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Host-specific serological response to Angiostrongylus vasorum infection in red foxes (Vulpes vulpes): implications for parasite epidemiology

Published online by Cambridge University Press:  08 May 2017

NINA GERMITSCH
Affiliation:
Institute of Parasitology, Vetsuisse Faculty, University of Zurich, Winterthurerstrasse 266a, 8057 Zürich, Switzerland
C. M. O. KAPEL
Affiliation:
Section for Organismal Biology, Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark
S. M. THAMSBORG
Affiliation:
Veterinary Parasitology Research Group, Department of Veterinary Disease Biology, Faculty of Health and Medical Sciences, University of Copenhagen, Dyrlaegevej 100, 1871 Frederiksberg C, Denmark
P. DEPLAZES
Affiliation:
Institute of Parasitology, Vetsuisse Faculty, University of Zurich, Winterthurerstrasse 266a, 8057 Zürich, Switzerland
M. SCHNYDER*
Affiliation:
Institute of Parasitology, Vetsuisse Faculty, University of Zurich, Winterthurerstrasse 266a, 8057 Zürich, Switzerland
*
*Corresponding author: Institute of Parasitology, University of Zurich, Winterthurerstrasse 266a, 8057 Zürich, Switzerland. E-mail: [email protected]

Summary

Angiostrongylus vasorum is a cardiovascular nematode increasingly found in dogs and foxes in endemic foci throughout Europe. The present study evaluates ELISAs for detection of circulating antigens and specific antibodies against A. vasorum in foxes. Blood and worm burdens (WBs) from carcasses of 215 Swiss wild red foxes (Vulpes vulpes) and from 75 farmed foxes of different age groups experimentally inoculated once or repeatedly with infective doses of 50, 100 or 200 third-stage larvae were obtained. Antigen detection in the naturally infected Swiss foxes had 91·2% sensitivity and 89·4% specificity, whereas the corresponding figures for antibody detection were 42·2 and 92·0%. The experimentally infected foxes became positive for circulating antigens 5–10 weeks post-inoculation (wpi) and remained highly positive up to 22 wpi, irrespectively of further challenge inoculation. The antibody responses in the same foxes were highly variable: high optical density (OD) values were reached 5–7 wpi in all animals, followed by a decrease in over half of the animals despite accumulating and consequently high WBs resulting in persistent infections. After each challenge, a slight increase of OD values was observed 7 weeks later. We hypothesize that infected foxes develop a variable and non-protective immunity. Such parasite tolerance allows long-term survival of A. vasorum in the animals, and may explain why the parasite appears to spread rapidly within a fox population, an epidemiological dynamic that is evident in many parts of Europe where A. vasorum has been found over the last decades.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2017 

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References

REFERENCES

Al-Sabi, M. N., Deplazes, P., Webster, P., Willesen, J. L., Davidson, R. K. and Kapel, C. M. (2010). PCR detection of Angiostrongylus vasorum in faecal samples of dogs and foxes. Parasitology Research 107, 135140.Google Scholar
Al-Sabi, M. N. S., Kapel, C. M. O., Johansson, A., Espersen, M. C., Koch, J. and Willesen, J. L. (2013). A coprological investigation of gastrointestinal and cardiopulmonary parasites in hunting dogs in Denmark. Veterinary Parasitology 196, 366372.Google Scholar
Caruso, J. P. and Prestwood, A. K. (1988). Immunopathogenesis of canine angiostrongylosis: pulmonary effects of infection. Comparative Immunology, Microbiology & Infectious Diseases 11, 8592.Google Scholar
Chapman, P. S., Boag, A. K., Guitian, J. and Boswood, A. (2004). Angiostrongylus vasorum infection in 23 dogs (1999–2002). Journal of Small Animal Practice 45, 435440.Google Scholar
Deplazes, P., Eckert, J., Mathis, A., von Samson-Himmelstjerna, G. and Zahner, H. (2016). Parasitology in Veterinary Medicine, 1st Edn. Wageningen Academic Publishers, Wageningen, Germany.Google Scholar
Drake, J., Gruntmeir, J., Merritt, H., Allen, L. and Little, S. E. (2015). False negative antigen tests in dogs infected with heartworm and placed on macrocyclic lactone preventives. Parasites & Vectors 8, 15.Google Scholar
Eichenberger, R. M., Lewis, F., Gabriel, S., Dorny, P., Torgerson, P. R. and Deplazes, P. (2013). Multi-test analysis and model-based estimation of the prevalence of Taenia saginata cysticercus infection in naturally infected dairy cows in the absence of a ‘gold standard’ reference test. International Journal for Parasitology 43, 853859.Google Scholar
Eleni, C., Grifoni, G., Di Egidio, A., Meoli, R. and De Liberato, C. (2014). Pathological findings of Angiostrongylus vasorum infection in red foxes (Vulpes vulpes) from Central Italy, with the first report of a disseminated infection in this host species. Parasitology Research 113, 12471250.Google Scholar
Fahrion, A. S., Staebler, S. and Deplazes, P. (2008). Patent Toxocara canis infections in previously exposed and in helminth-free dogs after infection with low numbers of embryonated eggs. Veterinary Parasitology 152, 108115.Google Scholar
Guardone, L., Schnyder, M., Macchioni, F., Deplazes, P. and Magi, M. (2013). Serological detection of circulating Angiostrongylus vasorum antigen and specific antibodies in dogs from central and northern Italy. Veterinary Parasitology 192, 192198.Google Scholar
Guilhon, J. and Cens, B. (1973). Angiostrongylus vasorum (Baillet, 1866): étude biologique et morphologique. Annales de Parasitologie Humaine et Comparée 48, 567596.Google Scholar
Hofer, S., Gloor, S., Muller, U., Mathis, A., Hegglin, D. and Deplazes, P. (2000). High prevalence of Echinococcus multilocularis in urban red foxes (Vulpes vulpes) and voles (Arvicola terrestris) in the city of Zurich, Switzerland. Parasitology 120, 135142.Google Scholar
Houpin, E., McCarthy, G., Ferrand, M., De Waal, T., O'Neill, E. J. and Zintl, A. (2016). Comparison of three methods for the detection of Angiostrongylus vasorum in the final host. Veterinary Parasitology 220, 5458.Google Scholar
Jefferies, R., Shaw, S. E., Viney, M. E. and Morgan, E. R. (2009). Angiostrongylus vasorum from South America and Europe represent distinct lineages. Parasitology 136, 107.Google Scholar
Jeffery, R. A., Lankester, M. W., McGrath, M. J. and Whitney, H. G. (2004). Angiostrongylus vasorum and Crenosoma vulpis in red foxes (Vulpes vulpes) in Newfoundland, Canada. Canadian Journal of Zoology 82, 6674.Google Scholar
Little, S. E., Raymond, M. R., Thomas, J. E., Gruntmeir, J., Hostetler, J. A., Meinkoth, J. H. and Blagburn, B. L. (2014). Heat treatment prior to testing allows detection of antigen of Dirofilaria immitis in feline serum. Parasites & Vectors 7, 1.Google Scholar
Lurati, L., Deplazes, P., Hegglin, D. and Schnyder, M. (2015). Seroepidemiological survey and spatial analysis of the occurrence of Angiostrongylus vasorum in Swiss dogs in relation to biogeographic aspects. Veterinary Parasitology 212, 219226.Google Scholar
Magi, M., Macchioni, F., Dell'Omodarme, M., Prati, M., Calderini, P., Gabrielli, S., Iori, A. and Cancrini, G. (2009). Endoparasites of red fox (Vulpes vulpes) in central Italy. Journal of Wildlife Diseases 45, 881885.Google Scholar
McCarthy, G., Ferrand, M., De Waal, T., Zintl, A., McGrath, G., Byrne, W. and O'Neill, E. (2016). Geographical distribution of Angiostrongylus vasorum in foxes (Vulpes vulpes) in the Republic of Ireland. Parasitology 143, 588593.Google Scholar
Morgan, E. R., Tomlinson, A., Hunter, S., Nichols, T., Roberts, E., Fox, M. T. and Taylor, M. A. (2008). Angiostrongylus vasorum and Eucoleus aerophilus in foxes (Vulpes vulpes) in Great Britain. Veterinary Parasitology 154, 4857.Google Scholar
Oliveira-Júnior, S. D., Barçante, J. M. P., Barçante, T. A., Dias, S. R. C. and Lima, W. S. (2006). Larval output of infected and re-infected dogs with Angiostrongylus vasorum (Baillet, 1866) Kamensky, 1905. Veterinary Parasitology 141, 101106.Google Scholar
Poli, A., Arispici, M., Mancianti, F. and Abramo, F. (1991). Pathology of naturally acquired Angiostrongylus vasorum infection in the red fox (Vulpes vulpes). Angewandte Parasitologie 32, 121.Google Scholar
Rosen, L., Ash, L. R. and Wallace, G. D. (1970). Life history of the canine lungworm Angiostrongylus vasorum. American Journal of Veterinary Research 31, 131141.Google Scholar
Saeed, I., Maddox-Hyttel, C., Monrad, J. and Kapel, C. M. O. (2006). Helminths of red foxes (Vulpes vulpes) in Denmark. Veterinary Parasitology 139, 168179.Google Scholar
Schnyder, M., Fahrion, A., Riond, B., Ossent, P., Webster, P., Kranjc, A., Glaus, T. and Deplazes, P. (2010). Clinical, laboratory and pathological findings in dogs experimentally infected with Angiostrongylus vasorum. Parasitology Research 107, 14711480.Google Scholar
Schnyder, M., Tanner, I., Webster, P., Barutzki, D. and Deplazes, P. (2011). An ELISA for sensitive and specific detection of circulating antigen of Angiostrongylus vasorum in serum samples of naturally and experimentally infected dogs. Veterinary Parasitology 179, 152158.Google Scholar
Schnyder, M., Schaper, R., Bilbrough, G., Morgan, E. R. and Deplazes, P. (2013 a). Seroepidemiological survey for canine angiostrongylosis in dogs from Germany and the UK using combined detection of Angiostrongylus vasorum antigen and specific antibodies. Parasitology 140, 14421450.Google Scholar
Schnyder, M., Schaper, R., Pantchev, N., Kowalska, D., Szwedko, A. and Deplazes, P. (2013 b). Serological detection of circulating Angiostrongylus vasorum antigen- and parasite-specific antibodies in dogs from Poland. Parasitology Research 112, 109117.Google Scholar
Schnyder, M., Stebler, K., Naucke, T. J., Lorentz, S. and Deplazes, P. (2014). Evaluation of a rapid device for serological in-clinic diagnosis of canine angiostrongylosis. Parasites & Vectors 7, 72.Google Scholar
Schnyder, M., Jefferies, R., Schucan, A., Morgan, E. and Deplazes, P. (2015). Comparison of coprological, immunological and molecular methods for the detection of dogs infected with Angiostrongylus vasorum before and after anthelmintic treatment. Parasitology 142, 12701277.Google Scholar
Schucan, A., Schnyder, M., Tanner, I., Barutzki, D., Traversa, D. and Deplazes, P. (2012). Detection of specific antibodies in dogs infected with Angiostrongylus vasorum. Veterinary Parasitology 185, 216224.Google Scholar
Simpson, V. R. (1996). Angiostrongylus vasorum infection in foxes (Vulpes vulpes) in Cornwall. Veterinary Record 139, 443445.Google Scholar
Sréter, T., Széll, Z., Marucci, G., Pozio, E. and Varga, I. (2003). Extraintestinal nematode infections of red foxes (Vulpes vulpes) in Hungary. Veterinary Parasitology 115, 329334.Google Scholar
Taylor, C. S., Garcia Gato, R., Learmount, J., Aziz, N. A., Montgomery, C., Rose, H., Coulthwaite, C. L., McGarry, J. W., Forman, D. W., Allen, S., Wall, R. and Morgan, E. R. (2015). Increased prevalence and geographic spread of the cardiopulmonary nematode Angiostrongylus vasorum in fox populations in Great Britain. Parasitology 142, 11901195.Google Scholar
Webster, P., Monrad, J., Kapel, C. M. O., Kristensen, A. T., Jensen, A. L. and Thamsborg, S. M. (2017). The effect of host age and inoculation dose on infection dynamics of Angiostrongylus vasorum in red foxes (Vulpes vulpes). Parasites & Vectors 10, 4.Google Scholar
Woolsey, I. D., Webster, P., Thamsborg, S. M., Schnyder, M., Monrad, J. and Kapel, C. M. O. (2017). The influence of repeated inoculations with the lung and heartworm nematode Angiostrongylus vasorum in the red fox (Vulpes vulpes) on larval excretion and worm burden. International Journal for Parasitology: Parasites and Wildlife, in press.Google Scholar
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