Hostname: page-component-76fb5796d-qxdb6 Total loading time: 0 Render date: 2024-04-27T03:43:32.060Z Has data issue: false hasContentIssue false
  • English
  • Français

Doubt and certainty about the pathways of invasive juvenile parasites inside hosts

Published online by Cambridge University Press:  07 April 2017

P. A. G. Wilson
P. A. G. Wilson
Affiliation:
Division of Biological Sciences, Institute of Cell, Animal and Population Biology, University of Edinburgh, West Mains Road, Edinburgh EH9 3FT, UK
Get access Rights & Permissions [Opens in a new window]

Summary

It is generally believed that the patterns of in-host migration of the infective stages of most invasive macroparasites of man and domestic animals are matters of established fact. In reality, the textbook treatment of this topic, and much of the experimental approach to it, are a legacy of an uncritical past. With few exceptions the true picture concerning particular host/parasite systems is confused by the acceptance of inadequate criteria of proof. In important instances these bogus ‘proofs’ have been generalized within a suspect inductive framework which employs the basic assumption that all migratory parasites that enter the same portal and travel to the same destination do so by the same route. The discussion of such issues serves as a background to the presentation in detail of a more rigorous conceptual and experimental framework.

Keywords

Helminthparasiteinfectivejuvenilelarvamigrationroutesproofs.
Type
Research Article
Information
Parasitology , Volume 109 , supplement S1: Parasites and behaviour , 1994 , pp. S57 - S67
Copyright
Copyright © Cambridge University Press 1994

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

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 - Occurrence of Strongyloides ratti in the host body] (Abstract). Japanese Journal of Parasitology 13, 317 [in Japanese].Google Scholar
Allen, R. E. ed. (1990). The Concise Oxford Dictionary. 8th Edition. Oxford: Clarendon Press.Google Scholar
Anderson, R. C. (1992). Nematode Parasites of Vertebrates: Their Development and Transmission. Wallingford: C.A.B. International.Google Scholar
Behnke, J. M. (1990 a). Immunity: non-hookworm models. In Hookworm Disease: Current Status and New Directions (ed. Schad, G. A. & Warren, K. S.), pp. 351–380. London: Taylor & Francis.Google Scholar
Behnke, J. M. (1990 b). Laboratory animal models. In Hookworm Disease: Current Status and New Directions (ed. Schad, G. A. & Warren, K. S.), pp. 105–128. London: Taylor & Francis.Google Scholar
Behnke, J. M., Paul, V. & Rajasekariah, G. R. (1986). The growth and migration of Necator americanus following infection of neonatal hamsters. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 146–9.CrossRefGoogle 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 Scholar
Bone, L. W. (1982). Chemotaxis of parasitic nematodes. In Cues That Influence Behavior of Internal Parasites (ed. Bailey, W. S.), pp. 52–62. New Orleans: Agricultural Research Service (Southern Region), U.S. Department of Agriculture.Google Scholar
Chalmers, A. F. (1982). What is this thing called Science? 2nd edn. Milton Keynes: Open University Press.Google Scholar
Croll, N. A. (1977). The location of parasites within their hosts. The behavioural component in the larval migration of Nippostrongylus brasiliensis in tissues of the rat. International Journal for Parasitology 7, 201–4.CrossRefGoogle Scholar
Croll, N. A. & Ma, K. (1978). The location of parasites within their hosts: The passage of Nippostrongylus brasiliensis through the lungs of the laboratory rat. International Journal for Parasitology 8, 289–95.CrossRefGoogle Scholar
Dawkins, J. J. S. (1989). Strongyloides ratti infections in rodents: value and limitations as a model for human strongyloidiasis. In Strongyloidiasis: A Major Roundworm Infection of Man (ed. Grove, D. I.), pp. 287–332. London: Taylor and Francis.Google Scholar
Douvres, F. W., Tromba, F. G. & Malakatis, G. M. (1969). Morphogenesis and migration of Ascaris suum larvae developing to the fourth stage in swine. Journal of Parasitology 55, 689–712.CrossRefGoogle Scholar
Foster, A. O. & Cross, S. X. (1934). The direct development of hookworms after oral infection. American Journal of Tropical Medicine 14, 565–73.Google Scholar
Fülleborn, F. (1914). Untersuchungen über den Infektionsweg bei Strongyloides und Ancylostomen und die Biologie dieser Parasiten. Archiv für Schiffs- und Tropen-Hygiene 18, 182–236 (Festschrift zur Eröffnung des neuen Instituts für Schiffs- und Tropenkrankheiten zu Hamburg. Verfasst von den Mitgliedern des Instituts. pp. 26–80).Google Scholar
Fülleborn, F. (1921). Über die Wanderung von Askaris-und anderen Nematodenlarven im Körper und intrauterine Askarisinfection. Archiv für Schiffs-und Tropen-Hygiene 25, 146–9.Google Scholar
Fülleborn, F. (1925). Über die Durchlässigkeit der Blutkapillaren für Nematodenlarven bzw. für unbewegliche Körper von ähnlicher Dicke, sowie über den Transport solcher Gebilde durch des Flimmerepithel der Luftwege. Archiv für Schiffs- und Tropen-Hygiene 29, 553–652.Google Scholar
Fülleborn, F. & Schilling-Torgau, V. (1911). Untersuchungen über den Infektionsweg bei Strongyloides und Ancylostomen: Vorläufige Mitteilung. Archiv für Schiffs- und Tropen-Hygiene 15, 569–71.Google Scholar
Genta, R. M. & Ward, P. A. (1980). The histopathology of experimental strongyloidiasis. American Journal of Pathology 99, 207–20.Google ScholarPubMed
Harley, J. P. & Gallicchio, v (1971). Trichinella spiralis: migration of larvae in the rat. Experimental Parasitology 30, 11–21.CrossRefGoogle Scholar
Kassai, T., Shnain, A. H., Kadhim, J. K., Altaif, K. I. & Jabbir, M. H. (1972). [Collection of lymph from sheep by cannulation of the thoracic duct and application of the method in hosts infected with Dictyocaulus filaria]. Magyar Allatorvosok Lapja 27, 691–6 [in Hungarian].Google Scholar
Kelley, G. W., Olsen, L. S. & Hoerlein, A. B. (1957). Rate of migration and growth of larval Ascaris suum in baby pigs. Proceedings of the Helminthological Society of Washington 24, 133–6.Google Scholar
Knopf, P. M., Cioli, D., Mangold, B. L. & Dean, D. A. (1986). Migration of Schistosoma mansoni in normal and passively immunised laboratory rats. American Journal of Tropical Medicine and Hygiene 35, 1173–84.CrossRefGoogle Scholar
Looss, A. (1905). Wanderung der Ancylostomum- und Strongyloides larven von der Haut nach dem Darm. Comptes Rendus de 6e Congrès Internationale de Zoologie. Berne, 1904. 225–233.Google Scholar
Looss, A. (1911). The anatomy and life-history of Agchylostoma duodenale Dub. Part II. The development in the free state. Records of the Egyptian Government School of Medicine 4, Cairo.Google Scholar
McLaren, D. J. & Smithers, S. R. (1987). The immune response to schistosomes in experimental hosts. In The Biology of Schistosomes: From Genes to Latrines. (ed. Rollinson, D. & Simpson, A. J. G.), pp. 233–263. London: Academic Press.Google Scholar
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 Tropical Medicine and Hygiene 32, 785–9.CrossRefGoogle Scholar
Mangold, B. L., Dean, D. A., Coulson, P. S. & Wilson, R. A. (1986). Site requirements and kinetics of immune-dependent elimination of intravascularly administered lung-stage schistosomula in mice immunised with highly irradiated cercariae of Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 35, 332–44.CrossRefGoogle Scholar
Martin, H. M. (1926). Studies on the Ascaris lumbricoides. College of Agriculture, University of Nebraska Agricultural Experimental Station Research Bulletin 37 Monograph 78pp.Google Scholar
Mimori, T., Korenaga, M., Chowdhury, 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, 11–27.CrossRefGoogle Scholar
Moqbel, R. & Denham, D. A. (1977). Strongyloides ratti: 1. Parasitological observations on primary and secondary infections in the small intestine of rats. Journal of Helminthology 51, 301–8.CrossRefGoogle Scholar
Murrell, K. D. (1980). Strongyloides ratti: Acquired resistance in the rat to the preintestinal migrating larvae. Experimental Parasitology 50, 417–25.CrossRefGoogle Scholar
Murrell, K. D. (1981). Protective role of immunoglobulin G in immunity to Strongyloides ratti. Journal of Parasitology 67, 167–73.CrossRefGoogle ScholarPubMed
Murrell, K. D. & Graham, C. E. (1983). Shedding of antibody complexes by Strongyloides ratti (Nematoda) larvae. Journal of Parasitology 69, 70–3.CrossRefGoogle Scholar
Nojima, H., Noda, S., Kawanabe, M. & Sato, A. (1987). Larval migration of Strongyloides ratti with reference to esophagus length. Journal of Parasitology 73, 228–30.CrossRefGoogle Scholar
Nolan, T. J. & Katz, F. F. (1981). Transmammary transmission of Strongyloides venezuelensis (Nematoda) in rats. Proceedings of the Helminthological Society of Washington 48, 8–12.Google Scholar
Nwaorgu, C. O. & Connan, R. M. (1980). The migration of Strongyloides papillosus in rabbits following infection by the oral and subcutaneous routes. Journal of Helminthology 54, 223–32.CrossRefGoogle Scholar
Prosser, C. L. (1973). Circulation of body fluids. In Comparative Animal Physiology. 3rd edn, Vol. II. (ed. Prosser, C. L.), pp. 822–856. Philadelphia: Saunders.Google Scholar
Ransom, B. H. & Cram, E. B. (1921). The course of migration of Ascaris larvae. The American Journal of Tropical Medicine 1, 129–60.Google Scholar
Ransom, B. H. & Foster, W. D. (1917). Life history of Ascaris lumbricoides and related forms. [Preliminary note]. Journal of Agricultural Research, Department of Agriculture, Washington 11, 395–8.Google Scholar
Ransom, B. H. & Foster, W. D. (1920). Observations on the life history of Ascaris lumbricoides. United States Department of Agriculture Bulletin 817, 47pp.Google Scholar
Roberts, F. H. S. (1934). The large roundworm of pigs, Ascaris lumbricoides L., 1758: Its life history in Queensland, economic importance and control. Bulletin of the Animal Health Station Yeerongpilly, Queensland, Australia Bulletin 1 Monograph 81pp.Google Scholar
Roberts, T. M. (1982). From receptor to response: prospects for research in behavioural parasitology. In Cues That Influence Behavior of Internal Parasites (ed. Bailey, W. S.), pp. 166–177. Agricultural Research Service (Southern Region), U.S. Department of Agriculture, New Orleans.Google Scholar
Schad, G. A. (1990). Hypobiosis and related phenomena in hookworm infection. In Hookworm Disease: Current Status and New Directions (ed. Schad, G. A. & Warren, K. S.), pp. 71–88. London: Taylor and Francis.Google Scholar
Schad, G. A., Aikens, L. M. & Smith, G. (1989). Strongyloides stercoralis: Is there a canonical migratory route through the host? Journal of Parasitology 75, 740–9.CrossRefGoogle Scholar
Spindler, L. A. (1958). The occurrence of the intestinal threadworms, Strongyloides ratti, in the tissues of rats, following experimental percutaneous infection. Proceedings of the Helminthological Society of Washington 25, 106–11.Google Scholar
Stewart, F. H. (1916). On the life history of Ascaris lumbricoides. British Medical Journal 2, 5–7.CrossRefGoogle Scholar
Stewart, F. H. (1917). On the development of Ascaris lumbricoides Lin. and Ascaris suilla Duj. in the rat and mouse. Parasitology 9, 213–27.CrossRefGoogle Scholar
Stewart, F. H. (1921). On the life history of Ascaris lumbricoides L. Parasitology 13, 37–47.CrossRefGoogle 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
Tanaka, M., Mimori, T., Minematsu, T. & Tada, I. (1989). The acquirement of growth ability for thirdstage larvae of Strongyloides ratti during the headpassage in the rat. International Journal for Parasitology 19, 757–60.CrossRefGoogle Scholar
Tindall, N. R. (1990). Aspects of the Migration of Invasive Parasitic Juvenile Nematodes in the Tissues of Laboratory Rodents. PhD Thesis, Faculty of Science, University of Edinburgh.Google Scholar
Tindall, N. R. & Wilson, P. A. G. (1988). Criteria for a proof of migration routes of immature parasites inside hosts exemplified by studies of Strongyloides ratti in the rat. Parasitology 96, 551–63.CrossRefGoogle Scholar
Tindall, N. R. & Wilson, P. A. G. (1990 a). A basis to extend the proof of migration routes of immature parasites inside hosts: estimated time of arrival of Nippostrongylus brasiliensis and Strongyloides ratti in the gut of the rat. Parasitology 100, 275–80.CrossRefGoogle Scholar
Tindall, N. R. & Wilson, P. A. G. (1990 b). An extended proof of migration routes of immature parasites inside hosts: pathways of Nippostrongylus brasiliensis and Strongyloides ratti in the rat are mutually exclusive. Parasitology 100, 281–8.CrossRefGoogle Scholar
Tindall, N. R. & Wilson, P. A. G. (1990 c). A technique for skin application of exact doses of Nippostrongylus brasiliensis to rats. Journal of Helminthology 64, 15–22.CrossRefGoogle Scholar
Twohy, D. W. (1955). The role of the skin and lungs in the development of Nippostrongylus muris. Journal of Parasitology 41, Suppl, Abstract 110.Google Scholar
Twohy, D. vv. (1956). The early migration and growth of Nippostrongylus muris in the rat. American Journal of Hygiene 63, 165–85.Google Scholar
Warren, E. G. (1971). Observations on the migration and development of Toxocara vitulorum in natural and experimental hosts. International Journal for Parasitology 1, 85–99.CrossRefGoogle Scholar
Wertheim, G. & Lengy, J. (1965). Growth and development of Strongyloides ratti Sandground 1925, in the albino rat. Journal of Parasitology 51, 636–9.CrossRefGoogle Scholar
Wilson, P. A. G. (1983). Roundworm juvenile migration in mammals: the pathways of skin-penetrators reconsidered. In Aspects of Parasitology (ed. Meerovitch, E.), pp. 459–485. Montreal: Institute of Parasitology.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., Cameron, M. & Scott, D. S. (1978 a). Strongyloides ratti in virgin female rats: studies of oestrous cycle effects and general variability. Parasitology 76, 221–7.CrossRefGoogle Scholar
Wilson, P. A. G., Cameron, M. & Scott, D. S. (1978 b ). Patterns of milk transmission of Strongyloides ratti. Parasitology 77, 87–96.CrossRefGoogle ScholarPubMed
Wilson, P. A. G., Gentle, M. & Scott, D. S. (1976 a). Milk-borne infection of rats with Strongyloides ratti and Nippostrongylus brasiliensis. Parasitology 72, 355–60.CrossRefGoogle Scholar
Wilson, P. A. G., Gentle, M. & Scott, D. S. (1976 b). Dynamic determinants of the route of larval Strongyloides ratti in lactating rats and the control of experimental error in quantitative studies of milk transmission of skin-penetrating roundworms. Parasitology 73, 399–406.CrossRefGoogle Scholar
Wilson, P. A. G. & Simpson, N. 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. (1982). Strongyloides ratti: studies of 75Se-labelled larvae of the homogonic strain in female hosts. Parasitology 84, 443–54.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, 79–91.CrossRefGoogle Scholar
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 Scholar
Wilson, R. A. (1987). Cercariae to liver worms: development and migration in the mammalian host. In The Biology of Schistosomes: From Genes to Latrines (ed. Rollinson, D. & Simpson, A. J. G.), pp. 115–146. London: Academic Press.Google Scholar
Wilson, R. A. & Coulson, P. S. (1986). Schistosoma mansoni: dynamics of migration through the vascular system of the mouse. Parasitology 92, 83–100.CrossRefGoogle Scholar
Yokogawa, S. (1922). The development of Heligmosomum muris Yokogawa, a nematode from the intestine of the wild rat. Parasitology 14, 127–66.CrossRefGoogle Scholar