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Resistance against migrating Ascaris suum larvae in pigs immunized with infective eggs or adult worm antigens

Published online by Cambridge University Press:  12 July 2001

F. J. SERRANO
Affiliation:
Parasitology Section, Department of Medicine and Animal Health, Facultad de Veterinaria, Universidad de Extremadura, Avda de la Univerdidad s/n, 10071 Cáceres, Spain
D. REINA
Affiliation:
Parasitology Section, Department of Medicine and Animal Health, Facultad de Veterinaria, Universidad de Extremadura, Avda de la Univerdidad s/n, 10071 Cáceres, Spain
E. FRONTERA
Affiliation:
Parasitology Section, Department of Medicine and Animal Health, Facultad de Veterinaria, Universidad de Extremadura, Avda de la Univerdidad s/n, 10071 Cáceres, Spain
A. ROEPSTORFF
Affiliation:
Danish Centre for Experimental Parasitology, Department of Veterinary Microbiology, The Royal Veterinary and Agricultural University, Ridebanevej 3, DK-1870 Frederiksberg C, Denmark
I. NAVARRETE
Affiliation:
Parasitology Section, Department of Medicine and Animal Health, Facultad de Veterinaria, Universidad de Extremadura, Avda de la Univerdidad s/n, 10071 Cáceres, Spain

Abstract

Resistance to Ascaris suum infections was investigated in 8- and 15-week-old Iberian pigs. Groups of 3 or 5 pigs were immunized weekly for 6 weeks with antigens of adult A. suum: a 97 kDa body wall (BW) fraction, a 42 kDa fraction of pseudocoelomic fluid (PF) or a 14 kDa PF-fraction; or were inoculated with increasing doses of infective eggs (500–20000), with or without abbreviation by pyrantel pamoate. All immunized pigs and unimmunized control pigs, were challenged with 10000 infective eggs 7 days after the last immunization. The number of liver lesions and lung larvae was substantially lower in the older pigs than in the younger ones 7 days after challenge, but the resistance in immunized pigs of both age groups was similar in comparison to the challenge controls of the same age. The highest degree of resistance against lung larvae was observed in pigs immunized with A. suum eggs (97–99%). The pigs immunized with the 14 kDa and 42 kDa PF-fractions were also well protected (67–93%), while no protection was produced by the 97 kDa BW fraction (0–49%). The reduction of white spots following immunization was less evident, with a maximum of 82% reduction in egg-inoculated young pigs.

Type
Research Article
Copyright
© 2001 Cambridge University Press

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References

ARCHER, G., COULITS, N., JINDRA, J. & ROBSON, J. (1985). Eosinophilia, mast cell hyperplasia and antibody production in rats following an intraperitoneal injection of Ascaris cuticle including in-vitro studies of immune eosinophil granule lysis. Pathology 17, 101107.CrossRefGoogle Scholar
BINDSEIL, E. (1967). Larvae of ascarids as the cause of liver lesions in pigs. Nordisk Veterinœr-Medicin 19, 209235.Google Scholar
BUCHWALDER, R., HIEPE, TH., RIBBECK, R. & RUMMEL, CH. (1984). Investigations into the course of experimental Ascaris suum invasions in pigs under field conditions. Helminthology 21, 221229.Google Scholar
CHRISTIE, J. F., FRASER, E. M. & KENNEDY, M. W. (1992). Comparison between the MHC-restricted antibody repertoire to Ascaris antigens in adjuvant-assisted immunization or infection. Parasite Immunology 14, 5973.CrossRefGoogle Scholar
CRANDALL, C. A. & AREAN, V. M. (1965). The protective effect of viable and nonviable Ascaris suum larvae and egg preparations in mice. American Journal of Tropical Medicine and Hygiene 14, 765769.CrossRefGoogle Scholar
DARAWSHE, S., TSAFADYAH, Y. & DANIEL, E. (1987). Quaternary structure of erythrocruorin from the nematode Ascaris suum. Evidence for unsaturated haem-binding sites. The Biochemical Journal 242, 689694.Google Scholar
DAY, R. W. & QUINN, G. P. (1989). Comparisons of treatments after analysis of variance in ecology. Ecological Monographs 59, 433463.CrossRefGoogle Scholar
ERIKSEN, L. (1982). Experimentally induced resistance to Ascaris suum in pigs. Nordisk Veterinœr-Medicin 34, 177187.Google Scholar
ERIKSEN, L., ANDERSEN, S., NIELSEN, K., PEDERSEN, A. & NIELSEN, J. (1980). Experimental Ascaris suum infection in pigs. Serological response, eosinophilia in peripheral blood, occurrence of white spots in the liver and worm recovery from the intestine. Nordisk Veterinœr-Medicin 32, 233242.Google Scholar
ERIKSEN, L., LIND, P., NANSEN, P., ROEPSTORFF, A. & URBAN, J. (1992a). Resistance to Ascaris suum in parasite naïve and naturally exposed growers, finishers and sows. Veterinary Parasitology 41, 137149.Google Scholar
ERIKSEN, L., NANSEN, P., ROEPSTORFF, A., LIND, P. & NILSSON, O. (1992b). Response to repeated inoculations with Ascaris suum eggs in pigs during the fattening period. I. Studies on worm population kinetics. Parasitology Research 78, 241246.Google Scholar
HASWELL-ELKINS, M. R., KENNEDY, M. W., MAIZELS, R. M., ELKINS, D. B. & ANDERSON, R. M. (1989). The antibody recognition profiles of humans naturally infected with Ascaris lumbricoides. Parasite Immunology 11, 615627.CrossRefGoogle Scholar
HELWIGH, A. B., CHRISTENSEN, C. M., ROEPSTORFF, A. & NANSEN, P. (1999). Concurrent Ascaris suum and Oesophagostomum dentatum infections in pigs. Veterinary Parasitology 82, 221234.CrossRefGoogle Scholar
HELWIGH, A. B. & NANSEN, P. (1999). Establishment of Ascaris suum in pigs: development of immunity following a single primary infection. Acta Veterinaria Scandinavica 40, 121132.Google Scholar
HILL, D. E., FETTERER, R. H., ROMANOWSKI, R. D. & URBAN, J. F. (1994). The effect of immunization of pigs with Ascaris suum cuticle components on the development of resistance to parenteral migration during a challenge infection. Veterinary Immunology and Immunopathology 42, 161169.CrossRefGoogle Scholar
JUNGERSEN, G., ERIKSEN, L., ROEPSTORFF, A., LIND, P., MEEUSEN, E. N. T. & NANSEN, P. (1999). Experimental Ascaris suum infections in the pig: protective memory response after three immunizations and effect of intestinal worm population. Parasite Immunology 21, 619630.CrossRefGoogle Scholar
KENNEDY, M. W. (1991). The antibody repertories in nematode infections. In Parasitic Nematodes-Antigens, Membranes and Genes (ed. KENNEDY, M. W.), pp. 219236. Burgess Science Press, Basingstoke, UK.
KENNEDY, M. W. & QURESHI, F. (1986). Stage-specific secreted antigens of the parasitic larval stages of the nematode Ascaris. Immunology 58, 515522.Google Scholar
LAEMMLI, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, London 277, 680685.CrossRefGoogle Scholar
PÉREZ-MARTÍN SERRANO, F., REINA, D., BREÑA, M. & NAVARRETE, I. (1991). Efecto de la climatología sobre la parasitofauna del cerdo ibérico de montanera en el sur de Extremadura (España). In I Congreso Internacional de las Asociaciones Suboccidental – Europeas de Parasitologia (ed. MAS-COMA, S. ESTEBAN, J. G. BARGUES, M. D. VALERO, M. A. & GALÁN-PUCHADES, M. T.), pp. 297. J. Aguilar Press, Valencia.
LUKES, S. (1992). Ascaris suum – vaccination of mice with liposome encapsulated antigen. Veterinary Parasitology 43, 105113.CrossRefGoogle Scholar
MCSHARRY, C., XIA, Y., HOLLAND, C. V. & KENNEDY, M. W. (1999). Natural immunity to Ascaris lumbricoides associated with immunoglobulin E antibody to ABA-1 allergen and inflammation indicators in children. Infection and Immunity 67, 484489.Google Scholar
MCREYNOLDS, L. A., KENNEDY, M. W. & SELKIRK, M. E. (1993). The polyprotein allergens of nematodes. Parasitology Today 9, 403406.CrossRefGoogle Scholar
NANSEN, P. & ROEPSTORFF, A. (1999). Parasitic helminths of the pig: factors influencing transmission and infection levels. International Journal for Parasitology 29, 877891.CrossRefGoogle Scholar
RHODES, M. B., KERALIS, M. B., STAUDINGER, L. A. & BAKER, P. K. (1986). Immunity of swine to Ascaris suum. Veterinary Parasitology 22, 8794.CrossRefGoogle Scholar
RHODES, M. B. & STAUDINGER, L. A. (1983). Antigens in perienteric fluid of Ascaris suum as detected through antibodies in pigs orally inoculated with fully embryonated eggs. Veterinary Parasitology 12, 179186.CrossRefGoogle Scholar
ROEPSTORFF, A., ERIKSEN, L., SLOTVED, H.-C. & NANSEN, P. (1997). Experimental Ascaris suum infection in the pig: worm population kinetics following single inoculations with three doses of infective eggs. Parasitology 115, 443452.CrossRefGoogle Scholar
ROEPSTORFF, A. & JORSAL, S. E. (1989). Prevalence of helminth infections in swine in Denmark. Veterinary Parasitology 33, 231239.CrossRefGoogle Scholar
RONEUS, O. (1966). Studies on the aetiology and pathogenesis of white spots in the liver of pigs. Acta Veterinaria Scandinavica 7 (Suppl. 16), 1112.Google Scholar
SCHWARTZ, B. & ALICATA, J. E. (1963). Ascaris larvae as a cause of liver and lung lesions in swine. Journal of Parasitology 19, 1724.Google Scholar
SERRANO, F., PÉREZ MARTÍN, E., REINA, D. & NAVARRETE, I. (1992). Trichinella strain, pig race and other parasitic infections as factors in the reliability of ELISA for the detection of swine trichinellosis. Parasitology 105, 111115.CrossRefGoogle Scholar
SMITH, H. V. (1991). Immune evasion and immunopathology in Toxocara canis infection. In Parasitic Nematodes-Antigens, Membranes and Genes (ed. KENNEDY, M. W.), pp. 116139. Burgess Science Press, Basingstoke, UK.
STANKIEWICZ, M. & FROE, D. L. (1995). Unabbreviated Ascaris suum immunizing infections of piglets lead to immunosuppression and increased numbers of intestinal parasites. Acta Parasitologica 40, 152155.Google Scholar
STANKIEWICZ, M., JESKA, E. L. & FROE, D. L. (1990). Acquired resistance to migrating larvae of Ascaris suum in young pigs by repeated drug-abbreviated infections. Journal of Parasitology 76, 383388.CrossRefGoogle Scholar
STANKIEWICZ, M., JONAS, W. & FROE, D. L. (1992). Patent infections of Ascaris suum in pigs: effect of previous exposure to multiple, high doses of eggs and various treatment regimes. International Journal for Parasitology 22, 597601.CrossRefGoogle Scholar
STEWART, T., SOUTHERN, L., GIBSON, R. & SIMMONS, L. (1985). Immunization of pigs against Ascaris suum by sequential experimental infections terminated with fenbendazole during larval migration. Veterinary Parasitology 17, 319326.CrossRefGoogle Scholar
STROMBERG, B. E. (1979). IgE and IgG1 antibody production by soluble products of Ascaris suum in the guinea-pig. Immunology 38, 489495.Google Scholar
URBAN, J. F. (1986). The epidemiology and control of swine parasites. Veterinary Clinics of North America – Food Animal Practice 2, 765778.CrossRefGoogle Scholar
URBAN, J. F., ALIZADEH, H. & ROMANOWSKI, R. D. (1988). Ascaris suum: Development of intestinal immunity to infective second-stage larvae in swine. Experimental Parasitology 66, 6677.CrossRefGoogle Scholar
URBAN, J. F. & ROMANOWSKI, R. D. (1985). Ascaris suum: Protective immunity in pigs immunized with products from eggs and larvae. Experimental Parasitology 60, 245254.CrossRefGoogle Scholar
URBAN, J. F. & TROMBA, F. G. (1982). Development of immune responsiveness to Ascaris suum antigens in pigs vaccinated with ultraviolet-attenuated eggs. Veterinary Immunology and Immunopathology 3, 399409.CrossRefGoogle Scholar
WINKFEIN, R. J., PASTERNAK, J., MUDRY, T. & MARTIN, L. H. (1985). Ascaris lumbricoides: characterization of the collagenous components of the adult cuticle. Experimental Parasitology 59, 197203.CrossRefGoogle Scholar