Startseite Liver fluke (Fasciola hepatica) naturally infecting introduced European brown hare (Lepus europaeus) in northern Patagonia: phenotype, prevalence and potential risk
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Liver fluke (Fasciola hepatica) naturally infecting introduced European brown hare (Lepus europaeus) in northern Patagonia: phenotype, prevalence and potential risk

  • Pablo F. Cuervo EMAIL logo , Sophia Di Cataldo , M. Cecilia Fantozzi , Erika Deis , Gabriela Diaz Isenrath , Gabriela Viberti , Patricio Artigas , Raquel Peixoto , M. Adela Valero , Roberto Mera y Sierra und Santiago Mas-Coma
Veröffentlicht/Copyright: 16. Juni 2015
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Abstract

Fascioliasis has recently been included in the WHO list of Neglected Zoonotic Diseases. Besides being a major veterinary health problem, fascioliasis has large underdeveloping effects on the human communities affected. Though scarcely considered in fascioliasis epidemiology, it is well recognized that both native and introduced wildlife species may play a significant role as reservoirs of the disease. The objectives are to study the morphological characteristics of Fasciola hepatica adults and eggs in a population of Lepus europaeus, to assess liver fluke prevalence, and to analyze the potential reservoir role of the European brown hare in northern Patagonia, Argentina, where fascioliasis is endemic. Measures of F. hepatica found in L. europaeus from northern Patagonia demonstrate that the liver fluke is able to fully develop in wild hares and to shed normal eggs through their faeces. Egg shedding to the environment is close to the lower limit obtained for pigs, a domestic animal whose epidemiological importance in endemic areas has already been highlighted. The former, combined with the high prevalence found (14.28%), suggest an even more important role in the transmission cycle than previously considered. The results obtained do not only remark the extraordinary plasticity and adaptability of this trematode species to different host species, but also highlight the role of the European brown hare, and other NIS, as reservoirs capable for parasite spillback to domestic and native cycle, representing a potentially important, but hitherto neglected, cause of disease emergence.

References

Abrous M., Comes A.M., Gasnier N., Rondelaud D., Dreyfuss G., Chauvin A., Ménard A., Agoulon A., Cabaret, J. 1998. Morphological variability in Fasciola hepatica eggs in ruminants, rodents and lagomorphs. Journal of Helminthology 72, 313-317. DOI: 10.1017/S0022149X0001666710.1017/S0022149X00016667Suche in Google Scholar PubMed

Afshan K., Fortes-Lima C.A., Artigas P., Valero M.A., 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. DOI: 2489301010.4081/gh.2014.22Suche in Google Scholar PubMed

Arru E., Deiana S., Nuvole A. 1967. Distomatosi epatica nei leporidi selvatici in Sardegna. Atti della Societa Italiana delle Scienze Veterinaria 21, 762-766Suche in Google Scholar

Bargues M.D., Mas-Coma S. 2005. Reviewing lymnaeid vectors of fascioliasis by ribosomal DNA sequence analyses. Journal of Helminthology 79, 257-267. DOI: 10.1079/JOH200529710.1079/JOH2005297Suche in Google Scholar

Bengis R.G., Leighton F.A., Fischer J.R., Artois M., Mörner T., Tate C. M. 2004. The role of wildlife in emerging and re-emerging zoonoses. Revue Scientifique et Technique - Office International des Epizooties 23, 497-51110.20506/rst.23.2.1498Suche in Google Scholar

Bonino N., Cossios D., Meneghetti J. 2010. Dispersal of the European hare, Lepus europaeus in South America. Folia Zoologica 59, 9-1510.25225/fozo.v59.i1.a3.2010Suche in Google Scholar

Daszak P., Cunningham A.A., Hyatt A.D. 2000. Emerging infectious diseases of wildlife - Threats to biodiversity and human health. Science 287, 443-449. DOI: 10.1126/science.287. 5452.443Suche in Google Scholar

Egerton J.R., Ostlind D.A., Blair L.S., Eary C.H., Suhayda D., Cifelli S., Riek R.F., Campbell W.C. 1979. Avermectins, new family of potent anthelmintic agents: efficacy of the B1a component. Antimicrobial Agents and Chemotherapy 15, 372-37810.1128/AAC.15.3.372Suche in Google Scholar PubMed PubMed Central

Fuentes M.V., Valero M.A., Bargues M.D., Esteban J.G., Angles R., Mas-Coma S. 1999. Analysis of climatic data and forecast indices for human fascioliasis at very high altitude. Annals of Tropical Medicine and Parasitology 93, 835-85010.1080/00034983.1999.11813491Suche in Google Scholar

Fuentes M.V., Malone J.B., Mas-Coma S. 2001. Validation of a mapping and predicting model for human fasciolosis transmission in Andean very high altitude endemic areas using remote sensing data. Acta Tropica 79, 87-95. DOI: 10.1016/S0001-706X (01)00106-1Suche in Google Scholar

Gayo V., Cuervo P., Rosadilla D., Birriel S., Dell’Oca L., Trelles A., Cuore U., Mera y Sierra R. 2011. Natural Fasciola hepatica infection in "Nutria" (Myocastor coypus), in Uruguay. Journal of Zoo and Wildlife Medicine 42, 354-356. DOI: 10. 1638/2010-0226.110.1638/2010-0226.1Suche in Google Scholar PubMed

Kaplan R.M. 2001. Fasciola hepatica: a review of the economic impact in cattle and considerations for control. Veterinary Therapeutics 2, 40-50Suche in Google Scholar

Kelly D.W., Paterson R.A., Townsend C.R., Poulin R., Tompkins D.M. 2009. Parasite spillback: a neglected concept in invasion ecology? Ecology 90, 2047-2056. DOI: 10.1890/08-1085.110.1890/08-1085.1Suche in Google Scholar PubMed

Kleinman F., González N., Rubel D., Wisnivesky C. 2004. Fasciola hepatica (Linnaeus, 1758) (Trematoda, Digenea) en liebres europeas (Lepus europaeus, Pallas 1778) (Lagomorpha, Leporidae) en la región Cordillerana Patagónica, Chubut, Argentina. Parasitología Latinoamericana 59, 68-71. DOI: 10.4067/S0717-7712200400010001410.4067/S0717-77122004000100014Suche in Google Scholar

Kruse H., Kirkemo A., Handeland K. 2004. Wildlife as source of zoonotic infections. Emerging Infectious Diseases 10, 2067-2072. DOI: 10.3201/eid1012.040707.10.3201/eid1012.040707Suche in Google Scholar

Kutzer E., Frey H. 1976. Die Parasiten der Feldhasen (Lepus europaeus) in Österreich. (Parasites of the European brown hare in Austria). Berliner und Münchener Tierärztliche Wochenschrift 89, 480-483Suche in Google Scholar

Lumbreras H., Cantella R., Burga R. 1962. Acerca de un procedimiento de sedimentación rápida para investigar huevos de Fasciola hepatica en las heces, su evaluación y uso en el campo. Revista Médica Peruana 31, 167-174Suche in Google Scholar

MacPherson D.W., McQueen R. 1993. Cryptosporidiosis: multiattribute evaluation of six diagnostic methods. Journal of Clinical Microbiology 31, 198-20210.1128/jcm.31.2.198-202.1993Suche in Google Scholar

Mas-Coma S., Fons R., Feliu C., Bargues M.D., Valero M.A., Galan- Puchades M.T. 1988. Small mammals as natural definitive hosts of the liver fluke, Fasciola hepatica Linnaeus, 1758 (Trematoda: Fasciolidae): a review and two new records of epidemiologic interest on the island of Corsica. Rivista di Parasitologia 5, 73-78Suche in Google Scholar

Mas-Coma S., Rodriguez A., Bargues M.D., Valero M.A., Coello J.R., Angles R. 1997. Secondary reservoir role of domestic animals other than sheep and cattle in fascioliasis transmission in the Northern Bolivian Altiplano. Research and Reviews in Parasitology 57, 39-46Suche in Google Scholar

Mas-Coma S., Bargues M.D., Valero M.A., Fuentes M.V. 2003. Adaptation capacities of Fasciola hepatica and their relationships with human fascioliasis: from below sea level up to the very high altitude. In: (Eds. C. Combes and J. Jourdane) Taxonomy, Ecology and Evolution of Metazoan Parasites, Perpignan, France, Presses Universitaires de Perpignan, 81-123Suche in 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. DOI:10.1016/j.ijpara.2005. 07.010Suche in Google Scholar

Mas-Coma S., Valero MA., Bargues MD. 2008. Effects of climate change on animal and zoonotic helminthiases. Revue Scientifique et Technique - Office International des Epizooties 27, 443-45710.20506/rst.27.2.1822Suche in 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. DOI: 10.1016/S0065-308X(09)69002-310.1016/S0065-308X(09)69002-3Suche in Google Scholar

Mas-Coma S., Agramunt V.H., Valero M.A. 2014a. Neurological and ocular fascioliasis in humans. Advances in Parasitology 84, 27-149. DOI: 10.1016/B978-0-12-800099-1.00002-810.1016/B978-0-12-800099-1.00002-8Suche in Google Scholar PubMed

Mas-Coma S., Bargues M.D., Valero M.A. 2014b. Diagnosis of human fascioliasis by stool and blood techniques: Update for the present global scenario. Parasitology, 141 (Special Issue), 1918-1946. DOI: 10.1017/S003118201400086910.1017/S0031182014000869Suche in Google Scholar PubMed

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. DOI: 10.1186/1756-3305-4-10410.1186/1756-3305-4-104Suche in Google Scholar PubMed PubMed Central

Mezo M., González-Warleta M., Castro-Hermida J.A., Manga-González M.Y., Peixoto R., Mas-Coma S., Valero M.A. 2013. The wild boar (Sus scrofa Linnaeus, 1758) as secondary reservoir of Fasciola hepatica in Galicia (NW Spain). Veterinary Parasitology 198, 274-283. DOI: 10.1016/j.vetpar.2013.09.00910.1016/j.vetpar.2013.09.009Suche in Google Scholar PubMed

Morrone J.J. 2006. Biogeographic areas and transition zones of Latin America and the Caribbean islands based on pangeographic and cladistic analyses of the entomofauna. Annual Review of Entomology 51, 467-494. DOI: 10.1146/annurev.ento.50.07 1803.130447Suche in Google Scholar

Nickel S., Gottwald A. 1979. Parasites of the GDR. 3. Endoparasites of the hare (Lepus europeus). Angewandte Parasitologie, 20, 57-62Suche in Google Scholar

Novaro A.J., Capurro A.F., Travaini A., Funes M.C., Rabinovich J.E. 1992. Pellet-count sampling based on spatial distribution: a case study of the European hare in Patagonia. Ecología Austral 2, 11-18Suche in Google Scholar

Olaechea F. V. 2007. Tremátodes y Céstodes: Fasciola hepatica. In: (Eds. V. H. Suárez, F. V. Olaechea, C. E. Rossanigo, and J. R. Romero), Enfermedades parasitarias de los ovinos y otros rumiantes menores en el cono sur de América, Buenos Aires, Argentina, Instituto Nacional de Tecnología Agropecuaria - INTA-, 159-168Suche in Google Scholar

Periago M.V., Valero M.A., Panova M., Mas-Coma S. 2006. Phenotypic comparison of allopatric populations of Fasciola hepatica and Fasciola gigantica from European and African bovines using a computer image analysis system (CIAS). Parasitology Research 99, 368-378. DOI: 10.1007/s00436-006-0174-310.1007/s00436-006-0174-3Suche in Google Scholar PubMed

Polley L. 2005. Navigating parasite webs and parasite flow: Emerging and re-emerging parasitic zoonoses of wildlife origin. International Journal for Parasitology 35, 1279-1294. DOI: 10.1016/j.ijpara.2005.07.00310.1016/j.ijpara.2005.07.003Suche in Google Scholar PubMed

Poulin R. 1997. Egg production in adult trematodes: adaptation or constraint. Parasitology 11, 195-204. DOI: 10.1017/S00 31182096008372Suche in Google Scholar

Poulin R., Paterson R.A., Townsend C.R., Tompkins D.M., Kelly D.W. 2011. Biological invasions and the dynamics of endemic diseases in freshwater ecosystems. Freshwater Biology 56, 676-688. DOI: 10.1111/j.1365-2427.2010.02425.x 10.1111/j.1365-2427.2010.02425.xSuche in Google Scholar

Rachowicz L.J., Hero J.M., Alford R.A., Taylor J.W., Morgan J.A.T., Vredenburg V.T., Collins J.P., Briggs C.J. 2005. The novel and endemic pathogen hypotheses: competing explanations for the origin of emerging infectious diseases of wildlife. Conservation Biology 19, 1441-1448. DOI: 10.1111/j.1523-1739. 2005.00255.x Suche in Google Scholar

Shimalov V.V. 2001. Helminth fauna of the hare (Lepus europaeus Pallas, 1778) in the southern part of Belarus. Parasitology Research 87, 85. DOI: 10.1007/s00436000025910.1007/s004360000259Suche in Google Scholar

Sidoti L., Mera y Sierra R.L., Cuervo P., Micó M., Bargues M.D., Mas-Coma S., Artigas P. 2009. Sheep and goat fascioliasis in the Mendoza province, Argentina. Acta Parasitologica Portuguesa 16, 112-113Suche in Google Scholar

Thieltges D.W., Reise K., Prinz K., Jensen K.T. 2009. Invaders interfere with native parasite-host interactions. Biological Invasions 11, 1421-1429. DOI: 10.1007/s10530-008-9350-y 10.1007/s10530-008-9350-ySuche in Google Scholar

Tompkins D.M., Poulin R. 2006. Parasites and biological invasions. In: (Eds. R. B. Allen, and W. G. Lee), Biological Invasions in New Zealand, Heidelberg, Berlin, Germany, Springer, 67-8610.1007/3-540-30023-6_5Suche in Google Scholar

Tropilo J. 1964. Intensity and extensity of invasion by Cysticercus pisiformis and Fasciola hepatica in hares (in Polish). Medycyna Weterynaryjna Warszawa 20, 259-269Suche in Google Scholar

Valero M.A., Mas-Coma S. 2000. Comparative infectivity of Fasciola hepatica metacercariae from isolates of the main and secondary reservoir animal host species in the Bolivian Altiplano high human endemic region. Folia Parasitologica 47, 17-2210.14411/fp.2000.004Suche in Google Scholar

Valero M.A., Marcos M.D., Fons R., Mas-Coma S. 1998. Fasciola hepatica development in the experimentally infected black rat Rattus rattus. Parasitology Research 84, 188-194. DOI: 10.1007/s00436005038110.1007/s004360050381Suche in Google Scholar

Valero M.A., Darce N.A., Panova M., Mas-Coma S. 2001a. Relationships between host species and morphometric patterns in Fasciola hepatica adults and eggs from the northern Bolivian Altiplano hyperendemic region. Veterinary Parasitology 102, 85-100. DOI: 10.1016/S0304-4017(01)00499-X10.1016/S0304-4017(01)00499-XSuche in Google Scholar

Valero M.A., Panova M., Mas-Coma S. 2001b. Developmental differences in the uterus of Fasciola hepatica between livestock liver fluke populations from Bolivian Highlands and European lowlands. Parasitology Research 87, 337-342. DOI: 10.1007/PL0000858810.1007/PL00008588Suche in Google Scholar

Valero M.A., Panova M., Comes A.M., Fons R., Mas-Coma S. 2002. Patterns in size and shedding of Fasciola hepatica eggs by naturally and experimentally infected murid rodents. Journal of Parasitology 88, 308-313. DOI: 10.1645/0022-3395(2002) 088[0308:PISASO]2.0.CO;2Suche in Google Scholar

Valero M. A., Santana M., Morales M., Hernandez J. L., Mas-Coma S. 2003. Risk of gallstone disease in advanced chronic phase of fascioliasis: an experimental study in a rat model. Journal of Infectious Diseases 188, 787-793. DOI: 10.1086/37728110.1086/377281Suche in Google Scholar PubMed

Valero M. A., Panova M., Mas-Coma S. 2005. Phenotypic analysis of adults and eggs of Fasciola hepatica by computer image analysis system. Journal of Helminthology 79, 217-225. DOI: 10.1079/JOH200530110.1079/JOH2005301Suche in Google Scholar PubMed

Valero M.A., Navarro M., Garcia-Bodelon M.A., Marcilla A., Morales M., Garcia J.E., Hernandez J. L., Mas-Coma S. 2006a. High risk of bacterobilia in advanced experimental chronic fasciolosis. Acta Tropica 100, 17-23. DOI: 10.1016/j.actatropica. 2006.09.002Suche in Google Scholar

Valero M. A., De Renzi M., Panova M., García-Bodelon M. A., Periago M. V., Ordoñez D., Mas-Coma S. 2006b. Crowding effect on adult growth, pre-patent period and egg sheding of Fasciola hepatica. Parasitology 133, 453-463. DOI: 10.1017/S003118200600059X Valero M.A., Girones N., Garcia-Bodelon M.A., Periago M.V., Chico-Calero I., Khoubbane M., Fresno M., Mas-Coma S. 2008. Anaemia in advanced chronic fasciolosis. Acta Tropica 108, 35-43. DOI: 10.1016/j.actatropica.2008.08.007.10.1016/j.actatropica.2008.08.007Suche in Google Scholar PubMed

Valero M.A., Perez-Crespo I., Periago M.V., Khoubbane M., Mas- Coma S. 2009. Fluke eggs characteristics for the diagnosis of human and animal fascioliasis by Fasciola hepatica and Fasciola gigantica. Acta Tropica 111, 150-159. DOI: 10.1016/ j.actatropica.2009.04.00510.1016/j.actatropica.2009.04.005Suche in Google Scholar PubMed

Valero M.A., Panova M., Pérez-Crespo I., Khoubbane M., Mas- Coma S. 2011. Correlation between egg-shedding and uterus development in Fasciola hepatica human and animal isolates: applied implications. Veterinary Parasitology 183, 79-86. DOI: 10.1016/j.vetpar.2011.07.00310.1016/j.vetpar.2011.07.003Suche in Google Scholar PubMed

Valero M.A., Perez-Crespo I., Khoubbane M., Artigas P., Panova M., Ortiz P., Maco V., Espinoza J. R., Mas-Coma S. 2012. Fasciola hepatica phenotypic characterization in Andean human endemic areas: valley versus altiplanic patterns analysed in liver flukes from sheep from Cajamarca and Mantaro, Peru. Infection, Genetics and Evolution 12, 403-410. DOI: 10.1016/j.meegid.2012.01.009 10.1016/j.meegid.2012.01.009Suche in Google Scholar PubMed

Walker S.M., Johnston C., Hoey E.M., Fairweather I., Borgsteede F.H.M., Gaasenbeek C.P.H., Prodohl P.A., Trudgett A. 2011. Potential role of hares in the spread of liver fluke in the Netherlands. Veterinary Parasitology 177, 179-181. DOI: 10.1016/j.vetpar.2010.11.04310.1016/j.vetpar.2010.11.043Suche in Google Scholar PubMed

Ziege S., Brauneis M., von Keyserlingk M., Wohlsein P. 2009. Fasziolose beim Europäischen Feldhasen (Lepus europaeus) in Nordwestdeutschland. Deutsche Tierarztliche Wochenschrifte 116, 60-63Suche in Google Scholar

Received: 2014-12-13
Revised: 2015-2-24
Accepted: 2015-4-17
Published Online: 2015-6-16
Published in Print: 2015-9-1

© W. Stefański Institute of Parasitology, PAS

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