Hostname: page-component-848d4c4894-cjp7w Total loading time: 0 Render date: 2024-06-17T20:21:39.790Z Has data issue: false hasContentIssue false

Activities of pumpkin seed oil against Biomphalaria alexandrina snails and the infective stages of Schistosoma mansoni with special emphasis on genotoxic and histopathological alterations

Published online by Cambridge University Press:  21 March 2024

S.E. Mohammed
Affiliation:
Medical Parasitology Department, Faculty of Medicine, Ain Shams University, Cairo, Egypt
H.S. Mossalem
Affiliation:
Environmental Research and Medical Malacology Division, Theodore Bilharz Research Institute, Imbaba, Giza, Egypt
R.M. Gad El-Karim
Affiliation:
Environmental Research and Medical Malacology Division, Theodore Bilharz Research Institute, Imbaba, Giza, Egypt
A.T. Morsy
Affiliation:
Respiratory Care Technology Department, Faculty of Applied Health Science Technology, Misr University for Science and Technology, Giza, Egypt
A.M. Ammar*
Affiliation:
Medical Parasitology Department, Faculty of Medicine, Ain Shams University, Cairo, Egypt
*
Corresponding author: A.M. Ammar; Email: dr_asma_mostafa@med.asu.edu.eg

Abstract

Schistosomiasis is a serious health issue in tropical regions, and natural compounds have gained popularity in medical science. This study investigated the potential effects of pumpkin seed oil (PSO) on Biomphalaria [B.] alexandrina snails (Ehrenberg, 1831), Schistosoma [S.] mansoni (Sambon, 1907) miracidium, and cercariae. The chemical composition of PSO was determined using gas chromatography/mass spectrometry. A bioassay was performed to evaluate the effects of PSO on snails, miracidia, and cercariae. The results showed no significant mortality of B. alexandrina snails after exposure to PSO, but it caused morphological changes in their hemocytes at 1.0 mg/ml for 24 hours. PSO exhibited larvicidal activity against miracidia after 2 hours of exposure at a LC50 of 618.4 ppm. A significant increase in the mortality rate of miracidia was observed in a dose- and time-dependent manner, reaching a 100% death rate after 10 minutes at LC90 and 15 minutes at LC50 concentration. PSO also showed effective cercaricidal activity after 2 hours of exposure at a LC50 of 290.5 ppm. Histological examination revealed multiple pathological changes in the digestive and hermaphrodite glands. The PSO had genotoxic effects on snails, which exhibited a significant increase [p≤0.05] in comet parameters compared to the control. The findings suggest that PSO has potential as a molluscicide, miracidicide, and cercaricide, making it a possible alternative to traditional molluscicides in controlling schistosomiasis.

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

Abaza, BE, Hamza, RS, Farag, TI, Abdel-Hamid, MA, and Moustafa, RA (2016) Characterization of the hemocytes of susceptible and resistant Biomphalaria alexandrina snail. Journal of the Egyptian Society of Parasitology 46(3), 671682. doi: 10.21608/JESP.2016.88324.Google ScholarPubMed
Abdel-Azeem, HH, Mohamed, AH, and Habib, MR (2023) Biochemical and histopathological responses of Biomphalaria alexandrina to RIPEX (plant growth regulator). Beni-Suef University Journal of Basic and Applied Sciences 12(1), 111. doi: 10.1186/s43088-023-00378-5.CrossRefGoogle Scholar
Abuseir, S (2023) A systematic review of frequency and geographic distribution of water-borne parasites in the Middle East and North Africa. Eastern Mediterranean Health Journal 29(2), 151161. doi: 10.26719/emhj.23.016.CrossRefGoogle ScholarPubMed
Ali, RE and Gad El-Karim, RM (2023) Impact of Ferula hermonis roots methanol extract on genotoxic, biochemical and reproductive aspects of Biomphalaria alexandrina snails. Egyptian Journal of Aquatic Biology and Fisheries 27(4), 127142. doi: 10.21608/ejabf.2023.307666.CrossRefGoogle Scholar
Al-Khalaifah, H (2022) Cellular and humoral immune response between snail hosts and their parasites. Frontiers in Immunology 13(981314). doi: 10.3389/fimmu.2022.981314.CrossRefGoogle ScholarPubMed
Al-Okbi, SY, Mohamed, DA, Kandil, E, and Ahmed, EK (2014) Functional ingredients and cardiovascular protective effect of pumpkin seed oils. Grasas Aceites 65(1), e007. doi: 10.3989/gya.062813.CrossRefGoogle Scholar
Ayyildiz, HF, Topkafa, M, and Kara, H (2019) Pumpkin (Cucurbita pepo L.) seed oil. In Fruit Oils: Chemistry and Functionality. Germany: Springer Nature, 765–88. doi: 10.1007/978-3-030-12473-1_41.CrossRefGoogle Scholar
Benalia, M, Djeridane, A, Gourine, N, Nia, S, Ajandouz, E, and Yousfi, M (2015) Fatty acid profile, tocopherols content and antioxidant activity of Algerian pumpkin seeds oil (Cucurbita pepo L). Mediterranean Journal of Nutrition and Metabolism 8(1), 925. doi: 10.3233/MNM-140023.CrossRefGoogle Scholar
Beshay, EV, Rady, AA, Afifi, AF, and Mohamed, AH (2019) Schistosomicidal, antifibrotic, and antioxidant effects of Cucurbita pepo L. seed oil and praziquantel combined treatment for Schistosoma mansoni infection in a mouse model. Journal of Helminthology 93(3), 286294. doi: 10.1017/S0022149X18000317.CrossRefGoogle Scholar
Cavalcanti, MG, Mendonça, AM, Duarte, GR, Barbosa, CC, De Castro, CM, Alves, LC, and Brayner, FA (2012) Morphological characterization of hemocytes from Biomphalaria glabrata and Biomphalaria straminea. Micron 43(2–3), 285291. doi: 10.1016/j.micron.2011.09.002.CrossRefGoogle ScholarPubMed
Coelho, PM and Caldeira, RL (2016) Critical analysis of molluscicide application in schistosomiasis control programs in Brazil. Infectious Diseases of Poverty 5(1), 57. doi: 10.1186/s40249-016-0153-6.CrossRefGoogle ScholarPubMed
Collins, A, Møller, P, Gajski, G, Vodenková, S, Abdulwahed, A, Anderson, D, Bankoglu, EE, Bonassi, S, Boutet-Robinet, E, Brunborg, G, and Chao, C (2023) Measuring DNA modifications with the comet assay: a compendium of protocols. Nature Protocols 18(3), 929989. doi: 10.1038/s41596-022-00754-y.CrossRefGoogle ScholarPubMed
Csikós, E, Horváth, A, Ács, K, Papp, N, Balázs, VL, Dolenc, MS, Kenda, M, Kočevar Glavač, N, Nagy, M, Protti, M, and Mercolini, L (2021) Treatment of benign prostatic hyperplasia by natural drugs. Molecules 26(23), 7141. doi: 10.3390/molecules26237141.CrossRefGoogle ScholarPubMed
El Sayed, K, Soliman, MG, Elfekky, FA, and Ouf, NA (2017) Susceptibility of Biomphalaria alexandrina snails to infection with Schistosoma mansoni miracidia under the effect of sodium alginates as an immunostimulant. European Journal of Biomedicine and Biotechnology 4(5), 115123.Google Scholar
El-Gindy, HI, Rawi, SM, and Abdel-Kader, A (1991) Comparative effect of different pesticides on the transaminases activities in hemolymph of Biomphalaria alexandrina snails. Journal of Egyptian Geriatric Society Zoology 6(2), 131138.Google Scholar
El-Karim, G (2022) Assessment of the antioxidant capacity of Lanistes carinatus tissue extract and its immune-boosting influence on Biomphalaria alexandrina against infection with Schistosoma mansoni. Egyptian Journal of Aquatic Biology and Fisheries 26(4), 361376. doi: 10.21608/ejabf.2022.249977.CrossRefGoogle Scholar
Eveland, LK and Haseeb, MA (2011) Laboratory Rearing of Biomphalaria glabrata Snails and Maintenance of Larval Schistosomes In Vivo and In Vitro. In: Toledo, R and Fried, B. (eds) Biomphalaria Snails and Larval Trematodes. New York, NY: Springer. pp 3355 doi: 10.1007/978-1-4419-7028-2_2.CrossRefGoogle Scholar
Fried, B (2016) An update on hemocytes in Biomphalaria snails. Journal of Hematology and Oncology Research 2(2), 2036. doi: 10.14302/issn.2372-6601.jhor-14-401.CrossRefGoogle Scholar
Grzybek, M, Kukula-Koch, W, Strachecka, A, Jaworska, A, Phiri, AM, Paleolog, J, and Tomczuk, K (2016) Evaluation of anthelmintic activity and composition of pumpkin (Cucurbita pepo L.) seed extracts—in vitro and in vivo studies. International Journal of Molecular Sciences 17(9), 1456. doi: 10.3390/ijms17091456.CrossRefGoogle Scholar
Habib, MR, Ghoname, SI, Ali, RE, El-Karim, RM, Youssef, AA, Croll, RP, and Miller, MW (2020) Biochemical and apoptotic changes in the nervous and ovotestis tissues of Biomphalaria alexandrina following infection with Schistosoma mansoni. Experimental Parasitology 213(Suppl C), 107887. doi: 10.1016/j.exppara.2020.107887.CrossRefGoogle ScholarPubMed
Hussein, SN and Shukur, MS (2020) In-vitro anthelmentic efficacy of pumpkin seed oil (Cucurbita pepo) on toxocariosis (Toxocara cati). Exploratory Animal & Medical Research 10(2), 154161.Google Scholar
Ibrahim, AM, El-Karim, RMG, Ali, RE, and Nasr, SM (2023) Toxicological effects of Saponin on the free larval stages of Schistosoma mansoni, infection rate, some biochemical and molecular parameters of Biomphalaria alexandrina snails. Pesticide Biochemistry and Physiology 191, 105357. doi: 10.1016/j.pestbp.CrossRefGoogle ScholarPubMed
Ibrahim, AM, Ghoname, SI, Mansour, SM, and El-Dafrawy, SM (2020) Effect of some medicinal plant extracts as molluscicidal and apoptotic agents on Biomphalaria alexandrina snails. Egyptian Journal of Aquatic Biology and Fisheries 24(2), 291300. doi: 10.21608/ejabf.2020.80284.CrossRefGoogle Scholar
Ježek, J, Mirtič, K, Rešetič, N, Hodnik, JJ, and Rataj, AV (2021) The effect of pumpkin seed cake and ground cloves (Syzygium aromaticum) supplementation on gastrointestinal nematode egg shedding in sheep. Parasite 28, 78 doi: 10.1051/parasite/2021076.CrossRefGoogle Scholar
Kengne Fokam, AC, Sumo, L, Bagayan, M, Nana-Djeunga, HC, Kuete, T, Nganjou, GSO, Tchami Mbagnia, MC, Djune-Yemeli, L, Wondji, CS, and Njiokou, F (2022) Exposition of intermediate hosts of schistosomes to Niclosamide (Bayluscide WP 70) revealed significant variations in mortality rates: implications for vector control. International Journal of Environmental Research and Public Health 19(19), 12873. doi: 10.3390/ijerph1 91912873.CrossRefGoogle ScholarPubMed
Larson, MD, Greenwood, D, Flanigan, K, and Krist, AC (2023) Field surveys reveal physicochemical conditions promoting occurrence and high abundance of an invasive freshwater snail (Potamopyrgus antipodarum). Aquatic Invasions 18(1), 83102. doi: 10.3391/ai.2023.18.1.103389.CrossRefGoogle Scholar
Le Clec’h, W, Anderson, TJ, and Chevalier, FD (2016) Characterization of hemolymph phenoloxidase activity in two Biomphalaria snail species and impact of Schistosoma mansoni infection. Parasites & Vectors 9, 111; doi: 10.1186/s13071-016-1319-6CrossRefGoogle ScholarPubMed
Manneck, T, Haggenmüller, Y, and Keiser, J (2010) Morphological effects and tegumental alterations induced by mefloquine on schistosomula and adult flukes of Schistosoma mansoni. Parasitology, 137(1), 85 98. doi: 10.1017/S0031182009990965.CrossRefGoogle ScholarPubMed
Moigradean, D, Poiana, MA, Alda, LM, and Gogoasa, I (2013) Quantitative identification of fatty acids from walnut and coconut oils using GC-MS method. Journal of Agroalimentary Processes and Technologies 19(4), 459463.Google Scholar
Mossalem, HS, Abdel-Hamid, H, and El-Shinnawy, NA (2013) Impact of artemether on some histological and histochemical parameters in Biomphalaria alexandrina. African Journal of Pharmacy and Pharmacology 7(31), 22202230. http://www.academicjournals.org/AJPP.CrossRefGoogle Scholar
Mossalem, HS and ElEnain, GL (2014) Evaluation of the pesticide Emamectin and methanol extract of wheat bran against Biomphalaria alexandrina snails, their hemocytes and their infection with Schistosoma mansoni. Agriculture and Food Sciences Research 1(1), 510. http://asianonlinejournals.com/index.php/AESR/article/view/182/159.Google Scholar
Mossalem, HS (2018) Effect of Mentha longifolia L (Family Lamiacea) ethanol extract on Cercarea, miracidia of Schistosoma mansoni by Scanned electron microscopy and Biomphalaria alexandrina. International Journal of Scientific & Engineering Research 9, 11661177.Google Scholar
Mtemeli, FL, Walter, I, and Shoko, R (2020) Molluscicidal effects of pumpkin seed extracts on Schistosoma vectors. Authorea preprint.Google Scholar
Mtemeli, FL, Walter, I, Tinago, T, and Shoko, R (2021) An assessment of the molluscicidal potential of Cucurbita maxima seed extracts on Biomphalaria pfeifferi and Bulinus globosus snails. All Life 14(1), 244255. doi: 10.1080/26895293.2021.1901788.CrossRefGoogle Scholar
Nandhakumar, S, Parasuraman, S, Shanmugam, MM, Rao, KR, Chand, P, and Bhat, BV (2011) Evaluation of DNA damage using single-cell gel electrophoresis (comet assay). Journal of Pharmacology & Pharmacotherapeutics 2(2), 107. doi: 10.4103/0976-500X.81903.Google ScholarPubMed
Oliveira, ALD, Levada, PM, Zanotti-Magalhaes, EM, Magalhães, LA, and Ribeiro-Paes, JT (2010) Differences in the number of hemocytes in the snail host Biomphalaria tenagophila, resistant and susceptible to Schistosoma mansoni infection. Genetics and Molecular Research 9(4), 24362445. doi: 10.4238/vol9-4gmr1143.CrossRefGoogle ScholarPubMed
Pereira Moreira, B, Weber, MH, Haeberlein, S, Mokosch, AS, Spengler, B, Grevelding, CG, and Falcone, FH (2022) Drug repurposing and de novo drug discovery of protein kinase inhibitors as new drugs against schistosomiasis. Molecules 27(4), 1414. doi: 10.3390/molecules27041414.CrossRefGoogle ScholarPubMed
Prommaban, A, Kuanchoom, R, Seepuan, N, and Chaiyana, W (2021) Evaluation of fatty acid compositions, antioxidant, and pharmacological activities of pumpkin (Cucurbita moschata) seed oil from aqueous enzymatic extraction. Plants 10(8), 1582. doi: 10.3390/plants10081582.CrossRefGoogle ScholarPubMed
Ritchie, LS, Lorez, V, and Cora, JM (1974) Prolonged application of an organotin against Biomphalaria glabrata and schistosomiasis control. In Molluscides in schistosomiasis control. New York, USA: Academic Press Inc, 7788.Google Scholar
Romeis, B (1989) Mikroskopische Technik, färbemethoden mit Elsanlizarin- Kristallviolett, 17 Auflage, Urban & Schwarzenberg, München– Wien – Baltimore. pp. 235236.Google Scholar
Šamec, D, Loizzo, MR, Gortzi, O, Çankaya, İT, Tundis, R, Suntar, İ, Shirooie, S, Zengin, G, Devkota, HP, Reboredo‐Rodríguez, P, and Hassan, ST (2022) The potential of pumpkin seed oil as a functional food—a comprehensive review of chemical composition, health benefits, and safety. Comprehensive Reviews in Food Science and Food Safety 21(5), 44224446. doi: 10.1111/1541-4337.13013.CrossRefGoogle ScholarPubMed
Sarquis, O, Pieri, OS, and dos Santos, JAA (1997) Effects of Bayluscide WP 70® on the survival and water-leaving behaviour of Biomphalaria straminea, snail host of schistosomiasis in northeast Brazil. Memórias Inst. Oswaldo Cruz 92, 619623. doi: 10.1590/S0074-02761997000500011.CrossRefGoogle ScholarPubMed
Selvi, BC and Santhanam, A (2016) Evaluation of anthelmintic activity using solvent extract of Padina tetrastromatica in Indian earthworm (Pheretima posthuma). International Journal of Therapeutic Applications 32, 7780. doi: 10.20530/IJTA_32_77-80.CrossRefGoogle Scholar
Silva, HAMF, Siqueira, WN, , JLF, Silva, LRS, Martins, MCB, Aires, AL, Amâncio, FF, Pereira, EC, Albuquerque, MCPA, Melo, AMMA, and Silva, NH (2018) Laboratory assessment of divaricatic acid against Biomphalaria glabrata and Schistosoma mansoni cercariae. Acta Tropica 178, 97102. doi: 10.1016/j. actatropica.2017.09.019.CrossRefGoogle ScholarPubMed
Singh, NP, McCoy, MT, Tice, RR, and Schneider EL (1988) A simple technique for quantitation of low levels of DNA damage in individual cells. Experimental Cell Research 175(1), 184191. doi: 10.1016/0014-4827(88)90265-0.CrossRefGoogle ScholarPubMed
Soliman, MG, El Sayed, K, Abou Ouf, NA, El Fekky, FAEH, and Gad, RM (2017) Influence of immunostimulatory β-glucan on Biomphalaria alexandrina snails under laboratory and simulated field conditions. European Journal of Biomedical and Pharmaceutical Sciences 4, 4150.Google Scholar
Spiegel, D (1981) Vietnam grief work using hypnosis. American Journal of Clinical Hypnosis 24(1), 3340.CrossRefGoogle ScholarPubMed
Wang, X, Tang, Y, Li, Z, Wu, Q, Qiao, X, Wan, F, Qian, W, and Liu, C (2023) Investigation of immune responses in Giant African Snail, Achatina immaculata, against a two-round lipopolysaccharide challenge. International Journal of Molecular Sciences 24(15), 12191. doi: 10.3390/ijms241512191.CrossRefGoogle ScholarPubMed
Wang, XY, He, J, Juma, S, Kabole, F, Guo, JG, Dai, JR, Li, W, and Yang, K (2019) Efficacy of China-made praziquantel for treatment of schistosomiasis haematobium in Africa: a randomized controlled trial. PLoS Neglected Tropical Diseases 13(4), e0007238. doi: 10.1371/journal.pntd.0007238.CrossRefGoogle ScholarPubMed
World Health Organization (1965) Molluscicide screening and evaluation. Bulletin of the World Health Organization 33(6), 567581.Google Scholar
Zhang, L and Zou, Z (2020) Molluscicidal activity of fatty acids in the kernel of Chimonanthus praecox cv. Luteus against the golden apple snail Pomacea canaliculata. Pesticide Biochemistry and Physiology 167, 104620. doi: 10.1016/j.pestbp.2020.104620CrossRefGoogle ScholarPubMed
Zheng, L, Deng, L, Zhong, Y, Wang, Y, Guo, W, and Fan, X (2021) Molluscicides against the snail-intermediate host of Schistosoma: a review. Parasitology Research 120, 139. doi: 10.1007/s00436-021-07288-4.CrossRefGoogle Scholar