Skip to main content
Log in

Infections with cardiopulmonary and intestinal helminths and sarcoptic mange in red foxes from two different localities in Denmark

  • Original Paper
  • Published:
Acta Parasitologica Aims and scope Submit manuscript

Abstract

Monitoring parasitic infections in the red fox is essential for obtaining baseline knowledge on the spread of diseases of veterinary and medical importance. In this study, screening for cardiopulmonary and intestinal helminths and sarcoptic mange (Sarcoptes scabiei) was done on 118 foxes originating from two distinct localities in Denmark, (Copenhagen) greater area and southern Jutland. Fifteen parasite species were recorded in 116 foxes (98.3%), nine parasitic species are of zoonotic potential. Parasite diversity was greater in foxes of Copenhagen in terms of overall parasite species richness and species richness of all helminth groups individually: trematodes; cestodes; and nematodes. Six parasite species were recovered from foxes of Copenhagen, but not from foxes of Southern Jutland: Echinochasmus perfoliatus; Echinostoma sp.; Pseudamphistomum truncatum; Dipylidium caninum; Angiostrongylus vasorum; and Sarcoptes scabiei, but Toxascaris leonina was only recorded in foxes of southern Jutland. A high prevalence and abundance of A. vasorum in foxes of Copenhagen was observed. The prevalence of four nematode species; Eucoleus (Capillaria) aerophilus, Uncinaria stenocephala, Toxocara canis, and Crenosoma vulpis, in foxes of both localities were comparable and ranging from 22.9% to 89%. The prevalence of Mesocestoides sp. was significantly higher in foxes of Copenhagen. Taenia spp. were detected using morphological and molecular analysis, which revealed the dominance of T. polyacantha in foxes of both localities. Infections with sarcoptic mange were evident only among foxes of Copenhagen (44.9%), which significantly affected the average weight of the infected animals. Further remarks on the zoonotic and veterinary implications of the parasites recovered are given.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Al-Sabi M.N.S., Kapel C.M.O. 2011. Multiplex PCR identification of Taenia spp in rodents and carnivores. Parasitology Research, 109, 1293–1298. DOI: 10.1007/s00436-011-2373-9.

    Article  PubMed  Google Scholar 

  • Al-Sabi M.N.S., Chriél M., Enemark H.L. 2013a. Endoparasites of the raccoon dog (Nyctereutes procyonoides) and the red fox (Vulpes vulpes) in Denmark 2009 to 2012 — a comparative study. International Journal for Parasitology: Parasites and Wildlife, 2, 144–151. DOI: 10.1016/j.ijppaw.2013.04.001.

    PubMed  Google Scholar 

  • Al-Sabi M.N.S., Willesen J., Koch J., Espersen M.C., Johansson A., Kapel C.M.O. 2013b. A coprological investigation of gastrointestinal and cardiopulmonary parasites in hunting dogs in Denmark. Veterinary Parasitology, 196, 366–372. DOI: 10.1016/j.vetpar.2013.03.027.

    Article  PubMed  Google Scholar 

  • Andras T. 2001. Data on the parasitological status of the red fox in Hungary (in Hungarian). Magyar Allatorvosok Lapja, 123, 100–107.

    Google Scholar 

  • Armua-Fernandez M.T., Nonaka N., Sakurai T., Nakamura S., Gottstein B., Deplazes P., Phiri I.G.K., Katakura K., Aku Y. 2011. Development of PCR/dot blot assay for specific detection and differentiation of taeniid cestode eggs in canids. Parasitology International, 60, 84–89. DOI: 10.1016/j.parint.2010.11.005.

    Article  CAS  PubMed  Google Scholar 

  • Bak U., Hessellund K., Lykkegaard J. 1997. Fox scabies. (In Danish.) Raveskab. MSc thesis, University of Aarhus, Denmark.

    Google Scholar 

  • Bolt G., Monrad J., Henriksen P., Dietz H.H., Koch J., Bindseil E., Jensen A.L. 1992. The fox (Vulpes vulpes) as a reservoir for canine angiostrongylosis in Denmark. Acta Veterinaria Scandinavica, 33, 357–362.

    CAS  PubMed  Google Scholar 

  • Borecka A., Gawor J., Malczewska M., Malczewski A. 2009. Prevalence of zoonotic helminth parasites of the small intestine in red foxes from central Poland. Medycyna Weterynaryjna, 65, 33–35.

    Google Scholar 

  • Borgsteede F.H. 1984. Helminth parasites of wild foxes (Vulpes vulpes L.) in The Netherlands. Zeitschrift Fur Parasitenkunde, 70, 281–285. DOI: 10.1007/BF00927813.

    Article  CAS  PubMed  Google Scholar 

  • Bornstein S., Mörner T., Samuel W.M. 2001. Sarcoptes scabiei and sarcoptic mange. In: Samuel WM, Pybus MJ, Kocan AA (ed) Parasitic Diseases of Wild Mammals, 2nd edn. Iowa State University Press, Ames, pp. 107–119.

    Chapter  Google Scholar 

  • Bush A.O., Lafferty K.D., Lotz J.M., Shostak A.W. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology, 83, 575–583. DOI: 10.2307/3284227.

    Article  CAS  PubMed  Google Scholar 

  • Bruzinskaite-Schmidhalter R., Sarkunas M., Malakauskas A., Mathis A., Torgerson P.R., Deplazes P. 2012. Helminths of red foxes (Vulpes vulpes) and raccoon dogs (Nyctereutes procyonoides) in Lithuania. Parasitology, 139, 120–127. DOI: 10.1017/S0031182011001715.

    Article  PubMed  Google Scholar 

  • Chai J.Y., Shin E.H., Lee S.H., Rim H.J. 2009. Foodborne intestinal flukes in Southeast Asia. Korean Journal of Parasitology, 47, S69–S102. DOI: 10.3347/kjp.2009.47.S.S69.

    Article  PubMed  Google Scholar 

  • Di Cerbo A.R., Manfredi M.T., Trevisiol K., Bregoli M., Ferrari N., Pirinesi F., Bazzoli S. 2008. Intestinal helminth communities of the red fox (Vulpes vulpes L) in the Italian Alps. Acta Parasitologica, 53, 302–311. DOI: 10.2478/s11686-008-0042-7.

    Article  Google Scholar 

  • Contesse P., Hegglin D., Gloor S., Bontadina F., Deplazes P. 2004. The diet of urban foxes (Vulpes vulpes) and the availability of anthropogenic food in the city of Zurich, Switzerland. Mammalian Biology, 69, 81–95. DOI: 10.1078/1616-5047-00123.

    Article  Google Scholar 

  • Danish Nature Agency 2012. Fox mange spreads to north west Zealand — Nature Agency. (Original text in Danish: Ræveskab breder sig til Nordvestsjæland — Naturstyrelsen). http://www.naturstyrelsen.dkNyheder/2012/Raeveskab_nordvestsjaelland.htm. Accessed: 4-June/2013.

    Google Scholar 

  • Davidson R.K., Gjerde B., Vikøren T., Lillehaug A., Handeland K. 2006. Prevalence of Trichinella larvae and extra-intestinal nematodes in Norwegian red foxes (Vulpes vulpes). Veterinary Parasitology, 136, 307–316. DOI: 10.1016/j.vetpar.2005.11.015.

    Article  PubMed  Google Scholar 

  • Davidson R.K., Bornstein S., Handeland K. 2008. Long-term study of Sarcoptes scabiei infection in Norwegian red foxes (Vulpes vulpes) indicating host/parasite adaptation. Veterinary Parasitology, 156, 277–283. DOI: 10.1016/j.vetpar.2008.05.019.

    Article  PubMed  Google Scholar 

  • Deblock S., Petavy A.F., Gilot B. 1988. Helminthes intestinaux du Renard commun (Vulpes vulpes L) dans le Massif central (France) (in French). Canadian Journal of Zoology, 66, 1562–1569. DOI: 10.1139/z88-228.

    Article  Google Scholar 

  • Deplazes P., Hegglin D., Gloor S., Romig T. 2004. Wilderness in the city: the urbanization of Echinococcus multilocularis. Trends in Parasitology, 20, 77–84. DOI: 10.1016/j.pt.2003.11.011.

    Article  PubMed  Google Scholar 

  • Denk D., Matiasek K., Just F.T., Hermanns W., Baiker K., Herbach N., Steinberg T., Fischer A. 2009. Disseminated angiostrongylosis with fatal cerebral haemorrhages in two dogs in Germany: A clinical case study. Veterinary Parasitology, 160, 100–108. DOI: 10.1016/j.vetpar.2008.10.077.

    Article  CAS  PubMed  Google Scholar 

  • van Doorn D.C.K., van de Sande A.H., Nijsse E.R., Eysker M., Ploeger H.W. 2009. Autochthonous Angiostrongylus vasorum infection in dogs in the Netherlands. Veterinary Parasitology, 162, 163–166. DOI: 10.1016/j.vetpar.2009.02.019.

    Article  PubMed  Google Scholar 

  • Eira C., Viganda J., Torres J., Miquel J. 2006. The helminth community of the red fox, Vulpes vulpes, in Dunas de Mira (Portugal) and its effect on host condition. Wildlife Biology in Practice, 2, 26–36. DOI: 10.2461/wbp.2006.2.5.

    Article  Google Scholar 

  • Enemark H.L., Al-Sabi M.N.S., Knapp J., Ståhl M., Chríel M. 2013. Detection of a high-endemic focus of Echinococcus multilocularis in red foxes in southern Denmark, January 2013. Euro Surveill 18(10): pii = 20420. Available online: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=2042018.

    Google Scholar 

  • Ferdushy T., Kapel C.M.O., Webster P., Al-Sabi M.N.S., Gronvold J.R. 2009. The occurrence of Angiostrongylus vasorum in terrestrial slugs from forests and parks in the Copenhagen area, Denmark. Journal of Helminthology, 83, 379–383. DOI: 10.1017/S0022149X09377706.

    Article  CAS  PubMed  Google Scholar 

  • Ferdushy T., Kapel C.M.O., Webster P., Al-Sabi M.N.S., Grønvold J.R. 2010. The effect of temperature and host age on the infectivity and development of Angiostrongylus vasorum in the slug Arion Lusitanicus. Parasitology Research, 107, 147–151. DOI: 10.1007/s00436-010-1850-x.

    Article  PubMed  Google Scholar 

  • Finnerup E. 1983. Angiostrongylus vasorum in dog: a survey and case history OT: Angiostrongylus vasorum hos hund: En oversigt og en kasuistik (in Danish). Dansk Veterinærtidsskrift, 66, 338–340.

    Google Scholar 

  • Forchhammer M.C., Asferg T. 2000. Invading parasites cause a structural shift in red fox dynamics. Proceedings of the Royal Society B-Biological Sciences, 267, 779–786. DOI: 10.1098/rspb.2000.1071.

    Article  CAS  PubMed Central  Google Scholar 

  • Gesy K., Pawlik M., Kapronczai L., Wagner B., Elkin B., Schwantje H., Jenkins E. 2013. An improved method for the extraction and quantification of adult Echinococcus from wildlife definitive hosts. Parasitology Research, 112, 2075–2078. DOI: 10.1007/s00436-013-3371-x.

    Article  PubMed  Google Scholar 

  • Gortazar C., Villafuerte R., Lucientes J., FernBndez-de-Luco D. 1998. Habitat related differences in helminth parasites of red foxes in the Ebro Valley. Veterinary Parasitology, 80, 75–81. DOI: 10.1016/S0304-4017(98)00192-7.

    Article  CAS  PubMed  Google Scholar 

  • Grilo C., Bissonette J.A., Santos-Reis A. 2009. Spatial-temporal patterns in Mediterranean carnivore road casualties: Consequences for mitigation. Biological Conservation, 142, 301–313. DOI: 10.1016/j.biocon.2008.10.026.

    Article  Google Scholar 

  • Guildal J.A., Clausen B. 1973. Endo parasites from 100 Danish red foxes (Vulpes vulpes (L)). Norwegian Journal of Zoology, 21, 329–330.

    Google Scholar 

  • Hart B.L. 1990. Behavioral adaptations to pathogens and parasites: Five strategies. Neuroscience and Biobehavioral Reviews, 14, 273–294. DOI: 10.1016/S0149-7634(05)80038-7.

    Article  CAS  PubMed  Google Scholar 

  • Jefferies R., Shaw S.E., Willesen J.L., Viney M.E., Morgan E.R. 2010. Elucidating the spread of the emerging canid nematode Angiostrongylus vasorum between Palaearctic and Nearctic ecozones. Infection, Genetics and Evolution, 10, 561–568. DOI: 10.1016/j.meegid.2010.01.013.

    Article  CAS  PubMed  Google Scholar 

  • Jensen B., Sequeira D.M. 1978. The diet of the red fox (Vulpes vulpes) in Denmark. Danish Review of Game Biology, 10, 2–16.

    Google Scholar 

  • Jones A., Pybus M.J. 2001. Taeniasis and echinococcosis. In: Samuel W.M., Pybus M.J., Kocan A.A. (Eds.). Parasitic Diseases of Wild Mammals. Iowa State University Press, Ames, Iowa, pp. 163–165.

    Google Scholar 

  • Kapel C.M.O., Saeed I. 2000. Echinococcus multilocularis (in Danish). Dansk Veterinærtidsskrift, 83, 14–16.

    Google Scholar 

  • Lassing H., Prosl H., Hinterdorfer F. 1998. Parasites of the red fox (Vulpes vulpes) in Styria. (in German). Wiener Tierürztlichen Monatsschrift, 85, 116–122.

    Google Scholar 

  • Loos-Frank B., Zeyhle E. 1982. The intestinal helminths of the red fox and some other carnivores in southwest Germany (in German). Zeitschrift Fur Parasitenkunde, 67, 99–113. DOI: 10.1007/BF00929518.

    Article  CAS  PubMed  Google Scholar 

  • Manas S., Ferrer D., Castellà J., López-Martín J.M. 2005. Cardiopulmonary helminth parasites of red foxes (Vulpes vulpes) in Catalonia, northeastern Spain. Veterinary Journal, 169, 118–120. DOI: 10.1016/j.tvjl.2003.12.011.

    Article  Google Scholar 

  • Martinez-Moreno F.J., Hernández S., López Cobos E., Becerra C., Acosta I., Martínez-Moreno A. 2007. Estimation of canine intestinal parasites in Córdoba (Spain) and their risk to public health. Veterinary Parasitology, 143, 7–13. DOI: 10.1016/j.vetpar.2006.08.004.

    Article  CAS  PubMed  Google Scholar 

  • Morgan E.R., Tomlinson A., Hunter S., Nichols T., Roberts E., Fox M.T., Taylor M.A. 2008. Angiostrongylus vasorum and Eucoleus aerophilus in foxes (Vulpes vulpes) in Great Britain. Veterinary Parasitology, 154, 48–57. DOI: 10.1016/j.vetpar.2008.02.030.

    Article  CAS  PubMed  Google Scholar 

  • Möhl K., Große K., Hamedy A., Wüste T., Kabelitz P., Lücker E. 2009. Biology of Alaria spp and human exposition risk to Alaria mesocercariae — a review. Parasitology Research, 105, 1–15. DOI: 10.1007/s00436-009-1444-7.

    Article  PubMed  Google Scholar 

  • OIE 2005. Taenia Infections: Taeniasis, Cysticercosis, Neurocysticercosis, Coenurosis, Neurocoenurosis. http://www.cfsph.iastate.edu/Factsheets/pdfs/taenia.pdf. Accessed 16-5-2013.

    Google Scholar 

  • Overskaug K. 1994. Behavioural changes in free-ranging red foxes (Vulpes vulpes) due to sarcoptic mange. Acta Veterinaria Scandinavica, 35, 457–459.

    CAS  PubMed  Google Scholar 

  • Pedersen K.M., Mehl N.B., Pedersen N.W. 1995. Angiostrongylus vasorum Der er oberveret en klart stigende tendens i forekomsten (in Dansih). Dansk Veterinærtidsskrift, 78, 779–782.

    Google Scholar 

  • Pence D.B., Ueckermann E. 2002. Sarcoptic mange in wildlife. Revue Scientifique Et Technique De L Office International Des Epizooties, 21, 385–398.

    CAS  Google Scholar 

  • Rajkovic-Janje R., Marinculic A., Bosnic S., Benic M., Vinkovic B., Mihaljevic Z. 2002. Prevalence and seasonal distribution of helminth parasites in red foxes (Vulpes vulpes) from the Zagreb County (Croatia) (in German). Zeitschrift Fur Jagdwissenschaft, 48, 151–160. DOI: 10.1007/BF02189989.

    Google Scholar 

  • Ramnath K-M.N. 2009. Behavioral effects of parasitism in animals. Journal of Exotic Pet Medicine, 18, 254–265. DOI: 10.1053/j.jepm.2009.10.004.

    Article  Google Scholar 

  • Reperant L.A., Hegglin D., Fischer C., Kohler L., Weber J.M., Deplazes P. 2007. Influence of urbanization on the epidemiology of intestinal helminths of the red fox (Vulpes vulpes) in Geneva, Switzerland. Parasitology Research, 101, 605–611. DOI: 10.1007/s00436-007-0520-0.

    Article  PubMed  Google Scholar 

  • R Core Team 2012. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/.

    Google Scholar 

  • Saeed I. 2005. Helminths of Danish red foxes: natural and experimental infections. PhD thesis. The Royal Veterinary and Agricultural University, Denmark.

    Google Scholar 

  • Saeed I., Maddox-Hyttel C., Monrad J., Kapel C.M.O. 2006. Helminths of red foxes (Vulpes vulpes) in Denmark. Veterinary Parasitology, 139, 168–179. DOI: 10.1016/j.vetpar.2006.02.015.

    Article  CAS  PubMed  Google Scholar 

  • Segovia J.M., Torres J., Miquel J. 2004. Helminth parasites of the red fox (Vulpes vulpes L., 1758) in the Iberian Peninsula: an ecological study. Acta Parasitologica, 49, 67–79.

    Google Scholar 

  • Soulsby E.J.L. 1982. Helminths, Arthropods and Protozoa of domesticated animals. 7th edn. Bailliére Tindall, London, UK.

    Google Scholar 

  • Stien A., Voutilainen L., Haukisalmi V., Fuglei E., Mork T., Yoccoz N., Ims R.A., Henttonen H. 2010. Intestinal parasites of the Arctic fox in relation to the abundance and distribution of intermediate hosts. Parasitology, 137, 149–157. DOI: 10.1017/S0031182009990953.

    Article  CAS  PubMed  Google Scholar 

  • Torchin M.E., Lafferty K.D., Dobson A.P., McKenzie V.J., Kuris A.M. 2003. Introduced species and their missing parasites. Nature, 421, 628–630. DOI: 10.1038/nature01346.

    Article  CAS  PubMed  Google Scholar 

  • Trachsel D., Deplazes P., Mathis A. 2007. Identification of taeniid eggs in the faeces from carnivores based on multiplex PCR using targets in mitochondrial DNA. Parasitology, 134, 911–920. DOI: 10.1017/S0031182007002235.

    Article  CAS  PubMed  Google Scholar 

  • Verster A. 1969.A taxonomic revision of the genus Taenia Linnaeus, 1758s. Onderstepoort Journal of Veterinary Research, 36, 3–58.

    CAS  PubMed  Google 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, 259–263.

    Article  CAS  PubMed  Google Scholar 

  • Wolfe A., Hogan S., Maguire D., Fitzpatrick C., Vaughan L., Wall D., Hayden T.J., Mulcahy G. 2001. Red foxes (Vulpes vulpes) in Ireland as hosts for parasites of potential zoonotic and veterinary significance. Veterinary Record, 149, 759–763.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mohammad N. S. Al-Sabi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Al-Sabi, M.N.S., Halasa, T. & Kapel, C.M.O. Infections with cardiopulmonary and intestinal helminths and sarcoptic mange in red foxes from two different localities in Denmark. Acta Parasit. 59, 98–107 (2014). https://doi.org/10.2478/s11686-014-0214-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.2478/s11686-014-0214-6

Keywords

Navigation