Al-Qadisiyah Journal of Veterinary Medicine Sciences

Reproductive Performance of Adult Male Rats Previously Exposed to Aflatoxicosis at Pre-puberty

Document Type : Research Paper

Authors

Deptartment of Physiology, Pharmacology, and Biochemistry, College of Veterinary Medicine, University of Al-Qadisiyah, Al-Diwaniyah City, Iraq.

Abstract

Aflatoxin-induced reproductive toxicity was investigated in adult male rats. To investigate the effect of pre-pubertal exposure to aflatoxin B1 (AFB1) on semen quality in male rats after puberty. Eighty premature male rats (35 days old) were assigned equally to control and treatment groups. The males were daily administered with distilled water and AFB1 (0.3mg/kg/day) per os, respectively. After 15, 25, and 35 days of treatment (pre-puberty, puberty, and post-puberty stags, respectively), ten males from each group were weighed, anesthetized, and sacrificed. Testes, epididymis, seminal vesicles, and prostates were dissected and weighed. At puberty (25 days of treatment) and post-puberty (35 days of treatment), the tail of the epididymis was dissected for semen analysis, including sperm motility, sperm count, sperm viability, and sperm abnormality. Following 15, 25, and 35 days of exposure, the AFB1-treated group revealed a decline in the relative weight of testes, epididymis, seminal vesicle, and prostate than the control group, early at the pre-pubertal stage, which continued at pubertal and post-pubertal-stages. Sperm motility, sperm count, and sperm viability were significantly decreased, while sperm abnormality was significantly increased in the AFB1 group, at puberty and post-puberty. Females matted with AFB1 treated males revealed significant decrease of pregnancy rate, number of offspring, and litter weight at birth in comparison with those matted with control males. Altogether, these results showed an adverse effect of pre-pubertal exposure to AFB1 on male reproductive performance with impaired spermatogenesis after puberty.

Keywords

References
  1. Rotimi OA, Onuzulu CD, Dewald AL, Ehlinger J, Adelani IB, Olasehinde OE, Rotimi SO, and Goodrich JM. Early Life Exposure to Aflatoxin B1 in Rats: Alterations in Lipids, Hormones, and DNA Methylation among the Offspring. Int J Environ Res Public Health. 2021; 18(2): 589. Doi: 10.3390/ijerph18020589.
  2. Nazhand A, Durazzo A, Lucarini M, Souto EB, and Santini A. Characteristics, occurrence, detection and detoxification of aflatoxins in foods and feeds. Foods. 2020; 9(5): 644. DOI: 10.3390/foods9050644.
  3. Moretti A, Pascale M, and Logrieco AF. Mycotoxin risks under a climate change scenario in Europe. Trends in food sci. Tech., 2019, 84: 38-40. DOI: ‏10.1016/j.tifs.2018.03.008.
  4. Mahmood M., and Youkhana S. Pathological changes of experimentally induced Aflatoxicosis in liver of broiler chickens. QJVMS (2012) Vol. 11 No. (1): 58-63.
  5. Benkerroum N. Aflatoxins: Producing-Molds, Structure, Health Issues and Incidence in Southeast Asian and Sub-Saharan African Countries. Int J Environ Res Public Health. 2020; 17: 1215. DOI: 10.3390/ijerph17041215. 
  6. Deng J, Zhao L, Zhang N-Y, Karrow NA, Krumm CS, Qi D-S, and Sun L-H. Aflatoxin B1 metabolism: Regulation by phase I and II metabolizing enzymes and chemoprotective agents. Mutat. Res. Rev. Mutat. Res., 2018; 778: 79–89. DOI: 10.1016/j.mrrev.2018.10.002. 
  7. Benkerroum N. Chronic and Acute Toxicities of Aflatoxins: Mechanisms of Action. Int J Environ Res Public Health. 2020, 17(2): 423. Doi: 10.3390/ijerph17020423.
  8. Li C, Liu X, Wu J, Ji X, and Xu Q. Research progress in toxicological effects and mechanism of aflatoxin B1 toxin. Peer J, 2022; 10: e13850. DOI: ‏10.7717/peerj.13850.
  9. Dhanasekaran D, Shanmugapriya S, Thajuddin N, and Panneerselvam A. Aflatoxins and Aflatoxicosis in Human and Animals. Aflatoxins - Biochemistry and Molecular Biology. 2011, Pp: 221–254 p. Doi: 10.5772/22717. https://www.intechopen.com/chapters/20393
  10. Nurul Adilah Z, and Mohd Redzwan S. Effect of dietary macronutrients on aflatoxicosis: a mini-review. J Sci Food Agric., 2017; 97(8): 2277-81. DOI: 10.1002/jsfa.8234.
  11. Saber H, Chebloune Y, Moussaoui A. Molecular Characterization of Aspergillus flavusStrains Isolated from Animal Feeds. Pol. J. Microbiol., 2022; 71(4): 589-599. DOI: 10.33073/pjm-2022-048.
  12. Usman M, Javed MR, Mehmood MA, Huma T, and Ijaz A. Isolation of aflatoxigenic Aspergillus flavus from animal-feed and exploration of the genetic basis of aflatoxin biosynthesis. Pak. Vet. J., 2019; 39(4): 541-547. DOI: 10.29261/pakvetj/2019.078.
  13. Mtimet N, Walke M, Baker D, Lindahl J, Hartmann M, and Grace D. Kenyan awareness of aflatoxin: An analysis of processed milk consumers. Poster presented at the 29th International Conference of Agricultural Economists (ICAE), Milan, Italy, 8-14 August. Nairobi: ILR,2015.
  14. Hasanzadeh S, Hosseini E, and Rezazadeh L. Effects of aflatoxin B1 on profiles of gonadotropic (FSH and LH), steroid (testosterone and 17β-estradiol) and prolactin hormones in adult male rat. Iran. J. Vet. Res.; 2011; 12: 332–336. DOI:10.22099/IJVR.2011.85.
  15. Murad AF, Ahmed S, and Abead S. Toxicity effect of aflatoxin B1 on reproductive system of albino male rats. Pak J Biol Sci, 2015; 18(3): 107–114. DOI: 10.3923/pjbs.2015.107.114.
  16.  Mohammed BJ, Al-Saaidi JAA, and Al-Zwean DHY. Reprotoxicological ameliorating effect of camel milk against aflatoxicosis in male rats. J Pharm Negative Results; 2022; 13(4): 456-462. DOI:10.47750/pnr.2022.13.04.058.
  1. Mohammed BJ, Al-Saaidi JAA, and Al-Zwean DHY. The protective role of camel milk against reprotoxicity, hepatotoxicity, and nephrotoxicity in aflatoxic-induced male rats. Research J. Pharm. and Tech.; 2023; 16(3): 1072-8. DOI:10.52711/0974-360X.2023.00179.
  2. El- Khoury D, Fayjaloun S, Nassar M, Sahakian J, and Aad PY. Updates on the effect of mycotoxins on male reproductive efficiency in mammals. Toxins, 2019; 11(9): 515.‏ DOI: 10.3390/toxins11090515.
  3. Faridha A, Faisal K, and Akbarsha MA. Aflatoxin treatment brings about generation of multinucleate giant spermatids (symplasts) through opening of cytoplasmic bridges: Light and transmission electron microscopic study in Swiss mouse. Reprod. Toxicol., 2007; 24: 403-408. DOI: 10.1016/j.reprotox.2007.04.071.
  4. Kudayer AM, Alsandaqchi AT, Saleh FM, and Alwan NA. Toxic effect of aflatoxin B1 on heart, lung, and testis of male albino rats: histopathology study. In IOP Conference Series: Materials Science and Engineering; 2019; 571(1): 012055. IOP Publishing. DOI:‏10.1088/1757-899X/571/1/012055
  5. Cheng D, Zheng XM, Li SW, Yang ZW, and Hu LQ. Effects of epidermal growth factor on sperm content and motility of rats with surgically induced varicoceles. Asian J. Androl., 2006; 8(6), 713-717. DOI: 10.1111/j.1745-7262.2006.00202.x.
  6. Hinting A. Methods of semen analysis. In: Assessment of human sperm fertilizing ability (Doctoral dissertation, Ph. D. thesis by Hinting A, 1989. University of Michigan state).‏
  7. Björndahl L, Söderlund I, and Kvist U. Evaluation of the one step eosin-nigrosin staining technique for human sperm vitality assessment. Human Reproduction (Oxford, England), 2003; 18(4): 813–816. DOI: 10.1093/HUMREP/DEG199.
  8. Alizadeh N, Abbasi M, Abolhassani F, Amidi F, Mahmoudi R, Hoshino Y, Sato E, Ragerdikashani I. Effects of aminoguanidine on infertile varicocelized rats: A functional and morphological study. Daru. 2010;18(1):51-6. PMID: 22615594; PMCID: PMC3232080.
  9. Schefler WC. Statistics for the biological sciences. Addison- Wesley Publishing Company, London, 2nd ed., 1979. DOI: 10.1002/bimj.19700120316.
  10. Rushing BR, and Selim MI. Structure and oxidation of pyrrole adducts formed between aflatoxin B2a and biological amines. Chem. Res. Toxicol., 2017; 30: 1275-85. DOI: 10.1021/acs.chemrestox.7b00002.
  11. Zhuang Z, Huang Y, Yang Y, and Wang S. Identification of AFB1-interacting proteins and interactions between RPSA and AFB1. J. Hazard. Mater.,  2016; 301: 297–303. DOI: 10.1016/j.jhazmat.2015.08.053. 
  12. Bedard LL, and Massey TE. Aflatoxin B1-induced DNA damage and its repair. Cancer Lett. 2006; 241: 174–183. DOI: 10.1016/j.canlet.2005.11.018. 
  13. Klaunig JE, Kamendulis LM, and Hocevar BA. Oxidative stress and oxidative damage in carcinogenesis. Toxicol. Pathol., 2009; 38: 96–109. DOI: 10.1177/0192623309356453. 
  14. Ayala A, Munoz MF, and Arguelles S. Lipid peroxidation: Production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxid. Med. Cell. Longev., 2014; 2014: 360438. DOI: 10.1155/2014/360438. 
  15. Yu J, and Zhang L. PUMA, a potent killer with or without p53. Oncogene, 2008; 27: S71-S83. DOI: 10.1038/onc.2009.45. 
  16. Ignatov AV, Bondarenko KA, and Makarova AV. Non-bulky lesions in human DNA: The ways of formation, repair, and replication. Acta Nat, 2017; 9: 12–26. DOI: 10.32607/20758251-2017-9-3-12-26. 
  17. Evans MD, Dizdaroglu M, and Cooke MS. Oxidative DNA damage and disease: Induction, repair and significance. Mutat. Res., 2004; 567: 1–61. DOI: 10.1016/j.mrrev.2003.11.001. 
  18. Cooke MS, Evans MD, Dizdaroglu M, and Lunec J. Oxidative DNA damage: Mechanisms, mutation, and disease. FASEB J., 2003; 17: 1195–1214. DOI: 10.1096/fj.02-0752rev.
  19. 34. He L, He T, Farrar S, Ji L, Liu T, and Ma X. Antioxidants maintain cellular redox homeostasis by elimination of reactive oxygen species. Cell Physiol. Biochem., 2017; 44: 532–553. DOI: 10.1159/000485089. 
  1. Achermann JC, and Jameson JL. Fertility and infertility: genetic contributions from the hypothalamic-pituitary-gonadal axis. Mol. Endocrinol., 1999; 13: 812–8. DOI: 10.1210/mend.13.6.0301.
  2. Oduwole OO, Peltoketo H, and Huhtaniemi IT. Role of follicle-stimulating hormone in spermatogenesis. Front Endocrinol, 2018; 9: 763. DOI: 10.3389/fendo.2018.00763.
  3. O'Donnell L, Pratis K, Stanton PG, Robertson DM, and McLachlan RI. Testosterone-dependent restoration of spermatogenesis in adult rats is impaired by a 5alpha-reductase inhibitor. J Androl., 1999; 20(1): 109-17. PMID: 10100481.
  4. Peltola V, Mäntylä E, Huhtaniemi I, and Ahotupa M. Lipid peroxidation and antioxidant enzyme activities in the rat testis after cigarette smoke inhalation or administration of polychlorinated biphenyls or polychlorinated naphthalenes. J Androl., 1994; 15(4): 353-61. PMID: 7982804.
  5. Chen H, Liu J, Luo L, Baig MU, Kim JM, and Zirkin BR. Vitamin E, aging and Leydig cell steroidogenesis. Exp Gerontol., 2005; 40(8-9): 728-36. DOI: 10.1016/j.exger.2005.06.004.
  6. Chowdhury P, Soulsby ME, and Scott JL. Effects of aminoguanidine on tissue oxidative stress induced by hindlimb unloading in rats. Ann Clin Lab Sci., 2009; 39: 64-70. PMID: 19201744.
Al-Qadisiyah Journal of Veterinary Medicine Sciences
Volume 23, Issue 1
May 2024
Pages 26-34
Files
Share
How to cite
Statistics