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The development of a mouse model to explore resistance and susceptibility to early Ascaris suum infection

Published online by Cambridge University Press:  06 October 2005

R. LEWIS ,
J. M. BEHNKE ,
P. STAFFORD  and
C. V. HOLLAND
R. LEWIS
Affiliation:
School of Natural Sciences, Department of Zoology, Trinity College, University of Dublin, Dublin 2, Ireland
J. M. BEHNKE
Affiliation:
School of Biology, University of Nottingham, University Park, Nottingham NG7 2RD, UK
P. STAFFORD
Affiliation:
School of Natural Sciences, Department of Zoology, Trinity College, University of Dublin, Dublin 2, Ireland
C. V. HOLLAND
Affiliation:
School of Natural Sciences, Department of Zoology, Trinity College, University of Dublin, Dublin 2, Ireland
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Abstract

Ascaris suum and Ascaris lumbricoides exhibit an over-dispersed frequency distribution in their host populations in both the adult and larval stages. The impact of host factors on this observed distribution is still poorly understood and difficult to investigate in the natural host populations. The use of a mouse model has been supported by the observations that the larval migratory pattern, in this host, mimics the pattern observed in the pig. We explored the extrinsic factors that might affect the quantitative recovery of larvae during this migration in order to standardize a model system facilitating accurate future assessment of host genetic variation on this phase of the infection. In Exp. 1 larvae accumulated in the livers of both C57BL/6j and BALB/c mice up to and including days 4–5 p.i. and then declined in both strains until day 9. Loss of larvae from the livers corresponded to arrival in the lungs and maximum accumulation on day 7 p.i. but recovery was considerably higher in C57BL/6j mice. It was concluded that day 7 recoveries gave the best indication of relative resistance/susceptibility to this parasite. In Exp. 2 A/J, BALB/c, CBA/Ca, C57BL/6j, C3H/HeN, DBA/2, NIH, SJL, and SWR mice were compared. C57BL/6j mice were identified as the most susceptible strain and CBA/Ca mice as having the most contrasting phenotype, but with a similar kinetic pattern of migration. Finally, in Exp. 3, a strong positive correlation between the size of the inoculum and the mean worm recovery from the lungs was found in CBA/Ca and C57BL/6j mice, but the difference between these strains was highly consistent, 66·6–80%, regardless of the initial dose. These results demonstrate that, using our protocols for infection and recovery, between-experiment variation in A. suum worm burdens is minimal, and that C57BL/6j mice are highly susceptible to infection compared to other strains. The mechanistic basis of this susceptibility in relation to the resistance of other strains is unknown, but the possibilities are reviewed.

Keywords

Ascaris suumAscaris lumbricoidesmouse modelpigsC57BL/6jCBA/Casusceptibilitylungsmigration
Type
Research Article
Information
Parasitology , Volume 132 , Issue 2 , February 2006 , pp. 289 - 300
Copyright
2005 Cambridge University Press

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References

REFERENCES

Beck, J. A., Lloyd, S., Hafezparaast, M., Lennon-Pierce, M., Eppig, J. T., Festing, M. F. W. and Fisher, E. M. C. ( 2000). Genealogies of mouse inbred strains. Nature Genetics 24, 23–25.CrossRefGoogle Scholar
Boes, J., Medley, G. F., Eriksen, L., Roepstorff, A. and Nansen, P. ( 1998). Distribution of Ascaris suum in experimentally and naturally infected pigs and comparison with Ascaris lumbricoides infections in humans. Parasitology 177, 589–596.CrossRefGoogle Scholar
Butcher, A. R., Palethorpe, H. M. and Grove, D. I. ( 2002). The susceptibility of inbred mice to infection with Brachylaima cribbi (Digenea: Brachylaimidae). Parasitology International 51, 109–115.CrossRefGoogle Scholar
Cooper, P. J., Chico, M. E., Sandoval, C., Espinel, I., Guevara, A., Kennedy, M. W., Urban, J. F. Jr., Griffin, G. E. and Nutman, T. B. ( 2000). Human infection with Ascaris lumbricoides is associated with a polarised cytokine response. Journal of Infectious Diseases 182, 1207–1213.CrossRefGoogle Scholar
Crompton, D. W. T. ( 2001). Ascaris and ascariasis. Advances in Parasitology 48, 285–375.CrossRefGoogle Scholar
Dawkins, H. J. S., Grove, D. I., Dunsmore, J. D. and Mitchell, G. F. ( 1980). Strongyloides ratti: susceptibility to infection and resistance to reinfection in inbred strains of mice as assessed by excretion of larvae. International Journal for Parasitology 10, 125–129.CrossRefGoogle Scholar
de Souza, J. B. and Riley, E. M. ( 2002). Cerebral malaria: the contribution of studies in animal models to our understanding of immunopathogenesis. Microbes and Infection 4, 291–300.CrossRefGoogle Scholar
Douvres, F. W. and Tromba, F. G. ( 1971). Comparative development of Ascaris suum in rabbits, guinea pigs, mice and swine in 11 days. Proceedings of the Helminthological Society of Washington 38, 246–252.Google Scholar
Eriksen, L. ( 1981). Host-parasite relations of Ascaris suum infection in pigs and mice. Ph.D. thesis. Institute of Internal Medicine, Royal Veterinary and Agriculture University, Copenhagen.
Eriksen, L. ( 1990). Ascaris suum influence of egg density and in vitro development from embyonated egg to infective egg. Acta Veterinaria Scandinavica 31, 489–491.Google Scholar
Holland, C. V. and Boes, J. ( 2002). Distributions and predisposition: people and pigs. In The Geohelminths: Ascaris, Trichuris and Hookworm ( ed. Holland, C. V. and Kennedy, M. W.), pp. 1–24. Kluwer Academic Publishers, Boston/Dordrecht/London.
Johnstone, C., Leventhal, R. and Soulsby, E. J. L. ( 1978). The spin method for recovering tissue larvae and its use in evaluating C57BL/6 mice as a model for the study of resistance to infection with Ascaris suum. Journal of Parasitology 64, 1015–1020.CrossRefGoogle Scholar
Lee, Y. H. and Kasper, L. H. ( 2004). Immune responses of different mouse strains after challenge with equivalent lethal doses of Toxoplasma gondii. Parasite 11, 89–97.CrossRefGoogle Scholar
Loeffler, W. ( 1932). Zur Differentialdiagnose der Lungen-infiltrierungen. II Ueber flüchtige Succedanininfiltrate (mit Eosinophilie). Beiträge zur Klinik der Tuberkulose 79, 368–382.CrossRefGoogle Scholar
Loeffler, W. ( 1956). Transient lung infiltrations with blood eosinophilia. International Archives of Allergy and Applied Immunity 8, 54–59.CrossRefGoogle Scholar
McSharry, C., Xia, Y., Holland, C. V. and Kennedy, M. W. ( 1999). Natural immunity to Ascaris lumbricoides associated with immunoglobulin E antibody to ABA-1 allergen and inflammation indicators in children. Infection and Immunity 67, 484–489.Google Scholar
Mitchell, G. E., Hogarth-Scott, R. S., Edwards, R. D., Lewers, H. M., Cousins, G. and Moore, T. ( 1976). Studies on immune response to parasite antigens in mice. 1. Ascaris suum larvae numbers and antiphosphorylcholine responses in infected mice of various strains and in hypothymic nu/nu mice. International Archives of Allergy and Applied Immunity 52, 64–78.Google Scholar
Mulcahy, G., O'Neill, S., Fanning, J., McCarthy, E. and Sekiya, M. ( 2005). Tissue migration by parasitic helminths- an immunoevasive strategy? Trends in Parasitology 21, 273–277.Google Scholar
Murrell, K. D., Eriksen, L., Nansen, P., Slotved, H.-C. and Rasmussen, T. ( 1997). Ascaris suum: A revision of its early migratory path and implications for human ascariasis. Journal of Parasitology 83, 255–260.CrossRefGoogle Scholar
Norozian-Amiri, S. M. B. and Behnke, J. M. ( 1993). Density-dependent effects on establishment of Necator americanus and Ancylostoma ceylanicum. Journal of Helminthology 67, 151–157.CrossRefGoogle Scholar
Oksanen, A., Eriksen, L., Roepstorff, A., IIsoe, B., Nansen, P. and Lind, P. ( 1990). Embryonation and infectivity of Ascaris suum eggs. A comparison of eggs collected from worm uteri with eggs isolated from pig faeces. Acta Veterinaria Scandinavica 31, 393–398.Google Scholar
O'Lorcain, P. and Holland, C. V. ( 2000). The public health importance of Ascaris lumbricoides. Parasitology 121 (Suppl.) S51–S71.CrossRefGoogle Scholar
Peisong, G., Mao, X.-Q., Enomoto, T., Feng, Z., Gloria-Bottini, F., Bottini, E., Shirakawa, T., Sun, D. and Hopkin, J. M. ( 2004). An asthma-associated genetic variant of STAT6 predicts low burden of Ascaris worm infection. Genes and Immunity 5, 58–62.CrossRefGoogle Scholar
Pemberton, A. D., Knight, P. A., Gamble, J., Colledge, W. H., Lee, J.-K., Pierce, M. and Miller, H. R. P. ( 2004). Innate BALB/c enteric responses to Trichinella spiralis: inducible expression of a novel goblet cell lectin, intelectin-2, and its natural deletion in C57BL/10 mice. Journal of Immunology 173, 1894–1901.CrossRefGoogle Scholar
Rodriguez-Sosa, M., David, J. R., Bojalil, R., Satoskar, A. R. and Terrazas, L. I. ( 2002). Cutting Edge: Susceptibility to the larval stage of the helminth parasite Taenia crassiceps is mediated by Th2 response induced via STAT6 signalling. Journal of Immunology 168, 3135–3139.CrossRefGoogle Scholar
Roepstorff, A., Eriksen, L., Slotved, H.-C. and Nansen, P. ( 1997). Experimental Ascaris suum infection in the pig: worm population kinetics following single inoculations with three doses of infective eggs. Parasitology 115, 443–452.CrossRefGoogle Scholar
Slotved, H.-C. ( 1997). Methods for quantitative recovery of larval and adult stages of nematodes (Ascaris suum and Oesophagostomum dentatum) in pigs and mice. Ph.D. thesis. Danish Centre for Experimental Parasitology, Royal Veterinary and Agricultural University, Copenhagen.
Slotved, H.-C., Eriksen, L., Murrell, K. D. and Nansen, P. ( 1997). Comparison of methods for recovery of Ascaris suum larvae from tissues of mice. International Journal for Parasitology 27, 1305–1310.CrossRefGoogle Scholar
Slotved, H.-C., Eriksen, L., Murrell, K. D. and Nansen, P. ( 1998). Early Ascaris suum migration in mice as a model for pigs. Journal of Parasitology 84, 16–18.CrossRefGoogle Scholar
Sprent, J. F. A. and Chen, H. H. ( 1949). Immunological studies in mice infected with the larvae of Ascaris lumbricoides. I. Criteria of immunity and immunizing effect of isolated worm tissues. Journal of Infectious Disease 84, 111–124.Google Scholar
Taffs, L. F. ( 1965). Immunological studies on experimental infection of guinea pigs and rabbits with Ascaris suum Goeze, 1782. IV. The histopathology of the liver and lung. Journal of Helminthology 39, 297–302.Google Scholar
Vogel, H. and Minning, W. ( 1942). Beiträge zur Klinik der Lungen-ascariasis und zur Frage der flüchtigen, eosinophilen Lungeninfiltrate. Beiträge zur Klinik der Tuberkulose 98, 620–654.CrossRefGoogle Scholar
Williams-Blangero, S., Vandeberg, J. L., Subedi, J., Aivaliotis, M. J., Rai, D. R., Upadhayay, R. P., Jha, B. and Blangero, J. ( 2002). Genes on chromosomes 1 and 13 have significant effects on Ascaris infection. Proceedings of the National Academy of Sciences, USA 99, 5533–5538.CrossRefGoogle Scholar