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A grid-cell based fecal sampling scheme reveals: land-use and altitude affect prevalence rates of Angiostrongylus vasorum and other parasites of red foxes (Vulpes vulpes)

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Abstract

In view of the role of foxes as a reservoir for Angiostrongylus vasorum, a nematode of the heart and lungs of dogs and foxes, its occurrence across Switzerland was investigated in foxes applying a standardized sampling scheme for fox fecal samples. In 72 study areas, which consisted of three 1-km2 grid cells, a total of 1481 samples were collected by walking transects following linear features in the terrain, and analyzed by a flotation-sieving method. The overall prevalence rate of A. vasorum in fecal samples was 8.8% (95% confidence interval, CI 7.4–10.3%), being significantly higher in the Swiss Plateau (11.4%, CI. 9.4–13.8%) compared with other bioregions, and more prevalent in areas with less than 50% of cultivated land (p = 0.043). Prevalence rates increased with decreasing altitudes being significantly higher below 400 m above sea level (20.6%, 95% CI 15.2–26.9%), while all samples collected above 900 m asl were negative. Eggs of Toxocara sp. (12.1%), Taeniidae (10.5%), Capillaria spp. (8.3%), Trichuris vulpis (5.5%), hookworms (5.3%), Toxascaris leonina (1.3%) and Strongyloides sp. (0.4%) were furthermore identified. Taeniid eggs were positively and Capillaria spp. negatively associated with the amount of cultivated land. The prevalence rates based on our fecal analyses were generally lower compared with previous studies from Switzerland which were based on fox necropsies. However, the grid cell–based sampling scheme with replicable transects for fox feces collection proved to be a suitable, non-invasive method for parasitic large-scale surveys providing information on the relative infectious pressure for the local dog population.

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References

  • Alho AM, Schnyder M, Meireles J, Belo S, Deplazes P, Madeira de Carvalho L (2014) Preliminary results on the seroprevalence of Angiostrongylus vasorum and co-infection with Dirofilaria immitis in shelter dogs from Portugal. Parasit Vectors 7(Suppl 1):O26 http://www.parasitesandvectors.com/content/7/S1/O26

  • Al-Sabi MN, Halasa T, Kapel CM (2014) Infections with cardiopulmonary and intestinal helminths and sarcoptic mange in red foxes from two different localities in Denmark. Acta Parasitol 59:98–107. https://doi.org/10.2478/s11686-014-0214-6

    Article  PubMed  Google Scholar 

  • Barutzki D, Schaper R (2009) Natural infections of Angiostrongylus vasorum and Crenosoma vulpis in dogs in Germany (2007-2009). Parasitol Res 105(Suppl 1):S39–S48

    Article  PubMed  Google Scholar 

  • Beerli O, Guerra D, Baltrunaite L, Deplazes P, Hegglin D (2017) Microtus arvalis and Arvicola scherman: key players in the Echinococcus multilocularis life cycle. Front Vet Sci 4:216. https://doi.org/10.3389/fvets.2017.00216

    Article  PubMed  PubMed Central  Google Scholar 

  • Bolt G, Monrad J, Henriksen P, Dietz HH, Koch J, Bindseil E, Jensen AL (1992) The fox (Vulpes vulpes) as a reservoir for canine angiostrongylosis in Denmark. Field survey and experimental infections. Acta Vet Scand 33:357–362

    CAS  PubMed  Google Scholar 

  • Borgsteede FH (1984) Helminth parasites of wild foxes (Vulpes vulpes L.) in the Netherlands. Z Parasitenkd 70:281–285

    Article  CAS  PubMed  Google Scholar 

  • Boschi C (2011) Die Schneckenfauna der Schweiz - Porträts aller Schweizer Schneckenarten. Haupt publisher, Berne

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Burlet P, Deplazes P, Hegglin D (2011) Age, season and spatio-temporal factors affecting the prevalence of Echinococcus multilocularis and Taenia taeniaeformis in Arvicola terrestris. Parasit Vectors 4:6. https://doi.org/10.1186/1756-3305-4-6

    Article  PubMed  PubMed Central  Google Scholar 

  • Cabanova V, Miterpakova M, Druga M, Hurnikova Z, Valentova D (2018) GIS-based environmental analysis of fox and canine lungworm distribution: an epidemiological study of Angiostrongylus vasorum and Crenosoma vulpis in red foxes from Slovakia. Parasitol Res 117:521–530. https://doi.org/10.1007/s00436-017-5728-z

    Article  PubMed  Google Scholar 

  • Chapman PS, Boag AK, Guitian J, Boswood A (2004) Angiostrongylus vasorum infection in 23 dogs (1999-2002). J Small Anim Pract 45:435–440

    Article  CAS  PubMed  Google Scholar 

  • Clopper CJ, Pearson ES (1934) The use of confidence or fiducial limits illustrated in the case of the binomial. Biometrika 26:404–413

    Article  Google Scholar 

  • Cuillé J, Darraspen E (1930) De la Strongylose cardio-pulmonaire du chien. Rev Gén de Méd Vét 466:625–639 694–710

    Google Scholar 

  • Deplazes P, Eckert J (1996) Diagnosis of the Echinococcus multilocularis infection in final hosts. Appl Parasitol 37:245–252

    CAS  PubMed  Google Scholar 

  • Deplazes P, Eckert J (2001) Veterinary aspects of alveolar echinococcosis--a zoonosis of public health significance. Vet Parasitol 98:65–87

    Article  CAS  PubMed  Google Scholar 

  • Deplazes P, Eckert J, Mathis A, von Samson-Himmelstjerna G, Zahner H (2016) Parasitology in veterinary medicine. Wageningen Academic Publishers, Wageningen

    Book  Google Scholar 

  • Dodd K (1973) Angiostrongylus vasorum (Baillet, 1866) infestation in a greyhound kennels. Vet Rec 92:195–197

    Article  CAS  PubMed  Google Scholar 

  • Ferdushy T, Hasan MT (2010) Survival of first stage larvae (L1) of Angiostrongylus vasorum under various conditions of temperature and humidity. Parasitol Res 107:1323–1327

    Article  PubMed  Google Scholar 

  • Fischer C, Réperant LA, Weber JM, Hegglin D, Deplazes P (2005) Echinococcus multlocularis infections of rural, residential and urban foxes (Vulpes vulpes) in the canton of Geneva, Switzerland. Parasite 12:339–346. https://doi.org/10.1051/parasite/2005124339

    Article  CAS  PubMed  Google Scholar 

  • Gerrikagoitia X, Barral M, Juste RA (2010) Angiostrongylus species in wild carnivores in the Iberian Peninsula. Vet Parasitol 174:175–180

    Article  CAS  PubMed  Google Scholar 

  • Gillis-Germitsch N, Kapel CMO, Thamsborg SM, Deplazes P, Schnyder M (2017) Host-specific serological response to Angiostrongylus vasorum infection in red foxes (Vulpes vulpes): implications for parasite epidemiology. Parasitology 144:1–10. https://doi.org/10.1017/S0031182017000427

    Article  CAS  Google Scholar 

  • Gloor S, Bontadina F, Hegglin D, Deplazes P, Breitenmoser U (2001) The rise of urban fox populations in Switzerland. Mamm Biol 66:155–164

    Google Scholar 

  • Gonseth Y, Wohlgemuth T, Sansonnens B, Buttler A (2001) Die biogeographischen Regionen der Schweiz. Erläuterungen und Einteilungsstandard. Umwelt Materialien 137, Bundesamt für Umwelt, Wald und Landschaft, Bern

  • Gottstein B (2001) Lungenwurm Angiostrongylus vasorum bei einem Fuchs in der Schweiz. BVET-Magazin 1:22

    Google Scholar 

  • Grandi G, Osterman Lind E, Schaper R, Schnyder M (2017) Canine angiostrongylosis in Sweden: a summary of five-year diagnostic activity (2011-2015) and a nationwide seroepidemiological survey using combined detection of specific antibodies and circulating antigens by ELISAs. Acta Vet Scand 59:85. https://doi.org/10.1186/s13028-017-0351-7

    Article  PubMed  PubMed Central  Google Scholar 

  • Guardone L, Schnyder M, Macchioni F, Deplazes P, Magi M (2013) Serological detection of circulating Angiostrongylus vasorum antigen and specific antibodies in dogs from central and northern Italy. Vet Parasitol 192:192–198. https://doi.org/10.1016/j.vetpar.2012.10.016

    Article  CAS  PubMed  Google Scholar 

  • Guerra D, Hegglin D, Bacciarini L, Schnyder M, Deplazes P (2014) Stability of the southern European border of Echinococcus multilocularis in the Alps: evidence that Microtus arvalis is a limiting factor. Parasitology:1–10. https://doi.org/10.1017/S0031182014000730

  • Guilhon J (1963) Recherches sur le cycle évolutif du Strongle des vaisseaux du chien. Bull Acad Vét Fr 36:431–442

    Article  Google Scholar 

  • Guilhon J, Bressou C (1960) Rôle des Limacidés dans le cycle évolutif d'Angiostrongylus vasorum (Baillet, 1866). C R Acad Sci 251:2252–2253

    CAS  Google Scholar 

  • Hartova-Nentvichova M, Salek M, Cerveny J, Koubek P (2010) Variation in the diet of the red fox (Vulpes vulpes) in mountain habitats: effects of altitude and season. Mamm Biol 75:334–340

    Article  Google Scholar 

  • Hausser J (1995) Atlas der Säugetiere der. Schweiz Ed Birkhäuser, Basel

    Google Scholar 

  • Helm J, Roberts L, Jefferies R, Shaw SE, Morgan ER (2015) Epidemiological survey of Angiostrongylus vasorum in dogs and slugs around a new endemic focus in Scotland. Vet Rec 172:46. https://doi.org/10.1136/vr.103006

    Article  Google Scholar 

  • Henry C, Poulle M-L, Roeder J-J (2005) Effect of sex and female reproductive status on seasonal home range size and stability in rural red foxes ( Vulpes vulpes ). Écoscience 12:202–209. https://doi.org/10.2980/i1195-6860-12-2-202.1

    Article  Google Scholar 

  • Hofer S, Gloor S, Muller U, Mathis A, Hegglin D, Deplazes P (2000) High prevalence of Echinococcus multilocularis in urban red foxes (Vulpes vulpes) and voles (Arvicola terrestris) in the city of Zurich, Switzerland. Parasitology 120(Pt 2):135–142

    Article  PubMed  Google Scholar 

  • Houpin E, McCarthy G, Ferrand M, De Waal T, O'Neill EJ, Zintl A (2016) Comparison of three methods for the detection of Angiostrongylus vasorum in the final host. Vet Parasitol 220:54–58. https://doi.org/10.1016/j.vetpar.2016.02.023

    Article  CAS  PubMed  Google Scholar 

  • Hurnikova Z, Miterpakova M, Mandelik R (2013) First autochthonous case of canine Angiostrongylus vasorum in Slovakia. Parasitol Res 112:3505–3508. https://doi.org/10.1007/s00436-013-3532-y

    Article  CAS  PubMed  Google Scholar 

  • Jefferies R, Morgan ER, Shaw SE (2009) A SYBR green real-time PCR assay for the detection of the nematode Angiostrongylus vasorum in definitive and intermediate hosts. Vet Parasitol 166:112–118

    Article  CAS  PubMed  Google Scholar 

  • Jeffery RA, Lankester MW, McGrath MJ, Whitney HG (2004) Angiostrongylus vasorum and Crenosoma vulpis in red foxes (Vulpes vulpes) in Newfoundland, Canada. Can J Zool 82:66–74

    Article  Google Scholar 

  • Jolly S, Poncelet L, Lempereur L, Caron Y, Bayrou C, Cassart D, Grimm F, Losson B (2015) First report of a fatal autochthonous canine Angiostrongylus vasorum infection in Belgium. Parasitol Int 64:97–99. https://doi.org/10.1016/j.parint.2014.10.008

    Article  PubMed  Google Scholar 

  • Kleijn D, Baquero RA, Clough Y, Diaz M, De Esteban J, Fernandez F, Gabriel D, Herzog F, Holzschuh A, Johl R, Knop E, Kruess A, Marshall EJ, Steffan-Dewenter I, Tscharntke T, Verhulst J, West TM, Yela JL (2006) Mixed biodiversity benefits of agri-environment schemes in five European countries. Ecol Lett 9:243–254; discussion 254-247. https://doi.org/10.1111/j.1461-0248.2005.00869.x

    Article  CAS  PubMed  Google Scholar 

  • Koch J, Willesen JL (2009) Canine pulmonary angiostrongylosis: An update. Vet J 179:348–359

    Article  CAS  PubMed  Google Scholar 

  • Lurati L, Deplazes P, Hegglin D, Schnyder M (2015) Seroepidemiological survey and spatial analysis of the occurrence of Angiostrongylus vasorum in Swiss dogs in relation to biogeographic aspects. Vet Parasitol 212:219–226. https://doi.org/10.1016/j.vetpar.2015.08.017

    Article  CAS  PubMed  Google Scholar 

  • Magi M, Macchioni F, Dell’Omodarme M, Prati MC, Calderini P, Gabrielli S, Iori A, Cancrini G (2009) Endoparasites of red fox (Vulpes vulpes) in Central Italy. J Wildl Dis 45:881–885

    Article  CAS  PubMed  Google Scholar 

  • Majoros G, Fukar O, Farkas R (2010) Autochtonous infection of dogs and slugs with Angiostrongylus vasorum in Hungary. Vet Parasitol 174:351–354

    Article  PubMed  Google Scholar 

  • Maksimov P, Hermosilla C, Taubert A, Staubach C, Sauter-Louis C, Conraths FJ, Vrhovec MG, Pantchev N (2017) GIS-supported epidemiological analysis on canine Angiostrongylus vasorum and Crenosoma vulpis infections in Germany. Parasit Vectors 10:108. https://doi.org/10.1186/s13071-017-2054-3

    Article  PubMed  PubMed Central  Google Scholar 

  • Mathis A, Deplazes P, Eckert J (1996) An improved test system for PCR-based specific detection of Echinococcus multilocularis eggs. J Helminthol 70:219–222

    Article  CAS  PubMed  Google Scholar 

  • Morgan ER, Tomlinson A, Hunter S, Nichols T, Roberts E, Fox MT, Taylor MA (2008) Angiostrongylus vasorum and Eucoleus aerophilus in foxes (Vulpes vulpes) in Great Britain. Vet Parasitol 154:48–57

    Article  CAS  PubMed  Google Scholar 

  • Nevarez A, Lopez A, Conboy G, Ireland W, Sims D (2005) Distribution of Crenosoma vulpis and Eucoleus aerophilus in the lung of free-ranging red foxes (Vulpes vulpes). J Vet Diagn Investig 17:486–489. https://doi.org/10.1177/104063870501700516

    Article  Google Scholar 

  • Otranto D, Cantacessi C, Dantas-Torres F, Brianti E, Pfeffer M, Genchi C, Guberti V, Capelli G, Deplazes P (2015) The role of wild canids and felids in spreading parasites to dogs and cats in Europe. Part II: helminths and arthropods. Vet Parasitol 213:24–37. https://doi.org/10.1016/j.vetpar.2015.04.020

    Article  PubMed  Google Scholar 

  • Papazahariadou A, Founta A, Papadopoulos E, Chliounakis S, Antoniadou-Sotiriadou K, Theodorides Y (2007) Gastrointestinal parasites of shepherd and hunting dogs in the Serres prefecture, northern Greece. Vet Parasitol 148:170–173

    Article  CAS  PubMed  Google Scholar 

  • Petavy AF, Deblock S, Prost C (1990) Epidemiology of alveolar echinococcosis in France. 1. Intestinal helminths in the red fox (Vulpes vulpes L.) from Haute-Savoie (in French). Ann Parasitol Hum Comp 65:22–27. https://doi.org/10.1051/parasite/1990651022

    Article  CAS  PubMed  Google Scholar 

  • Pilarczyk B, Balicka-Ramisz A, Ramisz A (2005) The occurrence of intestinal nematodes in red foxes in the Western Pomerania (in Polish). Wiad Parazytol 51:249–251

    PubMed  Google Scholar 

  • Poglayen G, Guberti V, Leoni B (1985) Parasites present in foxes (Vulpes vulpes) of the province of Forli (in Italian). Parassitologia 27:303–311

    CAS  PubMed  Google Scholar 

  • Putman RJ (1984) Facts from faeces. Mammal Rev 14:79–97

    Article  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). Z Jagdwiss 48:151–160

    Google Scholar 

  • Réperant LA, Hegglin D, Fischer C, Kohler L, Weber JM, Deplazes P (2007) Influence of urbanization on the epidemiology of intestinal helminths of the red fox (Vulpes vulpes) in Geneva, Switzerland. Parasitol Res 101:605–611. https://doi.org/10.1007/s00436-007-0520-0

    Article  PubMed  Google Scholar 

  • Richards DT, Harris S, Lewis JW (1995) Epidemiological studies on intestinal helminth parasites of rural and urban red foxes (Vulpes vulpes) in the United Kingdom. Vet Parasitol 59:39–51

    Article  CAS  PubMed  Google Scholar 

  • Roche MM, Kelliher DJ (1968) Angiostrongylus vasorum infestation in the dog: a case report. Ir Vet J 22:108–113

    Google Scholar 

  • Romstad A, Gasser RB, Monti JR, Polderman AM, Nansen P, Pit DS, Chilton NB (1997) Differentiation of Oesophagostomum bifurcum from Necator americanus by PCR using genetic markers in spacer ribosomal DNA. Mol Cell Probes 11:169–176

    Article  CAS  PubMed  Google Scholar 

  • Roth T, Amrhein V, Peter B, Weber D (2008) A Swiss agri-environment scheme effectively enhances species richness for some taxa over time agriculture. Ecosyst Environ 125:167–172. https://doi.org/10.1016/j.agee.2007.12.012

    Article  Google Scholar 

  • Sadlier LMJ, Webbon CC, Baker PJ, Harris S (2004) Methods of monitoring red foxes Vulpes vulpes and badgers Meles meles: are field signs the answer? Mammal Rev 34:78–98

    Article  Google Scholar 

  • Saeed I, Maddox-Hyttel C, Monrad J, Kapel CM (2006) Helminths of red foxes (Vulpes vulpes) in Denmark. Vet Parasitol 139:168–179

    Article  CAS  PubMed  Google Scholar 

  • Schnyder M, Maurelli MP, Morgoglione ME, Kohler L, Deplazes P, Torgerson P, Cringoli G, Rinaldi L (2010) Comparison of faecal techniques including FLOTAC for copromicroscopic detection of first stage larvae of Angiostrongylus vasorum. Parasitol Res 109:63–69

  • Schnyder M, Tanner I, Webster P, Barutzki D, Deplazes P (2011) An ELISA for sensitive and specific detection of circulating antigen of Angiostrongylus vasorum in serum samples of naturally and experimentally infected dogs. Vet Parasitol 179:152–158

    Article  CAS  PubMed  Google Scholar 

  • Schnyder M, Schaper R, Bilbrough G, Morgan ER, Deplazes P (2013a) 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. https://doi.org/10.1017/S0031182013001091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schnyder M, Schaper R, Pantchev N, Kowalska D, Szwedko A, Deplazes P (2013b) Serological detection of circulating Angiostrongylus vasorum antigen- and parasite-specific antibodies in dogs from Poland. Parasitol Res 112(Suppl 1):109–117. https://doi.org/10.1007/s00436-013-3285-7

    Article  PubMed  Google Scholar 

  • Schnyder M, Jefferies R, Schucan A, Morgan ER, Deplazes P (2015) Comparison of coprological, immunological and molecular methods for the detection of dogs infected with Angiostrongylus vasorum before and after anthelmintic treatment. Parasitology 142:1270–1277. https://doi.org/10.1017/S0031182015000554

    Article  CAS  PubMed  Google Scholar 

  • Schug K, Kramer F, Schaper R, Hirzmann J, Failing K, Hermosilla C, Taubert A (2018) Prevalence survey on lungworm (Angiostrongylus vasorum, Crenosoma vulpis, Eucoleus aerophilus) infections of wild red foxes (Vulpes vulpes) in Central Germany. Parasit Vectors 11:85. https://doi.org/10.1186/s13071-018-2672-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  • Sigrist NE, Hofer-Inteeworn N, Jud Schefer R, Kuemmerle-Fraune C, Schnyder M, Kutter APN (2017) Hyperfibrinolysis and hypofibrinogenemia diagnosed with rotational thromboelastometry in dogs naturally infected with Angiostrongylus vasorum. J Vet Intern Med 31:1091–1099. https://doi.org/10.1111/jvim.14723

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Staebler S, Ochs H, Steffen F, Naegeli F, Borel N, Sieber-Ruckstuhl N, Deplazes P (2005) Autochthonous infections with Angiostrongylus vasorum in dogs in Switzerland and Germany (in German). Schweiz Arch Tierheilkd 147:121–127

    Article  CAS  PubMed  Google Scholar 

  • Stefanic S, Shaikenov BS, Deplazes P, Dinkel A, Torgerson PR, Mathis A (2004) Polymerase chain reaction for detection of patent infections of Echinococcus granulosus ("sheep strain") in naturally infected dogs. Parasitol Res 92:347–351

    Article  PubMed  Google Scholar 

  • Stockdale PH, Hulland TJ (1970) The pathogenesis route of migration, and development of Crenosoma vulpis in the dog. Pathol Vet 7:28–42

    CAS  PubMed  Google Scholar 

  • Taubert A, Pantchev N, Vrhovec MG, Bauer C, Hermosilla C (2008) Lungworm infections (Angiostrongylus vasorum, Crenosoma vulpis, Aelurostrongylus abstrusus) in dogs and cats in Germany and Denmark in 2003-2007. Vet Parasitol 159:175–180

    Article  PubMed  Google Scholar 

  • Taylor CS, Garcia Gato R, Learmount J, Aziz NA, Montgomery C, Rose H, Coulthwaite CL, McGarry JW, Forman DW, Allen S, Wall R, Morgan ER (2015) Increased prevalence and geographic spread of the cardiopulmonary nematode Angiostrongylus vasorum in fox populations in Great Britain. Parasitology 142:1190–1195. https://doi.org/10.1017/S0031182015000463

    Article  CAS  PubMed  Google Scholar 

  • Thamsborg SM, Ketzis J, Horii Y, Matthews JB (2017) Strongyloides spp. infections of veterinary importance. Parasitology 144:274–284. https://doi.org/10.1017/S0031182016001116

    Article  PubMed  Google Scholar 

  • Tieri E, Pomilio F, Di Francesco G, Saletti MA, Totaro P, Troilo M, Menna S, Tampieri MP, Morelli D (2011) Angiostrongylus vasorum in 20 dogs in the province of Chieti, Italy. Vet Ital 47:77–88 65–76

    PubMed  Google Scholar 

  • Tolnai Z, Szell Z, Sreter T (2015) Environmental determinants of the spatial distribution of Angiostrongylus vasorum, Crenosoma vulpis and Eucoleus aerophilus in Hungary. Vet Parasitol 207:355–358. https://doi.org/10.1016/j.vetpar.2014.12.008

    Article  CAS  PubMed  Google Scholar 

  • van Doorn DC, van de Sande AH, Nijsse ER, Eysker M, Ploeger HW (2009) Autochthonous Angiostrongylus vasorum infection in dogs in the Netherlands. Vet Parasitol 162:163–166

    Article  PubMed  Google Scholar 

  • Vergles Rataj A, Posedi J, Zele D, Vengust G (2013) Intestinal parasites of the red fox (Vulpes vulpes) in Slovenia. Acta Vet Hung 61:454–462. https://doi.org/10.1556/AVet.2013.029

    Article  PubMed  Google Scholar 

  • Webbon CC, Baker PJ, Harris S (2004) Faecal density counts for monitoring changes in red fox numbers in rural Britain. J Appl Ecol 41:768–779

    Article  Google Scholar 

  • Willingham AL, Ockens NW, Kapel CM, Monrad J (1996) A helminthological survey of wild red foxes (Vulpes vulpes) from the metropolitan area of Copenhagen. J Helminthol 70:259–263

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wolff K, Eckert J, Leemann W (1969) Beitrag zur Angiostrongylose des Hundes. In: Dtsch Vet-med Ges, Zürich, 1969. Vortrag Tagung Fachgr. "Kleintierkrankheiten"

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Acknowledgments

We would like to thank Jeannine Hauri, Lucia Kohler and Katharina Huggel for their support with laboratory work; Prof. Alexander Mathis and Dr. Felix Grimm for their advice regarding biomolecular issues; Dr. Iskender Ziadinov for his help with the fox sampling; and Dr. Ramon Eichenberger for support.

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Koller, B., Hegglin, D. & Schnyder, M. A grid-cell based fecal sampling scheme reveals: land-use and altitude affect prevalence rates of Angiostrongylus vasorum and other parasites of red foxes (Vulpes vulpes). Parasitol Res 118, 2235–2245 (2019). https://doi.org/10.1007/s00436-019-06325-7

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