Elsevier

Aquatic Toxicology

Volume 228, November 2020, 105624
Aquatic Toxicology

Dietary Origanum vulgare essential oil attenuates cypermethrin-induced biochemical changes, oxidative stress, histopathological alterations, apoptosis, and reduces DNA damage in Common carp (Cyprinus carpio)

https://doi.org/10.1016/j.aquatox.2020.105624Get rights and content

Highlights

  • The 96 h LC50 value of cypermethrin (CP) for common carp was 4.134 μg/L.

  • CP induced serum biochemical changes and oxidative stress, histopathological alterations, and DNA damage in the exposed carps.

  • Origanum vulgare essential oil (OVEO) attenuated changes in serum biochemical parameters in CP-exposed carps.

  • OVEO alleviated oxidative stress in CP-exposed carps.

  • OVEO reduced histopathological changes, apoptosis, and DNA damage in CP-exposed carps.

Abstract

The study was designed to evaluate the possible protective roles of dietary Origanum vulgare essential oil (OVEO) against cypermethrin (CP)-induced serum biochemical changes and oxidative stress of common carp (Cyprinus carpio). Moreover, histopathological alterations, apoptosis, cell proliferation, and DNA damage in the gills and hepatic tissues were also assessed. Briefly, fish were allotted into six groups with three triplicates whereas a group fed on basal diet and did not exposed to CP and served as control (CTR), two groups were fed on diets supplemented with two levels of OVEO (0.5 % and 1.0 %), a group exposed to sub-lethal concentration of CP (1/10 of 96 h-LC50 = 0.4134 μg/L), and two other groups exposed to the same concentration of CP and fed on diets supplemented with both levels of OVEO (CP + 0.5 % OVEO, and CP + 1.0 % OVEO), respectively, for 30 days. CP induced significant elevation of serum alanine transaminase (ALT), aspartate transaminase (AST), alkaline phosphatase (ALP), urea, and creatinine levels indicating hepato-renal toxicity (P < 0.05). Besides, there was a significant decrease in serum catalase (CAT) and superoxide dismutase (SOD) activities (P < 0.05). Moreover, CP induced significant histopathologic alterations in gills, anterior kidneys, and hepatic tissues with activation of apoptosis (Caspase-3) and proliferating cell nuclear antigen (PCNA). Comet assay demonstrated significant DNA damage in gills and liver tissues of the CP-exposed group. Interestingly, a significant attenuation of serum ALT, AST, ALP, urea, creatinine, CAT, and SOD levels (P < 0.05) was noticed in CP-exposed fish and concurrently fed diets supplemented with either 0.5 % or 1.0 % OVEO. Moreover, histopathologic alterations and apoptosis were significantly reduced along with a concomitant significant decrease in DNA damage (P < 0.05) which indicated the mitigation of DNA damage. Conclusively, the study showed that OVEO is an effective counteractive treatment against CP-induced damage in exposed common carp and is recommended during the formulation of fish rations.

Introduction

Synthetic insecticides have been used for several years in agriculture practices to control pests and their existence in the surrounding aquatic environment will induce potential serious risk hazards to the living biota (El Euony et al., 2020; Naiel et al., 2020a, b). Synthetic pyrethroid insecticides include several types such as deltamethrin, permethrin, tetramethrin, resmethrin, γ-cyhalothrin, and cypermethrin can induce toxicological effects on the exposed aquatic organisms (Coats et al., 1989). Because of the absence of pyrethroid hydrolyzing enzymes (carboxylesterases), fish are extremely sensitive to pyrethroids toxicity (de Moraes et al., 2018d). Therefore, the processes of biotransformation and detoxification of pyrethroids in fish are reasonably slower than other organisms (Glickman et al., 1982).

Globally, cypermethrin (CP), as a 4th generation pyrethroid insecticide, is widely used to control cotton pests and several pests that infect crops. Also, it can be prescribed as “pour-on treatment” to control ectoparasites that infest farm animals such as ticks and mites (Muenstermann et al., 1988). However, its unrestricted use may lead to several toxic effects on exposed aquatic organisms (Ullah et al., 2018). Several reports showed that CP induced oxidative stress and genotoxicity in the exposed zebrafish (Danio rerio) (Paravani et al., 2018, 2019), apoptosis, neurotoxicity, and embryotoxicity in the exposed D. rerio embryos (Parlak, 2018). In cyprinid fishes, CP induced oxidative stress and malformations in rohu (Labeo rohita) during the early developmental stages (Dawar et al., 2016), immunotoxicity in common carp (Cyprinus carpio) (Soltanian and Fereidouni, 2017), and alterations in serum biochemical parameters alongside with hepatotoxicity in the exposed Catla catla (Vani et al., 2012; Sharma and Jindal, 2020). Furthermore, it induced neurotoxicity, histopathological alterations, and activation of apoptotic changes in the brain of C. catla (Jindal and Sharma, 2019).

Origanum vulgare L. is a unique medicinal plant with potent antioxidant, growth-promoting, and immune potentiating effects in fish (Abdel-Latif et al., 2020a, b). Its antioxidative capacity is linked to the presence of important phytochemicals in the essential oil of O. vulgare such as thymol, carvacrol, γ -terpinene, and p-cymene (Oniga et al., 2018; Alagawany et al., 2020). On the other hand, O. vulgare extract can beneficially attenuate hepatotoxicity and genotoxicity induced by cyclophosphamide in rats (Habibi et al., 2015a, b). Besides, it can mitigate oxidative stress caused by carbon tetrachloride (Botsoglou et al., 2008), gentamycin-induced nephrotoxicity (Mirzaei et al., 2016), and protect against inflammation, and histopathological changes in rats exposed to paraquat (Sharifi-Rigi et al., 2019).

Researchers paid great interest in finding potential compounds that are capable of diminishing CP-adverse effects in fish such as lycopene (Yonar, 2013), ascorbic acid (Korkmaz et al., 2009; Saha and Kaviraj, 2009), propolis (Orun et al., 2014), Delonix elata (Meenambal et al., 2012), and recently guava (Psidium guajava) leaves extract (Abdel-Tawwab and Hamed, 2020). However, the information regarding the protective roles of O. vulgare against insecticide toxicity in fish is relatively little. Recent reports showed that dietary supplementation of O. vulgare extract can beneficially attenuate the oxidative stress, alterations in hepatorenal functions, and histopathological changes induced by exposure of rainbow trout Oncorhynchus mykiss to diazinon (Rafieepour et al., 2019a, b). Therefore, this study was designed to evaluate the possible ameliorative effects of dietary O. vulgare essential oil (OVEO) against changes in serum biochemistry, oxidative stress, histopathological alterations, and immunohistochemical modulation induced by CP-exposure in common carp. Additionally, the protective role of OVEO against CP-induced genotoxicity (DNA damage) has been also evaluated.

Section snippets

Chemicals and tested compounds

Cypermethrin (CP; Dipacxon-39, Cenavisa laboratories, Camí Pedra Estela Resus, Spain) (imported by Agricultural Materials Co., Giza, Egypt) is a commercial product of an emulsifiable concentrate CP 10 % (each 1 mL contains 100 mg CP) (The batch number is 340−17-004, and the registration number is 10/2016). This product was prescribed as insecticide-acaricide for livestock farms. The stock and test solutions of CP were daily prepared by dissolving it in acetone.

A commercial product contains

The 96-h LC50 of CP in exposed C.carpio

During the 96-h LC50 experiment, no fish mortalities were recorded in the CTR group, meanwhile, there was a concentration-dependent increase in the fish mortalities was noticed in the fish exposed different levels of CP. Interestingly, throughout the 96-h exposure period, fish were off food, lethargic, and exhibited nervous manifestations just before death. Table 1 shows that the mean value of 96-h LC50 of CP for C. carpio according to Finney’s probit analysis is 4.134 μg/L with lower and upper

Discussion

Cypermethrin (CP) is a candidate pyrethroid insecticide for controlling agricultural pests and infestation of animals with ectoparasites. However, CP can be easily discharged into the aquatic environment inducing a great potential threat to the exposed aquatic organisms. Several studies discussed the toxicological aspects of CP in cultured cyprinid fishes (Vani et al., 2012; Dawar et al., 2016; Soltanian and Fereidouni, 2017; Jindal and Sharma, 2019; Sharma and Jindal, 2020). Moreover, numerous

Conclusions and future perspectives

Based on our results, it can be concluded that cypermethrin (CP) is serious life-threatening toxicant to the exposed fish as it induced negative consequences such as serum biochemical alterations, hepatorenal impairments, oxidative damage, histopathological alterations, apoptosis, cell proliferation, and DNA damage in the exposed C. carpio. Dietary supplementation with Origanum vulgare essential oil (OVEO) can be regarded as an excellent candidate for its protective roles against the adverse

Author statement file

Asmaa F. Khafaga

Collection of tissue samples.

Histopathological examinations.

Immunohistochemical analysis.

Mohammed A.E. Naiel

Statistical analysis.

Revising the manuscript before submission.

Mahmoud A.O. Dawood

Data collection, and writing the original manuscript.

Revising the manuscript before submission.

Hany M.R. Abdel-Latif

Experimental design and follow up fish.

Serum measurments and Comet assay.

Revision and submission of the manuscript.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

All authors would like to thank Prof. Dr. Yasser El-Sayed – Head of Department of Veterinary Forensic Medicine and Toxicology, Faculty of Veterinary Medicine, Damanhour University, Egypt for his help in the calculation of 96 h LC50 of CP using Finney’s probit analysis.

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