Wild Red Foxes ( Vulpes vulpes ) as Sentinels of Parasitic Diseases in the Province of Soria,Northern Spain

Abstract

Four hundred red foxes (Vulpes vulpes) were examined for ecto- (arthropods) and endoparasites (Leishmania spp., Trichinella spp., and intestinal parasites). Different species of flea (total prevalence, 40.50%), tick (16.25%), mite (7.25%), and fly (1.50%) were identified. The most prevalent flea was Pulex irritans (found on 29% of the foxes); the most prevalent tick, mite, and fly were Ixodes canisuga (on 5%), Sarcoptes scabiei (on 5.25%), and Hippobosca equina (on 1%), respectively. The endoparasites identified included Leishmania spp. (found in 12% of the foxes), Trichinella spp. (in 15.5%, with T. britovi the most prevalent species in 15.25%), Cestoda (in 72.75%, with Mesocestoides spp. the most prevalent in 69.50%), and intestinal ascarids (in 73.25%, with Ancylostoma caninum the most prevalent in 12.50%). No animal was free of parasites. The present results suggest that foxes can act as sentinels of diseases transmitted by ecto- and endoparasites.

Introduction

Wildlife provides a “zoonotic pool” by which humans may become exposed to pathogens capable of crossing the species barrier (Zeier et al. 2005, Gortázar et al. 2007). Contact between humans and wild animals may occur when they enter each other's ecosystems (Wakernagel et al. 2002). Sentinel species provide information on the spread of emerging parasitic diseases. Foxes are potentially ideal for monitoring such diseases because they can adapt to different ecosystems and are known to act as reservoirs of several diseases affecting wild and domestic animals (Aguirre 2009). As opportunistic carnivores, these animals make use of all kinds of food sources and are commonly found in humanized environments where they feed on waste human food.

To assess the use of this species as a sentinel of disease, the present study examined the ecto- (arthropods) and endoparasites (Leishmania spp., Trichinella spp., and intestinal parasites) carried by red foxes in the Province of Soria in northern Spain (which extends from 42°08′20″N to 41°04′15″S, and 01°47′45″E to 03°31′45″W).

Materials and Methods

Animal samples

Four hundred red foxes were examined for arthropod ectoparasites and endoparasites in the Soria Province, as can be seen in Figure 1. These foxes were either donated by licensed hunters or were found dead by forestry agents (usually road kills). The collection of specimens lasted 4 years.

FIG. 1.

Geographical distribution of the numbers of specimens collected and studied in Soria Province, northern Spain.

The specimens were quickly transported to the laboratory in sealed plastic bags (between 1–4 h, depending on geographical location) and examined immediately. The specimens found dead were estimated to be useful depending on the conditions of the carcasses, and those that were in poor condition were not included in the study.

The animals were classified as either juvenile (with milk teeth; <1 year old), adult (with permanent, unworn teeth; 1–5 years old), or old (with markedly worn teeth; over 5 years old). The sex of each animal was also noted.

Permission to take and study these animal samples was obtained from the regional government of Castilla y León in compliance with current legislation (protocol no. 06.01.017.006) and in keeping with the ethical guidelines of the Committee on Animal Experimentation of the University of Alcalá de Henares (protocol no. CEI 2011034).

Ectoparasites

All of the foxes were combed to harvest their arthropod ectoparasites. Members of Sarcoptes scabiei were extracted by KOH (10%) digestion of skin surface samples. All ectoparasites collected were stored in sterile tubes containing 70% ethanol for later examination under a binocular microscope. Morphometric keys were used to make identifications (Gil-Collado 1948, 1961, Feldman-Muhsam 1952, Hoogstraal 1956, Filippova 1981, Starkof 1981, Beaucournu and Launay 1990, Krantz 1998, Walker 2000).

Endoparasites

Leishmania

Free amastigotes and/or parasitized cells were detected in Giemsa-stained blood smears; all samples were examined by optical microscopy (1000×). When amastigotes were detected, blood samples from affected animals were cultured on blood agar. Species identification was performed by enzymatic characterization (13 systems [15 loci]) (Evans et al. 1989, Rioux and Lanotte 1990).

Trichinella

A total of 400 striated muscle samples were obtained from the diaphragm during necropsy and examined for cysts. Identification at the species level was performed by PCR as described elsewhere (García-Sánchez et al. 2009).

Intestinal parasites

The small intestine of each animal was sectioned at the pylorus and cecum and frozen at −20°C until analysis, whereupon it was opened longitudinally and inspected visually (either with the naked eye or using a binocular microscope). All macroparasites were collected and preserved in 10% formol for later identification. Mucosa samples were also examined under the binocular microscope to detect Echinococcus spp. The contents of the intestine were also examined under the binocular microscope after washing with a saline solution. Samples were preserved in 10% formol for later examination and identification of any parasites or their eggs.

Statistical analysis

The Fisher exact test and Pearson test chi-squared were used to compare the prevalence of the different types of parasites detected, taking fox gender and age into account. Significance was set at p < 0.05. Calculations were performed using Access 2000 and G-Stat v.1.2 software.

Results

Of the 400 foxes examined, 80 were collected in spring, 12 in summer, 42 in autumn, and 266 in winter (the main hunting season in Spain). None of the 400 animals examined was free of parasites. A total of 198 foxes (49.50%) were female and 202 (50.50%) were male; 61 (15.25%) were juvenile, 233 (58.25%) were adult, and 106 (26.5%) were old.

Ectoparasites

In all, 162 (40.50% of all those examined) carried fleas. Some 36.61% (78/202) of the males and 42.42% (84/198) of the females were infested; 45.90% (28/61) of the juveniles were infested, as were 38.62% (90/233) of the adults and 41.50% (44/106) of the old foxes (no statistical differences with respect to age or sex). Table 1 shows the different flea species (n = 13) detected. The most common species was Pulex irritans, which was found on 116 foxes (29% of all animals and on 71.60% of all flea-infested foxes). Twenty two foxes carried more than one species of flea, the most prevalent association being that of P. irritans and Ctenocephalides canis (in 10 foxes). No animals showed clinical dermatitis due to flea bites.

Table 1.

Prevalence of the Species of Ectoparasites

Ectoparasites	Number foxes infested	%
Fleas
Pullex irritans	116	29
Ctenocephalides canis	20	5
Chaetopsilla tricosa	8	2
Ctenocephalides felis	3	0.75
Myoxopsylla laverani	3	0.75
Spilopsyllus cuniculi	3	0.75
Nosopsyllus fasciatus	2	0.50
Paraceras melis	2	0.50
Archaeopsylla erinacei maura	1	0.25
Chaetopsylla matina	1	0.25
Ctenocephtalmus andorrensis	1	0.25
Odontopsyllus quirosi	1	0.25
Typhloceras poppei	1	0.25
Ticks
Ixodes canisuga	20	5
Ixodes ricinus	17	4.25
Rhipicephalus sanguineus	14	3.50
Ixodes hexagonus	11	2.75
Dermacentor marginatus	1	0.25
Rhipicephalus pusillus	1	0.25
Dermacentor reticulatus	1	0.25
Mites
Sarcoptes scabiei	21	5.25
Neotrombicula autumnalis	6	1.50
Cheyletiella yasguri	2	0.50
Flies
Hippobosca equina	4	1
Hippobosca capensis	1	0.25
Stomoxys calcitrans	1	0.25

Sixty-five foxes (16.25% of all those examined) carried ticks. Some 15.34% (31/202) of the males and 17.17% (34/198) of the females were infested; 8.19% (5/61) of the juveniles were infested, as were 15.87% (37/233) of the adults, and 21.69% (23/106) of the old foxes (no statistical differences with respect to age or sex). Table 1 shows the different tick species (n = 7). The most common tick found was Ixodes canisuga (5% of all animals and 30.76% of all tick-infested foxes). Eleven animals carried more than one species of tick; the most prevalent association was that of Ixodes hexagonus and Ixodes ricinus, which was seen in six foxes.

Twenty-nine foxes (7.25% of all those examined) carried mites. Another 34 showed lesions consistent with scabies. The intensity of these lesions varied from slight to covering more than 50% of the body (seen in two foxes). Some 7.92% (16/202) of the males and 6.56% (13/198) of the females were infested; 4.91% (3/61) of those with fleas were juveniles, 5.15% (12/233) were adults, and 13.2% (14/106) were old (no statistical differences with respect to age or sex). Table 1 shows the different mite species recorded (n = 3). Infestation with identifiable S. scabiei mites (on 5.25% of all animals and on 72.41% of all those mite-infested) was significantly more prevalent in the old animals than in the rest (p < 0.05) (detected on two juvenile animals, seven adults, and 12 old animals).

Fly species were found on six foxes (1.5% of all those examined). Some 0.25% (1/202) of the males and 2.52% (5/198) of the females were infested; 0% (0/61) of the juveniles carried flies, as did 2.14% (5/233) of the adults, and 0.94% (1/106) of the old foxes (no statistical differences with respect to age or sex). Three species were detected (Table 1). The most common species was Hippobosca equina, which was found on four foxes (1% of all animals and 66.6% of all fly-infested foxes).

Endoparasites

Leishmania infantum zimodema ZM-1 was detected in 48 foxes (12% of all those examined). Some 9.90% (20/202) of the males and 14.14% (28/198) of the females were infested; 24.59% (15/61) of the juveniles carried L. infantum, as did 8.58% (20/233) of the adults, and 12.26% (13/106) of the old foxes (significantly more prevalent in the juvenile animals than in the rest, p < 0.0001). Most of the affected animals showed no signs of disease. However, 2.5% of those infected showed enlarged livers and spleens, and two others showed cutaneous manifestations compatible with leishmaniosis.

Sixty-one foxes were found to carry Trichinella spp. (15.5% of all those examined). Some 14.85% (30/202) of the males and 15.65% (31/198) of the females were infested. The most prevalent was Trichinella britovi, which was found in 61 foxes (98.38% of all those infected with Trichinella spp.) (Table 2). Trichinella spiralis was found in just one old female fox. T. britovi was significantly (p < 0.0001) more prevalent among adults (12.87%, 30/233) and old foxes (28.30%, 30/106) than in juveniles (1.63%, 1/61).

Table 2.

Prevalence of the Species of Endoparasites

Endoparasites	Number foxes infested	%
Leishmania
Leishmania infantum zimodema ZM-1	48	12
Trichinella
Trichinella britovi	61	15.25
Trichinella spiralis	1	0.25
Cestode
Mesocestoides spp.	272	69.50
Dipylidium caninum	19	4.75
Echinococcus spp.	0	0
Intestinal ascaride
Ancylostoma caninum	50	12.50
Spirocerca lupi	20	5
Toxocara canis	10	2.50

A total of 291 foxes (72.75% of all those examined) were infected by cestodes. These parasites more commonly infected male foxes (77.72%; 157/202) than females (67.67%; 134/198) (p < 0.05). They were more prevalent in adult foxes (75.10%; 175/233) and old animals (76.41%; 81/106) than in juveniles (57. 37%; 35/61) (p < 0.03). The most common cestode detected was Mesocestoides spp. (detected in 272 foxes, 93.47% of all those infected by cestodes). Only two were infected by Mesocestoides spp. in the tetratyridial stage. No fox was found with Echinoccoccus granulosus (Table 2).

In all, 293 foxes (73.25% of all those examined) were infected with intestinal ascarids. Some 76.73% (155/202) of the males and 69.69% (138/198) of the females were infested. Ascarids were significantly (p = 0.0015) more prevalent in adult (74.24%, 173/233) and old foxes (81.13%, 86/106) than in juveniles (55.73%, 34/61). However, only 20% of the foxes carried ascaridia species that affect humans (Table 2). The most common species (p < 0.05) was Ancylostoma caninum (detected in 12.50% of all animals).

Discussion

The following sections discuss the present results of greatest relevance in the surveillance of human disease and the use of foxes as sentinels.

Ectoparasites

Unfortunately, foxes have usually been dead for some time when they reach the laboratory, and their ectoparasites are normally long gone. Even so, several ectoparasite species were detected in the present work.

Fleas

In the present work, the flea species found that can infest humans were P. irritans, C. canis, and C. felis (Bitam et al. 2010). P. irritans, commonly known as the human flea, was the most prevalent (29%). This species can infest a wide range of hosts, although carnivores are preferred (Domínguez-Peñafiel 2004, Domínguez-Peñafiel et al. 2011). In the south of Spain, the prevalence of P. irritans reaches 58% in foxes (Millán et al. 2007). The highest frequency in European foxes was reported from Hungary (43%) (Sréter et al. 2003); prevalence appears to be 0% in German foxes (Schöeffel et al. 1991). These differences could be due to different ecological environments, because small fluctuations in temperature can produce marked effect on the development cycle of several parasites.

Some of the present foxes carried P. irritans as well as other fleas species (up to three in total), with the association between the latter and C. canis the most common (seen in 10 foxes). An Egyptian study (el-Damarany 1997) has reported three species of flea on Vulpes rueppellii.

The other fleas detected in the present work were C. canis and C. felis (prevalence 5.00 and 0.75%, respectively) that are thought to be involved in emerging zoonotic diseases around the world. Ctenocephalides spp. are vectors of Bartonella hensenlae, Rickettsia typhi, and Rickettsia felis (Kaewmongkol et al. 2011, Kumsa et al. 2014). Millán et al. (2007) reported no C. canis on foxes in southern Spain. In Hungary, its prevalence has been reported at 11% (Sréter et al. 2003), whereas in Germany just 1% of foxes are reported affected (Schöeffel et al. 1991). The prevalence of C. felis in arthropods in northern Spain (Burgos) has previously been reported at 2.20% (Lledó et al. 2010), whereas in the south of the country no foxes are reported affected (Millan et al. 2007).

Ticks

All ticks found in this study have been linked as vectors of diseases that affect humans mainly transmitting bacteria like caused by members of Rickettsiae and Borrelia burgdorferi. I. canisuga was the most prevalent tick found in the present work. This species prefers carnivore hosts. It is reported as a new species involved in the epidemiology of Lyme disease. In areas of Spain where I. ricinus is absent, some 30% of I. canisuga ticks are reported to carry B. burgdorferi (Estrada-Peña et al. 1999). Recently, Hornok et al. (2013) reported Ehrlichia canis in I. canisuga larvae on red foxes, and proposed that this species might play a reservoir role in the epidemiology of canine ehrlichiosis.

I. ricinus is the tick that usually transmits B. burgdorferi to humans in Europe (Dantas-Torre et al. 2013), and Mediterranean spotted fever (MSF), caused by R. conorii, is mainly transmitted by Rhipicehalus sanguineus (Brouqui et al. 2007). Dermacentor marginatus is the main vector of Rickettsia slovaca and Dermacentor reticulatus may also act as a vector for this pathogen (Lledó et al. 2006).

Mites

S. scabiei was found on 5.25% of all the foxes examined and was the most prevalent of all mites detected. It is commonly found on foxes (Oleaga et al. 2011). The prevalence of S. scabiei in foxes has been reported at 33% for northern Spain (Domínguez-Peñafiel et al. 2011) and 23.1% for the Ebro Valley (Gortázar et al. 1998), much larger than the value recorded in the present study.

In serodiagnostic studies performed in Norway, the prevalence of animals with clinical scabies was reported to have fallen significantly between 1995 and 2005 (from 30% to 6.6%). This suggests that the red fox population is adapting to live with the parasite (Davidson et al. 2008).

The prevalence of Neotrombicula spp. in the present foxes was low (1.5%). These mites can act as vectors of Anaplasma phagocytophila (Fernández-Soto et al. 2001), a causal agent of seasonal human dermatitis (Stekolnikov et al. 2014).

Flies

None of the flies detected has any importance in the spread of human disease.

Endoparasites

It is curious to note that only we found statistical significant differences in terms of the prevalence of the study of endoparasites, but not in the study of ectoparasites. In particular, a significantly higher prevalence of the endoparasitosis is usually detected in adult and old animals that in juvenile foxes.

Leishmania

Some 12% of all the foxes examined were infected with L. infantum. It is reported that foxes are more commonly parasitized by Leishmania spp. than dogs, but suffer no symptoms, and mortality is low (Courtenay et al. 1994). The prevalence of L. infantum infection in foxes has been reported at 21% in Hungary (Sréter et al. 2003) and at 25% in Germany (Schöeffel et al. 1991). In the Province of Guadalajara (Spain), a prevalence of 74% has been reported in foxes, whereas it is about 7% in dogs of the Castilla la Mancha Region (to which Guadalajara belongs) (Criado-Fornelio et al. 2000). In the south of Spain, a prevalence of 14.1% has been reported in wild carnivores (Sobrino et al. 2008).

Trichinella

The prevelance of T. spiralis was just 0.25%, whereas that of T. britovi was 15.25%. Similar results have been reported from Poland (Okulewicz et al. 2005). T. spiralis has been reported in foxes from southwestern Spain with a prevalence of 33% (Pérez-Martín et al. 2000); in central Spain, a prevalence of 8.9% has been reported (Criado-Fornelio et al. 2000), whereas in Catalonia (northeastern Spain), the prevalence is just 0.3% (López-Olvera et al. 2011). No reports are available on the prevalence of T. britovi infection in Spain. However, in France, a prevalence of 2.7% has been reported for foxes (Aoun et al. 2012) and a value of 31% for foxes in Serbia (Zivojinovic et al. 2013). In Denmark (Al Sabi et al. 2013) and Corsica (Richomme et al. 2010), no Trichinella spp. has been detected in foxes. Therefore, a wild cycle of trichinellosis seems to occur in Spain. The present results were gathered via compression and trichinoscopy. The known limitations (Venturiello et al. 1998) of this methodology suggest the results may actually be underestimates.

Cestodes

Some 69.50% of all the cestodes detected belonged to Mesocestoides spp. In Galicia (northwestern Spain), only 2.5% of foxes carried these endoparasites (Álvarez et al. 1995), whereas in Greece a value of 73.2% has been reported (Papdopoulos et al. 1997). In Germany, the prevalence is reported at 54.1% (Pfeiffer et al. 1997), in Denmark at 35.6% (Saeed et al. 2006), in Slovenia at 27.6% (Vergles Rataj et al. 2013), and in Slovakia at 41.9% (Hrčkova et al. 2011).

Although this parasite rarely affects humans, some cases of mesocestoides infection have been reported (Eom et al. 1992, Fuentes et al. 2003). The symptoms recorded to date have not been problematic, but no infestations involving tetratyridia, which could cause great harm, have been documented. The two foxes parasitized in the present work, however, did contain tetratyridia.

The prevalence of Dipylidium caninum was 4.75%. Tapeworm infestation is more common in humans than mesocestoides infestation, especially in children (Szwaja et al. 2011, Taylor and Zitzman 2011, Narasimham et al. 2013). Infestation occurs accidentally and can cause diarrhea, abdominal pain, and discomfort. The present prevalence value in foxes is higher than those reported from Germany (0.2%) (Pfeiffer 1997) and Galicia (0.5%) (Álvarez et al. 1995), but lower than those from England (3.8%) (Richards et al. 1995), Slovenia (1.4%) (Vergles Rataj et al. 2013), and Italy (57.3%) (Magi et al. 2009).

No Echinococcus infection of any kind was detected in any of the examined foxes. This agrees with that reported by Criado-Fornelio et al. (2000) in the Province of Guadalajara. Dogs (Canis familiaris) are the definitive host of E. granulosus, but foxes have been reported to carry it in England (prevalence 0.1%) (Richards et al. 1995) and in Canberra, Australia (7%) (Jenkins and Craig 1992). Foxes play a fundamental role in the cycle of alveolar hydatid disease (caused by E. multilocularis) in Central and Northern Europe (Saeed et al. 2006, Vergles Rataj et al. 2013).

Intestinal ascarids

All the following intestinal ascarids can cause accidental disease in humans. The prevalence of A. caninum in the present foxes was 12.50%, which was higher than that obtained in the Spanish provinces of Salamanca (3.20%) (Simón 1975) and Guadalajara (4.4%) (Criado-Fornelio et al. 2000). In Germany, a prevalence of 7% was reported (Pfeiffer et al. 1997), while in Denmark it was just 0.6% (Saeed et al. 2006). The prevalence of Spirocerca lupi was 5%. In northwestern Italy, the prevalence in red foxes has been reported at 23.5% (Magi et al. 2014).

The prevalence of Toxocara canis was 2.50%. This agrees with that reported for the Province of Guadalajara by Criado-Fornelio et al. (2000), but is very different to the 23% reported for Galicia (Álvarez et al. 1995). In Italy a prevalence of 9.1% has been reported (Magi et al. 2009), in Germany 26.5% (Pfeiffer et al. 1997), in the United Kingdom 55.9% (Richards et al. 1995), and in Denmark 59.4% (Saeed et al. 2006).

Conclusions

The present results show that foxes could act as sentinels of diseases transmitted by both ecto- and endoparasites. Foxes move through several habitats, feed on many food sources, and carry a range of parasites that may cause disease, many of which are emerging, in humans. Because their behavior brings them into contact with domestic animals and humans, the risk of diseases entering human environments is not unappreciable.

Footnotes

Acknowledgments

The authors thank the Department of Parasitology of the Universidad Complutense (Madrid), the Reference Laboratory for Leishmaniosis of the Instituto de Salud Carlos III, and the Laboratorio de Sanidad y Medio Ambiente del Gobierno de La Rioja (Spain) for their help with this work.

Author Disclosure Statement

No competing financial interests exist.

References

Aguirre

. Wild canids as sentinels of ecological health: A conservation medicine perspective. Parasit Vectors, 2009; 2:s7.

Al Sabi

, Chriel

, Jensen

, Enemark

. Endoparasites of the racoon dog (Nyctereutes procyonides) and the red fox (Vulpes vulpes) in Denmark 2009–2012. A comparative study. Int J Parasites Wild, 2013; 17:144–151.

Álvarez

, Iglesias

, Garcia

, Paniagua

, et al. Intestinal helminths of the red fox (Vulpes vulpes L.) in Galicia (Northwest Spain). Wiad Parazytol, 1995; 41:429–442.

Aoun

, Lacour

, Levieuge

, Marie

, et al. Screening for Trichinella britovi infection in red fox (Vulpes vulpes) and wild boar (Sus scrofa) in southeastern France. J Wild Dis, 2012; 48:223–225.

Beaucournu

, Launay

. Faune de France (France et régions limitrophes). Les puces (Siphonaptera) de France et du Bassin méditerranén occidental. Fed Fran Soc Sci Natur Paris, 1990; 76.

Bitam

, Dittmar

, Parola

, Whiting

, et al. Fleas and flea-borne diseases. Int J Infect Dis, 2010; 14:667–676.

Brouqui

, Parola

, Fournier

, Raoult

. Spotted fever rickettsioses in southern and eastern Europe. FEMS Immunol Med Microbiol, 2007; 49:2–12.

Courtenay

, Macdonald

, Lainson

, Shaw

, et al. Epidemiology of canine leishmaniasis: A comparative serological study of dogs and foxes in Amazon Brazil. Parasitology, 1994; 109:273–279.

Criado-Fornelio

, Gutiérrez-Garcia

, Rodríguez-Caabeiro

, Reus-García

, et al. A parasitological survey of wild red foxes (Vulpes vulpes) from the province of Guadalajara, Spain. Vet Parasitol, 2000; 92:245–251.

10.

Dantas-Torres

, Otranto

. Species diversity and abundance of ticks in three habitats in southern Italy. Ticks Tick Borne Dis, 2013; 4:251–255.

11.

Davidson

, Bornstein

, Handeland

. Long-term study of Sarcoptes scabiei infection in Norwegian red foxes (Vulpes vulpes) indicating host/parasite adaptation. Vet Parasitol, 2008; 156:277–283.

12.

Domínguez-Peñafiel

. North Spain (Burgos) wild mammals ectoparasites. Parasite, 2004; 11:267–272.

13.

Domínguez-Peñafiel

, Giménez-Pardo

, Lledó

, Gegúndez

. Prevalence of ectoparasitic arthropods from wild and domestic animals in the Burgos province (Spain). Parasite, 2011; 18:251–260.

14.

el-Damaranay

. Helminth and arthropod parasites of sandy fox, Vulpes ruppeli (Fissipedea. Carnivora) from Sohag, with redescription of Platynosomum fastosum (Digenea: Dicrocoelidae). J Egypt Soc Parasitol, 1997; 27:755–772.

15.

Eom

, Kim

, Rim

. Second Case of human infection UIT Mesocestoides lineatus in Korea. Kisaengchunghak Chapchi, 1992; 30:147–150.

16.

Estrada-Peña

, Jongjean

. Ticks feeding on humans: A review of records on human biting Ixodoidea with special reference to pathogen transmission. Exp Appl Acarol, 1999; 23:685–715.

17.

Evans

, Godfrey

, Lanham

, Lanotte

, Modabber

, Schnur

. Characterization of Leishmania , In Evans

D.A

(Ed). Handbook on isolation, characterization and cryopreservation of Leishmania. UNDP/WORLD BANK/WHO special programme for Research and Training in Tropical Diseases (TDR). Geneva, Switzerland: World Health Organization, 1989:1–45.

18.

Feldman-Muhsam

. On the identity of Rhipicephalus sanguineus (Latreille). Bull. Res. Counc Israel, 1952: 2.

19.

Fernández-Soto

, Pérez-Sanchez

, Encinas-Grandes

. Molecular detection of Ehrlichia phagocytophila genogrouop organisms in larvae of Neotrombicula autummnalis (Acari: Trombiculidae) captured in Spain. J Parasitol, 2001; 87:11482–11483.

20.

Filippova

. On diagnosis of species of the genus Rhipicephalus Koch (Ixodoidea, Ixodidae) from the fauna of the USSR and adjoining territories by nymphal instat. Parazitol. Sborn, 1981; 30:47–68.

21.

Fuentes

, Galán-Puchades

, Malone

. Short report: A new case report of human Mesocestoides infection in the United States. Am Trop Med Hyg, 2003; 68:566–567.

22.

García.-Sánchez

, Nogal-Ruiz

, Manzano-Lorenzo

, Arroyo-Díaz

, et al. Trichinellosis survey in the wild boar from the Toledo mountains in south western Spain (2007–2008). J Helminthol, 2009; 83:117–120.

23.

Gil-Collado

. Ácaros Ixodoideos de España. Rev San Hig Públ, 1948; 22:389–349.

24.

Gil-Collado

. Insectos y ácaros de los animales domésticos. Salvat Ed. Barcelona, 1961.

25.

Gortázar

, Villafuerte

, Lucientes

, Fernández de Luco

. Habitat related differences in helminth parasites of red foxes in Ebro Valley. Vet Parasitol, 1998; 80:75–81.

26.

Gortázar

, Ferroglio

, Höfle

, Frölich

, et al. Diseases shared between wildlife and livestock: A European perspective. Eur J Wild Res, 2007; 53:241–256.

27.

Hoogstraal

. African Ixodoidea. I. Ticks of the Sudan (with special reference to Equatoria Province and with Preliminary Reviews of the Genera Boophilus, Margaropus and Hyalomma) . Washington, DC: US Navy, 1956:1101.

28.

Hornok

, Fuente

, Horváth

, Fernández de Mera

, et al. Molecular evidence of Ehrlichia canis and Rickettsia massillae in ixodid ticks of carnivores from south Hungary. Acta Vet Hung, 2013; 61:42–50.

29.

Hrčkova

, Miterpáková

, O'Connor

, Šnábel

, et al. Molecular and morphological circumscription of Mesocestoides tapeworms from red foxes (Vulpes vulpes) in central Europe. Parasitology, 2011; 138:638–647.

30.

Jenkins

, Craig

. The role of foxes (Vulpes vulpes) in the epidemiology of Echinococcus granulosus in urban environments. Med J Aust, 1992; 157:754–756.

31.

Kaewmongkol

, Kaewmongkol

, Fleming

, Adams

, et al. Zoonotic Bartonella species in fleas and blood from red foxes in Australia. Vector Borne Zoonotic Dis, 2011; 11:1549–1553.

32.

Krantz

. Manual of Acarology, 2 ^a ed. Corvallis, OR: Oregon State, University Book Stores, 1998:VII.

33.

Kumsa

, Parola

, Raoult

, Socolovschi

. Molecular detection of Rickettsia felis and Bartonella henselae in dog and cat fleas in Central Oromia, Ethiopia. Am J Trop Med Hyg, 2014; 90:457–462.

34.

Lledó

, Gegúndez

, Fernandes

, Sousa

, et al. The seroprevalence of human infection with Rickettsia slovaca, in an area of northern Spain. Ann Trop Med Parasitol, 2006; 100:337–343.

35.

Lledó

, Giménez-Pardo

, Domínguez-Peñafiel

, Sousa

, et al. Molecular detection of Hemoprotozoa and Rickettsiae sp in arthropods from wild animals in the Burgos province, Spain. Vector Borne Zoonotic Dis, 2010; 10:735–738.

36.

López-Olvera

, Vives

, Serrano

, Fernández-Rivera

, et al. Trichinella sp in red foxes (Vulpes vulpes) from Catalonia, NE Spain. Parasitol Res, 2011; 108:1589–1599.

37.

Magi

, Macchioni

, Dell'omodarme

, Prati

, Calderini

, Gabrielli

, Iori

, Cancrini

. Endoparasites of red fox (Vulpes vulpes) in Central Italy. J Wild Dis, 2009; 45:881–885.

38.

Magi

, Guardone

, Prati

, Mignone

, et al. Extraintestinal nematodes of the red fox (Vulpes vulpes) in northwest Italy. J Helminthol, 2014; 11:1–6.

39.

Millán

, Ruiz-Fons

, Márquez

, Viota

, et al. Ectoparasites of the endangered Iberian lynx Lynx pardinus and sympatric wild and domestic carnivores in Spain. Med Vet Entomol, 2007; 21:248–254.

40.

Narasimham

, Panda

, Mohanty

, Sahu

, et al. Dipyllidium caninum infection in a child: A rare case report. Indian J Med Microbiol, 2013; 31:82–84.

41.

Okulewicz

, Hildebrand

, Okulewicz

, Perec

. Red fox (Vulpes vulpes) as reservoir of parasites and source of zoonosis. [in Polish] Wiad Parazytol. 2005; 51:125–132.

42.

Oleaga

, Casais

, Balseiro

, Espí

, et al. New techniques for an old disease: Sarcoptic mange in the Iberian wolf. Vet Parasitol, 2011; 181:255–266.

43.

Papdopoulos

, Himonas

, Papazahariadou

, Antoniadou-Sotiriadou

. Helminths of foxes and other wild carnivores from rural areas in Greece. J Helminthol, 1997; 71:227–231.

44.

Pérez-Martín

, Serrano

, Reina

, Mora

, et al. Sylvatic trichinellosis in southwestern Spain. J Wildl Dis, 2000; 36:531–534.

45.

Pfeiffer

, Kuschfeldt

, Stoye

. Helminth fauna of the red fox (Vulpes vulpes LINNE 1758) in south Sachsen-Anhalt-1 Cestodes. Dtsch Tierarztl Wochenschr, 1997; 104:445–448.

46.

Richards

, Harris

, Lewis

. Epidemiological studies on intestinal helminth parasites of rural and urban red foxes (Vulpes vulpes) in the United Kingdom. Vet Parasitol, 1995; 59:39–51.

47.

Richomme

, Lacour

, Ducrot

, Gilot-Fromont

, et al. Epidemiological survey of trichinellosis in wild boar (Sus scrofa) and fox (Vulpes vulpes) in a French insular region, Corsica. Vet Parasitol, 2010; 172:150–154.

48.

Rioux

, Lanotte

. Leishmania infantum as a cause of cutaneous leishmaniasis. Trans R Soc Trop Med Hyg, 1990; 84:898.

49.

Saeed

, Maddox-Hyttel

, Monrad

, Kapel

. Helminths of red foxes (Vulpes vulpes) in Denmark. Vet Parasitol, 2006; 139:168–179.

50.

Schöeffel

, Schein

, Wittstadt

, Hentsche

. Parasite fauna of red foxes in Berlin (West). Berl Munch Tierartzl Wochenschr, 1991; 104:153–157.

51.

Simón

. Helmitofauna parasitaria de Vulpes vulpes y Genetta genetta en áreas del Oeste de la meseta norte de España. XII Congresso da União Internacional dos Biologistas da Caça, Lisboa Proc, 1975:279–282.

52.

Sobrino

, Ferroglio

, Oleaga

, Romano

, et al. Characterization of widespread canine leishmaniasis among wild carnivores from Spain. Vet Parasitol, 2008; 155:198–203.

53.

Sréter

, Széll

, Varga

. Ectoparasite infestations of red foxes (Vulpes vulpes) in Hungary. Vet Parasitol, 2003; 115:349–354.

54.

Starkof

. Ixodoidea d'Italia. Studio Monográfico. Il Pensiero Scientífico, Roma, 1981:385.

55.

Stekolnikov

, Santibañez

, Palomar

, Oteo

. Neotrombicula inopinata (Acari:Trombiculidae) a possible causative agent of trombiculiasis in Europe. Parasit Vectors, 2014; 3:90.

56.

Szwaja

, Romanski

, Zabazyk

. A case of Dipyllidium caninum infection in a child from the southeastern Polan. Wiad Parazytol, 2011; 57:175–178.

57.

Taylor

, Zitzman

. Dipyllidium caninum in a 4-month old male. Clin Lab Sci, 2011; 24:212–214.

58.

Venturiello

, Nuñez

, Galcgano

, Constantino

. Evalation of three immunoserological techniques in the detection of porcine trichinellosis. Vet Parasitol, 1998; 159:364–367.

59.

Vergles-Rataj

, Posedi

, Zele

, Vengust

. Intestinal parasites of the red fox (Vulpes vulpes) in Slovenia. Acta Vet Hung, 2013; 61:454–462.

60.

Wakernagel

, Schulz

, Deumling

, Linares

, et al. Tracking the ecological overshoot of the human economy. Proc Natl Acad Sci USA, 2002; 99:9266–9271.

61.

Walker

, Keirans

, Horak

. The Genus Rhipicephalus (Acari, Ixodidae): A Guide to the Brown Ticks of the World . Cambridge, UK: Cambridge University Press, 2000.

62.

Zeier

, Handermann

, Bahr

, Rensch

, et al. New ecological aspect of hantavirus infection: A change of paradigm and challenge of prevention. Virus Genes, 2005; 3:157–180.

63.

Zivojinovic

, Sofronic-Milosavljevic

, Cvetkovic

, Pozio

, et al. Trichinella infections in different host species of an endemic district of Serbia. Vet Parasitol, 2013; 192:136–138.