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Cited by 71Parasitic infections in humans and animalsHelminth infection and controlParasite Biology and Host Interactions

Prevalence of intestinal helminths of red foxes (Vulpes vulpes) in central Europe (Poland): A significant zoonotic threat

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Karamon, Jacek, Dąbrowska, Joanna, Kochanowski, Maciej, Samorek-Pieróg, Małgorzata, Sroka, Jacek, Różycki, Mirosław, Bilska-Zając, Ewa, Zdybel, Jolanta +1 more·2018·Parasites & Vectors
DOI 10.1186/s13071-018-3021-3PMC PMC6064108
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Abstract

BACKGROUND: The red fox (Vulpes vulpes) is widely distributed in the world; in central Europe, it is the most numerous wild species of the family Canidae. It can play the role of a definitive host for many intestinal parasites, including zoonotic helminths. Poland, with its geographical location (central Europe), is an interesting area for parasitological investigations of this species. The aim of this study was to evaluate and compare the prevalence of intestinal helminths in red foxes in different regions of Poland. METHODS: Intestines of 473 red foxes from four different regions were examined using the sedimentation and counting technique (SCT). In addition, 344 samples of faeces were examined using flotation. RESULTS: Overall, intestinal helminths were found in 98.9% of red foxes. The average prevalence of detected parasites was as follows: Mesocestoides spp. (84.1%); hookworms (67.9%); Alaria alata (61.5%); Toxocara/Toxascaris (49.5%); Taenia spp. (42.5%); Echinococcus multilocularis (25.6%); and Trichuris vulpis (2.3%). The prevalence of the majority of parasite species was similar in each region. Significant differences between regions were observed in the case of E. multilocularis: a low prevalence in the south-western and northern regions (0% and 0.9%, respectively) and a high prevalence in the south-east and northeast (39.3% and 42.7%, respectively). In the case of A. alata, important differences were found between northern (96.5% and 93.7% in northern and northeast regions, respectively) and southern regions (15.2% and 24.7% for south-western and south-east regions, respectively). The percentage of positive samples obtained with coproscopic examination (except for Trichuris) was significantly lower than that obtained with SCT. Analysis of the prevalence estimated in individual regions with the use of both methods (flotation and SCT) showed a high correlation for all parasite species (except for Mesocestoides spp.). The flotation method also allowed us to detect the eggs of the lung nematode Eucoleus aerophilus (syn. Capillaria aerophila) (76.2% of positive foxes). CONCLUSIONS: This study showed a very high percentage of red foxes infected with intestinal helminths in different parts of Poland. Depending on the location, some differences were observed regarding the prevalence of dangerous zoonotic parasites, which should be considered in the assessment of infection risk for humans.

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References 53 · Cited by 71

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  1. [1]Borecka A Gawor J Malczewska M Malczewski A Occurence of Echinococcus multilocularis in red foxes (Vulpes vulpes) in southern Poland Helminthologia 2008 45 24 27 10.2478/s11687-008-0004-5 · DOI
  2. [2]Oksanen A Siles-Lucas M Karamon J Possenti A Conraths FJ Romig T The geographical distribution and prevalence of Echinococcus multilocularis in animals in the European Union and adjacent countries: a systematic review and meta-analysis Parasit Vectors 2016 9 519 10.1186/s13071-016-1746-4 27682156 PMC5039905 · DOI
  3. [4]Bruzinskaite-Schmidhalter R Sarkunas M Malakauskas A Mathis A Torgerson PR Deplazes P Helminths of red foxes (Vulpes vulpes) and raccoon dogs (Nyctereutes procyonoides) in Lithuania Parasitology 2012 139 120 127 10.1017/S0031182011001715 21996514 · DOI · Paper page
  4. [5]Al-Sabi MNS Chriél M Jensen TH Enemark HL Endoparasites of the raccoon dog (Nyctereutes procyonoides) and the red fox (Vulpes vulpes) in Denmark 2009–2012 - a comparative study Int J Parasitol Parasites Wildl 2013 2 144 151 10.1016/j.ijppaw.2013.04.001 24533328 PMC3862527 · DOI
  5. [7]Schuster RK Shimalov VV A comparative study of helminths of raccoon dogs (Nyctereutes procynoides) and red foxes (Vulpes vulpes) sharing the same territory Asian Pac J Trop Dis 2017 7 708 714 10.12980/apjtd.7.2017D7-259 · DOI · Paper page
  6. [8]Jankovska I Brozova A Mateju Z Langrova I Lukesova D Sloup V Parasites with possible zoonotic potential in the small intestines of red foxes (Vulpes vulpes) from Northwest Bohemia (CzR) Helminthologia 2016 53 290 293 10.1515/helmin-2016-0028 · DOI · Paper page
  7. [10]Umhang G, Comte S, Raton V, Hormaz V, Boucher JM, Favier S, et al. Echinococcus multilocularis infections in dogs from urban and peri-urban areas in France. Parasitol Res. 2014;113:2219–22. 24687286
  8. [11]Petavy AF Tenora F Deblock S Sergent V Echinococcus multilocularis in domestic cats in France - a potential risk factor for alveolar hydatid disease contamination in humans Vet Parasitol 2000 87 151 156 10.1016/S0304-4017(99)00181-8 10622606 · DOI
  9. [12]Nijsse R Mughini-Gras L Wagenaar JA Franssen F Ploeger HW Environmental contamination with Toxocara eggs: a quantitative approach to estimate the relative contributions of dogs, cats and foxes, and to assess the efficacy of advised interventions in dogs Parasit Vectors 2015 8 397 10.1186/s13071-015-1009-9 26216217 PMC4517363 · DOI
  10. [13]Karamon J Kochanowski M Sroka J Cencek T Różycki M Chmurzyńska E Bilska-Zając E The prevalence of Echinococcus multilocularis in red foxes in Poland - current results (2009–2013) Parasitol Res 2014 113 317 322 10.1007/s00436-013-3657-z 24221887 PMC3898514 · DOI · Paper page
  11. [16]Karamon J, Sroka J, Cencek T, Michalski MM, Zieba P, Karwacki J. Prevalence of Echinococcus multilocularis in red foxes in two eastern provinces of Poland. Bull Vet Inst Pulawy. 2011;55:429–33.
  12. [17]Malczewski A Gawor J Malczewska M Infection of red foxes (Vulpes vulpes) with Echinococcus multilocularis during the years 2001–2004 in Poland Parasitol Res 2008 103 501 505 10.1007/s00436-008-0990-8 18536937 · DOI
  13. [18]Malczewski A Rocki B Ramisz A Eckert J Echinococcus multilocularis (Cestoda), the causative agent of alveolar echinococcosis in humans - first record in Poland J Parasitol 1995 81 318 321 10.2307/3283945 7707218 · DOI
  14. [22]Karamon J Samorek-Pierog M Moskwa B Rozycki M Bilska-Zajac E Zdybel J Wlodarczyk M Intestinal helminths of raccoon dogs (Nyctereutes procyonoides) and red foxes (Vulpes vulpes) from the Augustow Primeval Forest (north-eastern Poland) J Vet Res 2016 60 273 277 10.1515/jvetres-2016-0042 · DOI · Paper page
  15. [23]Sommer R, Benecke N. Late Pleistocene and early Holocene history of the canid fauna of Europe (Canidae). Mamm Biol. 2005;70:227–41.
  16. [24]Nakao M Xiao N Okamoto M Yanagida T Sako Y Ito A Geographic pattern of genetic variation in the fox tapeworm Echinococcus multilocularis Parasitol Int 2009 58 384 389 10.1016/j.parint.2009.07.010 19651237 · DOI
  17. [25]Hofer S Gloor S Muller U Mathis A Hegglin D Deplazes P High prevalence of Echinococcus multilocularis in urban red foxes (Vulpes vulpes) and voles (Arvicola terrestris) in the city of Zurich, Switzerland Parasitology 2000 120 135 142 10.1017/S0031182099005351 10726275 · DOI
  18. [27]Raynaud JP. Etude de l’efficacite d’une technique de coproscopie quantitative pour le diagnostic de routine et le controle des infestations parasitaires des bovins, ovins, equins et porcins. Ann Parasitol Hum Comp. 1970;45:321–42. 5531507
  19. [28]Newcombe RG Two-sided confidence intervals for the single proportion: comparison of seven methods Stat Med 1998 17 857 872 10.1002/(SICI)1097-0258(19980430)17:8<857::AID-SIM777>3.0.CO;2-E 9595616 · DOI · Paper page
  20. [29]Zalesny G Hildebrand J Molecular identification of Mesocestoides spp. from intermediate hosts (rodents) in central Europe (Poland) Parasitol Res 2012 110 1055 1061 10.1007/s00436-011-2598-7 21847599 · DOI
  21. [30]Hrckova G Miterpakova M O’Connor A Snabel V Olson PD Molecular and morphological circumscription of Mesocestoides tapeworms from red foxes (Vulpes vulpes) in central Europe Parasitology 2011 138 638 647 10.1017/S0031182011000047 21349216 · DOI
  22. [31]Magi M Guardone L Mignone W Prati MC Macchioni F Intestinal helminths of red foxes (Vulpes vulpes) in north-west Italy Helminthologia 2016 53 31 38 10.1515/helmin-2015-0073 · DOI · Paper page
  23. [32]Szell Z Tolnai Z Sreter T Environmental determinants of the spatial distribution of Mesocestoides spp. and sensitivity of flotation method for the diagnosis of mesocestoidosis Vet Parasitol 2015 212 427 430 10.1016/j.vetpar.2015.06.021 26150263 · DOI
  24. [34]Pfeiffer F, Kuschfeldt S, Stoye M. Helminth fauna of the red fox (Vulpes vulpes Linne 1758) in the south of Saxe-Anhalt - 1. Cestodes. Dtsch Tierarztl Wochenschr. 1997;104:445–8 (In German). 9445786
  25. [36]Richards DT Harris S Lewis JW Epidemiologic studies on intestinal helminth parasites of rural and urban red foxes (Vulpes vulpes) in the United Kingdom Vet Parasitol 1995 59 39 51 10.1016/0304-4017(94)00736-V 7571336 · DOI
  26. [38]Al-Sabi MNS Halasa T Kapel CMO Infections with cardiopulmonary and intestinal helminths and sarcoptic mange in red foxes from two different localities in Denmark Acta Parasitol 2014 59 98 107 10.2478/s11686-014-0214-6 24570055 · DOI
  27. [39]Papadopoulos H Himonas C Papazahariadou M Antoniadou-Sotiriadou K Helminths of foxes and other wild carnivores from rural areas in Greece J Helminthol 1997 71 227 231 10.1017/S0022149X00015960 9705680 · DOI
  28. [41]Murphy TM O’Connell J Berzano M Dold C Keegan JD McCann A The prevalence and distribution of Alaria alata, a potential zoonotic parasite, in foxes in Ireland Parasitol Res 2012 111 283 290 10.1007/s00436-012-2835-8 22350672 · DOI · Paper page
  29. [42]Miterpakova M Hurnikova Z Antolova D Dubinsky P Endoparasites of red fox (Vulpes vulpes) in the Slovak Republic with the emphasis on zoonotic species Echinococcus multilocularis and Trichinella spp Helminthologia 2009 46 73 79 10.2478/s11687-009-0015-x · DOI
  30. [43]Denzin N Schliephake A Froehlich A Ziller M Conraths FJ On the move? Echinococcus multilocularis in red foxes of Saxony-Anhalt (Germany) Transbound Emerg Dis 2014 61 239 246 10.1111/tbed.12026 23134586 · DOI
  31. [44]Karamon J, Kochanowski M, Dąbrowska J, Sroka J, Różycki M, Bilska-Zając E, Cencek T. Dynamics of Echinococcus multilocularis infection in red fox populations with high and low prevalence of this parasite in Poland (2007–2014). Bull Vet Inst Pulawy. 2015;59:213–7.
  32. [45]Karamon J Stojecki K Samorek-Pierog M Bilska-Zajac E Rozycki M Chmurzynska E Genetic diversity of Echinococcus multilocularis in red foxes in Poland: the first report of a haplotype of probable Asian origin Folia Parasitol 2017 64 007 10.14411/fp.2017.007 28360380 · DOI
  33. [46]Umhang G Karamon J Hormaz V Knapp J Cencek T Boue F A step forward in the understanding of the presence and expansion of Echinococcus multilocularis in eastern Europe using microsatellite EmsB genotyping in Poland Infect Genet Evol 2017 54 176 182 10.1016/j.meegid.2017.07.004 28688974 · DOI
  34. [47]Karamon J Samorek-Pierog M Kochanowski M Dabrowska J Sroka J Golab E First detection of Echinococcus multilocularis in dogs in a highly endemic area of Poland Folia Parasitol 2016 63 018 10.14411/fp.2016.018 27311792 · DOI
  35. [48]Shimalov VV Shimalov VT Helminth fauna of the red fox (Vulpes vulpes Linnaeus, 1758) in southern Belarus Parasitol Res 2003 89 77 78 12474048
  36. [50]Lalosevic V Lalosevic D Capo I Simin V Galfi A Traversa D High infection rate of zoonotic Eucoleus aerophilus infection in foxes from Serbia Parasite 2013 20 3 10.1051/parasite/2012003 23340229 PMC3718516 · DOI
  37. [51]Davidson RK Gjerde B Vikoren T Lillehaug A Handeland K Prevalence of Trichinella larvae and extra-intestinal nematodes in Norwegian red foxes (Vulpes vulpes) Vet Parasitol 2006 136 307 316 10.1016/j.vetpar.2005.11.015 16378689 · DOI
  38. [52]Tolnai Z Szell Z Sreter T Environmental determinants of the spatial distribution of Angiostrongylus vasorum, Crenosoma vulpis and Eucoleus aerophilus in Hungary Vet Parasitol 2015 207 355 358 10.1016/j.vetpar.2014.12.008 25547643 · DOI
  39. [53]Magi M Guardone L Prati MC Mignone W Macchioni F Extraintestinal nematodes of the red fox Vulpes vulpes in north-west Italy J Helminthol 2015 89 506 511 10.1017/S0022149X1400025X 24725462 · DOI

Authors
Karamon, J., Dąbrowska, J., Kochanowski, M., Samorek-Pieróg, M., Sroka, J., Różycki, M., Bilska-Zając, E., Zdybel, J., & Cencek, T.
Affiliations
National Veterinary Research Institute (PL)
Corresponding author
Karamon, Jacek
ORCID
Venue
Parasites & Vectors
Publisher
Springer Science and Business Media LLC
Published
2018-07-28
Volume
11
Issue
1
Pages
436-436
ISSN
1756-3305 (ISSN-L)
DOI
10.1186/s13071-018-3021-3
PMC
PMC6064108
OpenAlex
W2883779655
Cited by
71
References
53
Citations by year
2026: 5 · 2025: 7 · 2024: 7 · 2023: 10 · 2022: 8 · 2021: 12 · 2020: 10 · 2019: 11 · 2018: 1
FWCI
6.47
Type
journal article
Language
en
Open access
Licence
Locations
  • Parasites & Vectors (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, other-oa)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Polish Ministry of Science and Higher Education (NN 308 631 938)
  • Krajowy Naukowy Osrodek Wiodacy (05-1/KNOW2/2015)
Topics
  • Health Sciences › Medicine › Pathology and Forensic Medicine › Parasitic infections in humans and animals
  • Health Sciences › Veterinary › Small Animals › Helminth infection and control
  • Physical Sciences › Environmental Science › Ecology › Parasite Biology and Host Interactions
Keywords
red fox, intestinal helminths, helminth prevalence, zoonotic parasites, Echinococcus multilocularis, Alaria alata, Mesocestoides, hookworm, Toxocara, Taenia, Eucoleus aerophilus, fecal flotation, parasite detection methods
MeSH terms
Animals, Feces, Foxes, Helminthiasis, Animal, Intestinal Diseases, Parasitic, Intestines, Poland, Zoonoses

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