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Influence of Toxocara canis infection during pregnancy on offspring resistance towards re-infection

Published online by Cambridge University Press:  23 January 2006

K. REITEROVÁ
Affiliation:
Parasitological Institute of the Slovak Academy of Sciences, Hlinkova 3, 040 01 Koŝice, Slovak Republic
O. TOMASOVICOVÁ
Affiliation:
Parasitological Institute of the Slovak Academy of Sciences, Hlinkova 3, 040 01 Koŝice, Slovak Republic
P. DUBINSKÝ
Affiliation:
Parasitological Institute of the Slovak Academy of Sciences, Hlinkova 3, 040 01 Koŝice, Slovak Republic

Abstract

The impact of Toxocara canis infection of Balb/c mice mothers on the future immune response of their offspring towards reinfection with the same parasite was studied. Two groups of offspring, the first originating from the mothers infected with a single dose of 1000 Toxocara canis eggs and the second from non-infected mothers, were both challenged with 500 T. canis eggs per animal at 6 weeks of age. The proportions of spleen CD4+ and CD8+ T lymphocytes, the level of serum cytokines IFN-γ and IL-5, eosinophilia in peripheral blood, the production of specific antibodies and the number of migrating larvae were monitored. In both groups of offspring, the challenge infection resulted in an increase in CD4+ T-cell subtype in comparison with the non-infected healthy control, although after an initial decline a subsequent increase in CD8+ was observed. The immunoregulation index (CD4+/CD8+) was lower in the group of mice originating from infected mothers throughout the whole experiment compared to the offspring of non-infected mothers as well as in healthy control mice of the same age. In the offspring of infected mothers mainly, a reduced production of IFN-γ and of IL-5, suppressed eosinophilia and a higher level of protective antibodies was detected, compared to the control second group, in which the INF-γ concentration significantly increased after day 42 p.i. In the first group of offspring before challenge, 12·7±2·5 larvae in the brains and 32±2·1 larvae in the muscles transmitted from the infected mothers were detected. There was a significant reduction in larval recovery from brain on days 42 and 49 p.i. (56·7 and 56·8%, respectively), while from muscles in the same time there was a reduction of 46·7 and 39%, respectively, compared to the offspring of non-infected mothers. These results indicate a significant protective memory of immune mechanisms against T. canis induced in offspring of Toxocara-infected mother mice.

Type
Research Article
Copyright
2006 Cambridge University Press

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References

REFERENCES

Abo-Shehada, M. N., Al-Zubaidy, B. A. and Herbert, I. V. ( 1991). Acquired immunity to Toxocara canis infection in mice. Veterinary Parasitology 38, 282298.CrossRefGoogle Scholar
Aldawek, A. M., Levkut, M., Revajova, V. and Dvoroznakova, E. ( 2002). Larval toxocarosis in mice: immunoreactivity after multiple high dose infections. Acta Parasitologica 47, 249254.Google Scholar
Behm, C. A. and Ovington, K. S. ( 2000). The role of eosinophils in parasitic helminth infections: Insights from genetically modified mice. Parasitology Today 16, 202209.CrossRefGoogle Scholar
Bendelac, A., Matzinger, P., Seder, R. A., Paul, W. E. and Schwartz, R. H. ( 1992). Activation events during thymic selection. Journal of Experimental Medicine 175, 731742.CrossRefGoogle Scholar
Brabin, L. and Brabin, B. J. ( 1992). Parasitic infections in women and their consequences. Advances in Parasitology 31, 181.CrossRefGoogle Scholar
Buc, M. ( 1997). Clinical Immunology. VEDA, Press Slovak Academy of Sciences Press, Bratislava.
Carlier, Y. and Truyens, C. ( 1995). Influence of maternal infection on offspring resistance towards parasites. Parasitology Today 11, 9499.CrossRefGoogle Scholar
Cuellar, C., Fenoy, S., Del Aguia, C. and Guillen, J. L. ( 2001). Isotype specific immune response in murine experimental toxocariasis. Memorias do Instituto Oswaldo Cruz, Rio de Janeiro 96, 549553.CrossRefGoogle Scholar
Dent, L. A., Daly, C. M., Mayrhofer, G., Zimmerman, T., Hallett, A., Bignold, L. P., Creaney, J. and Parsons, J. C. ( 1999). Interleukin-5 transgenic mice show enhanced resistance to primary infections with Nippostrongylus brasiliensis but not primary infections with Toxocara canis. Infection and Immunity 67, 989993.Google Scholar
Dvoroznakova, E., Boroskova, Z. and Tomasovicova, O. ( 2002). Immune responses in mice immunized with Toxocara canis antigens. Helminthologia 39, 5966.Google Scholar
Farjat, J. A. B., Minvielle, M. C., Pezzani, B. C. and Niedfeld, G. ( 1995). Relationship between parasitic inoculum and immunological parameters in experimental toxocariasis. Zentralblatt für Bakteriologie – International Journal of Medical Microbiology Virology Parasitology and Infectious Diseases 282, 465473.CrossRefGoogle Scholar
Glickman, L. T. and Magnaval, J. F. ( 1993). Zoonotic roundworm infections. Infectious Disease of North America 7, 717732.Google Scholar
Glickman, L. T., Chaudry, I. U., Costantino, J., Clack, F. B., Cyppes, R. H. and Winslow, L. ( 1981). Pica patterns, toxocariasis, and elevated blood lead in children. American Journal of Tropical Medicine and Hygiene 30, 7780.CrossRefGoogle Scholar
Glickman, L. T. and Schantz, P. M. ( 1981). Epidemiology and pathogenesis of zoonotic toxocariasis. Epidemiology Revue 3, 231250.CrossRefGoogle Scholar
Gon, S., Saito, S., Takeda, Y., Miyata, H., Takatsu, K. and Sendo, F. ( 1997). Apoptosis and in vivo distribution and clearance of eosinophils in normal and Trichinella spiralis-infected rats. Journal of Leukocyte Biology 62, 309317.CrossRefGoogle Scholar
Havasiova-Reiterova, K., Tomasovicova, O. and Dubinsky, P. ( 1995). Effect of various doses of infective Toxocara canis and Toxocara cati eggs on the humoral response and distribution of larvae in mice. Parasitology Research 81, 1317.CrossRefGoogle Scholar
Holland, C. V. and Cox, D. M. ( 2001). Toxocara in the mouse: a model for parasite-altered host behaviour? Journal of Helminthology 75, 125135. DOI: 10.1079/JOH200169.CrossRefGoogle Scholar
Hrckova, G. and Velebny, S. ( 2001). Treatment of Toxocara canis infection in mice with liposome-incorporated benzimidazole carbamates and immunomodulator glucan. Journal of Helminthology 75, 141146. DOI: 10.1079/JOH2001081.CrossRefGoogle Scholar
Kayes, S. G. ( 1997). Human toxocariasis and the visceral larva migrans syndrome: correlative immunopathology. Chemical Immunology 66, 99124.CrossRefGoogle Scholar
Kovarik, J. and Siegrist, C. A. ( 1998). Immunity in early life. Immunology Today 19, 150152.CrossRefGoogle Scholar
Landers, D. V., Bronson, R. A., Pavia, C. S. and Stites, D. P. ( 1991). Immunology of reproduction. In Basic and Clinical Immunology ( ed. Stites, D. P. and Terr, A. I.), pp. 180210. Victoria Publishing, Harvard Funds, San Francisco.
Levkutova, M., Revajova, V., Levkut, M. and Leng, L. ( 1998). Subpopulations of lymphocytes in cattle naturally infected with papillomavirus. Acta Vetinaria Hungarica, 46, 1318.Google Scholar
Machnicka-Rowinska, B., Kolodziej-Sobocinska, M., Dziemian, E., Boroskova, Z. and Dvoroznakova, E. ( 2002). Local and systemic immune response in mice after single and multiple infection with Toxocara canis. Helminthologia 39, 185191.Google Scholar
Okada, K., Fujimoto, K., Kubo, K., Sekiguchi, M. and Sugane, K. ( 1996). Eosinophil chemotactic activity in bronchoalveolar lavage fluid obtained from Toxocara canis-infected rats. Clinical Immunology and Immunopathology 78, 256262.CrossRefGoogle Scholar
Oteifa, N. M., Moustafa, M. A., El-Gozamy, B. R. and Oteifa, N. M. ( 1996). Experimental congenital toxocariasis: effect on foetal future immune response. Journal of Egyptian Society of Parasitology 26, 629638.Google Scholar
Owhashi, M., Arita, H. and Niwaq, A. ( 1998). Production of eosinophil chemotactic factor by CD8+ T-cells in Toxocara canis-infected mice. Parasitology Research 84, 136138.Google Scholar
Pichler, W. J. ( 1997). Regulation of immune response: the TH1/TH2 concept. Swiss Medical Weekly 127, 341348.Google Scholar
Reiterová, K., Tomasovicová, O. and Dubinský, P. ( 2003). Influence of maternal infection on offspring immune response in murine larval toxocariasis. Parasite Immunology 25, 361368.CrossRefGoogle Scholar
Simister, N. E., Story, C. M., Chen, H. L. and Hunt, J. S. ( 1996). An IgG transporting Fc receptor expressed in the syncytiotrophoblast of human placenta. European Journal of Immunology 26, 15271531.CrossRefGoogle Scholar
Snapper, C. M., Finkelman, F. D. and Paul, M. ( 1988). Differential regulation of IgG1 and IgE synthesis by interleukin 4. Journal of Experimental Medicine 167, 183189.CrossRefGoogle Scholar
Takamoto, M., Wang, Z. X., Watanabe, N., Matsuzawa, A., Nariuchi, H. and Sugane, K. ( 1998). Eosinophilia, IgE production, and cytokine production by lung T cells in surface CD4-deficient mutant mice infected with Toxocara canis. Immunology 95, 97104.CrossRefGoogle Scholar
Velebny, S., Tomasovicova, O. and Stpiczińska, R. ( 1992). Pharmacokinetics of 3H-cambendazole in mice in the course of experimental trichinellosis. Helminthologia 29, 207210.Google Scholar