Current Issue
Forthcoming Papers
Archive
About the Journal
Publishers
Aims & Scope
Publication Ethics
Contact
Editorial Board
Advisory Board
Author Guidelines
Preparation of Manuscripts
Additional Information for Authors
Manuscript Submission Process Short Scheme
Review Process
Review Process
Referees 2024
Referees 2023
Referees 2022
Referees 2021
Referees 2020
Referees 2019
Referees 2018
Referees 2017
Referees 2016
Funding
RESEARCH PAPER
Control of infection of Biomphalaria alexandrina (Ehrenberg, 1831) with Schistosoma mansoni Sambon, 1907 using Eucalyptus camaldulensis
1
Medical Malacology Laboratory, Theodor Bilharz Research Institute, Giza, Egypt
2
Department of Medicinal Chemistry, Theodor Bilharz Research Institute, Giza, Egypt
Submission date: 2018-04-04
Final revision date: 2018-05-30
Acceptance date: 2018-06-06
Publication date: 2018-07-25
Corresponding author
Mohamed R. Habib
Medical Malacology Laboratory, Theodor Bilharz Research Institute, 12411 Giza, Egypt
Medical Malacology Laboratory, Theodor Bilharz Research Institute, 12411 Giza, Egypt
Folia Malacol. 2018;26(3):155-165
KEYWORDS
ethyl acetate extractEucalyptus camaldulensisBiomphalaria alexandrinaSchistosoma mansoniOxidative stressantioxidant activity
ABSTRACT
Schistosomiasis infection can be interrupted if the development of miracidia to cercariae in Biomphalaria alexandrina (Ehrenberg) is blocked. This requires an efficient snail’s antioxidant system which can be complemented with an exogenous antioxidant source to alleviate the oxidative stress of infection. For this purpose, leaves of Eucalyptus camaldulensis were air-dried, extracted with aqueous methanol (85%) and defatted with petroleum ether. The obtained defatted extract was used to prepare extracts with different solvents. Among these, ethyl acetate showed the highest antioxidant activity and was chosen for the experiments. The effect of ethyl acetate extract on the infection, survivorship, as well as levels of malondialdehyde (MDA), catalase (CAT) and reduced glutathione (GSH) in B. alexandrina were measured in control, untreated infected and treated infected snails on 1, 10, and 30 days post infection (dpi). The snails exposed to ethyl acetate extract showed a significant reduction in the infection rate compared to those infected and untreated. Moreover, the extract decreased the level of MDA and increased CAT and GSH activities in the haemolymph and tissues of the treated snails. The results suggest that ethyl acetate extract from leaves of E. camaldulensis can be used as an antiparasitic compound against the intramolluscan phase of S. mansoni Sambon, 1907.
REFERENCES (60)
1.
Abou-El-Naga I. F. 2013. Biomphalaria alexandrina in Egypt: Past, present and future. J. Biosci. 38: 665–672. https://doi.org/10.1007/s12038....
2.
Aebi H. 1984. Catalase in vitro. Methods Enzymol. 105: 121–126. https://doi.org/10.1016/S0076-....
3.
Al-Saimary I. E., Zeki A. 1999. In vitro chemotherapeutic effects of antibiotics and plant extract on protoscoleces viability of human hydatid cysts. J. Basrah Res. 20: 79–98.
4.
Amakura Y., Umino Y., Tsuji S., Ito H., Hatano T., Yoshida T., Tonogai Y. 2002. Constituents and their antioxidative effects in Eucalyptus leaf extract used as a natural food additive. Food Chem. 77: 47–56. https://doi.org/10.1016/S0308-....
5.
Batish D. R., Singh H. P., Kohli R. K., Kaur S. 2008. Eucalyptus essential oil as a natural pesticide. Forest Ecol. Manag. 256: 2166–2174. https://doi.org/10.1016/j.fore....
6.
Bayne C. J. 2009. Successful parasitism of vector snail Biomphalaria glabrata by the human blood fluke (trematode) Schistosoma mansoni: a 2009 assessment. Mol. Biochem. Parasitol. 165: 8–18. https://doi.org/10.1016/j.molb....
7.
Bayne C. J., Buckley P. M., DeWan P. C. 1980. Macrophagelike hemocytes of resistant Biomphalaria glabrata are cytotoxic for sporocysts of Schistosoma mansoni in vitro. J. Parasitol. 66: 413–419. https://doi.org/10.2307/328074....
8.
Bender R. C., Broderick E. J., Goodall C. P., Bayne C. J. 2005. Respiratory burst of Biomphalaria glabrata hemocytes: Schistosoma mansoni–resistant snails produce more extracellular H2O2 than susceptible snails. J. Parasitol. 91: 275–279. https://doi.org/10.1645/GE-415....
9.
Bender R. C., Goodall C. P., Blouin M. S., Bayne C. J. 2007. Variation in expression of Biomphalaria glabrata SOD1: a potential controlling factor in susceptibility/resistance to Schistosoma mansoni. Develop. Comp. Immunol. 31: 874–878. https://doi.org/10.1016/j.dci.....
10.
Beutler E., Duron O., Kellin B. M. 1963. Improved method for the determination of blood glutathione. J. Lab. Clin. Med. 61: 882–888.
11.
Brum Vieira P. de, Giordani R. B., Macedo A. J., Tasca T. 2015. Natural and synthetic compound anti-Trichomonas vaginalis: an update review. Parasitol. Res. 114: 1249–1261. https://doi.org/10.1007/s00436....
12.
Carvalho I. T., Estevinho B. N., Santos L. 2016. Application of microencapsulated essential oils in cosmetic and personal healthcare products – a review. Int. J. Cosm. Sci. 38: 109–119. https://doi.org/10.1111/ics.12....
13.
Cheng S. S., Huang C. G., Chen Y. J., Yu J. J., Chen W. J., Chang S. T. 2009. Chemical compositions and larvicidal activities of leaf essential oils from two eucalyptus species. Biores. Technol. 100: 452–456. https://doi.org/10.1016/j.bior....
14.
Chernin E., Dunavan C. A. 1962. The influence of host–parasite dispersion upon the capacity of Schistosoma mansoni miracidia to infection Australorbis glabratus. Amer. J. Trop. Med. Hyg. 11: 455–471. https://doi.org/10.4269/ajtmh.....
15.
Connors V. A., Lodes M. J., Yoshino T. P. 1991. Identification of a Schistosoma mansoni sporocyst excretory-secretory antioxidant molecule and its effect on superoxide production by Biomphalaria glabrata hemocytes. J. Invert. Pathol. 58: 387–395. https://doi.org/10.1016/0022-2....
16.
Cowan M. M. 1999. Plant products as antimicrobial agents. Clin. Microbiol. Rev. 12: 564–582.
17.
Dey B., Mitra A. 2013. Chemo-profiling of eucalyptus and study of its hypoglycemic potential. World J. Diabetes 4: 170. https://doi.org/10.4239/wjd.v4....
18.
Doenhoff M. J., Hagan P., Cioli D., Southgate V., Pica-Mattoccia L., Botros S., Coles G., Tchuem Tchuenté L. A., Mbaye A., Engels D. 2009. Praziquantel: its use in control of schistosomiasis in sub-Saharan Africa and current research needs. Parasitology 136: 1825–1835. https://doi.org/10.1017/S00311....
19.
El-Baz F. K., Mahmoud K., El-Senousy W. M., Darwesh O. M., ElGohary A. E. 2015: Antiviral–antimicrobial and schistosomicidal activities of Eucalyptus camaldulensis essential oils. Int. J. Pharm. Sci. Rev. Res. 31: 262–268.
20.
Fallon P. G., Doenhoff M. J. 1994. Drug-resistant schistosomiasis: resistance to praziquantel and oxamniquine induced in Schistosoma mansoni in mice is drug specific. Am. J. Trop. Med. Hyg. 51: 83–88. https://doi.org/10.4269/ajtmh.....
21.
Ghareeb M. A., Shoeb H. A., Madkour H. M., Refaey L. A., Mohamed M. A., Saad A. M. 2014. Antioxidant and cytotoxic activities of Tectona grandis Linn leaves. Int. J. Phytopharmacol. 5: 143–157.
22.
Ghisalberti E. L. 1996. Bioactive acylphloroglucinol derivatives from Eucalyptus species. Phytochemistry 41: 7–22. https://doi.org/10.1016/0031-9....
23.
Gilles M., Zhao J., An M., Agboola S. 2010. Chemical composition and antimicrobial properties of essential oils of three Australian Eucalyptus species. Food Chem. 119: 731–737. https://doi.org/10.1016/j.food....
24.
Haggag A. A., Rabiee A., Elaziz K. M. A., Gabrielli A. F., Hay R. A., Ramzy R. M. 2017. Mapping of Schistosoma mansoni in the Nile Delta, Egypt: Assessment of the prevalence by the circulating cathodic antigen urine assay. Acta Trop. 167: 9–17. https://doi.org/10.1016/j.acta....
25.
Hahn U. K., Bender R. C., Bayne C. J. 2001. Killing of Schistosoma mansoni sporocysts by hemocytes from resistant Biomphalaria glabrata: role of reactive oxygen species. J. Parasitol. 87: 292–299. https://doi.org/10.1645/0022-3....
26.
Harikrishnan R., Balasundaram C., Heo M. S. 2011. Impact of plant products on innate and adaptive immune system of cultured finfish and shellfish. Aquaculture 317: 1–15. https://doi.org/10.1016/j.aqua....
27.
Hassani S., Asghari G., Yousefi H., Kazemian A., Rafieiean M., Darani H. Y. 2013. Effects of different extracts of Eucalyptus camaldulensis on Trichomonas vaginalis parasite in culture medium. Adv. Biomed. Res. 2: 47. https://doi.org/10.4103/2277-9....
28.
Huang W. Y., Cai Y.Z., Zhang Y. 2009. Natural phenolic compounds from medicinal herbs and dietary plants: potential use for cancer prevention. Nutr. Cancer 62: 1–20. https://doi.org/10.1080/016355....
29.
Ittiprasert W., Miller A., Myers J., Nene V., El-Sayed N. M., Knight M. 2010. Identification of immediate response genes dominantly expressed in juvenile resistant and susceptible Biomphalaria glabrata snails upon exposure to Schistosoma mansoni. Mol. Biochem. Parasitol. 169: 27–39. https://doi.org/10.1016/j.molb....
30.
King C. H., Bertsch D. 2015. Historical perspective: snail control to prevent schistosomiasis. PLoS Negl. Trop. Dis. 9(4): e0003657. https://doi.org/10.1371/journa....
31.
Lambert R. J., Skandamis P. N., Coote P. J., Nychas G. J. 2001. A study of the minimum inhibitory concentration and mode of action of oregano essential oil, thymol and carvacrol. J. Appl. Microbiol. 91: 453–462. https://doi.org/10.1046/j.1365....
32.
Lotfy W. M., DeJong R. J., Abdel Kader A. A., Loker E. S. 2005. A molecular survey of Biomphalaria in Egypt: Is B. glabrata present? Amer. J. Trop. Med. Hyg. 73: 131–139.
33.
Meuleman E. A. 1971. Host-parasite interrelationships between the freshwater pulmonate Biomphalaria pfeifferi and the trematode Schistosoma mansoni. Neth. J. Zool. 22: 355–427. https://doi.org/10.1163/002829....
34.
Mitta G., Gourbal B., Grunau C., Knight M., Bridger J. M., Théron A. 2017. Chapter Three. The compatibility between Biomphalaria glabrata snails and Schistosoma mansoni: an increasingly complex puzzle. Adv. Parasitol. 97: 111–145. https://doi.org/10.1016/bs.apa....
35.
Mohamed A. H., Sharaf El-Din A. T., Mohamed A. M., Habib M. R. 2012. The relationship between genetic variability and the susceptibility of Biomphalaria alexandrina snails to Schistosoma mansoni infection. Mem. Inst. Oswaldo Cruz 107: 326–337. https://doi.org/10.1590/S0074-....
36.
Moné Y., Ribou A. C., Cosseau C., Duval D., Théron A., Mitta G., Gourbal B. 2011. An example of molecular co-evolution: reactive oxygen species (ROS) and ROS scavenger levels in Schistosoma mansoni/Biomphalaria glabrata interactions. Int. J. Parasitol. 41: 721–730. https://doi.org/10.1016/j.ijpa....
37.
Morgan J. A. T., Dejong R. J., Snyder S. D., Mkoji G. M., Loker E. S. 2001. Schistosoma mansoni and Biomphalaria: past history and future trends. Parasitology 123: 211–228. https://doi.org/10.1017/S00311....
38.
Mossalem H. S., Ghareeb M. A., Reffahy L. A., Mohamed A. S., Habib M. R. 2017. GAS Chromatography-Mass spectrometry analysis and antioxidant activity of Punica geranium L. Peels and its role as immunostimulant against Schistosoma mansoni infection in Biomphalaria alexandrina. Asian J. Pharm. Clin. Res. 10: 1–7.
39.
Mourão M. M., Dinguirard N., Franco G. R., Yoshino T. P. 2009. Role of the endogenous antioxidant system in the protection of Schistosoma mansoni primary sporocysts against exogenous oxidative stress. PLoS Negl. Trop. Dis. 3: e550. https://doi.org/10.1371/journa....
40.
Neelam A., Hany O., Sherwani S. K., Jabeen S., Nangyal H. 2014. Phytochemical and bioactivity of commercially available Eucalyptus oil against human pathogens. South Asian J. Life Sci. 2: 8–11. https://doi.org/10.14737/journ....
41.
Nerio L. S., Olivero-Verbel J., Stashenko E. 2010. Repellent activity of essential oils: a review. Biores. Technol. 101: 372–378. https://doi.org/10.1016/j.bior....
42.
Nosratabadi S. J., Sharifi I., Sharififar F., Bamorovat M., Daneshvar H., Mirzaie M. 2015. In vitro antileishmanial activity of methanolic and aqueous extracts of Eucalyptus camaldulensis against Leishmania major. J. Parasit. Dis. 39: 18–21. https://doi.org/10.1007/s12639....
43.
Pino J. A., Marbot R., Quert R., Garcia H. 2002. Study of essential oils of Eucalyptus resinifera, E. tereticornis and Corymbia maculata (Hook.) grown in Cuba. Flavour. Frag. J. 17: 1–14. https://doi.org/10.1002/ffj.10....
44.
Satoh K. 1978. Serum lipid peroxide in cerebrovascular disorders determined by a new colorimetric method. Clin. Chim. Acta 90: 37–43. https://doi.org/10.1016/0009-8....
45.
Serafino A., Vallebona P. S., Andreola F., Zonfrillo M., Mercuri L., Federic M., Rasi G., Garaci E., Pierimarchi P. 2008. Stimulatory effect of Eucalyptus essential oil on innate cell-mediated immune response. BMC Immunol. 9: 17. https://doi.org/10.1186/1471-2....
46.
Shoeb H. A., Madkour H. M. F., Refahy L. A., Mohamed M. A., Saad A. M., Ghareeb M. A. 2014. Antioxidant and cytotoxic activities of Gmelina arborea (ROXB.) leaves. Br. J. Pharm. Res. 4: 125–144. https://doi.org/10.9734/BJPR/2....
47.
Singab A. N., Ayoub N., Al-Sayed E., Martiskainen O., Sinkkonen J., Pihlaja K. 2011. Phenolic constituents of Eucalyptus camaldulensis Dehnh, with potential antioxidant and cytotoxic activities. Record Nat. Prod. 5: 271.
48.
Siramon P., Ohtani Y. 2007. Antioxidative and antiradical activities of Eucalyptus camaldulensis leaf oils from Thailand. J. Wood Sci. 53: 498–504. https://doi.org/10.1007/s10086....
49.
Siramon P., Ohtani Y., Ichiura H. 2009. Biological performance of Eucalyptus camaldulensis leaf oils from Thailand against the subterranean termite Coptotermes formosanus Shiraki. J. Wood Sci. 55: 41–46. https://doi.org/10.1007/s10086....
50.
Sokolow S. H., Wood C. L., Jones I. J., Swartz S. J., Lopez M., Hsieh M. H., Lafferty K. D., Kuris A. M., Rickards C., De Leo G. A. 2016. Global assessment of schistosomiasis control over the past century shows targeting the snail intermediate host works best. PLoS Negl. Trop. Dis. 10: e0004794. https://doi.org/10.1371/journa....
51.
Takahashi T., Kokubo R., Sakaino M. 2004. Antimicrobial activities of eucalyptus leaf extracts and flavonoids from Eucalyptus maculata. Lett. Appl. Microbiol. 39: 60–64. https://doi.org/10.1111/j.1472....
52.
Vermeire J. J., Yoshino T. P. 2007. Antioxidant gene expression and function in in vitro-developing Schistosoma mansoni mother sporocysts: possible role in self-protection. Parasitology 134: 1369–1378. https://doi.org/10.1017/S00311....
53.
Wang W., Wang L., Liang Y. S. 2012. Susceptibility or resistance of praziquantel in human schistosomiasis: a review. Parasitol. Res. 111: 1871–1877. https://doi.org/10.1007/s00436....
54.
Wong-Paz J. E., Contreras-Esquivel J. C., Rodríguez-Herrera R., Carrillo-Inungaray M. L., López L. I., Nevárez-Moorillón G. V., Aguilar C. N. 2015. Total phenolic content, in vitro antioxidant activity and chemical composition of plant extracts from semiarid Mexican region. Asian Pacific J. Trop. Med. 8: 104–111. https://doi.org/10.1016/S1995-....
55.
WHO (World Health Organization) 2017. Schistosomiasis weekly epidemiological record. WHO, Geneva, Switzerland.
56.
Wu X. J., Sabat G., Brown J. F., Zhang M., Taft A., Peterson N., Harms A., Yoshino T. P. 2009. Proteomic analysis of Schistosoma mansoni proteins released during in vitro miracidium-to-sporocyst transformation. Mol. Biochem. Parasitol. 164: 32–44. https://doi.org/10.1016/j.molb....
57.
Yoshino T. P., Dinguirard N., Kunert J., Hokke C. H. 2008. Molecular and functional characterization of a tandem-repeat galectin from the freshwater snail Biomphalaria glabrata, intermediate host of the human blood fluke Schistosoma mansoni. Gene 411: 46–58. https://doi.org/10.1016/j.gene....
58.
Yousif F., Ibrahim A., El-Bardicy S. N. 1998. Compatibility of Biomphalaria alexandrina, Biomphalaria glabrata and a hybrid of both to seven strains of Schistosoma mansoni from Egypt. J. Egypt Soc. Parasitol. 28: 863–881.
59.
Zelck U. E., Janowsky B. von 2004. Antioxidant enzymes in intramolluscan Schistosoma mansoni and ROS-induced changes in expression. Parasitology 128: 493–501. https://doi.org/10.1017/S00311....
60.
Zhang L., Ravipati A. S., Koyyalamudi S. R., Jeong S. C., Reddy N., Smith P. T., Bartlett J., Shanmugam K., Münch G., Wu M. J. 2011. Antioxidant and anti-inflammatory activities of selected medicinal plants containing phenolic and flavonoid compounds. J. Agric. Food Chem. 59: 12361–12367.
CITATIONS (6):
1.
Phytochemical analysis of Eucalyptus camaldulensis leaves extracts and testing its antimicrobial and schistosomicidal activities
Mosad Ghareeb, Mohamed Habib, Hanan Mossalem, Mohamed Abdel-Aziz
Bulletin of the National Research Centre
Mosad Ghareeb, Mohamed Habib, Hanan Mossalem, Mohamed Abdel-Aziz
Bulletin of the National Research Centre
2.
Biochemical and apoptotic changes in the nervous and ovotestis tissues of Biomphalaria alexandrina following infection with Schistosoma mansoni
Mohamed Habib, Samah Ghoname, Rasha Ali, Rasha El-Karim, Alaa Youssef, Roger Croll, Mark Miller
Experimental Parasitology
Mohamed Habib, Samah Ghoname, Rasha Ali, Rasha El-Karim, Alaa Youssef, Roger Croll, Mark Miller
Experimental Parasitology
3.
Effect of methyl gallate on immune response of Biomphalaria alexandrina (Ehrenberg, 1831) snails to infection with Schistosoma mansoni (Sambon, 1907)
Shereen Mansour, Sara Sayed, Marwa Abdel-Wareth
Parasitology Research
Shereen Mansour, Sara Sayed, Marwa Abdel-Wareth
Parasitology Research
4.
Impact of Schistosoma sp., infection on biological, behavioral, physiological, histological, and genotoxicological aspects of Biomphalaria alexandrina and Bulinus truncatus snails
Heba Dokmak, olfat hamam, amina ibrahim
Heba Dokmak, olfat hamam, amina ibrahim
5.
Impact of Schistosoma sp., Infection on Biological, Feeding, Physiological, Histological, and Genotoxicological Aspects of Biomphalaria alexandrina and Bulinus truncatus Snails
Hebat-Allah A. Dokmak, Olfat A. Hammam, Amina M. Ibrahim
Acta Parasitologica
Hebat-Allah A. Dokmak, Olfat A. Hammam, Amina M. Ibrahim
Acta Parasitologica
6.
Approaches of Inducing Tolerance to Murine Schistosomiasis mansoni applying Biomphalaria and Bulinus Proteins
Hanan S. Mossalem, Sami Mohamed Nasr, Azza Moustafa Fahmy, Shimaa Atta, Gehan Labib Abuelenain
Acta Parasitologica
Hanan S. Mossalem, Sami Mohamed Nasr, Azza Moustafa Fahmy, Shimaa Atta, Gehan Labib Abuelenain
Acta Parasitologica
| eISSN: | 2300-7125 |
| ISSN: | 1506-7629 |
We process personal data collected when visiting the website. The function of obtaining information about users and their behavior is carried out by voluntarily entered information in forms and saving cookies in end devices. Data, including cookies, are used to provide services, improve the user experience and to analyze the traffic in accordance with the Privacy policy. Data are also collected and processed by Google Analytics tool (more).
You can change cookies settings in your browser. Restricted use of cookies in the browser configuration may affect some functionalities of the website.
You can change cookies settings in your browser. Restricted use of cookies in the browser configuration may affect some functionalities of the website.
