Protective Effects of Tigernut (Cyperus esculentus) on Bisphenol A- Induced Testicular Toxicity in Wistar Rats

Protective Effects of Tigernut (Cyperus esculentus) on Bisphenol A- Induced Testicular Toxicity in Wistar Rats

Main Article Content

Abraham Abigail
Idaguko Chika Anna

Abstract

Bisphenol A (BPA) have been reported to induced reprotoxicity in rats. This study was conducted to find out the ameliorative properties of aqueous extract of Cyperus esculentus (tigernut) on BPA induced testicular toxicity in Wistar rats.


Methods: Twenty male rats were divided randomly into 4 groups (n=5): group A: (Control); group B: Bisphenol A (BPA) (25 mg/kg b.w/day); group C: tigernut (200 mg/kg b.w); group D: (25 mg/kg of BPA+ 200 mg/kg of tigernut extract. 25 mg/kg of BPA was dissolved in 0.2 ml of olive oil as vehicle and  administration was given by oral gavage for 4 weeks. The body weights were measured. Blood were collected for the testosterone (T) and luteinizing hormone (LH) assays; the epididymis were processed for sperm count, sperm motility, sperm viability and sperm abnormality test; while the testes were harvested for  histology


Results: There was a significantly (p < 0.05) decreased in body weight; reduced (sperm count, motility, viability, serum testosterone and luteinizing hormone) in BPA compared with control group. These parameters however increased significantly (p < 0.05) in tigernut (200mg) and BPA + tigernut (200mg) compared with BPA. Also,  histological examination showed widened interstitial spaces, some distorted seminiferous tubules, degeneration of basement membrane, scanty Leydig cells, fewer spermatozoa and  vacuolation  While BPA + tigernut  (group D); showed improved testicular architecture (preserved interstitial spaces and interstitial cells. restoration of the loss of the basement membrane  and closely packed seminiferous tubules with well-arranged germinal epithelium. Supplementation with tigernuts following BPA administration produces a reversal of the deleterious effect of BPA on the testis.

References

Abu, H. H., Muhamad, M. H., Budi, K. S, Buhari, J., & Husain, A. O. (2023). Managing Bisphenol A Contamination: Advances in Removal Technologies and Future Prospects. Water., 15(20):3573. https://doi.org/10.3390/w15203573

Adam, M., Esievo, K. A. N, (2020). Bisalla, M., Ayo, J. O., Aliyu, A.I. , Akanbi, O. B., Baba, A.Y., Raji, L. O., & Saleh, A. Reproduction Pathology of Experimentally Induced Lead Poisoning in Red Sokoto Buck: Protective Effect of Tiger Nut (Cyperus Esculentus) Assiut Veterinary Medical Journal., 66(165): 67-79,

Aghajani M. M. R., Shafi, H., Gholamitabar, T. M., Moslemi, L., Aghamohammadi, A., Hajitabar, F., Mirabi, P., & Mehdinezhad, G. N. (2023). The Correlation of Urine Bisphenol A with Semen Parameters in Men Referred to Infertility Centers: A Cross-Sectional Study. Int J Fertil Steril., 7;17(4):292-298. https://doi.org/10.22074/ijfs.2023.559352.1341. PMID: 37577915; PMCID: PMC10439992.

Akash, M. S. H., Rasheed, S., Rehman, K., Imran, M., & Assiri, M. A. (2023). Toxicological evaluation of bisphenol analogues: preventive measures and therapeutic interventions. RSC Adv., 19;13(31):21613-21628. https://doi.org/10.1039/d3ra04285e. PMID: 37476040; PMCID: PMC10354593.

Allouh, M. Z., Daradka, H. M. & Ghaida, J. H. A. (2015). Influence of Cyperus esculentus tubers (Tiger Nut) on male rat copulatory behavior. BMC Complement Altern Med 15, 331. https://doi.org/10.1186/s12906-015-0851-9

Amjad S., Rahman, M. S., & Pang, M. G. (2020). Role of Antioxidants in Alleviating Bisphenol A Toxicity. Biomolecules., 25;10(8):1105. https://doi.org/10.3390/biom10081105. PMID: 32722388; PMCID: PMC7465987

Bakare, A. A., Mosuro A. A., & Osibanjo, O. (2005). An in vivo evaluation of induction of abnormal sperm morphology in mice by landfill leachates. Mutat. Res., 582: 28-34.

Bjorndahl, L., Sodourlund, I., & Kvist, U. (2003). Evaluation of the one-step eosin-nigrosin staining technique for human sperm vitality assessment. Hum. Reprod., 18: 813-816.

Cheng, Y., Buffone, M. G., Kouadio M., Goodheart, M., Page, D. C., Gerton, G. L., Davidson, I., & Wang, P. J. (2007). Abnormal sperm in mice lacking the Taf7l gene. Mol Cell Biol., 27:2582–2589. https://doi.org/10.1128/MCB.01722-06.

Ekaluo, U. B., Ikpeme, E.V., & Udokpoh, E. A. (2009). Sperm head abnormality and mutagenic effects of aspirin, paracetamol and caffeine containing analgesics in rats. Int. J. Toxicol., 7: 1-9

Ekaluo, U. B., Ikpeme, E.V., Ibiang Y.B., & Amaechina, O.S. (2013). Attenuating role of vitamin C on sperm toxicity induced by monosodium glutamate in albino rats. J. Biol. Sci., 13: 298-301

Fonseca, M. I., Lorigo. M., & Cairrao, E. (2022). Endocrine-Disrupting Effects of Bisphenol A on the Cardiovascular System: A Review. Journal of Xenobiotics., 12(3):181-213. https://doi.org/10.3390/jox12030015

Gbotolorun, S. C., Salako, A. A., & Ogunlade, B. (2022). Tiger nut: Antidote for alcohol-induced testicular toxicity in male Sprague-Dawley rats. JBRA Assist Reprod., 17;26(2):222-231. https://doi.org/10.5935/1518-0557.20210061. PMID: 34672482; PMCID: PMC9118967.

Guide for the Care and Use of Laboratory Animals. (8TH ed.). (2011). National Academies Press.

Hassan, L. A., Anyanwu, G. E., Nto, N. J., Obikili, E. N., Finbarrs-Bello, E., & Abireh, L. (2018). Curative effect of aqueous extract of Cyperus esculentus on flutamide-induced testicular dysfunction in male Wistar rats. Journal of Experimental and Clinical Anatomy, 17:13 - 17.

Im, J., & Löffler, F. E. (2016). Fate of bisphenol A in terrestrial and aquatic environments. Environmental science & technology., 50(16): 8403-8416.

Kawa, I. A., Akbar M., Fatima, Q, Mir, S. A., Jeelani, H., Manzoor, S., & Rashid, F. (2021). Endocrine disrupting chemical Bisphenol A and its potential effects on female health. Diabetes Metab Syndr., 15(3):803-811.

https://doi.org/10.1016/j.dsx.2021.03.031. Epub. PMID: 33839640.

Kumar, M., Sarma, D. K., Shubham, S., Kumawat, M., Verma, V., Prakash, A., & Tiwari, R. (2020). Environmental Endocrine-Disrupting Chemical Exposure: Role in Non-Communicable Diseases. Frontiers in Public Health., 8

Kurniawan, S. B., Abdullah, S. R. S., Imron, M. F., & Ismail, N. (2020). Current state of marine plastic pollution and its technology for more eminent evidence: A review. J. Clean. Prod., 278, 123537.

Lahimer, M., Abou, D. M., Montjean, D., Cabry, R., Bach, V., Ajina, M., Ben, A. H, Benkhalifa, M., & Khorsi-Cauet, H. (2023). Endocrine disrupting chemicals and male fertility: from physiological to molecular effects. Front Public Health., 10;11:1232646. https://doi.org/10.3389/fpubh.2023.1232646. PMID: 37886048; PMCID: PMC10598475.

Li. X., Wen, Z., Wang, Y., Mo, J., Zhong, Y., & Ge, R-S. (2020). Bisphenols and Leydig cell development and function. Front Endocrinol., 11:447. https://doi.org/10.3389/fendo.2020.00447

Moussavi, G., & Haddad, F.A. (2019). Bacterial peroxidase-mediated enhanced biodegradation and mineralization of bisphenol A in a batch bioreactor. Chemosphere., 222, 549–555.

Munir, B., Qadir, A., & Tahir, M. (2017). Negative effects of bisphenol A on testicular functions in albino rats and their abolitions with Tribulus terristeris L. Braz. J. Pharm. Sci., 53(3):e00104

Norazit, A., Mohamad, J., Razak, S. A., Abdulla, M. A,, Azmil, A., & Mohd, M. A. (2012). Effects of Soya Bean Extract, Bisphenol A and 17β-Estradiol on the Testis and Circulating Levels of Testosterone and Estradiol Among Peripubertal Juvenile Male Sprague-Dawley Rats. Sains Malaysiana., 41(1): 63–69-

Nwakanma, A. A., Ekong, M., Ngwuben, I. C, Idaguko, C. A., & Elemuo, C.O . (2022). Cyperus esculentus L. Protects Testis and Sperm Morphology of Hyperglycaemic Rats. International Journal of Medical and Surgical Sciences., 9(3), 1–16. https://doi.org/10.32457/ijmss.v9i3.1924

Nwosu, L.C., Edo. G. I., & Ozgor. E. (2022). The phytochemical, proximate, pharmacological, GC-MS analysis of Cyperus esculentus (Tiger nut): A fully validated approach in health, food and nutrition. Food Biosci., 46:101551. https://doi.org/10.1016/j.fbio.2022.101551.

Ofem, O. E., Udonkang, M. I., Bassey, I. E., & Okechi, O. O. (2023). Cyperus esculentus (Tiger Nut) Improves Fertility and Testicular Histology in Male Sprague Dawley Rats. Tropical Journal of Natural Product Research (TJNPR)., 7(12), 5670–5676

Olukole, S. G., Ola-Davies, E. O., Lanipekun, D. O., & Oke, B. O. (2020). Chronic exposure of adult male Wistar rats to bisphenol A causes testicular oxidative stress: Role of gallic acid. Endocr Regul., 1;54 (1):14-21. https://doi.org/10.2478/enr-2020-0003. PMID: 32597147.

Oyedepo, T.A., & Odoje, O.F. (2014). Hepato-protective Activities of Tiger Nut (Cyperus esculentus) Against Hepatotoxicity Induced by Carbon Tetrachloride in Rats. J Pharm Toxicol Stud, V. 2(4), P. 37 – 41.

Qiu, Y., Yang, H., Li, C., & Xu, C. (2020). Progress in Research on Sperm DNA Fragmentation. Med Sci Monit., 22;26:e918746. https://doi.org/10.12659/MSM.918746. PMID: 32319429; PMCID: PMC7191954

Saeed, M. M., Fernández-Ochoa, Á., Saber, F. R., Sayed, R. H., Cádiz-Gurrea, M. L, Elmotayam, A. K, Leyva-Jiménez, F. J., Segura-Carretero, A., & Nadeem, R. I. (2022). The Potential Neuroprotective Effect of Cyperus esculentus L. Extract in Scopolamine-Induced Cognitive Impairment in Rats: Extensive Biological and Metabolomics Approaches. Molecules., 21;27(20):7118. https://doi.org/10.3390/molecules27207118. PMID: 36296710; PMCID: PMC9606906

Sánchez-Zapata, E., Pérez-Álvarez, J. A., & Fernández-López, J. (2012). Effects of tiger nut (Cyperus esculentus) milk liquid co-products on the quality of pork burgers. International Journal of Food Science & Technology,, 47(10):2198-2204

Santiago, J., Silva, J. V., Santos, M. A. S., & Fardilha, M. (2021). Fighting Bisphenol A-Induced Male Infertility: The Power of Antioxidants. Antioxidants (Basel)., 15;10(2):289. https://doi.org/10.3390/antiox10020289. PMID: 33671960; PMCID: PMC7919053.

Shamhari, A., Abd Hamid, Z., Budin, S. B., Shamsudin, N. J., & Taib, I. S. (2021). Bisphenol A and Its Analogues Deteriorate the Hormones Physiological Function of the Male Reproductive System: A Mini-Review. Biomedicines., 9(11):1744. https://doi.org/10.3390/biomedicines9111744. PMID: 34829973; PMCID: PMC8615890.

Sidorkiewicz, I., Zareba, K., Wolczynski, S., & Czerniecki, J. (2017). Endocrine-disrupting chemicals-Mechanisms of action on male reproductive system. Toxicol Ind Health., 33:601–9. https://doi.org/10.1177/0748233717695160

Smith, L. B., & Walker, W. H. (2014). The regulation of spermatogenesis by androgens. Seminars in Cell & Developmental Biology, 30: 2-13

Takahashi, O., & Oishi, S. (2003). Testicular toxicity of dietary or parenterally administered bisphenol A in rats and mice. Food Chemistry Toxicology., 41: 1035-1044.

Udefa, A. L., Amama, E. A., Archibong, E. A., Nwangwa, J. N., Adama, S., Inyang, V. U., Inyaka, G. U., Aju, G. J., Okpa, S., & Inah, I. O. (2020). Antioxidant, anti-inflammatory and anti-apoptotic effects of hydro-ethanolic extract of Cyperus esculentus L. (tigernut) on lead acetate-induced testicular dysfunction in Wistar rats. Biomed Pharmacother., 129:110491. https://doi.org/10.1016/j.biopha.2020.110491. PMID: 32768970.

Ullah, A., Pirzada, M., Jahan, S., Ullah, H., Turi, N., Ullah, W., Siddiqui, M. F., Zakria, M., Lodhi, K. Z., & Khan, M. M. (2018). Impact of low-dose chronic exposure to bisphenol A and its analogue bisphenol B, bisphenol F and bisphenol S on hypothalamo-pituitary-testicular activities in adult rats: A focus on the possible hormonal mode of action. Food Chem Toxicol., 121:24-36. https://doi.org/10.1016/j.fct.2018.08.024. PMID: 30120946.

amasaki, K., Sawaki, M., Noda, S., Imatanaka, N., & Takatsuki, M. (2002). Subacute oral toxicity study of ethynylestradiol and bisphenol A, based on the draft protocol for the 'Enhanced OECD Test Guideline no. 407'. Arch Toxicol., 76:65–74.

Yin, L., Dai, Y., Cui, Z., Jiang, X., Liu, W., Han, F., et al.. (2017). The regulation of cellular apoptosis by the ROS-triggered PERK/EIF2α/chop pathway plays a vital role in bisphenol A-induced male reproductive toxicity. Toxicol Appl Pharmacol., 314:98–108. https://doi.org/10.1016/j.taap.2016.11.013

Yu, Y., Lu, X., Zhang, T., Zhao, C., Guan, S., Pu, Y., & Gao, F. (2022). Tiger Nut (Cyperus esculentus L.): Nutrition, Processing, Function and Applications. Food., 19;11(4):601. https://doi.org/10.3390/foods11040601. PMID: 35206077; PMCID: PMC8871521.

Zhang, S., Li, P., Wei, Z., Cheng, Y, L. J., Yang, Y., Wang, Y., & Mu, Z. (2022). Cyperus (Cyperus esculentus L.): A Review of Its Compositions, Medical Efficacy, Antibacterial Activity and Allelopathic Potentials. Plants (Basel)., 21;11(9):1127. https://doi.org/10.3390/plants11091127. PMID: 35567128; PMCID: PMC9102041.