Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-28T17:45:22.622Z Has data issue: false hasContentIssue false

Death of schistosome cercariae during penetration of the skin

I. Penetration of bird skin by Austrobilharzia terrigalensis

Published online by Cambridge University Press:  06 April 2009

S. L. Rai
Affiliation:
Department of Zoology, The Australian National University, Canberra, A.C.T., Australia
J. A. Clegg
Affiliation:
Department of Zoology, The Australian National University, Canberra, A.C.T., Australia

Extract

The seagull, a natural host of Austrobilharzia terrigalensis, was infected with cercariae through a small area of breast skin; 40% of the schistosomula recovered from the skin shortly afterwards were dead. In budgerigar skin 29% of the schistosomula were dead, but mortality in the skin of ducklings was much higher (85%). The budgerigar is a useful laboratory host for this schistosome, but ducklings are completely resistant to experimental infection mainly because of the barrier effect of the skin.

Rapid recovery of schistosomula from budgerigar skin established that the majority of deaths occurred during the first 15 min after application of cercariae. In sections of skin fixed after 10 min nearly all the schistosomula were in the epidermis between the narrow stratum corneum and the living cells of the Malpighian layer. In seagull and budgerigar skin most schistosomula succeeded in crossing the Malpighian layer in the next 5 min, but in ducklings nearly all schistosomula completely failed to penetrate this layer.

In vitro experiments in which cercariae were allowed to penetrate through several layers of dead epidermis, isolated from dried budgerigar skin, into balanced saline, showed that schistosomula are not killed by host cells or a soluble toxic substance. The possibility that the epidermis contains an insoluble toxic substance could not be excluded.

The proportion of schistosomula which died during penetration of dead epidermis was related to the number of layers in the barrier, suggesting that schistosomula may die owing to exhaustion caused by the intense activity of penetration.

About 30% of the glycogen reserves of cercariae were utilized during penetration of budgerigar skin. In dead schistosomula the glycogen reserve had been reduced by 80%, but the significance of this observation is uncertain because much of the glycogen may have been autolysed after death of the schistosomula. Exposure of cercariae to glucose before penetration did not affect the proportion which died in the skin.

Schistosomula adapt to the osmotic pressure in the skin, which is one-third that of sea water, and 30 min after penetration they are rapidly killed if returned to sea water. This process of adaptation is not related to mortality of schistosomula during penetration of the skin.

We wish to acknowledge the expert technical assistance of Mrs J. Morgan. This investigation was supported in part by research grant AI-04707 from the National Institute of Allergy and Infectious Diseases, United States Public Health Service.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1968

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

Baker, J. R. (1946). The histochemical recognition of lipine. Q. Jl microsc. Sci. 87, 441–70.Google ScholarPubMed
Balmain, J. H., Biggers, J. D. & Claringbold, P. J. (1956). Micro-method for the estimation of glycogen in the genital organs of the mouse. Aust. J. biol. Sci. 9, 139–46.CrossRefGoogle Scholar
Batten, P. J. (1956). The histopathology of swimmer's itch. I. The skin lesions of Schistoso-matium douthitti and Gigantobilharzia huronensis in the unsensitized mouse. Am. J. Path. 32, 363–77.Google ScholarPubMed
Bearup, A. J. (1956). Life cycle of Austrobilharzia terrigalensis Johnston, 1917. Parasitology 46, 470–9.CrossRefGoogle ScholarPubMed
Cheng, T. C. & Snyder, R. W. (1962). Studies on host-parasite relationships between larval trematodes and their hosts. I. A review. II. The utilization of the host's glycogen by the intramolluscan larvae of Glythelmins pennsylvaniensis Cheng, and associated phenomena. Trans. Am. microsc. Soc. 81, 209–28.CrossRefGoogle Scholar
Clegg, J. A. (1965). In vitro cultivation of Schistosoma mansoni. Expl Parasit. 16, 133–47.CrossRefGoogle ScholarPubMed
Clegg, J. A. & Smithers, S. R. (1967). Death of schistosome cercariae during penetration of the skin. II. Penetration of mammalian skin by Schistosoma mansoni. Parasitology. 58, 111–28.CrossRefGoogle Scholar
Coutinho-Abath, J. O. & Jampolsky, R. (1957). Comportamento das cercarias de Schisto-soma mansoni na infectacao experimental de animais refratarios. I. Histopatologia das reacoes cutaneas observadas no pombo domestico (Columba livia domestica). Anais Soc. Biol. Pernamb. 15, 93125.Google Scholar
Ewers, W. H. (1965). The incidence of larval trematodes in adults of Velacumantus australis (Quoy and Gaimard) (Gasteropoda: Potamididae). J. Helminth. 39, 110.CrossRefGoogle ScholarPubMed
Ginetsinskaia, T. (1960). Glycogen in the body of cercariae and the dependence of its distribution upon the peculiarities of their biology. Dokl. Akad. Nauk. SSSR. 135, 1012–15. (In Russian.)Google Scholar
Ginetsinskaia, T. A. & Dobrovolskii, A. A. (1962). Glycogen and fat at various stages of the life cycles of trematodes. II. Biological significance of glycogen and fat. Vest. leningr. gos. Univ. 3, 2333. (In Russian.)Google Scholar
McFarlane, W. V. (1952). Schistosome dermatitis in Australia. Med. J. Aust. (1952), pp. 669–72.CrossRefGoogle Scholar
Medawar, P. B. (1941). Sheets of pure epidermal epithelium from human skin. Nature, Lond. 148, 783.CrossRefGoogle Scholar
Olivier, L. (1953). Observations on the migration of avian schistosomes in mammals previously unexposed to cercariae. J. Parasit. 39, 237–46.CrossRefGoogle ScholarPubMed
Pearse, A. G. E. (1961). Histochemistry: Theoretical and Applied. 2nd ed.London: J. and A. Churchill Ltd.Google Scholar
Rai, S. L. (1966). Biology of Austrobilharzia terrigalensis Johnston, 1917 (Trematoda: Schistosomatidae). Ph.D. Thesis, The Australian National University.Google Scholar
Schultz, H. E., Schmidtberger, R. & Haupt, H. (1958). Untersuchungen über die gebun-denen Kohlenhydrate in isolierten Plasma Proteiden. Biochem. Z. 329, 490507.Google Scholar
Standen, O. D. (1951). Some observations upon the maintenance of Australorbis glabratus in the laboratory. Ann. trop. Med. Parasit. 45, 80–3.CrossRefGoogle ScholarPubMed
Stirewalt, M. A. (1963 a). Seminar on immunity to parasitic helminths. IV. Schistosome infections. Expl Parasit. 13, 1844.CrossRefGoogle ScholarPubMed
Stirewalt, M. A. (1963 b). Chemical biology of secretions of larval helminths. Ann. N.Y. Acad. Sci. 113, 3653.CrossRefGoogle ScholarPubMed
Stirewalt, M. A. (1963 c). Cercaria vs. schistosomule (Schistosoma mansoni): Absence of pericercarial envelope in vivo and the early physiological and histological metamorphosis of the parasite. Expl Parasit. 13, 395406.CrossRefGoogle ScholarPubMed
Stirewalt, M. A. & Kruidenier, F. J. (1961). Activity of the acetabular secretory apparatus of cercariae of Schistosoma mansoni under experimental conditions. Expl Parasit. 11, 191211.CrossRefGoogle ScholarPubMed
Szabó, T. (1955). A modification of the technique of ‘skin-splitting’ with trypsin. J. Path. Bact. 70, 545.CrossRefGoogle ScholarPubMed