Parasites with possible zoonotic potential in the small intestines of red foxes (Vulpes vulpes) from Northwest Bohemia (CzR)

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Summary

We determined the prevalence of primarily zoonotic parasites in the small intestines of 40 (20 males and 20 females) red foxes living near human dwellings. The total prevalence of parasite infection was 77.5 % (31/40); the prevalence was 37.5 % (15/40) for Toxocara canis and 35 % (14/40) for Toxascaris leonina. The mean intensity infection was 3 and 11 helminths for T. canis and T. leonina, respectively. The prevalence of other intestinal helminths and mean infection intensity in this study are given: Echinococcus multilocularis 40 % (16/40) with 1000 individuals, Mesocestoides spp. 40 % (16/40) with 8 individuals, Uncinaria stenocephala 10 % (4/40) with 8 individuals, and Taenia pisiformis 10 % (4/40) with 1 individual. With regards to prevalence and intensity of infection, as well as prevalence of individual parasites, there were no significant differences (P≥0.05) between male and female red foxes.

Summary

We determined the prevalence of primarily zoonotic parasites in the small intestines of 40 (20 males and 20 females) red foxes living near human dwellings. The total prevalence of parasite infection was 77.5 % (31/40); the prevalence was 37.5 % (15/40) for Toxocara canis and 35 % (14/40) for Toxascaris leonina. The mean intensity infection was 3 and 11 helminths for T. canis and T. leonina, respectively. The prevalence of other intestinal helminths and mean infection intensity in this study are given: Echinococcus multilocularis 40 % (16/40) with 1000 individuals, Mesocestoides spp. 40 % (16/40) with 8 individuals, Uncinaria stenocephala 10 % (4/40) with 8 individuals, and Taenia pisiformis 10 % (4/40) with 1 individual. With regards to prevalence and intensity of infection, as well as prevalence of individual parasites, there were no significant differences (P≥0.05) between male and female red foxes.

Introduction

The red fox (Vulpes vulpes) is a representative of the canid family. It is widely distributed in the Northern Hemisphere, and it is the most abundant wild carnivore living in the territory of the Czech Republic. Annual captures in the Czech Republic currently range between 60 000 – 80 000, and populations continue to grow (Placata, 2011). The increase in the distribution and density of the red fox in most European countries could be explained by a mortality rate reduction, which is due to an intensive campaigns of vaccination against rabies (oral baits) as well as to the opportunist behaviour of this species (Hanosset et al., 2008; Červený et al., 2004). The red fox is a common host of several dangerous zoonotic parasites, primarily the tapeworm Echinococcus multilocularis, causative agent of alveolar echinococcosis, a parasitic disease that causes a severe hepatic disorder in humans (Letková et al., 2006). Soil contaminated with red fox feces is a significant risk factor for zoonotic disease infection. Endoparasites (primarily Echinococcus multilocularis and Toxocara canis, but also Uncinaria stenocephala, Mesocestoides spp. and Taenia spp. tapeworms) or ectoparasites, such as fleas, ticks and mites (Kočišová et al., 2006) of red foxes, can cause numerous health problems in humans and domesticated animals (mainly dogs).

Zoonotic roundworms (mainly T. canis) are not only present in their definitive hosts but also frequently occur in other animal species (Reiterová et al., 2013), including humans. In these paratenic hosts, larvae do not develop into the adult stage, but rather migrate throughout the tissues and remain there as L3 arrested larvae for an extended period of time (Strube et al., 2013).

Foxes live in close proximity to humans and domestic dogs, and this may have significant implications for public health. The aim of this study was to investigate the prevalence of zoonotic parasites in the small intestines of red foxes living near human dwellings.

Material and Methods

Forty (20 males and 20 females) red foxes were collected from an area surrounding the city of Karlovy Vary, in the northwest region of the Czech Republic (between October 2010 and March 2012). The study area covered approximately 6 km2 with a fox density of 0.9-6 foxes/1km2/year; average animal body weight was 5.5 kg (from 2.96 to 8.32 kg).

During necropsy, the small intestine was isolated and wrapped in plastic bags and frozen at -80°C until examination (app. one month) in order to inactivate the infective material. In order to detect intestinal helminths, a direct detection method was implemented using intestinal scraping or sedimentation techniques (ITS) (Tackmann et al., 2006).

Helminths were identified according to size and morphology using two microscopes: an Olympus CX 21 and an Olympus BX21.

Statistical evaluation

Basic descriptive statistics were computed. The normality of the data was tested separately using a Shapiro-Wilks test. Considering the results of the normality test, a nonparametric Mann-Whitney U test was used to evaluate differences between males and females. Statistica ver. 12 (Statsoft, 2013) was used for all statistical analyses.

Results and Discussion

Parasitic contamination of urban and rural environments by Canidae excrements is a growing problem (Ondriska et al., 2013; Papajová et al., 2014). The presence of red fox feces in the soil of urban and suburban areas can threaten the health of animals and humans, mainly due to the presence of zoonotic parasite eggs (primarily Echinococcus multilocularis and Toxocara canis). We examinated the gastrointestinal tracts of 40 red foxes from the above-mentioned monitored area and found 77.5 % (31/40) of them to be infected by intestinal helminths. There were no statistically significant differences (P≥0.05) between male and female red foxes with respect to prevalence and intensity of infection and prevalence of individual parasites. The prevalence of intestinal helminths and their mean intensity is presented in Table 1.

Table 1

Intestinal helminth prevalence and mean infection intensity in monitored red foxes

SpeciesPrevalence (%)Mean intensity of infection (min – max)
Echinococcus multilocularis40 (16/40)1000 (32 – 3500)
Mesocestoides spp.40 (16/40)8 (4 – 123)
Taenia pisiformis10 (4/40)1 (1)
Toxascaris leonina35 (14/40)11 (1 – 96)
Toxocara canis37.5 (15/40)3 (1 – 24)
Uncinaria stenocephala10 (4/40)8 (1 – 12)

Toxocariasis is a soil-transmitted helminthozoonosis, which is caused by Toxocara spp larvae infection in humans. Human infection is acquired through the ingestion of embryonated Toxocara eggs (eggs reach the environment via canid or felid stools and become infectious for humans and other hosts over the course of a few weeks). Dubná et al. (2007a) reported an 11.90 % prevalence of Toxocara eggs in 126 composite samples taken from child sandpits in Prague (Czech Republic). In paratenic hosts, such as humans and mice, hatched larvae migrate systematically throughout the body and have the ability to reach critical sites such as the eyes and central nervous system. Larvae of Toxascaris leonina can also invade the tissues of laboratory animals, and this species has the potential to cause human disease. Of the 42.5 % (17/40) of red foxes infected by roundworms (T. canis and/or T. leonina), 70.59 % (12/17) of them were infected simultaneously by both T. leonina and T. canis. Two of the red foxes (11.76 %) were infected with only T. leonina whereas three (17.65 %) were infected with only T. canis. The total prevalence of roundworms was 37.5 % (15/40) and 35 % (14/40) for Toxocara canis and Toxascaris leonina respectively. Letková et al. (2006) reported a 17.55 % prevalence of T. leonina and a 25.82 % prevalence of T. canis in red foxes (V .vulpes) from eastern Slovakia. Reperant et al. (2007) reported a lower prevalence of T. leonina in urban areas (8 %) in comparison to that of rural areas (59.6 %). This raises the question of whether rodent paratenic hosts play a major role in population dynamics of this species. Reiterová et al. (2013) reported anti-Toxocara antibodies in 6.6 % of small rodents trapped in Slovakia. Research carried out by Reperant et al. (2007) in Switzerland showed that as many as 59.6 % of foxes from rural areas were infected with T. leonina as opposed to only 8 % in urban areas. Reperant et al. (2007) found that T. canis and T. leonina co-occured in 14 % of the red fox population of Geneva, Switzerland. In our study, infection intensity ranged from 1 – 96 roundworms (Toxocara spp. and T. leonina) per fox. The co-occurence of Toxocara spp. and T. leonina in the definitive host is highly variable and is dependent on several factors: climate, environmental conditions, seasonal period and host age. This applies to infected wildlife as well as domestic animals (Okulewicz et al., 2012). Antolová et al. (2004) reported a 47.1 % prevalence of T. leonina and an 8.1 % prevalence of T. canis in red foxes from the Slovak Republic. Borecka et al. (2009) and Balicka-Ramisz et al. (2003) determined a 19.1 % and 39.8 % prevalence of T. canis in red foxes from Central and Western Poland respectively; they also determined a 0.0 % and 0.9 % prevalence of T. leonina in red foxes from Central and Western Poland respectively. Dubná et al. (2007b) monitored the prevalence of intestinal parasites in dogs from metropolitan Prague, rural areas surrounding Prague, and dog shelters in the Czech Republic; they reported T. canis in 6.2 % and 2.0 % of dogs in Prague and rural areas respectively; T. leonina was observed in 0.9 % and 1.7 % of canine faecal samples in metropolitan Prague and rural areas respectively.

In our study, we also observed the hookworm Uncinaria stenocephala, however, only 10 % (4/40) of foxes were infected with this helminth, with a mean infection intensity of 8 hookworms (Table 1). Uncinaria stenocephala is a nematode that belongs to the Ancylostomatidae family. Members of this family infect millions of people and animals worldwide. U. stenocephala is most pathogenic in dogs and other Canidae, which serve as the main hosts, and infection causes anemia or even death (Wasyl et al., 2013). Rataj et al. (2013) reported Uncinaria stenocephala as the most frequently identified nematodes in red foxes from Slovenia. Mesocestoides spp. are zoonotic cestodes of wild and domesticated carnivores. Although the adult tapeworms are relatively harmless intestinal parasites, the metacestode stages (tetrathyridia) can cause life-threatening peritonitis and pleuritis in several species including dogs, cats, non-human primates and, most likely, humans (Széll et al., 2015). In our study, Mesocestoides spp. tapeworms were found in 40 % (16/40) of red foxes, with a mean infection intensity of 8 individuals (table 1). Széll et al. (2015) reported a similar prevalence of Mesocestoides spp. tapeworms in red foxes from Hungary (45.8 %).

Our study also revealed the presence of Taenia pisiformis (in 10 % 4/40 of red foxes), with a mean infection intensity of 1 individual (Table 1). The natural life cycle of Taenia pisiformis includes canines as normal definitive hosts and lagomorphs as typical intermediate hosts. Cysticercus pisiformis, the larval stage of T. pisiformis, can bring about economic impacts in rabbit breeding and cause serious health problems to the host, including liver lesions, digestive disorders, growth retardation, weight loss, and even death (Rajasekariah et al., 1985). Rataj et al. (2013) reported a 2.1 % prevalence of Taenia pisiformis in red foxes from Slovenia. Our study revealed a 40 % (16/40) prevalence of Echinococcus multilocularis - the most dangerous zoonotic parasite for man - with a mean infection intensity of 1000 individuals (Table 1). Alveolar echinococcosis is a rare human disease that is often lethal if left untreated (Szilágyiová et al., 2015). It is caused by Echinococcus multilocularis at the larval stage. In Central Europe, the main definitive host of E. multilocularis is red fox. Red foxes from our monitored region (Northwest Bohemia) can wander into areas populated by humans, dogs and other domesticated animals, and can pose a significant threat to these inhabitants.

Conclusion

The tapeworm Echinococcus multilocularis and roundworm Toxocara canis, which possess severe zoonotic potential, were observed in red foxes from the monitored area. For this reason, these individuals were treated monthly with anthelmintic bait (50 bait pieces/km2) for an entire year following the study.

Acknowledgements

This study was supported by the Czech University of Life Sciences – University-wide internal grant agency (CIGA) project No. 20142053. We would also like to thank Mr. Brian Kavalir for his proofreading services.

The authors declare no conflicts of interest.

References

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  • Balicka-Ramisz A., Ramisz A., Pilarczyk B. Bienko R. (2003): Fauna of gastro-intestinal parasites in red foxes in Western Poland. Med. Wet., 59(10): 922 – 925

  • Bochert, A. (1954): Lehrbuch der Parasitologie für Tierärzte. S. Hirzel Verlag Leipzig. 448 pp.

  • Borecka, A., Gawor, J., Malczewska, M., Malczewski, A. (2009): Prevalence of zoonotic helminth parasite sof the small intestine in red foxes from central Poland. Med. Wet., 65(1): 33 – 35

  • Brochier, B., De Blander, H., Hanosset, R., Berkvens, Q., Losson, B., Saegerman, C. (2007): Echinococcus multilocularis and Toxocara canis in urban red fox (Vulpes vulpes) in Brussels, Belgium. Prevent. Vet. Med., 80: 65 – 73. DOI:

  • Červený, J., Kamler, K., Kholová, H., Koubek, P., Martínková, M. (2004) Hunting encyclopedy. Ottovo nakladatelství-Cesty, Praha, pp 591 (In Czech)

  • Dubná, S., Langrová, I., Jankovská, I., Vadlejch, J., Pekár, S., Nápravník, J., Fechtner, J. (2007a): Contamination of soil with Toxocara eggs in urban (Prague) ans rural areas in the Czech Republic. Vet. Parasitol., 144(1 – 2): 81 – 86. DOI:

  • Dubná, S., Langrová, I., Nápravník, J., Jankovská, I., Vadlejch, J., Pekár, S., Fechtner, J. (2007b): The prevalence of intestinal parasites in dogs from Prague, rural areas, and shelters of the Czech Republic. Vet. Parasitol., 145: 120 – 128. DOI:

  • Fillaux, A., Magnaval, A. (2013): Laboratory dianosis of human toxocariasis. Vet. Parasitol., 193: 327 – 336. DOI:

  • Hanosset, R., Saegerman, C., Adant, S., Massart, L., Losson, B. (2008): Echinococcus multilocularis in Belgium: prevalence in red foxes (Vulpes vulpes) and in different species of potential intermediate hosts. Vet. Parasitol., 151: 212 – 217. DOI:

  • Kočišová, A., Lazar, P., Letková, V., Čurlík, J., Goldová, M. (2006): Ectoparasitic species from red foxes (Vulpes vulpes) in East Slovakia. Vet. Arhiv, 76(SUPPL.): S59 – S63

  • Letková, V., Lazar, P., Čurlík, J., Goldová, M., Kočišová, A., Košuthová, L., Mojžišová, J. (2006): The red fox (Vulpes vulpes L.) as a source of zoonoses. Vet. Arhiv, 76(SUPPL.): S73 – S81

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  • Okulewicz, A., Perec-Matysiak, A., Bunkowska, K., Hildebrand, J. (2012): Toxocara canis, Toxocara cati and Toxascaris leonina in wild and domestic carnivores. Helminthologia 49(1): 3 – 10. DOI:

  • Ondriska, F., Mačuhová, K., Melicherová, J., Reiterová, K., Valentová, D., Beladičová, V., Halgoš, J. (2013) Toxocariasis in urban environment of western Slovakia. Helminthologia, 50(4): 261 – 268, 2013

  • Papajová, I., Pipiková, J., Papaj, J., Čižmár, A. (2014) Parasitic contamination of urban and rural environments in the Slovak Republic: dog's excrements as a source. Helminthologia, 51(4):273 – 280. DOI:

  • Placata, J. (2011): Overpopulations of foxes – a contributing factor to the decline in small game numbers. Myslivost, 11: 82 Retrieved from www.myslivost.cz (In Czech)

  • Rajasekariah, G.R., Rickard, O'donnell I.J. (1985): Taenia pisiformis: protective immunization of rabbits with solubilized oncospheral antigens. Exp. Parasitol., 59: 321 – 327

  • Rataj, A.V., Posedi, J., Zele, D., Vengust, G. (2013): Intestinal Parasites of the red fox (Vulpes vulpes) in Slovenia. Acta Vet. Hung., 61(4): 454 – 462. DOI:

  • Reiterová, K., Antolová, D., Zalesny, G., Stanko, M., Špilovská, S., Mošanský, L. (2013): Small rodents – permanent reservoirs of toxocarosis in different habitat sof Slovakia. Helminthologia, 50(1): 20 – 26. DOI:

  • Reperant, L.A., Hegglin, D., Fischer, C., Kohler, L., Weber, M., Deplazes, P. (2007): Influence of urbanization on the epidemiology of intestinal helminths of the red fox (Vulpes vulpes) in Geneva, Switzerland. Parasitol. Res., 101: 605 – 611. DOI:

  • Strube, C., Heuer, L., Janecek, E. (2013): Toxocara spp. infection in paratenic hosts. Vet. Parasitol., 193: 375 – 389. DOI:

  • Széll, Z., Tolnai, Z., Sréter, T. (2015): Environmental determinants of the spatial distribution of Mesocestoides spp. and sensitivity of flotation method for the diagnosis of mesocestoidosis. Vet. Parasitol., 212: 427 – 430. DOI:

  • Szilágyiová, M., Laca, L., Antolová, D., Nováková, E., Rosolanka, R., Reiterová, K., Šimeková, K. (2015): Importance of complex diagnostic approach in differential diagnosis of alveolar echinococcosis. Helminthologia, 52(4):298 – 302. DOI:

  • Tackmann, K., Mattis, R., Conraths, F.J. (2006): Detection of Echinococcus multilocularis in foxes: evaluation of a protocol of the intestinal scraping technique. J. Vet. Med. B. Infect. Dis. Vet. Public Health., 53(8): 395 – 398

  • Wasyl, K., Zawistowska-Deniziak, A., Bąska, P., Wędrychowicz, H., Wiśniewski, M. (2013): Molecular cloning and expression of the cDNA sequence encoding a novel aspartic protease from Uncinaria stenocephala. Exp. Parasitol., 134(2): 220 – 227

Antolová, D., Reiterová, K., Miterpáková, M., Stanko, M., Dubinský, P. (2004): Circulation of Toxocara spp. in suburban and rural ecosystems in the Slovak Republic. Vet. Parasitol., 126(3): 317 – 324. DOI:

Balicka-Ramisz A., Ramisz A., Pilarczyk B. Bienko R. (2003): Fauna of gastro-intestinal parasites in red foxes in Western Poland. Med. Wet., 59(10): 922 – 925

Bochert, A. (1954): Lehrbuch der Parasitologie für Tierärzte. S. Hirzel Verlag Leipzig. 448 pp.

Borecka, A., Gawor, J., Malczewska, M., Malczewski, A. (2009): Prevalence of zoonotic helminth parasite sof the small intestine in red foxes from central Poland. Med. Wet., 65(1): 33 – 35

Brochier, B., De Blander, H., Hanosset, R., Berkvens, Q., Losson, B., Saegerman, C. (2007): Echinococcus multilocularis and Toxocara canis in urban red fox (Vulpes vulpes) in Brussels, Belgium. Prevent. Vet. Med., 80: 65 – 73. DOI:

Červený, J., Kamler, K., Kholová, H., Koubek, P., Martínková, M. (2004) Hunting encyclopedy. Ottovo nakladatelství-Cesty, Praha, pp 591 (In Czech)

Dubná, S., Langrová, I., Jankovská, I., Vadlejch, J., Pekár, S., Nápravník, J., Fechtner, J. (2007a): Contamination of soil with Toxocara eggs in urban (Prague) ans rural areas in the Czech Republic. Vet. Parasitol., 144(1 – 2): 81 – 86. DOI:

Dubná, S., Langrová, I., Nápravník, J., Jankovská, I., Vadlejch, J., Pekár, S., Fechtner, J. (2007b): The prevalence of intestinal parasites in dogs from Prague, rural areas, and shelters of the Czech Republic. Vet. Parasitol., 145: 120 – 128. DOI:

Fillaux, A., Magnaval, A. (2013): Laboratory dianosis of human toxocariasis. Vet. Parasitol., 193: 327 – 336. DOI:

Hanosset, R., Saegerman, C., Adant, S., Massart, L., Losson, B. (2008): Echinococcus multilocularis in Belgium: prevalence in red foxes (Vulpes vulpes) and in different species of potential intermediate hosts. Vet. Parasitol., 151: 212 – 217. DOI:

Kočišová, A., Lazar, P., Letková, V., Čurlík, J., Goldová, M. (2006): Ectoparasitic species from red foxes (Vulpes vulpes) in East Slovakia. Vet. Arhiv, 76(SUPPL.): S59 – S63

Letková, V., Lazar, P., Čurlík, J., Goldová, M., Kočišová, A., Košuthová, L., Mojžišová, J. (2006): The red fox (Vulpes vulpes L.) as a source of zoonoses. Vet. Arhiv, 76(SUPPL.): S73 – S81

Nolan, T. (2008): Lab 3 Appendix: Ascarids, Oxyurids and Trichocephalids. University of Pennsylvania School of Veterinary Medicine. Computer Alded Learning.

Okulewicz, A., Perec-Matysiak, A., Bunkowska, K., Hildebrand, J. (2012): Toxocara canis, Toxocara cati and Toxascaris leonina in wild and domestic carnivores. Helminthologia 49(1): 3 – 10. DOI:

Ondriska, F., Mačuhová, K., Melicherová, J., Reiterová, K., Valentová, D., Beladičová, V., Halgoš, J. (2013) Toxocariasis in urban environment of western Slovakia. Helminthologia, 50(4): 261 – 268, 2013

Papajová, I., Pipiková, J., Papaj, J., Čižmár, A. (2014) Parasitic contamination of urban and rural environments in the Slovak Republic: dog's excrements as a source. Helminthologia, 51(4):273 – 280. DOI:

Placata, J. (2011): Overpopulations of foxes – a contributing factor to the decline in small game numbers. Myslivost, 11: 82 Retrieved from www.myslivost.cz (In Czech)

Rajasekariah, G.R., Rickard, O'donnell I.J. (1985): Taenia pisiformis: protective immunization of rabbits with solubilized oncospheral antigens. Exp. Parasitol., 59: 321 – 327

Rataj, A.V., Posedi, J., Zele, D., Vengust, G. (2013): Intestinal Parasites of the red fox (Vulpes vulpes) in Slovenia. Acta Vet. Hung., 61(4): 454 – 462. DOI:

Reiterová, K., Antolová, D., Zalesny, G., Stanko, M., Špilovská, S., Mošanský, L. (2013): Small rodents – permanent reservoirs of toxocarosis in different habitat sof Slovakia. Helminthologia, 50(1): 20 – 26. DOI:

Reperant, L.A., Hegglin, D., Fischer, C., Kohler, L., Weber, M., Deplazes, P. (2007): Influence of urbanization on the epidemiology of intestinal helminths of the red fox (Vulpes vulpes) in Geneva, Switzerland. Parasitol. Res., 101: 605 – 611. DOI:

Strube, C., Heuer, L., Janecek, E. (2013): Toxocara spp. infection in paratenic hosts. Vet. Parasitol., 193: 375 – 389. DOI:

Széll, Z., Tolnai, Z., Sréter, T. (2015): Environmental determinants of the spatial distribution of Mesocestoides spp. and sensitivity of flotation method for the diagnosis of mesocestoidosis. Vet. Parasitol., 212: 427 – 430. DOI:

Szilágyiová, M., Laca, L., Antolová, D., Nováková, E., Rosolanka, R., Reiterová, K., Šimeková, K. (2015): Importance of complex diagnostic approach in differential diagnosis of alveolar echinococcosis. Helminthologia, 52(4):298 – 302. DOI:

Tackmann, K., Mattis, R., Conraths, F.J. (2006): Detection of Echinococcus multilocularis in foxes: evaluation of a protocol of the intestinal scraping technique. J. Vet. Med. B. Infect. Dis. Vet. Public Health., 53(8): 395 – 398

Wasyl, K., Zawistowska-Deniziak, A., Bąska, P., Wędrychowicz, H., Wiśniewski, M. (2013): Molecular cloning and expression of the cDNA sequence encoding a novel aspartic protease from Uncinaria stenocephala. Exp. Parasitol., 134(2): 220 – 227

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