Hostname: page-component-848d4c4894-2pzkn Total loading time: 0 Render date: 2024-06-03T09:00:07.470Z Has data issue: false hasContentIssue false

An in vivo appraisal of Punica granatum peel extract’s ultrastructural effect on cystic echinococcosis in mice

Published online by Cambridge University Press:  13 May 2024

Nashaat E. Nassef
Affiliation:
Parasitology Department, Faculty of Medicine, Menoufia University, Yassin Abdel Ghaffar St. from Gamal Abdel Nasser St., Shebin El-Kom, Menoufia, Egypt
Sawsan S. Shendi
Affiliation:
Department of Clinical and Molecular Parasitology Department, National Liver Institute, Menoufia University, Shebin El-Kom, Menoufia, Egypt
Abdel-Gawad E. Saad
Affiliation:
Department of Clinical and Molecular Parasitology Department, National Liver Institute, Menoufia University, Shebin El-Kom, Menoufia, Egypt
Nancy M. Harba
Affiliation:
Parasitology Department, Faculty of Medicine, Menoufia University, Yassin Abdel Ghaffar St. from Gamal Abdel Nasser St., Shebin El-Kom, Menoufia, Egypt
Engy V.N. Beshay
Affiliation:
Parasitology Department, Faculty of Medicine, Menoufia University, Yassin Abdel Ghaffar St. from Gamal Abdel Nasser St., Shebin El-Kom, Menoufia, Egypt
Asmaa Shams El-Dein Mohamed
Affiliation:
Pathology Department, Faculty of Medicine, Menoufia University, Shebin El-Kom, Egypt
Marwa A. Gouda*
Affiliation:
Department of Clinical and Molecular Parasitology Department, National Liver Institute, Menoufia University, Shebin El-Kom, Menoufia, Egypt
*
Corresponding author: Marwa A. Gouda; Email: marwa_goda@liver.menofia.edu.eg

Abstract

In the past decade, interest has significantly increased regarding the medicinal and nutritional benefits of pomegranate (Punica granatum) peel. This study examined the effects of using pomegranate peel extract (PGE) alone and in combination with albendazole (ABZ) on ultrastructural and immunological changes in cystic echinococcosis in laboratory-infected mice. Results revealed that the smallest hydatid cyst size and weight (0.48 ± 0.47mm, 0.17 ± 0.18 gm) with the highest drug efficacy (56.2%) was detected in the PGE + ABZ group, which also exhibited marked histopathological improvement. Ultrastructural changes recorded by transmission electron microscopy including fragmentation of the nucleus, glycogen depletion, and multiple lysosomes in vacuolated cytoplasm were more often observed in PGE + ABZ group. IFN-γ levels were significantly increased in the group treated with ABZ, with a notable reduction following PGE treatment, whether administered alone or in combination with ABZ. Thus, PGE enhanced the therapeutic efficiency of ABZ, with improvement in histopathological and ultrastructural changes.

Type
Research Paper
Copyright
© The Author(s), 2024. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abdelbaset, AE, Yagi, K, Nonaka, N, Nakao, R (2021). Cystic echinococcosis in humans and animals in Egypt: An epidemiological overview. Current Research in Parasitology & Vector-Borne Diseases 1, 100061. https://doi.org/10.1016/j.crpvbd.2021.100061CrossRefGoogle ScholarPubMed
Alexova, R, Alexandrova, S, Dragomanova, S, Kalfin, R, Solak, A, Mehan, S, Petralia, M C, Fagone, P, Mangano, K, Nicoletti, F, Tancheva, L (2023). Anti-COVID-19 potential of ellagic acid and polyphenols of Punica granatum L. Molecules 28, 3772. https://doi.org/10.3390/molecules28093772CrossRefGoogle ScholarPubMed
Amri, M, Aissa, SA, Belguendouz, H, Mezioug, D, Touil-Boukoffa, C (2007). In vitro antihydatic action of IFN-gamma is dependent on the nitric oxide pathway. Journal of Interferon & Cytokine Research 27, 781787. https://doi.org/10.1089/jir.2007.0003CrossRefGoogle ScholarPubMed
Atayi, Z, Borji, H, Moazeni, M, Saboor Darbandi, M, Heidarpour, M (2018). Zataria multiflora would attenuate the hepatotoxicity of long-term albendazole treatment in mice with cystic echinococcosis. Parasitology International 67, 184187. https://doi.org/10.1016/j.parint.2017.11.007CrossRefGoogle ScholarPubMed
Calzada, F, Yépez-Mulia, L, Aguilar, A (2006). In vitro susceptibility of Entamoeba histolytica and Giardia lamblia to plants used in Mexican traditional medicine for the treatment of gastrointestinal disorders. Journal of Ethnopharmacology 108, 367370. https://doi.org/10.1016/j.jep.2006.05.025CrossRefGoogle ScholarPubMed
Corfield, A P (2015). Mucins: A biologically relevant glycan barrier in mucosal protection. Biochimica et Biophysica Acta 1850, 236252. https://doi.org/10.1016/j.bbagen.2014.05.003CrossRefGoogle ScholarPubMed
Díaz, Á (2017). Immunology of cystic echinococcosis (hydatid disease). British Medical Bulletin 124, 121133. https://doi.org/10.1093/bmb/ldx033.Google ScholarPubMed
Dikmen, M, Ozturk, N, Ozturk, Y (2011). The antioxidant potency of Punica granatum L. Fruit peel reduces cell proliferation and induces apoptosis on breast cancer. Journal of Medicinal Food 14, 16381646. https://doi.org/10.1089/jmf.2011.0062CrossRefGoogle ScholarPubMed
El-Sherbini, GT, El Gozamy, BR, Abdel-Hady, NM, Morsy, TA (2009). Efficacy of two plant extracts against vaginal trichomoniasis. Journal of the Egyptian Society of Parasitology 39, 4758.Google ScholarPubMed
Elissondo, M, Dopchiz, M, Ceballos, L, Alvarez, L, Sánchez Bruni, S, Lanusse, C, Denegri, G (2006). In vitro effects of flubendazole on Echinococcus granulosus protoscoleces. Parasitology Research 98, 317323. https://doi.org/10.1007/s00436-005-0026-6CrossRefGoogle ScholarPubMed
Ge, S, Duo, L, Wang, J, GegenZhula, , Yang, J, Li, Z, Tu, Y (2021). A unique understanding of traditional medicine of pomegranate, Punica granatum L. and its current research status. Journal of Ethnopharmacology 271, 113877. https://doi.org/10.1016/j.jep.2021.113877CrossRefGoogle ScholarPubMed
Harries, ML (1989). Carleton’s Histopathological Technique. New York, Toronto: Oxford University Press.Google Scholar
Hayouni, EA, Miled, K, Boubaker, S, Bellasfar, Z, Abedrabba, M, Iwaski, H, Oku, H, Matsui, T, Limam, F, Hamdi, M (2011). Hydroalcoholic extract based-ointment from Punica granatum L. peels with enhanced in vivo healing potential on dermal wounds. Phytomedicine 18, 976984. https://doi.org/10.1016/j.phymed.2011.02.011CrossRefGoogle ScholarPubMed
Heidarpour, M, Mohri, M, Borji, H, Moghdass, E (2012). Oxidative stress and trace elements in camel (Camelus dromedarius) with liver cystic echinococcosis. Veterinary Parasitology 187, 459463. https://doi.org/10.1016/j.vetpar.2012.01.015CrossRefGoogle ScholarPubMed
Jelowdar, A, Rafiei, A, Abbaspour, MR, Rashidi, I, Rahdar, M (2017). Efficacy of combined albendazol and praziquntel and their loaded solid lipid nanoparticles components in chemoprophylaxis of experimental hydatidosis. Asian Pacific Journal of Tropical Biomedicine 7, 549554. https://doi.org/10.1016/j.apjtb.2017.05.011CrossRefGoogle Scholar
Jurenka, JS (2008). Therapeutic applications of pomegranate (Punica granatum L.): a review. Alternative Medicine Review 13, 128144.Google ScholarPubMed
Kanatt, SR, Chander, R, Sharma, A (2010). Antioxidant and antimicrobial activity of pomegranate peel extract improves the shelf life of chicken products. International Journal of Food Science & Technology 45, 216222. https://doi.org/10.1111/j.1365-2621.2009.02124.xCrossRefGoogle Scholar
Kern, P, Menezes da Silva, A, Akhan, O, Müllhaupt, B, Vizcaychipi, KA, Budke, C, Vuitton, DA (2017). The Echinococcoses: Diagnosis, clinical management and burden of disease. Advances in Parasitology 96, 259369. https://doi.org/10.1016/bs.apar.2016.09.006CrossRefGoogle ScholarPubMed
Kim, S-H, Lee, H-S, Ryu, D-S, Choi, S-J, Lee, D-S (2011). Antibacterial activity of silver-nanoparticles against Staphylococcus aureus and Escherichia coli. Microbiology and Biotechnology Letters 39, 7785.Google Scholar
Küster, T, Stadelmann, B, Aeschbacher, D, Hemphill, A (2014). Activities of fenbendazole in comparison with albendazole against Echinococcus multilocularis metacestodes in vitro and in a murine infection model. International Journal of Antimicrobial Agents 43, 335342. https://doi.org/10.1016/j.ijantimicag.2014.01.013CrossRefGoogle Scholar
Labsi, M, Khelifi, L, Mezioug, D, Soufli, I, Touil-Boukoffa, C (2016). Antihydatic and immunomodulatory effects of Punica granatum peel aqueous extract in a murine model of echinococcosis. Asian Pacific Journal of Tropical Medicine 9, 211220. https://doi.org/10.1016/j.apjtm.2016.01.038CrossRefGoogle Scholar
Labsi, M, Soufli, I, Khelifi, L, Amir, ZC, Touil-Boukoffa, C (2019). A preventive effect of the combination of albendazole and pomegranate peel aqueous extract treatment in cystic echinococcosis mice model: An alternative approach. Acta Tropica 197, 105050. https://doi.org/10.1016/j.actatropica.2019.105050CrossRefGoogle ScholarPubMed
Lacey, E (1990). Mode of action of benzimidazoles. Parasitology Today 6, 112115. https://doi.org/10.1016/0169-4758(90)90227-uCrossRefGoogle ScholarPubMed
Mahmoudi, S, Mamishi, S, Banar, M, Pourakbari, B, Keshavarz, H (2019). Epidemiology of echinococcosis in Iran: A systematic review and meta-analysis. BMC Infectious Diseases 19, 929. https://doi.org/10.1186/s12879-019-4458-5CrossRefGoogle ScholarPubMed
Middha, SK, Usha, T, RaviKiran, T (2012). Influence of Punica granatum L. on region specific responses in rat brain during Alloxan-Induced diabetes. Asian Pacific Journal of Tropical Biomedicine 2, S905S909. https://doi.org/10.1016/S2221-1691(12)60334-7CrossRefGoogle Scholar
Moazeni, M, Roozitalab, A (2012). High scolicidal effect of Zataria multiflora on protoccoleces of hydatid cyst: an in vitro study. Comparative Clinical Pathology 21, 99104. https://doi.org/10.1007/s00580-010-1069-3CrossRefGoogle Scholar
Mourglia-Ettlin, G, Marqués, JM, Chabalgoity, JA, Dematteis, S (2011). Early peritoneal immune response during Echinococcus granulosus establishment displays a biphasic behavior. PLoS Neglected Tropical Diseases 5, e1293. https://doi.org/10.1371/journal.pntd.0001293CrossRefGoogle ScholarPubMed
Pensel, PE, Ullio Gamboa, G, Fabbri, J, Ceballos, L, Sanchez Bruni, S, Alvarez, LI, Allemandi, D, Benoit, JP, Palma, SD, Elissondo, MC (2015). Cystic echinococcosis therapy: Albendazole-loaded lipid nanocapsules enhance the oral bioavailability and efficacy in experimentally infected mice. Acta Tropica 152, 185194. https://doi.org/10.1016/j.actatropica.2015.09.016CrossRefGoogle ScholarPubMed
Riganò, R, Buttari, B, De Falco, E, Profumo, E, Ortona, E, Margutti, P, Scottà, C, Teggi, A, Siracusano, A (2004). Echinococcus granulosus-specific T-cell lines derived from patients at various clinical stages of cystic echinococcosis. Parasite Immunology 26, 4552. https://doi.org/10.1111/j.0141-9838.2004.00682.xCrossRefGoogle ScholarPubMed
Rogan, MT (1998). T-cell activity associated with secondary infections and implanted cysts of Echinococcus granulosus in BALB/c mice. Parasite Immunology 20, 527533. https://doi.org/10.1046/j.1365-3024.1998.00180.xCrossRefGoogle ScholarPubMed
Shaygannia, E, Bahmani, M, Zamanzad, B, Rafieian-Kopaei, M (2016). A review study on Punica granatum L. Journal of Evidence-Based Complementary & Alternative Medicine 21, 221227. https://doi.org/10.1177/2156587215598039CrossRefGoogle Scholar
Shi, H, Lei, Y, Wang, B, Wang, Z, Xing, G, Lv, H, Jiang, Y (2016). Protoscolicidal effects of chenodeoxycholic acid on protoscoleces of Echinococcus granulosus. Experimental Parasitology 167, 7682. https://doi.org/10.1016/j.exppara.2016.05.004CrossRefGoogle ScholarPubMed
Shirgholami, Z, Borji, H, Mohebalian, H, Heidarpour, M (2021). Effects of Allium sativum on IFN-γ and IL4 concentrations in mice with cystic echinococcosis. Experimental Parasitology 220, 108042. https://doi.org/10.1016/j.exppara.2020.108042CrossRefGoogle ScholarPubMed
Siles-Lucas, M, Casulli, A, Cirilli, R, Carmena, D (2018). Progress in the pharmacological treatment of human cystic and alveolar echinococcosis: Compounds and therapeutic targets. PLoS Neglected Tropical Diseases 12, e0006422. https://doi.org/10.1371/journal.pntd.0006422CrossRefGoogle ScholarPubMed
Singh, B, Singh, JP, Kaur, A, Singh, N (2018). Phenolic compounds as beneficial phytochemicals in pomegranate (Punica granatum L.) peel: A review. Food Chemistry 261, 7586. https://doi.org/10.1016/j.foodchem.2018.04.039CrossRefGoogle ScholarPubMed
Urrea-París, M, Moreno, M, Casado, N, Rodriguez-Caabeiro, F (2002). Relationship between the efficacy of praziquantel treatment and the cystic differentiation in vivo of Echinococcus granulosus metacestode. Parasitology Research 88, 2631. https://doi.org/10.1007/s004360100468CrossRefGoogle ScholarPubMed
Verma, VC, Gangwar, M, Yashpal, M, Nath, G (2013). Anticestodal activity of endophytic Pestalotiopsis sp. on protoscoleces of hydatid cyst Echinococcus granulosus. BioMed Research International 2013, 308515. https://doi.org/10.1155/2013/308515CrossRefGoogle ScholarPubMed
Wen, H, Vuitton, L, Tuxun, T, Li, J, Vuitton, DA, Zhang, W, McManus, DP (2019). Echinococcosis: Advances in the 21st Century. Clinical Microbiology Reviews 32, e0007518. https://doi.org/10.1128/CMR.00075-18CrossRefGoogle ScholarPubMed
WHO (2022). Ending the Neglect to Attain the Sustainable Development Goals: A Rationale for Continued Investment in Tackling Neglected Tropical Diseases 2021–2030. Geneva: World Health Organization.Google Scholar
Xu, X, Lu, X, Dong, X, Luo, Y, Wang, Q, Liu, X, Fu, J, Zhang, Y, Zhu, B, Ma, X (2017). Effects of hMASP-2 on the formation of BCG infection-induced granuloma in the lungs of BALB/c mice. Scientific Reports 7, 2300. https://doi.org/10.1038/s41598-017-02374-zCrossRefGoogle ScholarPubMed
Yin, J, Liu, C, Shen, Y, Zhang, H, Cao, J (2018). Efficacy of ursolic acid against Echinococcus granulosus in vitro and in a murine infection model. Parasites & Vectors 11, 58. https://doi.org/10.1186/s13071-018-2628-8CrossRefGoogle Scholar
Zhang, G, Wang, J, Luo, Y, Yuan, M, Gao, Q, Gao, H, Song, X, Shi, Y, Dong, K, Ma, X (2018). In vivo evaluation of the efficacy of Sophora moorcroftiana alkaloids in combination with Bacillus Calmette-Guérin (BCG) treatment for cystic echinococcosis in mice. Journal of Helminthology 92, 681686. https://doi.org/10.1017/S0022149X1700089XCrossRefGoogle ScholarPubMed
Zhang, S, Zhou, Y, Su, L, Zhang, X, Wang, H, Liu, B (2017). In vivo evaluation of the efficacy of combined albedazole-IFN-α treatment for cystic echinococcosis in mice. Parasitology Research 116, 735742. https://doi.org/10.1007/s00436-016-5339-0CrossRefGoogle ScholarPubMed