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Comparison of the deleterious effects of yaji and cadmium chloride on testicular physiomorphological and oxidative stress status: The gonadoprotective effects of an omega-3 fatty acid

  • Received : 2020.01.13
  • Accepted : 2020.04.01
  • Published : 2020.09.30

Abstract

Objective: This study investigated testicular oxidative stress status and physiomorphological function in Wistar rats fed with yaji and cadmium chloride (CdCl2). Methods: Sixty male albino Wistar rats (12 per group) were randomly assigned to five groups: group I (control), group II (300 mg/kg.bw of yaji), group III (500 mg/kg.bw of yaji), group IV (2.5 mg/kg.bw of CdCl2), and group V (2.5 mg/kg.bw of yaji+4 mg/kg.bw omega-3). Each group was evenly subdivided into two subgroups and treatment was administered for 14 days and 42 days, respectively. Semen quality (sperm count, progressive motility, normal morphology, and gonadosomatic index), hormones (testosterone, follicle-stimulating hormone, and luteinizing hormone), testicular oxidative stress markers (superoxide dismutase, catalase, glutathione peroxidase, and malonaldehyde) and testicular histomorphological features were examined. Results: Yaji caused significant (p< 0.05) dose- and duration-dependent reductions in semen quality, the gonadosomatic index, testosterone, follicle-stimulating hormone, and luteinizing hormone. Yaji also caused significant (p< 0.05) dose- and duration-dependent decreases in superoxide dismutase, catalase, and glutathione peroxidase activity, as well as increased testicular malonaldehyde levels. Yaji induced distortions in the testicular histological architecture. CdCl2 damaged testicular function by significantly (p< 0.05) reducing semen quality, reproductive hormone levels, and oxidative stress markers in albino Wistar rats. CdCl2 also altered the histology of the testis. Conclusion: This study shows that yaji sauce has similar anti-fertility effects to those of CdCl2, as it adversely interferes with male reproduction by impairing oxidative stress markers and the function and morphological features of the testis.

Keywords

References

  1. World Health Organization. Infertility definitions and terminology [Internet]. Geneva: World Health Organization; 2014 [cited 2020 Jul 10]. Available from: http://www.who.int/reproductivehealth/topics/infertility/definitions/en/index.html.
  2. Okonofua FE, Harris D, Odebiyi A, Kane T, Snow RC. The social meaning of infertility in Southwest Nigeria. Health Trans Rev 1997;7:205-20.
  3. Adetoro OO, Ebomoyi EW. The prevalence of infertility in a rural Nigerian community. Afr J Med Sci 1991;20:23-7.
  4. Ikechebelu JI, Adinma JI, Orie EF, Ikegwuonu SO. High prevalence of male infertility in southeastern Nigeria. J Obstet Gynaecol 2003;23:657-9. https://doi.org/10.1080/01443610310001604475
  5. Isidori AM, Pozza C, Gianfrilli D, Isidori A. Medical treatment to improve sperm quality. Reprod Biomed Online 2006;12:704-14. https://doi.org/10.1016/S1472-6483(10)61082-6
  6. Semet M, Paci M, Saias-Magnan J, Metzler-Guillemain C, Boissier R, Lejeune H, et al. The impact of drugs on male fertility: a review. Andrology 2017;5:640-63. https://doi.org/10.1111/andr.12366
  7. Carre J, Gatimel N, Moreau J, Parinaud J, Leandri R. Does air pollution play a role in infertility? A systematic review. Environ Health 2017;16:82. https://doi.org/10.1186/s12940-017-0291-8
  8. Corona G, Giagulli VA, Maseroli E, Vignozzi L, Aversa A, Zitzmann M, et al. Therapy of endocrine disease: testosterone supplementation and body composition: results from a meta-analysis study. Eur J Endocrinol 2016;174:R99-116. https://doi.org/10.1530/EJE-15-0262
  9. Tuttelmann F, Werny F, Cooper TG, Kliesch S, Simoni M, Nieschlag E. Clinical experience with azoospermia: aetiology and chances for spermatozoa detection upon biopsy. Int J Androl 2011;34:291-8. https://doi.org/10.1111/j.1365-2605.2010.01087.x
  10. Agarwal A, Prabakaran SA. Mechanism, measurement, and prevention of oxidative stress in male reproductive physiology. Indian J Exp Biol 2005;43:963-74.
  11. Saleh RA, Agarwal A, Sharma RK, Said TM, Sikka SC, Thomas AJ Jr. Evaluation of nuclear DNA damage in spermatozoa from infertile men with varicocele. Fertil Steril 2003;80:1431-6. https://doi.org/10.1016/S0015-0282(03)02211-8
  12. McCann D, Barrett A, Cooper A, Crumpler D, Dalen L, Grimshaw K, et al. Food additives and hyperactive behaviour in 3-year-old and 8/9-year-old children in the community: a randomised, doubleblinded, placebo-controlled trial. Lancet 2007;370:1560-7. https://doi.org/10.1016/S0140-6736(07)61306-3
  13. Gaby AR. Adverse effects of dietary fructose. Altern Med Rev 2005;10:294-306.
  14. Moore LK. Developing human. 2nd ed. Philadelphia: W.B. Saunders; 2003.
  15. Nwaopara AO, Anyanwu LC, Oyinbo CA, Anaikot IC. The histological changes in pancreas of Wister rats fed with diets containing Yaji (Local meat Sauce). J Exp Clin Anat 2004;3:44-7.
  16. Krishnaswamy K, Raghuramulu N. Bioactive phytochemicals with emphasis on dietary practices. Indian J Med Res 1998;108:167-81.
  17. Surh YJ, Lee SS. Capsaicin, a double-edged sword: toxicity, metabolism, and chemopreventive potential. Life Sci 1995;56:1845-55. https://doi.org/10.1016/0024-3205(95)00159-4
  18. Witchtl M. Herbal drugs and phytopharmaceuticals. 3rd ed. Boca Raton: CRC Press; 2004.
  19. McGee H. On food and cooking. New York: Scribner; 2004.
  20. Uzeh RE, Ohenhen RE, Adeniji OO. Bacterial contamination of tsire-suya, a Nigerian meat product. Pak J Nutr 2006;5:458-60. https://doi.org/10.3923/pjn.2006.458.460
  21. Nwaopara AO, Anibeze CI, Akpuaka FC. Induced histological features of hypoxia-ischaemia in the brain of rats fed with diet containing Yaji: the complex Nigerian meat sauce. Res J Appl Sci Eng Technol 2010;2:67-72.
  22. El-Din SB, Abd-El Aty OA. Biochemical and immunocytochemical studies of the testicular changes after treatment with Duloxetine hydrochloride and the possible protective effects of omega 3 in adult rat model of depression. AAMJ 2012;10:264-300.
  23. Jabbar SA, Mahde MS. Effect of dietary omega 3 essential polyunsaturated fatty acid on reproductive system of male rats that exposed to acrylamide. J Kerbala Univ 2011;9:155-66.
  24. Kumar AS, Deepthi KB, Prasad MV, Mary PG, Kumar SS, Swathi M. Evaluation of the protective effects of omega-3 fatty acids against methotrexate induced testicular toxicity in male albino mice. Int J Phytopharmacol 2011;2:48-52.
  25. Olutope MA, Solomon SA, Ayantayo AK. Ameliorative and protective effect of omega 3-fatty acid on testicular lipid concentration in ethanol- induced Wistar rats. Am J Biochem 2014;4:25-8.
  26. Odewumi CO, Latinwo LM, Ruden ML, Badisa VL, Fils-Aime S, Badisa RB. Modulation of cytokines and chemokines expression by NAC in cadmium chloride treated human lung cells. Environ Toxicol 2016;31:1612-9. https://doi.org/10.1002/tox.22165
  27. Bu T, Mi Y, Zeng W, Zhang C. Protective effect of quercetin on cadmium- induced oxidative toxicity on germ cells in male mice. Anat Rec (Hoboken) 2011;294:520-6. https://doi.org/10.1002/ar.21317
  28. Haidry MT, Malik A. Hepatoprotective and antioxidative effects of Terminalia arjuna against cadmium provoked toxicity in albino rats (Ratus norvigicus). Biochem Pharmacol 2014;3:1000130.
  29. Abdel Moneim AE, Bauomy AA, Diab MM, Shata MT, Al-Olayan EM, El-Khadragy MF. The protective effect of Physalis peruviana L. against cadmium-induced neurotoxicity in rats. Biol Trace Elem Res 2014;160:392-9. https://doi.org/10.1007/s12011-014-0066-9
  30. Nair AR, Lee WK, Smeets K, Swennen Q, Sanchez A, Thevenod F, et al. Glutathione and mitochondria determine acute defense responses and adaptive processes in cadmium-induced oxidative stress and toxicity of the kidney. Arch Toxicol 2015;89:2273-89. https://doi.org/10.1007/s00204-014-1401-9
  31. Baiomy AA. Protective role of grape seeds extract against cadmium toxicity in the lung of male wistar rats. J Cytol Histol 2016;5(004).
  32. Nwaopara AO, Odike MA, Inegbenebor U, Nwaopara SO, Ewere GI. A comparative study on the effects of excessive consumption of ginger, clove, red pepper and black pepper on the histology of the Kidney. Pak J Nutr 2008;7:287-91. https://doi.org/10.3923/pjn.2008.287.291
  33. Masopust J. Clinical biochemistry (in Czech). Prague: Karolinium; 2000.
  34. Nwaopara AO, Odike MA, Inegbenebor U, Adoye MI. The combined effects of excessive consumption of ginger, clove, red pepper and black pepper on the histology of the liver. Pak J Nutr 2007;6:524-7. https://doi.org/10.3923/pjn.2007.524.527
  35. Nwaopara AO, Anibeze C, Akpuaka F. Histological signs of neurodegeneration in the cerebrum of rats fed with diet containing Yaji: the complex Nigerian suya meat sauce. Asian J Med Sci 2010;2:16-21.
  36. Nwaopara AO, Odike MA, Inegbenebor U, Nwaopara SO, Ekhoye EI. A comparative study on the effects of excessive consumption of ginger, clove, red pepper and black pepper on the histology of the heart. Electron J Biomed 2008;3:61-4.
  37. Zemjanis R. Collection and evaluation of semen. In: Zemjanis R, editor. Diagnostic and therapeutic techniques in animal reproduction. Baltimore: William and Wilkins; 1977. p. 242
  38. Pant N, Srivastava SP. Testicular and spermatotoxic effects of quinalphos in rats. J Appl Toxicol 2003;23:271-4. https://doi.org/10.1002/jat.919
  39. Narayana K, Prashanthi N, Nayanatara A, Kumar HH, Abhilash K, Bairy KL. Effects of methyl parathion (o,o-dimethyl o-4-nitrophenyl phosphorothioate) on rat sperm morphology and sperm count, but not fertility, are associated with decreased ascorbic acid level in the testis. Mutat Res 2005;588:28-34. https://doi.org/10.1016/j.mrgentox.2005.08.012
  40. Amann RP. Sperm production rates: the testis. New York: Academic; 1970.
  41. Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 1979;95:351-8. https://doi.org/10.1016/0003-2697(79)90738-3
  42. Marklund S, Marklund G. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem 1974;47:469-74. https://doi.org/10.1111/j.1432-1033.1974.tb03714.x
  43. Sinha AK. Colorimetric assay of catalase. Anal Biochem 1972;47:389-94. https://doi.org/10.1016/0003-2697(72)90132-7
  44. Rotruck JT, Pope AL, Ganther HE, Swanson AB, Hafeman DG, Hoekstra WG. Selenium: biochemical role as a component of glutathione peroxidase. Science 1973;179:588-90. https://doi.org/10.1126/science.179.4073.588
  45. Ukoha UU, Egwu OA, Dimkpa U, Maduka SO, Okafor JI, Ndukwe, U, et al. Histological and weight changes in testes of male albino rats fed with diets containing Yaji (a local meat sauce). Int J Health Sci Res 2014;4:118-26.
  46. Piyachaturawat P, Kingkaeohoi S, Toskulkao C. Potentiation of carbon tetrachloride hepatotoxicity by piperine. Drug Chem Toxicol 1995;18:333-44. https://doi.org/10.3109/01480549509014327
  47. Malini T, Arunakaran J, Aruldhas MM, Govindarajulu P. Effects of piperine on the lipid composition and enzymes of the pyruvatemalate cycle in the testis of the rat in vivo. Biochem Mol Biol Int 1999;47:537-45.
  48. Malini T, Manimaran RR, Arunakaran J, Aruldhas MM, Govindarajulu P. Effects of piperine on testis of albino rats. J Ethnopharmacol 1999;64:219-25. https://doi.org/10.1016/S0378-8741(98)00128-7
  49. D'Cruz SC, Vaithinathan S, Saradha B, Mathur PP. Piperine activates testicular apoptosis in adult rats. J Biochem Mol Toxicol 2008;22:382-8. https://doi.org/10.1002/jbt.20251
  50. Nwaopara, AO, Odike MA, Ikhuoriah TA, Anyanwu LC. Potential health hazards in Yaji: the complex suya meat sauce. Medilink J 2007;8:34-8.
  51. Buch JG, Dikshit RK, Mansuri SM. Effect of certain volatile oils on ejaculated human spermatozoa. Indian J Med Res 1988;87:361-3.
  52. Mishra RK, Singh SK. Safety assessment of Syzygium aromaticum flower bud (clove) extract with respect to testicular function in mice. Food Chem Toxicol 2008;46:3333-8. https://doi.org/10.1016/j.fct.2008.08.006
  53. Dehghani F, Heshmatpour A, Panjeshanin M, Talaei-Khozaniet T. Toxic effects of water/alcoholic extract of Syzygium aromaticum on sperm quality, sex hormones and reproductive tissues in male mouse. Eur J Biol 2012;71:95-102.
  54. Chaieb K, Hajlaoui H, Zmantar T, Kahla-Nakbi AB, Rouabhia M, Mahdouani K, et al. The chemical composition and biological activity of clove essential oil, Eugenia caryophyllata (Syzigium aromaticum L. Myrtaceae): a short review. Phytother Res 2007;21:501-6. https://doi.org/10.1002/ptr.2124
  55. Ashkani H, Akbari A, Heydari ST. Epidemiology of depression among infertile and fertile couples in Shiraz, southern Iran. Indian J Med Sci 2006;60:399-406. https://doi.org/10.4103/0019-5359.27670
  56. Zini A, Garrels K, Phang D. Antioxidant activity in the semen of fertile and infertile men. Urology 2000;55:922-6. https://doi.org/10.1016/S0090-4295(00)00453-2
  57. Gil-Guzman E, Ollero M, Lopez MC, Sharma RK, Alvarez JG, Thomas AJ Jr, et al. Differential production of reactive oxygen species by subsets of human spermatozoa at different stages of maturation. Hum Reprod 2001;16:1922-30. https://doi.org/10.1093/humrep/16.9.1922
  58. Siciliano L, Tarantino P, Longobardi F, Rago V, De Stefano C, Carpino A. Impaired seminal antioxidant capacity in human semen with hyperviscosity or oligoasthenozoospermia. J Androl 2001;22:798-803.
  59. Khosrowbeygi A, Zarghami N. Levels of oxidative stress biomarkers in seminal plasma and their relationship with seminal parameters. BMC Clin Pathol 2007;7:6. https://doi.org/10.1186/1472-6890-7-6
  60. Zelen I, Mitrovic M, Jurisic-Skevin A, Arsenijevic S. Activity of superoxide dismutase and catalase and content of malondialdehyde in seminal plasma of infertile patients. Med Pregl 2010;63:624-9. https://doi.org/10.2298/MPNS1010624Z
  61. Shiva M, Gautam AK, Verma Y, Shivgotra V, Doshi H, Kumar S. Association between sperm quality, oxidative stress, and seminal antioxidant activity. Clin Biochem 2011;44:319-24. https://doi.org/10.1016/j.clinbiochem.2010.11.009
  62. Ihab M. The effects of the oral dosage of monosodium glutamate applied for short- and long-terms on the histology and ultrastructure of testes of the adult rats. J Anim Veter Adv 2012;11:124-33. https://doi.org/10.3923/javaa.2012.124.133
  63. Unchern S, Saito H, Nishiyama N. Death of cerebellar granule neurons induced by piperine is distinct from that induced by low potassium medium. Neurochem Res 1998;23:97-102. https://doi.org/10.1023/A:1022461706344
  64. Barber BJ, Blake NJ. Reproductive physiology. In: Shumway SE, Parsons GJ, editors. Biology and aquaculture. Amsterdam: Elsvier; 2006. p. 133-223.
  65. Nwaopara AO, Anibeze CI, Akpuaka FC. Histological signs of oligodendroglioma in the brain of rats fed with diet containing Yaji: the complex Nigerian suya meat sauce. J Clin Rev Opin 2009;1:21-5.
  66. Nwaopara AO, Oyadonghan GP, Olugbenga MA, Ujaddughe MO, Ekoh SN. The combined incidence of grade II and grade IV astrocytoma in the brain of rats fed with diet containing Yaji: a complex Nigerian Suya meat sauce. Int J Basic Appl Innov Res 2012;1:116-21.
  67. Ankarcrona M, Dypbukt JM, Bonfoco E, Zhivotovsky B, Orrenius S, Lipton SA, et al. Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 1995;15:961-73. https://doi.org/10.1016/0896-6273(95)90186-8
  68. Aydos K, Guven MC, Can B, Ergun A. Nicotine toxicity to the ultrastructure of the testis in rats. BJU Int 2001;88:622-6. https://doi.org/10.1046/j.1464-4096.2001.02384.x
  69. Goyal HO, Braden TD, Mansour M, Williams CS, Kamaleldin A, Srivastava KK. Diethylstilbestrol-treated adult rats with altered epididymal sperm numbers and sperm motility parameters, but without alterations in sperm production and sperm morphology. Biol Reprod 2001;64:927-34. https://doi.org/10.1095/biolreprod64.3.927
  70. Motahareh B, Haidar A, Seyed EH, Saeed CA. Effects of walnut oil on plasma levels of testosterone pre and post puberty in male rats. Am J Ethnomed 2014;4:266-75.
  71. Zak A, Zeman M, Tvrzicka E, Stolba P. The effect of fish oil on metabolic parameters in patients with type 2 diabetes mellitus associated with dyslipidemia. Cas Lek Cesk 1996;135:354-9.
  72. Ekhoye EI, Nwangwa EK, Aloamaka CP. Changes in some testicular biometric parameters and testicular function in cadmium chloride administered Wistar rats. Br J Med Res 2013;3:2031-41. https://doi.org/10.9734/BJMMR/2013/2821
  73. Ige SF, Olaleye SB, Akhigbe RE, Akanbi TA, Oyekunle OA, Udoh UA. Testicular toxicity and sperm quality following cadmium exposure in rats: ameliorative potentials of Allium cepa. J Hum Reprod Sci 2012;5:37-42. https://doi.org/10.4103/0974-1208.97798
  74. Akunna GG, Saalu LC, Ogunlade B, Enye LA. Spermatotoxicity in animal models exposed to fragrance components. J Med Sci 2014;14:46-50.
  75. Khanna S, Mitra S, Lakhera PC, Khandelwal S. N-acetylcysteine effectively mitigates cadmium-induced oxidative damage and cell death in Leydig cells in vitro. Drug Chem Toxicol 2016;39:74-80. https://doi.org/10.3109/01480545.2015.1028068
  76. Mendiola J, Moreno JM, Roca M, Vergara-Juarez N, Martinez-Garcia MJ, Garcia-Sanchez A, et al. Relationships between heavy metal concentrations in three different body fluids and male reproductive parameters: a pilot study. Environ Health 2011;10:6. https://doi.org/10.1186/1476-069X-10-6
  77. Xu LC, Wang SY, Yang XF, Wang XR. Effects of cadmium on rat sperm motility evaluated with computer assisted sperm analysis. Biomed Environ Sci 2001;14:312-7.
  78. Roychoudhury S, Massanyi P, Bulla J, Choudhury MD, Lukac N, Filipejova T, et al. Cadmium toxicity at low concentration on rabbit spermatozoa motility, morphology and membrane integrity in vitro. J Environ Sci Health A Tox Hazard Subst Environ Eng 2010;45:1374-83. https://doi.org/10.1080/10934529.2010.500909
  79. Tavilani H, Doosti M, Abdi K, Vaisiraygani A, Joshaghani HR. Decreased polyunsaturated and increased saturated fatty acid concentration in spermatozoa from asthenozoospermic males as compared with normozoospermic males. Andrologia 2006;38:173-8. https://doi.org/10.1111/j.1439-0272.2006.00735.x

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