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

Transcription

1 Journal of Helminthology (2015) 89, q Cambridge University Press 2014 doi: /s x x Extraintestinal nematodes of the red fox Vulpes vulpes in north-west Italy M. Magi 1, L. Guardone 1, M.C. Prati 2, W. Mignone 3 and F. Macchioni 1 * 1 Department of Veterinary Sciences, University of Pisa, Viale delle Piagge 2, Pisa, Italy: 2 Scuola Normale Superiore di Pisa, Piazza dei Cavalieri 7, Pisa, Italy: 3 Istituto Zooprofilattico Sperimentale of Piedmont, Liguria, Aosta Valley, via Nizza 4, Imperia, Italy (Received 10 July 2013; Accepted 6 March 2014; First Published Online 11 April 2014) 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 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. Introduction The red fox (Vulpes vulpes) is the most widespread European wild canid and is considered as the main wild reservoir for many parasites, including extraintestinal nematodes which represent a wide group of helminths transmittable to other animals and occasionally to humans. The most significant species are Angiostrongylus vasorum, Crenosoma vulpis, Dirofilaria immitis, Filaroides spp., Eucoleus aerophilus (syn. Capillaria aerophila) and Eucoleus boehmi (syn. Capillaria boehmi) which inhabit *Fax: fabio.macchioni@unipi.it the cardiorespiratory system, Dirofilaria repens and Acanthocheilonema spp. in subcutaneous tissues, Spirocerca lupi in the stomach, Pearsonema plica in the urinary tract and Trichinella spp. in striated muscles. Over the past decade an increasing number of studies concerning extraintestinal nematodes of foxes have been conducted in several European countries (table 1). Other studies have been carried out worldwide (Jeffery et al., 2004; Nevárez et al., 2005; Jefferies et al., 2009). This interest could be correlated to the growing awareness of the diffusion of these parasites in pets (Conboy, 2009; Callegari et al., 2010; Clark et al., 2013; Schulz et al., 2013). The aim of the present work was to investigate the extraintestinal parasitic fauna of foxes from north-west Italy (Liguria and Piedmont), an area previously little

2 Extraintestinal nematodes of foxes from Italy 507 Table 1. The prevalence (%) of extraintestinal nematodes in red foxes in Europe from 2003 to 2013: D, Germany; DK, Denmark; ES, Spain; GB, Great Britain; H, Hungary; IT, Italy; LTU, Lithuania; NOR, Norway; PT, Portugal; S, Serbia; 0, not infected;, not recorded. Country IT IT IT IT ES ES ES ES H DK DK PT NOR GB LTU D S Reference No. of foxes examined Angiostrongylus vasorum a Eucoleus aerophilus Eucoleus boehmi b Crenosoma vulpis Dirofilaria immitis Spirocerca lupi Physaloptera spp Pearsonema plica , Manfredi et al. (2003); 2, Ferroglio et al. (2009); 3, Magi et al. (2009); 4, Ferrantelli et al. (2010); 5, Segovia et al. (2004); 6, Mañas et al. (2005); 7, Martinez-Carrasco et al. (2007); 8, Gerrikagoitia et al. (2010); 9, Sréter et al. (2003); 10, Tønsberg et al. (2004); 11 Saeed et al. (2006) [ a only from the endemic area of New Zealand with 436 foxes examined]; 12, Eira et al. (2006); 13, Davidson et al. (2006); 14, Morgan et al. (2008); 15, Bružinskaitė-Schmidhalter et al. (2011); 16, Bork-Mimm & Rinder (2011); 17, Lalošević et al. (2013) [ b nine of ten foxes infected with E. boehmi ]. The search for Filaroides spp. in references 1, 3 and 15 was negative; 0.7% were infected with Dirofilaria repens and 9.3% with Acanthocheilonema reconditum (Magi et al., 2009), and 2.3% with A. dracunculoides (Bružinskaitė-Schmidhalter et al., 2011). The search for Aonchotheca putorii was negative in 7 and 15. studied, in order to increase knowledge on the diffusion of these parasites in Italy. Materials and methods Collection and examination of foxes From 2009 to 2012, 165 foxes (98 males and 67 females) from north-west Italy (the province of Imperia in Liguria and Cuneo in Piedmont) were examined. The foxes had been culled according to Italian law (157/92) and collected by the Istituto Zooprofilattico Sperimentale of Piedmont, Liguria and Aosta Valley (Imperia section). Individual data on the area of origin, sex, weight and age were recorded for each fox. The age was estimated from body size, dentition and extent of tooth wear (Harris, 1978). Foxes were classified as juvenile (#1 year of age, 37 foxes) or adult (.1 year of age, 128 foxes). The cardiorespiratory system was examined as follows. The trachea was observed under a stereomicroscope; pulmonary tissue smears were taken to search for eggs, microfilariae and larvae; heart and lungs were cut and examined. All the above-mentioned dissected organs were washed with tap water in a conical beaker to collect parasites. Only two foxes were sent to our laboratory with nasal cavities, which were inspected. The stomachs of 81 foxes were examined. Gastric walls were observed macroscopically, gastric contents were submitted to sedimentation and examined under a stereomicroscope. Kidneys of all the foxes were opened longitudinally and inspected. The urinary bladders of 74 foxes were opened, washed in a conical beaker and the sediment was examined by stereomicroscopy. The sediment was then centrifuged at 700 g for 5 min to collect eggs. Livers of 78 foxes were examined. The results are reported in Macchioni et al. (2013). Muscle samples (5 g) of all 165 foxes, taken from the tibialis anterior muscle, were subjected to in vitro digestion for the detection of larvae of Trichinella spp., according to Reg. EC No. 2075/ Rectal faecal samples of all foxes were subjected to coprological examination with flotation in centrifuge in a solution of zinc sulphate (specific gravity 1.350). Specific identification of parasites was based on the observation by optical microscopy of the morphology of eggs, larvae or adult worms, according to taxonomical keys (Levine, 1968; Campbell, 1991). All adult parasites found were isolated, counted, separated by gender, and stored in 70% alcohol. Data analysis Prevalences with a 95% confidence interval (CI), abundance, mean intensity and range were calculated (Thul et al., 1985; Bush et al., 1997). Multiple infections were also described. The negative binomial distribution was fitted to investigate the ecological equilibrium among hosts and the most prevalent parasites, as an indication of overdispersion (Bliss & Fisher, 1953). Results of the coprological tests were compared to necropsy (gold standard). Pearson s chi squared test and Fisher s exact test were carried out. Multivariate logistic regression was carried out, taking positivity for parasites as the dependent binary variable and gender and age as

3 508 M. Magi et al. covariates. The significance of tests was reached for P values less than Results and discussion The present epidemiological research shows that the red fox in the study area hosts a wide variety of extraintestinal nematodes (table 2). Nine nematode species (A. vasorum, E. aerophilus, E. boehmi, C. vulpis, Filaroides spp., S. lupi, Aonchotheca putorii, Physaloptera spp. and P. plica) were found. The most prevalent parasite was A. vasorum (78.2%) in the heart and lung arteries, followed by P. plica (56.8%) in the urinary bladder. No fox was found to be completely negative for parasites. For the most prevalent parasitic species a negative binomial distribution fitted the data, indicating an ecological equilibrium between hosts and parasites (all P values of the goodness-of-fit chi square tests were larger than 0.05). The parameters of the fitted distributions were: A. vasorum, k ¼ 0.545, P ¼ 0.068; E. aerophilus, k ¼ 0.214, P ¼ 0.108; P. plica, k ¼ 0.485, P ¼ No significant difference in the prevalence of parasites was observed between genders and age classes, except for P. plica (P value ¼ ). For this parasite, juvenile animals (93.3%) were more infected than adults (47.5%). These results were confirmed by logistic regression with positivity for parasite as the dependent variable and gender and age as covariates. Angiostrongylus vasorum (prevalence 78.2%), E. aerophilus (41.8%), C. vulpis (15.8%) and Filaroides spp. (4.8%) were found in the cardiopulmonary system. Altogether 67 multiple infections were recorded: two cases of quadruple infection with A. vasorum, E. aerophilus, C. vulpis and Filaroides spp.; 13 cases of triple infection and 52 cases of double infection, 38 of which included infections with A. vasorum and E. aerophilus. Co-infections with A. vasorum and E. aerophilus were the most frequent; however, the correlation was not statistically significant. The results of the copromicroscopy concerning extraintestinal parasites were as follows: E. aerophilus prevalence 25.5% (95% CI: %), A. putorii 6.7%, S. lupi 4.2% ( %), Physaloptera spp. 1.2% (0 2.9%). Two foxes were found to be positive for Physaloptera spp. with the coprological test, but it was not possible to examine their stomachs. Two other foxes were positive at necropsy, but negative after the coprological examination. The results of the coprological test concerning extraintestinal species were compared with necropsy considered as a gold standard and the sensitivity (S) and specificity (S 0 ) were calculated for E. aerophilus, S ¼ 0.49, S 0 ¼ 0.92; S. lupi, S ¼ 0.26, S 0 ¼ 0.97; A. putorii, S¼ 0.33, S 0 ¼ 0.97; and Physaloptera spp., S ¼ 0, S 0 ¼ 1. A low sensitivity of the coprological test is expected and was observed for E. aerophilus in foxes by Lalošević et al. (2013) and for S. lupi in dogs by Mylonakis et al. (2001). The coprological test also revealed the presence of intestinal parasites: Ancylostomatidae (prevalence 48.5%), Toxocara canis (18.2%), Molineus spp. (18.2%), Toxascaris leonina (14.5%), Coccidia (10.3%), Trichuris vulpis (4.8%), Mesocestoides spp. (3.6%) and Hymenolepis diminuta (3.0%). Angiostrongylus vasorum was found to be the most frequent cardiorespiratory parasite. The prevalence recorded in the present study is among the highest in Europe (table 1) and worldwide (56% in Canada, Jeffery et al., 2004). The presence of A. vasorum in our study area matches the predicted distribution described in the model by Morgan et al. (2009) based on climatic conditions. This species has been reported as a common parasite in foxes, and less frequently in dogs, in Europe, Africa, and North and South America (Morgan et al., 2005). However, over the past two decades, the number of reports in dogs has increased (Conboy, 2011). The prevalence of E. aerophilus found in the present work (41.8%) is the highest reported in Italy and is comparable with other studies available (table 1). Most surveys reported prevalences higher than 30%, although values vary from 5% (Eira et al., 2006, Portugal; Martinez- Carrasco et al., 2007, Spain) to 97.1% (Bružinskaitė- Schmidhalter et al., 2011, Lithuania)) (table 1). Eucoleus aerophilus may be responsible for rare zoonotic infections, and 12 cases have been reported in the literature: 8 in Russia, 1 in Morocco, 1 in Iran (Aftandelians et al., 1977), 1 in France and 1 in Serbia (Lalošević et al., 2008). The prevalence of C. vulpis observed in the present investigation is consistent with values found in other surveys (table 1). Higher values (78.4%) have been found in foxes in Canada by faecal examination (Nevárez et al., 2005). Table 2. The prevalence (%), abundance (A), mean intensity (MI) and range (R) of cardiopulmonary, gastric and urinary nematodes identified in the present study; N ¼ number of foxes examined; CI ¼ 95% confidence intervals;, not recorded. % CI A MI R Cardiopulmonary nematodes, N ¼ 165 Angiostrongylus vasorum Eucoleus aerophilus Crenosoma vulpis Filaroides spp Gastric nematodes, N ¼ 81 Spirocerca lupi Aonchotheca putorii Physaloptera spp Urinary nematodes, N ¼ 74 Pearsonema plica

4 Extraintestinal nematodes of foxes from Italy 509 Lung nematodes of the genus Filaroides were detected in eight foxes (4.8%). These parasites are quite rare in canids. In Europe, to the best of our knowledge, they have only been found in dogs (Caro-Vadillo et al., 2005). One of the two foxes whose nasal cavities we were able to examine was positive for E. boehmi and three adult worms were collected. Eucoleus boehmi is similar to E. aerophilus, but lives in the nasal and paranasal cavities of canids instead of in the trachea. Eggs of E. boehmi measure mm, contain a multicellular embryo that frequently does not entirely fill the egg, have a surface marked by delicate pits, and are bipolar plugged. The eggs of E. aerophilus are bigger, mm, have a net-like outer layer, polar plugs, and are entirely filled by one- or two-cell embryos (Campbell, 1991). Eucoleus boehmi was identified for the first time in foxes from Moravia and Austria (Supperer, 1953) and was then found in red foxes and wolves in Poland (Zarnowsky & Patyk, 1960), in foxes in Austria (Hinaidy, 1971), Germany (Schöffel et al., 1991), Hungary, Norway and Serbia (table 1). To the best of our knowledge, this is the first published report of E. boehmi in foxes in Italy. Filarial infections were not found in any animal in the present work. Wild canids are infected by D. immitis in areas where this parasite is endemic (Gortázar et al., 1994). This confirms that foxes are only epiphenomena in the epidemiology of D. immitis (Stancampiano et al., 1998). Spirocerca lupi (23.5%), A. putorii (8.6%) and Physaloptera spp. (2.5%) were found in the stomach (table 2). Spirocerca lupi lives in the oesophagus and stomach of wild canids (foxes, wolves, jackals) and domestic dogs in the Middle East, China, India, Japan, South America and southern USA (Pence & Stone, 1978; Ferrantelli et al., 2010). Reports of S. lupi in European red foxes are limited to the Iberian peninsula (Gortázar et al., 1998; Segovia et al., 2004; Eira et al., 2006) and Belarus (Shimalov & Shimalov, 2002). In Italy, this parasite has been found in foxes in Sardinia (Leoni et al., 1985; Polidori et al., 1985) and in Sicily (Ferrantelli et al., 2010) (table 1). Reports of Physaloptera spp. and A. putorii in foxes are rare (table 1): P. sibirica was found for the first time in Italy in foxes and badgers from Aosta Valley and Piedmont (Ferroglio et al., 2009), with a similar prevalence in foxes (2.63%) to the value found in the present study. This gastric parasite had previously only been reported in Spain (Miquel et al., 1996; Rodriguez & Carbonell, 1998; Segovia et al., 2004) and in Belarus (Shimalov & Shimalov, 2002). Aonchotheca putorii is more frequently found in mustelids (Sato et al., 1999). Pearsonema plica was found in the urinary bladder of 42 foxes (56.8%), while kidneys were negative. Eggs of this Trichuridae are shed in the urine and are characterized by a lemon shape, similar to the eggs of E. aerophilus and E. boehmi (Campbell, 1991). Pearsonema plica was found in Italy in foxes more than 20 years ago (Iori et al., 1990) and more recently in pets (Callegari et al., 2010; Rossi et al., 2011). The prevalence of this parasite in the present study is in agreement with other epidemiological studies (table 1). Although all the foxes examined were negative for Trichinella spp., we believe that monitoring should continue, since this host is one of the main reservoirs of many Trichinella species (Pozio, 2007; Chmurzyńska et al., 2013). Foxes that are positive for Trichinella spp. have been found in Liguria and Piedmont (Rossi et al., 1992) and a human case was reported in Cuneo (Romano et al., 2011). The present study confirms that red foxes represent an important wild reservoir of extraintestinal parasites that can be transmitted to domestic animals, particularly to dogs (Bolt et al., 1991). Furthermore, the presence of E. aerophilus is important, because this parasite can be responsible for zoonotic infections (Lalošević et al., 2008). Extraintestinal nematodes have been reported increasingly in pets worldwide and are considered as emerging parasites (Rinaldi et al., 2007; Conboy, 2009; Bork-Mimm & Rinder, 2011; Clark et al., 2013), due to the greater focus of parasitologists on these species. The apparent spread to domestic animals could be associated with the increase in the fox population (Deplazes et al., 2004). Epidemiological research on foxes could therefore provide useful information on these parasites. Financial support This research received no specific grant from any funding agency, commercial or not-for-profit sectors. None. Conflict of interest 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, 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, 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, Bork-Mimm, S. & Rinder, H. (2011) High prevalence of Capillaria plica infections in red foxes (Vulpes vulpes) in Southern Germany. Parasitology Research 108, 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, 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, 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, Campbell, B.G. (1991) Trichuris and other Trichinelloid nematodes of dogs and cats in the United States.

5 510 M. Magi et al. Compendium on Continuing Education for the Practicing Veterinarian 13, 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, 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, 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, Conboy, G. (2009) Helminth parasites of the canine and feline respiratory tract. The Veterinary Clinics of North America Small Animal Practice 39, Conboy, G. (2011) Canine angiostrongylosis: the French heartworm: an emerging threat in North America. Veterinary Parasitology 176, 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, Deplazes, P., Hegglin, D., Gloor, S. & Romig, T. (2004) Wilderness in the city: the urbanization of Echinococcus multilocularis. Trends in Parasitology 20, 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, 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, Ferroglio, E., Ragagli, C. & Trisciuoglio, A. (2009) Physaloptera sibirica in foxes and badgers from the Western Alps (Italy). Veterinary Parasitology 163, Gerrikagoitia, X., Barral, M. & Juste, R.A. (2010) Angiostrongylus species in wild carnivores in the Iberian Peninsula. Veterinary Parasitology 174, 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, 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, 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, Hinaidy, H.K. (1971) Die Parasitenfauna des Rotfuchses, Vulpes vulpes (L.), in Oesterreich. Zentralblatt für Veterinarmedizin Reihe B 18, Iori, A., Costantini, R. & Cancrini, G. (1990) Parassiti in volpi provenienti da alcune regioni italiane. Parassitologia 32, 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. 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, 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, 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. Leoni, A., Masala, S. & Garippa, G. (1985) Principali lesioni da Spirocerca lupi in Vulpes vulpes. Atti Società Italiana Scienze Veterinarie 39, Levine, N.D. (1968) Nematode parasites of domesticated animals and man. 477 pp. Minneapolis, USA, Burgess Publishing. 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, 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, 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, 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, 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, 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, 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, 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,

6 Extraintestinal nematodes of foxes from Italy 511 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, 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, 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, Pence, D.B. & Stone, J.E. (1978) Visceral lesions in wild carnivores naturally infected with Spirocerca lupi. Veterinary Pathology 15, Polidori, G.A., Mura, A., Moretti, A., Balzano, A. & Principato, M. (1985) Spirocerca lupi nella volpe in Sardegna. Atti Societa Italiana Scienze Veterinarie 39, Pozio, E. (2007) World distribution of Trichinella spp. infections in animals and humans. Veterinary Parasitology 149, 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, Rodriguez, A. & Carbonell, E. (1998) Gastrointestinal parasites of the Iberian lynx and other wild carnivores from central Spain. Acta Parasitologica 43, 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, 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, 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, Saeed, I., Maddox-Hyttel, C., Monrad, J. & Kapel, C.M.O. (2006) Helminths of red foxes (Vulpes vulpes)in Denmark. Veterinary Parasitology 139, 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, Schöffel, I., Schein, E., Wittstadt, U. & Hentsche, J. (1991) Zur Parasitenfauna des Rotfuchsen in Berlin (West). Berliner und Muencher Tieraerztliche Wochenschrift 104, 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, 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, Shimalov, V.V. & Shimalov, V.T. (2002) Helminth fauna of the red fox (Vulpes vulpes L. 1758) in Southern Belarus. Parasitology Research 89, Sréter, T., Szell, Z., Marucci, G., Pozio, E. & Vargac, I. (2003) Extraintestinal nematode infections of red foxes (Vulpes vulpes) inhungary. Veterinary Parasitology 115, 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. Supperer, R. (1953) Capillaria boehmi Spec. Nov., eine neue Haarwurm-Art aus den Stirnhoehlen des Fuchses. Zeitschrift fűr Parasitenkunde 16, 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, Tønsberg, H., Saeed, I. & Koch, J. (2004) Parasitologisk undersøgelse af jagthund og rav i Odsherred. Dansk Veterinær Tidsskrift 87, Zarnowsky, E. & Patyk, W. (1960) On the independence of the species Thominx böhmi (Supperer, 1953) and its occurrence. Acta Parasitologica Polonica 8,