Abstract
Angiostrongylus (A.) vasorum is a nematode that causes angiostrongylosis in domestic and wild canids. Red foxes (Vulpes vulpes) and raccoon dogs (Nyctereutes procyonoides) are suspected of providing a wildlife reservoir for A. vasorum infections in pet dogs. To obtain data on the occurrence of A. vasorum in wildlife, red fox and raccoon dog carcasses (hunted or found dead) were collected from January to September 2009 in the Federal State of Brandenburg, Germany. Lung tissue samples were subjected to DNA extraction and examined for the presence of A. vasorum DNA by means of real-time PCR. A. vasorum DNA was detected in 11 out of 122 (9.0 %) lungs of red foxes and in none of the lung samples of raccoon dogs. These data suggest that red foxes are a reservoir of A. vasorum infections for pet dogs in this area.
Article PDF
Similar content being viewed by others
References
Al-Sabi MNS, Chriel M, Jensen TH, Enemark HL (2013) Endoparasites of the raccoon dog (Nyctereutes procyonoides) and the red fox (Vulpes vulpes) in Denmark 2009–2012 – A comparative study. Int J Paras (Paras & Wildlife) 2:144–151
Al-Sabi MNS, Halasa T, Kapel CMO (2014) Infections with cardiopulmonary and intestinal helminths and sarcoptic mange in red foxes from two different localities in Denmark. Acta Parasitologica 59(1):98–107
Barutzki D, Schaper R (2003) Endoparasites in dogs and cats in Germany 1999–2002. Parasitol Res 90(3):149–150
Barutzki D, Schaper R (2009) Natural infections of Angiostrongylus vasorum und Crenosoma vulpis in dogs in Germany (2007 – 2009). Parasitol Res 105(1):39–48
Barutzki D, Schaper R (2011) Results of parasitological examinations of faecal samples from cats and dogs in Germany between 2003 and 2010. Parasitol Res 109(1):45–60
Barutzki D (2013) Nematodeninfektionen des Respirationstrakts bei Hunden in Deutschland. Tierärztliche Praxis Kleintiere 41:326–336
Blehaut TRW, Hardstaff JL, Chapman PS, Pfeiffer DU, Boag AK, Guitian FJ (2014) Spatial, demographic and clinical patterns of Angiostrongylus vasorum infection in the dog population of Southern England. Vet Rec 175:148
Bolt G, Monrad J, Frandsen F, Henriksen P, Dietz HM (1993) The common frog (Rana temporia) as a potential paratenic and intermediate host for Angiostrongylus vasorum. Parasitol Res 79:428–430
Bolt G, Monrad J, Koch J, Jensen AL (1994) Canine angiostrongylosis: a review. Vet Rec 135:447–452
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
Chapman PS, Boag AK, Guitian J, Boswood A (2004) Angiostrongylus vasorum infection in 23 dogs (1999 – 2002). J Small Anim Pract 45:435–440
Cury MC, Lima WS, Vitor RWA (1996) Enzyme-linked immunosorbent assay (ELISA) for the diagnosis of Angiostrongylus vasorum (Baillet, 1866) infection in dogs. Rev Med Vet 147:525–530
Cury MC, Guimarães MP, Lima WS, Vitor RWA (2002) Western blot analysis of the humoral response of dogs experimentally infected with Angiostrongylus vasorum (Baillet, 1866). Vet Parasitol 106:83–87
Demiaszkiewicz AW, Pyziel AM, Kuligowska I, Lachowicz J (2014) The first report of Angiostrongylus vasorum (Nematoda; Metastrongyloidea) in Poland, in red foxes (Vulpes vulpes). Acta Parasitologica 59(4):758–762
Eleni C, Grifoni G, Di Egidio A, Meoli R, De Liberato C (2014) Pathological findings of Angiostrongylus vasorum infection in red foxes (Vulpes vulpes) from Central Italy, with the first report of a disseminated infection in this host species. Parasitol Res 113:1247–1250
Elsheikha HM, Holmes SA, Wright I, Morgan ER, Lacher DW (2014) Recent advances in the epidemiology, clinical and diagnostic features, and control of canine cardio-pulmonary angiostrongylosis. Vet Res 45:92
Franssen F, Nijsse R, Mulder J, Cremers H, Dam C, Takumi K, van der Giessen J (2014) Increase in number of helminth species from Dutch red foxes over a 35 – year period. Parasit & Vect 7:166
Gerrikagoitia X, Barral M, Juste RA (2010) Angiostrongylus species in wild carnivores in the Iberian Peninsula. Vet Parasitol 174:175–180
Härtwig V, von Loewenich FD, Schulze C, Straubinger RK, Daugschies A, Dyachenko V (2014) Detection of Anaplasma phagocytophilum in red foxes (Vulpes vulpes) and raccoon dogs (Nyctereutes procyonoides) from Brandenburg, Germany. TTBD 5(3):277–280
Helm J, Gilleard JS, Jackson M, Redman E, Bell R (2009) A case of canine Angiostrongylus vasorum in Scotland confirmed by PCR and sequence analysis. J Small Anim Pract 50:255–259
Helm JR, Morgan ER, Jackson MW, Wotton P, Bell R (2010) Canine angiostrongylosis: an emerging disease in Europe. J Vet Emerg Crit Care 20(1):98–109
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
Jefferies R, Shaw SE, Willesen J, Viney ME, Morgan ER (2010) Elucidating the spread of the emerging canid nematode Angiostrongylus vasorum between Palaearctic and Nearctic ecozones. Infect Genet Evol 10:561–568
Jefferies R, Morgan ER, Helm J, Robinson M, Shaw SE (2011) Improved detection of canine Angiostrongylus vasorum infection using real-time PCR and indirect ELISA. Parasitol Res 109:1577–1583
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
Kirk L, Limon G, Guitian FJ, Hermosilla C, Fox MT (2014) Angiostrongylus vasorum in Great Britain: a nationwide postal questionnaire survey of veterinary practices. Vet Rec 175:118
Koch J, Willesen JL (2009) Canine pulmonary angiostrongylosis: an update. Vet J 179:348–359
Morgan ER, Shaw SE, Brennan SF, De Waal TD, Jones BR, Mulcahy G (2005) Angiostrongylus vasorum: a real heartbreaker. Trends Parasitol 21:49–51
Morgan ER, Tomlinson A, Hunter S, Nichols T, Roberts E, Fox MT, Taylor MA (2008) Angiostrongylus vasorum and Eucolaeus aerophilus in foxes (Vulpes vulpes) in Great Britain. Vet Parasitol 154:48–57
Morgan ER, Jefferies R, Krajewski M, Ward P, Shaw SE (2009) Canine pulmonary angiostrongylosis: The influence of climate on parasite distribution. Parasitol Int 58:406–410
Mozzer LR, Lima WS (2015) Gallus gallus domesticus: Paratenic host of Angiostrongylus vasorum. Vet Parasitol 207:81–84
Oliveira-Júnior SD, Barcante JMP, Barcante TA, Dias SRC, Lima WS (2006) Larval output of infected and re-infected dogs with Angiostrongylus vasorum (Baillet, 1866) Kamensky, 1905. Vet Parasitol 141:101–106
Philbey AW, Delgado D (2013) Detection of Angiostrongylus vasorum in red foxes in Scotland. Vet Rec 173:148
Routh A (2009) Angiostrongylus vasorum infection in a fox in northern England. Vet Rec 602 – 603
Saeed I, Maddox-Hyttel C, Monrad J, Kapel CMO (2006) Helminths of red foxes (Vulpes vulpes) in Denmark. Vet Parasitol 139:168–179
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
Schnyder M, Schaper R, Bilbrough G, Morgan ER, Deplazes P (2013) Seroepidemiological survey for canine angiostrongylosis in dogs from Germany and the UK using combined detection of Angiostrongylus vasorum antigen and specific antibodies. Parasitology 140(11):1442–1450
Schnyder M, Stebler K, Naucke TJ, Lorentz S, Deplazes P (2014) Evaluation of a rapid device for serological in-clinic diagnosis of canine Angiostrongylosis. Paras & Vect 7:72
Schucan A, Schnyder M, Tanner I, Barutzki D, Traversa D, Deplazes P (2012) Detection of specific antibodies in dogs infected with Angiostrongylus vasorum. Vet Parasitol 185:216–224
Schug K, Hermosilla C, Hirzmann J, Schaper R, Taubert A (2013) Endoparasitenfauna beim Rotfuchs in Deutschland unter besonderer Berücksichtigung von Angiostrongylus vasorum. Tagung DVG-Fachgruppe “Parasitologie und Parasitäre Erkrankungen” Gießen, 8.-10.July 2013:79 – 80
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 Parasitologica 49(1):67–79
Simpson VR, Neal C (1982) Angiostrongylus vasorum infection in dogs and slugs. Vet Rec 111:303–304
Simpson VR (1996) Angiostrongylus vasorum infection in foxes (Vulpes vulpes) in Cornwall. Vet Rec 139:443–445
Sutor A, Schwarz S, Conraths FJ (2011) Der Marderhund (Nyctereutes procyonoides) in Deutschland- ein etablierter Neubürger als Wirt und Vektor für Parasiten und andere Pathogene. BMTW 124:457–464
Sutor A, Schwarz S, Conraths FJ (2014) The biological potential of the raccoon dog (Nyctereutes procyonoides, Gray 1834) as an invasive species in Europe- new risks for disease spread? Acta Theriol 59:49–59
Taubert A, Pantchev N, Vrhovec MG, Bauer C, Hermosilla C (2009) Lungworm infections (Angiostrongylus vasorum, Crenosoma vulpis, Aelurostrongylus abstrusus) in dogs and cats in Germany and Denmark in 2003–2007. Vet Parasitol 159:175–180
Thiess A, Schuster R, Nöckler K, Mix H (2001) Helminthenfunde beim einheimischen Marderhund Nyctereutes procyonoides (Gray, 1834). BMTW 114:273–276
Traversa D, Torbidone A, Malatesta D, Guglielmini C (2008) Occurrence of fatal canine Angiostrongylus vasorum infection in Italy. Vet Parasitol 152:162–166
Traversa D, Guglielmini C (2008) Feline aelurostrongylosis and canine angiostrongylosis: A challenging diagnosis for two emerging verminous pneumonia infections. Vet Parasitol 157:163–174
Verzberger-Epshtein I, Markham RJF, Sheppard JA, Stryhn H, Whitney H, Conboy GA (2008) Serologic detection of Angiostrongylus vasorum infection in dogs. Vet Parasitol 151:53–60
Willingham AL, Ockens NW, Kapel CMO, Monrad J (1996) A helminthological survey of wild red foxes (Vulpes vulpes) from the metropolitan area of Copenhagen. J Helminthol 70:259–263
Yamakawa Y, McGarry JW, Denk D, Dukes-McEwan J, Macdonald N, Mas A, McConnell F, Tatton B, Valentine EG, Wayne J, Williams JM, Hetzel U (2009) Emerging canine angiostrongylosis in northern England: five fatal cases. Vet Rec 164:149–152
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0), which permits use, duplication, adaptation, distribution, and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
About this article
Cite this article
Härtwig, V., Schulze, C., Barutzki, D. et al. Detection of Angiostrongylus vasorum in Red Foxes (Vulpes vulpes) from Brandenburg, Germany. Parasitol Res 114 (Suppl 1), 185–192 (2015). https://doi.org/10.1007/s00436-015-4524-x
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-015-4524-x