Biological Trace Element Research

, Volume 140, Issue 3, pp 330–341

Testicular Histomorphometry and Ultrastructure of Rats Treated with Cadmium and Ginkgo biloba

  • Fabrícia de Souza Predes
  • Juliana Castro Monteiro
  • Sérgio Luis Pinto Matta
  • Márcia C. Garcia
  • Heidi Dolder


The aim of this study is to investigate the association of a single low dose of Cd and daily doses of Ginkgo biloba extract (GbE) on the testis and accessory glands of rats. The animals were treated with a single dose of 3 µmol/kg body weight of cadmium chloride (CdCl2) and/or 100 mg/kg body weight of GbE. The plasma testosterone levels; corporal, testicular, and accessory glands weight; gonadosomatic index, volumetric proportion; and absolute volume of testicular components did not change after the treatments. CdCl2 caused significant reduction in Leydig cells volume and altered Leydig cell morphology, as well as vacuolated Sertoli cells cytoplasm, irregular chromatin condensation of late spermatids, and modified acrosome formation. However, animals that received GbE did not show these alterations. The reversal of Cd-induced alterations by the extract is a strong indication that G. biloba is helpful in diminishing the effect of Cd toxicity.


Wistar rat Ginkgo biloba Cadmium Morphometry and ultrastructure 


  1. 1.
    Çavuşoğlu K, Yapar K, Yalçin E (2009) Royal Jelly (Honey Bee) Is a potential antioxidant against cadmium-induced genotoxicity and oxidative stress in albino mice. J Med Food 12:1286–1292PubMedCrossRefGoogle Scholar
  2. 2.
    Ren X, Zhou Y, Zhang J (2003) Metallothionein gene expression under different time in testicular Sertoli and spermatogenic cells of rats treated with cadmium. Reprod Toxicol 17:219–227PubMedCrossRefGoogle Scholar
  3. 3.
    Blanco A, Moyano R, Vivo J et al (2007) Quantitative changes in testicular structure in mice exposed to low doses of cadmium. Environ Toxicol Pharmacol 23:96–101CrossRefGoogle Scholar
  4. 4.
    Bizarro P, Acevedo S, Niño-Cabrera G et al (2003) Ultrastructural modifications in the mitochondrion of mouse Sertoli cells after inhalation of lead, cadmium or lead-cadmium mixture. Reprod Toxicol 17:561–566PubMedCrossRefGoogle Scholar
  5. 5.
    Wong C, Mruk DD, Lui W, Cheng CY (2004) Regulation of blood-testis barrier dynamics: an in vivo study. J Cell Science 117:783–798PubMedCrossRefGoogle Scholar
  6. 6.
    Hew KW, Heath GL, Jiwa AH, Welsh MJ (1993) Cadmium in vivo causes disruption of tight junction-associated microfilaments in rat Sertoli cells. Biol Reprod 49(4):840–849PubMedCrossRefGoogle Scholar
  7. 7.
    Wong C, Mruk DD, Siu MKY, Cheng CY (2005) Blood–testis barrier dynamics are regulated by α2-macroglobulin via the c-Jun N-terminal protein kinase pathway. Endocrinol 146:1893–1908CrossRefGoogle Scholar
  8. 8.
    Hew KW, Ericson WA, Welsh MJ (1993) A single low cadmium dose causes failure of spermiation in the rat. Toxicol Appl Pharmacol 122:15–21CrossRefGoogle Scholar
  9. 9.
    El-Demerdash FM, Yousef MI, Kedwany FS et al (2004) Cadmium-induced changes in lipid peroxidation, blood hematology, biochemical parameters and semen quality of male rats: protective role of vitamin E and β-carotene. Food Chem Toxicol 42:1563–1571PubMedCrossRefGoogle Scholar
  10. 10.
    Gupta RS, Kim J, Gomes C et al (2004) Effect of ascorbic acid supplementation on testicular steroidogenesis and germ cell death in cadmium-treated male rats. Mol Cell Endocrinol 221:57–66PubMedCrossRefGoogle Scholar
  11. 11.
    Asagba SO, Adaikpoh MA, Kadiri H et al (2007) Influence of aqueous extract of Hibiscus sabdariffa L. petal on cadmium toxicity in rats. Biol Trace Elem Res 115:47–57PubMedCrossRefGoogle Scholar
  12. 12.
    Jahangir T, Khan TH, Prasad L et al (2005) Pluchea lanceolata attenuates cadmium chloride induced oxidative stress and genotoxicity in Swiss albino mice. J Pharm Pharmacol 57:1199–1204PubMedCrossRefGoogle Scholar
  13. 13.
    Ola-Mudathir KF, Suru SM, Fafunso MA et al (2008) Protective roles of onion and garlic extracts on cadmium-induced changes in sperm characteristics and testicular oxidative damage in rats. Food Chem Toxicol 46:3604–3611PubMedCrossRefGoogle Scholar
  14. 14.
    El-Shahat AE, Gabr A, Meki A et al (2009) Altered testicular morphology and oxidative stress induced by cadmium in experimental rats and protective effect of simultaneous green tea extract. Int J Morphol 27:757–764CrossRefGoogle Scholar
  15. 15.
    Bridi R, Crossetti VM, Henriques AT (2001) The antioxidant activity of standardized extract of Ginkgo biloba (Egb 761) in rats. Phyto Res 15:449–451CrossRefGoogle Scholar
  16. 16.
    He S, Luo J, Wang YP et al (2006) Effects of extract from Ginkgo biloba on tetrachloride-induced liver injury in rats. World J Gastroenterol 12:3924–3928PubMedGoogle Scholar
  17. 17.
    Huang S, Luo Y, Wang L et al (2005) Effect of Ginkgo biloba extract on livers in aged rats. World J Gastroenterol 11:132–135PubMedGoogle Scholar
  18. 18.
    Wang W, Zhong X, Ma A et al (2008) Effects of Ginkgo biloba on testicle injury induced by diethylstilbestrol in mice. Am J Chin Med 36:1135–1144PubMedCrossRefGoogle Scholar
  19. 19.
    Şener G, Sehirlia Ö, Tozanb A et al (2007) Ginkgo biloba extract protects against mercury (II)-induced oxidative tissue damage in rats. Food Chem Toxicol 45:543–550PubMedCrossRefGoogle Scholar
  20. 20.
    Yeh K, Pub H, Kaphle K et al (2008) Ginkgo biloba extract enhances male copulatory behavior and reduces serum prolactin levels in rats. Horm Behav 53:225–231PubMedCrossRefGoogle Scholar
  21. 21.
    Al-yahya AA, Al-majed A, Al-bekairi AM et al (2006) Studies on the reproductive, cytological and biochemical toxicity of Ginkgo biloba in Swiss albino mice. J Ethnopharmacol 107:222–228PubMedCrossRefGoogle Scholar
  22. 22.
    Yano C L (2001) Aspectos estruturais e ultra-estruturais de testículos de ratos submetidos ao tratamento com cádmio e paracetamol. Campinas, SP: State University of Campinas. ThesisGoogle Scholar
  23. 23.
    Russell LD, Ettlin RA, Hikim APS et al (1990) Histological and histopathological evaluation of the testis, 1st edn. Cache River Press, ClearwaterGoogle Scholar
  24. 24.
    Mori H, Christensen K (1980) Morphometric analysis of Leydig cells in the normal rat testis. J Cell Biol 84:340–354PubMedCrossRefGoogle Scholar
  25. 25.
    França LR, Godinho CL (2003) Testis morphometry, seminiferous epithelium cycle length, and daily sperm production in domestic cats (Felis catus). Biol Reprod 68:1556–1561Google Scholar
  26. 26.
    Cabral FHC (1996) Alterações morfológicas testiculares provocadas pelo cádmio, paracetamol e cádmio associado ao paracetamol em ratos. (Thesis)Google Scholar
  27. 27.
    Beek TAV, Morazzoni P, Bombardelii E, Peterlongo F (1998) Ginkgo biloba L. Fitoterapia 69:195–244Google Scholar
  28. 28.
    Biswas NM, Gupta RS, Chattopadhyay A et al (2001) Effect of atenolol on cadmium-induced testicular toxicity in male rats. Reprod Toxicol 15:699–704PubMedCrossRefGoogle Scholar
  29. 29.
    Laskey JW, Rehnberg GL, Laws SC et al (1984) Reproductive effects of low acute doses of cadmium chloride in adult male rats. Toxicol Appl Pharmacol 154:256–263Google Scholar
  30. 30.
    Gupta RS, Sharma R, Chaudhary R et al (2003) Effect of textile waste water on the spermatogenesis of male albino rats. J Appl Toxicol 23:171–175PubMedCrossRefGoogle Scholar
  31. 31.
    Zeng X, Jin T, Zhou Y (2003) Changes of serum sex hormone levels and MT mRNA expression in rats orally exposed to cadmium. Toxicol 186:109–118CrossRefGoogle Scholar
  32. 32.
    Castro AP, Mello FB, Mello JB (2005) Avaliação toxicológica do Ginkgo biloba sobre a fertilidade e reprodução de ratos Wistar. Acta Scient Veterin 33:265–269Google Scholar
  33. 33.
    Creasy DM (2001) Pathogenesis of male reproductive toxicity. Toxicol Pathol 29:64–76PubMedCrossRefGoogle Scholar
  34. 34.
    Blottner S, Frölich K, Roelants H et al (1999) Influence of environmental cadmium on testicular proliferation in roe deer. Reprod Toxicol 13:261–267PubMedCrossRefGoogle Scholar
  35. 35.
    Russell LD, França LR (1995) Building a testis. Tissue Cell 2:129–147CrossRefGoogle Scholar
  36. 36.
    Kim I, Yang H (1999) Morphometric study of the testicular interstitium of the rat during postnatal development. Korean J Anat 32:849–858Google Scholar
  37. 37.
    Blanco A, Moyano MR, Molina AM et al (2009) Quantitative study of Leydig cell populations in mice exposed to low doses of cadmium. Bull Environ Contam Toxicol 82:756–760PubMedCrossRefGoogle Scholar
  38. 38.
    Yang J, Arnush M, Chenc Q (2003) Cadmium-induced damage to primary cultures of rat Leydig cells. Reprod Toxicol 17:553–560PubMedCrossRefGoogle Scholar
  39. 39.
    Keeney DS, Ewing LL (1990) Effects of hypophysectomy and alterations in spermatogenic function on Leydig cell volume, number, and proliferation in adult rats. J Androl 11:367–378PubMedGoogle Scholar
  40. 40.
    Ichihara I, Kawamura H, Nakano T et al (2001) Ultrastructural, morphometric, and hormonal analysis of the effects of testosterone treatment on Leydig cells and others interstitial cells in young adults rats. Ann Anat 183:413–426PubMedCrossRefGoogle Scholar
  41. 41.
    Queiroz EK, Waissmann W (2006) Occupational exposure and effects on the male reproductive system. Cad Saúde Públ 22:485–493CrossRefGoogle Scholar
  42. 42.
    Fiorini C, Tilloy-Ellul A, Chevalier S et al (2004) Sertoli cell junctional proteins as early targets for different classes of reproductive toxicants. Reprod Toxicol 18:413–421PubMedCrossRefGoogle Scholar
  43. 43.
    Morales E, Horn R, Pastor LM et al (2004) Involution of seminiferous tubules in aged hamsters: an ultrastructural, immunohistochemical and quantitative morphologic study. Histol Histopathol 19:445–455PubMedGoogle Scholar
  44. 44.
    Chung NPY, Cheng CY (2001) Is cadmium chloride-induced inter-Sertoli tight junction permeability barrier disruption a suitable in vitro model to study the events of junction disassembly during spermatogenesis in the rat testis? 142:1878–1888Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Fabrícia de Souza Predes
    • 1
    • 3
  • Juliana Castro Monteiro
    • 1
  • Sérgio Luis Pinto Matta
    • 2
  • Márcia C. Garcia
    • 1
  • Heidi Dolder
    • 1
  1. 1.Rua Charles Darwin, s/n, Department of Anatomy, Cellular Biology, Physiology and BiophysicsState University of CampinasCampinasBrazil
  2. 2.Department of General BiologyFederal University of ViçosaMinas GeraisBrazil
  3. 3.Departamento de Anatomia, Biologia Celular e Fisiologia e BiofísicaInstituto de Biologia, Universidade Estadual de Campinas-UNICAMPSão PauloBrazil

Personalised recommendations