Hostname: page-component-745bb68f8f-l4dxg Total loading time: 0 Render date: 2025-02-06T03:53:26.096Z Has data issue: false hasContentIssue false
  • English
  • Français

Extraintestinal nematodes of the red fox Vulpes vulpes in north-west Italy

Published online by Cambridge University Press:  11 April 2014

M. Magi ,
L. Guardone ,
M.C. Prati ,
W. Mignone  and
F. Macchioni
M. Magi
Affiliation:
Department of Veterinary Sciences, University of Pisa, Viale delle Piagge 2, 56124Pisa, Italy
L. Guardone
Affiliation:
Department of Veterinary Sciences, University of Pisa, Viale delle Piagge 2, 56124Pisa, Italy
M.C. Prati
Affiliation:
Scuola Normale Superiore di Pisa, Piazza dei Cavalieri 7, 56126Pisa, Italy
W. Mignone
Affiliation:
Istituto Zooprofilattico Sperimentale of Piedmont, Liguria, Aosta Valley, via Nizza 4, 18100Imperia, Italy
F. Macchioni*
Affiliation:
Department of Veterinary Sciences, University of Pisa, Viale delle Piagge 2, 56124Pisa, Italy
*
*Fax: 0039 050 2216941 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Extraintestinal nematodes of the red fox (Vulpes vulpes) are a wide group of parasites that infect wild and domestic carnivores and occasionally humans. Nematodes in the cardiopulmonary system, stomach, urinary apparatus and muscle tissue of 165 red foxes (Vulpes vulpes) from north-west Italy (Liguria and Piedmont) were investigated between 2009 and 2012. Of the cardiopulmonary nematodes, a high prevalence of Angiostrongylus vasorum and Eucoleus aerophilus (syn. Capillaria aerophila) was found, 78.2% and 41.8% respectively; Crenosoma vulpis (15.8%) and Filaroides spp. (4.8%) were also found. Spirocerca lupi (23.5%), Aonchotheca putorii (syn. Capillaria putorii) (8.6%) and Physaloptera spp. (2.5%) were detected in the stomach and Pearsonema plica (syn. Capillaria plica) (56.8%) in the bladder. Eucoleus boehmi (syn. Capillaria boehmi) was also detected in the nasal cavities of one of the two foxes examined. A coprological examination revealed eggs of E. aerophilus, A. putorii, S. lupi, Physaloptera spp. and eggs of intestinal parasites. Filarial worms were absent in all the 165 animals examined, nor was there evidence of Trichinella spp. in any of the foxes. The foxes were found to host a high prevalence of many species of extraintestinal nematodes. The prevalence of A. vasorum in foxes found in the present study is among the highest in Europe. In addition, to the best of our knowledge, E. boehmi and Filaroides spp. have never been reported before in this host in Italy.

Type
Short Communication
Information
Journal of Helminthology , Volume 89 , Issue 4 , July 2015 , pp. 506 - 511
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aftandelians, R., Raafat, F., Taffazoli, M. & Beaver, P.C. (1977) Pulmonary capillariasis in a child in Iran. American Journal of Tropical Medicine and Hygiene 26, 64–71.CrossRefGoogle Scholar
Bliss, C.I. & Fisher, R.A. (1953) Fitting the negative binomial distribution to biological data and note of the efficient fitting of negative binomial. Biometrics 9, 176–200.CrossRefGoogle Scholar
Bolt, G., Monrad, J., Henriksen, P., Dietz, H.H., Koch, J., Bindseil, E. & Jensen, A.L. (1991) The fox (Vulpes vulpes) as a reservoir for canine angiostrongylosis in Denmark. Field survey and experimental infections. Acta Veterinaria Scandinavica 33, 357–362.CrossRefGoogle Scholar
Bork-Mimm, S. & Rinder, H. (2011) High prevalence of Capillaria plica infections in red foxes (Vulpes vulpes) in Southern Germany. Parasitology Research 108, 1063–1067.CrossRefGoogle ScholarPubMed
Bružinskaitė-Schmidhalter, R., Šarkūnas, M., Malakauska, A., Mathis, A., Torgerson, P.R. & Deplazes, P. (2011) Helminths of red foxes (Vulpes vulpes) and raccoon dogs (Nyctereutes procyonoides) in Lithuania. Parasitology 139, 120–127.CrossRefGoogle Scholar
Bush, A.O., Lafferty, K.D., Lotz, J.M. & Shostak, A.W. (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.CrossRefGoogle Scholar
Callegari, D., Kramer, L., Cantoni, A.M., Di Lecce, R., Dodi, P.L. & Grandi, G. (2010) Canine bladderworm (Capillaria plica) infection associated with glomerular amyloidosis. Veterinary Parasitology 168, 338–341.CrossRefGoogle ScholarPubMed
Campbell, B.G. (1991) Trichuris and other Trichinelloid nematodes of dogs and cats in the United States. Compendium on Continuing Education for the Practicing Veterinarian 13, 769–778.Google Scholar
Caro-Vadillo, A., Martínez-Merlo, E., García-Real, I., Fermín-Rodríguez, M.L. & Mateo, P. (2005) Verminous pneumonia due to Filaroides hirthi in a Scottish terrier in Spain. Veterinary Record 157, 586–589.CrossRefGoogle Scholar
Chmurzyńska, E., Różycki, M., Bilska-Zajęc, E., Nöckler, K., Mayer-Scholl, A., Pozio, E., Cencek, T. & Karamon, J. (2013) Trichinella nativa in red foxes (Vulpes vulpes) of Germany and Poland: possible different origins. Veterinary Parasitology 198, 254–257.CrossRefGoogle ScholarPubMed
Clark, A.C., Lopez, F.R., Levine, J.M., Cooper, J.J., Craig, T.M., Voges, A.K., Johnson, M.C. & Porter, B.F. (2013) Intracranial migration of Eucoleus (Capillaria) boehmi in a dog. Journal of Small Animal Practice 54, 99–103.CrossRefGoogle Scholar
Conboy, G. (2009) Helminth parasites of the canine and feline respiratory tract. The Veterinary Clinics of North America – Small Animal Practice 39, 1109–1126.CrossRefGoogle ScholarPubMed
Conboy, G. (2011) Canine angiostrongylosis: the French heartworm: an emerging threat in North America. Veterinary Parasitology 176, 382–389.CrossRefGoogle ScholarPubMed
Davidson, R., Gjerde, B., Vikoren, T., Lillehaug, A. & Handeland, K. (2006) Prevalence of Trichinella larvae and extra intestinal nematodes in Norwegian red foxes (Vulpes vulpes). Veterinary Parasitology 136, 307–316.CrossRefGoogle ScholarPubMed
Deplazes, P., Hegglin, D., Gloor, S. & Romig, T. (2004) Wilderness in the city: the urbanization of Echinococcus multilocularis. Trends in Parasitology 20, 77–84.CrossRefGoogle ScholarPubMed
Eira, C., Viganda, J., Torres, J. & Miquel, J. (2006) The helminth community of the red fox, Vulpes vulpes, in Dunas de Mira (Portugal) and its effect on host condition. Wildlife Biology in Practice 2, 26–36.CrossRefGoogle Scholar
Ferrantelli, V., Riili, S., Vicari, D., Percipalle, M., Chetta, M., Monteverde, V., Gaglio, G., Giardina, G., Usai, F. & Poglayen, G. (2010) Spirocerca lupi isolated from gastric lesions in foxes (Vulpes vulpes) in Sicily (Italy). Polish Journal Veterinary Sciences 13, 465–471.Google ScholarPubMed
Ferroglio, E., Ragagli, C. & Trisciuoglio, A. (2009) Physaloptera sibirica in foxes and badgers from the Western Alps (Italy). Veterinary Parasitology 163, 164–166.CrossRefGoogle ScholarPubMed
Gerrikagoitia, X., Barral, M. & Juste, R.A. (2010) Angiostrongylus species in wild carnivores in the Iberian Peninsula. Veterinary Parasitology 174, 175–180.CrossRefGoogle ScholarPubMed
Gortázar, C., Castillo, J.A., Lucientes, J., Blanco, J.C., Arriolabengoa, A. & Calvete, C. (1994) Factors affecting Dirofilaria immitis prevalence in red foxes in north-eastern Spain. Journal of Wildlife Diseases 30, 545–547.CrossRefGoogle Scholar
Gortázar, C., Villafuerte, R., Lucientes, J. & Fernandez-de-Luco, D. (1998) Habitat related differences in helminth parasites of red foxes in the Ebro Valley. Veterinary Parasitology 80, 75–81.CrossRefGoogle ScholarPubMed
Harris, S. (1978) Age determination in the red fox (Vulpes vulpes) – an evaluation of technique efficiency as applied to a sample of suburban foxes. Journal of Zoology (London) 184, 91–117.CrossRefGoogle Scholar
Hinaidy, H.K. (1971) Die Parasitenfauna des Rotfuchses, Vulpes vulpes (L.), in Oesterreich. Zentralblatt für Veterinarmedizin Reihe B 18, 21–32.CrossRefGoogle Scholar
Iori, A., Costantini, R. & Cancrini, G. (1990) Parassiti in volpi provenienti da alcune regioni italiane. Parassitologia 32, 153–154.Google Scholar
Jefferies, R., Shaw, S.E., Viney, M.E. & Morgan, E.R. (2009) Angiostrongylus vasorum from South America and Europe represent distinct lineages. Parasitology 136, 107.CrossRefGoogle ScholarPubMed
Jeffery, R.A., Lankester, M.W., McGrath, M.J. & Whitney, H.G. (2004) Angiostrongylus vasorum and Crenosoma vulpis in red foxes (Vulpes vulpes) in Newfoundland, Canada. Canadian Journal of Zoology 82, 66–74.CrossRefGoogle Scholar
Lalošević, D., Lalošević, V., Klem, I., Stanojev-Jovanović, D. & Pozio, E. (2008) Pulmonary capillariasis miming bronchial carcinoma. American Journal of Tropical Medicine and Hygiene 78, 14–16.CrossRefGoogle ScholarPubMed
Lalošević, V., Lalošević, D., Capo, I., Simin, V., Galfi, A. & Traversa, D. (2013) High infection rate of zoonotic Eucoleus aerophilus infection in foxes from Serbia. Parasite 20, 3.CrossRefGoogle ScholarPubMed
Leoni, A., Masala, S. & Garippa, G. (1985) Principali lesioni da Spirocerca lupi in Vulpes vulpes. Atti Società Italiana Scienze Veterinarie 39, 570–573.Google Scholar
Levine, N.D. (1968) Nematode parasites of domesticated animals and man. 477 pp. Minneapolis, USA, Burgess Publishing.Google Scholar
Macchioni, F., Chelucci, L., Guardone, L., Mignone, W., Prati, M.C. & Magi, M. (2013) Calodium hepaticum (Nematoda: Capillaridae) in a red fox (Vulpes vulpes) in Italy with scanning electron microscopy of the eggs. Folia Parasitologica 60, 102–104.CrossRefGoogle Scholar
Magi, M., Macchioni, F., Dell'Omodarme, M., Prati, M.C., Calderini, P., Gabrielli, S., Iori, A. & Cancrini, G. (2009) Endoparasites of Vulpes vulpes in Central Italy. Journal of Wildlife Diseases 45, 881–886.CrossRefGoogle ScholarPubMed
Mañas, S., Ferrer, D., Castellà, J. & Loppez-Martin, J.M. (2005) Cardiopulmonary helminth parasites of red foxes (Vulpes vulpes) in Catalonia, northeastern Spain. Veterinary Journal 169, 118–120.CrossRefGoogle ScholarPubMed
Manfredi, M.T., Giacometti, A., Fraquelli, C. & Piccolo, G. (2003) Studio della popolazione elmintica in volpi (Vulpes vulpes) del Trentino Alto Adige. Journal of Mountain Ecology 7, 261–263.Google Scholar
Martinez-Carrasco, C., Ruiz de Ybanezj, M.R., Sagariminaga, L., Garijo, M.M., Moreno, F., Acosta, I., Hernandez, S. & Alonso, F.D. (2007) Parasites of the red fox (Vulpes vulpes Linnaeus, 1758) in Murcia, southeast Spain. Revue Médicine Vétérinarie 158, 331–335.Google Scholar
Miquel, J., Segovia, J.M., Feliu, C. & Torres, J. (1996) On Physaloptera sibirica Petrow et Gorbunow, 1931 (Nematoda: Physalopteridae) parasitizing Iberian mammals. Wiadomości Parazytologiczne 42, 435–442.Google ScholarPubMed
Morgan, E.R., Shaw, S.E., Brennan, S.F., De Waal, T.D., Jones, B.R. & Mulcahy, G. (2005) Angiostrongylus vasorum: a real heartbreaker. Trends in Parasitology 21, 49–51.CrossRefGoogle ScholarPubMed
Morgan, E.R., Tomlinson, A., Hunter, S., Nichols, T., Roberts, E., Fox, M.T. & Taylor, M.A. (2008) Angiostrongylus vasorum and Eucoleus aerophilus in foxes (Vulpes vulpes) in Great Britain. Veterinary Parasitology 154, 48–57.CrossRefGoogle ScholarPubMed
Morgan, E.R., Jefferies, R., Krajewski, M., Ward, P. & Shaw, S.E. (2009) Canine pulmonary angiostrongylosis: the influence of climate on parasite distribution. Parasitology International 58, 406–410.CrossRefGoogle ScholarPubMed
Mylonakis, M.E., Koutinas, A.F., Liapi, M.V., Saridomichelakis, M.N. & Rallis, T.S. (2001) A comparison of the prevalence of Spirocerca lupi in three groups of dogs with different life and hunting styles. Journal of Helminthology 75, 359–361.CrossRefGoogle ScholarPubMed
Nevárez, A., López, 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). Journal of Veterinary Diagnostic Investigation 17, 486–489.CrossRefGoogle ScholarPubMed
Pence, D.B. & Stone, J.E. (1978) Visceral lesions in wild carnivores naturally infected with Spirocerca lupi. Veterinary Pathology 15, 322–331.CrossRefGoogle ScholarPubMed
Polidori, G.A., Mura, A., Moretti, A., Balzano, A. & Principato, M. (1985) Spirocerca lupi nella volpe in Sardegna. Atti Societa Italiana Scienze Veterinarie 39, 789–792.Google Scholar
Pozio, E. (2007) World distribution of Trichinella spp. infections in animals and humans. Veterinary Parasitology 149, 3–21.CrossRefGoogle ScholarPubMed
Rinaldi, L., Calabria, G., Carbone, S., Carrella, A. & Cringoli, G. (2007) Crenosoma vulpis in dog: first case report in Italy and use of the FLOTAC technique for copromicroscopic diagnosis. Parasitology Research 101, 1681–1684.CrossRefGoogle ScholarPubMed
Rodriguez, A. & Carbonell, E. (1998) Gastrointestinal parasites of the Iberian lynx and other wild carnivores from central Spain. Acta Parasitologica 43, 128–136.Google Scholar
Romano, F., Motta, A., Melino, M., Negro, M., Gavotto, G., Decasteli, L., Careddu, E., Bianchi, C., Bianchi, D.M. & Pozio, E. (2011) Investigation on a focus of human trichinellosis revealed by an atypical clinical case: after wild-boar (Sus scrofa) pork consumption in northern Italy. Parasite 18, 85–87.CrossRefGoogle ScholarPubMed
Rossi, L., Pozio, E., Mignone, W., Ercolini, C. & Dini, V. (1992) Epidemiology of sylvatic trichinellosis in North Western Italy. Revue Scientifique et Technique (International Office of Epizootics) 11, 1039–1046.Google ScholarPubMed
Rossi, M., Messina, N., Ariti, G., Riggio, F. & Perrucci, S. (2011) Symptomatic Capillaria plica infection in a young European cat. Journal of Feline Medicine and Surgery 13, 793–795.CrossRefGoogle Scholar
Saeed, I., Maddox-Hyttel, C., Monrad, J. & Kapel, C.M.O. (2006) Helminths of red foxes (Vulpes vulpes) in Denmark. Veterinary Parasitology 139, 168–179.CrossRefGoogle ScholarPubMed
Sato, H., Inaba, T., Ihama, Y. & Kamiya, H. (1999) Parasitological survey on wild carnivora in north western Tohoku, Japan. Journal of Veterinary Medicine Sciences 61, 1023–1026.CrossRefGoogle ScholarPubMed
Schöffel, I., Schein, E., Wittstadt, U. & Hentsche, J. (1991) Zur Parasitenfauna des Rotfuchsen in Berlin (West). Berliner und Muencher Tieraerztliche Wochenschrift 104, 153–157.Google Scholar
Schulz, B.S., Seybold, N., Sauter-Louis, C. & Hartmann, K. (2013) Praevalenz von Angiostrongylus vasorum und Crenosoma vulpis bei Hunden in Bayern. Berliner und Münchener tierärztliche Wochenschrift 7, 62–68.Google Scholar
Segovia, J.M., 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, 67–79.Google Scholar
Shimalov, V.V. & Shimalov, V.T. (2002) Helminth fauna of the red fox (Vulpes vulpes L. 1758) in Southern Belarus. Parasitology Research 89, 77–78.Google Scholar
Sréter, T., Szell, Z., Marucci, G., Pozio, E. & Vargac, I. (2003) Extraintestinal nematode infections of red foxes (Vulpes vulpes) in Hungary. Veterinary Parasitology 115, 329–334.CrossRefGoogle ScholarPubMed
Stancampiano, L., Capelli, G., Schiavon, E., Mutinelli, F. & Bozzolan, G. (1998) Trichinellosis, sarcoptic mange, filariosis and intestinal helminths stability in a fox population (Vulpes vulpes). Parassitologia 40, 171.Google Scholar
Supperer, R. (1953) Capillaria boehmi Spec. Nov., eine neue Haarwurm-Art aus den Stirnhoehlen des Fuchses. Zeitschrift fűr Parasitenkunde 16, 51–55.CrossRefGoogle Scholar
Thul, J.E., Forrester, D.J. & Abercrombie, C.L. (1985) Ecology of parasitic helminths of wood ducks Aix sponsa in the Atlantic Flyway. Proceedings of the Helminthological Society of Washington 52, 297–310.Google Scholar
Tønsberg, H., Saeed, I. & Koch, J. (2004) Parasitologisk undersøgelse af jagthund og rav i Odsherred. Dansk Veterinær Tidsskrift 87, 14–18.Google Scholar
Zarnowsky, E. & Patyk, W. (1960) On the independence of the species Thominx böhmi (Supperer, 1953) and its occurrence. Acta Parasitologica Polonica 8, 205–213.Google Scholar