Hostname: page-component-5b777bbd6c-7sgmh Total loading time: 0 Render date: 2025-06-23T06:24:40.577Z Has data issue: false hasContentIssue false
  • English
  • Français

Fasciola hepatica infections in cattle and the freshwater snail Galba truncatula from Dakhla Oasis, Egypt

Published online by Cambridge University Press:  06 February 2017

W.M. Arafa ,
A.I. Hassan ,
S.A.M. Snousi ,
Kh.M. El-Dakhly ,
P.J. Holman ,
T.M. Craig  and
S.M. Aboelhadid
W.M. Arafa
Affiliation:
Department of Parasitology, Faculty of Veterinary Medicine Beni-Suef University, Beni-Suef 62511, Egypt
A.I. Hassan
Affiliation:
Regional Animal Health Research Laboratory, Animal Health Research Institute, Dakhla, El-Wadi El-Gadid, Egypt
S.A.M. Snousi
Affiliation:
Regional Animal Health Research Laboratory, Animal Health Research Institute, Dakhla, El-Wadi El-Gadid, Egypt
Kh.M. El-Dakhly
Affiliation:
Department of Parasitology, Faculty of Veterinary Medicine Beni-Suef University, Beni-Suef 62511, Egypt
P.J. Holman
Affiliation:
Department of Veterinary Pathobiology, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, Texas 77843-4467, USA
T.M. Craig
Affiliation:
Department of Veterinary Pathobiology, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, Texas 77843-4467, USA
S.M. Aboelhadid*
Affiliation:
Department of Parasitology, Faculty of Veterinary Medicine Beni-Suef University, Beni-Suef 62511, Egypt
*
*Fax: 0020822327982 E-mail: drshawky2001@yahoo.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Infection by Fasciola species was investigated in seven districts of Dakhla Oasis, Egypt, through abattoir inspection of cattle livers for adult worms and sedimentation of faecal samples from local cattle to detect Fasciola eggs. In addition, lymnaeid snails collected from the study area were examined microscopically for developmental stages of Fasciola spp. Abattoir inspection revealed that 51 out of 458 cattle livers (11.1%) contained adult flukes, which were identified morphologically as Fasciola hepatica. Examination of the cattle faecal samples revealed that 142 out of 503 (28.2%) contained Fasciola eggs. The collected snails, identified as Galba truncatula and Radix natalensis, showed larval stages of Fasciola in 71 out of 731 (9.7%) G. truncatula, while R. natalensis showed no infection. Specific duplex polymerase chain reaction (PCR) targeting the mitochondrial cox1 gene of F. hepatica and Fasciola gigantica was carried out on DNA extracted from pooled infected snails and adult worms. The F. hepatica size amplicon (1031 bp) was obtained from both the infected G. truncatula and the adult worms isolated from cattle livers from different districts. The amplicon sequences were identical to the published sequences of F. hepatica mitochondrial cox1 gene. In conclusion, the zoonotic importance of Fasciola infection and appropriate hygienic measures must be taken into consideration in Dakhla Oasis, Egypt.

Type
Research Papers
Information
Journal of Helminthology , Volume 92 , Issue 1 , January 2018 , pp. 56 - 63
Copyright
Copyright © Cambridge University Press 2017 

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.)

Article purchase

Temporarily unavailable

References

Abd El-Ghani, A.F. (1976) The present situation of Lymnaea snails in the New Valley. Proceedings of the 13th Arab Veterinary Congress, Cairo, Egypt, pp. 556–567.Google Scholar
Abdo, B.R.N. (2014) Epidemiological studies on fascioliasis in Assiut and New Valley Governorates . PhD VSc thesis, Animal Hygiene and Zoonoses Department, Faculty of Veterinary Medicine, Assiut University.Google Scholar
Abdulhakim, Y. & Addis, M. (2012) An abattoir study on the prevalence of fasciolosis in cattle, sheep and goats in Debre Zeit Town, Ethiopia. Global Veterinaria 8, 308–314.Google Scholar
Altschul, S.F., Gish, W., Miller, W., Myers, E.W. & Lipman, D.J. (1990) Basic local alignment search tool. Journal of Molecular Biology 215, 403–410.CrossRefGoogle Scholar
Amer, S., Dar, Y., Ichikawa, M., Fukuda, Y., Tada, C., Itagaki, T. & Nakai, Y. (2011) Identification of Fasciola species isolated from Egypt based on sequence analysis of genomic (ITS1 and ITS2) and mitochondrial (NDI and COI) gene markers. Parasitology International 60, 5–12.Google Scholar
Arafa, W.M., Shokeir, K.M. & Khateib, A.M. (2015) Comparing an in vivo egg reduction test and in vitro egg hatching assay for different anthelmintics against Fasciola species, in cattle. Veterinary Parasitology 214, 152–158.Google Scholar
Ashrafi, K., Valero, M.A., Panova, M., Periago, M.V., Massoud, J. & Mas-Coma, S. (2006) Phenotypic analysis of adults of Fasciola hepatica, Fasciola gigantica and intermediate forms from the endemic region of Gilan, Iran. Parasitology International 55, 249–260.Google Scholar
Atallah, S.T. (2008) Economic losses from fascioliasis in slaughtered animals: at abattoir levels. Minufiya Veterinary Journal 5, 2.Google Scholar
Bargues, M.D., Artigas, P., Khoubbane, M., Ortiz, P., Naquira, C. & Mas-CoMa, S. (2012) Molecular characterisation of Lymnaea truncatula, Lymnaea neotropica and L. schirazensis from Cajamarca, Peru and their potential role in transmission of human and animal fascioliasis. Parasites & Vectors 5, 174.Google Scholar
Biu, A.A., Paul, B.T., Konto, M. & Ya'uba, A.M. (2013) Cross sectional and phenotypic studies on fasciolosis in slaughter cattle in Maiduguri, Nigeria. Journal of Agriculture and Veterinary Sciences 5, 155–162.Google Scholar
Brown, D.S. (1994) Freshwater snails of Africa and their medical importance. 2nd edn. London, UK, Taylor and Francis.CrossRefGoogle Scholar
Caron, Y., Righi, S., Lempereur, L., Saegerman, C. & Losson, B. (2011) An optimized DNA extraction and multiplex PCR for the detection of Fasciola sp. in lymnaeid snails. Veterinary Parasitology 178, 93–99.Google Scholar
Cucher, M.A., Carnevale, S., Prepelitchi, L., Labbé, J.H. & Wisnivesky-Colli, C. (2006) PCR diagnosis of F. hepatica in field-collected Lymnaea columella and Lymnaea viatrix snails. Veterinary Parasitology 137, 74–82.CrossRefGoogle Scholar
Curtis, L.A. & Hubbard, K.M. (1990) Trematode infections in a gastropod host misrepresented by observing shed cercariae. Journal of Experimental Marine Biology and Ecology 143, 131–137.Google Scholar
Dar, Y.D., Rondelaud, D. & Dreyfuss, G. (2005) Update of fasciolosis-transmitting snails in Egypt (review and comment). Journal of the Egyptian Society of Parasitology 35, 477–490.Google Scholar
Dar, Y., Djuikwo Teukeng, F.F., Vignoles, P., Dreyfuss, G. & Rondelaud, D. (2010) Radix natalensis (Gastropoda: Lymnaeidae), a potential intermediate host of Fasciola hepatica in Egypt. Parasite 17, 251–256.CrossRefGoogle Scholar
Dar, Y., Amer, S., Mercier, A., Courtioux, B. & Dreyfuss, G. (2012) Molecular identification of Fasciola spp. (Digenea: Fasciolidae) in Egypt. Parasite 19, 177–182.Google Scholar
Dar, Y., Lounnas, M., Djuikwo Teukeng, F.F., Mouzet, R., Courtioux, B., Hurtrez-Boussès, S., Vignoles, P., Dreyfuss, G. & Rondelaud, D. (2013) Variations in local adaptation of allopatric F. hepatica to French Galba truncatula in relation to parasite origin. Parasitology Research 112, 2543–2549.CrossRefGoogle Scholar
Dar, Y., Vignoles, P., Rondelaud, D. & Dreyfuss, G. (2014) Role of the lymnaeid snail Pseudosuccinea columella in the transmission of the liver fluke Fasciola hepatica in Egypt. Journal of Helminthology 89, 699–706.Google Scholar
Diab, M.R. (1993) Biological studies on trematode larvae and freshwater snails. MVSc thesis, Faculty of Veterinary Medicine, Alexandria University.Google Scholar
Drury, R.A. & Wallingten, E.A. (1980) Carleton's histological technique. 5th edn. Oxford, Oxford University Press.Google Scholar
El-Kady, G.A., Shoukry, A., Reda, L.A. & El-badri, Y.S. (2000) Survey and population dynamics of freshwater snails in newly settled areas of the Sinai Peninsula. Egyptian Journal of Biology 2, 42–48.Google Scholar
El-Shazly, A.M., Helmy, M.M., Haridy, F.M., El-Sharkawy, E.M. & Morsy, T.A. (2002) Fasciola immature stages sought in Lymnaea species and Biomphalaria species in the water bodies of Dakahlia Governorate. Journal of the Egyptian Society of Parasitology 32, 109–118.Google Scholar
El-Shazly, A.M., El-Nahas, H.A., Soliman, M., Sultan, D.M., Abedl Tawab, A.H. & Morsy, T.A. (2006) The reflection of control programs of parasitic diseases upon gastrointestinal helminthiasis in Dakahlia Governorate, Egypt. Journal of the Egyptian Society of Parasitology 36, 467–480.Google Scholar
El-Shazly, A.M., Nabih, N., Salem, D.A. & Mohamed, M.Z. (2012) Snail populations in Dakahlia Governorate, Egypt, with special reference to lymnaeids. Egyptian Journal of Biology 14, 45–49.Google Scholar
Ghoneim, N.H., Hassan, M.A., El Newishy, A.M. & Mahmoud, S.M. (2011) Fasciola as a zoonotic parasite in slaughtered animals at Kalyobia abattoirs. Benha Veterinary Medical Journal 22, 207–213.Google Scholar
Haseeb, A.N., EL-Shazly, A.M., Arafa, M.A. & Morsy, A.T. (2002) A review on fascioliasis in Egypt. Journal of the Egyptian Society of Parasitology 32, 317–354.Google Scholar
Hussain, A.N. & Khalifa, M.A.K. (2010) Phenotypic description and prevalence of Fasciola species in Qena Governorate, Egypt with special reference to a new strain of Fasciola hepatica . Journal of King Saud University-Science 22, 1–8.Google Scholar
Ibrahim, A.M., Bishai, H.M. & Khalil, M.T. (1999) Freshwater molluscs of Egypt. Cairo, Egypt, National Biodiversity Unit, Egyptian Environmental Affairs Agency.Google Scholar
Ichikawa, M. & Itagaki, T. (2010) Discrimination of the ITS1 types of Fasciola spp. based on a PCR-RFLP method. Parasitology Research 106, 757–761.Google Scholar
Itagaki, T. & Tsutsumi, K. (1998) Triploid form of Fasciola in Japan: genetic relationships between Fasciola hepatica and Fasciola gigantica determined by ITS-2 sequence of nuclear rDNA. International Journal for Parasitology 28, 777–781.Google Scholar
Itagaki, T., Tsutsumi, K., Ito, K. & Tsutsumi, Y. (1998) Taxanomic status of the Japanese triploid forms of Fasciola: comparison of mitochondrial ND1 and COI sequences with F. hepatica and F. gigantica . Journal of Parasitology 84, 445–448.Google Scholar
Itagaki, T., Kikawa, M., Sakaguchi, K., Shimo, J., Terasaki, K., Shibahara, T. & Fukuda, K. (2005) Genetic characterization of parthenogenic Fasciola sp. in Japan on the basis of the sequences of ribosomal and mitochondrial DNA. Parasitology 131, 679–785.CrossRefGoogle Scholar
Jackson, J.H. (1958) Bilharezia. A background of its endemicity and control in Africa with particular reference to irrigation scheme. South African Journal of Laboratory Clinical Medicine 4, 1–54.Google Scholar
Kadir, M.A., Ali, N.H. & Ridha, R.G.M. (2012) Prevalence of helminthes, pneumonia and hepatitis in Kirkuk slaughter house, Kirkuk, Iraq. Iraqi Journal of Veterinary Science 26, 83–88.Google Scholar
Khan, U.J. & Maqbool, A. (2012) Prevalence of fasciolosis in cattle under different managemental conditions in Punjab. Pakistan Journal of Zoology 44, 1193–1196.Google Scholar
Kuraa, H.M. & Malek, S.S. (2014) Parasitological and serological study on Fasciola diagnosis in cattle and buffaloes in Assiut Governorate. Assiut Veterinary Medical Journal 60, 96–104.Google Scholar
Lambert, W.J., Corliss, E., Sha, J. & Smalls, J. (2012) Trematode infections in Littorina littorea on the New Hampshire Coast. Northeastern Naturalist 19, 461–474.Google Scholar
Le, T.H., Nguyen, K.T., Nguyen, N.T.B., Doan, H.T., Le, X.T.K., Hoang, C.T.M. & De, N.V. (2012) Development and evaluation of a single-step duplex PCR for simultaneous detection of Fasciola hepatica and Fasciola gigantica (family Fasciolidae, class Trematoda, phylum Platyhelminthes). Journal of Clinical Microbiology 50, 2720–2726.CrossRefGoogle Scholar
Lloyd, M.M. & Poulin, R. (2012) Fitness benefits of a division of labour in parasitic trematode colonies with and without competition. International Journal for Parasitology 42, 939–946.Google Scholar
Lotfy, W.M. & Hillyer, G.V. (2003) Fasciola species in Egypt. Experimental Pathology and Parasitology 6, 9–22.Google Scholar
Lotfy, W.M., El-Morshedy, H.N., Abou El-Hoda, M., El-Tawila, M.M., Omar, E.A. & Farag, H.F. (2002) Identification of the Egyptian species of Fasciola . Veterinary Parasitology 103, 323–332.Google Scholar
Marcilla, A., Bargues, M.D. & Mas-Coma, S. (2002) A PCR-RFLP assay for the distinction between Fasciola hepatica and Fasciola gigantica . Molecular and Cellular Probes 16, 327–333.Google Scholar
Martínez-Ibeas, A.M., Martínez-Valladares, M., González-Lanza, C., Miñambres, B. & Manga-González, M.Y. (2011) Detection of Dicrocoelium dendriticum larval stages in mollusc and ant intermediate hosts by PCR, using mitochondrial and ribosomal internal transcribed spacer (ITS-2) sequences. Parasitology 138, 1916–1923.Google Scholar
Mas-Coma, S., Bargues, M.D. & Valero, M.A. (2005) Fascioliasis and other plant-borne trematode zoonoses. International Journal for Parasitology 35, 1255–1278.Google Scholar
Ngele, K.K. & Ibe, E. (2014) Prevalence of Fasciolopsis in cattle slaughtered at Eke Market abattoir, Afikpo, Ebonyi state, Nigeria. Animal Research International 11, 1958–1963.Google Scholar
Periago, M.V., Valero, M.A., El Sayed, M., Ashrafi, K., El Wakeel, A., Mohamed, M.Y., Desquesnes, M., Curtale, F. & Mas-Coma, S. (2008) First phenotypic description of Fasciola hepatica/Fasciola gigantica intermediate forms from the human endemic area of the Nile Delta, Egypt. Infection Genetics & Evolution 8, 51–58.Google Scholar
Rognlie, M.C., Dimke, K.L., Potts, R.S. & Knapp, S.E. (1996) Seasonal transmission of Fasciola hepatica in Montana, USA, with detection of infected intermediate hosts using a DNA-based assay. Veterinary Parasitology 65, 297–305.Google Scholar
Shiferaw, M., Feyisa, B. & Ephrem, T. (2011) Prevalence of bovine fasciolosis and its economic significance in and around Assela, Ethiopia. Global Journal of Medical Research 11.Google Scholar
Soliman, F.M. (2008) Epidemiological review of human and animal fascioliasis in Egypt. The Journal of Infection in Developing Countries 2, 182–189.Google Scholar
Soulsby, E.J. (1982) Helminths, arthropods and protozoa of domesticated animals. 7th edn. London, Bailliere, Tindall and Cassell.Google Scholar
Spithil, T.M., Smooker, P.M. & Copeman, D.B. (1999) Fasciola gigantica: epidemiology, control, immunology and molecular biology. pp. 465–525 in Dalton, J.P. (Ed.) Fasciolosis. Oxon., CABI Publishing.Google Scholar
Studer, A. & Poulin, R. (2012) Seasonal dynamics in an intertidal mudflat: the case of a complex trematode life cycle. Marine Ecology Progress Series 455, 79–93.Google Scholar
Stunkard, H.W. & Hinchliffe, M.C. (1952) The morphology and life-history of Microbilharzia variglandis (Miller and Northup, 1926) Stunkard and Hinchliffe, 1951, avian blood-flukes whose larvae cause ‘swimmer's itch’ of ocean beaches. Journal of Parasitology 38, 248–265.CrossRefGoogle Scholar
Teklu, H., Abebe, N. & Kumar, N. (2015) Abattoir prevalence of bovine fasciolosis in the municipal abattoir of Wukro, Northern Ethiopia. Journal of International Academic Research for Multidisciplinary 2, 430–438.Google Scholar
Terasaki, K., Moriyama-Gonda, N. & Noda, Y. (1998) Abnormal spermatogenesis in the common liver fluke (Fasciola sp.) from Japan and Korea. Journal of Veterinary Medical Science 60, 1305–1309.Google Scholar
Tsegaye, B., Abebaw, H. & Girma, S. (2012) Study on coprological prevalence of bovine fasciolosis in and around Woreta, Northwestern Ethiopia. Journal of Veterinary Medicine and Animal Health 4, 89–92.Google Scholar
Urquhart, G.M., Armour, J., Duncan, J.L., Dunn, A.M. & Jennings, F.W. (1996) Veterinary parasitology. 2nd edn. London, Blackwell Science.Google Scholar
WHO (World Health Organization) (2007) Report of the WHO Informal Meeting on use of triclabendazole in fascioliasis control. WHO/CDS/NTD/PCT/2007.1. Geneva, WHO.Google Scholar
WHO (World Health Organization) (2015) Neglected tropical diseases. Available at http://www.who.int/neglected_diseases/diseases/en/ (accessed March 2016).Google Scholar