[en] In cattle experimentally infected with Fasciola hepatica, parasite specific IgG1 and IgG2 responses were studied. Additionally parasite specific IgE production was assessed by the Passive Cutaneous Anaphylaxis reaction. The primary infection was administered either as a single-dose or as a trickle infection over a 4-week period. Animals were challenged 4 months later. Titres of IgG1 and IgG2 against excretory-secretory parasite products (FhESAg), and against a whole-worm extract (FhSomAg) were measured by enzyme-linked immunosorbent assay (ELISA) in relation to weight gain, serum hepatic enzyme levels, and fluke infection rate. At necropsy, the mean number of flukes recovered was similar in both infected groups. The two ELISAs specific for bovine IgG1 showed analogous sensitivity and specificity (92% and 94%). Cross-reactivity was observed towards Echinococcus granulosus, Cysticercus tenuicollis, and C. ovis but not towards C. bovis, Cooperia spp., and Ostertagia spp. FhESAg gave rise to apparently more stable specific IgG1 titres as compared to FhSomAg. Mean IgG1 titres were significantly higher in the single-dose-infected group than in the trickle-infected group during the early migratory phase of the infection (week 2 to week 4 (FhSomAg) or week 6 (FhESAg)). IgG2 values were consistently lower than IgG1 levels. The kinetic response of both isotypes yielded a similar pattern. Specific IgE antibodies were detected in cattle of both infected groups from week 2 post-primary infection (PPI) onwards. The mean serum glutamate dehydrogenase (GLDH) and gamma-glutamyl transferase (gammaGT) activities were significantly higher in the single-dose-infected group for 3 weeks around peak levels (12-14 weeks PPI and 14-16 weeks PPI for GLDH and gammaGT respectively). Western blotting revealed a major antigenic fraction in FhESAg (26-30 kDa) recognized specifically by sera from F. hepatica infected calves as early as 6-8 weeks PPI. Experimental challenge caused no statistically significant modification of any parameter (IgG1 and IgG2 titres, enzymatic activities, immunoblotting) used to monitor the course of the infection. No correlation was found between fluke size and number, and antibody titres, suggesting that IgG1 production has little protective effect against F. hepatica infection.
Disciplines :
Veterinary medicine & animal health
Author, co-author :
Bossaert, K.
Farnir, Frédéric ; Université de Liège - ULiège > Département de productions animales > Biostatistique, économie, sélection animale
Losson, Bertrand ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires > Parasitologie et pathologie des maladies parasitaires
Language :
English
Title :
Humoral Immune Response in Calves to Single-Dose, Trickle and Challenge Infections with Fasciola Hepatica
Anderson P.H., Berrett S., Brush P.J., Hebert C.N., Parfitt J.W., Patterson D.S. Biochemical indicators of liver injury in calves with experimental fascioliasis. Vet. Rec. 100:1977;43-45.
Anderson P.H., Berrett S., Patterson D.S. Resistance to Fasciola hepatica in cattle. II. Biochemical and morphological observations. J. Comp. Pathol. 88:1978;245-251.
Anderson P.H., Matthews J.G., Berrett S., Brush P.J., Patterson D.S. Changes in plasma enzyme activities and other blood components in response to acute and chronic liver damage in cattle. Res. Vet. Sci. 31:1981;1-4.
Armour J., Dargie J.D. Immunity to Fasciola hepatica in the rat. Successful transfer of immunity by lymphoid cells and by serum. Exp. Parasitol. 35:1974;381-388.
Biguet J., Capron A., Tran Van Ky P. Les antigènes de Fasciola hepatica. Ann. Parasitol. 37:1962;221-231.
Brown W.C., Davis W.C., Dobbelaere D.A.E., Rice-Ficht A.C. CD4+ T-cell clones obtained from cattle chronically infected with Fasciola hepatica and specific for adult worm antigen express both unrestricted and Th2 cytokine profiles. Infect. Immun. 62:1994;818-827.
Brown W.C., Rice-Ficht A.C., Estes D.M. Bovine type 1 and type 2 responses. Vet. Immunol. Immunopathol. 63:1998;45-55.
Brown W.C., McElwain T.F., Palmer G.H., Chantler S.E., Estes D.M. Bovine CD4(+) T-lymphocyte clones specific for rhoptry-associated protein 1 of babesia bigemina stimulate enhanced immunoglobulin G1 (IgG1) and IgG2 synthesis. Infect. Immun. 67:1999;155-164.
Chauvin A., Bouvet G., Boulard C. Humoral and cellular immune responses to Fasciola hepatica experimental primary and secondary infection in sheep. Int. J. Parasitol. 25:1995;1227-1241.
Clery D., Torgerson P., Mulcahy G. Immune responses of chronically infected adult cattle to Fasciola hepatica. Vet. Parasitol. 62:1996;71-82.
Cornelissen J.B.W.J., de Leeuw W.A., van der Heijden P.J. Comparison of an indirect haemagglutination assay and an ELISA for diagnosing Fasciola hepatica in experimentally and naturally infected sheep. Vet. Q. 14:1992;152-156.
Dalton J.P., McGonigle S., Rolph T.P., Andrews S.J. Induction of protective immunity in cattle against infection with Fasciola hepatica by vaccination with cathepsin L proteinases and with hemoglobin. Infect. Immun. 64:1996;5066-5074.
Doy T.G., Hughes D.L., Harness E. Resistance of the rat to reinfection with Fasciola hepatica and the possible involvement of intestinal eosinophil leucocytes. Res. Vet. Sci. 25:1978;41-44.
Doy T.G., Hughes D.L. Evidence of two distinct mechanisms of resistance in the rat to reinfection with Fasciola hepatica. Int. J. Parasitol. 12:1982;357-361.
Doy T.G., Hughes D.L. Fasciola hepatica: site of resistance to reinfection in cattle. Exp. Parasitol. 57:1984;274-278.
Doyle J.J. Acquired immunity to experimental infection with Fasciola hepatica in cattle. Res. Vet. Sci. 12:1971;527-534.
Doyle J.J. Evidence of an acquired resistance in calves to a single experimental infection with Fasciola hepatica. Res. Vet. Sci. 13:1972;456-459.
Doyle J.J. Homocytotropic antibodies induced in calves by infection with Fasciola hepatica. Int. Arch. Allergy. 45:1973;744-751.
Doyle J.J. The relationship between the duration of a primary infection and the subsequent development of an acquired resistance to experimental infections with Fasciola hepatica in calves. Res. Vet. Sci. 14:1973;97-103.
Duffus W.P.H., Franks D. The interaction in vitro between bovine immunoglobulin and juvenile Fasciola hepatica. Parasitology. 82:1981;1-10.
Estes D.M., Closser N.M., Allen G.K. IFN-g stimulates IgG2 production from bovine B cells costimulated with anti-m and mitogen. Cell. Immunol. 154:1994;287-295.
Farrell C.J., Shen D.T., Wescott R.B., Lang B.Z. An enzyme-linked immunosorbent assay for diagnosis of Fasciola hepatica infection in cattle. Am. J. Vet. Res. 42:1981;237-240.
Genicot B., Mouligneau F., Lekeux P. Economic and production consequences of liver fluke disease in double-muscled fattening cattle. J. Vet. Med. 38:1991;203-208.
Hames, B.D., Rickwood, D., 1990. Gel Electrophoresis of Proteins: A Pratical Approach. Oxford University Press, New York, p.17.
Hanna R.E.B., Trudgett A. Fasciola hepatica: development of monoclonal antibodies and their use to characterize a glycocalyx antigen in migrating flukes. Parasite Immunol. 5:1983;409-425.
Haroun E.M., Hillyer G.V. Resistance to fascioliasis - A review. Vet. Parasitol. 20:1986;63-93.
Hayes T.J., Mitrovic M. The early expression of protective immunity to Fasciola hepatica in rats. J. Parasitol. 63:1977;584-587.
Hope Cawdery M.J., Strickland K.L., Conway A., Crowe P.J. Production effects of liver fluke in cattle: 1. The effects of infection on liveweight gain, feed intake and food conversion efficiency in beef cattle. Br. Vet. J. 133:1977;145-159.
Hughes D.L., Hanna R.E.B., Symonds H.W. Fasciola hepatica: Ig G and Ig A levels in the serum and bile of infected cattle. Exp. Parasitol. 52:1981;271-279.
Jenicek, M., Cleroux, R., 1983. Epidémiologie. Principe. Techniques. Applications. Edisem, Ste Hyacinthe, Québec, pp.31-34.
Keegan P.S., Trudgett A. Fasciola hepatica in the rat: immune responses associated with the development of resistance to infection. Parasite Immunol. 14:1992;657-669.
Letesson J.-J., Lostrie-Trussard N., Depelchin A. Production d'anticorps monoclonaux spécifiques d'isotypes d'immunoglobines bovines. Ann. Méd. Vét. 129:1985;131-141.
Luzon M., Meana A., Miranda M.E., Gomez-Bautista M. Prevalencia de la fasciolosis en vacuna en pastos humedos del Norte de España. Med. Vet. 13:1996;657-663.
López Abán J., Ramajo V., Pérez Arellano J.L., Oleaga A., Hillyer G.V., Muro A. A fatty acid binding protein from Fasciola hepatica induced protection in C57/BL mice from challenge infection with Schistosoma bovis. Vet. Parasitol. 83:1999;107-121.
Mage C., Mauran A., Moisset M. Contrôle de l'infestation de la grande douve des bovins: une organisation et une application en fermes. Bull. G. T. V. 2:1995;11-17.
Mulcahy G., O'Connor F., McGonigle S., Dowd A., Clery D., Andrews S.J., Dalton J.P. Correlation of specific antibody titre and avidity with protection in cattle immunized against Fasciola hepatica. Vaccine. 16:1998;932-939.
Oldham G. Antibodies to Fasciola hepatica antigens during experimental infections in cattle measured by ELISA. Vet. Parasitol. 13:1983;151-158.
Paz A., Sanchez-Andrade R., Panadero R., Diez-Baños P., Morrondo P. IgG isotype specific immune response in rats infected with Fasciola hepatica. Vet. Parasitol. 79:1998;229-237.
Pfister K., Daveau C.H., Ambroise-Thomas P. Partial purification of somatic and excretory-secretory products of adult Fasciola hepatica and their application for the serodiagnosis of experimental and natural fascioliasis using an ELISA. Res. Vet. Sci. 37:1984;39-43.
Poitou I., Baéza E., Boulard C. Kinetic responses of parasite-specific antibody isotypes, blood leucocyte pattern, blood leucocyte pattern and lymphocyte subsets in rats during primary infestation with Fasciola hepatica. Vet. Parasitol. 49:1993;179-190.
Ross J.G. Experimental infection of cattle with Fasciola hepatica: a comparison of low and high infection rates. Nature, London. 208:1965;907.
Ross J.G. Experimental infections of cattle with Fasciola hepatica. Challenge infections. Nature. 212:1966;1464-1465.
Santiago N., Hillyer G.V. Isolation of potential serodiagnostic Fasciola hepatica antigens by electroelution from polyacrylamide gels. Am. J. Trop. Med. Hyg. 35:1986;1210-1217.
Santiago N., Hillyer G.V., Garcia Rosa M.I., Morales M.H. Identification of functional Fasciola hepatica antigens in experimental infections in rabbits. Am. J. Trop. Med. Hyg. 35:1986;135-140.
Santiago N., Hillyer G.V. Antibody profiles by EITB and ELISA of cattle and sheep infected with Fasciola hepatica. J. Parasitol. 74:1988;810-818.
Sexton J.L., Milner A.R., Campbell N.J. Fasciola hepatica: immunoprecipitation analysis of biosyntically labelled antigens using sera from infected sheep. Parasite Immunol. 13:1991;105-108.
Sher A., Coffman R.L. Regulation of immunity to parasites by T cells and T cell-derived cytokines. Ann. Rev. Immunol. 10:1992;385-409.
Smith P.K., Krohn R.I., Hermanson G.T., Mallia A.K., Gartner F.H., Provenzano M.D., Fujimoto E.K., Goeke N.M., Olson B.J., Klenk D.C. Measurement of protein using bicinchoninic acid. Anal. Biochem. 150:1985;76-85.
Spithill T.W., Piedrafita D., Smooker P.M. Immunological approaches for the control of fasciolosis. Int. J. Parasitol. 27:1997;1221-1235.
Van Milligen F.J., Cornelissen J.B.W.J., Bokhout B.A. Location of induction and expression of protective immunity against Fasciola hepatica at the gut level: a study using an ex vivo infection model with ligated gut segments. J. Parasitol. 84:1998;771-777.
Van Milligen F.J., Cornelissen J.B.W.J., Hendriks I.M., Gaasenbeek C.P.H., Bokhout B.A. Protection to Fasciola hepatica in the gut mucosa of immune rats is associated with infiltrates of eosinophils, IgG1, IgG1 and IgG2a antibodies around the parasites. Parasite Immunol. 20:1998;285-292.
Vignali M., Acosta D., Rossi S., Lanzzeri S., Gama S., Maisonave J., Cristina J. Humoral immune response against Fasciola hepatica in bovines: primary characterization of protection induced by irradiated metacercariae. Parasitol. al dia. 20:1996;32-37.
Welch R.D., Smith P.H., Malone J.B., Holmes R.A., Geaghan J.P. Herd evaluation of Fasciola hepatica infection levels in Louisiana cattle by an enzyme-linked immunosorbent assay. Am. J. Vet. Res. 48:1987;345-347.
Williams D.J.L., Newson J., Naessens J. Quantitation of bovine immunoglobulin isotypes and allotypes using monoclonal antibodies. Vet. Immunol. Immunopathol. 24:1990;267-283.
Wyckoff III J.H., Bradley R.E. Diagnosis of Fasciola hepatica infection in beef calves by plasma enzyme analysis. Am. J. Vet. Res. 46:1985;1015-1019.
Wyckoff III J.H., Bradley R.E. An optimized enzyme-linked immunosorbent assay for quantitative diagnosis of bovine fascioliasis. J. Parasitol. 72:1986;439-444.
