Helminths of red foxes (Vulpes vulpes) in Denmark

Saeed, I.; Maddox-Hyttel, C.; Monrad, J.; Kapel, C.M.O.

doi:10.1016/j.vetpar.2006.02.015

Cited by 250Helminth infection and controlParasite Biology and Host InteractionsParasitic infections in humans and animals

Helminths of red foxes (Vulpes vulpes) in Denmark

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Saeed, I., Maddox-Hyttel, C., Monrad, J., Kapel, C.M.O.·2006·Veterinary Parasitology

DOI 10.1016/j.vetpar.2006.02.015

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Abstract

An epidemiological study of helminths in 1040 red foxes collected from various localities in Denmark during 1997-2002, revealed 21 helminth species at autopsy, including nine nematode species: Capillaria plica (prevalence 80.5%), Capillaria aerophila (74.1%), Crenosoma vulpis (17.4%), Angiostrongylus vasorum (48.6% from Northern Zealand (endemic area)), Toxocara canis (59.4%), Toxascaris leonina (0.6%), Uncinaria stenocephala (68.6%), Ancylostoma caninum (0.6%), and Trichuris vulpis (0.5%); seven cestodes: Mesocestoides sp. (35.6%), a number of Taeniid species (Taenia pisiformis, T. hydatigena, T. taeniaeformis, T. crassiceps, and unidentified Taenia spp.) (22.8%), and Echinococcus multilocularis (0.3%); four trematodes: Alaria alata (15.4%), Cryptocotyle lingua (23.8%), Pseudamphystomum truncatum (3.6% from Northern Zealand), and Echinochasmus perfoliatus (2.4% from Northern Zealand); one acanthocephalan: Polymorphus sp. (1.2%). Significant difference in prevalence was found for T. canis and A. vasorum according to host sex, and for T. canis, U. stenocephala, Mesocestoides sp., Taenia spp., A. alata, A. vasorum, and Capillaria spp. according to age groups (adult, young or cub). Prevalence and average worm intensity for each helminth species varied considerably according to geographical locality, season, and year. Aggregated distribution was found for several helminth species. The two species E. multilocularis and E. perfoliatus are first records for Denmark.

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The prevalence of Toxocara/Toxascaris nematodes in the study was similar to results obtained in other Polish regions and Europe.
“In the present study, the prevalence of these nematodes was similar to results obtained in other Polish regions [14,31,38,41] and Europe [1,2,3,8,10,13,16,19,37].”
From Distribution of Parasitic Helminths in the Small Intestine of the Red Fox (Vulpes vulpes) (2020) · cites this paper as [13]

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“The phenomenon of urbanisation and proliferation of this wild carnivore is actually evident across Europe, including Slovakia (Chautan et al. 2000; Deplazes et al. 2004; Saeed et al. 2006).”
Prevalence of Angiostrongylus vasorum, Aelurostrongylus abstrusus and Crenosoma vulpis larvae in native slug populations in Germany.
Lange, M., Penagos-Tabares, F., Hirzmann, J., Failing, K., Schaper, R., Bourgonie, Y. R. V., Backeljau, T., Hermosilla, C., & Taubert, A. (2018) · Veterinary parasitology · doi:10.1016/j.vetpar.2018.03.011 · Cited by 41 · see citing works
Canine angiostrongylosis: recent advances in diagnosis, prevention, and treatment
Cesare, A. D., & Traversa, D. (2014) · Veterinary medicine · doi:10.2147/vmrr.s53641 · Cited by 41 · see citing works
“2,4,56 59 It is also true that lack of awareness and misdiagnosis could have resulted in underestimation and missed diagnosis in dogs.”
A coprological investigation of gastrointestinal and cardiopulmonary parasites in hunting dogs in Denmark.
Al-Sabi, M. N. S., Kapel, C., Johansson, A. M., Espersen, M. C., Koch, J., & Willesen, J. (2013) · Veterinary parasitology · doi:10.1016/j.vetpar.2013.03.027 · Cited by 41 · see citing works
Self-citation
Angiostrongylus vasorum: the ‘French Heartworm’
Ferdushy, T., & Hasan, M. T. (2010) · Parasitology Research · doi:10.1007/s00436-010-2026-4 · Cited by 39 · see citing works
“…stage larvae (L1) were recovered from skin, diaphragm, liver, pancreas, brain and cerebellum, as well as from peripheral blood and cerebrospinal fluid of a chronically infected dog, and from muscle, kidney and cardiopulmonary blood vessels of fox (Oliveira-junior et al. 2004; Saeed et al. 2006).”
BackgroundInfluential
Seasonal variation in the prevalence of Toxocara eggs on children’s playgrounds in the city of Hanover, Germany
Kleine, A., Springer, A., & Strube, C. (2017) · Parasites & Vectors · doi:10.1186/s13071-017-2193-6 · Cited by 38
“For example, 59% of foxes were found to be infected with Toxocara canis in Denmark [34].”
Influential
Annotation of the Transcriptome from Taenia pisiformis and Its Comparative Analysis with Three Taeniidae Species
Yang, D.-Y., Fu, Y., Wu, X., Xie, Y., Nie, H.-M., Chen, L., Nong, X., Gu, X.-B., Wang, S.-X., Peng, X.-R., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032283 · Cited by 37 · see citing works
“pisiformis are widely distributed worldwide [7,10–13].”
Background
Conquering Switzerland: the emergence of Angiostrongylus vasorum in foxes over three decades and its rapid regional increase in prevalence contrast with the stable occurrence of lungworms
Gillis-Germitsch, N., Tritten, L., Hegglin, D., Deplazes, P., & Schnyder, M. (2020) · Parasitology · doi:10.1017/s0031182020000700 · Cited by 36 · see citing works
“vulpis L1 to resist deep freeze, up to −80°C (Saeed et al., 2006), unlike A.”
BackgroundInfluential
Gastrointestinal parasites of cats in Denmark assessed by necropsy and concentration McMaster technique.
Takeuchi-Storm, N., Mejer, H., Al-Sabi, M. N. S., Olsen, C. S., Thamsborg, S., & Enemark, H. (2015) · Veterinary parasitology · doi:10.1016/j.vetpar.2015.06.033 · Cited by 36 · see citing works
Echinococcus multilocularis and Toxocara canis in urban red foxes (Vulpes vulpes) in Brussels, Belgium.
Brochier, B., Blander, H. D., Hanosset, R., Berkvens, D., Losson, B., & Saegerman, C. (2007) · Preventive Veterinary Medicine · doi:10.1016/j.prevetmed.2007.01.004 · Cited by 36 · see citing works
Estimated prevalence of Echinococcus multilocularis in raccoon dogs Nyctereutes procyonoides in northern Brandenburg, Germany
Schwarz, S., Sutor, A., Staubach, C., Mattis, R., Tackmann, K., & Conraths, F. (2011) · doi:10.1093/czoolo/57.5.655 · Cited by 35
“In Europe new endemic areas of E. multilocularis have been identified in various countries such as Denmark (Saeed et al., 2006), Belgium (Vervaeke et al., 2005; Hanosset et al., 2008), the Netherlands (van der Giessen et al., 2004), Italy (Casulli et al., 2005), Lithuania (Šarkūnas et al., 2010) and Estonia (Moks et a…”
Background
Echinococcus multilocularis and other zoonotic parasites in red foxes in Estonia
Laurimaa, L., Moks, E., Soe, E., Valdmann, H., & Saarma, U. (2016) · Parasitology · doi:10.1017/s0031182016001013 · Cited by 34 · see citing works
“…the results of these two studies, Estonian red foxes seem to harbour a minimum of 21 helminth species, which is very similar with the results from a Danish study (n= 21; Saeed et al. 2006), but less than found in Iberia (n= 34; Segovia et al. 2004) and Belarus (n= 32; Shimalov and Shimalov, 2003).”
Result
Capillaria plica (syn. Pearsonema plica) infection in a dog with chronic pollakiuria: challenges in the diagnosis and treatment.
Basso, W., Spänhauer, Z., Arnold, S., & Deplazes, P. (2014) · Parasitology international · doi:10.1016/j.parint.2013.09.002 · Cited by 34
“In Europe, it is a frequent parasite of red foxes (Vulpes vulpes) with prevalences of 23.5% in The Netherlands [2], 78% in Germany [3], 93.3% in Lithuania [4], 53% in Norway [5], 80.5% in Denmark [6], 52% in Hungary [7] and 59% in Switzerland and Lichtenstein [8].”
BackgroundInfluential
In vitro activity of a serine protease from Monacrosporium thaumasium fungus against first-stage larvae of Angiostrongylus vasorum
Soares, F. E. F., Braga, F. R., Araújo, J. V., Lima, W. D. S., Mozer, L. R., & Queiroz, J. H. (2012) · Parasitology Research · doi:10.1007/s00436-011-2781-x · Cited by 34
“Angiostrongylus vasorum can cause serious consequences for its definitive hosts (domestic dogs and wild canids) (Oliveira et al. 2006; Saeed et al. 2006).”
Background
The prevalence and distribution of Alaria alata, a potential zoonotic parasite, in foxes in Ireland
Murphy, T. M., O’Connell, J., Berzano, M., Dold, C., Keegan, J. D., McCann, A., Murphy, D., & Holden, N. M. (2012) · Parasitology Research · doi:10.1007/s00436-012-2835-8 · Cited by 33 · see citing works
“carnivores elsewhere in continental Europe and Turkey (Borgsteede 1984; Saeed et al. 2006; Gicik et al. 2009; Mohl et al. 2009).”
Distribution of Angiostrongylus vasorum and its gastropod intermediate hosts along the rural–urban gradient in two cities in the United Kingdom, using real time PCR
Aziz, N. A., Daly, E. E., Allen, S., Rowson, B., Greig, C., Forman, D., & Morgan, E. (2016) · Parasites & Vectors · doi:10.1186/s13071-016-1338-3 · Cited by 33 · see citing works
Combining information from surveys of several species to estimate the probability of freedom from Echinococcus multilocularis in Sweden, Finland and mainland Norway
Wahlström, H., Isomursu, M., Hallgren, G., Christensson, D., Cedersmyg, M., Wallensten, A., Hjertqvist, M., Davidson, R., Uhlhorn, H., & Hopp, P. (2011) · Acta Veterinaria Scandinavica · doi:10.1186/1751-0147-53-9 · Cited by 33 · see citing works
“In Sweden, Finland and Norway, the climate is favourable for EM and susceptible hosts occur [13], hence it is possible that EM could be established if accidentally introduced.”
Background
Endoparasites of the Coyote (Canis latrans), a Recent Migrant to Insular Newfoundland
Bridger, K. E., Baggs, E., & Finney-Crawley, J. (2009) · Journal of Wildlife Diseases · doi:10.7589/0090-3558-45.4.1221 · Cited by 33
Parasite species of the endangered Iberian wolf (Canis lupus signatus) and a sympatric widespread carnivore
Figueiredo, A., Oliveira, L., de Carvalho, L. M. M., Fonseca, C., & Torres, R. (2016) · International Journal for Parasitology: Parasites and Wildlife · doi:10.1016/j.ijppaw.2016.04.002 · Cited by 32 · see citing works
“Likewise, the parasites found in the red fox had been previously described in Portugal (Carvalho-Varela and Marcos, 1993; Eira et al., 2006; Guerra, 2012; Silva et al., 2012) and in other European countries (Mizgajska et al., 2000; Saeed et al., 2006; Magi et al., 2009; Al-Sabi and Kapel.”
Background
Canine bladderworm (Capillaria plica) infection associated with glomerular amyloidosis.
Callegari, D., Kramer, L. D., Cantoni, A., Lecce, R. D., Dodi, P., & Grandi, G. (2010) · Veterinary parasitology · doi:10.1016/j.vetpar.2009.11.008 · Cited by 32
“Epidemiological studies in the fox, for example, report prevalences of infection that range from 50% to 80% (Sréter et al., 2003; Saeed et al., 2006).”
Background
Predators in northern Germany are reservoirs for parasites of One Health concern
Waindok, P., Raue, K., Grilo, M. L., Siebert, U., & Strübe, C. (2021) · Parasitology Research · doi:10.1007/s00436-021-07073-3 · Cited by 35 · see citing works
Detection of specific antibodies in cats infected with the lung nematode Aelurostrongylus abstrusus.
Zottler, E., Strube, C., & Schnyder, M. (2017) · Veterinary parasitology · doi:10.1016/j.vetpar.2017.01.015 · Cited by 30 · see citing works
“Infections with C. aerophila may occur, as dogs and in particular foxes are frequently infected with this parasite (Hauser et al., 2015; Magi et al., 2015; Saeed et al., 2006).”
Background
Occurrence of Mesocestoides canislagopodis (Rudolphi, 1810) (Krabbe, 1865) in mammals and birds in Iceland and its molecular discrimination within the Mesocestoides species complex
Skírnisson, K., Jouet, D., Ferté, H., & Nielsen, Ó. (2016) · Parasitology Research · doi:10.1007/s00436-016-5006-5 · Cited by 30
Laboratory assessment of sensitive molecular tools for detection of low levels of Echinococcus multilocularis-eggs in fox (Vulpes vulpes) faeces
Øines, Ø., Isaksson, M., Hagström, Å., Tavornpanich, S., & Davidson, R. (2014) · Parasites & Vectors · doi:10.1186/1756-3305-7-246 · Cited by 30
“Echinococcus multilocularis was first detected in mainland Fennoscandia in Denmark in 2005 [7]”
Background
Host-specific serological response to Angiostrongylus vasorum infection in red foxes (Vulpes vulpes): implications for parasite epidemiology
Gillis-Germitsch, N., Kapel, C., Thamsborg, S., Deplazes, P., & Schnyder, M. (2017) · Parasitology · doi:10.1017/s0031182017000427 · Cited by 28
“Over the last decades, increasing local and regional prevalence (Saeed et al. 2006; Morgan et al. 2008; Al-Sabi et al. 2013; Eleni et al. 2014; McCarthy et al. 2016) and accumulating reports of new endemic areas indicate an increased transmission and apparent geographical spread (Sréter et al.…”
BackgroundSelf-citation
Bioaccumulation of cadmium, lead and zinc in liver and kidney of red fox (Vulpes vulpes) from NW Spain: influence of gender and age
Pérez-López, M., Rodríguez, F. S., Hernández-Moreno, D., Rigueira, L., Fidalgo, L., & Beceiro, A. (2016) · Toxicological & Environmental Chemistry Reviews · doi:10.1080/02772248.2015.1107065 · Cited by 28 · see citing works
“The age of the animal was estimated by the general size, the animal’s dental development, and the degree of sexual maturity (Saeed et al. 2006; Cardoso et al., 2013).”
Background
Seroepidemiological survey and spatial analysis of the occurrence of Angiostrongylus vasorum in Swiss dogs in relation to biogeographic aspects.
Lurati, L., Deplazes, P., Hegglin, D., & Schnyder, M. (2015) · Veterinary parasitology · doi:10.1016/j.vetpar.2015.08.017 · Cited by 28 · see citing works
“vasorum detected at necropsy varies between 5% and 80% in Europe (Sreter et al., 2003; Saeed et al., 2006; Magi et al., 2009a) and up to 56% on Newfoundland island (Jeffery et al.”
Background
Eucoleus boehmi infection in red fox (Vulpes vulpes) from Italy
Veronesi, F., Morganti, G., Cesare, A. D., Lepri, E., Cassini, R., Zanet, S., Deni, D., Chiari, M., & Ferroglio, E. (2014) · Veterinary Parasitology · doi:10.1016/j.vetpar.2014.10.001 · Cited by 30 · see citing works
Opisthorchiidosis--a review.
Schuster, R. (2010) · Infectious Diseases - Drug Targets · doi:10.2174/187152610793180902 · Cited by 28
Distribution of Eurasian otter biliary parasites, Pseudamphistomum truncatum and Metorchis albidus (Family Opisthorchiidae), in England and Wales
Sherrard-Smith, E., Cable, J., & Chadwick, E. (2009) · Parasitology · doi:10.1017/s0031182009006362 · Cited by 28 · see citing works
Present status, actions taken and future considerations due to the findings of E. multilocularis in two Scandinavian countries.
Wahlström, H., Enemark, H., Davidson, R., & Oksanen, A. (2015) · Veterinary parasitology · doi:10.1016/j.vetpar.2015.07.037 · Cited by 27
A walk on the wild side: A review of the epidemiology of Toxocara canis and Toxocara cati in wild hosts
Holland, C. V. (2023) · International Journal for Parasitology Parasites and Wildlife · doi:10.1016/j.ijppaw.2023.10.008 · Cited by 29 · see citing works
“For example, Martinez-Carrasco et al. (2007) recorded prevalences of 12.5% by egg count versus 45.5% by worm count and Saeed and Kapel (2006) recorded prevalence based on eggs as 41%, but that based on worms as 76%.”
BackgroundInfluential
Cardiopulmonary nematodes of wild carnivores from Denmark: Do they serve as reservoir hosts for infections in domestic animals?
Lemming, L., Jørgensen, A. C., Nielsen, L. B., Nielsen, S. T., Mejer, H., Chriel, M., & Petersen, H. H. (2020) · International Journal for Parasitology: Parasites and Wildlife · doi:10.1016/j.ijppaw.2020.08.001 · Cited by 26 · see citing works
Epizootic and zoonotic helminths of the bobcat (Lynx rufus) in Illinois and a comparison of its helminth component communities across the American Midwest
Hiestand, S. J., Nielsen, C., & Jiménez, F. (2014) · Parasite · doi:10.1051/parasite/2014005 · Cited by 26
“This could be influenced by temperature changes, ability for larval development in the environment, and potential seasonal dietary shifts and how that may impact transmission from intermediate hosts [56].”
Protothecal pyogranulomatous meningoencephalitis in a dog without evidence of disseminated infection
Márquez, M., Ródenas, S., Molín, J., Rabanal, R., Fondevila, D., Añor, S., & Pumarola, M. (2012) · The Veterinary Record · doi:10.1136/vr.100661 · Cited by 26
High prevalence of Capillaria plica infections in red foxes (Vulpes vulpes) in Southern Germany
Bork-Mimm, S., & Rinder, H. (2011) · Parasitology Research · doi:10.1007/s00436-010-2196-0 · Cited by 26
Alaria alata in Terms of Risks to Consumers’ Health
Korpysa-Dzirba, W., Różycki, M., Bilska-Zając, E., Karamon, J., Sroka, J., Bełcik, A., Wasiak, M., & Cencek, T. (2021) · Foods · doi:10.3390/foods10071614 · Cited by 27 · see citing works
Unravelling the genetic diversity and relatedness of Echinococcus multilocularis isolates in Eurasia using the EmsB microsatellite nuclear marker.
Umhang, G., Bastid, V., Avcioglu, H., Bagrade, G., Bujanić, M., Čabrilo, O. B., Casulli, A., Dorny, P., van der Giessen, J., Guven, E., et al. (2021) · Infection, Genetics and Evolution · doi:10.1016/j.meegid.2021.104863 · Cited by 25
Epidemiological survey of zoonotic helminths in feral cats in Gran Canaria island (Macaronesian archipelago-Spain)
Rodríguez-Ponce, E., González, J. F., de Felipe, M. C., Hernández, J. N., & Jaber, J. R. (2016) · Acta Parasitologica · doi:10.1515/ap-2016-0059 · Cited by 27 · see citing works
Viability of Cryptocotyle lingua metacercariae from Atlantic cod (Gadus morhua) after exposure to freezing and heating in the temperature range from −80 °C to 100 °C
Borges, J. N., Skov, J., Bahlool, Q. Z. M., Møller, O., Kania, P., Santos, C. P., & Buchmann, K. (2015) · doi:10.1016/j.foodcont.2014.09.021 · Cited by 25
Molecular and morphometric study of metacercariae and adults of Pseudamphistomum truncatum (Opisthorchiidae) from roach (Rutilus rutilus) and wild American mink (Mustela vison).
Skov, J., Kania, P., Jørgensen, T. R., & Buchmann, K. (2008) · Veterinary parasitology · doi:10.1016/j.vetpar.2008.05.011 · Cited by 24
Levels of infection of intestinal helminth species in the golden jackal Canis aureus from Serbia.
Ćirović, D., Pavlović, I., Penezić, A., Kulišić, Z., & Selaković, S. (2015) · Journal of Helminthology · doi:10.1017/s0022149x13000552 · Cited by 24
Wild Red Foxes (Vulpes vulpes) as Sentinels of Parasitic Diseases in the Province of Soria, Northern Spain
Lledó, L., Giménez-Pardo, C., Saz, J. V., & Serrano, J. L. (2015) · Vector Borne and Zoonotic Diseases · doi:10.1089/vbz.2014.1766 · Cited by 23 · see citing works
“In Italy a prevalence of 9.1% has been reported (Magi et al. 2009), in Germany 26.5% (Pfeiffer et al. 1997), in the United Kingdom 55.9% (Richards et al. 1995), and in Denmark 59.4% (Saeed et al. 2006).”
Influential
Genetically distinct isolates of Spirocerca sp. from a naturally infected red fox (Vulpes vulpes) from Denmark.
Al-Sabi, M. N. S., Hansen, M. S., Chriel, M., Holm, E., Larsen, G., & Enemark, H. (2014) · Veterinary parasitology · doi:10.1016/j.vetpar.2014.07.002 · Cited by 23

Authors: Saeed, I., Maddox-Hyttel, C., Monrad, J., & Kapel, C. M. O.
Corresponding author: Saeed, I.
ORCID: Saeed, I.
Kapel, C.M.O.
Venue: Veterinary Parasitology
Publisher: Elsevier BV
Published: 2006-06
Volume: 139
Issue: 1-3
Pages: 168-179
ISSN: 0304-4017 (ISSN-L)
DOI: 10.1016/j.vetpar.2006.02.015
OpenAlex: W2091646424
Cited by: 250
References: 0
Citations by year: 2026: 2 · 2025: 9 · 2024: 6 · 2023: 8 · 2022: 4 · 2021: 16 · 2020: 19 · 2019: 17 · 2018: 9 · 2017: 14 · 2016: 16 · 2015: 22 · 2014: 22 · 2013: 21 · 2012: 9
FWCI: 16.30
Type: journal article
Language: en
Open access: green
pubmed.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Veterinary Parasitology (publishedVersion)
PubMed (publishedVersion)
Research at the University of Copenhagen (University of Copenhagen) (publishedVersion)
Technical University of Denmark, DTU Orbit (Technical University of Denmark, DTU) (submittedVersion)
Zenodo (CERN European Organization for Nuclear Research) (submittedVersion)
Topics: Health Sciences › Veterinary › Small Animals › Helminth infection and control
Physical Sciences › Environmental Science › Ecology › Parasite Biology and Host Interactions
Health Sciences › Medicine › Pathology and Forensic Medicine › Parasitic infections in humans and animals
Keywords: helminths, red fox, nematodes, cestodes, trematodes, Acanthocephala, Toxocara canis, Angiostrongylus vasorum, Capillaria, Taenia, Echinococcus multilocularis, Cryptocotyle lingua, Alaria alata, parasite prevalence, geographic distribution, host age and sex effects, Denmark
MeSH terms: Age Factors, Animals, Animals, Wild, Cestoda, Denmark, Female, Foxes, Helminthiasis, Animal, Helminths, Male, Nematoda, Phylogeny, Seasons, Sex Factors, Trematoda

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Helminths of red foxes (Vulpes vulpes) in Denmark

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