Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-28T01:18:23.589Z Has data issue: false hasContentIssue false
  • English
  • Français

Increased prevalence and geographic spread of the cardiopulmonary nematode Angiostrongylus vasorum in fox populations in Great Britain

Published online by Cambridge University Press:  01 June 2015

C. S. TAYLOR ,
R. GARCIA GATO ,
J. LEARMOUNT ,
N. A. AZIZ ,
C. MONTGOMERY ,
H. ROSE ,
C. L. COULTHWAITE ,
J. W. MCGARRY ,
D. W. FORMAN  and
S. ALLEN
...Show all authors
C. S. TAYLOR
Affiliation:
Veterinary Parasitology & Ecology Group, University of Bristol, School of Biological Sciences, Bristol Life Sciences Building, 24, Tyndall Avenue, Bristol BS8 1TQ, UK
R. GARCIA GATO
Affiliation:
Animal and Plant Health Agency, Sand Hutton, York, North Yorkshire YO411LZ, UK
J. LEARMOUNT
Affiliation:
Animal and Plant Health Agency, Sand Hutton, York, North Yorkshire YO411LZ, UK
N. A. AZIZ
Affiliation:
Veterinary Parasitology & Ecology Group, University of Bristol, School of Biological Sciences, Bristol Life Sciences Building, 24, Tyndall Avenue, Bristol BS8 1TQ, UK Faculty of Bioresource and Food Industry, Universiti Sultan Zainal Abidin, School of Animal Sciences, Tembila Campus, 22200 Besut, Terengganu, Malaysia
C. MONTGOMERY
Affiliation:
Veterinary Parasitology & Ecology Group, University of Bristol, School of Biological Sciences, Bristol Life Sciences Building, 24, Tyndall Avenue, Bristol BS8 1TQ, UK
H. ROSE
Affiliation:
Veterinary Parasitology & Ecology Group, University of Bristol, School of Biological Sciences, Bristol Life Sciences Building, 24, Tyndall Avenue, Bristol BS8 1TQ, UK
C. L. COULTHWAITE
Affiliation:
School of Veterinary Science, University of Liverpool, Great Newton Street, Liverpool L3 5RP, UK
J. W. MCGARRY
Affiliation:
School of Veterinary Science, University of Liverpool, Great Newton Street, Liverpool L3 5RP, UK
D. W. FORMAN
Affiliation:
Swansea Ecology Research Team, Department of Biosciences, Swansea University, Singleton Park, Swansea SA2 8PP, UK
S. ALLEN
Affiliation:
Swansea Ecology Research Team, Department of Biosciences, Swansea University, Singleton Park, Swansea SA2 8PP, UK
R. WALL
Affiliation:
Veterinary Parasitology & Ecology Group, University of Bristol, School of Biological Sciences, Bristol Life Sciences Building, 24, Tyndall Avenue, Bristol BS8 1TQ, UK
E. R. MORGAN*
Affiliation:
Veterinary Parasitology & Ecology Group, University of Bristol, School of Biological Sciences, Bristol Life Sciences Building, 24, Tyndall Avenue, Bristol BS8 1TQ, UK
*
* Corresponding author. Veterinary Parasitology & Ecology Group, University of Bristol, School of Biological Sciences, Bristol Life Sciences Building, 24, Tyndall Avenue, Bristol BS8 1TQ, UK. E-mail: eric.morgan@bristol.ac.uk
Get access Rights & Permissions [Opens in a new window]

Summary

The nematode Angiostrongylus vasorum is becoming more widely recorded globally, and is of increasing concern as a cause of disease in dogs. Apparent geographic spread is difficult to confirm due to a lack of standardized disease recording systems, increasing awareness among veterinary clinicians, and recent improvements in diagnostic technologies. This study examines the hypothesis that A. vasorum has spread in recent years by repeating the methods of a previous survey of the fox population. The hearts and lungs of 442 foxes from across Great Britain were collected and examined by dissection and flushing of the pulmonary circulation and microscopic inspection of tracheal scrapes. Sampling and parasite extraction methods were identical to an earlier survey in 2005 to ensure comparability. Prevalence of A. vasorum was 18·3% (exact binomial confidence bounds 14·9–22·3), compared with 7·3% previously (5·3–9·9, n = 546), and had increased significantly in most regions, e.g. 7·4% in the Northern UK (previously zero) and 50·8% in the south-east (previously 23·2%). Other nematodes identified were Crenosoma vulpis (prevalence 10·8%, CI 8·1–14·2) and Eucoleus aerophilus (31·6%, CI 27·3–36·2). These data support the proposal that A. vasorum has increased in prevalence and has spread geographically in Great Britain.

Keywords

angiostrongylosisepidemiologydistributionclimatehelminthparasitewildlife diseasecanine
Type
Research Article
Information
Parasitology , Volume 142 , Issue 9 , August 2015 , pp. 1190 - 1195
Check for updates
Copyright
Copyright © Cambridge University Press 2015 

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

Anonymous (2007). Consultation on Working Towards a Wildlife Health Strategy. Department for Environment, Food and Rural Affairs, UK, 37 pp.Google Scholar
Balastrieri, A., Remonti, L., Ferrari, N., Ferrari, A., Lo Valvo, T. and Robetto, S. (2006). Sarcoptic mange in wild carnivores and its co-occurrence with parasitic helminths in the Western Italian Alps. European Journal of Wildlife Research 52, 196–201.CrossRefGoogle Scholar
Chapman, P., Boag, A. K., Guitan, J. and Boswood, A. (2004). Angiostrongylus vasorum infection in 23 dogs (1999–2002). Journal of Small Animal Practice 45, 435–440.Google Scholar
Chomel, B. B., Belotto, A. and Meslin, F. X. (2007). Wildlife, exotic pets and emerging zoonoses. Emerging Infectious Diseases 13, 6–11.Google Scholar
Cobb, M. A. and Fisher, M. A. (1990). Angiostrongylus vasorum: transmission in south east England. Veterinary Record 121, 529.Google Scholar
Conboy, G. A. (2011). Canine angiostrongylosis: the French heartworm: an emerging threat in North America. Veterinary Parasitology 176, 382–389.CrossRefGoogle ScholarPubMed
Daszak, P., Cunningham, A. A. and Hyatt, A. D. (2000). Emerging infectious diseases of wildlife: threats to biodiversity and human health. Science 287, 443–449.CrossRefGoogle ScholarPubMed
Demiaszkiewicz, A. W., Pyziel, A. M., Kuligowska, I. and Lachowicz, J. (2014). The first report of Angiostrongylus vasorum (Nematoda; Metastrongyloidea) in Poland, in red foxes (Vulpes vulpes). Acta Parasitologica 59, 758–762.Google Scholar
Deplazes, P., Hegglin, D., Gloor, S. and Romig, T. (2004). Wilderness in the city: the urbanization of Echinococcus multilocularis . Trends in Parasitology 20, 77–84.CrossRefGoogle ScholarPubMed
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, 1247–1250.CrossRefGoogle ScholarPubMed
Elsheikha, H. M., Holmes, S. A., Wright, I., Morgan, E. R. and Lacher, D. W. (2014). Recent advances in the epidemiology, clinical and diagnostic features, and control of canine cardio-pulmonary angiostrongylosis. Veterinary Research 45, 92.Google Scholar
Franssen, F., Nijsse, R., Mulder, J., Cremers, H., Dam, C., Takumi, K. and van der Giessen, J. (2014). Increase in number of helminth species from Dutch red foxes over a 35-year period. Parasites and Vectors 7, 1–10.Google Scholar
Helm, J., Gilleard, J. S., Jackson, M., Redman, E. and Bell, R. (2009). A case of canine Angiostrongylus vasorum in Scotland confirmed by PCR and sequence analysis. Journal of Small Animal Practice 50, 255–259.CrossRefGoogle ScholarPubMed
Helm, J. R., Morgan, E. R., Jackson, M. W., Wotton, P. and Bell, R. (2010). Canine angiostrongylosis: an emerging disease in Europe. Journal of Veterinary Emergency and Critical Care 20, 98–109.Google Scholar
Hurnikova, Z., Miterpakova, M. and Mandelik, R. (2013). First autochthonous case of canine Angiostrongylus vasorum in Slovakia. Parasitology Research 112, 3505–3508.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 – Revue Canadienne de Zoologie 82, 66–74.Google Scholar
Jolly, S., Poncelot, L., Lempereur, L., Caron, Y., Bayrou, C., Cassart, D., Grimm, F. and Losson, B. (2015). First report of a fatal autochthonous canine Angiostrongylus vasorum infection in Belgium. Parasitology International 64, 97–99.CrossRefGoogle ScholarPubMed
Jones, G. W., Neal, C. and Turner, G. R. (1980). Angiostrongylus vasorum infection in dogs in Cornwall. Veterinary Record 106, 83.CrossRefGoogle ScholarPubMed
Kirk, L., Limon, G., Guitan, F. J., Hermosilla, C. and Fox, M. T. (2014). Angiostrongylus vasorum in Great Britain: a nationwide postal questionnaire survey of veterinary practices. Veterinary Record 175, 118.Google Scholar
Kistler, W. M., Brown, J. D., Allison, A. B., Nemeth, N. M. and Yabsley, M. J. (2014). First report of Angiostrongylus vasorum and Hepatozoon from a red fox (Vulpes vulpes) from West Virginia, U.S.A. Veterinary Parasitology 200, 216–220.Google Scholar
Koch, J. and Willesen, J. L. (2009). Canine pulmonary angiostrongylosis: an update. Veterinary Journal 179, 348–359.Google Scholar
Letková, V., Lazar, P., Goldová, M. and Košuthová, L. (2006). The red fox (Vulpes vulpes) as a source of zoonoses. Veterinarski Arhiv 76, S73–S81.Google Scholar
Magi, M., Guardone, L., Dell'Omodarme, M., Prati, M. C., Mignone, W., Torracca, B., Monni, G. and Macchioni, F. (2009). Angiostrongylus vasorum in red foxes (Vulpes vulpes) and badgers (Meles meles) from central and Northern Italy. Hystrix – Italian Journal of Mammalogy 20, 121–126.Google Scholar
McGarry, J. W. and Morgan, E. R. (2009). Identification of first-stage larvae of metastrongyles from dogs. Veterinary Record 165, 258–261.CrossRefGoogle ScholarPubMed
Morgan, E. R. (2014). Canine pulmonary angiostrongylosis: can a worm change its spots? Veterinary Record 175, 116–117.Google Scholar
Morgan, E. R. and Shaw, S. (2010). Angiostrongylus vasorum infection in dogs: continuing spread and developments in diagnosis and treatment. Journal of Small Animal Practice 51, 616–621.CrossRefGoogle ScholarPubMed
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, 48–57.Google Scholar
Morgan, E. R., Jefferies, R., Krajewski, M., Ward, P. and Shaw, S. E. (2009). Canine pulmonary angiostrongylosis: the influence of climate on parasite distribution. Parasitology International 58, 406–410.CrossRefGoogle ScholarPubMed
Morgan, E. R., Jefferies, R., Van Otterdijk, L., McEniry, R. B., Allen, F., Bakewell, M. and Shaw, S. E. (2010). Angiostrongylus vasorum infection in dogs: presentation and risk factors. Veterinary Parasitology 173, 255–261.Google Scholar
Philbey, A. W. and Delgado, D. (2013). Detection of Angiostrongylus vasorum in red foxes in Scotland. Veterinary Record 173, 148–148.Google Scholar
Poli, A., Arispici, M., Mancianti, F. and Abramo, F. M. A. (1991). Pathology of naturally acquired Angiostrongylus vasorum infection in the red fox Vulpes vulpes . Angewissenschaft Parasitenkunde 32, 121–126.Google ScholarPubMed
Saeed, I., Maddox-Hyttel, C., Monrad, J. and Kapel, C. M. O. (2006). Helminths of red foxes (Vulpes vulpes) in Denmark. Veterinary Parasitology 139, 168–179.CrossRefGoogle ScholarPubMed
Schnyder, M., Schaper, R., Bilbrough, G., Morgan, E. R. and Deplazes, P. (2013). Seroepidemiological survey for canine angiostrongylosis in dogs from Germany and the UK using combined detection of Angiostrongylus vasorum antigen and specific antibodies. Parasitology 140, 1442–1450.CrossRefGoogle ScholarPubMed
Simin, S., Kosic, L. S., Kuruca, L., Pavlovic, I., Savovic, M. and Lalosevic, V. (2014). Moving the boundaries to the South-East: first record of autochthonous Angiostrongylus vasorum infection in a dog in Vojvodina province, northern Serbia. Parasites and Vectors 7, 396.CrossRefGoogle Scholar
Simpson, V. (2014). Angiostrongylus vasorum in Cornwall. Veterinary Record 175, 178–179.CrossRefGoogle ScholarPubMed
Simpson, V. R. and Neal, C. (1982). Angiostrongylus vasorum infection in dogs and slugs. Veterinary Record 111, 303–304.Google Scholar
South, A. (1992). Terrestrial Slugs: Biology, Ecology and Control. Chapman and Hall Ltd, London.Google Scholar
Taylor, L. H., Latham, S. M. and Woolhouse, M. E. (2001). Risk factors for disease emergence. Philosophical Transactions of the Royal Society 356, 983–989.CrossRefGoogle ScholarPubMed
Tønsberg, H., Saeed, I. and Koch, J. (2004). Parasitological examination of hunting dogs and foxes in Odsherred. Danish Veterinary Journal 87, 14–18.Google Scholar
Traversa, D. (2013). Canine angiostrongylosis in Italy: occurrence of Angiostrongylus vasorum in dogs with compatible clinical pictures. Parasitology Research 112, 2473–2480.Google Scholar
Traversa, D., Di Cesare, A. and Conboy, G. (2010). Canine and feline cardiopulmonary parasitic nematodes in Europe: emerging and underestimated. Parasites and Vectors 3, 1–22.Google Scholar
Ubelaker, J. E. (1986). Systematics of species referred to the genus Angiostrongylus . Journal of Parasitology 72, 237–244.Google Scholar
Webbon, C., Baker, P. and Harris, S. (2004). Faecal density counts for monitoring changes in red fox numbers in rural Britain. Journal of Applied Ecology 41, 768–779.Google Scholar
Yamakawa, Y., McGarry, J. W., Denk, D., Dukes-McEwan, J., McDonald, N., Mas, A., McConnell, F., Tatton, B., Valentine, E. G., Wayne, J., Williams, J. M. and Hetzel, U. (2009). Emerging canine angiostrongylosis in northern England: five fatal cases. Veterinary Record 164, 149–152.Google Scholar