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Population dynamics of Toxocara canis in pigs receiving a single or multiple infection

Published online by Cambridge University Press:  05 December 2003

K. TAIRA
Affiliation:
Danish Centre for Experimental Parasitology, Department of Veterinary Microbiology, The Royal Veterinary and Agricultural University, Dyrlaegevej 100, DK-1870 Frederiksberg C, Denmark
I. SAEED
Affiliation:
Danish Centre for Experimental Parasitology, Department of Veterinary Microbiology, The Royal Veterinary and Agricultural University, Dyrlaegevej 100, DK-1870 Frederiksberg C, Denmark
P. LIND
Affiliation:
Danish Veterinary Laboratory, Department of Immunology and Biochemistry, Bülowsvej 27, DK-1790 Copenhagen V, Denmark
K. D. MURRELL
Affiliation:
Danish Centre for Experimental Parasitology, Department of Veterinary Microbiology, The Royal Veterinary and Agricultural University, Dyrlaegevej 100, DK-1870 Frederiksberg C, Denmark
C. M. O. KAPEL
Affiliation:
Danish Centre for Experimental Parasitology, Department of Veterinary Microbiology, The Royal Veterinary and Agricultural University, Dyrlaegevej 100, DK-1870 Frederiksberg C, Denmark

Abstract

The population dynamics of Toxocara canis in pigs, and their immune response to a primary and a challenge infection, were studied by parasitological, haematological and serological parameters. Seventy pigs were divided into 4 groups; 35 pigs received a primary infection (group A), 15 pigs received both a primary and a challenge infection (group B), 15 pigs received the challenge infection only (group C), and 5 pigs served as helminth-free controls (group NC). A dose of 50000 eggs was administered for the primary infection (day 0) and a dose of 10000 eggs was given for the challenge infection (day 28). On days 7, 14, 21 and 28 p.i., 5 pigs of group A, and on days 35, 42 and 49 p.i., 5 pigs from each of groups A, B and C were necropsied. Numbers of recovered larvae varied widely among the 5 pigs of each group on all days of necropsy. Toxocara canis larvae were recovered predominantly from the lungs; migration of larvae to other organs or tissues from the lungs was restricted. In group A, the larval burden in the lungs peaked on day 14 p.i., and the larval densities decreased significantly over time. Thereafter, the majority of larvae were recovered from the lungs until the end of the experiment (day 49 p.i.). A few larvae were found in the muscles and brain until day 42 p.i., and 2 larvae were found in the eyes of 2 pigs on day 35 p.i. There was little evidence of protective immunity to a challenge infection in this experiment. The eosinophil levels tended not to increase in pigs receiving a challenge infection, in contrast to the challenge control pigs. The fact that T. canis larvae migrate and persist in the tissues of pigs for more than 1 month suggests a zoonotic risk in infected pigs. The relevance of these data to the population biology and immunology of porcine and human toxocarosis is discussed.

Type
Research Article
Copyright
2003 Cambridge University Press

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References

REFERENCES

ABO-SHEHADA, M. N., AL ZUBAIDY, B. A. & HERBERT, I. V. ( 1984). The migration of larval Toxocara canis in mice. I. Migration through the intestine in primary infections. Veterinary Parasitology 17, 6573.Google Scholar
ALJEBOORI, T. I. & IVEY, H. M. ( 1970). Toxocara canis infection in baboons. I. Antibody, white-cell, and serum-protein responses following infection. The American Society of Tropical Medicine and Hygiene 19, 249254.Google Scholar
ALTMAN, D. G. ( 1991). Practical Statistics for Medical Research. Chapman and Hall, London.
BARDON, R., CUELLAR, C. & GUILLEN, J. L. ( 1994). Larval distribution of Toxocara canis in BALB/c mice at nine weeks and one year post-inoculation. Journal of Helminthology 68, 359360.CrossRefGoogle Scholar
BEAVER, P. C. ( 1966). Zoonoses, with particular reference to parasites of veterinary importance. In Biology of Parasites. Emphasis on Veterinary Parasites ( ed. Soulsby, E. J. L. ), pp. 215227. Academic Press Inc, New York.
BISSERU, B. ( 1969). Studies on the liver, lung, brain and blood of experimental animals infected with Toxocara canis. Journal of Helminthology 43, 267272.CrossRefGoogle Scholar
BOES, J. & HELWIGH, A. B. ( 2000). Animal models of intestinal nematode infections of humans. Parasitology 121 (Suppl.), S97S111.CrossRefGoogle Scholar
BURREN, C. H. ( 1968). Experimental toxocariasis. I. Some observation on the histopathology of the migration of Toxocara canis larvae in the mouse. Zeitschrift für Parasitenkunde 30, 152161.Google Scholar
CHAUDHURI, R. N. & SAHA, T. K. ( 1959). Tropical eosinophilia experiments with Toxocara canis. Lancet 2, 493494.CrossRefGoogle Scholar
DEPLAZES, P. & ECKERT, J. ( 2001). Veterinary aspects of alveolar echinococcosis – a zoonosis of public health significance. Veterinary Parasitology 98, 6587.CrossRefGoogle Scholar
DONE, J. T., RICHARDSON, M. D. & GIBSON, T. E. ( 1960). Experimental visceral larva migrans in the pig. Research in Veterinary Science 1, 133151.Google Scholar
DUNSMORE, J. D., THOMPSON, R. C. A. & BATES, I. A. ( 1983). The accumulation of Toxocara canis larvae in the brains of mice. International Journal for Parasitology 13, 517521.CrossRefGoogle Scholar
EPE, C., SABEL, T., SCHNIEDER, T. & STOYE, M. ( 1994). The behavior and pathogenicity of Toxocara canis larvae in mice of different strains. Parasitology Research 80, 691695.CrossRefGoogle Scholar
GALVIN, T. J. ( 1964). Experimental Toxocara canis infections in chickens and pigeons. Journal of Parasitology 50, 124127.CrossRefGoogle Scholar
GILLESPIE, S. H. ( 1993). The clinical spectrum of human toxocarisasis. In Toxocara and Toxocariasis: Clinical, Epidemiological and Molecular Perspectives ( ed. Lewis, J. W. & Maizels, R. M. ), pp. 5561. Institute of Biology, London.
GLICKMAN, L. T. & SCHANTZ, P. M. ( 1981). Epidemiology and pathogenesis of zoonotic toxocariasis. Epidemiologic Reviews 3, 230250.CrossRefGoogle Scholar
HELWIGH, A. B., LIND, P. & NANSEN, P. ( 1999). Visceral larva migrans: Migratory pattern of Toxocara canis in pigs. International Journal for Parasitology 29, 559565.CrossRefGoogle Scholar
HOLLAND, C. V., O'LORCAIN, P. O., TAYLOR, M. R. H. & KELLY, A. ( 1995). Sero-epidemiology of toxocariasis in school children. Parasitology 110, 535542.CrossRefGoogle Scholar
HOTEZ, P. J. ( 2002). Reducing the global burden of human parasitic disease. Comparative Parasitology 69, 140145.CrossRefGoogle Scholar
KAYES, S. G. ( 1997). Human toxocariasis and the visceral larva migrans syndrome: correlative immunopathology. In Immunopathogenetic Aspects of Disease Induced by Helminth Parasites ( ed. Freedman, D. O.), pp. 99124. Chemical Immunology, Basel, Karger.CrossRef
KAYES, S. G. & OAKS, J. A. ( 1980). Toxocara canis: T lymphocyte function in murine visceral larva migrans and eosinophilia onset. Experimental Parasitology 49, 4755.CrossRefGoogle Scholar
MAGNAVAL, J. F., BERRY, A., FABRE, R. & MORASSIN, B. ( 2001). Eosinophil cationic protein as a possible marker of active human Toxocara infection. Allergy 56, 10961099.CrossRefGoogle Scholar
MAGNAVAL, J. F., GALINDO, V., GLICKMAN, L. T. & CLANET, M. ( 1997). Human Toxocara infection of the central nervous system and neurological disorders: a case-control study. Parasitology 115, 537543.CrossRefGoogle Scholar
MILLER, E. R. & ULLREY, D. E. ( 1987). The pig as a model for human nutrition. Veterinary Immunology and Immunopathology 7, 361382.CrossRefGoogle Scholar
NAGAKURA, K. ( 1989). Toxocariasis possibly caused by ingesting raw chicken. Journal of Infectious Diseases 160, 735736.CrossRefGoogle Scholar
NAKAMURA, S., SOTOYAMA, T., HAYASAKA, S., KAMEYAMA, Y., MARUYAMA, S. & KATSUBE, Y. ( 1991). Parasitism of Toxocara canis larvae in Japanese quails by inoculation of the ascarid eggs. Journal of Veterinary Medical Science 53, 865872.CrossRefGoogle Scholar
OSHIMA, T. ( 1961). Standardization of techniques for infecting mice with Toxocara canis and observations on the normal migration routes of the larvae. Journal of Parasitology 47, 652656.CrossRefGoogle Scholar
PEDERSEN, S. & SAEED, I. ( 2001). Acquired immunity to Trichuris suis infection in pigs. Parasitology 123, 95101.CrossRefGoogle Scholar
ROEPSTORFF, A. & NANSEN, P. ( 1998). The Epidemiology, Diagnosis and Control of Helminth Parasites of Swine. FAO Animal Health Manual No. 3. FAO, Rome, Italy.
RONEUS, O. ( 1966). Studies on the aetiology and pathogenesis of white spots in the liver of pigs. Acta Veterinaria Scandinavica 7, 1112.Google Scholar
SALEM, G. & SCHANTZ, P. ( 1992). Toxocaral visceral larva migrans after ingestion of raw lamb liver. Clinical Infectious Diseases 15, 743744.CrossRefGoogle Scholar
SMITH, M. H. D. & BEAVER, P. C. ( 1953). Persistence and distribution of Toxocara larvae in the tissues of children and mice. Pediatrics 12, 491497.Google Scholar
SOMMERFELT, I. E., SANTILLAN, G., LOPEZ, C., RIBICICH, M. & FRANCO, A. J. ( 2001). Immunological and hematological response in experimental Toxocara canis-infected pigs. Veterinary Parasitology 96, 127134.CrossRefGoogle Scholar
SPRENT, J. F. A. ( 1952). On the migratory behavior of the larvae of various Ascaris species in white mice. I. Distribution of larvae in tissues. Journal of Infectious Diseases 90, 165176.Google Scholar
STURCHLER, D., WEISS, N. & GASSNER, M. ( 1990). Transmission of toxocariasis. Journal of Infectious Diseases 162, 571.CrossRefGoogle Scholar
TAIRA, K., SAEED, I. & KAPEL, C. M. O. ( 2002). Dose-dependent egg excretion in foxes (Vulpes vulpes) after a single infection with Toxocara canis eggs. Parasitology Research 88, 941943.CrossRefGoogle Scholar
WILLINGHAM, A. L. & HURST, M. ( 1996). The pig as a unique host model for Schistosoma japonicum infection. Parasitology Today 12, 132134.CrossRefGoogle Scholar
WILLINGHAM, A. L., OCKENS, N. W., KAPEL, C. M. O. & MONRAD, J. ( 1996). A helminthological survey of wild red foxes (Vulpes vulpes) from the metropolitan area of Copenhagen. Journal of Helminthology 70, 259263.CrossRefGoogle Scholar