Journal of Ethnopharmacology and Toxicology, Volume 1, Issue 1 : 6-12. Doi : 10.37446/jet/ra/1.1.2023.6-12
Review Article

OPEN ACCESS | Published on : 31-Dec-2023

Pesticides as an ovarian toxicant: a short review

  • Ichrak Khaled
  • Laboratory of Biotechnology and Biomonitoring of the Environment and Oasis Ecosystems (LBBEEO), University of Gafsa, Gafsa, Tunisia.
  • Issam Saidi
  • Laboratory of Biotechnology and Biomonitoring of the Environment and Oasis Ecosystems (LBBEEO), University of Gafsa, Gafsa, Tunisia.

Abstract

Pesticides are extensively used in controlling agricultural pests. Pesticide exposure of a variety of populations manifests an array of adverse effects and a large number of studies have shown that pesticides are extremely toxic to female reproductive systems. It has been reported that these pollutants induce oxidative stress, apoptosis, endocrine disorders, and epigenetic alterations, which are directly implicated in the declining fertility of females in non-target species. The literature and information present in this review highlighted the toxic effects of pesticides on the female reproductive system along with their possible mechanisms in ovarian tissue.

Keywords

pesticides, female, oxidative stress, apoptosis, endocrine, epigenetic

References

  • Agarwal, A., Aponte-Mellado, A., Premkumar, B. J., Shaman, A., & Gupta, S. (2012). The effects of oxidative stress on female reproduction: a review. Reproductive biology and endocrinology10, 1-31.

    Andersen, H. R., David, A., Freire, C., Fernández, M. F., d'Cruz, S. C., Reina-Pérez, I., & Blaha, L. (2022). Pyrethroids and developmental neurotoxicity-A critical review of epidemiological studies and supporting mechanistic evidence. Environmental Research, 113935.

    Arab, S. A., Nikravesh, M. R., Jalali, M., & Fazel, A. (2018). Evaluation of oxidative stress indices after exposure to malathion and protective effects of ascorbic acid in ovarian tissue of adult female rats. Electronic physician, 10(5), 6789.

    Arif, A., Quds, R., & Mahmood, R. (2021). Bioallethrin enhances generation of ROS, damages DNA, impairs the redox system and causes mitochondrial dysfunction in human lymphocytes. Scientific Reports, 11(1), 8300.

    Bhardwaj, J. K., Mittal, M., Saraf, P., & Kumari, P. (2020). Pesticides induced oxidative stress and female infertility: a review. Toxin Reviews, 39(1), 1-13.

    Bretveld, R. W., Thomas, C. M., Scheepers, P. T., Zielhuis, G. A., & Roeleveld, N. (2006). Pesticide exposure: the hormonal function of the female reproductive system disrupted?. Reproductive Biology and Endocrinology, 4, 1-14.

    Caron-Beaudoin, É., Viau, R., & Sanderson, J. T. (2018). Effects of neonicotinoid pesticides on promoter-specific aromatase (CYP19) expression in Hs578t breast cancer cells and the role of the VEGF pathway. Environmental Health Perspectives, 126(4), 047014.

    Combarnous, Y. (2017). Endocrine Disruptor Compounds (EDCs) and agriculture: The case of pesticides. Comptes rendus biologies, 340(9-10), 406-409.

    De Rosa, E., Montuori, P., Triassi, M., Masucci, A., & Nardone, A. (2022). Occurrence and Distribution of Persistent Organic Pollutants (POPs) from Sele River, Southern Italy: Analysis of Polychlorinated Biphenyls and Organochlorine Pesticides in a Water–Sediment System. Toxics, 10(11), 662.

    Dupont, C., Armant, D. R., & Brenner, C. A. (2009). Epigenetics: definition, mechanisms and clinical perspective. In Seminars in Reproductive Medicine, 27, 351-357.

    Fakai, M. I., Abd Malek, S. N., & Karsani, S. A. (2019). Induction of apoptosis by chalepin through phosphatidylserine externalisations and DNA fragmentation in breast cancer cells (MCF7). Life sciences, 220, 186-193.

    Gajendiran, A., & Abraham, J. (2018). An overview of pyrethroid insecticides. Frontiers in Biology, 13, 79-90.

    Gerunova, L. K., Bardina, E. G., Gerunov, T. V., & Sechkina, I. V. (2019, August). Pesticides as endocrine disruptors and neurotoxicants. In IOP Conference Series: Earth and Environmental Science, 315, 052049.

    Gore, A. C. (2016). Endocrine-disrupting chemicals. JAMA internal medicine, 176(11), 1705-1706.

    He, Q. K., Xu, C. L., Li, Y. P., Xu, Z. R., Luo, Y. S., Zhao, S. C., ... & Liu, Y. (2022). Captan exposure disrupts ovarian homeostasis and affects oocytes quality via mitochondrial dysfunction induced apoptosis. Chemosphere286, 131625.

    Iwuozor, K. O., Emenike, E. C., Gbadamosi, F. A., Ighalo, J. O., Umenweke, G. C., Iwuchukwu, F. U., ... & Igwegbe, C. A. (2023). Adsorption of organophosphate pesticides from aqueous solution: a review of recent advances. International Journal of Environmental Science and Technology, 20(5), 5845-5894.

    Jain, D., Verma, R. K., Sharma, V., Kaur, A., Rai, A. R., Kumari, P., & Parihar, K. (2023). Associations between high levels pesticide and adverse reproductive outcomes in females: A comprehensive review. Materials Today: Proceedings.

    Jallouli, M., Dhouib, I. E. B., Dhouib, H., Gharbi, N., & El Fazaa, S. (2015). Effects of dimethoate in male mice reproductive parameters. Regulatory toxicology and pharmacology73(3), 853-858.

    Kara, M., & Öztaş, E. (2020). Reproductive toxicity of insecticides. Animal Reproduction in Veterinary Medicine, 237-245.

    Kubsad, D., Nilsson, E. E., King, S. E., Sadler-Riggleman, I., Beck, D., & Skinner, M. K. (2019). Assessment of glyphosate induced epigenetic transgenerational inheritance of pathologies and sperm epimutations: generational toxicology. Scientific reports, 9(1), 6372.

    Lemaire, G., Mnif, W., Mauvais, P., Balaguer, P., & Rahmani, R. (2006). Activation of α-and β-estrogen receptors by persistent pesticides in reporter cell lines. Life sciences, 79(12), 1160-1169.

    Liu, K., Li, Y., Iqbal, M., Tang, Z., & Zhang, H. (2022). Thiram exposure in environment: A critical review on cytotoxicity. Chemosphere, 295, 133928.

    Manikkam, M., Haque, M. M., Guerrero-Bosagna, C., Nilsson, E. E., & Skinner, M. K. (2014). Pesticide methoxychlor promotes the epigenetic transgenerational inheritance of adult-onset disease through the female germline. PloS one, 9(7), e102091.

    Marettova, E., Maretta, M., & Legáth, J. (2017). Effect of pyrethroids on female genital system. Review. Animal reproduction science, 184, 132-138.

    Mizushima, N. (2007). Autophagy: process and function. Genes & development, 21(22), 2861-2873.

    Mossa, A. T. H., Refaie, A. A., Ramadan, A., & Bouajila, J. (2013). Amelioration of prallethrin-induced oxidative stress and hepatotoxicity in rat by the administration of Origanum majorana essential oil. BioMed research international, 2013.

    Muñoz-Quezada, M. T., Lucero, B. A., Gutiérrez-Jara, J. P., Buralli, R. J., Zúñiga-Venegas, L., Muñoz, M. P., ... & Iglesias, V. (2020). Longitudinal exposure to pyrethroids (3-PBA and trans-DCCA) and 2, 4-D herbicide in rural schoolchildren of Maule region, Chile. Science of the Total Environment749, 141512.

    Muranli, F. D. G. (2013). Genotoxic and cytotoxic evaluation of pyrethroid insecticides λ-cyhalothrin and α-cypermethrin on human blood lymphocyte culture. Bulletin of environmental contamination and toxicology90, 357-363.

    Nilsson, E., Larsen, G., Manikkam, M., Guerrero-Bosagna, C., Savenkova, M. I., & Skinner, M. K. (2012). Environmentally induced epigenetic transgenerational inheritance of ovarian disease. PloS one, 7(5), e36129.

    Prasad, S., Tiwari, M., Pandey, A. N., Shrivastav, T. G., & Chaube, S. K. (2016). Impact of stress on oocyte quality and reproductive outcome. Journal of biomedical science, 23, 1-5.

    Qi, S. Y., Xu, X. L., Ma, W. Z., Deng, S. L., Lian, Z. X., & Yu, K. (2022). Effects of organochlorine pesticide residues in maternal body on infants. Frontiers in Endocrinology, 13, 890307.

    Ravula, A. R., & Yenugu, S. (2021). Pyrethroid based pesticides–chemical and biological aspects. Critical Reviews in Toxicology, 51(2), 117-140.

    Sadowska-Woda, I., Wójcik, N., Karowicz-Bilińska, A., & Bieszczad-Bedrejczuk, E. (2010). Effect of selected antioxidants in β-cyfluthrin-induced oxidative stress in human erythrocytes in vitro. Toxicology in Vitro, 24(3), 879-884.

    Shah, H. K., Sharma, T., & Banerjee, B. D. (2020). Organochlorine pesticides induce inflammation, ROS production, and DNA damage in human epithelial ovary cells: An in vitro study. Chemosphere, 246, 125691.

    Sharma, D., & Sangha, G. K. (2018). Antioxidative effects of aqueous extract of broccoli sprouts against Triazophos induced hepatic and renal toxicity in female Wistar rats. Journal of Applied Biomedicine16(2), 100-110.

    Sharma, D., Kumari, S., Rani, P., Onteru, S. K., Roy, P., Tyagi, R. K., ... & Singh, D. (2021). Organochlorine pesticide dieldrin upregulate proximal promoter (PII) driven CYP19A1 gene expression and increases estrogen production in granulosa cells. Reproductive Toxicology, 106, 103-108.

    Sharma, D., Sangha, G. K., & Khera, K. S. (2015). Triazophos-induced oxidative stress and histomorphological changes in ovary of female Wistar rats. Pesticide biochemistry and physiology, 117, 9-18.

    Sharma, R.K., Chauhan, P.K. and Fulia, A. (2011). Vitamin E: anantioxidant therapy to protect endosulphan induced follicular toxicity. International journal of pharmacology, 7, 821–828.

    Sifakis, S., Androutsopoulos, V. P., Tsatsakis, A. M., & Spandidos, D. A. (2017). Human exposure to endocrine disrupting chemicals: effects on the male and female reproductive systems. Environmental toxicology and pharmacology, 51, 56-70.

    Slimani, S., Hamouda, S., Souadi, C., Silini, S., Abdennour, C., & Delimi, L. (2018). The fungicide thiram may disrupt reproductive cycle of domestic male pigeon (Columba livia domestica) subjected to a long photoperiod. Pakistan J. Zool50(5), 1693-1701.

    Song, J., Ma, X., Li, F., & Liu, J. (2022). Exposure to multiple pyrethroid insecticides affects ovarian follicular development via modifying microRNA expression. Science of The Total Environment, 828, 154384.

    Taxvig, C., Hadrup, N., Boberg, J., Axelstad, M., Bossi, R., Bonefeld-Jørgensen, E. C., & Vinggaard, A. M. (2013). In vitro-in vivo correlations for endocrine activity of a mixture of currently used pesticides. Toxicology and applied pharmacology, 272(3), 757-766.

    Terayama, H., Sakabe, K., Kiyoshima, D., Qu, N., Sato, T., Suyama, K., ... & Mori, C. (2022). Effect of neonicotinoid pesticides on Japanese water systems: Review with focus on reproductive toxicity. International Journal of Molecular Sciences, 23(19), 11567.

    Tiemann, U. (2008). In vivo and in vitro effects of the organochlorine pesticides DDT, TCPM, methoxychlor, and lindane on the female reproductive tract of mammals: a review. Reproductive Toxicology, 25(3), 316-326.

    Voss, A. K., & Strasser, A. (2020). The essentials of developmental apoptosis. F1000Research, 9.

    Wang, W., Yang, L. L., Luo, S. M., Ma, J. Y., Zhao, Y., Shen, W., & Yin, S. (2018). Toxic effects and possible mechanisms following malathion exposure in porcine granulosa cells. Environmental Toxicology and Pharmacology64, 172-180.

    Yong, W., Jiao, J., Kou, Z., Wang, C., & Pang, W. (2021). Resveratrol ameliorates malathion-induced estrus cycle disorder through attenuating the ovarian tissue oxidative stress, autophagy and apoptosis. Reproductive toxicology, 104, 8-15.

    Zama, A. M., & Uzumcu, M. (2009). Fetal and neonatal exposure to the endocrine disruptor methoxychlor causes epigenetic alterations in adult ovarian genes. Endocrinology150(10), 4681-4691.

    Zhong, M., Zhai, Q., Zhang, R., Yin, H., Li, J., Ma, Z., ... & Li, Y. (2021). Effect of pyrethroid pesticides on the testis of male rats: A meta-analysis. Toxicology and Industrial Health, 37(4), 229-239.