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Wildlife Ecology Elective 2009


Potential of Irish Red Foxes (Vulpes vulpes) to act as an agent of zoonotic diseases

By Fiona BB Dolan

Introduction
The red fox (Vulpes vulpes) is a member of the Canidae family and is found throughout Europe and worldwide. They have a broad based diet due to their nature to scavenge and are also at the top of the wildlife food chain. As a result they are the mostly likely animal to consume any and all pollutants and diseases in their environment, thus they are also the reservoir of many helminth and protozoal parasites. Unfortunately many of these parasites are pathogenic to humans.
The risk of contracting infection from foxes is of growing concern in Ireland due to their increasing presence in urban areas. They are attracted by the abundance of food, which they scavenge from waste or source easily from people deliberately leaving out food. Also, the healthy interest people are showing for hill walking and other such country based activities brings them into the habitat of the fox and increases the risks of contracting an infection.
Here, I will examine the potential pathogens and the extent of the risk of their transmission to humans. One study, briefly examined the risk of transmission of bacterial infection, by investigating the presence of the bacteria in the faeces (Nagano, Y., et al., 2006), but I will focus on the parasitic pathogens. The parasites perceived to be of greatest importance including Toxoplasma gondii, Neospora caninum, Cryptosporidium spp., were evaluated from the samples of foxes euthanized for the various investigations.

 

Data analysis
Bacteria
In the 2006 published study by Nagano et al., they examined fox faeces samples for the most important zoonotic bacterial pathogens, i.e. Salmonella spp., Shigella spp., Campylobacter spp., Yersinia enterocolitica and E. Coli O157:H7. Out of the 124 faecal samples, all were negative for the latter mentioned bacteria.
Parasites
Protozoans
The apicomplexa protozoa Toxoplasma gondii and Neospora caninum and the microsporidia protozoa, Encephalitozoon cuniculi and Encephalitozoon intestinalis have been closely scruntizied as important transmissible zoonosis from foxes. Murphy, et al., found that T. gondii is more prevalent that N. caninum; out of the 345 animals examined, the prevalence of T. gondii was recorded to be 55.8% and N. caninum, 2.7%. In an earlier study of ‘urban’ foxes, i.e. foxes in and around the Dublin area, it was established that 47% had antibodies against T. gondii, but only 1 out of 70 tested was positive for N. caninum (Wolfe, et al., 2001). Neosporosis is an important disease in domestic mammals such as dogs, cattle and horses. The epidemiology is not clear and the role of wild carnivores, such as foxes, has yet to be determined. Further research is required to determine the zoonotic character of N. caninum – certainly some people are at more risk than others – such as farmers and their families.
The results of Encephalitozoon study indicates that the species is widely distributed in the environment and it is thought to be excreted through the urine of foxes. E. intestinalis infection is the second most significant infection in immune-suppressed patients in Ireland. The epidemiology of the human infection remains to be clarified; therefore the role of the fox is uncertain.
Cryptosporidia spp., another apicomplexa protozoan, has also had its prevalence in Irish foxes examined. Gastrointestinal diseases caused by Cryptosporidia spp in humans have been reported in over 40 countries worldwide; therefore it is now considered an important parasitic pathogen. Again the epidemiology is unclear but it is important to investigate the role foxes may play. Although only 124 samples were available for examination, they were from 19 out of the 26 counties of the Republic of Ireland. The results suggest a very small presence (1.6%) of Cryptosporidia spp, mainly C. parvum, in Irish foxes (Nagano et al., 2006).
Helminths
Trematodes
The prevalence of Alaria alata was investigated in two ways, presence as a helminth and as an egg in faecal samples of 77 red foxes. It is one of the most prevalent intestinal helminths of Irish foxes, after Uncinaria stenocephala and Toxocara canis, at 27.3% and 10.1% of the 77 samples respectively (Wolfe, et al., 2001). After comparison of two detection methods, intestinal washing and faecal flotation, it was observed that the faecal flotation method under-estimated the presence of A. alata by 71.4%. The life cycle of A. alata is complex, involving frogs and snails as intermediate hosts. The final hosts are carnivores, however small rodents and other animals which feed on frogs can become paratenic hosts. Carnivores can contract the trematode from intermediate or paratenic hosts. In humans, A. alata causes respiratory problems or ocular lesions after ingestion of under-cooked frog legs or wild goose meat respectively. Humans may also act as a paratenic host.
Nematodes
The two most prevalent nematode species in Irish foxes are Uncinaria stenocephala and Toxocara canis (Wolfe et al., 2001). U. stenocephala is a hookworm and the most prevalent (92.2%) among the urban foxes examined in the study. The eggs of U. stenocephala were also the most abundant (67.1%). However this helminth is not at the forefront of zoonosis concerns, Toxocara canis findings were much more significant. 37.7% of the 77 foxes tested carried T. canis, with 26.6% having eggs of the species. A comparative study of intestinal washes and faecal flotation showed an underestimation of 31%. Human toxocarosis, especially in children, is linked with dog ownership, especially breeding bitches, but foxes are also involved in the epidemiology. There is a risk from both direct and indirect infection. Direct infection from soil contaminated by eggs or indirectly from dogs (who have been contaminated by foxes). As mentioned earlier, human activity and urban foraging of foxes increases the risk of transmission. The morphology and genetics of T. canis in dogs and foxes is identical.
Another common nematode of foxes is Capillaria aerophila, which is present in the respiratory tract. Capillaria eggs were found during faecal flotation examinations of Irish foxes in and around the Dublin area. They were the second most common species identified at 36.7%, after U. stenocephala (Wolfe et al, 2001). However Wolfe et al., suspected that the prevalence of this species in foxes is actually probably twice as high and further study is necessary.


Conclusion
Currently there is no evidence of a real threat to Irish citizens from the red fox. The results do indicate that further study and monitoring of foxes in Ireland is necessary. In order to accurately ascertain the zoonotic potential of red foxes more precise data on the prevalence of each parasitic pathogen in the fox will need to be gained. It will also be necessary to tract their movements and the movements of humans and where and how they overlap. This should identify the source of infection and methods of transmission. Perhaps the cycle will be possible to break and if not, the source of infection or method of transmission could be monitored and controlled.


References
Murphy, T. M., Walochnik, J., Hassl, A., Moriarty, J., Mooney, J., Toolan, D., Sanchez-Miguel, C., O’Loughlin, A., McAuliffe, A., 2007. Study on the prevalence of Toxoplasma gondii and Neospora caninum and molecular evidence of Encephalitozoon (Septata) intestinalis infections in red foxes (Vulpes vulpes) in rural Ireland. Veterinary Parasitology 146 (2007), 227-234.
Nagano, Y., Finn, M.B., Lowery, C.J., Murphy T., Moriarty, J., Power, E., Toolan, D., O’Loughlin, A., Watabe, M., McCorry K.A., Crothers, E., Dooley, J.S.G., Rao, J.R., Rooney, P.J., Millar, B.C., Matsuda, M., Elborn, J.S., Moore, J.E., 2006. Occurence of Crptosporidium parvum and bacterial pathogens in faecal material in the Red Fox (Vulpes vulpes) population. Veterinary Research Communications, Vol. 31, No.5, 559-564.
Wolfe, A., Hogan, S., Maguire, D., Fitzpatrick, C., Vaughan, L., Wall, D., Hayden, T.J., Mulcahy, G., 2001. Red foxes (Vulpes vulpes) in Ireland as hosts for parasites of potential zoonotic and veterinary significance. Veterinary Record 149, 759-763.

 

 
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