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The relationship between IgA activity against 4th-stage larvae and density-dependent effects on the number of 4th-stage larvae of Teladorsagia circumcincta in naturally infected sheep

Published online by Cambridge University Press:  23 August 2004

M. J. STEAR
Affiliation:
Department of Veterinary Clinical Studies, Institute of Comparative Medicine, University of Glasgow Veterinary School, Bearsden Road, Glasgow G61 1QH, Scotland, UK
K. BAIRDEN
Affiliation:
Department of Veterinary Clinical Studies, Institute of Comparative Medicine, University of Glasgow Veterinary School, Bearsden Road, Glasgow G61 1QH, Scotland, UK
G. T. INNOCENT
Affiliation:
Department of Veterinary Clinical Studies, Institute of Comparative Medicine, University of Glasgow Veterinary School, Bearsden Road, Glasgow G61 1QH, Scotland, UK
S. MITCHELL
Affiliation:
Department of Veterinary Clinical Studies, Institute of Comparative Medicine, University of Glasgow Veterinary School, Bearsden Road, Glasgow G61 1QH, Scotland, UK
S. STRAIN
Affiliation:
Department of Veterinary Clinical Studies, Institute of Comparative Medicine, University of Glasgow Veterinary School, Bearsden Road, Glasgow G61 1QH, Scotland, UK
S. C. BISHOP
Affiliation:
Roslin Institute (Edinburgh), Roslin, Midlothian EH25 9PS, Scotland, UK

Abstract

The number of Teladorsagia circumcincta 4th-stage larvae in naturally infected lambs from a single farm varied among lambs and among different years. Within each year the distribution of 4th-stage larvae among lambs was similar to that expected from a negative binomial distribution. The ratio of 4th-stage larvae to adult T. circumcincta was low in two years with a low mean intensity of infection but high in two years with a higher mean intensity of infection. The negative binomial distribution is defined by the mean and by k, a parameter that measures dispersion; k was low when mean infection intensity was low but higher when mean infection intensity was high. As k is an inverse index of overdispersion this indicated that the distribution of 4th-stage larvae was more overdispersed at low levels of infection. In a combined analysis, the number of adult T. circumcincta and the plasma IgA activity against 4th-stage larvae were both associated with increased numbers of 4th-stage larvae. There was a statistical interaction between the number of adults and IgA activity that moderated their combined effect.

Type
Research Article
Copyright
© 2004 Cambridge University Press

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References

REFERENCES

ANDERSON, R. M. & MICHEL, J. F. ( 1977). Density-dependent survival in populations of Ostertagia ostertagi. International Journal for Parasitology 7, 321329.CrossRefGoogle Scholar
ARMOUR, J. & BRUCE, R. G. ( 1974). Inhibited development in Ostertagia ostertagi infections – a diapause phenomenon in a nematode. Parasitology 69, 161174.CrossRefGoogle Scholar
ARMOUR, J. & COOP, R. L. ( 1991). Pathogenesis and control of gastrointestinal helminthiasis. In Diseases of Sheep ( ed. Martin, W. B. & Aitken, I. D. ), pp. 122130. Blackwell Scientific Publications, Oxford.
ARMOUR, J., JARRETT, W. F. H. & JENNINGS, F. W. ( 1966). Experimental Ostertagia circumcincta infections in sheep: development and pathogenesis of a single infection. American Journal of Veterinary Research 27, 12671278.Google Scholar
BARGER, I. A. ( 1985). The statistical distribution of trichostrongylid nematodes in grazing lambs. International Journal for Parasitology 15, 645649.CrossRefGoogle Scholar
BLISS, C. I. & FISHER, R. A. ( 1953). Fitting the negative binomial distribution to biological data. Biometrics 9, 176200.CrossRefGoogle Scholar
BORGSTEEDE, F. H. M. & EYSKER, M. ( 1987). Strains of cattle parasites in the Netherlands with different propensities for inhibited development. Veterinary Parasitology 24, 93101.CrossRefGoogle Scholar
DONALD, A. D. ( 1968). Population studies on the infective stage of some nematode parasites of sheep. III. The distribution of strongyloid egg output in flocks of sheep. Parasitology 58, 951960.CrossRefGoogle Scholar
DUNSMORE, J. D. ( 1960). Retarded development of Ostertagia species in sheep. Nature, London 186, 986987.CrossRefGoogle Scholar
DUNSMORE, J. D. ( 1961). Effect of whole-body irradiation and cortisone on the development of Ostertagia species in sheep. Nature, London 192, 139140.CrossRefGoogle Scholar
EFRON, B. & TIBSHIRANI, R. J. ( 1993). An Introduction to the Bootstrap. Chapman and Hall, London.CrossRef
EYSKER, M. ( 1997). Some aspects of inhibited development of trichostrongylids in ruminants. Veterinary Parasitology 72, 265283.CrossRefGoogle Scholar
FINKELMAN, F. D. & URBAN, J. F. ( 2001). The other side of the coin: the protective role of the T(H)2 cytokines. Journal of Allergy and Clinical Immunology 107, 772780.CrossRefGoogle Scholar
GRENCIS, R. K. ( 1997). Th2-mediated host protective immunity to intestinal nematode infections. Philosophical Transactions of the Royal Society of London, Series B 352, 13771384.CrossRefGoogle Scholar
GRENFELL, B. T., WILSON, K., ISHAM, V. S., BOYD, H. E. G. & DIETZ, K. ( 1995). Modelling patterns of parasite aggregation in natural populations: trichostrongylid nematode–ruminant interactions as a case study. Parasitology 111, S135S151.CrossRefGoogle Scholar
HUNTER, G. C. & QUENOUILLE, M. H. ( 1952). A statistical examination of the worm egg count sampling technique for sheep. Journal of Helminthology 26, 157170.CrossRefGoogle Scholar
McCULLAGH, P. & NELDER, J. A. ( 1989). Generalized Linear Models, 2nd Edn. Chapman and Hall, London.
MES, T. H. M. ( 2003). Technical variability and required sample size of helminth egg isolation procedures. Veterinary Parasitology 115, 311320.CrossRefGoogle Scholar
PATERSON, S. & VINEY, M. E. ( 2002). Host immune responses are necessary for density dependence in nematode infections. Parasitology 125, 283292.CrossRefGoogle Scholar
ROBERTS, J. L. & SWAN, R. A. ( 1982). Quantitative studies of ovine haemonchosis. 3. The interpretation and diagnostic significance of the changes in serial egg counts of Haemonchus contortus in a sheep flock. Veterinary Parasitology 9, 211216.Google Scholar
SINSKI, E., BAIRDEN, K., DUNCAN, J. L., EISLER, M. C., HOLMES, P. H., McKELLAR, Q. A., MURRAY, M. & STEAR, M. J. ( 1995). Local and plasma antibody-responses to the parasitic larval stages of the abomasal nematode Ostertagia circumcincta. Veterinary Parasitology 59, 107118.CrossRefGoogle Scholar
SMITH, W. D., JACKSON, F., JACKSON, E. & WILLIAMS, J. ( 1985). Age immunity to Ostertagia circumcincta: comparison of the local immune responses of 4 1/2 and 10 month-old lambs. Journal of Comparative Pathology 95, 235245.CrossRefGoogle Scholar
SMITH, W. D., JACKSON, F., JACKSON, E., WILLIAMS, J. & MILLER, H. R. P. ( 1984). Manifestations of resistance to ovine ostertagiasis associated with immunological responses in the gastric lymph. Journal of Comparative Pathology 94, 591601.CrossRefGoogle Scholar
STEAR, M. J., BAIRDEN, K., BISHOP, S. C., GETTINBY, G., McKELLAR, Q. A., PARK, M., STRAIN, S. A. J. & WALLACE, D. S. ( 1998). The processes influencing the distribution of parasitic nematodes among naturally infected lambs. Parasitology 117, 165171.CrossRefGoogle Scholar
STEAR, M. J., BAIRDEN, K., DUNCAN, J. L., GETTINBY, G., McKELLAR, Q. A., MURRAY, M. & WALLACE, D. S. ( 1995 a). The distribution of faecal nematode egg counts in Scottish Blackface lambs following natural, predominantly Ostertagia circumcincta infection. Parasitology 110, 573581.Google Scholar
STEAR, M. J., BISHOP, S. C., DOLIGALSKA, M., DUNCAN, J. L., HOLMES, P. H., IRVINE, J., McCRIRIE, L., McKELLAR, Q. A., SINSKI, E. & MURRAY, M. ( 1995 b). Regulation of egg production, worm burden, worm length and worm fecundity by host responses in sheep infected with Ostertagia circumcincta. Parasite Immunology 17, 643652.Google Scholar
STEAR, M. J., PARK, M. & BISHOP, S. C. ( 1996). The key components of resistance to Ostertagia circumcincta in lambs. Parasitology Today 12, 438441.CrossRefGoogle Scholar
STRAIN, S. A. J., BISHOP, S. C., HENDERSON, N. G., KERR, A., McKELLAR, Q. A., MITCHELL, S. & STEAR, M. J. ( 2002). The genetic control of IgA activity against Teladorsagia circumcincta and its association with parasite resistance in naturally infected sheep. Parasitology 124, 545552.CrossRefGoogle Scholar
TAYLOR, L. R. ( 1961). Aggregation, variance and the mean. Nature, London 189, 732735.CrossRefGoogle Scholar
URQUHART, G. M., ARMOUR, J., DUNCAN, J. L., DUNN, A. M. & JENNINGS, F. W. ( 1987). Veterinary Parasitology. Longman Scientific and Technical, Avon.
VAN DE VEN, R. & WEBER, N. ( 1999). On the asymptotic behaviour of estimators of the shape parameter of the negative binomial distribution. ISI 99 52nd Session. 419–420. In Bulletin of the International Statistical Institute, Edita Ltd, Helsinki.
WILSON, K. & GRENFELL, B. T. ( 1997). Generalized linear modelling for parasitologists. Parasitology Today 13, 3338.CrossRefGoogle Scholar