Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-11-24T22:02:26.743Z Has data issue: false hasContentIssue false

Field and experimental studies on Dicrocoelium dendriticum and dicrocoeliasis in northern Spain

Published online by Cambridge University Press:  12 April 2024

M.Y. Manga-González*
Affiliation:
Departamento de Sistemas de Producción y Sanidad Animal, Estación Agrícola Experimental, Consejo Superior de Investigaciones Científicas, Apartado 788, 24080, León, Spain
C. González-Lanza
Affiliation:
Departamento de Sistemas de Producción y Sanidad Animal, Estación Agrícola Experimental, Consejo Superior de Investigaciones Científicas, Apartado 788, 24080, León, Spain
*
*Fax: +34 987 317161, E-mail: [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

The transmission, control and the relationship between Dicrocoelium dendriticum and its definitive (sheep and cattle) and intermediate (molluscs and ants) hosts under natural and experimental conditions are described. Eleven species of molluscs and four of ants were found infected with larval D. dendriticum in León province, north-west Spain. Infected ants were observed between April and November and in tetania at 7.5–26.9°C. The highest shedding of eggs by sheep and cattle was detected in winter. Two treatments applied in November and January were the most effective. In experimentally infected molluscs, the parasite was not visible under the stereomicroscope, at least until 50 days post-infection (p.i.). The prepatent period in experimentally infected lambs was 49–79 days p.i. The number of eggs per gram increased with the days p.i. and the parasite burden. The aspartate aminotransferase, alanine aminotransferase, gamma-glutamyl transpeptidase, leukocyte and neutrophil values of infected lambs increased, but those of lymphocytes decreased. Using the enzyme-linked immunosorbert assay technique, the IgG antibody response to excretory–secretory and somatic antigens of D. dendriticum was positive from day 30 p.i., although the maximum antibody levels were observed on day 60 p.i. The number of worms per lamb ranged between 30 and 2063. Cholangitis and cholangiectasia of the septal bile and hepatic ducts were observed. The best enzymatic systems for adult and larval D. dendriticum characterization were lactate dehydrogenase, glucose phosphate isomerase and phosphoglucomutase. Genetic variability of adult D. dendriticum was high using the random amplified polymorphic DNA technique.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2005

References

Alunda, J.M. & Rojo-Vázquez, F.A. (1982) Susceptibility of some populations of Cernuella (Xeromagna) cespitum arigonis (Schmidt, 1875) (Gastropoda, Helicidae) from the Douro basin (Iberian Peninsula) to the infection by Dicrocoelium dendriticum (Trematoda). Malacologia 22, 3943.Google Scholar
Alunda, J.M. & Rojo-Vázquez, F.A. (1983a) Survival and infectivity of Dicrocoelium dendriticum eggs under field conditions in NW Spain. Veterinary Parasitology 13, 245249.CrossRefGoogle ScholarPubMed
Alunda, J.M. & Rojo-Vázquez, F.A. (1983b) Effect of infection rate and host age on the intramolluscan development of Dicrocoelium dendriticum. Helminthologia 20, 251258.Google Scholar
Aacute;lvarez-Nogal, R., Manga-González, M.Y., González-Lanza, C. & Del-Pozo, P. (1992) Preliminary study on Dicrocoelium dendriticum (Trematoda) first larval stages in experimentally infected. Cernuella (Xeromagna) cespitum arigonis (Mollusca) Abstracts of the VIth European Multicolloquium of Parasitology. The Hague, Netherlands, 163.Google Scholar
Ambrosi, M. (1991) La diagnostica coprologica nelle elmintiasi di allevamento: caso delle distomatosi dei ruminanti. Praxis Veterinaria 12, 1720.Google Scholar
Ambrosi, M. & Principato, M. (1981) Dicroceliosi ovina: variazioni stagionali della positività coproscopica in animali spontaneamente parassitati. Obiettivi e Documenti Veterinari 2, 5556.Google Scholar
Ambrosi, M., Baldelli, B., Piergili Fioretti, D., Polidori, G.A., Grelloni, V., Moretti, A. & Principato, M. (1980) Dicroceliosi ovina: insorgenza e decorso della infezione da Dicrocoelium dendriticum studiati con metodi parassitologici e sierologici (ELISA) in quattro gruppi di ovini di traccia Rivista di Parassitologia 41, 299307.Google Scholar
Badie, A. (1978) La dicroceliose ovine: incidence des facteurs climatiques et contribution à la mise au point d'une méthode de prevision. Annales de Parasitologie Humaine et Comparée 53, 373385.CrossRefGoogle Scholar
Boray, J.C. (1985) Flukes of domestic animals. pp.179218 in Gaafar, S.M., Howard, W.E. & Marsh, R.E. (Eds) Parasites, pests and predators, B.V., Amsterdam, Elsevier Science Publishers.Google Scholar
Cabanas, E., Manga-González, M.Y. & González-Lanza, C. (1989) Eliminación mensual de huevos de Dicrocoelium dendriticum (Trematoda) por ovinos marcados de los montes Cántabro-Leoneses. Actas del VI Congreso Nacional y I Congreso Ibérico de Parasitología Cáceres, Spain 126.Google Scholar
Calamel, M. & Giauffret, A. (1976) Interprétation des résultats dans le diagnostic coproscopique de la dicrocoeliose. Recueil de Médecine Vétérinaire 152, 99104.Google Scholar
Camara, L., Pfister, K. & Aeschlimann, A. (1996) Analyse histopathologique de foie de bovin infesté par Dicrocoelium dendriticum. Veterinary Research 27, 8792.Google ScholarPubMed
Campo, R., González-Lanza, C., Manga-González, M.Y. Rollinson, D. (1992a) Characterization of adult and larval stages of Dicrocoelium dendriticum (Trematoda) by enzyme electrophoresis. Abstracts of the VIth European Multicolloquium of Parasitology. The Hague, Netherlands, 210.Google Scholar
Campo, R., Manga-González, M.Y., González-Lanza, C. & Del-Pozo, P. (1992b) Detección isoenzimática de las primeras fases larvarias de Dicrocoelium dendriticum (Trematoda) en moluscos hospedadores intermediarios infestados experimentalmente. Cuadernos de Investigación Biológica 17, 44.Google Scholar
Campo, R., Manga-González, M.Y., González-Lanza, C., Rollinson, D. & Sandoval, H. (1998) Characterization of adult Dicrocoelium dendriticum by isoelectric focusing. Journal of Helminthology 72, 109116.CrossRefGoogle ScholarPubMed
Campo, R., Manga-González, M.Y. & González-Lanza, C. (2000) Relationship between egg output and parasitic burden in lambs experimentally infected with different doses of Dicrocoelium dendriticum (Digenea). Veterinary Parasitology 87, 139149.CrossRefGoogle ScholarPubMed
Cavani, C., Losi, G., Manfredini, M., Pavoncelli, R.M., Pietrobelli, M. & Restani, R. (1982) Ricerche sull'influenza della dicroceliasi sulle caratteristiche quantitative e qualitative della produzione di latte in pecore. Obiettivi e Documenti Veterinari 3, 5963.Google Scholar
Chandra, G. (1973) First detection of Dicrocoelium eggs in the faeces of experimentally infected lambs, guinea pigs and pigs. Haryana Agricultural University Journal of Research 3, 3134.Google Scholar
Cordero-del-Campillo, M., Rojo-Vázquez, F.A., Díez-Baños, P. & Chaton-Schaffner, M. (1982) Efficacité de l'albendazole contre une infestation naturelle a Dicrocoelium dendriticum chez le mouton. Revue de Médecine Vétérinaire 133, 4149.Google Scholar
Cordero-del-Campillo, M., Catañón-Ordóñez, L. & Reguera-Feo, A. (1994) Indice-catálogo de zooparásitos ibéricos. Secretariado de Publicaciones, Universidad de León, León, Spain.Google Scholar
Cross, P.C. & Mercer, K.L. (1998) Cell and tissue ultrastructure: a functional perspective, New York, WH Freeman and Company.Google Scholar
Del Río, J. (1967) Epizootiología de la dicroceliosis en la provincia de León. Anales de la Facultad de Veterinaria de León 13, 211285.Google Scholar
Dementev, I.S. ]#x0026; Karabaev, D.K. (1968) [Infection of terrestrial molluscs and ants by Dicrocoelium dendriticum larvae in south-eastern Kazakhstan]. Vestik sel'-skokhozyaistvennoi Nauki, Alma-Ata 12, 5155.Google Scholar
Dementev, I.S., Serikbaeva, B.K. ]#x0026; Karabaev, D.K. (1978) [The effect of vitamin C and cobalt chloride on the pathological process in dicrocoeliasis in sheep]. Trudy Kazakhskogo Nauchno-Issledovatel'skogo Veterinarnogo Instituta (Voprosy veterinarnoi parazitologii v Kazakhstane) 17, 7981.Google Scholar
Desco, M., Cano, M.J., Duarte, J., Rodríguez, F., Fernández-Caleya, D., Álvarez-Valdivielso, M., Antoranz, J.C., Rubio, M.A., García-Barreno, P. & Del Cañizo, J.F. (1989) Blood biochemistry values of sheep (Ovis aries ligeriensis). Comparative Biochemistry and Physiology 94A, 717719.CrossRefGoogle Scholar
Ferre, I., Ortega-Mora, L.M. & Rojo-Vázquez, F.A. (1994) Prevalence of Dicrocoelium dendriticum infection in sheep in León province (NW Spain). Preventive Veterinary Medicine 21, 147154.CrossRefGoogle Scholar
Ferreras, M.C., Manga-González, M.Y., Pérez, C., García-Iglesias, M.J., Campo, R., González-Lanza, C., Escudero, A. & García-Marín, J.F. (2000) Local immune response to experimental ovine dicrocoeliosis. Acta Parasitologica 45, 198.Google Scholar
Frank, W., Lucius, R. & Romig, T. (1984) Studies on the biology, pathology, ecology and epidemiology of Dicrocoelium hospes Looss, 1907 in West Africa (Ivory Coast) 3858 in Markl, H. & Bittner, A. (Eds)Recent German research on problems of parasitology, animal health and animal breeding in the tropics and subtropics. Deutsche Forschungsgemeinschaft, Bonn and the Institute for Scientific Co-operation, Tübingen, Federal Republic of Germany.Google Scholar
Gittenberger, E. & Manga-González, M.Y. (1977) Some new species of the genus Helicella (Pulmonata Helicidae) from the province León, Spain. Zoologische Mededelingen 51, 177189.Google Scholar
Gómez, B.J., Manga-González, M.Y., Angulo, E. & González-Lanza, C. (1996) Alteraciones histopatológicas producidas por Dicrocoelium dendriticum (Trematoda) en dos especies de Cernuella (Mollusca) sacrificadas a los tres meses post-infestación. Iberus 14, 189195.Google Scholar
González-Lanza, C., Manga-González, M.Y. & Del-Pozo, P. (1993) Coprological study of the Dicrocoelium dendriticum (Digenea) egg elimination by cattle in highland areas in León Province, Northwest Spain. Parasitology Research 79, 488491.CrossRefGoogle ScholarPubMed
González-Lanza, C., Manga-González, M.Y., Campo, R. & Del-Pozo, P. (1997) Larval development of Dicrocoelium dendriticum in Cernuella (Xeromagna) cespitum arigonis under controlled laboratory conditions. Journal of Helminthology 71, 311317.CrossRefGoogle ScholarPubMed
González-Lanza, C., Manga-González, M.Y., Campo, R., Del-Pozo, P., Sandoval, H., Oleaga, A. & Ramajo, V. (2000) IgG antibody response to ES or somatic antigens of Dicrocoelium dendriticum (Trematoda) in experimentally infected sheep. Parasitology Research 86, 472479.CrossRefGoogle ScholarPubMed
Gundlach, J.L., Furmaga, S., Uchacz, S. & Sadzikowski, A. (1982) Przypadek przewleklej dikroceliozy owiec i próba jej leczenia. Medycyna Weterynaryjna 38, 204206.Google Scholar
Hohorst, W. & Lämmler, G. (1962) Experimentelle Dicrocoeliose-Studien. Zeitschrift für Tropenmedizin und Parasitologie 13, 377397.Google Scholar
Huntley, J.F., Newlands, G. & Miller, H.R. (1984) The isolation and characterization of globule leucocytes: their derivation from mucosal mast cells in parasitized sheep. Parasite Immunology 6, 371390.CrossRefGoogle ScholarPubMed
Jithendran, K.P. & Bhat, T.K. (1996) Prevalence of dicrocoeliosis in sheep and goats in Himachal Pradesh, India. Veterinary Parasitology 61, 265271.CrossRefGoogle ScholarPubMed
Jonlija, R., Cankovic, M. ]#x0026; Rozman, M. (1972) [Examination of ants the second intermediary hosts of Dicrocoelium lanceolatum in Bosnia and Hercegovina, I]. Veterinaria 21, 317322.Google Scholar
Kalkan, A. (1971) Dicrocoelium dendriticum (Rudolphi, 1819) Looss, 1899 in Turkey. l. Field studies of intermediate and final hosts in the South Marmara region, 1968. British Veterinary Journal 127, 6775.CrossRefGoogle Scholar
Karanfilovski, G. (1983) Economic losses caused by fascioliasis and dicrocoeliasis to livestock production in Pljevlja and surrounding area (in Serbo-Croatian). Veterinaria Yugoslavica 32, 253260.Google Scholar
Katayama, F. (1996) Alterations of the mucin components in bile duct epithelium associated with proliferating cholangitis.An experimental study. Hokkaido Igaku Zasshi 71, 585598.Google ScholarPubMed
Kopp, H. (1975) Untersuchungen über die Eiausscheidung von Fasciola hepatica und Dicrocoelium dendriticum bei Schaf und Rind im Verlauf eines Jahres Inaugural-Disertation zur Erlangung der Tiermedizinischen Doktorwürde des Fachbereichs Tiermedizin der Ludwig- Maximillians-Universität München, Germany 152.Google Scholar
Manga-González, M.Y. (1983) Los Helicidae (Gastropoda, Pulmonata) de la Provincia de León Institución ‘Fray Bernardino de Sahagún’, Excma. Diputación Provincial de León Consejo Superior de Investigaciones Científicas (CECEL) León, Spain.Google Scholar
Manga-González, M.Y. (1987) Some aspects of the biology and helminthofauna of Helicella (Helicella) itala (Linnaeus, 1758) (Mollusca). Natural infection by Dicrocoeliidae (Trematoda). Revista Ibérica de Parasitología Vol. Extraordinario 131148.Google Scholar
Manga-González, M.Y. (1992) Some land molluscs species involved in the life cycle of Dicrocoelium dendriticum (Trematoda) in the wild in the province of León (NW, Spain) .pp.248249 in Giusti, F. & Manganelli, G. (Eds)Abstracts of the 11th International Malacological Congress, Siena, Italy Unitas Malacological. University of Siena.Google Scholar
Manga-González, M.Y. & Cordero, M. (1979) New malacological records for the province of León (NW Spain) and percentages of infestation by Trematoda. Malacologia 18, 6166.Google Scholar
Manga-González, M.Y. & Quiroz-Romero, H. (1999) Dicroceliosis. 272282 in Cordero del Campillo, M., Rojo Vázquez, F.A., Martínez Fernández, A.R., Sánchez Acedo, M.C., Hernández Rodríguez, S., Navarrete López-Cozar, I., Díez Baños, P., Quiroz Romero, H. & Carvalho Valera, (Eds)Parasitología veterinaria. McGraw-Hill Interamericana.Google Scholar
Manga-González, M.Y. & Rollinson, D. (1986) Preliminary observations on the use of isoelectric focusing of enzymes for the identification of Helicella species (Mollusca, Stylommatophora) from León province (Spain). Iberus 6, 155165.Google Scholar
Manga-González, M.Y., González-Lanza, C. & Del-Pozo, M.P. (1991) Dynamics of the elimination of Dicrocoelium dendriticum (Trematoda, Digenea) eggs in the faeces of lambs and ewes in the Porma basin (León, NW Spain). Annales de Parasitologie Humaine et Comparée 66, 5761.CrossRefGoogle ScholarPubMed
Manga-González, M.Y., González-Lanza, C., Del-Pozo, M.P. & Campo, R. (1995) Studies on experimental infection by Dicrocoelium dendriticum (Trematoda) of Cernuella (Xeromagana) cespitum arigonis (Mollusca) specimens in a natural environment. Abstracts of 12th International Malacological Congress, Vigo, Spain 456458.Google Scholar
Manga-González, M.Y., González-Lanza, C. & Del-Pozo, M.P. (1998) Study on the experimental susceptibility of two Cernuella species (Mollusca: Stylommatophora) to Dicrocoelium dendriticum (Digenea). Abstracts, World Congress of Malacology, Washington D.C, USA 205.Google Scholar
Manga-González, M.Y., González-Lanza, C., Cabanas, E. & Campo, R. (2001a) Contributions to and review of dicrocoeliosis, with special reference to the intermediate hosts of Dicrocoelium dendriticum . Parasitology 123, S91S114.CrossRefGoogle Scholar
Manga-González, M.Y., González-Lanza, C. & Lavín, P. (2001b) Encuesta parasitológica y ensayos con netobimin frente a Dicrocoelium dendriticum y Fasciola hepatica en ganado vacuno mantenido en pastoreo. Acta Parasitológica Portuguesa 8, 348.Google Scholar
Manga-González, M.Y., Ferreras, M.C., Campo, R., González-Lanza, C., Perez, V. & García-Marin, J.F. (2004) Hepatic marker enzymes, biochemical parameters and pathological effects in lambs experimentally infected with Dicrocoelium dendriticum (Digenea). Parasitology Research 93, 344355.CrossRefGoogle ScholarPubMed
Massoud, J. (1981) Histopathology of liver in Iranian sheep naturally infected with Dicrocoelium dendriticum. Annals of Tropical Medicine and Parasitology 75, 293298.CrossRefGoogle ScholarPubMed
Mohamed, A.R.E. & Mummery, V. (1990) Human dicrocoeliasis. Report on 208 cases from Saudi Arabia. Tropical and Geographical Medicine 42, 17.Google Scholar
Oleaga, A., Ramajo, V., Muro, A., Rodriguez-Osorio, M., Gómez-García, V, González-Lanza, C. & Manga-González, M.Y. (1999) Estudio de antígenos de Dicrocoelium dendriticum. Resúmenes del VI Congreso Ibérico de Parasitología. Córdoba, Spain, 163.Google Scholar
Otranto, D. & Traversa, D. (2002) A review of dicrocoeliosis of ruminants including recent advances in the diagnosis and treatment. Veterinary Parasitology 107, 317335.CrossRefGoogle ScholarPubMed
Otranto, D. & Traversa, D. (2003) Dicrocoeliosis of ruminants: a little known fluke disease. Trends in Parasitology 19, 1215.CrossRefGoogle ScholarPubMed
Paraschivescu, D. (1981) Untersuchungen zur künstlichen Infektion von Shaflämmern mit dem Kleinen Leberegel Dicrocoelium dendriticum Rudolphi über den Zwischenwirt Formica pratensis Retz. Waldhygiene 14, 7378.Google Scholar
Paraschivescu, D. (1983) Untersuchungen zur Temperaturabhängigkeit der Tetaniephase von Formica pratensis bei einer Infektion mit Stadien des Kleinen Leberegels Dicrocoelium dendriticum. Waldhygiene 15, 2124.Google Scholar
Petrov, Y.F. ]#x0026; Abalikhin, B.G. (1983) [Biochemical indicators and the microflora of the bile and intestinal contents in sheep with dicrocoeliasis]. Veterinariya, Moscow 3, 4547.Google Scholar
Prunescu, C., Prunescu, P., Fromunda, V., Paraschivescu, D. ]#x0026; Popescu, S. (1979) [Histopathological changes of the liver in hamsters with experimental dicroceliasis]. Archiva Veterinaria 14, 8390.Google Scholar
Quiroz-Romero, H., Campo, R. & Manga-González, M.Y. (1996) Valoración de modelos quimioterapéuticos en el control de Dicrocoelium dendriticum en ganado ovino en la provincia de León, España Memoria de la Reunión Nacional de Investigación Pecuaria, Morelos 1996 Cuernavaca, Mexico 85.Google Scholar
Rahko, T. (1972) Studies on the pathology of dicrocoeliasis and fascioliasis in the goat. I. The histopathology of the liver and bile ducts. Acta Veterinaria Scandinavica 13, 554562.CrossRefGoogle ScholarPubMed
Ranucci, S. & Grol-Ranucci, H. (1978) Ricerche ematochimiche in ovini con lesioni parassitaire del fegato. Clinica Veterinaria 101, 324333.Google Scholar
Ranucci, S., Mughetti, L., Ambrosi, M. & Grelloni, V. (1981) Rilievi ematochimici, anatomo-istopatologici e parassitologici in ovini infetti da dicroceliosi. Rivista di Zootecnia e Veterinaria 9, 173175.Google Scholar
Revilla-Nuín, B., Manga-González, M.Y., Rodríguez-Aparicio, L.B. & Del-Pozo, P., González-Lanza, C. (2003) Estudios preliminares sobre la caracterización de antígenos de Dicrocoelium dendriticum. Resúmenes del XXVI Congreso de la Sociedad Española de Bioquímica y Biología Molecular. A Coruña, Spain 234.Google Scholar
Revilla-Nuín, B., Manga-González, M.Y., Del-Pozo-Carnero, M.P. & González-Lanza, C. (2004) Purification and identification of a Dicrocoelium dendriticum specific antigens. Resúmenes del IX European Multicolloquium of Parasitology. Valencia, Spain 298.Google Scholar
Robles, L.C., Manga-González, M.Y. & González-Lanza, C. (2001) Preliminary chromatographic study of Dicrocoelium dendriticum antigen. Abstracts of the 18th International Conference of the World Association for the Advancement of Veterinary Parasitology. Stresa, Italy 34.Google Scholar
Rojo-Vázquez, F.A., Cordero-del-Campillo, M., Díez-Baños, P. & Chaton-Schaffner, M. (1981) Relation existant entre le nombre d'oeufs dans les fèces et la charge parasitaire lors des infestations naturelles a Dicrocoelium dendriticum chez les ovins. Revue de Médecine Vétérinaire 132, 601607.Google Scholar
Rozman, M., Gradjanin, S. & Cankovic, M. (1974) The transitory hosts of Dicrocoelium dendriticum in the mountain area of Bosnia and Herzegovina. 513514 Proceedings of the Third International Congress of Parasitology. Munich, Vienna FACTA Publication.Google Scholar
Salimova, M. (1972) ]#x005B;Experimental dicrocoeliasis of Karakul lambs]. Trudy VII Vsesoyuznoi Konferentsii po Prirodnoi Ochagovosti Boleznei i Obshchim Voprosam Parazitologii Zhivotnykh 6, 155157.Google Scholar
Sánchez-Campos, S., Tuñón, M.J., González, P., Campo, R., Ferreras, M.C., Manga-González, M.Y. & González-Gállego, J. (1996) Effects of experimental dicrocoeliosis on oxidative drug metabolism in hamster liver. Comparative Biochemistry and Physiology 115C 5560.Google Scholar
Sánchez-Campos, S., Tuñón, M.J, González, P. & González-Gallego, J. (1999) Oxidative stress and changes in liver antioxidant enzymes induced by experimental dicroceliosis in hamsters. Parasitology Research 85, 468474.CrossRefGoogle ScholarPubMed
Sánchez-Campos, S., González, P., Ferreras, C, García-Iglesias, M.J., González-Gallego, J. & Tuñón, M.J(2000) Morphologic and biochemical changes caused by experimentally induced dicroceliosis in hamsters (Mesocricetus auratus). Comparative Medicine 50, 147152.Google ScholarPubMed
Sandoval, H., Manga-González, M.Y., Campo, R., García, P., Castro, J.M. & Pérez-de-la-Vega, M. (1999) Preliminary study on genetic variability of Dicrocoelium dendriticum determined by random amplified polymorphic DNA. Parasitology International 48, 2126.CrossRefGoogle Scholar
Scala, A., Coda, S., Ximenes, L.A. & Cavedagna, G. (1991) Dicroceliasi ovina in Sardegna: Tassi di prevalenza, lesioni anatomo-istopatologiche e tests ematochimici. Atti della Federatione Mediterranea Sanità e Produzione Ruminanti 1, 209214 Google Scholar
Schuster, R. (1991) Factors influencing the metacercarial intensity in ants and the size of Dicrocoelium dendriticum metacercarial cysts. Journal of Helminthology 65, 275279.CrossRefGoogle ScholarPubMed
Schuster, R. (1993) Infection patterns in the first intermediate host of Dicrocoelium dendriticum. Veterinary Parasitology 47, 235243.CrossRefGoogle ScholarPubMed
Spindler, E.M., Zahler, M. & Loos-Frank, B. (1986) Behavioural aspects of ants as second intermediate hosts of Dicrocoelium dendriticum. Zeitschrift für Parasitenkunde 72, 689692.CrossRefGoogle Scholar
Srivastava, G.C., Kolev, G. & Georgiev, M. (1978) A surgical approach to trace the route of migration of Dicrocoelium dendriticum in the laboratory animals. Rivista di Parassitologia 39, 131137.Google Scholar
Tarry, D.W. (1969) Dicrocoelium dendriticum : the life cycle in Britain. Journal of Helminthology 43, 403416.CrossRefGoogle Scholar
Theodoridis, Y., Duncan, J.L., MacLean, J.M. & Himonas, C.A. (1991) Pathophysiological studies on Dicrocoelium dendriticum infection in sheep. Veterinary Parasitology 39, 6166.CrossRefGoogle ScholarPubMed
Wedrychowicz, H., Ducommun, D., Górski, P. & Pfister, K. (1995) Somatic antigens of adult Dicrocoelium dendriticum recognised by bile antibodies of naturally infected cattle. Veterinary Parasitology 56, 4756.CrossRefGoogle ScholarPubMed
Wedrychowicz, H., Ducommun, D., Klockiewicz, M. & Pfister, K. (1996) Surface and ES antigens of adult Dicrocoelium dendriticum inducing bile antibody responses in naturally infected cattle. Acta Parasitologica 41, 139144.Google Scholar
Wolff, K., Hauser, B. & Wild, P. (1984) Dicrocoeliose des Schafes: Untersuchungen zur Pathogenese und zur Regeneration der Leber nach Therapie. Berliner und Münchener Tierärztliche Wochenschrift 97, 378387.Google Scholar
Yamashiro, M., Kouda, W., Kono, N., Tsuneyama, K., Matsui, O. & Nakanuma, Y., (1998) Distribution of intrahepatic mast cells in various hepatobiliary disorders. An immunohistochemical study. Virchows Archiv 433, 471479.CrossRefGoogle ScholarPubMed