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Ultrastructural changes to the tegumental system and gastrodermal cells of adult Fasciola hepatica following treatment in vivo with a commercial preparation of myrrh (Mirazid)

Published online by Cambridge University Press:  20 October 2016

M.M.O. Abdelaal
Affiliation:
Zoology Department, Faculty of Science, Al-Azhar University, Nasr City, Cairo, Egypt Parasite Therapeutics Research Group, School of Biological Sciences, Medical Biology Centre, The Queen's University of Belfast, 97 Lisburn Road, Belfast BT9 7BL, Northern Ireland, UK
G.P. Brennan
Affiliation:
Parasite Therapeutics Research Group, School of Biological Sciences, Medical Biology Centre, The Queen's University of Belfast, 97 Lisburn Road, Belfast BT9 7BL, Northern Ireland, UK
A. Abdel-Aziz
Affiliation:
Zoology Department, Faculty of Science, Al-Azhar University, Nasr City, Cairo, Egypt
I. Fairweather*
Affiliation:
Parasite Therapeutics Research Group, School of Biological Sciences, Medical Biology Centre, The Queen's University of Belfast, 97 Lisburn Road, Belfast BT9 7BL, Northern Ireland, UK
*
*Fax: +44-28-90975877 E-mail: [email protected]

Abstract

An in vivo study in the laboratory rat model has been carried out to monitor changes to the tegument and gut of adult Fasciola hepatica following treatment with myrrh (‘Mirazid’). Rats infected with the triclabendazole-resistant Dutch isolate were dosed orally with Mirazid at a concentration of 250 mg/kg and flukes recovered 2, 3 and 7 days post-treatment (pt). The flukes were processed for examination by scanning and transmission electron microscopy. A variety of changes to the external surface were observed, culminating in the sloughing of the tegumental syncytium. Internal changes to the syncytium and tegumental cell bodies were more severe and were evident from 2 days pt onwards. Swelling of the basal infolds (leading to flooding of the surface layer) and a decline in secretory body production were the major changes seen. The gastrodermal cells were less severely affected than the tegument, pointing to a trans-tegumental route of uptake for Mirazid by the fluke. Some loss of muscle fibres in the main somatic muscle layers was observed, which may be correlated with the decline in movement of flukes seen at recovery.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2016 

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References

Abo-Madyan, A.A., Morsy, T.A. & Motawea, S.M. (2004a) Efficacy of myrrh in the treatment of schistosomiasis (haematobium and mansoni) in Ezbet-El-Bakly, Tamiya Center, El-Fayoum Governorate, Egypt. Journal of the Egyptian Society of Parasitology 34, 423426.Google Scholar
Abo-Madyan, A.A., Morsy, T.A., Motawea, S.M. & Morsy, A.T.A. (2004b) Clinical trial of Mirazid in treatment of human fascioliasis, Ezbert El-Bakly (Tamyia Center) Al-Fayoum Governate. Journal of the Egyptian Society of Parasitology 34, 807818.Google Scholar
Al-Mathal, E.M. & Fouad, M.A. (2004) Myrrh (Commiphora molmol) in treatment of human and sheep dicrocoeliasis dendriticum in Saudia Arabia. Journal of the Egyptian Society of Parasitology 34, 713721.Google Scholar
Andersson, M., Bergendorff, O., Shan, R., Zygmunt, P. & Sterner, O. (1997) Minor components with smooth muscle relaxing properties from scented myrrh (Commiphora guidotti). Planta Medica 63, 251254.Google Scholar
Anthony, J.P., Fyfe, L. & Smith, H. (2005) Plant active components – a resource for antiparasitic agents? Trends in Parasitology 21, 462468.Google Scholar
Badria, F., Abou Mohamed, G., El-Mowafy, A., Massoud, A. & Salama, O. (2001) Mirazid: a new schistosomicidal drug. Pharmaceutical Biology 93, 127131.Google Scholar
Basyoni, M.M.A. & El-Sabaa, A.-A.A. (2013) Therapeutic potential of myrrh and ivermectin against experimental Trichinella spiralis infection in mice. Korean Journal of Parasitology 51, 297304.CrossRefGoogle ScholarPubMed
Botros, S., William, S., Ebeid, F., Cioli, D., Katz, N., Day, T.A. & Bennett, J.L. (2004) Lack of evidence for an antischistosomal activity of myrrh in experimental animals. American Journal of Tropical Medicine and Hygiene 71, 206210.Google Scholar
Botros, S., Sayed, H., El-Dusoki, H., Sabry, H., Rabie, I., El-Ghannan, M., Hassanein, M., El-Wahab, Y.A. & Engels, D. (2005) Efficacy of Mirazid in comparison with praziquantel in Egyptian Schistosoma mansoni-infected school children and households. American Journal of Tropical Medicine and Hygiene 72, 199223.CrossRefGoogle ScholarPubMed
Botros, S., El-Lakkany, N.M., Badawy, A.A., Mahmoud, S.S., Ebeid, F.A. & Fenwick, A. (2009) Mirazid shows insignificant activity against ovine fascioliasis. Annals of Tropical Medicine and Parasitology 103, 605616.Google Scholar
Claeson, P., Andersson, R. & Samuelson, G. (1991) T-cadinol – a pharmacologically active constituent of scented myrrh – introductory pharmacological characterization and high-field H-1-NMR and C-13-NMR data. Planta Medica 57, 352356.CrossRefGoogle Scholar
Crump, A. (2006) New medicines from nature's armamentarium. Trends in Parasitology 22, 5154.Google Scholar
El-Boshy, M.E., Husein, S.H., Fatma, M.A., Engy, F.R. & Osama, A.M. (2015) Comparative studies on triclabendazole and mirazid in guinea pigs experimentally infected with Fasciola gigantica . Journal of Bioanalysis and Biomedicine 7, 1317.Google Scholar
El-Malky, M.A., Lu, S.H., El-Beshbishi, S.N., Saudy, N.S. & Ohta, N. (2013) Effect of Mirazid in Schistosoma japonicum-infected mice: parasitological and parasitological assessment. Parasitology Research 112, 373377.Google Scholar
El-Mathal, E.M. & Fouad, M.A. (2005) Human fascioliasis among immigrant workers in Saudi Arabia. Journal of the Egyptian Society of Parasitology 35, 11991207.Google ScholarPubMed
Fairweather, I. (2009) Triclabendazole progress report, 2005–2009: an advancement of learning? Journal of Helminthology 83, 139150.Google Scholar
Fairweather, I. (2011) Liver fluke isolates: a question of provenance. Veterinary Parasitology 176, 18.Google Scholar
Fairweather, I., Anderson, H.R. & Threadgold, L.T. (1986) Fasciola hepatica: tegumental changes induced in vivo by the deacetylated (amine) metabolite of diamphenethide, Experimental Parasitology 62, 336348.CrossRefGoogle Scholar
Fairweather, I., Threadgold, L.T. & Hanna, R.E.B. (1999) Development of Fasciola hepatica in the mammalian host. pp. 47111 in Dalton, J.P. (Ed.) Fasciolosis. Oxon, UK, CAB International Publishing.Google Scholar
Fairweather, I., McShane, D.D., Shaw, L., Ellison, S.E., O'Hagan, N.T., York, E.A., Trudgett, A. & Brennan, G.P. (2012) Development of an egg hatch assay for the diagnosis of triclabendazole resistance in Fasciola hepatica: proof of concept. Veterinary Parasitology 183, 249259.Google Scholar
Fathy, F.M. (2011) Effect of mirazid (Commiphora molmol) on experimental giardiasis. Journal of the Egyptian Society of Parasitology 41, 155177.Google ScholarPubMed
Halferty, L., Brennan, G.P., Hanna, R.E.B., Edgar, H.W., Meaney, M., McConville, M., Trudgett, A., Hoey, L. & Fairweather, I. (2008) Tegumental surface changes in juvenile Fasciola hepatica in response to treatment in vivo with triclabendazole. Veterinary Parasitology 155, 4958.Google Scholar
Halferty, L., Brennan, G.P., Trudgett, A., Hoey, L. & Fairweather, I. (2009) Relative activity of triclabendazole metabolites against the liver fluke, Fasciola hepatica . Veterinary Parasitology 159, 126138.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 100, 771778.Google Scholar
Haridy, F.M., El Garhy, M.F. & Morsy, T.A. (2003) Efficacy of Mirazid (Commiphora molmol) against fascioliasis in Egyptian sheep. Journal of the Egyptian Society of Parasitology 33, 917924.Google Scholar
Haridy, F.M., Dawoud, H.A. & Morsy, T.A. (2004) Efficacy of Commiphora molmol (Mirazid) against sheep naturally infected with moneziasis expansa in Al-Santa Center, Gharbia Governate, Egypt. Journal of the Egyptian Society of Parasitology 34, 775782.Google Scholar
Haridy, F.M., El-Sherbiny, G.T. & Morsy, T.A. (2006) Some parasitic flukes infecting farm animals in Al-Santa Center, Gharbia Governate, Egypt. Journal of the Egyptian Society of Parasitology 36, 259264.Google Scholar
Hassan, M., El-Motaiem, M., Afify, H., Abaza, B., El-Shafei, M. & Massoud, M.A. (2003) In vitro effect of Mirazid in Schistosoma mansoni worms. Journal of the Egyptian Society of Parasitology 33, 9991008.Google ScholarPubMed
Hegazi, A.G., Abd El Hady, F.K. & Shalaby, H.A. (2007a) An in vitro effect of propolis on adult worms of Fasciola gigantica . Veterinary Parasitology 144, 279286.Google Scholar
Hegazi, A.G., Abd El Hady, F.K. & Shalaby, H.A. (2007b) Inhibitory effect of Egyptian propolis on Fasciola gigantica eggs with reference to its effect on Clostridium oedematiens and correlation to chemical composition. Pakistan Journal of Biological Sciences 10, 32953305.CrossRefGoogle ScholarPubMed
Iqbal, Z., Akhtar, M.S., Sindhu, Z., Khan, M. & Jabbar, A. (2003) Herbal dewormers in livestock – a traditional therapy. International Journal of Agriculture and Biology 2, 199206.Google Scholar
Kayser, O., Kiderlen, A.F. & Croft, S.L. (2003) Natural products as antiparasitic drugs. Parasitology Research 90, 5562.Google Scholar
Keiser, J. & Morson, G. (2008) Fasciola hepatica: tegumental alterations in adult flukes following in vitro and in vivo administration of artesunate and artemether. Experimental Parasitology 118, 228237.Google Scholar
Keiser, J. & Utzinger, J. (2012) Antimalarials in the treatment of schistosomiasis. Current Pharmaceutical Design 18, 35313538.Google ScholarPubMed
Keiser, J., Utzinger, J., Vennerstrom, J.L., Dong, Y., Brennan, G. & Fairweather, I. (2007) Activity of artemether and OZ78 against triclabendazole-resistant Fasciola hepatica . Transactions of the Royal Society for Tropical Medicine and Hygiene 101, 12191222.Google Scholar
Keiser, J., Veneziano, V., Rinaldi, L., Mezzino, L., Duthaler, U. & Cringoli, G. (2010) Anthelmintic activity of artesunate against Fasciola hepatica in naturally infected sheep. Research in Veterinary Science 88, 107110.CrossRefGoogle ScholarPubMed
Keiser, J., Vargas, M. & Winter, R. (2012) Anthelmintic properties of mangostin and mangostin diacetate. Parasitology International 61, 369371.Google Scholar
Keiser, J., Xiao, S.-H., Xue, J., Chang, Z.S., Odermatt, P., Tessana, S., Tanner, M. & Utzinger, J. (2006) Effect of artesunate and artemether against Clonorchis sinensis and Opisthorchis viverrini in rodent models. International Journal of Antimicrobial Agents 28, 370373.CrossRefGoogle ScholarPubMed
Kim, T.I., Yoo, W.G., Li, S., Hong, S.-T., Keiser, J. & Hong, S.-J. (2009) Efficacy of artesunate and artemether against Clonorchis sinensis in rats. Parasitology Research 106, 153156.Google Scholar
Kirchofer, C., Vargas, M., Braissant, O., Dong, Y., Wang, X., Vennerstrom, J.L. & Keiser, J. (2011) Activity of OZ78 analogues against Fasciola hepatica and Echinostoma caproni . Acta Tropica 118, 5662.Google Scholar
Kumar, D., McGeown, J.G., Reynoso-Ducoing, O., Ambrosio, J. & Fairweather, I. (2003) Observations on the musculature and isolated muscle fibres of the liver fluke, Fasciola hepatica . Parasitology 127, 457473.Google Scholar
Mahmoud, M.M. & El-Gayar, E.K. (2008) Effect of Mirazid ‘Commiphora molmol’ in treatment of experimental goat fascioliasis. Suez Canal Veterinary Medicine Journal 13, 114.Google Scholar
Mahmoud, M.M., Abou-El Dobal, S. & Soliman, K. (2008) Immune response in Fasciola gigantica experimentally infected rabbits treated with either carnosine or Mirazid. Research Journal of Parasitology 3, 4049.Google Scholar
Massoud, A., El Sisi, S., Salama, O. & Massoud, A. (2001) Preliminary study of the therapeutic efficacy of a new fasciolicidal drug derived from Commiphora molmol (myrrh). American Journal of Tropical Medicine and Hygiene 65, 9699.Google Scholar
Massoud, A., El Ebiary, F.H., Abou-Gamra, M.M., Mohamed, G.F. & Shaker, S.M. (2004) Evaluation of schistosomicidal activity of myrrh extract: parasitological and histological study. Journal of the Egyptian Society of Parasitology 34, 10511076.Google Scholar
Massoud, A.M., El-Sherbini, E.T., Mos, N., Saleh, N.M., Abouel-Nour, M.F. & Morsy, A.T. (2010) Mirazid in treatment of three zoonotic trematodes in beni-Sweif and Dakhalia Governates. Journal of the Egyptian Society of Parasitology 40, 119134.Google Scholar
Massoud, A.M., Shalaby, H.A., El Khateeb, R.M., Mahmoud, M.S. & Kutkat, M.A. (2012) Effects of Mirazid and myrrh volatile oil on adult Fasciola gigantica under laboratory conditions. Asian Pacific Journal of Tropical Biomedicine 2, 875884.Google Scholar
Massoud, A.M., Shalaby, H.A.M., El Khateeb, R.M., Mahmoud, M.S. & Kurkat, M.A.A. (2013) Tegumental histological effects of Mirazid and myrrh volatile oil on adult Fasciola gigantica . Asian Pacific Journal of Tropical Biomedicine 3, 501504.Google Scholar
McConville, M., Brennan, G.P., Flanagan, A., Hanna, R.E.B., Edgar, H.W.J., Castillo, R., Hernández-Campos, A. & Fairweather, I. (2009) Surface changes in adult Fasciola hepatica following treatment in vivo with the experimental fasciolicide, compound alpha. Parasitology Research 105, 757767.Google Scholar
McKinstry, B., Fairweather, I., Brennan, G.P. & Forbes, A.B. (2003) Fasciola hepatica: tegumental surface alterations following treatment in vivo and in vitro with nitroxynil (Trodax). Parasitology Research 91, 251263.Google Scholar
McKinstry, B., Brennan, G.P., Halferty, L., Forbes, A.B. & Fairweather, I. (2007) Ultrastructural changes induced in the tegument and gut of Fasciola hepatica following in vivo and in vitro drug treatment with nitroxynil (Trodax). Parasitology Research 101, 929941.Google Scholar
McMahon, C., Edgar, H.W.J., Hanna, R.E.B., Ellison, S.E., Flanagan, A.M., McCoy, M., Kajugu, P.-E., Gordon, A.W., Irwin, D., Barley, J.E., Malone, F.E., Brennan, G.P. & Fairweather, I. (2016) Liver fluke control on sheep farms in Northern Ireland: a survey of changing management practices in relation to disease prevalence and perceived triclabendazole resistance. Veterinary Parasitology 216, 7283.Google Scholar
Meaney, M., Fairweather, I., Brennan, G.P., McDowell, L.S.L. & Forbes, A.B. (2003) Fasciola hepatica: effects of the fasciolicide clorsulon in vitro and in vivo on the tegumental surface, and a comparison of the effects on young- and old-mature flukes. Parasitology Research 91, 238250.Google Scholar
Meaney, M., Fairweather, I., Brennan, G.P. & Forbes, A.B. (2004) Transmission electron microscope study of the ultrastructural changes induced in the tegument and gut of Fasciola hepatica following in vivo treatment with clorsulon. Parasitology Research 92, 232241.Google Scholar
Meaney, M., Haughey, S., Brennan, G.P. & Fairweather, I. (2005) Ultrastructural observations on oral ingestion and trans-tegumental uptake of clorsulon by the liver fluke, Fasciola hepatica . Parasitology Research 95, 201212.Google Scholar
Meister, I., Duthaler, U., Huwyler, J., Rinaldi, L., Bosco, A., Cringoli, G. & Keiser, J. (2013) Efficacy and pharmacokinetics of OZ78 and MT04 against a natural infection with Fasciola hepatica in sheep. Veterinary Parasitology 198, 102110.Google Scholar
Morsy, T.A., Salem, H.S., Haridy, F.M., Rifaat, M.M., Abo-Zenadah, N.Y. & Adel el-Kadi, M. (2005) Farm animals’ fascioliasis in Ezbet El-Bakly (Tamyia Center), Al-Fayoum Governate. Journal of the Egyptian Society of Parasitology 35, 825832.Google Scholar
Mottier, L., Alvarez, L., Fairweather, I. & Lanusse, C. (2006) Resistance-induced changes in triclabendazole transport in Fasciola hepatica: ivermectin reversal effect. Journal of Parasitology 6, 13551360.Google Scholar
Ndjonka, D., Rapado, L.N., Silber, A.M., Liebau, E. & Wrenger, C. (2013) Natural products as a source for treating Neglected Parasitic Diseases. International Journal of Molecular Sciences 14, 33953439.Google Scholar
O'Neill, J.F., Johnston, R.C., Halferty, L., Brennan, G.P., Keiser, J. & Fairweather, I. (2009) Adult triclabendazole-resistant Fasciola hepatica: morphological changes in the tegument and gut following in vivo treatment with artemether in the rat model. Journal of Helminthology 83, 151163.Google Scholar
O'Neill, J.F., Johnston, R.C., Halferty, L., Brennan, G.P. & Fairweather, I. (2015) Ultrastructural changes in the tegument and gut of adult Fasciola hepatica following in vivo treatment with artesunate. Experimental Parasitology 154, 143154.Google Scholar
Osman, M.M., El-Taweel, H.A., Shehab, A.Y. & Farag, H.F. (2010) Ineffectiveness of myrrh-derivative Mirazid against schistosomiasis and fascioliasis in humans. Eastern Mediterranean Health Journal 16, 932936.Google Scholar
Robinson, G. & Threadgold, L.T. (1975) Electron microscope studies of Fasciola hepatica . XIII. The fine structure of the gastrodermis. Experimental Parasitology 37, 2036.Google Scholar
Sheir, Z., Nasr, A.A., Massoud, A., Salama, O., Badra, G.A., El-Shennawy, H., Hassan, N. & Hammad, S.M. (2001) A safe, effective, herbal antischistosomal therapy derived from Myrrh. American Journal of Tropical Medicine and Hygiene 65, 700704.Google Scholar
Skuce, P.J. & Fairweather, I. (1990) The effect of the hydrogen ionophore closantel upon the pharmacology and ultrastructure of the adult liver fluke Fasciola hepatica . Parasitology Research 76, 241250.CrossRefGoogle ScholarPubMed
Soliman, O.E., El-Arman, M., Abdul-Samie, E.R., El-Nemer, H.I. & Massoud, A. (2004) Evaluation of myrrh (Mirazid) therapy in fascioliasis and intestinal schistosomiasis in children: immunological and parasitological study. Journal of the Egyptian Society of Parasitology 34, 941966.Google Scholar
Stitt, A.W. & Fairweather, I. (1994) The effect of the sulphoxide metabolite of triclabendazole (‘Fasinex’) on the tegument of mature and immature stages of the liver fluke, Fasciola hepatica . Parasitology 108, 555567.Google Scholar
Toner, E., Brennan, G.P., Wells, K., McGeown, J.G. & Fairweather, I. (2008) Physiological and morphological effects of genistein against the liver fluke, Fasciola hepatica . Parasitology 135, 11891203.Google Scholar
Toner, E., McConvery, F., Brennan, G.P., Meaney, M. & Fairweather, I. (2009) A scanning electron microscope study on the route of entry of triclabendazole into the liver fluke, Fasciola hepatica . Parasitology 126, 523535.CrossRefGoogle Scholar
Toner, E., Brennan, G.P., McConvery, F., Meaney, M. & Fairweather, I. (2010) A transmission electron microscope study on the route of entry of triclabendazole into the liver fluke, Fasciola hepatica . Parasitology 137, 855870.Google Scholar
Vissiennon, C., Goos, K.H., Goos, O. & Nieber, K. (2015) Antispasmodic effects of myrrh due to calcium antagonistic effects in inflamed rat small intestinal preparations. Planta Medica 81, 116122.Google Scholar
Yakoot, M. (2010) A short review of the anthelmintic role of Mirazid. Arquivos de Gastroenterologia 47, 393394.Google Scholar