Skip to main content

Echinococcus multilocularis and other zoonotic parasites in red foxes in Estonia


Red fox (Vulpes vulpes) is the most widely distributed canid in the world and an important source of multiple zoonotic pathogens capable of causing life-threatening diseases, such as rabies and alveolar echinococcosis. Informing general public of potential risks related to foxes is becoming more important since the fox densities have increased in many countries and the species is colonizing urban areas in Europe and around the world with increasing pace, bringing zoonotic pathogens to the immediate neighbourhood of humans and their companion animals. The aim of this study was to examine the parasite fauna of red foxes in Estonia. We found in Estonian foxes a total of 17 endoparasite taxa, including ten zoonotic species. All the analysed individuals were infected and the average parasite species richness was 6·37. However, the infection rates varied to a very large extent for different parasite species, ranging from 0·9 to 91·5%. Of zoonotic species, the highest infection rate was observed for Alaria alata (90·7%), Eucoleus aerophilus (87·6%) and Uncinaria stenocephala (84·3%). The prevalence of tapeworm Echinococcus multilocularis, a causative agent for alveolar echinococcosis, was also relatively high (31·5%), presenting a potential risk to human health.

Corresponding author
*Corresponding author. Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Vanemuise 46, 51014 Tartu, Estonia. E-mail:
Hide All
Abuladze K. I. (1964). Common Cestodology, Part 4: Taeniidae—Tapeworms of Animals and Humans and Causal Agents of their Illnesses. Nauka, Moscow. (in Russian)
Arlian L. G. (1989). Biology, host relations, and epidemiology of Sarcoptes scabiei . Annual Review of Entomology 34, 139161.
Bateman P. W. and Fleming P. A. (2012). Big city life: carnivores in urban environments. Journal of Zoology 287, 123.
Bružinskaite-Schmidhalter R., Šarkunas M., Malakauskas A., Mathis A., Torgerson P. R. and Deplazes P. (2012). Helminths of red foxes (Vulpes vulpes) and raccoon dogs (Nyctereutes procyonoides) in Lithuania. Parasitology 139, 120127.
Cavallini P. (1995). Variation in the body size of the red fox. Annales Zoologici Fennici 32, 421427.
Conraths F. J. and Deplazes P. (2015). Echinococcus multilocularis: epidemiology, surveillance and state-of-the-art diagnostics from a veterinary public health perspective. Veterinary Parasitology 213, 149161.
Davidson R. K., Romig T., Jenkins E., Tryland M. and Robertson L. J. (2012). The impact of globalisation on the distribution of Echinococcus multilocularis . Trends in Parasitology 28, 239247.
Deplazes P., Hegglin D., Gloor S. and Romig T. (2004). Wilderness in the city: the urbanization of Echinococcus multilocularis . Trends in Parasitology 20, 7784.
Eckert J., Gemmell M. A., Meslin F.-X. and Pawlowski Z. S. (eds.) (2001). WHO/OIE Manual on Echinococcosis in Humans and Animals: A Public Health Problem of Global Concern. WHO/OIE, Paris.
Fuglei E., Stien A., Yoccoz N. G., Ims R. A., Eide N. E., Prestrud P., Deplazes P. and Oksanen A. (2008). Spatial distribution of Echinococcus multilocularis, Svalbard, Norway. Emerging Infectious Diseases 14, 7375.
Gloor S., Bontadina F., Hegglin D., Deplazes P. and Breitenmoser U. (2001). The rise of urban fox populations in Switzerland. Mammalian Biology 66, 155164.
Harris S. and Rayner J. M. V. (1986). Urban fox (Vulpes vulpes) population estimates and habitat requirements in several British cities. Journal of Animal Ecology 55, 575591.
Heptner V. G. and Naumov N. P. (1998). Mammals of the Soviet Union Vol. II Part 1a. Sirenia and Carnivora (Sea cows; Wolves and Bears), pp. 82123. Amerind Publishing Co, New Delhi.
Heukelbach J. and Feldmeier H. (2006). Scabies. Lancet 367, 17671774.
Hofer S., Gloor S., Müller 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 Zürich, Switzerland. Parasitology 120, 135142.
Hrčkova G., Miterpakova M., O'Connor A., Šnabel V. and Olson P. D. (2011). Molecular and morphological circumscription of Mesocestoides tapeworms from red foxes (Vulpes vulpes) in central Europe. Parasitology 138, 638647.
Jenkins D. J. and Craig N. A. (1992). The role of foxes Vulpes vulpes in the epidemiology of Echinococcus granulosus in urban environments. Medical Journal of Australia 157, 754756.
Kauhala K. and Kowalczyk R. (2011). Invasion of the raccoon dog Nyctereutes procyonoides in Europe: history of colonization, features behind its success, and threats to native fauna. Current Zoology 57, 584598.
Keidans P., Kruklite A. and Keidane D. (2005). Endoparasites of red foxes in Latvia. Bulletin of the Scandinavian-Baltic Society for Parasitology 14, 81.
Knapp J., Nakao M., Yanagida T., Okamoto M., Saarma U., Lavikainen A. and Ito A. (2011). Phylogenetic relationships within Echinococcus and Taenia tapeworms (Cestoda: Taeniidae): an inference from nuclear protein-coding genes. Molecular Phylogenetics and Evolution 61, 628638.
Knapp J., Gottstein B., Saarma U. and Millon L. (2015). Taxonomy, phylogeny and molecular epidemiology of Echinococcus multilocularis: from fundamental knowledge to health ecology. Veterinary Parasitology 213, 8591.
Kozlov D. P. (1977). Key of Helminths of Carnivores. Nauka, Moscow. (in Russian)
Laloševic D., Laloševic V., Klem I., Stanojev-Jovanovic D. and Pozio E. (2008). Pulmonary capillariasis miming bronchial carcinoma. The American Journal of Tropical Medicine and Hygiene 78, 1416.
Laurimaa L., Davison J., Plumer L., Süld K., Oja R., Moks E., Keis M., Hindrikson M., Kinkar L., Laurimäe T., Abner J., Remm J., Anijalg P. and Saarma U. (2015 a). Non-invasive molecular diagnostics identifies Echinococcus multilocularis spillover to an urban area in Estonia. Emerging Infectious Diseases 21, 163164.
Laurimaa L., Süld K., Moks E., Valdmann H., Umhang G., Knapp J. and Saarma U. (2015 b). First report of the zoonotic tapeworm Echinococcus multilocularis in raccoon dogs in Estonia, and comparisons with other countries in Europe. Veterinary Parasitology 212, 200205.
Laurimaa L., Davison J., Süld K., Plumer L., Oja R., Moks E., Keis M., Hindrikson M., Kinkar L., Laurimäe T., Abner J., Remm J., Anijalg P. and Saarma U. (2015 c). First report of highly pathogenic Echinococcus granulosus genotype G1 in dogs in European urban environment. Parasites & Vectors 8, 182.
Laurimaa L., Süld K., Davison J., Moks E., Valdmann H. and Saarma U. (2016). Alien species and their zoonotic parasites in native and introduced ranges: the raccoon dog example. Veterinary Parasitology 219, 2433.
Letkova V., Lazar P., Čurlik J., Goldova M., Kočišova A., Košuthova L. and Mojžišova J. (2006). The red fox (Vulpes vulpes L.) as a source of zoonoses. Veterinarski Arhiv 76 (Suppl.), S73S81.
Macdonald D. W. and Reynolds J. C. (2008). Vulpes vulpes. The IUCN Red List of Threatened Species 2008: e.T23062A9412884.
Marcinkute A., Šarkunas M., Moks E., Saarma U., Jokelainen P., Bagrade G., Laivacuma S., Strupas K., Sokolovas V. and Deplazes P. (2015). Echinococcus infections in the Baltic region. Veterinary Parasitology 213, 121131.
Moks E. (2008). Tapeworm parasites Echinococcus multilocularis and E. granulosus in Estonia: phylogenetic relationships and occurrence in wild carnivores and ungulates. PhD thesis. University of Tartu.
Moks E., Saarma U. and Valdmann H. (2005). Echinococcus multilocularis in Estonia. Emerging Infectious Diseases 11, 19731974.
Moks E., Jõgisalu I., Saarma U., Talvik H., Järvis T. and Valdmann H. (2006). Helminthologic survey of the wolf (Canis lupus) in Estonia, with an emphasis on Echinococcus granulosus . Journal of Wildlife Diseases 42, 359365.
Moks E., Jõgisalu I., Valdmann H. and Saarma U. (2008). First report of Echinococcus granulosus G8 in Eurasia and a reappraisal of the phylogenetic relationships of “genotypes” G5–G10. Parasitology 135, 647654.
Newman T. J., Baker P. J. and Harris S. (2002). Nutritional condition and survival of red foxes with sarcoptic mange. Canadian Journal of Zoology 80, 154161.
Oja R. (2011). Side effects of supplementary feeding of wild boar (Sus scrofa) on ground-nesting birds, other mammals and plants. Master thesis. University of Tartu (in Estonian).
Oksanen J., Blanchet F. G., Kindt R., Legendre P., Minchin P. R., O'Hara R. B., Simpson G. L., Solymos P., Stevens M. H. H. and Wagner H. (2015). Vegan: community ecology package. R package version 2.2-1.
Parre J. (1985). Veterinaarparasitoloogia. Valgus, Tallinn. (in Estonian).
Pärtel A. (2013). Self-declaration by Estonia on the recovery of its rabies-free status. OIE Bulletin 3, 5861.
Plumer L., Davison J. and Saarma U. (2014). Rapid urbanization of red foxes in Estonia: distribution, behaviour, attacks on domestic animals, and health-risks related to zoonotic diseases. PLoS ONE 9, e115124.
R Development Core Team (2014). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
Saarma U., Jõgisalu I., Moks E., Varcasia A., Lavikainen A., Oksanen A., Simsek S., Andresiuk V., Denegri G., Gonzalez L. M., Ferrer E., Garate T., Rinaldi L. and Maravilla P. (2009). A novel phylogeny for the genus Echinococcus, based on nuclear data, challenges relationships based on mitochondrial evidence. Parasitology 136, 317328.
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.
Schöffel I., Schein E., Wittstadt U. and Hentsche J. (1991). Parasite fauna of red foxes in Berlin (West). Berliner und Münchener Tierärztliche Wochenschrift 104, 153157.
Segovia J. M., Torres J. and Miquel J. (2004). Helminth parasites of the red fox (Vulpes vulpes L., 1758) in the Iberian Peninsula: an ecological study. Acta Parasitologica 49, 6779.
Shimalov V. V. and Shimalov V. T. (2003). Helminth fauna of the red fox (Vulpes vulpes Linnaeus, 1758) in southern Belarus. Parasitology Research 89, 7778.
Smith G. C., Gangadharan B., Taylor Z., Laurenson M. K., Bradshaw H., Hide G., Hughes J. M., Dinkel A., Romig T. and Craig P. S. (2003). Prevalence of zoonotic important parasites in the red fox (Vulpes vulpes) in Great Britain. Veterinary Parasitology 118, 133142.
Stone L. and Roberts A. (1990). The checkerboard score and species distributions. Oecologia 85, 7479.
Süld K., Valdmann H., Laurimaa L., Soe E., Davison J. and Saarma U. (2014). An invasive vector of zoonotic disease sustained by anthropogenic resources: the raccoon dog in northern Europe. PLoS ONE 9(5), e96358.
Szell Z., Marucci G., Pozio E. and Sreter T. (2013). Echinococcus multilocularis and Trichinella spiralis in golden jackals (Canis aureus) of Hungary. Veterinary Parasitology 197, 393396.
Tamminga N., Bierman W. F. W. and de Vries P. J. (2009). Cutaneous larva migrans acquired in Brittany, France. Emerging Infectious Diseases 15, 18561858.
Thompson R. C. (1983). The susceptibility of the European red fox (Vulpes vulpes) to infection with Echinococcus granulosus of Australian sheep origin. Annals of Tropical Medicine and Parasitology 77, 7582.
Umhang G., Forin-Wiart M.-A., Hormaz V., Caillot C., Boucher J.-M., Poulle M.-L. and Franck B. (2015). Echinococcus multilocularis detection in the intestines and feces of free-ranging domestic cats (Felis s. catus) and European wildcats (Felis s. silvestris) from northeastern France. Veterinary Parasitology 214, 7579.
Veeroja R. and Männil P. (2015). Status of Game Populations in Estonia and Proposal for Hunting in 2015. Estonian Environment Agency, Tartu, pp. 6769. (in Estonian)
Venables W. N. and Ripley B. D. (2002) Modern Applied Statistics with S., 4th Edn. Springer, New York. ISBN 0-387-95457-0.
Vos A. (1995). Population dynamics of the red fox (Vulpes vulpes) after the disappearance of rabies in county Garmisch-Partenkirchen, Germany, 1987–1992. Annales Zoologici Fennici 32, 9397.
Vuitton D. A., Demonmerot F., Knapp J., Richou C., Grenouillet F., Chauchet A., Vuitton L., Bresson-Hadni S. and Millon L. (2015). Clinical epidemiology of human AE in Europe. Veterinary Parasitology 213, 110120.
Wasiluk A. (2009). Alariosis – newly diagnosed trematodiasis. Wiadomosci Parazytologiczne 55, 349352. (in Polish with English summary)
Ziadinov I., Deplazes P., Mathis A., Mutunova B., Abdykerimov K., Nurgaziev R. and Torgerson P. R. (2010). Frequency distribution of Echinococcus multilocularis and other helminths of foxes in Kyrgyzstan. Veterinary Parasitology 171, 286292.
Zvegintsova N. S., Dumenko V. P. and Varodi E. I. (2007). Helminths of the red fox (Vulpes vulpes) in the Askania Nova Biosphere Reserve (Ukraine). Vestnik Zoologii 41, 153157. (in Russian with English summary)
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *


Type Description Title
Supplementary materials

Laurimaa supplementary material
Table S1

 Word (21 KB)
21 KB


Altmetric attention score

Full text views

Total number of HTML views: 4
Total number of PDF views: 81 *
Loading metrics...

Abstract views

Total abstract views: 343 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 16th January 2018. This data will be updated every 24 hours.