Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-06T07:03:03.815Z Has data issue: false hasContentIssue false

Schistosoma mansoni: dynamics of migration through the vascular system of the mouse

Published online by Cambridge University Press:  06 April 2009

R. A. Wilson
Affiliation:
Department of Biology, University of York, York YO1 5DD
Patricia S. Coulson
Affiliation:
Department of Biology, University of York, York YO1 5DD

Summary

Autoradiography of compressed mouse tissues has been used to estimate the numbers of Se-labelled schistosomula present in different mouse organs. Day 7 parasites extracted from the lungs of donor mice were delivered by injection to the lungs, systemic organs and liver of recipient mice as a discrete pulse. The numbers detected in various locations with time post-injection were then used to analyse the dynamics of intravascular migration. Approximately 98% of cercaria-associated label was lost during the first 14 days of parasite life, two-thirds of this in the first 7 h post-infection. Nevertheless, 99–113% of schistosomula could be detected 30 min post-injection into the locations chosen. The efficiency of the parasite delivery system was 95%. The time required for the number of foci in the lungs to decline to 50%, after injection of parasites via the femoral vein, was 55 h. Adjustment of this data to allow for parasites returning to the lungs after passage round the systemic vasculature gave a value of 30–35 h for the true mean time of lung transit. The distribution of parasites to systemic organs after their exit from the lungs was proportional to the fractional distribution of cardiac output. The probability (P) of a schistosomulum being distributed to splanchnic beds was estimated at 0·32 and its P of being trapped in the hepatic portal distributaries within the liver as 0·72–0·86. On this basis, the entire hepatic portal population of adult schistosomes would be recruited during 2–3 circuits of parasites around the pulmonary-systemic vasculature. The mean transit time of schistosomula through intestinal capillaries was 6·5 h whilst that through other systemic organs combined (muscles, kidneys, brain, etc) was 16 h, considerably more rapid than lung transit. The time taken for schistosomula to pass between organs, in arterial and venous blood, was shown to be less than 30 min in both cases (probably much less).

Type
Research Article
Copyright
Copyright © Cambridge University Press 1986

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

Crabtree, J. E. & Wilson, R. A. (1980). Schistosoma mansoni, a scanning electron microscope study of the developing schistosomulum. Parasitology 81, 553–64.CrossRefGoogle ScholarPubMed
Dean, D. A. & Mangold, B. L. (1984). Autoradiographic analysis of resistance to reinfection with Schistosoma mansoni in mice. Evidence that most worm elimination occurs in the liver. American Journal of Tropical Medicine and Hygiene 33, 97103.CrossRefGoogle ScholarPubMed
Dean, D. A., Mangold, B. L., Georgi, J. R. & Jacobson, R. H. (1984). Comparison of Schistosoma mansoni migration patterns in normal and irradiated cercaria-immunized mice by means of autoradiographic analysis. Evidence that worm elimination occurs after the skin phase in immunised mice. American Journal of Tropical Medicine and Hygiene 33, 8996.CrossRefGoogle Scholar
Georgi, J. R. (1982). Schistosoma mansoni: quantification of skin penetration and early migration by differential external radioassay and autoradiography. Parasitology 84, 263–81.CrossRefGoogle ScholarPubMed
Georgi, J. R., Dean, D. A. & Mangold, B. L. (1983). Schistosoma mansoni: temporal distribution of radioselenium-labelled schistosomula in lungs of mice during the first two weeks of infection. Parasitology 86, 31–6.CrossRefGoogle 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 Tropical Medicine and Hygiene 32, 785–9.CrossRefGoogle ScholarPubMed
Mangold, B. L. & Dean, D. A. (1984). The migration and survival of gamma-irradiated Schistosoma mansoni larvae and the duration of host-parasite contact in relation to the induction of resistance in mice. Parasitology 88, 249–66.CrossRefGoogle Scholar
Mastin, A. J., Bickle, Q. D. & Wilson, R. A. (1983). Schistosoma mansoni: migration and attrition of irradiated and challenge schistosomula in the mouse. Parasitology 87, 87102.CrossRefGoogle ScholarPubMed
Miller, P. & Wilson, R. A. (1978). Migration of the schistosomula of Schistosoma mansoni from skin to lungs. Parasitology 77, 281302.CrossRefGoogle ScholarPubMed
Miller, P. & Wilson, R. A. (1980). Migration of the schistosomula of Schistosoma mansoni from the lungs to the hepatic portal system. Parasitology 80, 267–88.CrossRefGoogle Scholar
Quintana, A., Raczka, E. & Bonaccorsi, A. (1979). Cardiac output distribution measured with radioactive microspheres in the mouse. Pharmacological Research Communications 11, 245–52.CrossRefGoogle ScholarPubMed
Raczka, E., Quintana, A., Poggi, A. & Donati, M. B. (1983). Distribution of cardiac output during development of two metastizing murine tumors. European Journal of Cancer and Clinical Oncology 19, 1021–9.CrossRefGoogle Scholar
Smithers, S. R. & Terry, R. J. (1965). The infection of laboratory hosts with cercariae of Schistosoma mansoni and the recovery of adult worms. Parasitology 55, 695700.CrossRefGoogle ScholarPubMed
Thurlby, P. L. & Trayhurn, P. (1980). Regional blood flow in genetically obese (ob/ob) mice. Pflügers Archives 385, 193201.CrossRefGoogle ScholarPubMed
Wetterlin, S., Aronsen, K. F., Björkman, I. & Ahlgren, I. (1977). Studies on the methods for determination of the distribution of cardiac output in the mouse. Scandinavian Journal of Clinical Laboratory Investigation 37, 451–4.CrossRefGoogle ScholarPubMed
Wheater, P. R. & Wilson, R. A. (1979). Schistosoma mansoni: a histological study of migration in the laboratory mouse. Parasitology 75, 4962.CrossRefGoogle Scholar
Wilson, R. A., Coulson, P. S. & McHugh, S. M. (1983). A significant part of the ‘concomitant immunity’ of mice to Schistosoma mansoni is the consequence of a leaky hepatic portal system, not immune killing. Parasite Immunology 5, 595601.CrossRefGoogle Scholar
Wilson, R. A., Coulson, P. S. & Dixon, B. (1986). Migration of the schistosomula of Schistosoma mansoni in mice vaccinated with radiation-attenuated cercariae, and normal mice: an attempt to identify the timing and site of parasite death. Parasitology 92, 101116.CrossRefGoogle ScholarPubMed
Wilson, R. A., Draskau, T., Miller, P. & Lawson, J. R. (1978). Schistosoma mansoni: the activity and development of the schistosomulum during migration from the skin to the hepatic portal system. Parasitology 77, 5773.CrossRefGoogle Scholar