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In vitro and in vivo effects of hesperidin treatment on adult worms of Schistosoma mansoni

Published online by Cambridge University Press:  09 May 2013

G. Allam  and
A.S.A. Abuelsaad
G. Allam*
Affiliation:
Department of Microbiology, College of Medicine, Taif University, Taif, Saudi Arabia Department of Zoology, Faculty of Science, Beni-Suef University, Beni-Suef, Egypt
A.S.A. Abuelsaad
Affiliation:
Department of Microbiology, College of Medicine, Taif University, Taif, Saudi Arabia Department of Zoology, Faculty of Science, Beni-Suef University, Beni-Suef, Egypt
*
*Fax: +966 2 7250528; E-mail: [email protected]
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Abstract

Hesperidin has been reported to exert a wide range of pharmacological effects, including antifungal, antiviral, antioxidant, anti-inflammatory and anticarcinogenic activities. Herein, the schistosomicidal activity of this compound was evaluated in vitro and in vivo. Using an in vitro assay, a concentration of 200 μg/ml of hesperidin resulted in the mortality of 100% adult worms of Schistosoma (S.) mansoni within 72 h and a partial tegumental alteration in 10% of worms. However, after 144 h incubation, 50 and 100 μg/ml concentrations showed 0% and 10% mortality in adult worms, respectively, without any changes to the tegument. Sublethal doses did not influence egg output nor the development of eggs deposited by pairs of adult worms. In an in vivo study, mice infected with S. mansoni and treated with 600 mg hesperidin/kg body weight showed a respective reduction of 50, 45.2, 50 and 47.5% of males, females, worm pairs and total worm burden. In addition, a respective reduction, based on the number of eggs/g tissue, of 41.5, 63.7 and 58.6% was observed in the liver, intestine and liver/intestinal tissue combined. Furthermore, S. mansoni-specific IgG level significantly increased with hesperidin treatment, whereas IgA and IgE levels were not significantly changed. IgM levels decreased in response to cercarial antigen preparation but were not altered in response to soluble worm or soluble egg antigen. As in hesperidin-treated mice, praziquantel-treated mice showed a similar pattern of specific antibody response to S. mansoni antigens. The present study represents the first report on the effects of the schistosomicidal activity of hesperidin.

Type
Research Papers
Information
Journal of Helminthology , Volume 88 , Issue 3 , September 2014 , pp. 362 - 370
Copyright
Copyright © Cambridge University Press 2013 

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References

Allam, G. (2009) Immunomodulatory effects of curcumin treatment on murine schistosomiasis mansoni. Immunobiology 214, 712–727.CrossRefGoogle ScholarPubMed
Barthe, G.A., Jourdan, P.S., McIntosh, C.A. & Mansell, R.L. (1988) Radioimmunoassay for quantitative determination of hesperidin and analysis of its distribution in Citrus sinensis . Phytochemistry 27, 249–254.Google Scholar
Biała, G. & Langwiński, R. (1996) Rewarding properties of some drugs studied by place preference conditioning. Polish Journal of Pharmacology 48, 425–430.Google Scholar
Boisseau, M.R. (2002) Pharmacological targets of drugs employed in chronic venous and lymphatic insufficiency. International Angiology 21, 33–39.Google Scholar
Brindley, P.J. & Sher, A. (1987) The chemotherapeutic effect of praziquantel against Schistosoma mansoni is dependent on host antibody response. Journal of Immunology 139, 215–220.Google Scholar
Bruce, J.I. & Radke, M.G. (1971) Culturing Biomphalaria and Oncomelania (Gastropoda) for large-scale studies of schistosomiasis. I. Cultivation of Biomphalaria glabrata and maintenance of Schistosoma mansoni in the laboratory. Biomedical Report of the 406th Medical Laboratory 19, 1–84.Google Scholar
Cantilena, L.R. & Klaassen, C.D. (1982) The effect of chelating agents on the excretion of endogenous metals. Toxicology and Applied Pharmacology 63, 344–350.Google Scholar
Capron, M. & Capron, A. (1994) Immunoglobulin E and effector cells in schistosomiasis. Science 264, 1876–1877.CrossRefGoogle ScholarPubMed
Chatterjee, S., Mbaye, A., De Man, J.G. & Van Marck, E.A.E. (2002) Does the neuropeptide somatostatin have therapeutic potential against schistosomiasis? Trends in Parasitology 18, 295–298.Google Scholar
Cheever, A.W. (1968) Condition affecting the accuracy of potassium hydroxide digestion techniques for counting Schistosoma mansoni eggs in tissues. Bulletin of the World Health Organization 39, 328–331.Google ScholarPubMed
Chen, M., Gu, H., Ye, Y., Lin, B., Sun, L., Deng, W., Zhang, J. & Liu, J. (2010) Protective effects of hesperidin against oxidative stress of tert-butyl hydroperoxide in human hepatocytes. Food and Chemical Toxicology 48, 2980–2987.Google Scholar
Chitsulo, L., Engels, D., Montresor, A. & Savioli, L. (2000) The global status of schistosomiasis and its control. Acta Tropica 77, 41–51.Google Scholar
Cioli, D., Valle, C., Angelucci, F. & Miele, A.E. (2008) Will new antischistosomal drugs finally emerge? Trends in Parasitology 24, 379–382.Google Scholar
Dunne, D. & Mountford, A. (2001) Resistance to infection in humans and animal models. pp. 133–212 in Mahmoud, A.A.F. (Ed.) Schistosomiasis. London, UK, Imperial College Press.Google Scholar
Duvall, R.H. & DeWitt, W.B. (1967) An improved perfusion technique for recovering adult schistosomes from laboratory animals. American Journal of Tropical Medicine and Hygiene 16, 483–486.Google Scholar
El Ridi, R. (2002) Toward a complete immunity-inducing vaccine for schistosomiasis. Journal of Parasitology 88, 1049–1050.Google Scholar
El-Sayed, E.M., Abo-Salem, O.M., Abd-Ellah, M.F. & Abd-Alla, G.M. (2007) Hesperidin, and antioxidant flavonoid, prevent acrylonitrile-induced oxidative stress in rat brain. Journal of Egyptian Society of Toxicology 37, 87–93.Google Scholar
Engels, D., Chitsulo, L., Montresor, A. & Savioli, L. (2002) The global epidemiological situation of schistosomiasis and new approaches to control and research. Acta Tropica 82, 139–146.Google Scholar
Finkelstein, J.L., Schleinitz, M.D., Carabin, H. & McGarvey, S.T. (2008) Decision-model estimation of the age-specific disability weight for schistosomiasis japonica: a systematic review of the literature. PLoS Neglected Tropical Disease 2, e158.Google Scholar
Flisser, A. & McLaren, D.J. (1989) Effect of praziquantel treatment on lung stage larvae of Schistosoma mansoni in vivo . Parasitology 98, 203–211.Google Scholar
Hamed, M.A. & Hetta, M.H. (2005) Efficacy of Citrus reticulata and Mirazid in treatment of Schistosoma mansoni . Memórias do Instituto Oswaldo Cruz Rio de Janeiro 100, 771–778.CrossRefGoogle ScholarPubMed
Hoffmann, K.F., James, S.L., Cheever, A.W. & Wynn, T.A. (1999) Studies with double cytokines-deficient mice reveal that highly polarized Th1 and Th2 type cytokine and antibody responses contribute equally to vaccine-induced immunity to Schistosoma mansoni . Journal of Immunology 163, 927–938.Google Scholar
Hosseinimehr, S.J. & Nemati, A. (2006) Radioprotective effects of hesperidin against gamma irradiation in mouse bone marrow cells. British Journal of Radiology 79, 415–418.Google Scholar
Huang, H.-Q., Li, S.-C., Qin, Z.-H., Cao, S.-L., Yao, Y., Liu, Y.-S., Li, H.-Y., Cai, M.-S., Li, Z.-J. & Shi, Y.-E. (2005) Synthesis and bioactivities of two multiple antigen peptides as potential vaccine against Schistosoma . Bioorganic Medicinal Chemistry Letters 15, 2415–2419.Google Scholar
Ismail, M., Botros, S., Metwally, A., William, S., Farghally, A., Tao, L.F., Day, T.A. & Bennett, J.L. (1999) Resistance to praziquantel: direct evidence from Schistosoma mansoni isolated from Egyptian villagers. American Journal of Tropical Medicine and Hygiene 6, 932–935.Google Scholar
Jankovic, D., Wynn, T.A., Kullberg, M.C., Hieny, S., Caspar, P., James, S., Cheever, A.W. & Sher, A. (1999) Optimal vaccination against Schistosoma mansoni requires the induction of both B cells and IFN-gamma-dependent effector mechanisms. Journal of Immunology 162, 345–351.Google Scholar
Jovanovic, S.V., Steenken, S., Tosic, M., Marjonovic, B. & Simic, M.G. (1994) Flavonoids as antioxidants. Journal of the American Chemical Society 116, 4846–4851.Google Scholar
Kabatereine, N.B., Kemijumbi, J., Ouma, J.H., Sturrock, R.F., Butterworth, A.E., Madsen, H., Ornbierg, N., Dunne, D.W. & Vennervald, B.J. (2003) Efficacy and side effects of praziquantel treatment in a highly endemic Schistosoma mansoni focus at lake Albert, Uganda. Transactions of the Royal Society of Tropical Medicine and Hygiene 97, 599–603.CrossRefGoogle Scholar
Kamaraj, S., Anandakumar, P., Jagan, S., Ramakrishnan, G. & Devaki, T. (2010) Modulatory effect of hesperidin on benzo(a)pyrene induced experimental lung carcinogenesis with reference to COX-2, MMP-2 and MMP-9. European Journal of Pharmacology 15, 320–327.Google Scholar
Kawaguchi, K., Mizuno, T., Aida, K. & Uchino, K. (1997) Hesperidin as an inhibitor of lipases from porcine pancreas and Pseudomonas . Bioscience, Biotechnology and Biochemistry 61, 102–104.Google Scholar
Kayser, O., Kiderlen, A.F. & Croft, S.L. (2003) Natural products as antiparasitic drugs. Parasitology Research 90, S55–S62.Google Scholar
Krolicki, Z. & Lamer-Zarawaska, E. (1984) Investigation of antifungal effect of flavonoids. Part 1. Herba Polonica 30, 53–57.Google Scholar
Lahlou, M. (2004) Study of the molluscicidal activity of some phenolic compounds: structure-activity relationship. Pharmaceutical Biology 42, 258–261.Google Scholar
Lammie, P.J., Fenwick, A. & Utzinger, J. (2006) A blueprint for success, integration of neglected tropical disease control programmes. Trends in Parasitology 22, 313–321.Google Scholar
Lowry, O.H., Rosenbrough, N.J., Farr, A.L. & Randall, R.J. (1951) Protein measurement with Folin-Phenol reagent. Journal of Biological Chemistry 193, 265–275.Google Scholar
Magalhães, L.G., Machado, C.B., Morais, E.R., Moreira, E.B., Soares, C.S., da Silva, S.H., Da Silva Filho, A.A. & Rodrigues, V. (2009) In vitro schistosomicidal activity of curcumin against Schistosoma mansoni adult worms. Parasitology Research 104, 1197–1201.Google Scholar
Magalhães, L.G., Kapadia, G.J., da Silva Tonuci, L.R., Caixeta, S.C., Parreira, N.A., Rodrigues, V. & Da Silva Filho, A.A. (2010) In vitro schistosomicidal effects of some phloroglucinol derivatives from Dryopteris species against Schistosoma mansoni adult worms. Parasitology Research 106, 395–401.Google Scholar
Mangold, B.L. & Dean, D.A. (1986) Passive transfer with serum and IgG antibodies with irradiated cercariae-induced resistance against Schistosomiasis mansoni in mice. Journal of Immunology 136, 2644–2647.Google Scholar
Mølgaard, P., Nielsen, S.B., Rasmussen, D.E., Drummond, R.B., Makaza, N. & Andreassen, J. (2001) Anthelmintic screening of Zimbabwean plants traditionally used against schistosomiasis. Journal of Ethnopharmacology 74, 257–264.Google Scholar
Montanari, A., Chen, J. & Widmer, W. (1998) Citrus flavonoids: a review of past biological activity against disease. Discovery of new flavonoids from Dancy tangerine cold pressed peel oil solids and leaves. Advances in Experimental Medicine and Biology 439, 103–116.Google Scholar
Olszanecki, R., Gebska, A., Kozlovski, V.I. & Gryglewski, R.J. (2002) Flavonoids and nitric oxide synthase. Journal of Physiology and Pharmacology 53, 571–584.Google Scholar
Parreira, N.A., Magalhães, L.G., Morais, D.R., Caixeta, S.C., de Sousa, J.P., Bastos, J.K., Cunha, W.R., Silva, M.L., Nanayakkara, N.P., Rodrigues, V. & da Silva Filho, A.A. (2010) Antiprotozoal, schistosomicidal, and antimicrobial activities of the essential oil from the leaves of Baccharis dracunculifolia . Chemistry and Biodiversity 7, 993–1001.Google Scholar
Pica-Mattoccia, L. & Cioli, D. (2004) Sex- and stage-related sensitivity of Schistosoma mansoni to in vivo and in vitro praziquantel treatment. International Journal of Parasitology 34, 527–533.Google Scholar
Pires Das Neves, R.N., Carvalho, F., Carvalho, M., Fernandes, E., Soares, E., Bastos, M.D. & Pereira, M.D. (2004) Protective activity of hesperidin and lipoic acid against sodium arsenite acute toxicity in mice. Toxicologic Pathology 32, 527–535.Google Scholar
Sanderson, L., Bartlett, A. & Whitfield, P.J. (2002) In vitro and in vivo studies on the bioactivity of a ginger (Zingiber officinale) extract towards adult schistosomes and their egg production. Journal of Helminthology 76, 241–247.Google Scholar
Schubert, M. (1948) Conditions for drug testing in experimental Schistosomiasis mansoni in mice. American Journal of Tropical Medicine and Hygiene 28, 121–136.Google Scholar
Silva, L.M., Menezes, R.M., De Oliveira, S.A. & Andrade, Z.A. (2003) Chemotherapeutic effects on larval stages of Schistosoma mansoni during infection and reinfection of mice. Revista da Sociedade Brasileira de Medicina Tropical 36, 335–341.CrossRefGoogle ScholarPubMed
Standen, O.D. (1949) Experimental schistosomiasis II: maintenance of Schistosoma mansoni in the laboratory, with some notes on experimental infection with S. haematobium . Annals of Tropical Medicine and Parasitology 43, 268–283.Google Scholar
Steinmann, P., Keiser, J., Bos, R., Tanner, M. & Utzinger, J. (2006) Schistosomiasis and water resources development, systematic review, meta-analysis, and estimates of people at risk. Lancet Infectious Diseases 6, 411–425.Google Scholar
Tian, Q., Miller, E.G., Ahmad, H., Tang, L. & Patil, B.S. (2001) Differential inhibition of human cancer cell proliferation by citrus limonoids. Nutrition and Cancer 40, 180–184.Google Scholar
Winawer, S., Fletcher, R., Rex, D., Bond, J., Burt, R., Ferrucci, J., Ganiats, T., Levin, T., Woolf, S., Johnson, D., Kirk, L., Litin, S. & Simmang, C. (2003) Colorectal cancer screening and surveillance: clinical guidelines and rationale - update based on new evidence. Gastroenterology 124, 544–560.Google Scholar
World Health Organization (1993) The control of schistosomiasis. WHO Technical Report Series No. 830 . pp. 1–86. Geneva, Switzerland, World Health Organization.Google Scholar
Xiao, S.H., Keiser, J., Chollet, J., Utzinger, J., Dong, Y., Endriss, Y., Vennerstrom, J.L. & Tanner, M. (2007) In vitro and in vivo activities of synthetic trioxolanes against major human schistosome species. Antimicrobial Agents and Chemotherapy 51, 1440–1445.Google Scholar
Ying, L., ZhiSheng, W. & AnGuo, Z. (2009) Effects of hesperidin and chlorogenic acid on performance, antioxidance and immunity of weaned piglets. Chinese Journal of Veterinary Science 29, 1233–1236.Google Scholar
Zhang, C., Lu, Y., Tao, L., Tao, X., Su, X. & Wei, D. (2007) Tyrosinase inhibitory effects and inhibition mechanisms of nobiletin and hesperidin from citrus peel crude extracts. Journal of Enzyme Inhibition and Medicinal Chemistry 22, 91–98.Google Scholar