Sains Malaysiana 49(6)(2020): 1333-1344

http://dx.doi.org/10.17576/jsm-2020-4906-11

Fenitrothion Impaired Sexual Behaviour and Reproductive Performance in Male Sprague-Dawley Rats

(Fenitrotion Menjejaskan Tingkah Laku Seksual dan Prestasi Reproduktif Tikus Jantan Sprague-Dawley)

NUR AFIZAH YUSOFF¹, MAHANEEM MOHAMED², SITI BALKIS BUDIN¹ & IZATUS SHIMA TAIB¹*

¹Biomedical Science Programme, Centre of Diagnostic, Therapeutic and Investigations, Faculty of Health Sciences, Universiti Kebangsaan Malaysia, Jalan Raja Muda Abdul Aziz, 50300 Kuala Lumpur, Federal Territory, Malaysia

²Department of Physiology, School of Medical Sciences, Universiti Sains Malaysia, 16150 Kubang Kerian, Kelantan Darul Naim, Malaysia

Received: 14 August 2019/Accepted: 31 January 2020

ABSTRACT

Fenitrothion (FNT) induces oxidative damage in various organs including male reproductive organ such as testis and sperm; however, its effects on the male sexual behaviours and reproductive performance remain unclear. Therefore, this study aimed to evaluate the effects of FNT administration on male sexual behaviour and reproductive performance. Fertile male Sprague-Dawley rats were randomly divided into three groups (n=8/group): Control - receiving corn oil (1 mL kg^-1); FNT-10 and FNT-20 receiving 10 and 20 mg kg^-1 of FNT, respectively. FNT was administered via oral force feeding for 28 consecutive days prior to mating with untreated female rats. After mating, the rats were sacrificed to obtain plasma and sperm for further evaluation. Results showed that FNT-20 alone decreased AChE activity (P<0.05) compared to the control and FNT-10. Both doses of FNT also decreased sperm quality compared to control (P<0.05). A significant difference was found (P<0.05) for the presence of intromission and ejaculation among all groups. The mount and intromission latencies as well as post-ejaculation interval were increased (P<0.05) in FNT groups compared to the control group. The total mount and mount frequency were decreased (P<0.05) in FNT-10 and FNT-20 compared to the controls group. For reproductive performance, there was a significant difference (P<0.05) for the mating and pregnancy indexes among all groups. Furthermore, both doses of FNT reduced the number of dams, delivered pups and male pups compared to the control (P<0.05). In conclusion, FNT impaired sexual behaviour and reproductive performance of male rats.

Keywords: Infertility; organophosphate; parturition; sexual behaviour; sperm damage

ABSTRAK

Fenitrotion (FNT) mengaruh kerosakan oksidatif dalam pelbagai organ termasuklah organ reproduktif lelaki seperti testis dan sperma; walau bagaimanapun, kesannya terhadap tingkah laku seksual dan prestasi reproduktif masih belum diketahui. Oleh itu, kajian ini bertujuan untuk menilai kesan pemberian FNT terhadap tingkah laku seksual dan prestasi reproduktif. Tikus jantan Sprague-Dawley subur dibahagikan secara rawak kepada tiga kumpulan (n=8/kumpulan): Kawalan - menerima minyak jagung (1 mL kg^-1); FNT-10 dan FNT-20 menerima 10 dan 20 mg kg^-1 FNT, setiap satunya. FNT diberikan secara oral paksa berturutan selama 28 hari sebelum pengawanan dilakukan dengan tikus betina tidak dirawat. Selepas pengawanan, tikus dikorbankan untuk mendapatkan plasma dan sperma bagi penilaian selanjutnya. Keputusan menunjukkan FNT-20 sahaja menurunkan aktiviti AChE (P<0.05) berbanding kumpulan kawalan dan FNT-10. Kedua-dua dos FNT juga menurunkan kualiti sperma berbanding kumpulan kawalan (P<0.05). Terdapat perbezaan signifikan (P<0.05) bagi kehadiran intromisi dan ejakulasi antara semua kumpulan. Latensi pemanjatan dan intromisi serta selang selepas ejakulasi turut meningkat (P<0.05) pada kumpulan FNT berbanding kumpulan kawalan. Sebaliknya, hanya FNT-20 yang menyebabkan pengurangan frekuensi intromisi dan peningkatan latensi ejakulasi berbanding kumpulan kawalan (P<0.05). Jumlah dan frekuensi pemanjatan adalah menurun (P<0.05) pada kumpulan FNT-10 dan FNT-20 berbanding kumpulan kawalan. Bagi prestasi reproduktif, terdapat perbezaan signifikan (P<0.05) pada indeks pengawanan dan kehamilan antara semua kumpulan. Tambahan lagi, kedua-dua dos FNT telah mengurangkan bilangan betina hamil, progeni yang dilahirkan dan progeni jantan berbanding kumpulan kawalan (P<0.05). Kesimpulannya, FNT menjejaskan tingkah laku seksual dan prestasi reproduktif tikus jantan.

Kata kunci: Kelahiran; ketaksuburan; kerosakan sperma; organofosfat; tingkah laku seksual

REFERENCES

Agarwal, A., Mulgund, A., Hamada, A. & Chyatte, M.R. 2015. A unique view on male infertility around the globe. Reproductive Biology and Endocrinology 13: 37-46.

Al-Gubory, K.H. 2014. Environmental pollutants and lifestyle factors induce oxidative     stress and poor prenatal development. Reproductive. BioMedicine Online 29(1): 17-31.

Besong, E.B., Ateufack, G., Babiaka, S.B. & Kamanyi, A. 2018. Leaf-methanolic extract of Pseudopanax arboreus (Araliaceae) (L. F. Phillipson) reverses amitriptyline-induced sexual dysfunction in male rats. Biochemistry Research International 2018: 2869727-2869741.

Budin, S.B., Han, K.J., Jayusman, P.A., Taib, I.S., Ghazali, A.R. & Mohamed, J. 2013. Antioxidant activity of tocotrienol rich fraction prevents fenitrothion-induced renal damage in rats. Journal of Toxicologic Pathology 26(2): 111-118.

Budin, S.B., Saimin, H., Taib, I.S. Jayusman, P.A. & Mohamed, J. 2012. A histological studies of rats’ lung subacutely treated with fenitrothion. International Journal of Collaborative Research on Internal Medicine and Public Health 4: 744­-752.

Cao, J.F., Zhang, P.Z., Xu, C.W., Huang, T.T., Bai, Y.G. & Chen, K.S. 2012. Effect of aqueous extract of Arctium lappa L. (burdock) roots on the sexual behavior of male rats. BMC Complementary and Alternative Medicine 12(1): 1-8.

Čolović, M.B., Krstić, D.Z., Lazarević-Pašti, T.D., Bondžić, A.M. & Vasić, V.M. 2013. Acetylcholinesterase inhibitors: Pharmacology and toxicology. Current Neuropharmacology 11(3): 315-335.

Damalas, C.A. & Koutroubas, S.D. 2016. Farmers’ exposure to pesticides: Toxicity types and ways of prevention. Toxics 4(1): 1-10.

Dasuki, M.S., Emylia, K.Z., Izani, N.N. & Mohsin, S.S.J. 2012. Evaluation of antioxidant and antiproliferative activities on methanolic extract of Smilax myosotiflora tuber. Internal Medicine Journal 19(3): 188-192.

D’Souza, U.J.A. 2017. Pesticide toxicity and oxidative stress: A review. Borneo Journal of Medical Sciences 11(1): 9-19.

Elhalwagy, M.E., Darwish, N.S. & Zaher, E.M. 2008. Prophylactic effect of green tea polyphenols against liver and kidney injury induced by fenitrothion insecticide. Pesticide Biochemistry and Physiology 91(2): 81-89.

Ellman, G.L., Courtney, K.D., Andres Jr., V. & Featherstone, R.M. 1961. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochemical Pharmacology 7(2): 88-95.

Franklin, M.R. & Yost, G.S. 2000. Biotransformation: A balance between bioactivation and detoxification. In Principles of Toxicology Environmental and Industrial Applications, edited by Phillip, R.S. & Willis, L. New Jersey: John Wiley & Sons Inc. pp. 57-59.

Ho, C.C., Singam, P., Hong, G.E. & Zainuddin, Z.M. 2011. Male sexual dysfunction in Asia. Asian Journal of Andrology 13(4): 537-542.

Hull, E.M. & Dominguez, J.M. 2007. Sexual behaviour in male rodents. Hormones and Behavior 52(1): 45-55.

Ito, Y., Tomizawa, M., Suzuki, H., Okamura, A., Ohtani, K., Nunome, M., Noro, Y., Wang, D., Nakajima, T. & Kamijima, M. 2014. Fenitrothion action at the endocannabinoid system leading to spermatotoxicity in Wistar rats. Toxicology and Applied Pharmacology 279(3): 331-337.

Jacobsen, P.R., Axelstad, M., Boberg, J., Isling, L.K., Christiansen, S., Mandrup, K.R., Berthelsen, L.O., Vinggaard, A.M. & Hass, U. 2012. Persistent developmental toxicity in rat offspring after low dose exposure to a mixture of endocrine disrupting pesticides. Reproductive Toxicology 34(2): 237-250.

Jayusman, P.A., Budin, S.B., Ghazali, A.R., Taib, I.S. & Louis, S.R. 2014. Effects of palm oil tocotrienol-rich fraction on biochemical and morphological alterations of liver in fenitrothion-treated rats. Pakistan Journal of Pharmaceutical Sciences 27(6): 1873-1880.

Kaur, R.P., Gupta, V., Christopher, A.F. & Bansal, P. 2015. Potential pathways of pesticide action on erectile function - A contributory factor in male fertility. Asian Pacific Journal of Reproduction 4(4): 322-330.

Kenfack, A., Ngoula, F., Dzeufiet, P.D.W., Ngouateu, O.B., Martine, T.M.A., Chombong, J.K., Zeukeng, G.M.Z., Nyuysemo, I.L., Guiekep, A.J.N., Nain, T.P., Kamtchouing, P., Tchoumboué, J. & Vemo, N.B. 2015. Persistence of the reproductive toxicity of chlorpiryphos-ethyl in male Wistar rat. Asian Pacific Journal of Reproduction 4(1): 37-40.

Kpomah, E.D., Uwakwe, A.A. & Abbey, B.W. 2012. Aphrodisiac studies of diherbal mixture of Zanthoxylum leprieurii guill. & perr. and Piper guineense schumach. & thonn. On male Wistar rats. Global Journal of Research on Medicinal Plants & Indigenous Medicine 1(9): 381-390.

Li, C., Taneda, S., Suzuki, A.K., Furuta, C., Watanabe, G. & Taya, K. 2006. Anti-androgenic activity of 3-methyl-4-nitrophenol in diesel exhaust particles. European Journal of Pharmacology 543(1-3): 194-199.

Lim, J.H., Kim, S.H., Kim, K.H., Park, N.H., Shin, I.S., Moon, C., Park, S.H., Kim, S.H. & Kim, J.C. 2010. Reproductive and developmental toxicity of amitraz in Sprague-Dawley rats. Journal of the Korean Society of Clinical Toxicology 26(1): 67-74.

Lionetto, M.G., Caricato, R., Calisi, A., Giordano, M.E. & Schettino, T. 2013. Acetylcholinesterase as a biomarker in environmental and occupational medicine: New insights and future perspectives. BioMed Research International 2013: 321213-321220.

Lotti, F. & Maggi, M. 2018. Sexual dysfunction and male infertility. Nature Reviews Urology 15(5): 287-307.

Malhat, F.M. 2012. Residues and dissipation of fenitrothion in green bean (Phaseolus vulgaris) and soil. International Scholarly Research Notices 2012: 365317-365320.

Mansour, S.A. & Mossa, A.T.H. 2011. Adverse effects of exposure to low doses of chlorpyrifos in lactating rats. Toxicology and Industrial Health 27(3): 213-224.

Mehrpour, O., Karrari, P., Zamani, N., Tsatsakis, A.M. & Abdollahi, M. 2014. Occupational exposure to pesticides and consequences on male semen and fertility: A review. Toxicology Letters 230(2): 146-156.

Miyake, M., Ito, Y., Suzuki, H., Tomizawa, M., Sato, H., Liu, M., Okamura, A., Nakajima, T., Ohtani, K., Takino, H., Inagaki, H. & Kamijima, M. 2018. Epididymal phospholipidosis is a possible mechanism for spermatotoxicity induced by the organophosphorus insecticide fenitrothion in rats. Toxicology Letters 285: 27-33.

Mohamed, M., Sulaiman, S.A. & Sirajudeen, K.N.S. 2013. Protective effect of honey against cigarette smoke induced-impaired sexual behaviour and fertility of male rats. Toxicology and Industrial Health 29(3): 264-271.

Mor, I., Sklan, E.H., Podoly, E., Pick, M., Kirschner, M., Yogev, L., Bar-Sheshet, I.S., Schreiber, L., Geyer, B. & Mor, T. 2008. Acetylcholinesterase-R increases germ cell apoptosis but enhances sperm motility. Journal of Cellular and Molecular Medicine 12(2): 479-495.

Mor, I., Grisaru, D., Titelbaum, L., Evron, T., Richler, C., Wahrman, J., Sternfeld, M., Yogev, L., Meiri, N., Seidman, S. & Soreq, H. 2001. Modified testicular expression of stress-associated ‘readthrough’ acetylcholinesterase predicts male infertility. Federation of American Societies for Experimental Biology 15(11): 2039-2041.

Mueller, U. 2001. Pesticide residues in food 2000: Fenitrothion. FAO and WHO. http://www.inchem.org/documents/jmpr/jmpmono/v00pr01.htm. Accessed on 10 December 2018.

NIH (National of Health). 1993. National of Health consensus conference. Impotence. NIH consensus development panel on impotence. Journal of the American Medical Association 270: 83-90.

Numan, M. 2015. Neurobiology of Social Behaviour: Toward an Understanding of the Prosocial and Antisocial Brain. 1st Edition. San Diego: Elsevier, Inc.

Pope, C.N. 2006. Central Nervous System Effects and Neurotoxicity. Toxicology of Organophosphate and Carbamate compounds. 1st edition. Georgia: Elsevier, Inc.

Rastrelli, G. & Maggi, M. 2017. Erectile dysfunction in fit and healthy young men: Psychological or pathological? Translational Andrology and Urology 6(1): 79-90.

Seed, J., Chapin, R.E., Clegg, E.D., Dostal, L.A., Foote, R.H., Hurtt, M.E., Klinefelter, G.R., Makris, S.L., Perreault, S.D., Schrader, S., Seyler, D., Sprando, R., Treinen, K.A., Veeramachaneni, D.N. & Wise, L.D. 1996. Methods for assessing sperm motility, morphology, and counts in the rat, rabbit, and dog: A consensus report. ILSI risk science institute expert working group on sperm evaluation. Reproductive Toxicology 10(3): 237-244.

Singh, P., Gupta, R., Patidar, D. & Singh, R.K. 2014. Male infertility: Causes and      contributors. International Journal of Pharmaceutical Sciences and Research 5(6): 2095-2112. 

Swaney, W.T., Dubose, B.N., Curley, J.P. & Champagne, F.A. 2012. Sexual experience affects reproductive behavior and preoptic androgen receptors in male mice. Hormones and Behavior 61(4): 472-478.

Taib, I.S., Budin, S.B., Ghazali, A.R., Jayusman, P.A., Louis, S.R. & Mohamed, J. 2013. Fenitrothion induced oxidative stress and morphological alterations of sperm and testes in male Sprague-dawley rats. Clinics 68(1): 93-100.

Tamura, H., Yoshikawa, H., Gaido, K.W., Ross, S.M., DeLisle, R.K., Welsh, W.J. & Richard, A.M. 2003. Interaction of organophosphate pesticides and related compounds with the androgen receptor. Environmental Health Perspectives 111(4): 545-552.

United Nation Department of Economic and Social Affairs. 2017. World Population Prospects -Revision: Global fertility rate. https://www.un.org/development/desa/publications/graphic/wpp2017globalfertilityrate. Accessed on 21 June 2017.

Uygun, U., Koksel, H. & Atli, A. 2005. Residue levels of malathion and its metabolites and fenitrothion in post-harvest treatment wheat during storage, milling and baking. Food Chemistry 92(4): 643-647.

Wan Yaacob, W.M.H., Norliza, A. & Sulain, M.D. 2013. Aphrodisiac properties of methanolic extract of Smilax myosotiflora tubers in male rats. International Journal of Medical Sciences and Biotechnology 1(2): 41-50.

WHO (World Health Organization). 2008. Fenitrothion in Drinking-Water. Guidelines for Drinking-water Quality. 3rd ed. Geneva.

WHO (World Health Organization). 2014. Sexual and reproductive health: Infertility is a global public health issue. http://www.who.int/reproductivehealth/topics/infertility/perspective/en. Accessed on 1 October 2017.

Yakubu, M.T. & Afolayan, A.J. 2009. Effect of aqueous extract of Bulbine natalensis (Baker) stem on the sexual behaviour of male rats. International Journal of Andrology 32(6): 629-636.

Yasuhara, F., Kempinas, W.G. & Pereira, O.C.M. 2005. Reproductive and sexual behavior changes in male rats exposed perinatally to picrotoxin. Reproductive Toxicology 19(4): 541-546.

Zhang, X.J. & Greenberg, D.S. 2012. Acetylcholinesterase involvement in apoptosis. Frontiers in Molecular Neuroscience 5(2012): 40.

*Corresponding author; email: izatusshima@ukm.edu.my