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High Levels of Cadmium and Lead in Seminal Fluid and Blood of Smoking Men are Associated with High Oxidative Stress and Damage in Infertile Subjects

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Abstract

We measured the levels of malondialdehyde (MDA), protein carbonyls, glutathione S-transferase (GST) and reducte glutathione (GSH) in seminal plasma and spermatozoa from 95 subjects including 50 infertile patients to evaluate the association between oxidative stress and damage and the components of the anti-oxidant defenses in seminal plasma and spermatozoa of infertile subjects and concentrations of cadmium (Cd) and lead (Pb) in the blood and seminal plasma because of tobacco smoke exposure. The reactive oxygen species (ROS) in spermatozoa were also evaluated by luminol (5-amino-2,3-dihydro-1,4-phthalazinedione)-enhanced chemiluminescence assay. The sperm count, motility, and morphology in the smokers infertile group were found to be lower than those in the fertile male group and nonsmokers infertile group (p < 0.001). Concentrations of Cd, Pb, MDA, protein carbonyls, and ROS levels in the smokers infertile group were significantly higher than those in the fertile male and nonsmokers infertile male groups (p < 0.001). However, GSH levels and GST activities were decreased in the smokers infertile male group than those in the fertile male and nonsmokers infertile male groups (p < 0.001). The results indicate that smoking could affect semen quality and oxidative lipid and protein damage in human spermatozoa. From Pearson correlation analysis, positive correlations were demonstrated between the seminal plasma Cd and seminal plasma protein carbonyls and between seminal plasma Pb and spermatozoa ROS levels in smokers of the subfertile group, while there was a significant positive correlation between blood Cd and ROS levels in smokers of the fertile group. There was also a significant negative correlation of the Cd level of the blood and GSH levels of the sperm and seminal plasma. These findings suggest that cigarette smoking enhances the levels of Cd and Pb in seminal plasma and blood and the extent of oxidative damage associated with a decrease in components of the anti-oxidant defenses in the sperm of infertile males.

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References

  1. Gopalkrishnan K (1998) Characteristics of semen parameters in a selected population of Indian men over a period of ten years. Curr Sci 75:939–942

    Google Scholar 

  2. Stohs SJ, Baggihi D (1995) Oxidative mechanisms in the toxicity of metal ions. Free Radic Med 18:321–336

    Article  CAS  Google Scholar 

  3. Pruski AM, Dixon DR (2002) Effects of cadmium on nuclear integrity and DNA repair efficiency in the gill cells of Mytilus edulis L. Aquat Toxicol 57:127–137

    Article  PubMed  CAS  Google Scholar 

  4. Liu J, Shen HM, Ong CN (2001) Role of intracellular thio depletion, mitochondrial dysfuction and reactive oxygen species in Salvia miltiorrhiza-induced apoptosis in human hepatoma HepG2 cells. Life Sci 69:1833–1850

    Article  PubMed  CAS  Google Scholar 

  5. Halliwell B, Gutteridge JMC (1999) Free radicals in biology and medicine. Oxford University Press, Oxford, pp 584–591

    Google Scholar 

  6. Frei B, Forte TM, Ames BN, Cross CE (1991) Gaz phase oxidants of cigarette smoke induce lipid peroxidation and changes in lipoprotein properties in human blood plasma. Protective effect of ascorbic acid. Biochem J 277:133–138

    PubMed  CAS  Google Scholar 

  7. Chiba M, Masironi R (1992) Toxic and trace elements in tobacco and tobacco smoke. Bull World Health Organ 70:269–275

    PubMed  CAS  Google Scholar 

  8. Saldivar L, Luna M, Reyes E, Soto R, Fortoul TI (1991) Cadmium determination in Mexican-produced tobacco. Environ Res 55:91–96

    Article  PubMed  CAS  Google Scholar 

  9. Elinder CG, Kjellstrom T, Hogstedt C (1985) Cancer mortality of cadmium workers. Br J Ind Med 42:651–655

    PubMed  CAS  Google Scholar 

  10. Elliott P, Arnold R, Cockings S, Eaton N, Jarup L, Jones J, Quinn M, Rosato M, Thornton I, Toledano M, Tristan E, Wakefield J (2000) Risk of mortality, cancer incidence, and stroke in a population potentially exposed to cadmium. Occup Environ Med 57:94–97

    Article  PubMed  CAS  Google Scholar 

  11. Muntner P, He J, Vupputuri S, Coresh J, Batuman V (2003) Blood lead and chronic kidney disease in the general United States population: results from NHANES III. Kidney Int 63:1044–1050

    Article  PubMed  Google Scholar 

  12. Nash D, Magder L, Lustberg M, Sherwin RW, Rubin RJ, Kaufmann RB, Silbergerd EK (2003) Blood lead, blood pressure, and hypertension in perimenopausal and postmenopausal women. JAMA 289:1523–1532

    Article  PubMed  CAS  Google Scholar 

  13. Navas-Acien A, Selvin E, Sharrett AR, Calderon-Aranda E, Silbergeld E, Guallar E (2004) Lead cadmium, smoking, and increased risk of peripheral arterial disease. Circulation 109:3196–3201

    Article  PubMed  CAS  Google Scholar 

  14. Schrag SD, Dixon RI (1995) Occupational exposures associated with male reproductive dysfunction. Annu Rev Pharmacol Toxicol 25:567–592

    Article  Google Scholar 

  15. Bench G, Corzett MH, Martinelli R, Balhorn R (1999) Cadmium concentrations in the testis, sperm, and spermatids of mice subjected to long-term cadmium chloride exposure. Cytometry 35:30–36

    Article  PubMed  CAS  Google Scholar 

  16. Gennart JP, Buchet JP, Roels H, Ghyselen P, Ceulemans E, Lauwerys R (1992) Fertility of male workers exposed to cadmium, lead, or manganese. Am J Epidemiol 135:1208–1219

    PubMed  CAS  Google Scholar 

  17. Xu C, Johnson JE, Singh PK, Jones MM, Yan H, Carter CE (1996) In vivo studies of cadmium-induced apoptosis in testicular tissue of the rat and its modulation by a chelating agent. Toxicology 107:1–8

    Article  PubMed  CAS  Google Scholar 

  18. Hew KW, Ericson WA, Welsh MJ (1993) A single low cadmium dose causes failure of spermiation in the rat. Toxicol Appl Pharmacol 121:15–21

    Article  PubMed  CAS  Google Scholar 

  19. Yang JM, Arnush M, Chen QY, Wu XD, Pang B, Jiang XZ (2003) Cadmium-induced damage to primary cultures of rat Leydig cells. Reprod Toxicol 142:553–560

    Article  CAS  Google Scholar 

  20. Saarenen M, Kantola M, Saarikoski S, Vanha-Pettula T (1989) Human seminal plasma cadmium: comparison with fertility and smoking habits. Andrologia 21:140–145

    Article  Google Scholar 

  21. Plechaty MM, Nolland B, Sunderman FW (1977) Lead concentrations in semen of healthy men without occupational exposure to lead. Ann Clin Lab Sci 7:515–518

    PubMed  CAS  Google Scholar 

  22. Xu B, Chia ES, Tsakok FM, Ong CN (1993) Trace elements in blood and seminal plasma and their relationship to sperm quality. Reprod Toxicol 7:613–618

    Article  PubMed  CAS  Google Scholar 

  23. World Health Organization (WHO) (1999) Laboratory manual for the examination of human semen and semen–cervical mucus interaction, 4th edn. Cambridge University Press, New York

    Google Scholar 

  24. Brys M, Nawrocka AD, Miekos E, Zyudek C, Fonksizki M, Barecki A, Krajewska WM (1997) Zinc and cadmium analyses in human prostate neoplasm. Biol Trace Elem Res 59:145–152

    PubMed  CAS  Google Scholar 

  25. Aydemir B, Kiziler AR, Onaran I, Alici B, Ozkara H, Akyolcu MC (2006) Impact of Cu and Fe concentrations on oxidative damage in male infertility. Biol Trace Elem Res 112:193–203

    Article  PubMed  CAS  Google Scholar 

  26. Saleh RA, Agarwal A (2002) Oxidative stress and male infertility: from research bench to clinical practice. J Androl 23:737–751

    PubMed  CAS  Google Scholar 

  27. Aitken RJ, Irvine DS, Wu FC (1991) Prospective analysis of sperm-oocyte fusion and reactive oxygen species generation as criteria for the diagnosis of infertility. Am J Obstet Gynecol 164:542–551

    PubMed  CAS  Google Scholar 

  28. Buege JA, Aust STD (1978) Microsomal lipid peroxidation. Methods Enzymol 52:302–310

    PubMed  CAS  Google Scholar 

  29. Anderson ME (1985) Determination of glutathione and glutathione disulfide in biological samples. Methods Enzymol 113:548–555

    PubMed  CAS  Google Scholar 

  30. Habig WH, Pabst MJ, Jakoby WB (1974) The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139

    PubMed  CAS  Google Scholar 

  31. Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz AG, Ahn BW, Shaltiel S, Stadtman ER (1990) Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 186:464–473

    Article  PubMed  CAS  Google Scholar 

  32. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin Phenol Reagent. J Biol Chem 193:269–275

    Google Scholar 

  33. Agency for Toxic Substances and Disease Registry (1993) U.S. and public health services, Toxicological profile of lead. US Department of Health and Human Services, Public Health Services, Atlanta, GA

    Google Scholar 

  34. Agency for Toxic Substances and Disease Registry (1993) U.S. and public health service, Toxicological profile of cadmium. US Department of Health and Human Services, Public Health Services, Atlanta, GA

    Google Scholar 

  35. Chia SE, Ong CN, Lee ST, Tsakok FM (1992) Blood concentration of lead, cadmium, mercury, zinc and copper and human semen parameters. Arch Androl 29:177–183

    PubMed  CAS  Google Scholar 

  36. Alabi NS, Whanger PD, Wu AS (1985) Interactive effect of organic and inorganic selenium with cadmium and mercury on spermatozoa oxygen consumption and motility in vitro. Biol Reprod 33:911–919

    Article  PubMed  CAS  Google Scholar 

  37. Murthy RC, Gupta SK, Saxena DK (1995) Nuclear alterations during acrosomal cap formation in spermatids of lead treated rats. Reprod Toxicol 9:483–489

    Article  PubMed  CAS  Google Scholar 

  38. Keck C, Bramkamp G, Behre HM, Muller C, Jockenhovel F, Nieschlag E (1995) Lack of correlation between cadmium in seminal plasma and fertility status of nonexposed individuals and two cadmium-exposed patients. Reprod Toxicol 9:35–40

    Article  PubMed  CAS  Google Scholar 

  39. Xu DX, Shen HM, Zhu QX, Chua L, Wang QN, Chia SE, Ong CN (2003) The associations among semen quality, oxidative DNA damage in human spermatozoa and concentrations of cadmium, lead and selenium in seminal plasma. Mutat Res 534:155–163

    PubMed  CAS  Google Scholar 

  40. Alkan I, Simsek F, Haklar G, Kervancioglu E, Ozveri H, Yalcin S, Akdas A (1997) Reactive oxygen species production by the spermatozoa of patients with idiopathic infertility: relationship to seminal plasma antioxidants. J Urol 157:140–143

    Article  PubMed  CAS  Google Scholar 

  41. Fraga CG, Motchnik PA, Wyrobek AJ, Rempel DM, Ames BN (1996) Smoking and low antioxidant levels increase oxidative damage to sperm DNA. Mutat Res 351:199–203

    PubMed  Google Scholar 

  42. Garg N, Singh R, Dixit J, Jain A, Tewari V (2006) Levels of lipid peroxides and antioxidants in smokers and nonsmokers. J Periodont Res 41:405–410

    Article  PubMed  CAS  Google Scholar 

  43. Mukhtar H, Lee PI, Bend R (1978) Glutathione S-transferase activities in rat and Mouse sperm and human semen. Biochem Biophys Res Commun 83:1093–1098

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by The Research Fund of İstanbul University (Project number T-1171/18062001). This study was also presented in the 6th International Conference of the Balkan Physical Union, 22–26 August 2006, Istanbul, Turkey.

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Authors and Affiliations

  1. Department of Biophysics, Cerrahpaşa Faculty of Medicine, Istanbul University, 34098, Istanbul, Turkey

    Ali Riza Kiziler, Birsen Aydemir & Mehmet Can Akyolcu

  2. Department of Medical Biology, Cerrahpaşa Faculty of Medicine, Istanbul University, 34098, Istanbul, Turkey

    Ilhan Onaran

  3. Department of Urology, Cerrahpaşa Faculty of Medicine, Istanbul University, 34098, Istanbul, Turkey

    Bulent Alici & Hamdi Ozkara

  4. Department of Biophysics, Medical Faculty, Trakya University, 22030, Edirne, Turkey

    Tevfik Gulyasar

  5. Ramazanoglu Mah Kaynarca Cad, No 76 Botas Lojmanları Pendik, 34892, Istanbul, Turkey

    Ali Riza Kiziler

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  1. Ali Riza Kiziler
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  2. Birsen Aydemir
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  3. Ilhan Onaran
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  4. Bulent Alici
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  7. Mehmet Can Akyolcu
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Correspondence to Ali Riza Kiziler.

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Kiziler, A.R., Aydemir, B., Onaran, I. et al. High Levels of Cadmium and Lead in Seminal Fluid and Blood of Smoking Men are Associated with High Oxidative Stress and Damage in Infertile Subjects. Biol Trace Elem Res 120, 82–91 (2007). https://doi.org/10.1007/s12011-007-8020-8

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  • DOI: https://doi.org/10.1007/s12011-007-8020-8

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