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Equines as reservoirs of human fascioliasis: transmission capacity, epidemiology and pathogenicity in Fasciola hepatica-infected mules

Published online by Cambridge University Press:  10 September 2020

R. Mera y Sierra Open the ORCID record for R. Mera y Sierra [Opens in a new window] ,
G. Neira ,
M.D. Bargues Open the ORCID record for M.D. Bargues [Opens in a new window] ,
P.F. Cuervo Open the ORCID record for P.F. Cuervo [Opens in a new window] ,
P. Artigas Open the ORCID record for P. Artigas [Opens in a new window] ,
L. Logarzo ,
G. Cortiñas ,
D.E.J. Ibaceta ,
A. Lopez Garrido  and
E. Bisutti
...Show all authors
R. Mera y Sierra
Affiliation:
Centro de Investigación en Parasitología Regional, Universidad Juan Agustín Maza, Avenida de Acceso Este – Lateral Sur 2245, S. José, Guaymallén, Mendoza, Argentina
G. Neira
Affiliation:
Centro de Investigación en Parasitología Regional, Universidad Juan Agustín Maza, Avenida de Acceso Este – Lateral Sur 2245, S. José, Guaymallén, Mendoza, Argentina Consejo Nacional de Investigaciones Científicas y Técnicas, Avenida de Acceso Este – Lateral Sur 2245, S. José, Guaymallén, Mendoza, Argentina
M.D. Bargues*
Affiliation:
Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Avenida Vicente Andrés Estellés s/n, 46100Burjassot, Valencia, Spain
P.F. Cuervo
Affiliation:
Laboratorio de Ecología de Enfermedades, Instituto de Ciencias Veterinarias del Litoral (ICIVET Litoral), Universidad Nacional del Litoral – Consejo Nacional de Investigaciones Científicas y Técnicas, R.P. Kreder 2805, Esperanza, Santa Fe, Argentina
P. Artigas
Affiliation:
Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Avenida Vicente Andrés Estellés s/n, 46100Burjassot, Valencia, Spain
L. Logarzo
Affiliation:
Centro de Investigación en Parasitología Regional, Universidad Juan Agustín Maza, Avenida de Acceso Este – Lateral Sur 2245, S. José, Guaymallén, Mendoza, Argentina
G. Cortiñas
Affiliation:
Centro de Investigación en Parasitología Regional, Universidad Juan Agustín Maza, Avenida de Acceso Este – Lateral Sur 2245, S. José, Guaymallén, Mendoza, Argentina
D.E.J. Ibaceta
Affiliation:
Centro de Investigación en Parasitología Regional, Universidad Juan Agustín Maza, Avenida de Acceso Este – Lateral Sur 2245, S. José, Guaymallén, Mendoza, Argentina
A. Lopez Garrido
Affiliation:
Centro de Investigación en Parasitología Regional, Universidad Juan Agustín Maza, Avenida de Acceso Este – Lateral Sur 2245, S. José, Guaymallén, Mendoza, Argentina
E. Bisutti
Affiliation:
Centro de Investigación en Parasitología Regional, Universidad Juan Agustín Maza, Avenida de Acceso Este – Lateral Sur 2245, S. José, Guaymallén, Mendoza, Argentina
S. Mas-Coma
Affiliation:
Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Avenida Vicente Andrés Estellés s/n, 46100Burjassot, Valencia, Spain
*
Author for correspondence: M.D. Bargues, E-mail: [email protected]
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Abstract

Fascioliasis is a zoonotic disease caused by liver flukes transmitted by freshwater lymnaeid snails. Donkey and horse reservoir roles have been highlighted in human endemic areas. Liver fluke infection in mules has received very limited research. Their role in disease transmission, epidemiological importance and Fasciola hepatica pathogenicity are studied for the first time. Prevalence was 39.5% in 81 mules from Aconcagua, and 24.4% in 127 from Uspallata, in high-altitude areas of Mendoza province, Argentina. A mean amount of 101,242 eggs/mule/day is estimated. Lymnaeids from Uspallata proved to belong to ribosomal DNA internal transcribed spacer (ITS) markers ITS-1 and ITS-2 combined haplotype 3C of Galba truncatula. These lymnaeids were experimentally susceptible to infection by egg miracidia from mules. Infectivity, number of cercariae/snail and shedding period fit the enhanced F. hepatica/G. truncatula transmission pattern at very high altitude. This indicates that the mule is able to maintain the F. hepatica cycle independently. Individual burdens of 20 and 97 flukes were found. Mule infection susceptibility is intermediate between donkey and horse, although closer to the latter. Anatomo-pathology and histopathology indicate that massive infection may cause mule death. Haematological value decreases of red blood cells, haemoglobin, leucocytes and lymphocytes indicate anaemia and strong immunosuppression. Strongly increased biochemical marker values indicate liver function alterations. The mule probably played a role in the past exchanges with Chile and Bolivia through Mendoza province. Evidence suggests that mules could contribute to the spread of both F. hepatica and G. truncatula to human fascioliasis-endemic areas in these countries.

Keywords

Fasciola hepaticamulesequinesGalba truncatulaDNA sequencingdisease transmissionepidemiologypathogenicityArgentina
Type
Research Paper
Information
Journal of Helminthology , Volume 94 , 2020 , e189
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

Acici, M, Bolukbas, CS, Gurler, AT, Umur, S and Buyuktanir, O (2013) Seroprevalence of fasciolosis in equines of the Black Sea Region, Turkey. Journal of Equine Veterinary Science 33, 62–66.CrossRefGoogle Scholar
Afshan, K, Fortes-Lima, CA, Artigas, P, Valero, MA, Qayyum, M and 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.CrossRefGoogle ScholarPubMed
Alcaino, H and Aguilar, A (1985) Actividad antihelmíntica del Closantel y de la combinación febantbl + triclorfón en caballos fina sangre de carrera. Archivos de Medicina Veterinaria 17, 103–109.Google Scholar
Alcaino, H, Gorman, T, Guevara, G and Fernandez, JD (1983) Distomatosis y parásitos del intestino grueso de equino de la zona centro sur de Chile. Archivos de Medicina Veterinaria 15, 27–35.Google Scholar
Alcaino, H, Vega, F, Klein, P, Gorman, T and Apt, W (1988) Fascioliasis en caballos y conejos silvestres (Oryctolagus cuniculus) en la provincia de Curicó, Chile. Parasitología al Día 12, 136–140.Google Scholar
Alcaino, H, Gorman, T, Gonzalez, V, Vega, F and Apt, W (1990) Fascioliasis en caballos, cerdos y conejos silvestres en la provincia de Talca, VII Región, Chile. Parasitología al Día 14, 9–13.Google Scholar
Alcaino, H, Apt, W, Vega, F, Gorman, T and Apt, P (1992) Fasciolasis animal en la VII Región de Chile: áreas de distribución e infección en caballos y conejos silvestres. Parasitología al Día 16, 11–16.Google Scholar
Alcaino, H, Parra, L and Gorman, T (2005) Fasciolasis en equinos fina sangre de carrera de los hipódromos de la zona central de Chile 2002-2003. Parasitología Latinoamericana 60, 61–64.CrossRefGoogle Scholar
Alves, RM, van Rensburg, LJ and van Wyk, JA (1988) Fasciola in horses in the Republic of South Africa: a single natural case of Fasciola hepatica and the failure to infest ten horses either with F. hepatica or Fasciola gigantica. Onderstepoort Journal of Veterinary Research 55, 157–163.Google ScholarPubMed
Apt, W, Aguilera, X, Vega, F, et al. (1993) Prevalencia de fascioliasis en humanos, caballos, cerdos y conejos silvestres en tres provincias de Chile. Boletín de la Oficina Sanitaria Panamericana 115, 405–414.Google Scholar
Artigas, P, Bargues, MD, Mera y Sierra, R, Agramunt, VH and Mas-Coma, S (2011) Characterisation of fascioliasis lymnaeid intermediate hosts from Chile by DNA sequencing, with emphasis on Lymnaea viator and Galba truncatula. Acta Tropica 120, 245–257.CrossRefGoogle ScholarPubMed
Askari, Z, Mas-Coma, S, Bouwman, AS, Boenke, N, Stôllner, T, Aali, A, Rezaiian, M and Mowlavi, G (2018) Fasciola hepatica eggs in paleofaeces of the Persian onager Equus hemionus onager, a donkey from Chehrabad archaeological site, dating back to the Sassanid Empire (224-651 AD), in ancient Iran. Infection, Genetics and Evolution 62, 233–243.CrossRefGoogle Scholar
Awad, WS, Ibrahim, AK and Salib, FA (2009) Using indirect ELISA to assess different antigens for the serodiagnosis of Fasciola gigantica infection in cattle, sheep and donkeys. Research in Veterinary Science 86, 466–471.CrossRefGoogle ScholarPubMed
Badawy, A, Abouzaid, N and Merwad, A (2014) Occurrence of zoonotic fascioliasis in donkeys in Egypt with emphasis on PCR-RFLP of 28S rRNA gene. Revue de Médecine Vétérinaire 165, 167–171.Google Scholar
Bargues, MD and Mas-Coma, S (2005) Reviewing lymnaeid vectors of fascioliasis by ribosomal DNA sequence analyses. Journal of Helminthology 79, 257–267.CrossRefGoogle ScholarPubMed
Bargues, MD, Mangold, AJ, Muñoz-Antoli, C, Pointier, JP and Mas-Coma, S (1997) SSU rDNA characterization of lymnaeid snails transmitting human fascioliasis in South and Central America. Journal of Parasitology 83, 1086–1092.CrossRefGoogle ScholarPubMed
Bargues, MD, Horak, P, Patzner, RA, Pointier, JP, Jackiewicz, M, Meier-Brook, C and Mas-Coma, S (2003) Insights into the relationships of Palaearctic and Nearctic lymnaeids (Mollusca: Gastropoda) by rDNA ITS-2 sequencing and phylogeny of stagnicoline intermediate host species of Fasciola hepatica. Parasite 10, 243–255.CrossRefGoogle ScholarPubMed
Bargues, MD, Mera y Sierra, R, Gomez, HG, Artigas, P and Mas-Coma, S (2006) Ribosomal DNA ITS-1 sequencing of Galba truncatula (Gastropoda: Lymnaeidae) and its potential impact on fascioliasis transmission in Mendoza, Argentina. Animal Biodiversity and Conservation 29, 191–194.Google Scholar
Bargues, MD, Mera y Sierra, R, Gomez, HG, Artigas, P and Mas-Coma, S (2007a) Caracterización molecular de Galba truncatula, vector principal de la Fascioliasis, en Argentina. Implicaciones en salud pública. Enfermedades Emergentes, Barcelona 9, 77–82.Google Scholar
Bargues, MD, Artigas, P, Mera y Sierra, RL, Pointier, JP and Mas-Coma, S (2007b) Characterisation of Lymnaea cubensis, L. viatrix and L. neotropica n. sp., the main vectors of Fasciola hepatica in Latin America, by analysis of their ribosomal and mitochondrial DNA. Annals of Tropical Medicine and Parasitology 101, 621–641.CrossRefGoogle Scholar
Bargues, MD, Gonzalez, C, Artigas, P and Mas-Coma, S (2011a) A new baseline for fascioliasis in Venezuela: lymnaeid vectors ascertained by DNA sequencing and analysis of their relationships with human and animal infection. Parasites & Vectors 4, 200.CrossRefGoogle Scholar
Bargues, MD, Artigas, P, Khoubbane, M, Flores, R, Glöer, P, Rojas-Garcia, R, Ashrafi, K, Falkner, G and Mas-Coma, S (2011b) Lymnaea schirazensis, an overlooked snail distorting fascioliasis data: genotype, phenotype, ecology, worldwide spread, susceptibility, applicability. PLoS ONE 6, e24567.CrossRefGoogle Scholar
Bargues, MD, Artigas, P, Khoubbane, M, Ortiz, P, Naquira, C and Mas-Coma, S (2012) Molecular characterisation of Galba truncatula, Lymnaea neotropica and L. schirazensis from Cajamarca, Peru and their potential role in transmission of human and animal fascioliasis. Parasites & Vectors 5, 174.CrossRefGoogle ScholarPubMed
Bargues, MD, Malandrini, JB, Artigas, P, Soria, CC, Velazquez, JN, Carnevale, S, Mateo, L, Khoubbane, M and Mas-Coma, S (2016) Human fascioliasis endemic areas in Argentina: multigene characterisation of the lymnaeid vectors and climatic environmental assessment of the transmission pattern. Parasites & Vectors 9, 306.CrossRefGoogle ScholarPubMed
Bargues, MD, Gayo, V, Sanchis, J, Artigas, P, Khoubbane, M, Birriel, S and Mas-Coma, S (2017) DNA multigene characterization of Fasciola hepatica and Lymnaea neotropica and its fascioliasis transmission capacity in Uruguay, with historical correlation, human report review and infection risk analysis. PLoS Neglected Tropical Diseases 11, e0005352.CrossRefGoogle ScholarPubMed
Bargues, MD, Artigas, P, Angles, R, Osca, D, Duran, P, Buchon, P, Gonzales-Pomar, RK, Pinto-Mendieta, J and Mas-Coma, S (2020) Genetic uniformity, geographical spread and anthropogenic habitat modifications of lymnaeid vectors found in a One Health initiative in the highest human fascioliasis hyperendemic of the Bolivian Altiplano. Parasites & Vectors 13, 171.CrossRefGoogle Scholar
Belfaiza, M, Abrous, M, Rondelaud, D, Moncef, M and Dreyfuss, G (2004) The use of Tetraphyll as food for snails increases the intensity of cercarial shedding in Galba truncatula infected with Fasciola hepatica. Parasitology Research 94, 86–90.Google ScholarPubMed
Boissier, J, Moné, H, Mitta, G, Bargues, MD, Molyneux, D and Mas-Coma, S (2015) Schistosomiasis reaches Europe. Lancet Infectious Diseases 15, 757–758.CrossRefGoogle ScholarPubMed
Bucknell, DG, Gasser, RB and Beveridge, I (1995) The prevalence and epidemiology of gastrointestinal parasites in horses of Victoria, Australia. International Journal for Parasitology 25, 711–724.CrossRefGoogle ScholarPubMed
Cade, DW (1992) Landscape, system, and identity in the post-Conquest Andes. Annals of the Association of American Geographers 82, 460–477.CrossRefGoogle Scholar
ChartsBin (2015) Mules stock by country, ChartsBin.com. Available at /http://chartsbin.com/view/35644, (accessed 2 August 2020).Google Scholar
Chen, MG and Mott, KE (1990) Progress in assessment of morbidity due to Fasciola hepatica infection: a review of recent literature. Tropical Diseases Bulletin 87, R1–R38.Google Scholar
Chougar, L, Mas-Coma, S, Artigas, P, Harhoura, K, Aissi, M, Agramunt, VH and Bargues, MD (2020) Genetically “pure” Fasciola gigantica discovered in Argelia: DNA multimarker characterization, trans-Saharan introduction from a Sahel origin and spreading risk into northwestern Maghreb countries. Transboundary and Emerging Diseases. [published online ahead of print, 2020 Apr 18]. DOI:10.1111/tbed.13572.CrossRefGoogle Scholar
Collins, DR (1961) Fascioliasis in Mexican burro. Journal of the American Veterinary Medicine Association 139, 1321–1323.Google ScholarPubMed
Cox, DD and Todd, AC (1962) Survey of gastrointestinal parasitism in Wisconsin dairy cattle. Journal of the American Veterinary Medical Association 141, 706–709.Google ScholarPubMed
Cuervo, P, Sidoti, L, Fantozzi, MC, Neira, G, Gerbeno, L and Mera y Sierra, R (2013) Fasciola hepatica infection and association with gastrointestinal parasites in Creole goats from western Argentina. Revista Brasileira de Parasitologia Veterinaria 22, 53–57.CrossRefGoogle ScholarPubMed
Cuervo, P, Cataldo, SD, Fantozzi, MC, et al. (2015) Liver fluke (Fasciola hepatica) naturally infecting introduced European brown hare (Lepus europaeus) in northern Patagonia: phenotype, prevalence and potential risk. Acta Parasitologica 60, 536–543.CrossRefGoogle ScholarPubMed
Dorchies, P (2010) La fasciolose des équidés, une infestation parasitaire inhabituelle. Buletin des Groupements Techniques Vétérinaires 57, 71–78.Google Scholar
Encina, FA (1952) Historia de Chile desde la prehistoria hasta 1.891. 3rd edn. 694 pp. Santiago de Chile, Editorial Nascimento.Google Scholar
Esteban, JG, Gonzalez, C, Bargues, MD, Angles, R, Sanchez, C, Naquira, C and Mas-Coma, S (2002) High fascioliasis infection in children linked to a man-made irrigation zone in Peru. Tropical Medicine and International Health 7, 339–348.CrossRefGoogle ScholarPubMed
Everaert, GPJ, Jawhari, M and Gaufreteau, A (1974) De la presence de grandes douves Fasciola gigantica sur des foies d'asins du Maroc. Revue de Medecine Veterinaire 125, 541–544.Google Scholar
Farro, ME (2008) Redes y medios de transporte en el desarrollo de expediciones científicas en Argentina (1850-1910). História, Ciências, Saúde – Manguinhos 15, 679–696.CrossRefGoogle Scholar
Flynn, DO and Giraldez, A (2002) Cycles of silver: global economic unity through the mid-eighteenth century. Journal of World History 13, 391–427.CrossRefGoogle Scholar
Galli-Valerio, B (1893) Lésions déterminées par la Fasciola hepatica chez le cheval. Archivio per le Scienze Mediche 9, 173.Google Scholar
Gandhi, P, Schmitt, EK, Chen, CW, Samantray, S, Venishetty, VK and Hughes, D (2019) Triclabendazole in the treatment of human fascioliasis: a review. Transactions of the Royal Society of Tropical Medicine and Hygiene 113, 797–804.CrossRefGoogle ScholarPubMed
Giberti, H (1954) Historia económica de la ganadería Argentina. 217 pp. Buenos Aires, Editorial Raigal.Google Scholar
Girones, N, Valero, MA, Garcia-Bodelon, MA, Chico-Calero, MI, Punzon, C, Fresno, M and Mas-Coma, S (2007) Immune suppression in advanced chronic fascioliasis: an experimental study in a rat model. Journal of infectious Diseases 195, 1504–1512.CrossRefGoogle ScholarPubMed
Gonzalez-Miguel, J, Valero, MA, Reguera-Gomez, M, Mas-Bargues, C, Bargues, MD, Simon-Martin, F and Mas-Coma, S (2019) Numerous Fasciola plasminogen-binding proteins may underlie blood-brain barrier leakage and explain neurological disorder complexity and heterogeneity in the acute and chronic phases of human fascioliasis. Parasitology 146, 284–298.CrossRefGoogle ScholarPubMed
Gonzalez, LC, Esteban, JG, Bargues, MD, Valero, MA, Ortiz, P, Naquira, C and Mas-Coma, S (2011) Hyperendemic human fascioliasis in Andean valleys: an altitudinal transect analysis in children of Cajamarca province, Peru. Acta Tropica 120, 119–129.CrossRefGoogle ScholarPubMed
Graber, M (1969) Helminthes parasites de certains anirnaux demostiques et sauvages du Tchad. Bulletin of Epizootic Diseases of Africa 17, 403–428.Google Scholar
Greene, HM, Hurson, MJ and Wickler, SJ (2006) Haematological and respiratory gas changes in horses and mules exercised at altitude (3800 m). Equine Veterinary Journal, Equine Exercise Physical Supplement 36, 551–556.CrossRefGoogle Scholar
Grelck, H, Horchner, F and Wohrl, H (1977) Experimental infection of ponies with Fasciola hepatica. Berliner und Muenchner Tieraerztliche Wochenschrift 90, 371–373.Google Scholar
Guilhon, J and Graber, M (1963) Action du phloroglucinate de piperazine surquelques Helminthes des Equides. Revue d'Elevage et de Medecine Veterinaire des Pays Tropicaux 16, 305–308.CrossRefGoogle Scholar
Haridy, FM, Morsy, TA, Gawish, NI, Antonios, TN and Abdel Gawad, AG (2002) The potential reservoir role of donkeys and horses in zoonotic fascioliasis in Gharbia Governorate, Egypt. Journal of the Egyptian Society of Parasitology 32, 561–570.Google ScholarPubMed
Haridy, FM, Morsy, GH, Abdou, NE and Morsy, TA (2007) Zoonotic fascioliasis in donkeys: ELISA (Fges) and postmortem examination in the Zoo, Giza, Egypt. Journal of the Egyptian Society of Parasitology 37, 1101–1110.Google Scholar
Howell, AK, Malalana, F, Beesley, NJ, et al. (2020) Fasciola hepatica in UK horses. Equine Veterinary Journal 52, 194–199.CrossRefGoogle ScholarPubMed
Junin, B and Queirolo, M (2018) Los valores ocultos de Campo Los Andes. Available at http://www.unidiversidad.com.ar/los-valores-ocultos-de-campo-los-andes (accessed 22 February 2018).Google Scholar
Kim, BJ (2011) Trade and tribute along the Silk Road before the third century A.D. Journal of Central Eurasian Studies 2, 1–24.Google Scholar
Krajl, M, Srebocvan, V, Marzan, B, Turner, V and Wikerhauser, T (1960) Fasciolose aiguë chez les chevaux avec un aperçu particulier sur le diagnostic différentiel de l'anémie infectieuse du cheval. Veterinarski Arhiv Zagreb 30, 192–199.Google Scholar
Krawiecki, JM (1986) A propos d'un cas clinique de fasciolose hépatique chez un cheval de sport. Pratique Vétérinaire Equine 18, 173–176.Google Scholar
Lacoste, P (2008) El arriero y el transporte terrestre en el cono sur (Mendoza 1780-1800). Revista de Indias 68, 35–68.Google Scholar
Larkin, M, Blackshields, G, Brown, N, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948.CrossRefGoogle ScholarPubMed
Lumbreras, H, Cantella, R and 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, 167–174.Google Scholar
Malandrini, JB, Soria, CC, Carnevale, S, Velazquez, J and Pizarro, MC (2009) Estudio de la fascioliasis desde una perspectiva multidisciplinaria. In Colegio Medico Veterinario de la Provincia de Córdoba, XXVIII Jornadas de Actualización en Ciencias Veterinarias, Villa Giardino, Córdoba, 25–27 September 2009.Google Scholar
Malandrini, JB, Soria, CC, Foresi, I and Correa, S (2002) Fasciolosis en Catamarca. Primeros resultados. pp. 287–293 in , Universidad Nacional de Catamarca (Ed) La Investigación Científica en la Facultad de Ciencias de la Salud, en los Umbrales del Siglo XXI. Catamarca, Editorial Universitaria.Google Scholar
Martinez, PS (1961) Historia económica de Mendoza durante el Virreinato 1776-1810. 478 pp.Madrid, Universidad Nacional de Cuyo – Instituto Gonzalo Fernández de Oviedo.Google Scholar
Mas-Coma, S, Rodriguez, A, Bargues, MD, Valero, MA, Coello, JR and 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, 39–46.Google Scholar
Mas-Coma, S, Angles, R, Esteban, JG, Bargues, MD, Buchon, P, Franken, M and Strauss, W (1999) The Northern Bolivian Altiplano: a region highly endemic for human fascioliasis. Tropical Medicine and International Health 4, 454–467.CrossRefGoogle ScholarPubMed
Mas-Coma, S, Funatsu, IR and Bargues, MD (2001) Fasciola hepatica and lymnaeid snails occurring at very high altitude in South America. Parasitology 123, S115–S127.CrossRefGoogle ScholarPubMed
Mas-Coma, S, Valero, MA and Bargues, MD (2009a) Climate change effects on trematodiases, with emphasis on zoonotic fascioliasis and schistosomiasis. Veterinary Parasitology 163, 264–280.CrossRefGoogle Scholar
Mas-Coma, S, Valero, MA and Bargues, MD (2009b) 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.CrossRefGoogle Scholar
Mas-Coma, S, Bargues, MD and Valero, MA (2014a) Diagnosis of human fascioliasis by stool and blood techniques: Update for the present global scenario. Parasitology 141, 1918–1946.CrossRefGoogle Scholar
Mas-Coma, S, Agramunt, VH and Valero, MA (2014b) Neurological and ocular fascioliasis in humans. Advances in Parasitology 84, 27–149.CrossRefGoogle Scholar
Mas-Coma, S, Bargues, MD and Valero, MA (2018) Human fascioliasis infection sources, their diversity, incidence factors, analytical methods and prevention measures. Parasitology 145, 1665–1699.CrossRefGoogle ScholarPubMed
McGonigle, S and Dalton, JP (1995) Isolation of Fasciola hepatica haemoglobin. Parasitology 111, 209–215.CrossRefGoogle ScholarPubMed
McLean, AK and Wang, W (2013) Pilot study comparing hematologic and serum biochemical parameters in healthy horses (Equus caballus) and mules. Journal of Equine Veterinary Science 33, 352–354.CrossRefGoogle Scholar
McLean, AK, Wang, W, Navas Gonzalez, FJ and Rodriguez, JB (2016) Reference intervals for hematological and blood biochemistry reference values in healthy mules and hinnies. Comparative Clinical Pathology 25, 871–878.CrossRefGoogle Scholar
Mera y Sierra, RL, Artigas, P, Cuervo, P, Deis, E, Sidoti, L, Mas-Coma, S and Bargues, MD (2009) Fascioliasis transmission by Lymnaea neotropica confirmed by nuclear rDNA and mtDNA sequencing in Argentina. Veterinary Parasitology 166, 73–79.CrossRefGoogle ScholarPubMed
Mera y Sierra, R, Agramunt, VH, Cuervo, P and Mas-Coma, S (2011) Human fascioliasis in Argentina: retrospective overview, critical analysis and baseline for future research. Parasites & Vectors 4, 104.CrossRefGoogle ScholarPubMed
Mitchell, P (2018) The donkey in human history. An archaelogical perspective. 306 pp. Oxford, Oxford University Press.Google Scholar
Moisant, C, Jolivet, J and Pitre, J (1972) La fasciolose des équidés. Observations en Normandie. Essais de traitement avec le rafoxanide. Recueil de Médécine Vétérinaire de l'Ecole d'Alfort 148, 444–450.Google Scholar
Montes, GA, Zurita, L and Uhart, R (1984) Medición de aspartato amino transferasa, gamma glutamil transpeptidasa, proteína total y albúmina sérica en fasciolasis equina. Zentralblatt fuer Veterinaermedizin 34B, 338–342.Google Scholar
Muñoz, L, Rubilar, L, Zamora, D, Sepulveda, O, Rehhof, C and Ortiz, R (2008) Fasciolosis en equinos fina sangre de carrera del Club Hípico Concepción, Chile. Parasitología Latinoamericana 63, 88–91.CrossRefGoogle Scholar
Nansen, P, Andersen, S and Hesselholt, M (1975) Experimental infection of the horse with Fasciola hepatica. Experimental Parasitology 37, 15–19.CrossRefGoogle ScholarPubMed
Neira, G, Godoy, D, Logarzo, L and Mera y Sierra, R (2019) Helmintos digestivos en caballos de la provincia de Mendoza, Argentina. Revista Jornadas de Investigación 11, 44.Google Scholar
Olaechea, FV (2007) Tremátodes y Céstodes: Fasciola hepatica. pp. 159–168in Suárez, VH, Olaechea, FV, Rossanigo, CE and Romero, JR (Eds) Enfermedades parasitarias de los ovinos y otros rumiantes menores en el cono sur de América. Buenos Aires, Instituto Nacional de Tecnología Agropecuaria – INTA.Google Scholar
Owen, JM (1977) Liver fluke infection in horses and ponies. Equine Veterinary Journal 9, 29–31.CrossRefGoogle ScholarPubMed
Palmer, DG, Lyon, J, Palmer, MA and Forshaw, D (2014) Evaluation of a copro-antigen ELISA to detect Fasciola hepatica infection in sheep, cattle and horses. Australian Veterinary Journal 92, 357–361.CrossRefGoogle ScholarPubMed
Pandey, VS (1983) Observations on Fasciola hepatica in donkeys from Morocco. Annals of Tropical Medicine and Parasitology 77, 159–162.CrossRefGoogle ScholarPubMed
Quigley, A, Sekiya, M, Egan, S, Wolfe, A, Negredo, C and Mulcahy, G (2017) Prevalence of liver fluke infection in Irish horses and assessment of a serological test for diagnosis of equine fasciolosis. Equine Veterinary Journal 49, 183–188.CrossRefGoogle ScholarPubMed
Roberts, FHS and O'Sullivan, PJ (1950) Methods for egg counts and larval cultures for strongyles infesting the gastro-intestinal tract of cattle. Australian Journal of Agricultural Research 1, 99–102.CrossRefGoogle Scholar
Rondelaud, D, Abrous, M and Dreyfuss, G (2002) The influence of different food sources on cercarial production in Lymnaea truncatula experimentally infected with Digenea. Veterinary Research 33, 95–100.CrossRefGoogle ScholarPubMed
Rondelaud, D, Dreyfuss, G and Vignoles, P (2006) Clinical and biological abnormalities in patients after fasciolosis treatment. Médecine et Maladies Infectieuses 36, 466–468.CrossRefGoogle ScholarPubMed
Sanchis Polto, J, Madeira de Carvalho, LM, Bonilla, R, Duque de Araujo, AM, Arroyo, F, Suarez, J, Solari, MA, Romero, JA and Sanchez Andrade, R (2014) Horse handling conditions and emergence of Neglected Infections: Fasciolosis. pp. 127–145in Paz-Silva, A, Arias Vázquez, M and Sánchez-Andrade Fernandez, R (Eds) Horses: breeding, health disorders and effects on performance and behavior. New York, Nova Publishers.Google Scholar
SENASA (2016) Distribución de Existencias Equinas por Categoría - Marzo 2016. Available at https://datos.agroindustria.gob.ar/dataset/existencias-equinas (accessed 31 January 2019).Google Scholar
Serrera, RM (1992) Tráfico terrestre y red vial en las Indias Españolas. 336 pp. Barcelona, Editorial Lunwerg.Google Scholar
Soulé, C, Boulard, C, Levieux, D, Barnouin, J and Plateau, E (1989) Fasciolose équine expérimentale: évolution des paramètres sérologiques, enzymatiques et parasitaires. Annales des Recherches Vétérinaires 20, 295–307.Google Scholar
Tamura, K, Stecher, G, Peterson, D, Filipski, A and Kumar, S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.CrossRefGoogle ScholarPubMed
USDA-NRCS (2000) Agricultural waste management field handbook. Washington, DC, United States Department of Agriculture.Google Scholar
Valero, MA, Darce, NA, Panova, M and 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.CrossRefGoogle Scholar
Valero, MA, Panova, M and Mas-Coma, S (2001b) Developmental differences in the uterus of Fasciola hepatica between livestock liver fluke populations from Bolivian highland and European lowlands. Parasitology Research 87, 337–342.CrossRefGoogle Scholar
Valero, MA, Santana, M, Morales, M, Hernandez, JL and 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.CrossRefGoogle ScholarPubMed
Valero, MA, Panova, M and Mas-Coma, S (2005) Phenotypic analysis of adults and eggs of Fasciola hepatica by computer image analysis system. Journal of Helminthology 79, 217–225.CrossRefGoogle ScholarPubMed
Valero, MA, Navarro, M, Garcia-Bodelon, MA, Marcilla, A, Morales, M, Garcia, JE, Hernandez, JL and Mas-Coma, S (2006) High risk of bacterobilia in advanced experimental chronic fasciolosis. Acta Tropica 100, 17–23.CrossRefGoogle ScholarPubMed
Valero, MA, Girones, N, Garcia-Bodelon, MA, Periago, MV, Chico-Calero, I, Khoubbane, M, Fresno, M and Mas-Coma, S (2008) Anaemia in advanced chronic fasciolosis. Acta Tropica 108, 35–43.CrossRefGoogle ScholarPubMed
Valero, MA, Perez-Crespo, I, Chillon-Marinas, C, Khoubbane, M, Quesada, C, Reguera-Gomez, M, Mas-Coma, S, Fresno, M and Girones, N (2017) Fasciola hepatica reinfection potentiates a mixed Th1/Th2/Th17/Treg response and correlates with the clinical phenotypes of anemia. PLoS ONE 12, e0173456.CrossRefGoogle ScholarPubMed
Valero, MA, Bargues, MD, Khoubbane, M, et al. (2016) Higher physiopathogenicity by Fasciola gigantica than by the genetically close F. hepatica: experimental long-term follow-up of biochemical markers. Transactions of the Royal Society of Tropical Medicine and Hygiene 110, 55–66.CrossRefGoogle Scholar
Villavicencio, AF, Bargues, MD, Artigas, A, Guaman, R, Ulloa, SM, Romero, J, Osca, D and Mas-Coma, S (2019) Lymnaeid snail vectors of fascioliasis, including the first finding of Lymnaea neotropica in Ecuador, assessed by ribosomal DNA sequencing in the southern zone close to the Peru border. Acta Parasitologica 64, 839–849.CrossRefGoogle ScholarPubMed
Williams, DJL and Hodgkinson, JE (2017) Fasciolosis in horses: a neglected, re-emerging disease. Equine Veterinary Education 29, 202–204.CrossRefGoogle Scholar
Zumaquero-Rios, JL, Sarracent-Perez, J, Rojas-Garcia, R, Rojas-Rivero, L, Martinez-Tovilla, Y, Valero, MA and Mas-Coma, S (2013) Fascioliasis and intestinal parasitoses affecting schoolchildren in Atlixco, Puebla State, Mexico: epidemiology and treatment with nitazoxanide. PLoS Neglected Tropical Diseases 7, e2553.CrossRefGoogle ScholarPubMed