Hostname: page-component-848d4c4894-ttngx Total loading time: 0 Render date: 2024-05-12T20:01:37.129Z Has data issue: false hasContentIssue false
  • English
  • Français

Schistosomicidal, antifibrotic and antioxidant effects of Cucurbita pepo L. seed oil and praziquantel combined treatment for Schistosoma mansoni infection in a mouse model

Published online by Cambridge University Press:  15 April 2018

E.V.N. Beshay ,
A.A. Rady ,
A.F. Afifi  and
A.H. Mohamed
E.V.N. Beshay*
Affiliation:
Parasitology Department, Faculty of Medicine, Menoufia University. Menoufia, Egypt
A.A. Rady
Affiliation:
Parasitology Department, Faculty of Medicine, Menoufia University. Menoufia, Egypt
A.F. Afifi
Affiliation:
Parasitology Department, Faculty of Medicine, Menoufia University. Menoufia, Egypt
A.H. Mohamed
Affiliation:
Zoology Department, Faculty of Science, Menoufia University. Menoufia, Egypt
*
Author for correspondence: E.V.N Beshay, E-mail: engyvictor@med.menofia.edu.eg
Get access Rights & Permissions [Opens in a new window]

Abstract

Despite the seriousness of schistosomiasis, its treatment depends only on praziquantel (PZQ), which has begun to lose its efficacy against the emergent Schistosoma mansoni-resistant strains. Therefore, the discovery of a novel schistosomicidal drug is an urgent priority. This study was designed to evaluate treatment with Cucurbita pepo L. (pumpkin) seed oil (PSO) alone and combined with PZQ against S. mansoni in experimentally infected mice. The study involved five groups: GI was the normal control; GII was the infected control; GIII was treated with an oral dose of PZQ of 500 mg/kg/day for two successive days, starting in the sixth week post infection; GIV was treated with an oral dose of PSO of 50 mg/kg/day for four weeks, starting in the fourth week post infection; and GV was treated with combined PSO–PZQ. Worm burden, tissue egg load and oogram pattern were estimated, and the ultrastructure alterations were examined. Histopathological examination of granuloma diameters, collagen deposition (Picro Sirius red stain), and angiogenesis (immunohistochemical expression of CD34+) was conducted and serum liver enzymes were measured to assess the liver condition. Moreover, the oxidative stress was evaluated by determining the amounts of malondialdehyde and superoxide dismutase in liver homogenates. The results revealed significant changes in all the assessed parameters with PSO administration. However, PZQ was significantly more effective as an antiparasitic agent, whereas PSO was better in terms of fibrosis and oxidative stress. The most significant results were obtained in group V, which may be attributed to a synergy between PZQ and PSO, with antiparasitic, antioxidant and antifibrotic properties.

Type
Research Paper
Information
Journal of Helminthology , Volume 93 , Issue 3 , May 2019 , pp. 286 - 294
Copyright
Copyright © Cambridge University Press 2018 

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

Abdel Fattah, NS and Ahmed, NS (2012) Evidence of intra-hepatic vascular proliferation remodeling early after cure in experimental schistosomiasis mansoni: an immunohistochemical descriptive study. Experimental Parasitology 130, 58–62.Google Scholar
Al-Olayan, EM, El-Khadragy, MF, Alajmi, RA, Othman, MS, Bauomy, AA, Ibrahim, SR and Moneim, AEA (2016) Ceratonia siliqua pod extract ameliorates Schistosoma mansoni-induced liver fibrosis and oxidative stress. BMC Complementary and Alternative Medicine 16, 434.Google Scholar
Andjelkovic, M, Van Camp, J, Trawka, A and Verhé, R (2010) Phenolic compounds and some quality parameters of pumpkin seed oil. European Journal of Lipid Science and Technology 112, 208–217.Google Scholar
Andrade, ZA (2004) Schistosomal hepatopathy. Memórias do Instituto Oswaldo Cruz 99, 51–57.Google Scholar
Bardaa, S, Halima, NB, Aloui, F, Mansour, RB, Jabeur, H, Bouaziz, M and Sahnoun, Z (2016) Oil from pumpkin (Cucurbita pepo L.) seeds: evaluation of its functional properties on wound healing in rats. Lipids in Health and Disease 15, 73.Google Scholar
Bergquist, R, Utzinger, J and Keiser, J (2017) Controlling schistosomiasis with praziquantel: how much longer without a viable alternative? Infectious Diseases of Poverty 6, 74.Google Scholar
Caili, F, Huan, S and Quanhong, L (2006) A review on pharmacological activities and utilization technologies of pumpkin. Plant Foods for Human Nutrition 61, 70–77.Google Scholar
Carleton, HM, Drury, RAB and Wallington, EA (1980) Carleton's histological technique. Oxford, Oxford University Press.Google Scholar
Chai, JY (2013) Praziquantel treatment in trematode and cestode infections: an update. Infection & Chemotherapy 45, 32–43.Google Scholar
Cheever, AW, Macedonia, JG, Deb, S, Cheever, EA and Mosimann, JE (1992) Persistence of eggs and hepatic fibrosis after treatment of Schistosoma mansoni-infected mice. The American Journal of Tropical Medicine and Hygiene 46, 752–758.Google Scholar
Colley, DG and Secor, WE (2014) Immunology of human schistosomiasis. Parasite Immunology 36, 347–357.Google Scholar
Coulon, S, Heindryckx, F, Geerts, A, Van Steenkiste, C, Colle, I and Van Vlierberghe, H (2011) Angiogenesis in chronic liver disease and its complications. Liver International 31, 146–162.Google Scholar
De Maria, N, Colantonl, A, Fagiuoli, S, Liu, GJ, Rogers, BK, Farinati, F, Van Thiel, DH and Floyd, RA (1996) Association between reactive oxygen species and disease activity in chronic hepatitis C. Free Radical Biology and Medicine 21, 291–295.Google Scholar
Dhawan, V, Handu, SS, Nain, CK and Ganguly, NK (2005) Chronic L-arginine supplementation improves endothelial cell vasoactive functions in hypercholesterolemic and atherosclerotic monkeys. Molecular and Cellular Biochemistry 269, 1–11.Google Scholar
Dkhil, MA, Abdel Moneim, AE and Al-Quraishy, S (2014) Berberine protects against Schistosoma mansoni-induced oxidative damage in renal and testicular tissues of mice. Pakistan Journal of Zoology 46, 763–771.Google Scholar
Drifka, CR, Loeffler, AG, Mathewson, K et al. (2016) Comparison of picrosirius red staining with second harmonic generation imaging for the quantification of clinically relevant collagen fiber features in histopathology samples. Journal of Histochemistry and Cytochemistry 64, 519–529.Google Scholar
Elpek, GÖ (2015) Angiogenesis and liver fibrosis. World Journal of Hepatology 7, 377–391.Google Scholar
El-Sayad, M, Abu Helw, S, El-Taweel, H and Aziz, M (2017) Antiparasitic activity of Mirazid, myrrh total oil and nitazoxanide compared to praziquantel on Schistosoma mansoni: scanning electron microscopic study. Iranian Journal of Parasitology 12, 446–452.Google Scholar
Faghiri, Z and Skelly, PJ (2009) The role of tegumental aquaporin from the human parasitic worm, Schistosoma mansoni, in osmoregulation and drug uptake. The Journal of the Federation of American Societies for Experimental Biology 23, 2780–2789.Google Scholar
Glew, RH, Glew, RS, Chuang, LT, Huang, YS, Millson, M, Constans, D and Vanderjagt, DJ (2006) Amino acid, mineral and fatty acid content of pumpkin seeds (Cucurbita spp.) and Cyperus esculentus nuts in the Republic of Niger. Plant Foods for Human Nutrition 61, 49–54.Google Scholar
Gönnert, R and Andrews, P (1977) Praziquantel, a new broad-spectrum antischistosomal agent. Parasitology Research 52, 129–150.Google 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, 1456.Google Scholar
Halliwell, B and Gutteridge, JMC (2015) Free radicals in biology and medicine. 5th edn. Oxford, Oxford University Press.Google Scholar
Harnett, W and Kusel, JR (1986) Increased exposure of parasite antigens at the surface of adult male Schistosoma mansoni exposed to praziquantel in vitro. Parasitology 93, 401–405.Google Scholar
Herbert, DR, Orekov, T, Roloson, A et al. (2010) Arginase I suppresses IL-12/IL-23p40-driven intestinal inflammation during acute schistosomiasis. The Journal of Immunology 184, 6438–6446.Google Scholar
Iqbal, Z, Nadeem, QK, Khan, MN, Akhtar, MS and Waraich, FN (2001) In vitro anthelmintic activity of Allium sativum, Zingiber officinale, Curcurbita mexicana and Ficus religiosa. International Journal of Agriculture & Biology 3, 454–457.Google Scholar
Kanse, SM, Liang, O, Schubert, U, Haas, H, Preissner, KT, Doenhoff, MJ and Dennis, RD (2005) Characterisation and partial purification of Schistosoma mansoni egg-derived pro-angiogenic factor. Molecular and Biochemical Parasitology 144, 76–85.Google Scholar
Liang, YS, Bruce, JI and Boyd, DA (1987) Laboratory cultivation of schistosome vector snails and maintenance of schistosome life cycles. Proceedings of the First Sino–American Symposium 1, 34–48.Google Scholar
Liang, YJ, Luo, J, Yuan, Q et al. (2011) New insight into the antifibrotic effects of praziquantel on mice in infection with Schistosoma japonicum. PLoS ONE 6, e20247. doi: 10.1371/journal.pone.0020247.Google Scholar
Mahmoud, LH, Basiouny, SO and Dawoud, HA (2002) Treatment of experimental heterophyiasis with two plant extracts, areca nut and pumpkin seed. Journal of the Egyptian Society of Parasitology 32, 501–506.Google Scholar
Mati, VL and Melo, AL (2013) Current applications of oogram methodology in experimental schistosomiasis; fecundity of female Schistosoma mansoni and egg release in the intestine of AKR/J mice following immunomodulatory treatment with pentoxifylline. Journal of Helminthology 87, 115–124.Google Scholar
Matos-Rocha, TJ, Cavalcanti, MG, Veras, DL et al. (2016) Ultrastructural changes in Schistosoma mansoni male worms after in vitro incubation with the essential oil of Mentha x villosa huds. Revista do Instituto de Medicina Tropical de São Paulo 58, 7.Google Scholar
Melman, SD, Steinauer, ML, Cunningham, C et al. (2009) Reduced susceptibility to praziquantel among naturally occurring Kenyan isolates of Schistosoma mansoni. PLoS Neglected Tropical Diseases 3, e504. doi: 10.1371/journal.pntd.0000504.Google Scholar
Nishikimi, M, Rao, NA and Yagi, K (1972) The occurrence of superoxide anion in the action of reduced phenazine methosulphate and molecular oxygen. Biochemical and Biophysical Research Communications 46, 849–854.Google Scholar
Ohkawa, H, Ohishi, N and Yagi, K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Analytical Biochemistry 95, 351–358.Google Scholar
Othman, AA, Shoheib, ZS, Abdel-Aleem, GA and Shareef, MM (2008) Experimental schistosomal hepatitis: protective effect of coenzyme Q10 against the state of oxidative stress. Experimental Parasitology 120, 147–155.Google Scholar
Pereira, AS, Padilha, RJ, Lima-Filho, JL and Chaves, ME (2011) Scanning electron microscopy of the human low-density lipoprotein interaction with the tegument of Schistosoma mansoni. Parasitology Research 109, 1395–1402.Google Scholar
Pinlaor, S, Hiraku, Y, Yongvanit, P et al. (2006) iNOS-dependent DNA damage via NF kappa β expression in hamsters infected with Opisthorchis viverrini and its suppression by the antihelminthic drug praziquantel. International Journal of Cancer 119, 1067–1072.Google Scholar
Rezig, L, Chouaibi, M, Msaada, K and Hamdi, S (2012) Chemical composition and profile characterisation of pumpkin (Cucurbita maxima) seed oil. Industrial Crops and Products 37, 82–87.Google Scholar
Semenza, GL (2012) Hypoxia-inducible factors in physiology and medicine. Cell 148, 399–408.Google Scholar
Shaw, MK and Erasmus, DA (1987) Schistosoma mansoni: structural damage and tegumental repair after in vivo treatment with praziquantel. Parasitology 94, 243–254.Google Scholar
Smithers, SR and Terry, RJ (1965) The infection of laboratory hosts with cercariae of Schistosoma mansoni and the recovery of the adult worms. Parasitology 55, 695–700.Google Scholar
Steinmann, P, Keiser, J, Bos, R, Tanner, M and Utzinger, J (2006) Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. The Lancet Infectious Diseases 6, 411–425.Google Scholar
Tekwu, EM, Bosompem, KM, Anyan, WK et al. (2017) In vitro assessment of anthelmintic activities of Rauwolfia vomitoria (Apocynaceae) stem bark and roots against parasitic stages of Schistosoma mansoni and cytotoxic study. Journal of Parasitology Research 2017, 2583969.Google Scholar
Von Lichtenberg, FC (1962) Host response to eggs of S. mansoni. I. Granuloma formation in the unsensitized laboratory mouse. The American Journal of Pathology 41, 711–731.Google Scholar
World Health Organization (WHO) Expert Committee (2002) Prevention and control of schistosomiasis and soil-transmitted helminthiasis. World Health Organization Technical Report Series 912, 1–57.Google Scholar
Supplementary material: File

Beshay et al. supplementary material

Tables S1-S2 and Figures S1-S2

Download Beshay et al. supplementary material(File)
File 7.2 MB