Epidemiological and genetic characterization of larval stages of Fasciola gigantica in snail intermediate hosts in Karnataka State, India
-
Rangappa Rajanna
, Susan Jacob Siju
Abstract
Fasciolosis in ruminants in India is caused by the liver fluke Fasciola gigantica. Radix (Lymnaea) spp. are known to carry the infective stages of this parasite. Understanding the seasonal prevalence of F. gigantica infection in the intermediate host is of extreme importance in order to elucidate the transmission dynamics of the parasite. So the present study was designed to determine the bioclimatic distribution of larval stages of F. gigantica in Radix spp. snails as well as to explore the genetic diversity of F. gigantica in three geographical regions (Deccan plateau, Western Ghats and coastal region) of Karnataka. The lymnaeid snails were sampled (n = 2077) for a period of one year (June 2015 to May 2016) at 24 sites. The snails were morphologically identified and the infection status was established through cercarial shedding and nested polymerase chain reaction (PCR) based technique targeting second internal transcribed spacers (ITS-2) of nuclear ribosomal DNA. The sensitivity of PCR (8.2%) for detection of F. gigantica infection within snail is significantly higher than cercarial shedding (4.3%) with an overall prevalence of 5.1%. The prevalence of infection was higher in winter than in the rainy and summer seasons (6.2% instead of 4.6% and 4.3% respectively). Deccan plateau (5.8%) showed a higher prevalence of infection compared to Western Ghats (5.2%) and Coastal region (3.6%). The sequencing ITS-2 region permitted the identification of the parasite as F. gigantica which is having high implication in studying the population genetic structure of the parasite in the country. In conclusion, overall results indicated that Radix spp. snails harboured F. gigantica developmental stages throughout the year and nested PCR was found to be sensitive and specific for detection of F. gigantica infection in snails compared to routine parasitological techniques.
Conflict of Interest: The authors of this study declare that they have no conflict of interest.
Acknowledgements
The authors are thankful to the Director of the ICAR-National Institute of Veterinary Epidemiology and Disease Informatics for providing facilities for completion of this study.
References
Amor N., Farjallah S., Salem M., Lamine D.M., Paolo M., Said K., et al. 2011. Molecular characterization of Fasciola gigantica from Mauritania based on mitochondrial and nuclear ribosomal DNA sequences. Experimental Parasitology, 30, 1–10. 10.1016/j.exppara.2011.07.002Search in Google Scholar
Bardhan D., Kumar R.R., Nigam C.S., Mishra H., Bhoj S. 2014. Estimation of milk losses due to fasciolosis in Uttarakhand. Agricultural Economics Research Review, 27, 281–288. 10.5958/0974-0279.2014.00031.7Search in Google Scholar
Bargues M.D., Mas-Coma S. 1997. Phylogenetic analysis of lymnaeid snails based on 18S rDNA sequences. Molecular Biology and Evolution, 14, 569–577. 10.1093/oxfordjournals.molbev.a025794Search in Google Scholar
Bargues M.D., Artigas P., Khoubbane M., Ortiz P., Naquira C., MasComa S. 2012. Molecular characterization of Galba truncatula, Lymnaea neotropica and L. schirazensis from Cajamarca, Peru and their potential role in transmission of human and animal fascioliasis. Parasites and Vectors, 5, 174. 10.1186/1756-3305-5-174Search in Google Scholar
Bauri R. 2015. Epidemiological studies on some important trematodes of domestic ruminants in snail intermediate hosts in Uttar Pradesh. Thesis submitted to the Deemed University, Indian Veterinary Research Institute, Izatnagar – 243 122 (U.P.), IndiaSearch in Google Scholar
Charlier J., Duchateau L., Claerebout E., Williams D., Vercruysse J. 2007. Associations between anti-Fasciola hepatica antibody levels in bulk-tank milk samples and production parameters in dairy herds. Preventive Veterinary Medicine, 78, 57–6610.1016/j.prevetmed.2006.09.010Search in Google Scholar
Dung B.T., Doanh P.N., The D.T., Loan H.T., Losson B., Caron Y. 2013. Morphological and molecular characterization of lymnaeid snails and their potential role in the transmission of Fasciola spp. in Vietnam. Korean Journal of Parasitology, 51, 657–662. 10.3347/kjp.2013.51.6.657Search in Google Scholar
Gloer P. 2002. Uberfamilie Lymnaeoidea Rafinesque 1815. Familie Lymnaeid ae Lamarck 1812. In: Glöer P. (ed.) Die Süβwasser-gastropoden Nord-und Mitteleuropas. Bestimmungschlüssel, Lebensweise, Verbreitung. Die TierweltDeutschlands 73. Conchbooks, Hackenheim, pp. 200–232. (In German)Search in Google Scholar
Hillis D.M., Dixon M.T. 1991. Ribosomal DNA: Molecular evolution and phylogenetic inference. The Quarterly Review of Biology, 66, 411–453. 10.1086/417338Search in Google Scholar
Hope Cawdery M.J., Strickland K.L., Conway A., Crow P.J. 1977. Production effects of liver fluke in cattle. The effects of infection on live weight gain, food intake and food conversion efficiency in beef cattle. British Veterinary Journal, 133, 145–5910.1016/S0007-1935(17)34136-2Search in Google Scholar
Islam Z., Alam M.Z., Akter S., Roy B.C., Mondal M.M.H. 2012. Distribution patterns of vector snails and trematode cercaria in their vectors in some selected areas of Mymensingh. Journal of Environmental Science and Natural Resources, 5, 37–46. 10.3329/jesnr.v5i2.14599Search in Google Scholar
Jouet D., Ferte H., Depaquit J., Rudolfova J., Latour P., Zanella D., et al. 2008. Trichobilharzia spp. in natural conditions in Annecy Lake, France. Parasitology Research, 103, 51–58. 10.1007/s00436-008-0926-3Search in Google Scholar PubMed
Lyholt H.C.K., Buchmann K. 1996. Diplostomum spathaceum: effects of temperature and light on cercarial shedding and infection of rainbow trout. Diseases of Aquatic Organisms, 25, 169–173. 10.3354/dao025169Search in Google Scholar
Malek A.E., Cheng T.C. (Ed.). 1974. Medical and Economic Malacology. Academic Press, London, pp. 1–398Search in Google Scholar
Mehra U.R., Verma A.K., Dass R.S., Sharma R.L., Yadav S.C. 1999. Effects of Fasciola gigantica infection on growth and nutrient utilization of buffalo calves. Veterinary Research, 145: 699–702Search in Google Scholar
Nilsson C., Ericsson U., Medin M., Sundberg I. 1998. Freshwater snails in south Sweden – compared with 1940 – century-Environmental Protection Agency, Report 4903Search in Google Scholar
Oakley G.A., Owen B., Knapp N.H.H. 1979. Production effects of subclinical liver fluke infection in growing dairy heifers. Veterinary Record, 104: 503–50710.1136/vr.104.22.503Search in Google Scholar
Raina O.K., Jacob S.S., Sankar M., Bhattacharya D., Bandyopadhyay S., Varghese A., et al. 2015. Genetic characterization of Fasciola gigantica from different geographical regions of India by ribosomal DNA markers. Journal of Parasitic Diseases, 39, 27–32. 10.1007/s12639-013-0276-7Search in Google Scholar
Rao N.V.S. (Ed.). 1989. Hand book of fresh water molluscs of India. Zoological Survey of India, Calcutta, India, pp. 1–289Search in Google Scholar
Remigio E.A. 2002. Molecular phylogenetic relationships in the aquatic snail genus Lymnaea, the intermediate host of the causative agent of fascioliasis: insights from broader taxon sampling. Parasitology Research, 88, 687–696. 10.1007/s00436-002-0658-8Search in Google Scholar
Rondelaud D., Titi A., Vignoles P., Mekroud A., Dreyfuss G. 2013. Consequence of temperature changes on cercarial shedding from Galba truncatula infected with Fasciola hepatica or Paramphistomum daubneyi. Parasite, 20, 1–7. 10.1051/parasite/2013009Search in Google Scholar
Ross J.G. 1970. The economics of Fasciola hepatica infections in cattle. British Veterinary Journal, 126, 13–1510.1016/S0007-1935(17)48559-9Search in Google Scholar
Schweizer G., Braun U., Deplazes P., Torgerson P.R. 2005. Estimating the financial losses due to bovine fasciolosis in Switzerland. Veterinary Record, 157,188–193. 10.1136/vr.157.7.188Search in Google Scholar PubMed
Sierra R.M.Y., Artigas P., Cuervo P., Deis E., Sidoti L., Mas Coma S., et al. 2009. Fascioliasis transmission by Lymnaea neotropica confirmed by nuclear rDNA and mtDNA sequencing in Argentina. Veterinary Parasitology, 166, 73–79. 10.1016/j.vetpar.2009.08.001Search in Google Scholar PubMed
Snedecor G.W, Cochran W.G (Sixth Ed.). 1968. Statistical Methods Iowa State University Press, Ames10.1097/00010694-196809000-00018Search in Google Scholar
Spithill T.W., Smooker P.M., Copeman D.B. 1999. Fasciola gigantica: epidemiology, control, immunology and molecular Biology. In: Dalton J.P. (Ed.) Fasciolosis. CABI Publishing; Oxon, UK, 465–525Search in Google Scholar
Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729.10.1093/molbev/mst197Search in Google Scholar PubMed PubMed Central
Vassilev G.D., Jooste R.L. 1991. Production losses and control of fasciolosis in cattle in Zimbabwe. Zimbabwe Veterinary Journal, 22, 45–56Search in Google Scholar
Yadav C.L., Vatsya S., Garg R., Kumar R.R., Banerjee P.S., Rajesh G. 2007. Seasonal prevalence of Fasciola gigantica infection in sheep and goats in western Uttar Pradesh. Journal of Parasitic Diseases, 31, 141–144Search in Google Scholar
Yakhchali M., Viayeh R.M., Imani-Baran A. 2014. PCR-RFLP analysis of 28S rDNA for specification of Fasciola gigantica (Cobbold, 1855) in the infected Lymnaea auricularia (Linnaeus, 1785) snails from northwestern Iran. Iranian Journal of Parasitology, 9, 358–364Search in Google Scholar
Yakhchali M., Viayeh R.M., Imani Baran A.2015. Molecular detection of the infection with Fasciola hepatica in field-collected snails of Galba truncatula and Lymnaea stagnalis from West Azarbaijan. Iran Archives of Razi Institute, 70, 195–202. 10.7508/ARI.2015.03.008Search in Google Scholar
© 2018 W. Stefański Institute of Parasitology, PAS
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