Prevelance of Bovine Cysticercosis in Egypt and the Cysticidal Effect of Two Extracts Obtained from Balanites aegyptiaca and Moringa oleifera on Mice Model Affected with T. saginata Cysticerci

Omnia M. Kandil^1*, Noha M. F. Hassan¹, Doaa Sedky¹, Hatem A. Shalaby¹, Heba M. Ashry¹, Nadia M. T. Abu El Ezz¹, Sahar M. Kandeel², Mohamed S. Abdelfattah³, L. Ying^4,5, Ebtesam M. Al-Olayan⁶

¹Parasitology and Animal Diseases Department, Veterinary Research Institute, National Research Centre, Dokki, Cairo, Egypt.
²Chemistry of Natural Compounds Department, Pharmaceutical and Drugs Industries Research Institute, National Research Centre, Dokki, Cairo, Egypt.
³Chemistry Department, Faculty of Science, Helwan University, Cairo, Egypt.
⁴State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University, Xining, China.
⁵College of Agriculture and Animal Husbandry, Qinghai University, Xining, China.
⁶Department of Zoology, Collage of Science, King Saud University, Riyadh, Saudi Arabia.

DOI: 10.4236/ojas.2024.142004                

Abstract

The aim of the present study was to determine the prevalence of bovine cysticercosis in both cattle and buffloas, in Egypt and to assess the cysticidal efficacy of Balanites aegyptiaca fruits (B. aegyptiaca) and Moringa oleifera seeds (M. oleifera) extracts in experimentally infected mice. The study detected the level of tumor necrosis factor (TNF-α) to monitor the immune and inflammatory responses of experimentally infected mice. Through meat inspection, a total number of 2125 male bovine, 2 to 5 years old, (1125 cattle and 1000 buffloes) were examined under the authority of Albsatine and Alwaraq official abattoirs in Cairo Governorate, Egypt covering the period extended from March 2022 to April 2023. The overall prevalence of the disease among bovine was 7.8% (6.31% of cattle and 9.5% of buffloes). Besides, B. aegyptiaca and M. oleifera extracts showed cysticidal activity in experimentally infected mice. A decrease in the numbers of cysticerci was found in all treated mice groups, and up to 88% reduction was achieved in the B. aegyptiaca-treated group; higher than that was recorded in both M. oleifera (72.23%) and albendazole-treated ones (80.56%). Postmortem findings proved that M. oleifera and B. aegyptiaca reduced cysticerci numbers comparable to a commercial anthelmintic. The study showed a significant decrease (P < 0.001) in TNF-α levels after treatment with Balanites and Moringa extracts, compared with the untreated control and the albendazole-treated groups.

Keywords

Prevalence, Balanites aegyptiaca, Moringa oleifera, Mice, T. saginata Cysticerci

1. Introduction

Bovine cysticercosis remains one of the serious parasitic diseases caused by the larval stage of the zoonotic cestode Taenia saginata; Taenidae family [1] [2] . The disease deems the most continual reported zoonosis observed through post-mortem inspection of meat at slaughter houses all over the world [3] . The infection is a widespread in different countries e.g. Egypt [4] [5] [6] , Saudi Arabia [7] and Ethiopia [8] . It negatively affected beef quality causing great financial losses for the beef sector besides its adverse impact on public health. The annual financial losses in Africa related to bovine cysticercosis were about $1.8 billion [9] . In Egypt, the economic losses due to infection reached 87,032 Egyptian Pounds per year among slaughtered’ cattle [4] .

Bovine are the intermediate hosts of Taenia saginata. While humans act as the definitive host whereas they harbor the adult worm in the intestine and causing taeniosis [1] . The infection of animals starts through eating contaminated food and water with eggs of T. saginata disseminated in stool of infected human. The eggs hatch and hexacanth embryos (oncospheres) release to penetrate the intestinal mucosa reaching the blood circulation then they attached to heart, masseter muscles and other muscular sites mainly forming cysticerci [10] [11] . Taeniosis is arised from consumption of human to raw or under cooked beef contained cystiserci. Then, the adult worms develop and live in the intestines. Millions of eggs may be discharged into the environment each day when the terminal segments holding eggs are detached from the adult parasite [12] . There are 77 million people act as T. saginata carriers worldwide, of which 40% reside in Africa [13] . So, there are great risks for spreading the infection between cattle and buffaloes particularly in Africa.

Albendazole (ABZ) is usually used in treatment of bovine cysticercosis, with a variable efficiency according to the number, type and location of the cysts [14] . Cysticidal treatment induces parasite killing, resulting in a post inflammatory response, which can potentially hinder treatment and require anti-inflammatory drugs as corticosteroid treatment to control inflammation but it might pose significant health risks [15] .

Utilizing of safe natural potent anti-parasitics of a plant origin is aimed mainly to avoid chemotherapeutics residues in meat and to delay or prevent development of drug resistance [16] .

Balanites aegyptiaca is one of the foremost common wild plant species disseminated in African and known by its numerous employments for medicinal purposes [17] . B. aegyptiaca contained a wide assortment of bioactive compounds which have organic, pharmacological action like saponins, flavonoids, alkaloids, terpenoids [17] . It has a wide of range of medicinal benefits e.g. anthelmintic impact [18] , anti bacterial effect [19] , anti-cancer [20] , anti-inflamatory [21] , hepatoprotective activity [22] and Wound healing activity [23] .

Furthermore, Moringa oleifera is one of the most beneficial trees that is suitable for food applications and possesses anthelminthic [24] , anti-inflammatory, antimicrobial, and anti-oxidant [25] [26] . It has also modulating the immune system, and displaying anti-oxidant, anti-diabetic, and anti-tumor activity [27] . The bioactive constituents of M. oleifera incorporate flavanoids, enolic corrosive, alkaloids and sterols and terpene (glucosinolate and isothiocyanate) [28] .

On the other hand, tumor necrosis factor-alpha (TNF-α) is a pleiotropic cytokine with having significant roles in homeostasis and disease pathogenesis. It is an essential cytokine that acts as an endogenous mediator having immune and inflammatory functions [29] [30] . It is mainly expressed by activated macrophages, natural killer cells, and T cells, and activated cells bearing the TNF-α receptor such as monocytes, macrophages, and dendritic cells, which then produce inflammatory factors [31] .

Studying of the prevalence of bovine cysticercosis provides usefull data for the good understanding of disease epidemiology and outlines the required prevention and control measures to combat it. Prevention of the infection and/or treatment of live animals using potent natural product, to destroy the developed cystiserci would be of great impacts on getting healthy beef, decreases the economical losses and control risks of public infection. Therefore, this study is intended to determine the prevalence of bovine cysticercosis among cattle and buffaloes in Cairo Governorate, Egypt. Besides, the study also aimed to detect cysticidal activity of methanolic extracts of B. aegyptiaca and M. oleifera as anti-parasitic alternatives compared to albendazole (reference drug) on mice model infected with cysticerci through postmortem examination and monitoring the level of TNF-α as an important indicator for the animal immune and inflammatory response.

2. Material and Methods

2.1. Ethical Approval

The tests were conducted in compliance with the prerequisites and suggestions of the International Animal Ethics Committee and the Ethical Committee of the Faculty of Science, Helwan University, Cairo, and the current Egyptian Law and Directions for the protection of experimental animals to minimize negative states (harm) and improve feeding and housing conditions, under certificate number HU2021/Z/MSO0121-01.

2.2. Prevalence of Bovine Cysticercosis

Abattoirs survey was done from the period extended from March 2022 to April 2023 through meat examination under the authority of Albsatine and Alwaraq official abattoirs in Cairo Governorate, Egypt. Two thousands one hundred twenty five of cattle and buffaloes (1125 cattle and 1000 buffloes) aged from 2 to 5 years old were exposed to meat inspection after slaughtering. At Albastatine abattoir 1300 animals (640 cattle and 660 buffaloes) and at Alwaraq abattoir 825 animals (485 cattle and 340 buffloes) were examined. Detection of cyst was conducted via applying several cuts in different organs like diaphragm, cardiac and, skeletal muscles, neck, tongue, kidney, liver and lung. Macroscopical and microscopical examinations of the collected cysts were carried out to determine the cyst viability. The cysts were recorded as non viable and degenerated when they were calcified (solid), cheesy (smooth) or dull (empty). Microscopical investigation of cysts was applied to identify the viability of the cyst through incubation of fluid evacuated from the cyst in a solution of 30% bull bile solution diluted in ordinary saline at 37˚C for 90 minutes [32] .

2.3. Plants

B. aegyptiaca fruits were acquired from neighborhood markets in Cairo Governorate, Egypt. The plant materials were distinguished and affirmed by the laboratory of Medicinal and Aromatic Plants Research Department, National Research Centre. The B. aegyptiaca fruits were cleaned with tap water, shade-dried and mechanically ground utilizing a research facility mortar and pestle. M. oleifera seed were provided from the Egyptian Scientific Society for M. oleifera at the National Research Centre, Dokki, Giza. Seeds were powdered and kept in a closed bottle. The methanolic extract of both plants was prepared according to [33] [34] as follows: the powdered seeds of M. oleifera and the powdered fruit of B. aegyptiaca (500 g) were separately soaked in methyl alcohol (1:10) at 27˚C for 48h with shaking and then filtration was applied through filter paper for each extract. The concentration of methanolic extracts was made under reduced pressure using a rotary evaporator at 40˚C. The methanolic extracts were put at 4˚C until treatments. At the time of treatment, the prepared extract was dissolved in distilled water with the addition of a few drops of Tween-80 [35] .

2.4. Parasite; in Vitro Hatching of Oncospheres

T. saginata adult worm was obtained from infected humans with taeniasis during stool analysis in a private hospital. The eggs of T. saginata were collected from the gravid proglottids of adult worms, and stored at 4˚C. In vitro hatched oncospheres was carried using sodium hypochlorite (0.5% in PBS) technique Sigma-Aldrich [36] . One ml of egg suspension in PBS was added with 2 ml of 1.0% NaClO and 7 ml of distilled water for approximately 4 minutes with shaking to facilitate in vitro hatching of oncospheres, then the solution was incubated for 30 min. Centrifugation of the suspension was achieved for 10 min at 3000 rpm followed by removal of the supernatant leaving 1 ml of sediment. The sediment was rinsed with distilled water several times and the viability of the oncospheres was assessed by a microscopic examination using 0.4% Trypan blue solution Sigma-Aldrich [37] .

2.5. Detection of Cysticidal Efficacy of Plant Extracts on Mice Model

2.5.1. Animals

Sixty four male mice BALB/c strain weighing 25 to 30 g and 6 - 8 weeks old were utilized. The mice were housed in a well-ventilated animal room beneath standardized conditions of 24˚C; relative humidity (50 ± 5)% and 12 h light/dark cycle. All supplements including water were provided to animals at the Animal House, National Research Center, Giza, Egypt.

2.5.2. Experiment

The mice were experimentally infected with activating oncosphere of T. saginata through oral administration of 5000 oncospheres in 0.5 ml PBS/mouse. After 35 days, four mice were sacrificed and inspected for the presence of cysticeri. After 60 days post infection, the mice were divided into four groups of 15 mice each. Group 1 infected untreated (controls positive), Group 2 infected and treated with B. aegyptiaca methanolic extract at 9 gm/kg b.w.; 2 doses three days interval [38] , Group 3 infected and treated with M. olifera methanolic extract at 150 mg/kg b.w.; 2 doses three days interval [39] , The Group 4 infected and treated with albendazole at 10 mg/kg b.w.; single dose (The Egyptian Company for Chemicals and Pharmaceuticals (ADWIA) 10th of Ramadan City) [40] and Group 5 received an equal volume of distilled water (normal control).

2.5.3. Post Mortem Examination

After 16 weeks post treatment, the mice were anesthetized using Ketamine/Xylazine Pfizer 0.1 ml/20gm mouse wt. IP, sacrificed and the internal organs were examined for cysticeri and photographed using digital camera.

2.6. Estimation of Serum Level of TNF-α

During the in vivo experiment that extended 16 weeks, blood samples (0.1 - 0.2 ml) were collected by retro-orbital venous plexus puncture from each mouse every two weeks post-treatment. The serum samples were stored at −20˚C till utilized. The TNF-α concentration in serum of all the experimental mice groups, was measured employed a commercial quantitative sandwich ELISA (Bioneovan Co., Ltd., https://www.inovbio.com/, Cata. No.: In-Mo1920), that was specific for mouse TNF-α and sensitive down to 5 pg/ml at wave length 450.

2.7. Statistical Analysis

Information were measurably analyzed utilizing a one-way examination of variance (ANOVA) taken after by Duncan’s numerous for differences between groups. Contrasts were considered significant at P < 0.05 for differences between groups level utilizing SPSS statistical software version 16. The Chi square test by factual computer bundle for social science (SPSS) adaptation 15.0 (SPSS Inc., Chicago, IL), and P < 0.05 was utilized to analyze the impact of hazard components; age, on the in general parasitic disease. Factors were significant at P ≤ 0.05.

3. Results

3.1. Prevalence of Bovine Cysticercosis among Bovine

The post mortem inspection of 2125 animals (1125 cattle and 1000 buffaloes) carcasses at Albasatin and Alwaraq abattoirs revealed that (166/2125) 7.8% of bovine were infected with cysticercosis, separately 6.31% (71/1125) for cattle and 9.5% (95/1000) for buffaloes. Total prevalence of infection of bovine at Albasatin abattoir was recorded (94/1300) 7.23% and it was recorded that (45/640) 7.03% cattle and (49/660) 7.42% buffaloes were positive. Meanwhile, at Alwaraq abattoir 72 bovine carcasses out of 825 were infected 8.72%; (26/485) 5.36% for cattle and (46/340) 13.52% for buffaloes as presented in Table 1. The risk of age was studied as demonstrated in Table 2. It was elicited that (65/955) 6.8% of cattle more than 2 years were positive, but 6 out of 170 cattle (3.52%) were lesser than 2 years. Furthermore, (93/815) 11.4% of buffaloes more than two years were infected compared to those less than two years (2/185) 1.08%. Out of 195 collected cysts from the inspected carcasses (116/195) 59.48% were found viable and (79/195) 40.51% were degenerated (Table 3).

Table 1. Abattoirs in Cairo Governorate, Egypt.

Table 2. Association between the age of inspected bovine and the suspected infection with cytisercosis.

**High significant.

Table 3. Different viability of cysticerci in the inspected animals carcasses.

**High significant.

3.2. Plants Cysticidal Activity and Post Mortem Findings

After 16 weeks of treatment, the total numbers of cysticerci in mice experimentally infected with T. saginata oncospheres are recorded as shown in Table 4. On gross examination, there was a marked (P < 0.05) decrease in the numbers of cysticerci found in all treated groups than in the untreated infected control. In the latter, the total number of cysticerci was 36; half of them were found in the intestine. In contrast, none of the B. aegyptiaca treated mice had cysticerci in the intestine showing reduction superior to 88%, and most of cysticerci were recovered from kidney 50.0%. Whereas, 20.0 and 14.29% of the total number of cysticerci were recovered from the intestine of M. oleifera and albendazole treated mice, respectively, and most of cysticerci were recovered from peritoneum (50.0 and 42.85%, respectively) with reduction reached to 72 and 80%, respectively. Besides, the cysts of the treated groups were smaller in size than that of the control one (tumor-like cysts). Most of them had firm contents especially in B. aegyptiaca treated group in which the cyst was difficult to detect and appeared as a small white or yellow spot (Figure 1).

3.3. Serum Level of TNF-α

The dynamics of serum level of TNF-α (Th-1 pro-inflammatory cytokine) in all tested groups during 16 weeks post-treatment was determined by sandwich ELISA (Table 5). The data presented illustrated that the serum levels of TNF-α in mice experimentally infected with T. saginata oncospheres (G1) were significantly (P < 0.001) increased compared to the other groups (G2, G3, G4 and G5). After treatment with B. aegyptiaca methanolic extract (G2) the serum levels of TNF-α markedly (P < 0.001) decreased in comparison with the other treated groups (G1, G3, and G4), This reduction in the level of TNF-α started from the fourth week post treatment and remained later until the sixteenth week post treatment. Meanwhile Group (3) infected mice and treated with M. olifera seeds methanolic extract showed significant reduction (P < 0.001) in the level of TNF-α in comparison with the G1 and G4, this reduction in the level of TNF-α started from the second week post treatment until the sixteenth week post treatment. On the other hand, the level of TNF in Group (4) mice infected with T. sagenita oncospheres and treated with albendazole (G4) showed significant increase in the level of TNF-α in comparison with G2, and G3, this elevation from the fourth week post treatment.

Table 4. Effect of B. aegyptiaca, M. oleifera, and albendazole on reduction of number T. saginata cysticerci of mice in comparison to the untreated control group.

Figure 1. Macrographs showing cysts in internal organs of the different groups of BALB/c mice at the 16th week post treatment. (a) Untreated infected control group; (b) Albendazole treated group; (c) Moringa treated group; (d) Balanites treated group.

4. Discussion

Bovine cysticercosis is a major obstacle affecting livestock production due to the losses in the meat industry resulting from meat condemnation [1] [2] . The current study revealed that the prevalence of the disease among slaughtered bovine

Table 5. The dynamics of serum level of TNF-α in all treated groups during 16 weeks post-treatment.

Different small letters at the same row indicate to significant differences between animal groups while different capital letters at the same column indicate to significant differences between weeks post treatment at P ≤ 0.05, NS = Non-significant. pg/ml = picogram/milliliter. All data were statistically analyzed and presented as means ± standard error (SE).

at Albasatin and Alwaraq abattoirs in Cairo Governorate, Egypt were 7.8%, separately 6.31% for cattle and 9.5% for buffaloes. These results might be in accordance with that reported by [41] who reported that 9.07% of buffaloes slaughtered in Kaliouba Governorate, were infected with cysticercosis. Besides, [6] who found that 7.3% of the inspected cattle in North Egypt had cysticercosis lesions during postmortem inspection. Moreover, similar findings were observed by [5] in Egypt where the infection rate was (7.5%). Lower infection rate than our findings were recorded by [42] in Nigeria 3%, and [43] 3.6% in Ethiopia [8] conducted a cross-sectional study on the disease, in slaughtered cattle at municipal abattoirs in Ethiopia and recorded very high prevalence 27.3%. These differences in the prevalence might be due to variation in the climate conditions, immune status of animals and the followed hygienic and control measures in the suspected areas around world.

Concerning the age, this study declared that the infection rate was significantly higher in adult cattle than young ones. That was in agreement with [44] while [45] revealed that the age factor did not affect the prevalence of the disease among cattle. The findings elicited that 59.48% of the collected cysts were viable while 40.51% were degenerated. This result was consistent with [41] while it disagreed with [8] who detected that the degenerated cysts were more than the viable ones. Major financial losses were recorded through condemnation of meat containing cystiserci during inspection of cattle carcasses. So, Adequate prevention and treatment of the diseases is a must. Albendazole is used in treament of cysticercosis [46] . On oral administration of albendazole, albendazole sulphone, an inactive form of albendazole, was promptly biotransformed from the active intermediate metabolite albendazole sulphoxide. Albendazole has a low water solubility similar to other benzimidazole carbamates, which limited its oral absorption and reduced its bioavailability [47] . However, some studies demonstrated an elevated cysticidal activity of albendazole and high percentage of reduction in the number of T. saginata cysticerci after treatment reached to 100% for animals treated with 7.5 mg/kg dosage on the 40th day after treatment [48] . Besides, [49] reported that ABZ induced degenerative alterations in parasite tegument cells, damaging its metabolism, resulting in immobilization and death of the cyst. On contrary, [46] suggested that albendazole had inconsequential viability values against T. saginata hatchings parasitizing tentatively contaminated bovines. But, there is a lot of interest in creating new cysticidal medications, particularly ones derived from medicinal plants that possess a variety of bioactive substances that may result in a variety of parasite-killing processes, and limiting the likelihood of anthelmintic resistance.

In the present study, there was a marked decrease in the numbers of cysticerci found in all treated groups and up to 88% reduction was achieved in the B. aegyptiaca treated group; higher than that was recorded in both M. oleifera and albendazole treated ones. The number of cysticerci recovered in different parts of the animals that the rate of absorption of dead cysts was more note worthy within the muscles, thorax and leg than within the intestine, but in Balanites treated group that appeared the greatest absorption of dead cysts in the intestine. Indeed, the effect of this difference in the rate of absorption was to change the overall distribution of cysticerci within the animals. Thus in Balanites treated group, the majority of cysticerci (50%) was found in kidney, whereas in Moringa and albendazole treated groups, 50 and 42%, respectively, of the total remaining cysts were found in the peritoneum. These findings might be attributed to the bioactive compounds present in the plant extracts which induced different parasiticidal mechanisms. Previous publications concerning B. aegyptiaca promising anthelmintic efficacy [50] [51] [52] [53] and [18] were available. B. aegyptiaca had a high saponin content and a high potency of anthelmintic activity as assured by [54] . The destructive effect of saponins was linked with their capacity to combine with the cholesterol molecules existing in cuticle membranes of the larvae and herewith led to damage of membrane integrity [55] .

Concerning M. oleifera, it was recorded to hold various bioactive as polyphenols, phenolic acids, flavonoids, alkaloids, glucosinolates, isothiocyanates, tannins and saponin and thiocarbamates [56] and [34] , with pharmacological activities such as antiparasitic property [57] . Moreover, [24] proved that M. oleifera methanolic extract had fasciolicide activity and the hepato-protective impacts on rabbits experimentally infected with Fasciola hepatica. Phytochemical screening detected tannins in the ethanolic extract as the primary secondary metabolites in M. oleifera seeds and were implicated in some plants for helminthicidal activities [58] . In addition to the essential oil, flavonoid, flavones which have been previously reported to have an antiparasitic effect [59] .

It was reported that TNF-α serum level has an importante role in regulating inflammation both locally and systemically [60] . TNF-α produced by activated lymphocytes, macrophages, neutrophils, mast cells, eosinophils, and neurons. In the present study the TNF-α cytokine production is significantly elevated in mice experimentally infected with T. saginata oncospheres (G1) this result was consistent with [61] who studied postoncosphere development in an in vitro model and the capacity of Taenia solium and Taenia saginata for in vivo infection. They recorded that T. saginata 30-day postoncosphere stimulated a profile of pro-inflammatory cytokines (IL-1, IL-6, IL-12, TNF-α), as well as a combination of TH1 and TH2 related cytokines (IL-4, IL-5, IL13 and IFN-γ) that was stronger than the response produced by T. solium. Suggesting that this global immune response stimulated by different forms could permit survival or destruction of the parasite depending of their life-cycle stage. Following treatment of infected mice with B. aegyptiaca (G2) showed significant reduction in the level TNF-α started from the fourth week post treatment. Previous studies showed that B. aegyptiaca fruits exhibit potent anti-inflammatory effect. The anti-inflammatory response of B. aegyptiaca could be attributed to polyphenols, which affect macrophages by inhibiting a number of crucial inflammatory response regulators, including TNF-α [62] . Furthermore, flavonoids have been shown to have the capacity to lower the levels of a number of pro-inflammatory cytokines such as TNF-α [63] .

Results of the present study revealed that, therapeutic administration of M. oleifera seeds extract caused a significant decrease in serum TNF-α level. The anti-inflamatory effect of M. oleifera seeds attributed to isothiocyanates which have been proved to have anti-inflammatory as well as immunomodulatory activities [64] . In addition to isovitexin which has been reported to be responsible for inhibition of TNF-α level [34] . On the other hand, a significant increase in the serum TNF-α level was seen in the mice infected with T. saginata oncospheres and treated with albendazole (G4) which is similar to the finding of [15] who found that the sudden destruction of the parasite by a cysticidal drug is accompanied by acute inflammation and significant up regulation of TNF-α. Also A remarkable feature of Taenia infections is that damaged cysts by anthelmintic treatment provoke inflammatory responses [65] .

5. Conclusion

It was concluded that bovine cysticercosis is a common disease among bovine; cattle and buffaloes in Egypt. The B. aegyptiaca fruits and M. oleifera seed methanolic extracts possessed both potent anti parasitic and anti-inflammatory effects against T. saginata cysticercosis. The in vivo efficacy of M. oleifera extract was comparable to a commercial anthelmintic and the B. aegyptiaca extract was superior in reduction of cysticerci numbers.

Author Contributions

Conceptualization and Supervision, O.M.K. and H.S.A.; Methodology, O.M.K., N.M.F.H., D.S., H.M.A., N.M.T.A., S.M.K. and M.S.A.; Validation, O.M.K., E.M.A. Y.L. and E.O.; Formal Analysis, O.M.K., H.S.A., D.S. and N.M.F.H.; Writing Original Draft Preparation, O.M.K., H.S.A., N.M.F.H. and D.S.; Writing, Review & Editing, O.M.K., H.S.A., N.M.F.H., D.S. and H.M.A. All the authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by Researchers Supporting project number (RSP2024R111) King Saud University, Riyadh, Saudi Arabia and the Special Project for Scientific and Technological International Cooperation of the Science and Technology Department, Qinghai Province (No. 2021-HZ-801).

Data Availability Statement

The macrographs data used to support the findings of this study are included within the article

Conflicts of Interest

The authors declare no conflicts of interest regarding the publication of this paper.

References

[1]	Laranjo-González, M., Devleesschauwer, B., Jansen, F., Dorny, P., Dupuy, C., Requena-Méndez, P. and Allepuz, A. (2018) Epidemiology and Economic Impact of Bovine Cysticercosis and Taeniosis Caused by Taenia saginata in North-Eastern Spain (Catalonia). Parasites & Vectors, 11, Article No. 376. https://doi.org/10.1186/s13071-018-2931-4
[2]	El-Dakhly, K.M., Hany, S.A., Arafa, W.M., Abdel-Fatah, O.R., Abdel-Atty, N.S. and El-Nahass, E.S. (2023) The Prevalence and Molecular Detection of Bovine Cysticercosis and Its Impact on Slaughtered Cattle in Egypt. Journal of Parasitic Diseases, 47, 527-534. https://doi.org/10.1007/s12639-023-01596-5
[3]	Rossi, G.A.M., Van Damme, I. and Gabriël, S. (2020) Systematic Review and Meta-Analysis of Bovine Cysticercosis in Brazil: Current Knowledge and Way Forward. Parasites & Vectors, 13, Article No. 92. https://doi.org/10.1186/s13071-020-3971-0
[4]	Elkhtam, A.O., Mostafa, I.A. and Shawish, R.R. (2016) Prevalence and Economic Impact of Cysticercus bovis in Slaughtered Cattle in Menoifia Governorate, Egypt. Alexandria Journal of Veterinary Sciences, 50, 130-134. https://doi.org/10.5455/ajvs.231438
[5]	Dyab, A. (2017) Taenia saginata in Man and Cysticercosis in Cattle and Buffaloes in Aswan Governorate, Egypt. Journal of the Egyptian Society of Parasitology, 47, 389-394. https://doi.org/10.21608/jesp.2017.77792
[6]	El-Sayad, M.H., Farag, H., El-Taweel, H., Fadly, R., Salama, N., Ahmed, A.A. and Abd El-Latif, N.F. (2021) Cysticercus bovis in Cattle Slaughtered in North Egypt: Overestimation by the Visual Inspection Method. Veterinary World, 14, 155-160. https://doi.org/10.14202/vetworld.2021.155-160
[7]	Almasri, M., Ahmed, Q.A., Turkestani, A. and Memish, Z.A. (2019) Hajj Abattoirs in Makkah: Risk of Zoonotic Infections among Occupational Workers. Veterinary Medicine and Science, 5, 428-434. https://doi.org/10.1002/vms3.169
[8]	Abera, A., Sibhat, B. and Assefa, A. (2022) Epidemiological Status of Bovine Cysticercosis and Human Taeniasis in Eastern Ethiopia. Parasite Epidemiology and Control, 17, e00248. https://doi.org/10.1016/j.parepi.2022.e00248
[9]	Harrison, L.J.S. (1996) Epidemiology and Control of Taenia saginata Cysticercosis. 1996 Centre for Tropical Veterinary Medicine, University of Edinburgh.
[10]	Gholami, N., Mosayebi, M., Abadi, P.D.R., Atigh, H.R., Reza Sedaghat, R., Zadeh, M.H.N. and Majid Farahani, M. (2020) Bovine cysticercosis in Feedlot Cattle in Central Region of Iran. Journal of Parasitic Diseases, 44, 25-30. https://doi.org/10.1007/s12639-019-01157-9
[11]	Fesseha, H. and Asefa, I. (2023) Prevalence and Associated Risk Factors of Cysticercosis bovis in Bishoftu Municipal Abattoir, Central Ethiopia. Environ Health Insights, 17. https://doi.org/10.1177/11786302231164298
[12]	Murrell, K.D. (2005) Epidemiology of Taeniosis and Cysticercosis. WHO/FAO/OIE Guidelines for the Surveillance, Prevention and Control of Taeniosis/Cysticercosis. WHO/FAO/OIE, Paris, 27-43.
[13]	Megersa, B., Tesfaye, E., Regassa, A., Abebe, R. and Abunna, F. (2010) Bovine Cysticercosis in Cattle Slaughtered at Jimma Municipal Abattoir, South Western Ethopia: Prevalence, Cyst Viability and Its Socio-Economic Importance. Veterinary World, 3, 257-262. https://doi.org/10.5455/vetworld.2010.257-262
[14]	Romo, M.L., Wyka, K., Carpi, A., et al. (2015) The Effect of Albendazole Treatment on Seizure Outcomes in Patients with Symptomatic Neurocysticercosis. Transactions of the Royal Society of Tropical Medicine and Hygiene, 109, 738-746. https://doi.org/10.1093/trstmh/trv078
[15]	Mahanty, S., Orrego, M.A., Cangalaya, C., Adrianzen, M.P., Arroyo, G., Calcina, J., et al. (2017) TNF-α Blockade Suppresses Pericystic Inflammation following Anthelmintic Treatment in Porcine Neurocysticercosis. PLOS Neglected Tropical Diseases, 11, e0006059. https://doi.org/10.1371/journal.pntd.0006059
[16]	Kandil, O.M., Nassar, S.A., Nasr, S.M., Shalaby, H.A., Hendawy, S. and Moghazy, F.M. (2015) Synergetic Effect of Egyptian Propolis in Immunization of BALB/c Mice against Bovine cysticercosis. Asian Pacific Journal of Tropical Biomedicine, 5, 324-330. https://doi.org/10.1016/S2221-1691(15)30352-X
[17]	Chothani, D.L. and Vaghasiya, H.U. (2011) A Review on Balanites Aegyptiaca Del (Desert Date): Phytochemical Constituents, Traditional Uses and Pharmacological Activity. Pharmacognosy Reviews, 5, 55-62. https://doi.org/10.4103/0973-7847.79100
[18]	Hassan, N.M.F., Zaghawa, A.A., Abu-Elezz, N.M.T., Nayel, M.A. and Salama, A.A. (2021) Efficacy of Some Egyptian Native Plantextracts against Haemonchus contortus in Vitro and in Experimentally Infected Sheep along with the Associated Haematological and Biochemical Alterations. Bulletin of the National Research Centre, 45, Article No. 180. https://doi.org/10.1186/s42269-021-00636-5
[19]	Sedky, D., Mohamed, A.M., Fouad, R., Khafagi, M.H.M., Omer, E.A., Elbayoumy, M.K., Effat, M.M. and Abou-Zeina, H.A.A. (2022) Assessment of Phytochemical, Antioxidant and Antibacterial Activity of Balanites aegyptiaca and Curcuma longa against Some Bacterial Pathogens Isolated from Dairy Cow Infected with Mastitis. Advances in Animal and Veterinary Sciences, 10, 160-169. https://doi.org/10.17582/journal.aavs/2022/10.1.160.169
[20]	Gnoula, C., Mégalizzi, V., De Nève, N., Sauvage, S., Ribaucour, F., Guissou, P., et al. (2008) Balanitin-6 and -7: Diosgenyl Saponins Isolated from Balanites aegyptiaca Del. Display Significant Anti-Tumor Activity in Vitro and in Vivo. International Journal of Oncology, 32, 5-15. https://doi.org/10.3892/ijo.32.1.5
[21]	Gaur, K., Nema, R.K., Kori, M.L., Sharma, C.S. and Singh, V. (2008) Anti-Inflammatory and Analgesic Activity of Balanites aegyptiaca in Experimental Animal Models. International Journal of Green Pharmacy, 2, 214-217. https://doi.org/10.4103/0973-8258.44735
[22]	Abdel-Kader, M.S. and Alqasoumi, S.I. (2008) Evaluation of the Hepatoprotective Effect of the Ethanol Extracts of Solanum nigrum, Cassia fistula, Balanites aegyptiaca and Carthamus tinctorius against Experimentally Induced Liver Injury in Rats. Alexandria Journal of Pharmaceutical Sciences, 22, 47-50.
[23]	Annan, K. and Dickson, R. (2008) Evaluation of Wound Healing Actions of Hoslundia opposita Vahl, Anthocleista nobilis G. Don. and Balanites aegyptiaca L. Journal of Science and Technology (Ghana), 28, 26-35. https://doi.org/10.4314/just.v28i2.33091
[24]	Kandil, O.M., Hassan, N.M.F., Sedky, D., Ata, E.B., Nassar, S.A., Shalaby, H.A., Nanev, V., Tsocheva-Gaytandzhieva, N. and Gabrashanska, M. (2018) Anthelmintic Efficacy of Moringa oleifera Seed Methanolic Extract against Fasciola hepatica. Journal of Parasitic Diseases, 42, 391-401. https://doi.org/10.1007/s12639-018-1014-y
[25]	Mbikay, M. (2012) Therapeutic Potential of Moringa oleiferaleaves in Chronichyperglycemia and Dyslipidemia: A Review. Frontiers in Pharmacology, 3, Article 17024. https://doi.org/10.3389/fphar.2012.00024
[26]	Atta, A.H., Nasr, S.M., Almaweri, A.H., Sedky, D., Mohamed, A.M., Desouky, H.M. and Shalaby, M.A. (2018) Phytochemical, Antioxidant and Hepatoprotective Effects of Different Fractions of Moringa oleifera Leaves Methanol Extract against Liver Injury in Animal Model. Asian Pacific Journal of Tropical Medicine, 11, 423-429. https://doi.org/10.4103/1995-7645.237186
[27]	Chandrashekar, K.S., Thakur, A. and Prasanna, K.S. (2010) Anti-Inflammatory Activity of Moringa oleifera Stem Back Extracts against Carrageenen Induced Rat Paw Edema. Journal of Chemical and Pharmaceutical Research, 2, 179-181.
[28]	Saini, R.K., Sivanesan, I. and Keum, Y.S. (2016) Phytochemicals of Moringa oleifera: A Review of Their Nutritional, Therapeutic and Industrial Significance. 3 Biotech, 6, Article No. 203. https://doi.org/10.1007/s13205-016-0526-3
[29]	Bradley, J.R. (2008) TNF-Mediated Inflammatory Disease. The Journal of Pathology, 214, 149-160. https://doi.org/10.1002/path.2287
[30]	Jang, D.I., Lee, A.H., Shin, H.Y., Song, H.R., Park, J.H., Kang, T.B., Lee, S.R. and Yang, S.H. (2021) The Role of Tumor Necrosis Factor α (TNF-α) in Autoimmune Disease and Current TNF-α Inhibitors in Therapeutics. International Journal of Molecular Sciences, 22, Article 2719. https://doi.org/10.3390/ijms22052719
[31]	Kalliolias, G.D. and Ivashkiv, L.B. (2016) TNF Biology Pathogenic Mechanisms and Emerging Therapeutic Strategies. Nature Reviews Rheumatology, 12, 49-62. https://doi.org/10.1038/nrrheum.2015.169
[32]	Gracey, J.F., Collins, D.S. and Huey, R.J. (1999) Meat Hygiene. 10th Edition, Harcourt Brace and Company Limited, London, 673-678.
[33]	Jaheed, E., Mohamed, A.H., Nasr, S.M., Mahran, K., Mohammed, F.F., Sedky, D. and Abou-Zeina, H.A. (2020) Therapeutic Effect of Balanites Aegyptiaca Fruit’s Ethanol Extract in Egyptian Baladi Goats Experimentally Infected with Haemonchus Contortus: Blood Serum Biochemical, Oxidative Stress Markers and Pathological Studies. Egyptian Journal of Veterinary Sciences, 51, 119-136. https://doi.org/10.21608/ejvs.2019.20398.1140
[34]	Atta, A.H., Mouneir, S.M., Nasr, S.M., Sedky, D., Mohamed, A.M., Atta, S.A. and Desouky, H.M. (2019) Phytochemical Studies and Anti-Ulcerative Colitis Effect of Moringa oleifera Seeds and Egyptian Propolis Methanol Extracts in a Rat Model. Asian Pacific Journal of Tropical Biomedicine, 9, 98-108. https://doi.org/10.4103/2221-1691.254603
[35]	Harborne, J.B. (1984) Phytochemical Methods. 2nd Edition, Chapman and Hall, New York. https://doi.org/10.1007/978-94-009-5570-7
[36]	Ito, A., Yamada, T. and Ishiguro, T. (1996) Vaccination of Rats with Frozen Eggs, Ethanol-Fixed Eggs and Frozen Oncospheres with or without Embryophoric Blocks of Taenia taeniaeformis. Japanese Journal of Parasitology, 45, 330-332.
[37]	Wang, I.C., Ma, Y.X., Kuo, C.H. and Fan, P.C. (1997) A Comparative Study on Egg Hatching Methods and Oncosphere Viability Determination for Taenia solium Eggs. International Journal for Parasitology, 27, 1311-1314. https://doi.org/10.1016/S0020-7519(97)00087-8
[38]	Koko, W.S., Galal, M. and Khalid, H.S. (2000) Fasciolicidal Efficacy of Albizia anthelmintica and Balanites aegyptiaca Compared with Albendazole. Journal of Ethnopharmacology, 71, 247-252. https://doi.org/10.1016/S0378-8741(00)00172-0
[39]	Almanzor, D.E., Clemente, R.J.C., Fornillos, M.A., Gomez, F.R.M., Ladiao, B.D. and Calzada Tamodtamod, R. (2014) In Vivo Trials of Moringa oleifera Lam. Extracts as Antischistosomal Treatment on Schistosoma japonicum Infected Mice. Journal of Interdisciplinary and Multidisciplinary Research, 2, 49-56.
[40]	Lopez-Garcia, M.L., Torrado-Duran, S., Torrado-Duran, J., Martínez-Fernández, A.R. and Bolás-Fernández, F. (1997) Albendazole versus Ricobendazole (Albendazole-Sulphoxide) against Enteral and Parenteral Stages of Trichinella spiralis in Mice. International Journal for Parasitology, 27, 781-785. https://doi.org/10.1016/S0020-7519(97)00052-0
[41]	Fahmy, H.A., Khalifa, N.O., EL-Madawy, R.S., Afify, J.S., Aly, N.S. and Kandil, O.M. (2015) Prevalence of Cysticercosis and Taenia saginata in Man. Global Veterinaria, 15, 372-380.
[42]	Usip, L., Isaac, L., Amadi, E., Utah, E. and Akpaudo, U. (2011) The Occurrence of Cysticercosis in Cattle and Taeniasis in Man in Uyo, Capital City of AkwaIbom State, Nigeria. Nigerian Journal of Agriculture, Food, and Environment, 7, 47-51.
[43]	Ibrahim, N. and Zerihun, F. (2012) Prevalence of Taenia saginata Cysticerci in Cattle Slaughtered in Addis Ababa Municipal Abattoir, Ethiopia. Global Veterinaria, 8, 467-471.
[44]	Dorny, P., Vercammen, F., Brandt, J., Vansteenkiste, W., Berkvens, D. and Geerts, S. (2000) Sero-Epidemiological Study of Taenia saginata Cysticerci in Belgian Cattle. Veterinary Parasitology, 88, 43-49. https://doi.org/10.1016/S0304-4017(99)00196-X
[45]	Oryan, A., Moghaddar, N. and Gaur, S. (1995) Taenia saginata Cysticercosis in Cattle with Special Reference to Its Prevalence, Pathogenesis and Economic Implications in Fars Province of Iran. Veterinary Parasitology, 57, 319-327. https://doi.org/10.1016/0304-4017(94)00691-5
[46]	Lopes, W.D.Z., Cruz, B.C., Soares, V.E., Nunes, J.L.N., Teixeira, W.F.P., Maciel, W.G., Buzzulini, C., Pereira, J.C.M., Felippelli, G., Soccol, V.T., de Oliveira G.P. and da Costa, A.J. (2014) Historic of Therapeutic Efficacy of Albendazol Sulphoxide Administered in Different Routes, Dosages and Treatment Schemes, against Taenia saginata Cysticercus in Cattle Experimentally Infected. Experimental Parasitology, 137, 14-20. https://doi.org/10.1016/j.exppara.2013.11.007
[47]	Garcia, J.J., Bolas, F. and Torrado, J.J. (2003) Bioavailability and Efficacy Characteristics of Two Different Oral Liquid Formulations of Albendazole. International Journal of Pharmaceutics, 250, 351-358. https://doi.org/10.1016/S0378-5173(02)00559-8
[48]	Barbosa, F.C., Cabral, D.D. and Sopelete, M.C. (2003) Eficácia do sulfóxido de albendazol na cisticercose bovina. Hora Vet, 132, 18-20.
[49]	Jung-Cook, H. (2012) Pharmacokinetic Variability of Anthelmintics: Implications for the Treatment of Neurocysticercosis. Expert Review of Clinical Pharmacology, 5, 21-30. https://doi.org/10.1586/ecp.11.72
[50]	Jaheed, E., Mohamed, A.H., Hassan, N.M.F., Mahran, K.M.A., Nasr, S.M. and Abou-Zeina, H.A.A. (2019) Evaluation of the Curative Effect of Balanites aegyptiaca Fruits Ethanolic Extract on Haemonchosis Experimentally Induced in Egyptian Baladi Goats: Phytoanalytical, Parasitological and Hematological Studies. Journal of Parasitic Diseases, 43, 638-650. https://doi.org/10.1007/s12639-019-01143-1
[51]	Shalaby, H.A., El Namaky, A.H., Khalil, F.A. and Kandil, O.M. (2012) Efficacy of Methanolic Extract of Balanites aegyptiaca Fruit on Toxocara vitulorum. Veterinary Parasitology, 183, 386-392. https://doi.org/10.1016/j.vetpar.2011.07.045
[52]	Shalaby, H., Nasr, S. and Farag, T. (2016) Tegumental Effects of Methanolic Extract of Balanites aegyptiaca Fruits on Adult Paramphistomum microbothrium (Fischoeder 1901) under Laboratory Conditions. Iranian Journal of Parasitology, 11, 396-405.
[53]	Shalaby, H.A., Hassan, N.M.F., Nasr, S.M., Farag, T.K., Abu El Ezz, N.M.T. and Abou-Zeina, H.A.A. (2020) An Anthelmintic Assessment of Balanites aegyptiaca Fruits on Some Multiple Drug Resistant Gastrointestinal Helminthes Affecting Sheep. Egyptian Journal of Veterinary Sciences, 51, 93-103. https://doi.org/10.21608/ejvs.2019.19195.1119
[54]	Gnoula, C., Guissou, P., Duez, P., Frederich, M. and Dubois, J. (2007) Nematocidal Compounds from the Seeds of Balanites aegyptiaca Isolation and Structure Elucidation. International Journal of Pharmacology, 3, 280-284. https://doi.org/10.3923/ijp.2007.280.284
[55]	Wiesman, Z. and Chapagain, B.P. (2006) Larvicidal Activity of Saponin Containing Extracts and Fractions of Fruit Mesocarp of Balanites aegyptiaca. Fitoterapia, 77, 420-424. https://doi.org/10.1016/j.fitote.2006.05.012
[56]	Jaja-Chimedza, A., Graf, B.L., Simmler, C., Kim, Y., Kuhn, P., Pauli, G.F., et al. (2017) Biochemical Characterization and Anti-Inflammatory Properties of an Isothiocyanate-Enriched Moringa (Moringa oleifera) Seed Extract. PLOS ONE, 12, e0182658. https://doi.org/10.1371/journal.pone.0182658
[57]	Wang, L., Chen, X. and Wu, A. (2016) Mini Review on Antimicrobial Activity and Bioactive Compounds of Moringa oleifera. Medicinal chemistry, 6, 578-582. https://doi.org/10.4172/2161-0444.1000402
[58]	Cabardo Jr., D.E. and Portugaliza, H.P. (2017) Anthelmintic Activity of Moringa oleifera Seed Aqueous and Ethanolic Extracts against Haemonchus contortus Eggs and Third Stage Larvae. International Journal of Veterinary Science and Medicine, 5, 30-34. https://doi.org/10.1016/j.ijvsm.2017.02.001
[59]	Mead, J. and McNair, N. (2006) Antiparasitic Activity of Flavonoids and Isoflavones against Cryptosporidium parvum and Encephalitozoon intestinalis. FEMS Microbiology Letters, 259, 153-157. https://doi.org/10.1111/j.1574-6968.2006.00263.x
[60]	Boshtam, M., Asgary, S., Kouhpayeh, S., Shariati, L. and Khanahmad, H. (2017) Aptamers against Pro- and Anti-Inflammatory Cytokines: A Review. Inflammation, 40, 340-349. https://doi.org/10.1007/s10753-016-0477-1
[61]	Palma, S., Chile, N., Carmen-Orozco, R.P., Trompeter, G., Fishbeck, K., Cooper,V., et al. (2019) In Vitro Model of Postoncosphere Development, and in Vivo Infection Abilities of Taenia solium and Taenia saginata. PLOS Neglected Tropical Diseases, 13, e0007261. https://doi.org/10.1371/journal.pntd.0007261
[62]	González, R., Ballester, I., López-Posadas, R., Suárez, M.D., Zarzuelo, A., Martínez-Augustin, O. and Sánchez de Medina, F. (2011) Effects of Flavonoids and Other Polyphenols on Inflammation. Critical Reviews in Food Science and Nutrition, 51, 331-362. https://doi.org/10.1080/10408390903584094
[63]	Comalada, M., Ballester, I., Bailon, E., Sierra, S., Xaus, J., de Medina, F. and Zarzuelo, A. (2006) Inhibition of Pro-Inflammatory Markers in Primary Bone Marrow-Derived Mouse Macrophages by Naturally Occurring Flavonoids: Analysis of the Structure-Activity Relationship. Biochemical Pharmacology, 72, 1010-1021. https://doi.org/10.1016/j.bcp.2006.07.016
[64]	Kim, Y., Wu, A.G., Jaja-Chimedza, A., Graf, B.L., Waterman, C., Verzi, M.P., et al. (2017) Isothiocyanate-Enriched Moringa Seed Extract Alleviates Ulcerative Colitis Symptoms in Mice. PLOS ONE, 12, e0184709. https://doi.org/10.1371/journal.pone.0184709
[65]	Vazquez, V. and Sotelo, J. (1992) The Course of Seizures after Treatment for Cerebral Cysticercosis. The New England Journal of Medicine, 327, 696-701. https://doi.org/10.1056/NEJM199209033271005