Chronic consumption of contaminated feed with 2,4-dichlorophenoxyacetic acid (2,4-D) herbicide in rodents: effects on male reproductive health

Authors

DOI:

https://doi.org/10.11606/issn.2176-7262.rmrp.2023.203196

Keywords:

Pesticide exposure , Spermatozoa , Reproduction , Environmental exposure , Rats

Abstract

Introduction: The herbicide 2,4 dichlorophenoxyacetic acid (2,4-D) is one of the most widely used pesticides in the world. There is evidence that this herbicide can induce deleterious effects in non-target organisms, including impairment of reproduction function. Objective: The aim of this study was to evaluate the reproductive effects of
the chronic consumption of contaminated feed with 2,4-D in rats using food environmental spraying simulation. Methods: Animals orally exposed received nebulized chow with 2,4-D solution in different concentrations for 180 days: 0 (control - CG), 20.69 (LCG), 34.63 (MCG), or 51.66 ppm day−1 (HCG). Results: Sperm quality was impaired to 2,4-D. The percentage of sperm with progressive movement, number of sperm in the testis and daily sperm production were decreased in all exposed groups to the herbicide compared to CG. Sperm counts in the
caput/corpus and cauda epididymis were reduced in MCG and HCG, and sperm transit time was delayed in the epididymis of LCG. There was a negative impact on sperm morphology and plasma membrane integrity in MCG and HCG, respectively. Germ cell exfoliation within the lumen of the seminiferous tubules and epithelial vacuolization in epididymis were found in the HCG. Conclusion: This is the first study to describe the negative impact on male reproductive morphophysiology after chronic exposure to 2,4-D using food nebulization in environmentally relevant concentrations, based on agronomic use of the herbicide. The reproductive injuries identified raise concerns about the impacts of wide population exposure to 2,4-D.

 

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Author Biographies

  • Jamile Silveira Tomizzi Simões, Universidade do Oeste Paulista, Presidente Prudente, (SP), Brazil.

    Mestre e Doutoranda

  • Douglas Gonçalves, Universidade do Oeste Paulista, Presidente Prudente, (SP), Brazil.

    Biólogo

  • Gisele Alborghetti Nai, Universidade do Oeste Paulista, Presidente Prudente, (SP), Brazil

    Docente do Programa de Pós-Graduação em Ciência Animal

  • Renata Calciolari Rossi, Universidade do Oeste Paulista, Presidente Prudente, (SP), Brazil

    Docente do Programa de Pós-Graduação em Meio Ambiente e Desenvolvimento Regional

  • Ana Paula Alves Favareto, Universidade do Oeste Paulista, Presidente Prudente, (SP), Brazil.

    Docente do Programa de Pós-Graduação em Meio Ambiente e Desenvolvimento Regional

References

FAO. World agriculture: towards 2030/2050 – Interim report. Rome. 2006. (http://www.fao.org/fileadmin/user_upload/esag/docs/Interim_report_AT2050web.pdf)

Parfitt J, Barthel M, Macnaughton S. Food waste within food supply chains: quantification and potential for change to 2050. Philos Trans R Soc Lond B Biol Sci 2010;365(1554):3065-81. https://doi.org/10.1098/rstb.2010.0126.

McLaughlin D, Kinzelbach W. Food security and sustainable resource management. Water Resour Res.. 2015;51(7):4966-4985. https://doi.org/10.1002/2015WR017053

Song Y. Insight into the mode of action of 2, 4-dichlorophenoxyacetic acid (2, 4-D) as an herbicide. J Integr Plant Biol 2014;56:106–113. https://doi.org/10.1111/jipb.12131.

IARC – INTERNATIONAL AGENCY FOR RESEARCH ON CANCER. DDT, Lindane, and 2,4-D. IARC. Lyon (FR): IARC, 2018 (IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, nº 113) https://monographs.iarc.who.int/wp-content/uploads/2018/07/mono113.pdf Accessed May 2021.

Islam F, Wang J, Farooq MA, Khan MSS, Xu L, Zhu J, Zhao M, Muños S, Li QX, Zhou W. Potential impact of the herbicide 2,4-dichlorophenoxyacetic acid on human and ecosystems. Environ Int. 2018;111:332-351. https://doi.org/10.1016/j.envint.2017.10.020.

de Oliveira Mantovani R, Pinheiro DG, De Oliveira GLF, Perrud SN, Teixeira GR, Nai GA, Veras ASC, de Almeida Tavares ME, de Oliveira Mendes L, Pacagnelli FL. Effect of different doses of 2,4-dichlorophenoxyacetic acid (2,4-D) on cardiac parameters in male Wistar rats. Environ Sci Pollut Res Int. 2021; 28(3):3078-3087. https://doi.org/ 10.1007/s11356-020-10699-y.

Rocha DR, Nery JF, Furini LN, Constantino CJL, Eller LKW, Nai GA, Nakagaki WR. Effects of consumption of contaminated feed with 2,4-dichlorophenoxyacetic acid (2,4-D) on the rat tibia: analysis by Raman spectroscopy and mechanical properties. Lasers Med Sci. 2020;35(8):1703-1709. https://doi.org/ 10.1007/s10103-020-02961-z.

Parizi JLS, de Mello Odorizzi GAS, Sato GMRH, Patrão IB, Nai GA. Oral mucosa changes associated with chronic oral and inhalation exposure to 2,4-dichlorophenoxiacetic acid (2,4-D) in Wistar rats. Toxicol Res (Camb). 2020;24;9(6):746-757. https://doi.org/10.1093/toxres/tfaa085.

Garabrant DH, Philbert MA. Review of 2,4-dichlorophenoxyacetic acid (2,4-D) epidemiology and toxicology.Crit Rev Toxicol. 2002;32(4):233-57. https://doi.org/10.1080/20024091064237.

Guerrero-Bosagna, C., Savenkova, M., Haque, M.M., Nilsson, E., Skinner, M.K. Environmentally induced epigenetic transgenerational inheritance of altered Sertoli cell transcriptome and epigenome: molecular etiology of male infertility. PLoS One. 2013;8, e59922. https://doi.org/ 10.1371/journal.pone.0059922.

Harada Y, Tanaka N, Ichikawa M, Kamijo Y, Sugiyama E, Gonzalez FJ, Aoyama T. PPARalpha-dependent cholesterol/testosterone disruptionin Leydig cells mediates 2,4-dichlorophenoxyacetic acid-induced testicular toxicity in mice. Arch Toxicol. 2016;90(12):3061-3071. https://doi.org/10.1007/s00204-016-1669-z.

Mello FA, Quinallia G, Marion AL, Jorge FC, Marinelli LM, Salge AKM, Fagiani MAB, Mareco EA, Favareto APA, Silva RCR. Evaluation of the nasal cavity mice submitted to the inhalation exposure to the herbicide 2,4-dichlorophenoxyacetic acid, Medicina (Ribeirão Preto, Online). 2018;51:247-253. https://doi.org/10.11606/issn.2176-7262.v51i4p247-253

Perobelli JE, Alves TR, de Toledo FC, Fernandez CDB, Anselmo-Franci JA, Klinefelter GR, Kempinas WDG. Impairment on sperm quality and fertility of adult rats after antiandrogen exposure during prepuberty. Reprod Toxicol. 2012; 33:308–315. https://doi.org/10.1016/j.reprotox.202011.12.011

Seed J, Chapin RE, Clegg ED, Dostal LA, Foote RH, Hurtt ME, Klinefelter GR, Makris SL, Perreault SD, Schrader S, Seyler D, Sprando R, Treinen KA, Veeramachaneni DN, Wise LD. 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. Reprod Toxicol. 1996;10(3):237–244. https://doi.org/10.1016/0890-6238(96)00028-7

Filler R. Methods for evaluation of rat epididymal sperm morphology. In: Chapin RE, Heindel JH (eds) Methods in toxicology: male reproductive toxicology. Academic Press, San Diego, 1993;pp 334–343.

WHO. Laboratory manual for the examination of human semen and sperm-cervical mucus interaction, 4th edn. Cambridge University Press, United Kingdom. 128p. https://www.aab.org/images/WHO%204th%20manual.pdf. 1999. Accessed May 2019.

Robb GW, Amann RP, Killian GJ. Daily sperm production and epididymal sperm reserves of pubertal and adult rats. J Reprod Fertil. 1978;54(1):103–107. https://doi.org/10.1530/jrf.0.0540103

Fernandes GS, Arena AC, Fernandez CD, Mercadante A, Barbisan LF, Kempinas WG. Reproductive effects in male rats exposed to diuron. Reprod Toxicol. 2007;23(1):106–112. https://doi.org/10.1016/j.reprotox.2006.09.002

Kempinas, WDG, Klinefelter GR. Interpreting histopathology in the epididymis. Spermatogenesis. 2014;4(2)1-12https://doi.org/ 10.4161/21565562.2014.979114.

Grant J, Hoorens S, Sivadasan S, Loo MV, Davanzo J, Hale L, Butz W. Trends in European fertility: should Europe try to increase its fertility rate...or just manage the consequences? Int J Androl. 2006;29:17–24. https://doi.org/10.1111/j.1365-2605.2005.00634.x.

Cooper TG, Noonan E, von Eckardstein S, Auger J, Baker HW, Behre HM, et al. World Health Organization reference values for human semen characteristics. Hum Reprod Update. 2010;16(3):231-245. https://doi.org/10.1093/humupd/dmp048.

Rolland M, LeMoal J, Wagner V, Royère D, De Mouzon J. Decline in semen concentration and morphology in a sample of 26,609 men close to general population between 1989 and 2005 in France. Hum Reprod. 2013;28(2):462–470. https://doi.org/10.1093/humrep/des415.

Mann U, Shiff B, Patel P. Reasons for worldwide decline in male fertility. Curr Opin Urol. 2020;30(3):296-301. https://doi.org/10.1097/MOU.0000000000000745.

Marouani N, Tebourbi O, Cherif D, Hallegue D, Yacoubi MT, Sakly M, Benkhalifa M, Ben Rhouma K. Effects of oral administration of 2,4-dichlorophenoxyacetic acid (2,4-D) on reproductive parameters in male Wistar rats. Environ Sci Pollut Res Int. 2017;4(1):519-526. https://doi.org/10.1007/s11356-016-7656-3.

Joshi SC, Tibrewall P, Sharma A, Sharma P. Evaluation of toxic effect of 2,4-D (2,4-Dichlorophenoxyacetic acid) on fertility and biochemical parameters of male reproductive system of albino rats. Int J Pharm Pharm Sci. 2021;4(3)338-342.

Prins SG, Birch L, Greene GL. Androgen receptor localization in different cell types of the adult rat prostate. Endocrinology 1991;129:3187–3199. https://doi.org/ 10.1210/endo-129-6-3187.

Davies KJ. Adaptive homeostasis. Mol Aspects Med. 2016;49:1-7. https://doi.org/10.1016/j.mam.2016.04.007.

Tuschl H, Schwab C. Cytotoxic effects of the herbicide 2, 4dichlorophenoxyacetic acid in HepG2 cells. Food Chem Tox. 2003;41(3)385–393. https://doi.org/10.1016/s0278-6915(02)00238-7.

Zhang X, Cui W, Wang K, Chen R, Chen M, Lan K, Wei Y, Pan C, Lan X. Chlorpyrifos inhibits sperm maturation and induces a decrease in mouse male fertility. Environ Res. 2020;188:109785. https://doi.org/ 10.1016/j.envres.2020.109785.

Tan Z, Zhou J, Chen H, Zou Q, Weng S, Luo T, Tang Y. Toxic effects of 2,4-dichlorophenoxyacetic acid on human sperm function in vitro. J Toxicol Sci 2016;41(4):543-9. https://doi.org/10.2131/jts.41.543.

Lerda D, Rizzi R. Study of reproductive function in persons occupationally exposed to 2,4-dichlorophenoxyacetic acid (2,4-D). Mutat Res. 1991;262:47–50. https://doi.org/10.1016/0165-7992(91)90105-d.

Cosentino MJ, Cockett ATK. Structure and function of the epididymis. Urol Res. 1986;14:229-240. https://doi.org/10.1007/BF00256565.

Mathias FT. Estudo do efeito das nanopartículas de sais de prata sobre parâmetros reprodutivos e funcionais espermáticos em ratos Wistar. Guarapuava: Unicentro; 2013. 93f.

Altoé L S , Reis I B, Gomes Mlm, Dolder H, Monteiro Pirovani Jc. Could vitamin C and zinc chloride protect the germ cells against sodium arsenite? Hum Exp Toxicol. 2017; 36(10):1049-1058. https://doi.org/10.1177/0960327116679714.

Kempinas WD, Suarez JD, Roberts NL, Strader LF, Ferrell J, Goldman JM, Narotsky MG, Perreault SD, Evenson DP, Ricker DD, Klinefelter GR. Fertility of rat epididymal sperm after chemically and surgically induced sympathectomy. Biol Reprod. 1998;59(4):897-904. https://doi.org/10.1095/biolreprod59.4.897.

Zhang D, Wu Y, Yuan Y, Liu W, Kuang H, Yang J, Yang B, Wu L, Zou W, Xu C. Exposure to 2,4-dichlorophenoxyacetic acid induces oxidative stress and apoptosis in mouse testis. Pestic Biochem Physiol. 2017;141:18-22. https://doi.org/10.1016/j.pestbp.2016.10.006.

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Published

2023-08-15

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Original Articles

How to Cite

1.
Simões JST, Gonçalves D, Nai GA, Rossi RC, Favareto APA. Chronic consumption of contaminated feed with 2,4-dichlorophenoxyacetic acid (2,4-D) herbicide in rodents: effects on male reproductive health. Medicina (Ribeirão Preto) [Internet]. 2023 Aug. 15 [cited 2024 Jun. 1];56(2):e-203196. Available from: https://www.periodicos.usp.br/rmrp/article/view/203196