An investigation on some toxic effects of pyriproxyfen in adult male mice

Document Type : Original Article

Authors

1 Department of Zoology, Government College University, Katchery Road, Lahore, Pakistan

2 Department of Parasitology, University of Veterinary and Animal Sciences, Lahore, Pakistan

Abstract

Objective(s): Pyriproxyfen as an insect growth regulator is widely used globally for pest management. There are reports on adverse effects of insecticides such as organ toxicity, endocrine disruptions, and teratogenicity in animals and humans. We aimed to investigate reproductive toxicity of pyriproxyfen in adult male mice.
Materials and Methods: 48 male Swiss albino mice were divided into eight groups and received the different 1200, 600, 320, 200, 100, 40, 20, 0 mg/kg/day doses orally, and body weights were accessed for 28 consecutive days. In the end, mice were sacrificed, testes were dissected and weighed. Probable testicular tissue alterations were examined by histopathological studies. In addition, the diameter of seminiferous tubules and Leydig cells distribution were assessed in all experimental and control groups.
Results: Pyriproxyfen treatment caused significant (P<0.05) reduction in body and organ weights in mice. However, the shrinkage and displacement of seminiferous tubules, reduced lumen diameter, and vacuolization occurred in seminiferous tubules in higher doses exposed animals in comparison to controls. The relative testis weights, mean diameter of seminiferous tubules, and Leydig cells distribution remained unchanged at low doses.
Conclusion: These findings reveal that pyriproxyfen caused reduction in body weight gain as well as damage to the testicular architecture in mice and thus may potentially interfere with spermatogenesis. Findings in an outbred strain of mice can be extrapolated fairly reliably to the human model. The chemical can thus be further exploited to study its effects on impairment of fertility and as an endocrine disruptor.

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1.Eddleston M, Karalliedde L, Buckley N, Fernando R, Hutchinson G, Isbister G, et al. Pesticide poisoning in the developing world-A minimum pesticides list. Lancet 2002; 360:1163-1167.
2.Ferrer A. Pesticide poisoning. An Sist Sanit Navar 2003; 26:155-171.
3.PAN-UK. Pesticide Action Network UK. http://www.panuk.org. 2009.
4.Uggini GK, Patel PV, Balakrishnan S. Embryotoxic and teratogenic effects of pesticides in chick embryo: a comparative study using two commercial formulations. Environ Toxicol 2010; 27:166-174.
5.Yang CC, Deng JF. Intermediate syndrome following organophosphate insecticide poisoning. J Chin Med Assoc 2007; 70:467-472.
6.Gangola S, Khati P, Sharma A. Mycoremediation of Imidaclopridin the Presence of Different Soil Amendments using Trichoderma longibrachiatum and Aspergillus oryzae Isolated from Pesticide Contaminated Agricultural fields of Uttarakhand. J Bioremediat Biodegrad 2015; 6:1-5.
7.Tunaz H, Uygun N. Insect growth regulators for insect pest control. Turk J Agric For 2004; 28:377-387.
8.Dhadialla TS, Carlson GR, Le DP. New insecticides with ecdysteroidal and juvenile hormone activity. Annu Rev Entomol 1998; 43:545-569.
9.World Health Organization (WHO). Global assessment of the state-of-the-science of endocrine disruptors. International Program on Chemical Safety. 2002.
10.Tomlin C. The Pesticide Manual. 14th ed. BCPC Publications Berkshire UK; 2006.p. 923-924.
11.World Health Organization (WHO): Pesticides and their application for the control of vectors and pests of public health importance, 6th ed. Geneva, World Health Organization, Department of Control of Neglected Tropical Diseases, Pesticide Evaluation Scheme, (2006).(WHO/CDS/NTD/WHOPES/GCDPP/2006.1;http://whqlibdoc.who.int/hq/2006/WHO_CDS_NTD_WHOPES_GCDPP_2006.1_eng.pdf (verified 23 September 2008).
12.Mehrnoush G, Mehrdad S, Saeid K. Effect of pyriproxyfen on function and tissue of testis in adult rat. Int J Curr Res Rev 2013; 5:66-74.
13.Evans D, Nijhout F, Parens R, Morales AJ, Bar-Yam Y. A possible link between pyriproxyfen and microcephaly. arXiv preprint arXiv:1604.03834. 2016.
14.Bergstrom R, Adami HO, Möhner M, Zatonski W, Storm H, Ekbom A, et al. Increase in testicular cancer incidence in six European countries: A birth cohort phenomenon. J Natl Cancer Inst 1996; 88:727-733.
15.Moller H. Trends in incidence of testicular cancer and prostate cancer in Denmark. Hum Reprod 2001; 16:1007-1011.
16.Sekhar PR, Savithri Y, Kishore S, Jayasankar A, Rao KJ. Synergistic effect of sodium fluoride and cypermethrin on the somatic index and histopathology of albino mice testes. Fluoride 2011; 44:103-111.
17.Slaoui M, Fiette L. Histopathology procedures: from tissue sampling to histopathological evaluation. Methods Mol Biol. 2011; 691:69-82.
18.Wheater PR, Burkitt HG, Daniels VG. Functional Histology: Text and Colour Atlas. 2nd ed. Churchill Livingstone, New York; 1979.
19.Vendramini V, Sasso-Cerri E, Miraglia SM. Amifostine reduces the seminiferous epithelium damage in doxorubicin-treated prepubertal rats without improving the fertility status. Reprod Biol Endocrinol 2010; 8:1-13.
20. Srinivasa J, Maxim P, Urban J, D’Souza A. Effects of pesticides on male reproductive functions. Iran J Med Sci 2015; 30:153-159.
21.Crissman JW, Goodman DG, Hildebrandt PK, Maronpot RR, Prater DA, Riley JH, et al. Best practices guideline: toxicologic histopathology. Toxicol Pathol 2004; 32:126-131.
22.Heikal TM, Ghanem HZ, Soliman MS. Protective effect of green tea extracts against dimethoate induced DNA damage and oxidant/antioxidant status in male rats. Biohealth Sci Bull 2011; 3:1-11.
23.Choi SM, Lee BM. An alternative mode of action of endocrine disrupting chemicals and chemoprevention. J Toxicol Environ Health 2004; 7:451-463.
24.Ngoula F, Watcho P, Kenfack A, Manga JN, Defang HF, Pierre K, et al. Effect of dimethoate (an organophosphate insecticide) on the reproductive system and fertility of adult male rat. Am J Pharmacol Toxicol 2014; 9:75-83.
25.Espinoza-Navarro O, Bustos-Obregón E. Effects of Malathion on Cellularity and Sperm Differentiation in Testis and Epididymis of Adult Rats. Int J Morphol 2014; 32:119-124.
26.Patrick-Iwuanyanwu KC, Udowelle NA, Okereke CJ. Testicular toxicity and sperm quality following exposure to Solignum®: A Permethrin-containing wood preservative in adult male Wistar rats. J Interdiscipl Histopathol 2016; 4:13-16.
27.Babazadeh M, Najafi G. Effect of chlorpyrifos on sperm characteristics and testicular tissue changes in adult male rats. Vet Res Forum 2017; 8:319-326.
28.Barros AL, Cavalheiro GF, Souza AV, Traesel GK, Anselmo-Franci JA,  Kassuya CA, et al. Subacute toxicity assessment of diflubenzuron, an insect growth regulator, in adult male rats. Environ Toxicol 2014; 31:407-414.
29.Mohafrash SMM, Abdel-Hamid HF, Mossa ATH. Adverse Effects of Sixty Days Sub-chronic Exposure to β-cyfluthrin on Male Rats. J Environ Sci Technol 2017; 10:1-12.
30.Omotoso GO, Onanuga IO, Ibrahim RB. Histological effects of permethrin insecticide on the testis of adult wistar rats. Ibnosina J Med Biomed Sci 2014; 6:125-129.
31.Sanchez-Pena LC, Reyes BE, Lopez-Carrillo L, Recio R, Morán-Martınez J, Cebrian ME, et al. Organophosphorous pesticide exposure alters sperm chromatin structure in Mexican agricultural workers. Toxicol Appl Pharmacol 2004; 196:108-113.
32.Creasy DM. Pathogenesis of male reproductive toxicity. Toxicol Pathol 2001; 29:64-76.
33.Lanning LL, Creasy DM, Chapin RE, Mann PC, Barlow NJ, Regan KS, et al. Recommended approaches for the evaluation of testicular and epididymal toxicity. Toxicol Pathol 2002; 30:507-20.
34.Amann RP. Use of animal models for detecting specific alterations in reproduction. Toxicol Sci 1982; 2:13-26.
35.Sakr SA,  Azab AE. Effect of pyrethroid inhalation on the testis of albino rat. Pak J Biol Sci 2001; 4:498-500.
36.Joshi SC, Mathur R, Gulati N. Testicular toxicity of chlorpyrifos (an organophosphate pesticide) in albino rat. Toxicol Ind Health 2007; 23:439-444.
37.El-Kashoury AA, El-Din HA. Chlorpyrifos (from different source): Effect on testicular biochemistry of male Albino rats. J American Sci 2010; 6:252-261.
38.Al‐Sarar AS, Abobakr Y, Bayoumi AE, Hussein HI, Al‐Ghothemi M. Reproductive toxicity and histopathological changes induced by lambda‐cyhalothrin in male mice. Environ Toxicol 2014; 29:750-62.
39.Lebaili N, Saadi L, Mosbah R, Mechri N. Exploration of the cytotoxic effects of an insecticide, lambda cyhalothrin, on sexual exocrine function in the white rat. Commun Agric Appl Biol Sci 2008; 73:883-889.
40.Fattahi E, Parivar K, Jorsaraei SGA, Moghadamnia AA. The effects of diazinon on testosterone, FSH and LH levels and testicular tissue in mice.  Iran J Reprod Med Medicine 2009; 7:59-64.
41.Taib IS, Budin SB, Ghazali AR, Jayusman PA, Louis SR, Mohamed J. Fenitrothion induced oxidative stress and morphological alterations of sperm and testes in male sprague-dawley rats. Clinics 2013; 68:93-100.
42.Najafi G, Razi M, Hoshyar A, Shahmohamadloo S, Feyzi S. The effect of chronic exposure with imidacloprid insecticide on fertility in mature male rats. Int J Fertil Steril 2010; 4:9-16.
43.Huang LG, Lin P, Gong CY, Zhang J, Zhou Q, Gong XD, Zeng L. Pathological changes in the testes of the rats with hypospadia induced by dichlorvos. Zhonghua nan ke xue= National journal of andrology 2006; 12:693-695.
44.Farag AT, El-Aswad AF, Shaaban NA. Assessment of reproductive toxicity of orally administered dimethoate in male mice. Reprod Toxicol 2007; 23:232-238.
45.Sayim F. Histopathologic effects of dimethoate on testis in rats. Bull Environ Contam Toxicol 2007; 78:479-484.
46.Choudhary N, Goyal R, Joshi SC. Effect of malathion on reproductive system of male rats. J Environ Biol 2008; 29:259-262.
47.Verma R, Mohanty B. Early-life exposure to dimethoate-induced reproductive toxicity: evaluation of effects on pituitary-testicular axis of mice. Toxicol Sci 2009; 112:450-458.
48.Adamkovicova M, Toman R, Cabaj M, Massanyi P, Martiniakova M, Omelka R, et al. Effects of subchronic exposure to cadmium and diazinon on testis and epididymis in rats. Scientific World Journal 2014; 2014:1-9.