Skip to main content
SpringerLink
Log in

Pycnogenol® prevents hexavalent chromium-induced spermatotoxicity in rats

  • Original Paper
  • Published:
Molecular & Cellular Toxicology Aims and scope Submit manuscript

Abstract

This study evaluated the ability of Pycnogenol ® (PYC) as an antioxidant to protect against hexavalent chromium [Cr(VI)]-induced spermatotoxicity and oxidative damage in rats. Twenty-four male rats were randomly assigned to four experimental groups: vehicle control, Cr(VI), Cr(VI)&PYC 10, and Cr(VI) &PYC 20 groups. Spermatotoxicity was assessed by reproductive organ weights, sperm analysis, and oxidative damage in testes and epididymides. The 6-day repeated oral dose of Cr(VI) produced a significant decrease in the sperm head count and sperm motility. Increased malondialdehyde (MDA) concentration and reduced glutathione (GSH) content, and decreased catalase (CAT), superoxide dismutase (SOD) and glutathione-S-transferase (GST) activities were also observed in both testicular and epididymal tissues. On the contrary, concomitant administration of PYC significantly attenuated Cr(VI)-induced spermatotoxicity, as evidenced by the elevation of sperm head count and sperm motility in a dose-dependent manner. PYC treatment also reduced MDA concentration and increased GSH levels and CAT, SOD, and GST activities in testicular and epididymal tissues, indicating that concomitant administration with PYC efficiently prevented the Cr (VI)-induced oxidative damage in rats. These results indicate that PYC has a protective effect on spermatotoxicity induced by Cr(VI) in rats, and that the protective effects of PYC may be due to both the inhibition of lipid peroxidation and the increase in antioxidant activity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Sharpe, R. M. Declining sperm counts in men — is there an endocrine cause? J Endocrinol 136:357–360 (1993).

    Article  PubMed  CAS  Google Scholar 

  2. Alexander, B. H. et al. Lung cancer in chromate-exposed aerospace workers. J Occup Environ Med 38: 1253–1258 (1996).

    Article  PubMed  CAS  Google Scholar 

  3. Saryan, L. A. & Reedy, M. Chromium determinations in a case of chromic acid ingestion. J Anal Toxicol 12: 162–164 (1988).

    PubMed  CAS  Google Scholar 

  4. Von Burg, R. & Liu, D. Chromium and hexavalent chromium. J Appl Toxicol 13:225–230 (1993).

    Article  Google Scholar 

  5. Elbetieha, A. & Al-Hamood, M. H. Long-term exposure of male and female mice to trivalent and hexavalent chromium compounds: effect on fertility. Toxicology 116:39–47 (1997).

    Article  PubMed  CAS  Google Scholar 

  6. Bataineh, H., Al-Hamood, M. H., Elbetieha, A. & Bani Hani, I. Effect of long-term ingestion of chromium compounds on aggression, sex behavior and fertility in adult male rat. Drug Chem Toxicol 20:133–149 (1997).

    Article  PubMed  CAS  Google Scholar 

  7. Ernst, E. Testicular toxicity following short-term exposure to tri- and hexavalent chromium: an experimental study in the rat. Toxicol Lett 51:269–275 (1990).

    Article  PubMed  CAS  Google Scholar 

  8. Li, H. et al. Effect of Cr (VI) exposure on sperm quality: human and animal studies. Ann Occup Hyg 45:505–511 (2001).

    PubMed  CAS  Google Scholar 

  9. Katz, S. A. & Salem, H. The toxicology of chromium with respect to its chemical speciation: a review. J Appl Toxicol 13:217–224 (1993).

    Article  PubMed  CAS  Google Scholar 

  10. Bagchi, D. et al. Induction of oxidative stress by chronic administration of sodium dichromate [chromium VI] and cadmium chloride [cadmium II] to rats. Free Radical Biol Med 22:471–478 (1997).

    Article  CAS  Google Scholar 

  11. Bagchi, D., Bagchi, M. & Stohs, S. J. Chromium (VI)-induced oxidative stress, apoptotic cell death and modulation of p53 tumor suppressor gene. Mol Cell Biochem 222:149–158 (2001).

    Article  PubMed  CAS  Google Scholar 

  12. Bagchi, D. et al. Cytotoxicity and oxidative mechanisms of different forms of chromium. Toxicology 180: 5–22 (2002).

    Article  PubMed  CAS  Google Scholar 

  13. Boşgelmez I. I., Söylemezoğlu, T. & Güvendik, G. The protective and antidotal effects of taurine on hexavalent chromium-induced oxidative stress in mice liver tissue. Biol Trace Elem Res 125:46–58 (2008).

    Article  PubMed  Google Scholar 

  14. Soudani, N. et al. Protective effects of selenium (Se) on chromium (VI) induced nephrotoxicity in adult rats. Ecotoxicol Environ Saf 73:671–678 (2010).

    Article  PubMed  CAS  Google Scholar 

  15. Das, K. K., Dhundasi, S. A. & Das, S. N. Hexavalent chromium and its effect on health: possible protective role of garlic (Allium sativum Linn). J Basic Clin Physiol Pharmacol 22:3–10 (2011).

    Article  PubMed  Google Scholar 

  16. Packer, L., Rimbach, G. & Virgili, F. Antioxidant activity and biologic properties of a procyanidin-rich extract from pine (Pinus maritima) bark, pycnogenol. Free Radical Bio Med 27:704–724 (1999).

    Article  CAS  Google Scholar 

  17. Rohdewald, P. A review of the French maritime pine bark extract (Pycnogenol), a herbal medication with a diverse clinical pharmacology. Int J Clin Pharm Ther 40:158–168 (2002).

    CAS  Google Scholar 

  18. Elstner, E. F. & Kleber, E. Radical Scavenger properties of leucocyanidine. In: Das, N. P. (Ed), Flavonoids in biology and medicine IIIcurrent issues in flavonoids research. Natl Univ of Singapore Press, Singapore, pp. 227–235 (1990).

    Google Scholar 

  19. Bors, W. & Michel, C. Chemistry of the antioxidant effect of polyphenols. Ann NY Acad Sci 957:57–69 (2002).

    Article  PubMed  CAS  Google Scholar 

  20. Guo, Q., Zhao, B. & Packer, L. Electron spin resonance study of free radicals formed from a procyanidin-rich pine (Pinus maritima) bark extract, pycnogenol. Free Radical Bio Med 27:1308–1312 (1999).

    Article  CAS  Google Scholar 

  21. Yang, Y. S. et al. Protective effects of Pycnogenol® on carbon tetrachloride-induced hepatotoxicity in Sprague-Dawley rats. Food Chem Toxicol 46:380–387 (2008).

    Article  PubMed  CAS  Google Scholar 

  22. Hsieh, Y. Y., Chang, C. C. & Lin, C. S. Seminal malondialdehyde concentration but not glutathione peroxidase activity is negatively correlated with seminal concentration and motility. Int J Biol Sci 2:23–29 (2006).

    Article  PubMed  CAS  Google Scholar 

  23. Thiele, J. J. et al. Ascorbic acid and urate in human seminal plasma: determination and interrelationships with chemiluminescence in washed semen. Hum Reprod 10:110–115 (1995).

    Article  PubMed  CAS  Google Scholar 

  24. Aitken, R. J., Buckingham, D. & Harkiss, D. Use of a xanthine oxidase free radical generating system to investigate the cytotoxic effects of reactive oxygen species on human spermatozoa. J Reprod Fertil 97:441–450 (1993).

    Article  PubMed  CAS  Google Scholar 

  25. Alvarez, J. G. & Storey, B. T. Differential incorporation of fatty acids into and peroxidative loss of fatty acids from phospholipids of human spermatozoa. Mol Reprod Dev 42:334–346 (1995).

    Article  PubMed  CAS  Google Scholar 

  26. Sivonová, M. et al. The effect of Pycnogenol on the erythrocyte membrane fluidity. Gen Physiol Biophys 23:39–51 (2004).

    PubMed  Google Scholar 

  27. Zi, S. X. et al. Oligomeric proanthocyanidins from grape seeds effectively inhibit ultraviolet-induced melanogenesis of human melanocytes in vitro. Int J Mol Med 23:197–204 (2009).

    PubMed  CAS  Google Scholar 

  28. Sugiyama, M. Role of physiological antioxidants in chromium (VI)-induced cellular injury. Free Radical Biol Med 12:397–407 (1992).

    Article  CAS  Google Scholar 

  29. Ernst, E. & Bonde, J. P. Sex hormones and epididymal sperm parameters in rats following sub-chronic treatment with hexavalent chromium. Hum Exp Toxicol 11:255–258 (1992).

    Article  PubMed  CAS  Google Scholar 

  30. Vaca, C. E., Wilhelm, J. & Harms-Ringdahl, M. Interaction of lipid peroxidation products with DNA. A review. Mutat Res 195:137–149 (1998).

    Google Scholar 

  31. Hockenbery, D. M. et al. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 75:241–251 (1993).

    Article  PubMed  CAS  Google Scholar 

  32. Chance, B., Sies, H. & Boveris, A. Hydroperoxide metabolism in mammalian organs. Physiol Rev 59:527–605 (1979).

    PubMed  CAS  Google Scholar 

  33. Geetha, S. et al. Evaluation of antioxidant activity of leaf extract of Seabuckthorn (Hippophae rhamnoides L.) on chromium (VI) induced oxidative stress in albino rats. J Ethnopharmacol 87:247–251 (2003).

    Article  PubMed  CAS  Google Scholar 

  34. Wang, X. F. et al. Oral administration of Cr (VI) induced oxidative stress, DNA damage and apoptotic cell death in mice. Toxicology 228:16–23 (2006).

    Article  PubMed  CAS  Google Scholar 

  35. Chandra, A. K., Chatterjee, A., Ghosh, R. & Sarkar, M. Effect of curcumin on chromium-induced oxidative damage in male reproductive system. Environ Toxicol Pharmacol 24:160–166 (2007).

    Article  PubMed  CAS  Google Scholar 

  36. Akunna, G. G. et al. Ameliorative effect of Moringa oleifera (drumstick) leaf extracts on chromium-induced testicular toxicity in rat testes. World J Life Sci Med Res 2:20 (2012).

    Google Scholar 

  37. Valko, M. et al. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39:44–84 (2007).

    Article  PubMed  CAS  Google Scholar 

  38. Acharya, U. R., Mishra, M., Tripathy, R. R. & Mishra, I. Testicular dysfunction and antioxidative defense system of Swiss mice after chromic acid exposure. Reprod Toxicol 22:87–91 (2002).

    Article  Google Scholar 

  39. Moini, H., Guo, Q. & Packer, L. Enzyme inhibition and protein-binding action of the procyanidin-rich french maritime pine bark extract, pycnogenol: effect on xanthine oxidase. J Agric Food Chem 48:5630–5639 (2000).

    Article  PubMed  CAS  Google Scholar 

  40. Roseff, S. J. Improvement in sperm quality and function with French maritime pine tree bark extract. J Reprod Med 47:821–824 (2002).

    PubMed  Google Scholar 

  41. Stanislavov, R., Nikolova, V. & Rohdewald, P. Improvement of seminal parameters with Prelox®: a randomized, double-blind, placebo-controlled, cross-over trial. Phytother Res 23:297–302 (2009).

    Article  PubMed  CAS  Google Scholar 

  42. Kim, J. C., Kim, K. H. & Chung, M. K. Testicular cytotoxicity of DA-125, a new anthracycline anticancer agent, in rats. Reprod Toxicol 13:391–397 (1999).

    Article  PubMed  CAS  Google Scholar 

  43. Chung, M. K., Han, S. S. & Kim, J. C. Evaluation of the toxic potentials of a new camptothecin anticancer agent CKD-602 on fertility and early embryonic development in rats. Regul Toxicol Pharmacol 45:273–281 (2006).

    Article  PubMed  CAS  Google Scholar 

  44. Berton, T. R. et al. The effect of vitamin E acetate on ultraviolet-induced mouse skin carcinogenesis. Mol Carcinogen 23:175–184 (1998).

    Article  CAS  Google Scholar 

  45. Moron, M. S., Depierre, J. W. & Mannervik, B. Levels of glutathione, glutathione reductase and glutathione S-transferase activities in rat lung and liver. Biochim Biophys Acta 582:67–78 (1979).

    Article  PubMed  CAS  Google Scholar 

  46. Aebi, H. Catalase in vitro. In: Packer, L. (Ed.), Methods in Enzymology, vol. 105. Academic Press, San Diego, pp. 121–126 (1984).

    Google Scholar 

  47. McCord, J. M. & Fridovich, I. Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244:6049–6055 (1969).

    PubMed  CAS  Google Scholar 

  48. Habig, W. H. et al. 2-Propylthiouracil does not replace glutathione for the glutathione transferases. J Biol Chem 259:7409–7410 (1984).

    PubMed  CAS  Google Scholar 

  49. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254 (1976).

    Article  PubMed  CAS  Google Scholar 

  50. Dunnett, C. W. New tables for multiple comparisons with a control. Biometrics 20:482–491 (1964).

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. College of Veterinary Medicine, Chonnam National University, Gwangju, 500-757, Korea

    Sung-Hwan Kim, In-Chul Lee, Hyung-Seon Baek, Changjong Moon, Seong-Soo Kang, Chun-Sik Bae, Sung-Ho Kim, Dong-Ho Shin & Jong-Choon Kim

Authors
  1. Sung-Hwan Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. In-Chul Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hyung-Seon Baek
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Changjong Moon
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Seong-Soo Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chun-Sik Bae
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sung-Ho Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Dong-Ho Shin
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jong-Choon Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jong-Choon Kim.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kim, SH., Lee, IC., Baek, HS. et al. Pycnogenol® prevents hexavalent chromium-induced spermatotoxicity in rats. Mol. Cell. Toxicol. 8, 249–256 (2012). https://doi.org/10.1007/s13273-012-0030-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13273-012-0030-8

Keywords

Search

Navigation