Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-17T21:41:05.228Z Has data issue: false hasContentIssue false

Epidemiology of fascioliasis in human endemic areas

Published online by Cambridge University Press:  13 July 2018

S. Mas-Coma*
Affiliation:
Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Av. Vicent Andrés Estellés s/n, 46100 Burjassot, Valencia, Spain
*
*Fax: 00 34 96 3544769 E-mail: S.Mas.Coma@uv.es

Abstract

Considered a secondary zoonotic disease until the mid-1990s, human fascioliasis is at present emerging or re-emerging in many countries, including increases of prevalence and intensity and geographical expansion. Research in recent years has justified the inclusion of fascioliasis in the list of important human parasitic diseases. At present, fascioliasis is a vector-borne disease presenting the widest known latitudinal, longitudinal and altitudinal distribution. Fasciola hepatica has succeeded in expanding from its European original geographical area to colonize five continents, despite theoretical restrictions related to its biology and in turn dependent upon environmental and human activities. Among the different epidemiological situations, human hypo- to hyperendemic areas, including epidemics, are noteworthy. A global analysis of the distribution of human cases shows that the expected correlation between animal and human fascioliasis only appears at a basic level. Areas presenting very high human prevalences and intensities, especially in children and females, have been recently described. In hypo- to hyperendemic areas of Central and South America, Europe, Africa and Asia, human fascioliasis presents a range of epidemiological characteristics related to a wide diversity of environments. Thus far well-known epidemiological patterns of fascioliasis may not always explain the transmission characteristics in any given area and control measures should consider the results of ecoepidemiological studies undertaken in the zones concerned.

Type
Review Article
Copyright
Cambridge University Press 2015

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.)

References

Abreu, F., Aidos, A., Rebelo, I., Lacerda, C. & Palminha, J.M. (1996) Intérêt du bithionol dans le traitement de la distomatose hépatique de l'enfant. Archives de Pediatrie 3, 189191.CrossRefGoogle Scholar
Anon (1988) Parasitic diseases: hepatic distomiasis caused by Fasciola hepatica . Weekly Epidemiological Record (WHO) 63, 109111.Google Scholar
Ashrafi, K., Massoud, J., Holakuei, K., Mahmoodi, M., Jo-Afshani, M.A., Valero, M.A., Fuentes, M.V., Khoubbane, M., Artigas, P., Bargues, M.D. & Mas-Coma, S. (2004) Evidence suggesting that Fasciola gigantica might be the most prevalent causal agent of fascioliasis in northern Iran. Iranian Journal of Public Health 33, 3137.Google Scholar
Aspöck, H., Auer, H. & Picher, O. (1999) Parasites and parasitic diseases in prehistoric human populations in Central Europe. Helminthologia 36, 139145.Google Scholar
Assmar, M., Milaninia, A., Amir-Khani, A., Yadegari, D., Forghan-Parast, K., Nahravanian, H., Piazak, N., Esmayli, A., Hovanesian, A. & Valadkhani, Z. (1991) Seroepidemiological investigation of fascioliasis in northern Iran. Medical Journal of the Islamic Republic of Iran 5, 2327.Google Scholar
Bargues, M.D., Vigo, M., Horak, P., Dvorak, J., Patzner, R.A., Pointier, J.P., Jackiewicz, M., Meier-Brook, C. & Mas-Coma, S. (2001) European Lymnaeidae (Mollusca: Gastropoda), intermediate hosts of trematodiases, based on nuclear ribosomal DNA ITS-2 sequences. Infection, Genetics and Evolution 1, 85107.CrossRefGoogle ScholarPubMed
Bendezu, P. (1969) Liver fluke in humans. Veterinary Record 85, 532533.CrossRefGoogle ScholarPubMed
Bjorland, J., Bryan, R.T., Strauss, W., Hillyer, G.V. & McAuley, J.B. (1995) An outbreak of acute fascioliasis among Aymara Indians in the Bolivian Altiplano. Clinical Infectious Diseases 21, 12281233.CrossRefGoogle ScholarPubMed
Bouchet, F. (1997) Helminth eggs: trace elements of neolithic and paleolithic parasitosis on French sites. Comptes Rendus de la Société de Biologie et de ses Filiales 191, 529536.Google ScholarPubMed
Bouix-Busson, D. & Rondelaud, D. (1985) Etude de l'aptitude à l'infestation fasciolienne chez Lymnaea glabra Müller et chez L. truncatula dans des peuplements mono- et bispécifiques. Bulletin de la Société Française de Parasitologie 33, 9598.Google Scholar
Bouix-Busson, D. & Rondelaud, D. (1986) L'infestation de Lymnaea glabra Müller par Fasciola hepatica L. Etude expérimentale sur le terrain. Annales de Parasitologie Humaine et Comparée 61, 215225.CrossRefGoogle Scholar
Claxton, J.R., Zambrano, H., Ortiz, P., Amoros, C., Delgado, E., Escurra, E. & Clarkson, M.J. (1997) The epidemiology of fasciolosis in the inter-Andean valley of Cajamarca, Peru. Parasitology International 46, 281288.CrossRefGoogle Scholar
Coudert, J. & Triozon, F. (1958) Recherche sur l'épidémiologie de la distomatose humaine à Fasciola hepatica. A propos d'une épidémie récente de 500 cas. Revue d'Hygiène et de Médicine Sociale 6, 840864.Google Scholar
Curtale, F., Hammoud, E.S., El Wakeel, A., Mas-Coma, S. & Savioli, L. (2000) Human fascioliasis, an emerging public health problem in the Nile Delta, Egypt. Research and Reviews in Parasitology 60, 129134.Google Scholar
Curtale, F., Hassanein, Y.A.E.W., El Wakeel, A., Mas-Coma, S. & Montresor, A. (2003a) Distribution of human fascioliasis by age and gender among rural population in the Nile Delta, Egypt. Journal of Tropical Pediatrics 49, 264268.CrossRefGoogle ScholarPubMed
Curtale, F., Mas-Coma, S., Hassanein, Y.A.E.W., Barduagni, P., Pezzotti, P. & Savioli, L. (2003b) Clinical signs and household characteristics associated with human fascioliasis among rural population in Egypt: a case-control study. Parassitologia 45, 511.Google ScholarPubMed
Chen, M.G. & Mott, K.E. (1990) Progress in assessment of morbidity due to Fasciola hepatica infection: a review of recent literature. Tropical Diseases Bulletin 87, R1R38.Google Scholar
Danis, M., Nozais, J.P. & Chandenier, J. (1985) La distomatose à Fasciola hepatica . II: La fasciolose humaine en France. Acta Veterinaria 907, VIIVIII.Google Scholar
Diaz, J., Pina, B., Lastre, M., Rivera, L. & Perez, O. (1990) Fascioliasis humana epidémica. Cuba 1983. VI. Estudio clínico de 40 niños del Hospital Provincial de Sagua La Grande. GEN 44, 385388.Google ScholarPubMed
Dittmar, K. & Teegen, W.R. (2003) The presence of Fasciola hepatica (liver-fluke) in humans and cattle from a 4,500 year old archaeological site in the Saale-Unstrut Valley, Germany. Memorias do Institituto Oswaldo Cruz 98, (Suppl. 1), 141143.CrossRefGoogle ScholarPubMed
Dreyfuss, G., Moukrim, A., Rondelaud, D. & Vareille-Morel, C. (1994) Field observations concerning infection of Lymnaea palustris by Fasciola hepatica. Journal of Helminthology 68, 115118.CrossRefGoogle ScholarPubMed
Esteban, J.G., Flores, A., Aguirre, C., Strauss, W., Angles, R. & Mas-Coma, S. (1997a) Presence of very high prevalence and intensity of infection with Fasciola hepatica among Aymara children from the Northern Bolivian Altiplano. Acta Tropica 66, 114.CrossRefGoogle ScholarPubMed
Esteban, J.G., Flores, A., Angles, R., Strauss, W., Aguirre, C. & Mas-Coma, S. (1997b) A population-based coprological study of human fascioliasis in a hyperendemic area of the Bolivian Altiplano. Tropical Medicine and International Health 2, 695699.CrossRefGoogle Scholar
Esteban, J.G., Bargues, M.D. & Mas-Coma, S. (1998) Geographical distribution, diagnosis and treatment of human fascioliasis: a review. Research and Reviews in Parasitology 58, 1342.Google Scholar
Esteban, J.G., Flores, A., Angles, R. & Mas-Coma, S. (1999) High endemicity of human fascioliasis between Lake Titicaca and La Paz valley, Bolivia. Transactions of the Royal Society of Tropical Medicine and Hygiene 93, 151156.CrossRefGoogle Scholar
Esteban, J.G., Gonzalez, C., Bargues, M.D., Angles, R., Sanchez, C., Naquira, C. & Mas-Coma, S. (2002) High fascioliasis infection in children linked to a man-made irrigation zone in Peru. Tropical Medicine and International Health 7, 339348.CrossRefGoogle ScholarPubMed
Esteban, J.G., Gonzalez, C., Curtale, F., Muñoz-Antoli, C., Valero, M.A., Bargues, M.D., El Sayed, M., El Wakeel, A., Abdel-Wahab, Y., Montresor, A., Engels, D., Savioli, L. & Mas-Coma, S. (2003) Hyperendemic fascioliasis associated with schistosomiasis in villages in the Nile Delta of Egypt. American Journal of Tropical Medicine and Hygiene 69, 429437.CrossRefGoogle ScholarPubMed
Fernandez Calienes, A., Fraga, J., Pointier, J.P., Yong, M., Sanchez, J., Coustau, C., Gutierrez, A. & Theron, A. (2004) Detection and genetic distance of resistant populations of Pseudosuccinea columella (Mollusca: Lymnaeidae) to Fasciola hepatica (Trematoda: Digenea) using RAPD markers. Acta Tropica 92, 8387.CrossRefGoogle Scholar
Forghan-Parast, K. (1993) Clinicoepidemiological study of human fascioliasis in Gilan. Journal of the Medical College, Gilan University of Medical Sciences 2, 6364.Google Scholar
Gaillet, P., Liance, M., Rivollet, D. & Houin, R. (1983) Situation de la fasciolose humaine en France, enquête retrospective portant sur les 30 dernières années. Bulletin de la Société Francaise de Parasitologie 1, 7982.Google Scholar
Gasnier, N., Rondelaud, D., Abrous, M., Carreras, F., Boulard, C., Diez-Baños, P. & Cabaret, J. (2000) Allopatric combination of Fasciola hepatica and Lymnaea truncatula is more efficient than sympatric ones. International Journal for Parasitology 30, 573578.CrossRefGoogle ScholarPubMed
Giap, L.H. (1987) Distomatose hépatique à Fasciola hepatica . Laboratoire de Parasitologie, Université de Bordeaux II, 74 pp.Google Scholar
Gil-Benito, A., Ciolkovitch, A., Mas-Coma, S. & Quilici, M. (1991) Enquête sur la distomatose à Fasciola hepatica en Corse. Méditerranée Médicale, Marseille 403, 2125.Google Scholar
Gitard, R., Coquilhat, P., Silicany, V., Blanc, B. & Nicoli, R.M. (1965) La distomatose humaine à Fasciola hepatica Linnaeus, 1758 en Corse. Bulletin de la Société de Pathologie Exotique 3, 471474.Google Scholar
Gonzalez, J.F., Perez, O., Rodriguez, G., Arus, E. & Lastre, M. (1985) Fasciolasis humana epidémica, Cuba 1983. VI Estudio Clínico de 44 adultos de Hospital General de Fomento. GEN 39, 276281.Google ScholarPubMed
Gonzalez, J.F., Perez, R., Perez, O., Gonzalez de la Torre, R., Lastre, M., Brito, E. & Diaz, J. (1987) Fasciolasis humana epidémica, Cuba 1983. II. Estudio epidemiológico. GEN 41, 5357.Google Scholar
Gutierrez, A., Pointier, J.P., Yong, M., Sanchez, J. & Theron, A. (2003a) Evidence of phenotypic differences between resistant and susceptible isolates of Pseudosuccinea columella (Gastropoda: Lymnaeidae) to Fasciola hepatica (Trematoda: Digenea) in Cuba. Parasitology Research 90, 129134.CrossRefGoogle Scholar
Gutierrez, A., Pointier, J.P., Fraga, J., Jobet, E., Modat, S., Perez, R.T., Yong, M., Sanchez, J., Loker, E.S. & Theron, A. (2003b) Fasciola hepatica: identification of molecular markers for resistant and susceptible Pseudosuccinea columella snail hosts. Experimental Parasitology 105, 211218.CrossRefGoogle ScholarPubMed
Hillyer, G.V., Soler de Galanes, M., Rodriguez-Perez, J., Bjorland, J., Silva de Lagrava, M., Ramirez Guzman, S. & Bryan, R.T. (1992) Use of the Falcon Assay Screening Test–Enzyme-Linked Immunosorbent Assay (FAST–ELISA) and the Enzyme-Linked Immunoelectrotransfer Blot (EITB) to determine the prevalence of human fascioliasis in the Bolivian Altiplano. American Journal of Tropical Medicine and Hygiene 46, 603609.CrossRefGoogle ScholarPubMed
Hopkins, D.R. (1992) Homing in on helminths. American Journal of Tropical Medicine and Hygiene 46, 626634.CrossRefGoogle Scholar
Knobloch, J. (1985) Human fascioliasis in Cajamarca/Perú. II. Humoral antibody response and antigenaemia. Tropical Medicine and Parasitology 36, 9193.Google ScholarPubMed
Knobloch, J., Delgado, A.E., Alvarez, G.A., Reymann, U. & Bialek, R. (1985) Human fascioliasis in Cajamarca/Perú. I. Diagnostic methods and treatement with praziquantel. Tropical Medicine and Parasitology 36, 8890.Google Scholar
Laborde, M. (1985) Contribution a l'étude de la distomatose à Fasciola hepatica dans le Sud-Ouest de la France. Thèse Doctorat d'Etat en Médecine, Université de Bordeaux II. Thèse No. 487, Bordeaux, France.Google Scholar
Marcos Raymundo, L.A., Maco Flores, V., Terashima, A., Samalvides, F., Miranda, E., Tantalean, M., Espinoza, J.R. & Gotuzzo, E. (2004) Hiperendemicidad de Fasciolosis humana en el Valle del Mantaro, Perú: factores de riesgo de la infeccion por Fasciola hepatica . Revista de Gastroenterología de Peru 24, 158164.Google Scholar
Mas-Coma, S. (2004) Human fascioliasis. pp.305322 in Cotruvo, J.A., Dufour, A., Rees, G., Bartram, J., Carr, R., Cliver, D.O., Craun, G.F., Fayer, R. & Gannon, V.P.J. (Eds) Waterborne zoonoses: identification, causes and control . World Health Organization (WHO) London, IWA Publishing.Google Scholar
Mas-Coma, S. & Bargues, M.D. (1997) Human liver flukes: a review. Research and Reviews in Parasitology 57, 145218.Google Scholar
Mas-Coma, S., Angles, R., Strauss, W., Esteban, J.G., Oviedo, J.A. & Buchon, P. (1995) Human fasciolasis in Bolivia: a general analysis and a critical review of existing data. Research and Reviews in Parasitology 55, 7393.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, 3946.Google Scholar
Mas-Coma, S., Esteban, J.G. & Bargues, M.D. (1999a) Epidemiology of human fascioliasis: a review and proposed new classification. Bulletin of the World Health Organization 77, 340346.Google ScholarPubMed
Mas-Coma, S., Bargues, M.D. & Esteban, J.G. (1999b) Human fasciolosis pp. 411434 in Dalton, J.P. (ED.) Fasciolosis . Wallingford, Oxon CAB International.Google Scholar
Mas-Coma, S., Angles, R., Esteban, J.G., Bargues, M.D., Buchon, P., Franken, M. & Strauss, W. (1999c) The Northern Bolivian Altiplano: a region highly endemic for human fascioliasis. Tropical Medicine and International Health 4, 454467.CrossRefGoogle ScholarPubMed
Mas-Coma, S., Funatsu, I.R. & Bargues, M.D. (2001) Fasciola hepatica and lymnaeid snails occurring at very high altitude in South America. Parasitology 123, S115S127.CrossRefGoogle ScholarPubMed
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. pp.81123 Combes, C. & Jourdane, J. (EDs) Taxonomy, ecology and evolution of metazoan parasites . Vol. 2, Perpignan, Presses Universitaires de Perpignan.Google Scholar
Massoud, J. (1990) Fascioliasis outbreak of man and drug test (Triclabendazol) in Caspian littoral, northern part of Iran, 1989. Bulletin de la Société Française de Parasitologie 8, (Suppl. 1), 438.Google Scholar
Massoud, J. (1993) Present status of human fascioliasis in Iran. p. 19 in Food-borne trematodes . World Health Organization Manual, Manila, Mimeogr. Rep. Sch/SG/93 wGoogle Scholar
Menard, A., Agoulon, A., L'Hostis, M., Rondelaud, D., Collard, S. & Chauvin, A. (2001) Myocastor coypus as a reservoir host of Fasciola hepatica in France. Veterinary Research 32, 499508.CrossRefGoogle ScholarPubMed
Mendonça, M.M, de, Barata, M.C., Rombert, P.C. & Martins, A.M.F. (1996) As primeiras serologias positivas da fasciolose humana em S. Miguel (Açores). Garcia de Orta, Série de Zoologia 21, 161164.Google Scholar
Millan, J.C., Mull, R., Freise, S. & Richter, J. (2000) The efficacy and tolerability of triclabendazole in Cuban patients with latent and chronic Fasciola hepatica infection. American Journal of Tropical Medicine and Hygiene 63, 264269.CrossRefGoogle ScholarPubMed
Mitterpak, J. (1968) Zu den Besonderheiten der Epizootologie von Fasziolose in den tropischen Bedingungen von Kuba. Wiadomósci Parazytologiczne 14, 503507.Google Scholar
Moghaddam, A.S., Massoud, J., Mahmoodi, M., Mahvi, A.H., Periago, M.V., Artigas, P., Fuentes, M.V., Bargues, M.D. & Mas-Coma, S. (2004a) Human and animal fascioliasis in Mazandaran province, northern Iran. Parasitology Research 94, 6169.CrossRefGoogle ScholarPubMed
Moghaddam, A.S., Massoud, J., Mahmoodi, M., Khoubbane, M., Artigas, P., Periago, M.V., Fuentes, M.V., Bargues, M.D. & Mas-Coma, S. (2004b) Distributional outline of lymnaeid snails (Gastropoda) in the fascioliasis endemic area of Mazandaran, Iran. Acta Parasitologica 49, 145152.Google Scholar
O'Neill, S.M., Parkinson, M., Strauss, W., Angles, R. & Dalton, J.P. (1998) Inmunodiagnosis of Fasciola hepatica (fascioliasis) in a human population in the Bolivian Altiplano using purified cathepsin L cysteine proteinase. American Journal of Tropical Medicine and Hygiene 58, 417423.CrossRefGoogle Scholar
Oviedo, J.A., Mas-Coma, S., Dominici, J.L. & Roche, B. (1992) Distribution and ecology of Lymnaea truncatula (Müller, 1774) (Gastropoda: Basommatophora: Lymnaeidae), intermediate host of fasciolosis, in the island of Corsica (France). p. 218 in VIth European Multicolloquium of Parasitology (EMOP VI), The Hague (7–11 September 1992), AbstractsGoogle Scholar
Perez, A., Celestino, M., Millan, J.C. & Finlay, C.M. (1997) Brote de Fasciola hepatica en humanos: estudio epidemiológico. pp. 122123 in XIII Congreso Latino Americano de Parasitoloía (FLAP), La Habana, Cuba, Libro de Resúmenes.Google Scholar
Pourtaghva, M., Shafi, A., Saberi, A., Bahar, K. & Solymanlou, F. (1990) Fasciolase en Iran. Bulletin de la Société Française de Parasitologie 8, (Suppl. 1), 404.Google Scholar
Price, E.W. (1953) The fluke situation in American ruminants. Journal of Parasitology 39, 119.CrossRefGoogle ScholarPubMed
Rim, H.J., Farag, H.F., Sornmani, S. & Cross, J.H. (1994) Food-borne trematodes: ignored or emerging?. Parasitology Today 10, 207209.CrossRefGoogle Scholar
Ripert, C., Tribouley, J., Luong Dinh Giap, G., Combe, A. & Laborde, M. (1987) Epidémiologie de la fasciolose humaine dans le sud ouest de la France. Bulletin de la Société Française de Parasitologie 5, 227230.Google Scholar
Rombert, P.C. & Gracio, M.A. (1984) Fasciolíase hepática humana: sua distribuição em Portugal. O Médico 110, 7783.Google Scholar
Sabokbar, R.D. (1960) Geographical distribution of Fasciola hepatica and its relation with human distomatosis. Journal of the School of Medicine of the Tehran University 17, 251260.Google Scholar
Sahba, G.H., Arfaa, F., Farahmandian, I. & Jalali, H. (1972) Animal fascioliasis in Khuzestan, southwestern Iran. Journal of Parasitology 58, 712716.CrossRefGoogle ScholarPubMed
Sampaio Silva, M.L., Correia da Costa, J.M., Viana da Costa, A.M., Pires, M.A., Lopes, S.A., Castro, A.M. & Monjour, L. (1996) Antigenic components of excretory–secretory products of adult Fasciola hepatica recognized in human infections. American Journal of Tropical Medicine and Hygiene 54, 146148.CrossRefGoogle ScholarPubMed
Sohrabi, A.K. (1969) Human cases of distomatosis along the Caspian Sea. Paper presented in the 3rd Veterinary Congress, Tehran (in Persian)Google Scholar
Sorribes, J., Pascual, F.J., Aubary, M.J., Gil-Benito, A. & Mas-Coma, S. (1989) La Fascioliasis en España: revisión de la casuística humana en las dos últimas décadas. p. 259 in VI Congreso Nacional y I Congreso Ibérico de Parasitología , Cáceres, Spain, Resúmenes de Comunicaciones.Google Scholar
Sorribes, J., Aubary, M.J., Bargues, M.D. & Mas-Coma, S. (1990) Revisión de los casos humanos de Fascioliasis en España entre los años 1970 y 1989. p. 186 in Congreso de Zoonosis. 1° Interautonómico. Reunión de la International Zoonoses Association (IZA) , Valencia, Spain, Resúmenes.Google Scholar
Stork, M.G., Venables, G.S., Jennings, S.M.F., Beesley, J.R., Bendezu, P. & Capron, A. (1973) An investigation of endemic fasciolasis in Peruvian village children. Journal of Tropical Medicine and Hygiene 76, 231235.Google Scholar
Talaie, H., Emami, H., Yadegarinia, D., Nava-Ocampo, A.A., Massoud, J., Azmoudeh, M. & Mas-Coma, S. (2004) Randomized trial of a single, double and triple dose of 10 mg/kg of a human formulation of triclabendazole in patients with fascioliasis. Clinical and Experimental Pharmacology and Physiology 31, 777782.CrossRefGoogle ScholarPubMed
Turrientes, M.C., Saenz de Sta. Maria, A., Ceballos, E., Diaz, M., Barreno, M., Muro, A., Pardo, J. & Lopez-Velez, R. (2004) Fasciolosis importada y autóctona. p. 188 in Mas-Coma, S. (Coord.) IV Congreso de la Sociedad Española de Medicina Tropical y Salud Internacional (SEMTSI 4), Valencia (18–22 July 2004), Abstracts, Enfermedades Emergentes 6 (3), No. 119Google 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, 1722.CrossRefGoogle ScholarPubMed
Valero, M.A., Marcos, M.D., Fons, R. & Mas-Coma, S. (1998) Fasciola hepatica development in experimentally infected black rat, Rattus rattus . Parasitology Research 84, 188194.CrossRefGoogle ScholarPubMed
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, 85100.CrossRefGoogle ScholarPubMed
Valero, M.A., Panova, M. & 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, 337342.CrossRefGoogle ScholarPubMed
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, 308313.CrossRefGoogle ScholarPubMed
World Health Organization (1995) Control of foodborne trematode infections. WHO Technical Report Series No. 849, 1157.Google Scholar
Yadegari, D. & Talaie, H. (1996) Six years follow-up of triclabendazole in human fascioliasis. p. 167 in 7th Iranian Congress of Internal Medicine , Shahid Beheshti, University of Medical Sciences (16–19 May 1996), Abstracts.Google Scholar
Yadegari, D., Forghan-Parast, K. & Assmar, M. (1990) Investigation of an epidemic of fascioliasis in North Iran. Bulletin de la Société Française de Parasitologie 8, (Suppl. 2) 868.Google Scholar
Yadegari, D., Talaie, H. & Massoud, J. (1999) Clinical trial of triclabendazole on human fascioliasis: long term follow up. Medical Journal of the Islamic Republic of Iran 13, 8991.Google Scholar