossRefGoogle Scholar
  81. 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.CrossRefGoogle Scholar
  82. 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.Google Scholar
  83. 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.CrossRefGoogle Scholar

Copyright information

© European Union 2015

Authors and Affiliations

  • Iwona Rotter
    • 1
  • Danuta I. Kosik-Bogacka
    • 2
  • Barbara Dołęgowska
    • 3
  • Krzysztof Safranow
    • 4
  • Magdalena Kuczyńska
    • 5
  • Maria Laszczyńska
    • 6
  1. 1.Independent Laboratory of Medical RehabilitationPomeranian Medical UniversitySzczecinPoland
  2. 2.Department of Biology and Medical ParasitologyPomeranian Medical UniversitySzczecinPoland
  3. 3.Department of Microbiology and Immunology DiagnosticsPomeranian Medical UniversitySzczecinPoland
  4. 4.Department of Biochemistry and Medical ChemistryPomeranian Medical UniversitySzczecinPoland
  5. 5.Department of Human Sciences in MedicinePomeranian Medical UniversitySzczecinPoland
  6. 6.Department of Histology and Developmental BiologyPomeranian Medical UniversitySzczecinPoland

Personalised recommendations