Biological Trace Element Research

, Volume 173, Issue 2, pp 362–371 | Cite as

Effects of Arctium lappa on Cadmium-Induced Damage to the Testis and Epididymis of Adult Wistar Rats

  • Fabricia de Souza PredesEmail author
  • M. A. S. Diamante
  • M. A. Foglio
  • H. Dolder


The protective role of Arctium lappa (AL) on the testes of rats acutely exposed to cadmium (Cd) was tested. The rats were randomly divided into a control group (C-group) and three major experimental groups, which were further subdivided into minor groups (n = 6) according to the experimental period (7 or 56 days). The C-group was subdivided into C-7 and C-56 [receiving a single saline solution, intraperitoneal (i.p.), on the first day]; the AL-group, AL-7, and AL-56, received AL extract (300 mg/kg/daily); the Cd group, Cd-7 and Cd-56, received a single i.p. dose of CdCl2 (1.2 mg/kg body weight (BW)) on the first day; the CdAL group, CdAL-7 and CdAL-56, received the same Cd dose, followed by AL extract. Water or AL extract was administered daily by gavage. After either 7 or 56 days, the testis and accessory glands were removed after whole-body perfusion. Exposure to Cd and CdAL decreased the weight of the testis and epididymis, the gonadosomatic index, seminiferous tubular (ST) diameter, and ST volumetric proportion, and increased the volumetric proportion of interstitium after 56 days. In the epididymis caput, the tubular volumetric proportion decreased along with an increase of interstitial volumetric proportion and epithelium height after 56 days. The alterations observed were less severe only after 7 days. A progressive testicular damage resulted mainly in tubules lined only by Sertoli cells. The sperm number and cell debris decreased in the epididymis. We demonstrated that the testicular damage induced by single acute i.p. exposure to Cd occurred despite the daily oral intake of AL extract.


Cadmium Reproductive male toxicity Arctium lappa extract 


Compliance with ethical standards


This work was supported by grants and scholarships from the Fundação de Amparo à Pesquisa do Estado de São Paulo (grant number 2006⁄06142-8) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving animals were in accordance with the Committee for Ethics in Animal Experimentation of UNICAMP (1232–1).


  1. 1.
    Eleawa SM, Alkhateeb MA, Alhashem FH, Bin-Jaliah I, Sakr HF, Elrefaey HM, Khalil MA (2014) Resveratrol reverses cadmium chloride-induced testicular damage and subfertility by downregulating p53 and Bax and upregulating gonadotropins and Bcl-2 gene expression. J Reprod Dev 60:115–127CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Cavuşoğlu 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 12:1286–1292CrossRefPubMedGoogle Scholar
  3. 3.
    Fouad AA, Qureshi H, Al-Sultan AI, Yacoubi MT, Ali AA (2009) Protective effect of hemin against cadmium-induced testicular damage in rats. Toxicology 257:153–160CrossRefPubMedGoogle Scholar
  4. 4.
    Fouad AA, Jresat I (2014) Thymoquinone therapy abrogates toxic effect of cadmium on rat testes. Andrologia 46:1–8CrossRefGoogle Scholar
  5. 5.
    Blanco A, Moyano R, Vivo J, Flores-Acuña R, Molina A, Blanco C, Monterde JG (2007) Quantitative changes in the testicular structure in mice exposed to low doses of cadmium. Environ Toxicol Pharmacol 23:96–101CrossRefPubMedGoogle Scholar
  6. 6.
    Bizarro P, Acevedo S, Niño-Cabrera G, Mussali-Galante P, Pasos F, Avila-Costa MR, Fortoul TI (2003) Ultrastructural modifications in the mitochondrion of mouse Sertoli cells after inhalation of lead, cadmium or lead–cadmium mixture. Reprod Toxicol 17:561–566CrossRefPubMedGoogle Scholar
  7. 7.
    Herak-Kramberger C, Saboli I, Blanuša M, Smith PJ, Brown D, Breton S (2000) Cadmium inhibits vacuolar H+ ATPase-mediated acidification in the rat epididymis. Biol Reprod 63:599–606CrossRefPubMedGoogle Scholar
  8. 8.
    Huang Y, Su M, Jiang FR, Xu TL (2005) Damage of epididymis chronically exposed to cadmium and the antagonistic effect of vitamin E. Chin J Epidemiol 24:386–388Google Scholar
  9. 9.
    El-Shahat A, Gabr A, Meki A, Mehana ES (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
  10. 10.
    Asagba S, Adaikpoh M, Kadiri H, Obi FO (2007) Influence of aqueous extract of Hibiscus sabdariffa L. petal on cadmium toxicity in rats. Biol Trace Elem Res 115:47–57CrossRefPubMedGoogle Scholar
  11. 11.
    Jahangir T, Khan T, Prasad L, Sultana S (2005) Pluchea lanceolata attenuates cadmium chloride induced oxidative stress and genotoxicity in Swiss albino mice. J Pharm Pharmacol 57:1199–1204CrossRefPubMedGoogle Scholar
  12. 12.
    Ola-Mudathir K, Suru S, Fafunso M, Obioha UE, Faremi TY (2008) Protective roles of onion and garlic extracts on cadmium-induced changes in sperm characteristics and testicular oxidative damage in rats. Food Chem Toxicol 46:3604–3611CrossRefPubMedGoogle Scholar
  13. 13.
    Othman MS, Nada A, Zaki HS, Moneim AEA (2014) Effect of Physalis peruviana L. on cadmium-induced testicular toxicity in rats. Biol Trace Elem Res 159:278–287CrossRefPubMedGoogle Scholar
  14. 14.
    Predes FS, Diamante MAS, Foglio MA, Camargo CA, Aoyama H, Miranda SC, Dolder H (2014) Hepatoprotective effect of Arctium lappa root extract on cadmium toxicity in adult Wistar rats. Biol Trace Elem Res 160:250–257CrossRefGoogle Scholar
  15. 15.
    Lin C, Lin J, Yang JJ, Chuang SC, Ujiie T (1996) Anti-inflammatory and radical scavenge effects of Arctium lappa. Am J Chin Med 24:127–137CrossRefPubMedGoogle Scholar
  16. 16.
    Lin S, Chung T, Lin CC, Ueng TH, Lin YH, Lin SY, Wang LY (2000) Hepatoprotective effects of Arctium lappa on carbon tetrachloride-and acetaminophen-induced liver damage. Am J Chin Med 28:163–173CrossRefPubMedGoogle Scholar
  17. 17.
    Lin S, Lin C, Lin CC, Lin YH, Chen CF, Chen IC, Wang LY (2002) Hepatoprotective effects of Arctium lappa linne on liver injuries induced by chronic ethanol consumption and potentiated by carbon tetrachloride. J Biomed Sci 9:401–409PubMedGoogle Scholar
  18. 18.
    Predes FS, Ruiz AL, Carvalho JE, Foglio MA, Dolder H (2011) Antioxidative and in vitro antiproliferative activity of Arctium lappa root extracts. BMC Complem Altern Med 11:25–30CrossRefGoogle Scholar
  19. 19.
    Predes FS, Diamante MAS, Dolder H (2010) Testis response to two low doses of cadium in Wistar rats. Int J Exp Pathol 91:125–131CrossRefGoogle Scholar
  20. 20.
    Giaginis C, Gatzidou E, Theocharis S (2006) DNA repair systems as targets of cadmium toxicity. Toxicol Appl Pharmacol 213:282–290CrossRefPubMedGoogle Scholar
  21. 21.
    Russell LD, Ettlin RA, Sinha- Hikim AP, Clegg ED (1990) Histological and histopathological evaluation of the testis. Cache River Press, ClearwaterGoogle Scholar
  22. 22.
    Creasy D (2001) Pathogenesis of male reproductive toxicity. Toxicol Pathol 29:64–76CrossRefPubMedGoogle Scholar
  23. 23.
    Manna P, Sinha M, Sil P (2008) Cadmium induced testicular pathophysiology: prophylactic role of taurine. Reprod Toxicol 26:282–291CrossRefPubMedGoogle Scholar
  24. 24.
    Prozialeck W, Edwards J, Woods J (2006) The vascular endothelium as a target of cadmium toxicity. Life Sci 79:1493–1506CrossRefPubMedGoogle Scholar
  25. 25.
    Monsefi M, Alaee S, Moradshahi A, Rohani L (2009) Cadmium-induced infertility in male mice. Environ Toxicol 25:94–102Google Scholar
  26. 26.
    Prozialeck W, Edwards J, Nebert DW, Woods JM, Barchowsky A, Atchison WD (2008) The vascular system as a target of metal toxicity. Toxicol Scis 102:207–218CrossRefGoogle Scholar
  27. 27.
    Siu E, Mruk D, Porto CS, Cheng CY (2009) Cadmium-induced testicular injury. Toxicol Appl Pharmacol 238:240–249CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    França LR, Russell LD (1998) The testis of domestic animals. In: Regadera J, Martinez-Garcia R (eds) Male reproduction: a multidisciplinary overview. Churchill Livingstone, Madrid, pp 192–219Google Scholar
  29. 29.
    Sinha Hikim A, Bartke A, Russell L (1988) Morphometric studies on hamster testes in gonadally active and inactive states: light microscope findings. Biol Reprod 39:1225–1237CrossRefPubMedGoogle Scholar
  30. 30.
    Sacerdote F, Cavicchia J (1983) Ultrastructural effects of cadmium on the rat epididymis. Int J Androl 6:533–540CrossRefPubMedGoogle Scholar
  31. 31.
    Predes FS, Matta SLP, Monteiro JC, Oliveira TTD (2009) Investigation of liver tissue and biochemical parameters of adult wistar rats treated with Arctium lappa L. Braz Arch Biol Technol 52:335–340CrossRefGoogle Scholar
  32. 32.
    JianFeng C, PengYing Z, ChengWei X, TaoTao H, YunGui B, KaoShan C (2012) Effect of aqueous extract of Arctium lappa L. (burdock) roots on the sexual behavior of male rats. BMC Compl Altern Med 12:1–8CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Fabricia de Souza Predes
    • 1
    Email author
  • M. A. S. Diamante
    • 2
  • M. A. Foglio
    • 3
  • H. Dolder
    • 2
  1. 1.Department of Biological ScienceState University of Paraná/ Campus ParanaguáParanaguáBrazil
  2. 2.Department of Structural and Functional BiologyState University of CampinasCampinasBrazil
  3. 3.Pluridisciplinary Centre for ChemicalBiological and Agricultural Research at the State University of Campinas (CPQBA/UNICAMP)CampinasBrazil

Personalised recommendations