Short Communications
Giardia and Cryptosporidium in red foxes (Vulpes vulpes): Screening for coproantigens in a population of central Italy and mini-review of the literature
Roberto Amerigo Papini * ,
Ranieri Verin

Mac Vet Rev 2019; 42 (1): 101 - 106

10.2478/macvetrev-2019-0013

Received: 16 April 2018

Received in revised form: 27 November 2018

Accepted: 29 January 2019

Available Online First: 17 February 2019

Published on: 15 March 2019

Correspondence: Roberto Amerigo Papini, roberto.amerigo.papini@unipi.it
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Abstract

Giardia and Cryptosporidium are common protozoan parasites affecting several animal species and humans. The aim of this survey was to investigate, for the first time, their prevalence in red fox (Vulpes vulpes) faecal samples in central Italy. Seventy-one red foxes of different ages and sexes were examined for antigenic detection of Giardia and Cryptosporidium in fecal samples by means of a commercial rapid immunochromatographic test. The sample was randomly selected from foxes culled during a population control program. They were divided into groups based on sex and age (≤1-year-old and >1-year-old). Five (7%) and one (1.4%) out of 71 fecal samples were positive for the Giardia or Cryptosporidium antigens by immunochromatographic assay, respectively, and no coinfections were observed. The present prevalence rates of Giardia and Cryptosporidium antigens in faeces from V. vulpes suggest that this host species is likely to play only a limited role in the spread of the two protozoa in the study area. A concise review of the literature related to Giardia and Cryptosporidium in V. vulpes is presented.

Keywords: Giardia, Cryptosporidium, coproantigens, red fox, Vulpes vulpes


References

1. Feng, Y., Xiao, L. (2011). Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Clin Microbiol Rev. 24(1):110-140. https://doi.org/10.1128/CMR.00033-10 PMid:21233509 PMCid:PMC3021202
2. Leitch, G. J., He, Q. (2011). Cryptosporidiosis–an overview. J Biomed Res. 25(1):1-16. https://doi.org/10.1016/S1674-8301(11)60001-8 
3. Thomson, S., Hamilton, C. A., Hope, J. C., Katzer, F., Mabbott, N. A., Morrison, L. J., Innes, E. A. (2017). Bovine cryptosporidiosis:impact, hostparasite interaction and control strategies. Vet Res. 48(1):42. https://doi.org/10.1186/s13567-017-0447-0 PMid:28800747 PMCid:PMC5553596
4. Hoffmann, M., Sillero-Zubiri, C. (2016). Vulpes vulpes. [Internet]. The IUCN red list of threatened species 2016:e.T23062A46190249. [cited April 5, 2018]. http://dx.doi.org/10.2305/IUCN.UK.2016-1.RLTS.T23062A46190249.en 
5. Freuling, C. M., Hampson, K., Selhorst, T., Schröder, R., Meslin, F. X., Mettenleiter, T. C., Müller T. (2013). The elimination of fox rabies from Europe:determinants of success and lessons for the future. Philos Trans R Soc Lond B Biol Sci. 368 (1623):20120142. https://doi.org/10.1098/rstb.2012.0142 PMid:23798690 PMCid:PMC3720040
6. Sartore, S., Mulatti, P., Trestini, S., Lorenzetto, M., Gagliazzo, L., Marangon, S., Bonfanti, L. (2018). The economic implications of sylvatic rabies eradication in Italy. Zoonoses Public Health 65(1):147–157. https://doi.org/10.1111/zph.12383 PMid:28795513
7. Reperant, L. A., Hegglin, D., Fischer, C., Kohler, L., Weber, J. 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(3):605-611. https://doi.org/10.1007/s00436-007-0520-0 PMid:17393184
8. Karamon, J., Dabrowska, J., Kochanowski, M., Samorek-Pieróg, M., Sroka, J., et al. (2018). Prevalence of intestinal helminths of red foxes (Vulpes vulpes) in central Europe (Poland):a significant zoonotic threat. Parasit Vectors. 11, 436. https://doi.org/10.1186/s13071-018-3021-3 PMid:30055657 PMCid:PMC6064108
9. Zhou, L., Fayer, R., Trout, J. M., Ryan, U. M., Schaefer, F. W., Xiao, L. (2004). Genotypes of Cryptosporidium species infecting fur-bearing mammals differ from those of species infecting humans. Appl Environ Microbiol. 70(12):7574–7577. https://doi.org/10.1128/AEM.70.12.7574-7577.2004 PMid:15574965 PMCid:PMC535153
10. Hamnes, I. S., Gjerde, B. K., Forberg, T., Robertson, L. J. (2007). Occurrence of Giardia and Cryptosporidium in Norwegian red foxes (Vulpes vulpes). Vet Parasitol. 143(3-4):347-353. https://doi.org/10.1016/j.vetpar.2006.08.032 PMid:17045400
11. Nagano, Y., Finn, M. B., Lowery, C. J., Murphy, T., Moriarty, J., Power, E., et al. (2007). Occurrence of Cryptosporidium parvum and bacterial pathogens in faecal material in the red fox (Vulpes vulpes) population. Vet Res Comm. 31(5):559–564. https://doi.org/10.1007/s11259-007-3519-1 PMid:17225081
12. Beck, R., Sprong, H., Lucinger, S., Pozio, E., CaccióS. M. (2011). A large survey of Croatian wild mammals for Giardia duodenalis reveals a low prevalence and limited zoonotic potential. Vector Borne Zoonotic Dis. 11(8):1049-1055. https://doi.org/10.1089/vbz.2010.0113 PMid:21142957
13. Ng, J., Yang, R., Whiffin, V., Cox, P., Ryan, U. (2011). Identification of zoonotic Cryptosporidium and Giardia genotypes infecting animals in Sidney's water catchments. Exp Parasitol. 128(2):138-144. https://doi.org/10.1016/j.exppara.2011.02.013 PMid:21334325
14. Robinson, G., Chalmers, R. M., Stapleton, C., Palmer, S. R., Watkins, J., Francis, C., Kay, D. (2011). A whole water catchment approach to investigating the origin and distribution of Cryptosporidium species. J Appl Microbiol. 111(3):717–730. https://doi.org/10.1111/j.1365-2672.2011.05068.x PMid:21649804
15. Ravaszova, P., Halanova, M., Goldova, M., Valencakova, A., Malcekova, B., Hurníková, Z., Halan, M. (2012). Occurrence of Cryptosporidium spp. in red foxes and brown bear in the Slovak Republic. Parasitol Res. 110(1):469–471. https://doi.org/10.1007/s00436-011-2523-0 PMid:21744018
16. Nolan, M. J., Jexa, A. R., Koehlera, A. V., Haydon, S. R., Stevens, M. A., Gasser, R. B. (2013). Molecular-based investigation of Cryptosporidium and Giardia from animals in water catchments in southeastern Australia. Water Res. 47(5):1726-1740. https://doi.org/10.1016/j.watres.2012.12.027 PMid:23357792
17. Debenham, J. J., Landuyt, H., Troell, K., Tysnes, K., Robertson, L. J. (2017). Occurrence of Giardia in Swedish red foxes (Vulpes vulpes). J Wildl Dis. 53(3):649-652. https://doi.org/10.7589/2017-01-002 PMid:28362140
18. Mateo, M., de Mingo, M. H., de Lucio, A., Morales, L., Balseiro, A., Espí, A., et al. (2017). Occurrence and molecular genotyping of Giardia duodenalis and Cryptosporidium spp. in wild mesocarnivores in Spain. Vet Parasitol. 235, 86-93. https://doi.org/10.1016/j.vetpar.2017.01.016 PMid:28215875
19. Otranto, D., Cantacessi, C., Pfeffer, M., Dantas-Torres, F., Brianti, E., Deplazes, P., et al. (2015). The role of wild canids and felids in spreading parasites to dogs and cats in Europe. Part I:Protozoa and tick-borne agents. Vet Parasitol. 213(1-2):24-37. https://doi.org/10.1016/j.vetpar.2015.04.020 PMid:26049678
20. Cavallini, P., Santini, S. (1995). Age determination in the red fox in the Mediterranean habitat. Z Siiugetierk. 60, 136-142.
21. Mekaru, S. R., Marks, S. L., Felley, A. J., Chouicha, N., Kass, P. H. (2007). Comparison of direct immunofluorescence, immunoassays, and fecal flotation for detection of Cryptosporidium spp. and Giardia spp. in naturally exposed cats in 4 Northern California animal shelters. J Vet Intern Med. 21(5):959-965. https://doi.org/10.1111/j.1939-1676.2007.tb03049.x PMid:17939549
22. D'Ovidio, D., Rinaldi, L., Ianniello, D., Donnelly, T. M., Pepe, P., Capasso, M., Cringoli, G. (2014). FLOTAC for diagnosis of endo-parasites in pet squirrels in southern Italy. Vet Parsitol. 200(1-2):221-224. https://doi.org/10.1016/j.vetpar.2013.11.021 PMid:24389007
23. Perec-Matysiak, A., Buńkowska-Gawlik, K., Zaleśny, G., Hildebrand, J. (2015). Small rodents as reservoirs of Cryptosporidium spp. and Giardia spp. in south-western Poland. Ann Agric Environ Med. 22(1):1-5. https://doi.org/10.5604/12321966.1141359 PMid:25780818


Copyright

© 2019 Papini R.A. This is an open-access article published under the terms of the Creative Commons Attribution License which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Acknowledgment

The authors wish to thank all the hunters engaged in fox control program within the territorial hunting areas of the Pisa province, named ATC 14 and ATC 15, for allowing us to collect animal data and to sample culled red foxes.

Conflict of Interest Statement

The authors declared that they have no potential conflict of interest with respect to the authorship and/or publication of this article.

Citation Information

Macedonian Veterinary Review. Volume 42, Issue 1, Pages 101-106, p-ISSN 1409-7621, e-ISSN 1857-7415, DOI: 10.2478/macvetrev-2019-0013, 2019