Vulpes vulpes (Linnaeus, 1758)

Duscher, Georg G., Leschnik, Michael, Fuehrer, Hans-Peter & Joachim, Anja, 2015, Wildlife reservoirs for vector-borne canine, feline and zoonotic infections in Austria, International Journal for Parasitology: Parasites and Wildlife 4 (1), pp. 88-96 : 88-91

2.1.1. Red foxes ( Vulpes vulpes )

Foxes obviously play a key role in the interface between wildlife, pets and humans. Reasons for this include the increasing population density of foxes, their susceptibility to relevant pathogens, their hunting preference for small mammals which leads to frequent ingestion of intermediate hosts, and their wide distribution and vicinity to human settlements as a consequence of their

http://dx.doi.org/ 10.1016/j.ijppaw.2014.12.001

synanthropic lifestyle ( Wandeler et al., 2003; Deplazes et al., 2004; Duscher et al., 2005, 2006; Torina et al., 2013). The red fox was the main reservoir for sylvatic rabies in Central Europe, which was very common and a threat to human and animal health before the oral fox vaccination campaign which started in the 1980s in Austria ( Müller et al., 2009). Due to the intensive surveillance and baiting, rabies is now considered eradicated from Austria. However, spillover from neighbouring countries may still occur, and the surveillance system in Austria is still in place. The vaccination against rabies is held responsible for the increasing fox population in Central Europe ( Romig et al., 1999; Chautan et al., 2000; Deplazes et al., 2004; Duscher et al., 2006). Especially in cities such as Zurich ( Switzerland), an increased population of foxes is being reported ( Hofer et al., 2000; Wandeler et al., 2003; Deplazes et al., 2004; Mackenstedt et al., 2014). In Austria we confirmed this trend, albeit at a slower speed ( Duscher et al., 2006). Higher fox densities and closer relationships to human dwellings consequently increase the contact rates among foxes and between foxes, pets and humans ( Romig et al., 1999; Duscher et al., 2006). Therefore the foxes are held responsible for harbouring and transmitting a wide range of vector-borne and zoonotic diseases in Europe, including in Austria.

Most prominent is the occurrence of the small fox tapeworm, Echinococcus multilocularis ( Duscher et al., 2006) . Foxes become infected by ingestion of metacestodes in infected intermediate rodent hosts. The adult worms produce numerous eggs which are shed with the faeces. Foxes tend to use their faeces as marks on elevated positions, e.g. on stones at river banks (Duscher, 2011), supporting the distribution of eggs and the contact with them for the infection of intermediate and accidental hosts such as humans. Around 2–13 cases of human alveolar echinococcosis caused by E. multilocularis are reported annually in Austria ( Schneider et al., 2013), mostly with an unknown geographic source of infection. Prevalences in foxes are around 4% on average with higher rates in the western part ( Duscher et al., 2006). In dogs, prevalences are probably below 0.1% ( Dyachenko et al., 2008), although systematic data for Austria are lacking. Beside their known role as definitive hosts, dogs also can become infected as intermediate hosts due to egg ingestions ( Mätz-Rensing et al., 2002; Weiss et al., 2008); sporadic cases are reported by veterinary practitioners (Anja Joachim, unpublished data).

Another metazoan parasite present in Austrian foxes is Toxocara canis ( Suchentrunk and Sattmann, 1994) : it was found in 42.9% of 307 foxes originating from several regions of Austria. Similar results with 48% of 629 foxes sampled in Lower and Upper Austria were obtained (Georg G. Duscher, unpublished data). This nematode is responsible for human cases of various forms of toxocariasis such as visceral or ocular larva migrans, neurotoxocariasis etc. in humans ( Macpherson, 2013). Reports of human cases in Austria are rare, but a serological study revealed 6.3% of 1046 examined people with previous contact to this roundworm ( Poeppl et al., 2013). Estimations suggest several hundred cases of undiagnosed overt cases per year ( Auer, 2011). In addition, the fox reservoir is also important in maintaining the T. canis population in dogs.

Foxes are also known as carriers of Trichinella britovi in Austria. About 2% of the foxes, mainly with higher prevalences in the alpine region, harboured larvae of this nematode ( Krois et al., 2005). In Europe it is the most prevalent Trichinella species ( Pozio and Zarlenga, 2013). As a consequence of the expanding wild boar population into regions with red foxes, a potential risk is arising due to overlapping habitats of wild boar and infected foxes ( Duscher et al., 2005). Scavenging on infected dead foxes by wild boar may consequently lead to human infections by consumption of undercooked wild boar meat; however, so far no case of human Trichinella infection from this source has been reported from Austria. Reasons therefore are various such as overlooked cases, the disability to identify the origin of infection, traditional dining habitats of inhabitants or even negligible risk. But the risk of Trichinella infections from wild boar was discussed after findings of larvae and some seropositive animals in a fenced area ( Edelhofer et al., 1984). This finding was later revised because no muscle larvae were found and further evidence from other animals was lacking, and it was assumed that the positive case was introduced from Russia.Cross-reactivity was assumed for the serologically positive cases ( Edelhofer et al., 1996). Human Trichinella infections have been recorded in Austria but are usually considered to be imported ( Auer, 2005). Nevertheless, based on several changes in the recent past such as the increasing of fox population ( Duscher et al., 2006) and of overlapping areas of foxes with wild boars ( Duscher et al., 2005), together with changing the cooking habits to raw or undercooked meals, transmission of Trichinella is favoured.

A similar route via wild boar meat could be taken by the trematode Alaria alata (Duscher, 2011) . Foxes harbour the adult stages of this helminth. The eggs develop in the water and infect snails as first intermediate hosts, followed by amphibians as second intermediate hosts. Several animals such as snakes and wild boar are discussed as paratenic hosts ( Möhl et al., 2009). By ingestion of the metacercariae, the natural definitive host, the fox, becomes infected and the life cycle is completed. A fatal human case was reported in relation to an infection with a closely related species, A. americanum ( Freeman et al., 1976) ; human infections in Austria have not been recorded so far. Similar to Trichinella , drawing conclusions about actual risk is almost impossible due to the lack of reliable diagnostic tools in humans and integral data of this parasite in definitive, paratenic and intermediate hosts. But in this case undercooked wild boar represents a potential treat of this zoonosis.

Foxes might also act as carriers of vector-borne zoonotic Dirofilaria spp. ( Lok, 1988). Mosquitoes transmit these filaroids among canids and to felids ( McCall et al., 2008). Beside cutaneous lesions induced by Dirofilaria repens , a cardio-pulmonary manifestation evoked by Dirofilaria immitis is known to occur in Austria, with the latter only as imported cases so far ( Duscher et al., 2009; Silbermayr et al., 2014). Both species are responsible for human diseases, usually with cutaneous and ocular locations due to D. repens and pulmonary lesions due to D. immitis ( Simón et al., 2009) . In Austria imported infections with both species have been documented in dogs and humans. However, in both dogs and humans some cases have been determined as autochthonous ( Auer and Susani, 2008). D. repens was found in mosquitoes in Austria for the first time in 2012, and can now be considered as endemic in Austria, presumably invaded from the eastern neighbouring countries ( Silbermayr et al., 2014).

Foxes are also carriers of tick-transmitted protozoa such as Babesia microti -like pathogens, also known as Babesia annae , Theileria annae or “ Babesia sp. from Spanish dog” ( Criado-Fornelio et al., 2003). Those piroplasmids are known to cause diseases in dogs with azotaemia, haemolytic anaemia, renal failure and mortality ( Camacho et al., 2004, 2005). In Austria 50% of 36 foxes were positive for this pathogen ( Duscher et al., 2014). The vector ticks are thought to be Ixodes hexagonus ( Camacho et al., 2003) as well as I. ricinus and Ixodes canisuga ( Najm et al., 2014a) . Their zoonotic potential is not known. Further studies are required to define the complete intermediate and final host range of B. microti -like pathogens.

Foxes also harbour another apicomplexan, Hepatozoon canis . This tick-transmitted pathogen, unlike any other, needs to be ingested by the vertebrate host ( Baneth et al., 2003). Generally this happens during grooming or by ingestion of ticks on prey. Similar to H. americanum , vertical transmission from bitches to their progeny has been described ( Murata et al., 1993), and transmission via infected prey tissue, e.g. rodents containing meronts, is also discussed ( Johnson et al., 2009; Hornok et al., 2013). The zoonotic potential of this pathogen seems to be negligible. The main vector tick of H. canis , R. sanguineus , is not considered endemic in Austria ( Estrada-Peña et al., 2012), although sporadically, imported ticks can be found ( Prosl and Kutzer, 1986; Duscher and Leschnik, 2011). Nevertheless, H. canis is reported from areas where the main vector tick is also missing, e.g. Germany or Hungary ( Gärtner et al., 2008; Farkas et al., 2014; Najm et al., 2014b). In Austria about 58% of 36 foxes in eastern areas were positive for this pathogen ( Duscher et al., 2014). Other tick species that are endemic in these countries as well as in Austria, such as Dermacentor or Haemaphysalis species, might also act as vectors, as suggested for Haemaphysalis longicornis and Haemaphysalis flava in Japan and Amblyomma ovale and Rhipicephalus microplus in Brazil ( de Miranda et al., 2011; Otranto et al., 2011; Hornok et al., 2013). Recent studies found I. ricinus to be unsuitable as vector ( Giannelli et al., 2013). Similar to B. microti -like pathogens, transmission by competent ixodid vectors still has to be confirmed in further studies. Interestingly, sporadic imported cases, but neither endemic B. microti -like infections nor H. canis cases, could so far be diagnosed in dogs from Austria. As diagnosis of H. canis in the patent phase is easily made by microscopic detection of large gamonts formed in white blood cells of dogs, it appears highly unlikely that this infection has been overlooked in dogs in the past. It is currently unknown why this infection circulates in foxes but not in dogs, as both can frequently be infested with ticks of the same genera and species ( Duscher et al., 2013a).

Foxes and other wild carnivores might also play a role in the maintenance of a sylvatic cycle of Toxoplasma gondii infection ( Karbowiak et al., 2010) as 35% of Austrian foxes tested positive by serology ( Wanha et al., 2005); however, systematic data on the sylvatic and domestic cycles, e.g. in peri-urban areas, are missing.