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Criteria for a proof of migration routes of immature parasites inside hosts exemplified by studies of Strongyloides ratti in the rat

Published online by Cambridge University Press:  06 April 2009

N. R. Tindall
Affiliation:
University of Edinburgh, Department of Zoology, West Mains Road, Edinburgh EH9 3JT
P. A. G. Wilson
Affiliation:
University of Edinburgh, Department of Zoology, West Mains Road, Edinburgh EH9 3JT

Summary

The first rigorous proof applicable to the migration pathway of an infective juvenile macroparasite inside its host is presented. Third-stage larvae of a homogonic strain of Strongyloides ratti applied in exact doses of less than 20 to the skin of the flank of young rats were recovered 16–40 h later in the naso-frontal part of the head. The peak proportion of the dose recovered between 20 and 25 h in this site had a mean value of 0·316 ± 0·021 in 48 animals. In 40 other rats infected simultaneously the mean proportion of the dose that reached the small intestine was at least 0·837+0·013. Proof resides in verification of the inequality > 1. With appropriate statistical tests the excess of the sum of the means of these two proportions over unity is shown to have a probability of occurring by chance of 1 in 3·5 × 106. Thus it is effectively certain that the naso-frontal portion of the head is part of at least one pathway taken by this parasite on its way from the skin to the intestine of its host. By suitable protection of the infection site it was confirmed that migration to the head was achieved by an internal route and not as a result of grooming. Larvae were recovered from the cranium in the same rats over the period 15–40 h, but the peak proportion of the dose occurred at 20 h, and < in this location. Whether the cranium is also part of the pathway is therefore still undecided. The significance of this novel analysis in the general context of in-host migration of infective stages is discussed and it is concluded, following its application to data sets from other authors, that the only cases in which proof can be demonstrated are the anterior skull of the rat for S. ratti (present data) and the lung of the same host for Nippostrongylus brasiliensis (Twohy, 1956).

Type
Research Article
Copyright
Copyright © Cambridge University Press 1988

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References

REFERENCE

Abadie, S., (1963). The life cycle of Strongyloides ratti. Journal of Parasitology 49, 241–8.CrossRefGoogle ScholarPubMed
Abe, Y., (1964). [Studies on the intestinal threadworms — Strongyloides — the occurrence of Strongyloides ratti in the host body] (Abstract). Japanese Journal of Parasitology 133, 317 (in Japanese).Google Scholar
Bell, R. G., Adams, L. S., & Gerb, J., (1981). Strongyloides ratti: Dissociation of the rat's protective immunity into systemic and intestinal components. Experimental Parasitology 52, 386–95.CrossRefGoogle ScholarPubMed
Fülleborn, F., (1914). Untersuchungen über den Infektionsweg bei Strongyloides und Ancylostomen und die Biologie dieser Parasiten. Archiv für Schiffs- und Tropenhygiene 18, 182236. (Festschrift zur Eroffnung des neuen Institute für Schiffs- und Tropenkrankenheiten zu Hamburg. Verfasst von Mitgliedern des Instituts, pp. 2680).Google Scholar
Fülleborn, F., & Schilling-Torgau, V., (1911). Untersuchungen über den Infektionsweg bei Strongyloides und Ancylostomen. Vorläufige Mitteilung. Archiv für Schiffs- und Tropenhygiene 15, 569–71.Google Scholar
Genta, R. M., & Ward, P. A., (1980). The histopathology of experimental strongyloidiasis. American Journal of Pathology 99, 207–19.Google ScholarPubMed
Mangold, B. L., & Dean, D. A., (1983). Autoradiographic analysis of Schistosoma mansoni migration from skin to lungs in naive mice. Evidence that most attrition occurs after the skin phase. American Journal of Hygiene 32, 785–9.Google ScholarPubMed
Milton, J. S., & Tsokos, J. O., (1983). Statistical Methods in the Biological and Health Sciences. Auckland, Hamburg, Lisbon, London: McGraw-Hill International.Google Scholar
Mimori, T., Korenaga, M., Chowdhuhy, N., & Tada, I., (1982). Growth and morphological changes of Strongyloides ratti in rats. Japanese Journal of Parasitology 31, 361–8.Google Scholar
Moqbel, R., (1980). Histopathological changes following primary, secondary and repeated infections of rats with Strongyloides ratti, with special reference to tissue eosinophils. Parasite Immunology 2, 1117.CrossRefGoogle Scholar
Murrell, K. D., (1980). Strongyloides ratti: acquired resistance in the rat to preintestinal migrating larvae. Experimental Parasitology 50, 417–25.CrossRefGoogle ScholarPubMed
Schmidt, G. D., & Roberts, L. S., (1985). Foundations of Parasitology, 3rd Edn.Times Mirror/Mosby: St Louis, Toronto, Santa Clara.Google Scholar
Tada, I.. Mimori, T., & Nakai, M., (1979). Migration route of Strongyloides ratti in albino rats. Japanese Journal of Parasitology 28, 219–27.Google Scholar
Twohy, D. W., (1956). The early migration of Nippostrongylus muris in the rat. American Journal of Hygiene 63, 165–85.Google ScholarPubMed
Wertheim, G., & Lengy, J., (1965). Growth and development of Strongyloides ratti Sandground 1925, in the albino rat. Journal of Parasitology 51, 636–9.CrossRefGoogle ScholarPubMed
Wilson, P. A. G., (1983). Roundworm juvenile migration in mammals: the pathways of skinpenetrators reconsidered. In Aspects of Parasitology (ed. Meerovitch, E.), pp. 459–85. Institute of Parasitology, Montreal.Google Scholar
Wilson, P. A. G., (1987). Studies on the effect of contralateral versus ipselateral challenge of rats primed on one side with Strongyloides ratti. Journal of Helminthology 61, 173–8.CrossRefGoogle ScholarPubMed
Wilson, P. A. G., & Simpson, X. E., (1981). Dynamics of infection in rats given low doses of homogonic and heterogonic Strongyloides ratti. Parasitology 83, 459–75.CrossRefGoogle Scholar
Wilson, P. A. G., Simpson, N. E., & Seaton, D. S., (1986). The effect of method of infection on the pathway of juvenile Strongyloides ratti in the host. Journal of Helminthology 60, 7991.CrossRefGoogle ScholarPubMed
Wilson, P. A. G., Steven, G. E., & Simpson, N. E., (1982). Strongyloides ratti (homogonic): the time course of early migration in the generalized host deduced from experiments in lactating rats. Parasitology 85, 533–42.CrossRefGoogle ScholarPubMed
Zamirdin, M., & Wilson, P. A. G., (1974). Strongyloides ratti: relative importance of maternal sources of infection. Parasitology 69, 445–53.CrossRefGoogle ScholarPubMed