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. 2023 Dec 1;12(6):1152–1158. doi: 10.1093/toxres/tfad109

Impact of Coriandrum sativum seeds extract on albino rats’ testicular toxicity caused by carbendazim

Ehab Tousson 1,✉, Somaya Y Shalaby 2, Doaa M El-Gharbawy 3, Mohamed A Akela 4, Mohamed Rabea 5, Eman H Kandil 6
PMCID: PMC10734600  PMID: 38145095

Abstract

Background

A broad spectrum carbamate fungicide called carbendazim (Carb) is used to combat a number of different fungal diseases. One of the extensively utilized medicinal plants in oriental countries is Coriandrum sativum.

Aim

In the current study, the impact of C. sativum seeds extract (CSE) on albino rats’ testicular toxicity caused by carbendazim was investigated.

Materials and methods

A total of 50 male albino rats were classified into 5 groups [Gp1, Control Gp; Gp2, Coriandrum Gp (CSE); Gp 3, carbendazim Gp (Carb); Gp 4, Co treated CSE with Carb (CSE + Carb); Gp 5, Post treated Carb with CSE (Carb + CSE)].

Results

Carb induced elevation in serum LH. FSH, testicular malondialdehyde (MDA), testicular nitric oxide (NO) markers and testicular injury and it reduced serum testosterone, testicular glutathione (GSH), testicular catalase and PCNA. Treatments of Carb with CSE (CSE + Carb and/or Carb + CSE) improved these parameters and reduced testicular toxicity with best results for Carb + CSE than CSE + Carb.

Conclusions

The above findings revealed that; Carb induced testicular toxicity and it supported the hypothesis that the antioxidant characteristics of one or more of CSE constituents can reduce the testicular toxicity of Carb.

Keywords: carbendazim, Coriandrum sativum, testis, antioxidant

Introduction

Assessments of the reproductive toxicity of fungicide that are widely used to control some of the most common fungal diseases in crops and are important public health issues. One of the most prevalent environmental toxins, systemic benzimidazole fungicide carbendazim (methyl-2-benzimidazole carbamate), is a byproduct of benomyl and has negative effects on both human and animal reproductive health.1–3 According to the World Health Organisation,4 carbendazim (Carb) is a “Toxic Substance.” In contrast, prolonged exposure to Carb led to lower survival rates, and changes in the structure and functions in different body organs.5–7 Carbendazimi plays a significant role in the toxicology of both benzimidazole and thiophanate fungicides as it is also the major metabolite of benomyl.7 Growing reports of declining sperm counts and escalating reproductive diseases in the general population have contributed to the increased interest in the toxicology of the male reproductive system in recent years.

In order to cure a range of diseases, medicinal plants produce a variety of chemical components.8–10 For the inhibition and management of testicular toxicity and damage, the effects of antioxidants or free radical scavengers have been extensively studied.11–13 Antioxidants have demonstrated positive results in several of those trials, particularly for the prevention and treatment of testicular toxicity.14–16

The culinary herb coriander (C. sativum), often known as Chinese parsley, is an annual that is grown for both its seeds and leaves. With the discovery of several polyphenolics and antioxidant elements found in it, the coriander plant has been shown to have a significant role in the pathogenesis of numerous disorders.17 In medicine is utilised for its antioxidant, antibacterial, antifungal, and digestive properties.18,19 This study was carried out to investigate the toxic effects of Carb on rat testis induced vibration in testicular hormones, oxidative stress and tissue injury in addition to the potential ameliorative role of CSE in treatments.

Materials and methods

Carbendazim (carb)

Carbendazim was got from kafr el zayat pesticides & Chemicals Company, kafr el zayat, Egypt (KZC, Egypt) and it was freshly made with maize oil and given orally.

Coriander seeds extracts (CSE) production

According to,19 coriander seeds (CS) were ground into a powder, steeped in boiling water for 24 h, extracted, and then kept at −30 °C in the dark until usage.

Animals and experimental groups

50 male albino rats (Rattus norvigicus) weighing 140 g plus 10 g were used in the studies. Rats were kept in the lab for a week before to the experiment, fed a conventional rodent diet, and given unlimited access to water. The ambient temperature in the randomly picked home conditions ranged from 23–25 °C, a two-week supply of easily accessible commercial food and water, a 12-h cycle of light and darkness, and relative humidity. Rats were raised and taken care of during the study period in compliance with the Institutional Animal Care Committee-approved animal care handbook (MUFS-S-HI-1-23). Five groups of 10 rats each were formed using random and equal distribution of the animals.

Gp1: Control Gp served as a negative control and were not given any treatments.

Gp2: Coriandrum Gp (CSE) where rats treated orally (50 mg/kg body weight) for 3 days weekly for 8 weeks.

Gp 3: Carbendazim Gp (Carb) as a positive control where rats treated orally with carbendazim (100 mg/kg body weight) for 3 days weekly for 8 weeks.

Gp 4: Co treated CSE with Carb (CSE + Carb) for 8 weeks.

Gp 5: Post treated Carb with CSE (Carb+CSE) where rats treated with Carb for 8 weeks and then treated with CSE for another 8 weeks.

Blood and serum samples

Rats were starved for 12 h at the end of the experiment, euthanized by sodium pentobarbital for complete dissection. The inferior vena cava’s serum was drawn out and detached by centrifugation at 3,500 rpm for 15 min. In order to analyse the collected serum and estimate blood parameters, it was kept at a temperature of −18 ° C.

Hormone assay

Mahgoob et al.20 evaluated the amounts of testosterone, while Odell et al.21,22 determined the levels of follicle stimulating hormone (FSH) and luteinizing hormone (LH).

Oxidative and antioxidants parameters estimations in testicular homogenate

According to Mesbah et al.23 and Aldubayan et al.24 lipid peroxidation (MDA) and glutathione (GSH) activities in homogenate were estimated respectively. While catalase and nitric oxide (NO) activities were estimated according to Saggu et al.25 and Robbins and Grisham26 methods respectively.

Histopathological and immuohistochemical examination

The testes tissues were immediately immersed in 10% buffer neutral formalin solution for one to two days prior to processing for paraffin sectioning. According to Tousson et al.,27 staining the sections with haematoxylin and eosin (H&E) allowed for the histological evaluation.

According to Tousson et al.,27 the remaining paraffin-embedded testes sections were deparaffinized and hydrated for PCNA immunoreactivity. The avidin-biotin complex (ABC) kit (Elite–ABC, Vector Laboratories, CA, USA) with specific antibodies was used for detection of Proliferating cell nuclear antigen (PCNA) was detected (dilution 1:100, DAKO Japan Co, Ltd, Tokyo, Japan).

Statistical analysis

The statistics were presented together with the standard error of the mean. The study was carried out using the 16th version of the Statistical Package for the Social Sciences. The significance of group differences was also assessed using a student t-test. The threshold for statistical significance was set at P 0.05.

Results

Impacts of CSE on testicular functions

Figure 1 exposed that; Carb induced a significant depletion in the level of total testosterone, and elevation in FSH and LH as compared control and CSE groups. Treatment of Carb with CSE as co-treatment group (CSE + Carb) or post treatment group (Carb + CSE) revealed a significant depletion in the level of FSH and LH and elevation in total testosterone, as compared to Carb group with best results for Carb + CSE.

Fig. 1.

Fig. 1

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Variations in sexual hormones in different Gps. The significance of difference was analyzed by one—way ANOVA and Dunnett test (compare all vs. Carb Gp) using computer program. Values are expressed as means ± SEM. One—way ANOVA was significant at P < 0.05. Dunnett test was significant from corresponding amitriptyline group value at *P < 0.05, **P < 0.01, and ***P < 0.001.

Oxidative stress and antioxidant parameters in testicular homogenates

Figure 2 demonstrated a statistically significant elevation in the level of MDA and NO while a significant depletion in CAT, and GSH in testicular homogenates in the Carb group compared to the control and CSE groups. In distinction; when Carb were treated with CSE (CSE + Carb or as Carb + CSE), testicular homogenates showed a significant elevation in CAT, and GSH and a significant depletion in MDA and NO with best results for Carb + CSE.

Fig. 2.

Fig. 2

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Variations in oxidative stress and antioxidant parameters in testicular homogenates in different Gps. The significance of difference was analyzed by one – Way ANOVA and Dunnett test (compare all vs. carb Gp) using computer program. Values are expressed as means ± SEM. One—way ANOVA was significant at P < 0.05. Dunnett test was significant from corresponding amitriptyline group value at*P < 0.05, **P < 0.01, and ***P < 0.001.

Histological observations

Seminiferous tubules in the testes of the rats in the control and CSE groups had a normal architecture, according to histological analysis (Fig. 3A and B). The sertoli cells and spermatogenic epithelium that line the tubules rest on the basal lamina. The many spermatogenic cells (spermatogonia, spermatocytes, spermatids, and spermatozoa) are found in the germ cells. Testes sections from rats given Carb for 8 weeks exhibited significantly decreased, irregular, and distributed numbers of germ cells together with decreased quantities of spermatozoa and significantly inhibited spermatogenesis (Fig. 3C and D). Testes sections in treated rats with Carb and CSE (CSE + Carb or as Carb + CSE), showed normal distribution of spermatogenic cells, elevation in spermatozoa numbers with best results for Carb + CSE. (Fig. 3E and F).

Fig. 3.

Fig. 3

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Photomicrographs of rat testes sections stained with HE. Rat testes from the control and CSE groups showed seminiferous tubules with a normal structure and sperm-filled stars (A&B). C&D: Testes sections from the carb group showed uneven (arrows) and distributed numbers of germ cells together with a decrease in the quantity of spermatozoa (stars). E&F: Testes sections in treated rats with carb and CSE (CSE + carb or as carb+CSE), showed normal distribution of spermatogenic cells and elevation in spermatozoa numbers (stars).

Effect of CSE on testicular PCNA immunoreactivity

In the control and CSE groups, only the spermatogonia displayed a robust positive reaction to PCNA-ir, whilst the other spermatogenic cell types displayed a negative reaction (Figs. 4A and B). In contrast, rats treated with carb were found to have a slight positive affinity for PCNA in the spermatogonia in the testis sections (Fig. 4C and D). Testes sections in CSE + Carb showed moderate affinity while in Carb + CSE revealed strong affinity for PCNA in the spermatogonia (Fig. 3E and F).

Fig. 4.

Fig. 4

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Photographs of testicular sections from the various groups stained with PCNA-ir. A&B: Spermatogonia in testes sections from the control and CSE groups displayed a high positive affinity (arrows). C&D: Following carb treatments, mildly positive affinities were seen in the spermatogonia (arrows). E: Spermatogonia in CSE + carb showed a somewhat favourable affinity (arrows). F: Spermatogonia from carb+CSE showed a strong positive affinity (arrows).

Discussion

The broad range carbamate fungicide carbendazim (Carb) is crucial for controlling plant diseases. Carb poisoning was brought on by prolonged exposure in human organs. Therefore, the current study aimed to show the impact of CSE on Carb induced testicular toxicity. Current results revealed depletion in testosterone levels and elevation in LH and FSH as compared to control and CSE groups while the treatments with CSE improved this modulation. Salimi et al.28 revealed that Carb had negative effects on spermatogenesis, resulting in decreased fertility in male rats. Current findings support their findings. Additionally, our findings support those of Moffit et al.,1 who claimed that carbs induced histopathological changes in testis and changes in enzymes activities. According to Gawande et al.,29 testicular damage caused by carbendazim has been shown through histopathology, and serum and testis residue levels have decreased. Our results agree with30 who found that; Coriandrum sativum (coriander) extract improved sexual hormones in diabetic rats. These findings were supported by the work of numerous researchers who found that carbendazim has a number of negative effects on male reproduction.31,32

The induction of oxidative stress, which is brought on by an imbalance between the generation of reactive oxygen species (ROS) and the ability of antioxidant defences, results in an excess production of ROS.33–35 According to Yang et al.36; Sule et al.37 and Salimi et al.,38 it has been discovered that many pesticides cause oxidative stress, which produces free radicals and an alternative antioxidant or oxygen free radical scavenging enzyme system. Current results revealed elevation in MDA and NO levels and depletion in GSH and catalase as compared to control and CSE groups while the treatments with CSE improved this modulation as compared to Carb group. The findings of the current study showed that carbendazim caused rats to experience oxidative stress. This might be the result of an imbalance in cellular oxidative status, as seen by the rise in MDA levels and fall in CAT and GSH activity. In line with this finding, Metwally et al.32 and Hamdy et al.39 noted that carbs significantly increased MDA and significantly decreased SOD and GPx activity in the rat testis. Our results also agree with Rajeswary et al.29 who found that carbendazim-treated rats, induced significantly diminished in antioxidant enzymes SOD, CAT, GPx, GR, GST, and nonenzymatic antioxidants such as GSH and markedly elevation in LPO and ROS. Our results agree with Alankooshi et al.17 who find that CSE induced a significant decrease in testicular MDA and a significant decrease in testicular catalase, SOD and GSH in thyroidectomies rats.

Current results revealed that; carbendazim induced testicular toxicity and damage in seminiferous tubules with reduction in spermatozoa numbers and the treatments with CSE have the ability to improve this damage with best histopathological improvements in post treatment than co-treatments. Our findings support those of Sakr et al.40 and Salem et al.,41 who found that carbendazim caused oxidative stress and testis damage in rats. Also, our outcomes support Gotoh et al.42 who clear that; the quantity of patent efferent ductules influences the extent of testicular injury following carbendazim exposure. Our findings support Sharma et al.43 and Islam et al.44 who claimed that coriander has preventive efficacy on the testis of mice exposed to lead. Our findings concur with those of Al-Rubaye,45 who investigated the inhibition of albino mouse male reproductive system activity by an aqueous extract of coriander leaves.

Conclusion

Carbamate fungicide (carbendazim; Carb) induced testicular toxicity where it changes testicular functions, oxidative stress, structure, and PCNA expression. Treatments of carbendazim with C. sativum seeds extract (CSE + Carb or Carb + CSE) modulates and improved these parameters with best results for post treatments than co-treatments.

Author contributions

Ehab Tousson and Somaya Y. Shalaby proposed the idea and the experimental design, analyzed the data, reviewed drafts of the paper, approved the final draft, and supervised the work.

Mohamed A. Akela and Mohamed Rabea performed the experiments, collected data and wrote the first draft of the manuscript.

Doaa M. El-Gharbawy and Eman H. Kandil performed the statistical analysis, approved the final manuscript and managed the literature searches.

Funding

No fund.

Conflict of interest statement. None declared.

Data availability

All the data and material were available. The data of this article are included within the article and its additional files.

Ethics approval

Animal Care after the protocol approval code Serial No: MUFS-S-HI-1-23.

Consent for publication

Not applicable.

Contributor Information

Ehab Tousson, Department of Zoology, Faculty of Science, Tanta University, Egypt.

Somaya Y Shalaby, Department of Zoology, Faculty of Science, Menoufia University, Egypt.

Doaa M El-Gharbawy, Forensic Medicine and Clinical Toxicology Department, Faculty of Medicine, Tanta University, Egypt.

Mohamed A Akela, Department of Biology, College of Science and Humanities in Al-Kharj, Prince Sattam bin Abdulaziz University, Al-Kharj 11942, Saudi Arabia.

Mohamed Rabea, Department of Zoology, Faculty of Science, Menoufia University, Egypt.

Eman H Kandil, Department of Zoology, Faculty of Science, Menoufia University, Egypt.

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Data Availability Statement

All the data and material were available. The data of this article are included within the article and its additional files.

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