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Molecular evidence shows that the liver fluke Fasciola gigantica is the predominant Fasciola species in ruminants from Pakistan

Published online by Cambridge University Press:  11 March 2015

U. Chaudhry ,
B. van Paridon ,
M.Z. Shabbir ,
M. Shafee ,
K. Ashraf ,
T. Yaqub  and
J. Gilleard
U. Chaudhry
Affiliation:
Department of Comparative Biology and Experimental Medicine, Faculty of Veterinary Medicine, University of Calgary, Alberta, Canada
B. van Paridon*
Affiliation:
Department of Biology, Faculty of Science, University of Lethbridge, Alberta, Canada
M.Z. Shabbir
Affiliation:
Quality Operations Laboratory, University of Veterinary and Animal Sciences, Lahore, Pakistan
M. Shafee
Affiliation:
Centre for Advanced Studies in Vaccine and Biotechnology, University of Baluchistan, Quetta, Pakistan
K. Ashraf
Affiliation:
Department of Parasitology, University of Veterinary and Animal Sciences, Lahore, Pakistan
T. Yaqub
Affiliation:
Quality Operations Laboratory, University of Veterinary and Animal Sciences, Lahore, Pakistan
J. Gilleard
Affiliation:
Department of Comparative Biology and Experimental Medicine, Faculty of Veterinary Medicine, University of Calgary, Alberta, Canada
*
*E-mail: [email protected]
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Abstract

Fascioliasis is an important disease affecting livestock, with great costs to producers worldwide. It has also become a serious issue for human populations in some endemic areas as an emerging zoonotic infection. There are two Fasciola species of liver fluke responsible for this disease, which occur worldwide, Fasciola hepatica and Fasciola gigantica. Identifying these two species on the basis of adult or egg morphology requires specialist knowledge due to the similarity of characters, and may misidentify putative intermediate or hybrid forms. In this study we sequenced the internal transcribed spacer 2 (ITS-2) rDNA of liver flukes collected from multiple species of hosts from seven localities in the Punjab and Baluchistan provinces of Pakistan, to determine the distribution of these two species. All 46 flukes processed in this study, collected from seven sites, showed the rDNA ITS-2 genotype corresponding to F. gigantica, contradicting previous reports, based on adult and egg morphology, that both species are present in Pakistan, with F. hepatica being the more common.

Type
Research Papers
Information
Journal of Helminthology , Volume 90 , Issue 2 , March 2016 , pp. 206 - 213
Copyright
Copyright © Cambridge University Press 2015 

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References

Adlard, R.D., Barker, S.C., Blair, D. & Cribb, T.H. (1993) Comparison of the second internal transcribed spacer (ribosomal DNA) from populations and species of Fasciolidae (Digenea). International Journal for Parasitology 23, 423–425.Google Scholar
Afshan, K., Valero, M.A., Qayyum, M., Peixoto, R.V., Magraner, A. & Mas-Coma, S. (2013) Phenotypes of intermediate forms of Fasciola hepatica and F. gigantica in buffaloes from Central Punjab, Pakistan. Journal of Helminthology 88, 1–10.Google Scholar
Afshan, K., Fortes-Lima, C.A., Artigas, P., Valero, A.M., Qayyum, M. & Mas-Coma, S. (2014) Impact of climate change and man-made irrigation systems on the transmission risk, long-term trend and seasonality of human and animal fascioliasis in Pakistan. Geospatial Health 8, 317–334.Google Scholar
Agatsuma, T., Arakawa, Y., Iwagami, M., Honzako, Y., Cahyaningsih, U., Kang, S.Y. & Hong, SJ. (2000) Molecular evidence of natural hybridization between Fasciola hepatica and F. gigantica . Parasitology International 49, 231–238.Google Scholar
Ahmed, S., Nawaz, M., Gul, R., Zakir, M. & Razzaq, A. (2005) Diversity and prevalence of trematodes in livers of sheep and goat in Quetta, Pakistan. Pakistan Journal of Zoology 37, 205–210.Google Scholar
Ai, L., Dong, S.J., Zhang, W.Y., Elsheikha, H.M., Mahmmod, Y.S., Lin, R.Q., Yuan, Z.G., Shi, Y.L., Huang, W.Y. & Zhu, X.Q. (2010) Specific PCR-based assays for the identification of Fasciola species: their development, evaluation and potential usefulness in prevalence surveys. Annals of Tropical Medicine and Parasitology 104, 65–72.Google Scholar
Akhtar, A., Arshad, M., Shakeebullah, H., Hidayatullah, U. & Ameer, M. (2012) Prevalence of Fasciola hepatica in sheep and goats in district Dera Ismail Khan. Journal of Science 64, 31–34.Google Scholar
Ali, H., Ai, L., Song, H.Q., Ali, S., Lin, R.Q., Seyni, B., Issa, G. & Zhu, X.Q. (2008) Genetic characterisation of Fasciola samples from different host species and geographical localities revealed the existence of F. hepatica and F. gigantica in Niger. Parasitology Research 102, 1021–1024.CrossRefGoogle Scholar
Amor, N., Farjallah, S., Salem, M., Lamine, D.M., Merella, P., Said, K. & Ben Slimane, B. (2011a) Molecular characterization of Fasciola gigantica from Mauritania based on mitochondrial and nuclear ribosomal DNA sequences. Experimental Parasitology 129, 127–136.Google Scholar
Amor, N., Halajian, A., Farjallah, S., Merella, P., Said, K. & Ben Slimane, B. (2011b) Molecular characterization of Fasciola spp. from the endemic area of northern Iran based on nuclear ribosomal DNA sequences. Experimental Parasitology 128, 196–204.Google Scholar
Ashraf, S., Iqbal, Z., Ali, M., Chaudary, H.R., Sial, N., Ahsan, U., Ali, A. & Asif, Z. (2014) Seasonal prevalence of Fasciola hepatica infection in buffaloes of Bahawalpur District of Punjab, Pakistan. Journal of Infection and Molecular Biology 2, 30–31.Google 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.CrossRefGoogle ScholarPubMed
Drummond, A.J., , A.B., Buxton, S., Cheung, M., Cooper, A., Duran, C., Field, M., Heled, J., Kearse, M., Markowitz, S., Moir, R., Stones-Havas, S., Sturrock, S., Thierer, T. & Wilson, A. (2012) Geneious v5.6. Available at http://www.geneious.com/ (accessed accessed 17 February 2015).Google Scholar
El-Rahimy, H.H., Mahgoub, A.M., El-Gebaly, N.S., Mousa, W.M. & Antably, A.S. (2012) Molecular, biochemical, and morphometric characterization of Fasciola species potentially causing zoonotic disease in Egypt. Parasitology Research 111, 1103–1111.Google Scholar
Farjallah, S., Ben Slimane, B., Piras, C.M., Amor, N., Garippa, G. & Merella, P. (2013) Molecular characterization of Fasciola hepatica from Sardinia based on sequence analysis of genomic and mitochondrial gene markers. Experimental Parasitology 135, 471–478.Google Scholar
Freites, A., Colmenares, C., Alarcon-Noya, B., Garcia, M.E. & Diaz-Suarez, O. (2009) Human fasciolosis in Mara municipality, Zulia state. Venezuela: prevalence and associated factors. Investigacion Clinica 50, 497–506.Google Scholar
Gadahi, J.A., Arshed, M.J., Ali, Q., Javaid, S.B. & Shah, S.I. (2009) Prevalence of gastrointestinal parasites of sheep and goat in and around Rawalpindi and Islamabad, Pakistan. Veterinary World 2, 51–53.Google Scholar
Garippa, S.F. (2009) Genetic characterization of Fasciola hepatica from Tunisia and Algeria base. Parasitology Research 105, 1617–1621.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 ScholarPubMed
Hossain, M.M., Paul, S., Rahman, M.M., Hossain, F.M.A., Hossain, M.T. & Islam, M.R. (2011) Prevalence and economic significance of caprine fascioliasis at Sylhet district of Bangladesh. Pakistan Veterinary Journal 31, 113–116.Google Scholar
Huang, W.Y., He, B., Wang, C.R. & Zhu, X.Q. (2004) Characterisation of Fasciola species from Mainland China by ITS-2 ribosomal DNA sequence. Veterinary Parasitology 120, 75–83.CrossRefGoogle ScholarPubMed
Huang, Y., Niu, B.F., Gao, Y., Fu, L.M. & Li, W.Z. (2010) CD-HIT Suite: a web server for clustering and comparing biological sequences. Bioinformatics 26, 680–682.CrossRefGoogle ScholarPubMed
Ichikawa, M. & Itagaki, T. (2010) Discrimination of the ITS1 types of Fasciola spp. based on a PCR-RFLP method. Parasitology Research 106, 757–761.CrossRefGoogle ScholarPubMed
Ijaz, M., Kahn, M.S., Avais, M., Ashraf, K., Ali, M.M. & Khan, M.Z.U. (2007) Infection rate and chemotherapy of various helminthes in diarrheic sheep in and around Lahore. Journal of Animal and Plant Sciences 19, 13–16.Google Scholar
Iqbal, M.U., Sajid, M.S., Hussain, A. & Khan, M.K. (2007) Prevalence of helminth infections in dairy animals of Nestle milk collection areas of Punjab (Pakistan). Italian Journal of Animal Science 6, 935–938.CrossRefGoogle 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.I., Ito, K. & Tsutsumi, Y. (1998) Taxonomic 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, 679–685.CrossRefGoogle ScholarPubMed
Itagaki, T., Sakaguchi, K., Terasaki, K., Sasaki, O., Yoshihara, S. & Van Dung, T. (2009) Occurrence of spermic diploid and aspermic triploid forms of Fasciola in Vietnam and their molecular characterization based on nuclear and mitochondrial DNA. Parasitology International 58, 81–85.Google Scholar
Kakar, M.N., Masood, M.I., Janbaz, K.H., Qadir, M.I., Masood, I. & Kakarsulemankhel, J.K. (2011) Prevalence of Fascioliasis in cows and buffaloes Quetta, Pakistan. Pharmacology Online 2, 974–978.Google Scholar
Karahocagil, M.K., Akdeniz, H., Sunnetcioglu, M., Cicek, M., Mete, R., Akman, N., Ceylan, E., Karsen, H. & Yapici, K. (2011) A familial outbreak of fascioliasis in Eastern Anatolia: a report with review of literature. Acta Tropica 118, 177–183.Google Scholar
Khan, M.K., Sajid, M.S., Khan, M.N., Iqbal, Z. & Iqbal, M.U. (2009) Bovine fasciolosis: prevalence, effects of treatment on productivity and cost benefit analysis in five districts of Punjab, Pakistan. Research in Veterinary Science 87, 70–75.Google Scholar
Le, T.H., De, N.V., Agatsuma, T., Thi Nguyen, T.G., Nguyen, Q.D., McManus, D.P. & Blair, D. (2008) Human fascioliasis and the presence of hybrid/introgressed forms of Fasciola hepatica and Fasciola gigantica in Vietnam. International Journal for Parasitology 38, 725–730.CrossRefGoogle ScholarPubMed
Le, T.H., Nguyen, K.T., Nguyen, N.T., Doan, H.T., Le, X.T., Hoang, C.T. & 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.Google Scholar
Liu, G.H., Gasser, R.B., Young, N.D., Song, H.Q., Ai, L. & Zhu, X.Q. (2014) Complete mitochondrial genomes of the ‘intermediate form’ of Fasciola and Fasciola gigantica, and their comparison with F. hepatica . Parasites and Vectors 7, 150–159.Google Scholar
Lotfy, W.M., Brant, S.V., DeJong, R.J., Le, T.H., Demiaszkiewicz, A., Rajapakse, R.P., Perera, V.B., Laursen, J.R. & Loker, E.S. (2008) Evolutionary origins, diversification, and biogeography of liver flukes (Digenea, Fasciolidae). American Journal of Tropical Medicine and Hygiene 79, 248–255.Google Scholar
Marcilla, A., Barques, 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.CrossRefGoogle ScholarPubMed
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
Mas-Coma, S., Valero, M.A. & Bargues, M.D. (2009) Fasciola, lymnaeids and human fascioliasis, with a global overview on disease transmission, epidemiology, evolutionary genetics, molecular epidemiology and control. Advances in Parasitology 69, 41–146.Google Scholar
Mas-Coma, S., Valero, M.A. & Bargues, M.D. (2014) Fascioliasis. Advances in Experimental Medicine and Biology 766, 77–114.Google Scholar
Mera y Sierra, R., Agramunt, V.H., Cuervo, P. & Mas-Coma, S. (2011) Human fascioliasis in Argentina: retrospective overview, critical analysis and baseline for future research. Parasites and Vectors 4, 104.Google Scholar
Prasad, P.K., Tandon, V., Biswal, D.K., Goswami, L.M. & Chatterjee, A. (2008) Molecular identification of the Indian liver fluke, Fasciola (Trematoda: Fasciolidae) based on the ribosomal internal transcribed spacer regions. Parasitology Research 103, 1247–1255.Google Scholar
Qureshi, A.W., Tanveer, A., Qureshi, S.W., Maqbool, A., Gill, T.J. & Ali, S.A. (2005) Epidemiology of human fasciolosis in rural areas of Lahore, Pakistan. Punjab University Journal of Zoology 20, 159–168.Google Scholar
Raina, O.K., Jacob, S.S., Sankar, M., Bhattacharya, S., Bandyopadyay, S., Varghese, A., Chamuah, J.K. & Lalrinkima, H. (2013) Genetic characterization of Fasciola gigantica from different geographical regions of India by ribosomal DNA markers. Journal of Parasitic Diseases 39, 1–6.Google Scholar
Rokni, M.B., Mirhendi, H., Mizani, A., Mohebali, M., Sharbatkhori, M., Kia, E.B., Abdoli, H. & Izadi, S. (2010) Identification and differentiation of Fasciola hepatica and Fasciola gigantica using a simple PCR-restriction enzyme method. Experimental Parasitology 124, 209–213.Google Scholar
Shahzad, W., Mehmood, K., Munir, R., Aslam, W., Ijaz, M., Ahmad, M., Khan, S. & Sabir, A.J. (2012) Prevalence and molecular diagnosis of Fasciola hepatica in sheep and goats in different districts of Punjab. Pakistan. Pakistan Veterinary Journal 32, 535–538.Google Scholar
Spithill, T.W. & Dalton, J.P. (1998) Progress in development of liver fluke vaccines. Parasitology Today 14, 224–228.CrossRefGoogle ScholarPubMed
Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution 30, 2725–2729.CrossRefGoogle ScholarPubMed
Urquhart, G.M. & Armour, J. (1996) Veterinary parasitology. Oxford, Blackwell.Google Scholar
Velusamy, R., Singh, B.P., Ghosh, S., Chandra, D., Raina, O.K., Gupta, S.C. & Jayraw, A.K. (2006) Prepatent detection of Fasciola gigantica infection in bovine calves using metacercarial antigen. Indian Journal of Experimental Biology 44, 749–753.Google ScholarPubMed