Folia Parasitologica 68:010 (2021) | DOI: 10.14411/fp.2021.010
Endoparasite prevalence and infection risk factors among cats in an animal shelter in Estonia
- 1 Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Estonia;
- 2 Veterinary and Food Laboratory, Department of bacteriology-pathology, Tartu, Estonia
Cats are important hosts for different zoonotic parasites that can be hazardous to human health. To date, few studies have attempted to identify the factors affecting parasitic infections in shelter animals. This study aims to analyse the presence of endoparasites in shelter cats in Tartu, Estonia, and identify factors affecting endoparasite prevalence and intensity. The risk factors considered were age, location (urban vs rural cats) and time spent in shelter. In total, 290 faecal samples were collected from cats at an animal shelter in 2015-2016 and investigated for endoparasites using the concentration flotation technique. In total, 138 shelter cats (47.6%) were infected with endoparasites and their overall prevalence was: Toxocara cati (36.6%), Cystoisospora spp. (12.4%), Taeniidae gen. sp. (4.1%), Toxoplasma gondii/Hammondia hammondi (3.4%), Eucoleus aerophilus (2.1%), Cryptosporidium spp. (2.1%), Ancylostoma sp. (0.7%) and Giardia sp. (0.7%). Coinfections occurred in 38 cats (13.1%) most frequently of T. cati and Cystoisospora spp. (4.5%), Cystoisospora spp. and T. gondii/H. hammondi (2.1%). Where species identification of cestode and nematode samples was not possible according to morphology, genetic analysis of the mitochondrial cox1 gene was carried out. DNA was successfully analysed for 6 out of 13 samples that required genetic identification, revealing Ancylostoma tubaeforme in one nematode sample and Hydatigera taeniaeformis in five cestode samples. Cats from rural areas had significantly higher endoparasite prevalence than cats from urban areas. Helminth prevalence decreased to some extent due to anthelmintic treatment in cats available for adoption (held ≥15 days in the shelter), whereas the prevalence of infection with protists increased significantly in these animals. It is important to note that the analysis revealed lower infection intensity for quarantine cats (held 1-14 days in the shelter) compared with cats available for adoption. The relatively high prevalence of endoparasites (including zoonotic) in shelter cats ready for adoption suggests that current anthelminthic procedures require improvements.
Keywords: rural cats, shelter cats, Toxocara cati, Hydatigera taeniaeformis, urban cats, shelter management
Received: August 25, 2020; Revised: November 2, 2020; Accepted: November 19, 2020; Published online: April 20, 2021 Show citation
| ACS | AIP | APA | ASA | Harvard | Chicago | Chicago Notes | IEEE | ISO690 | MLA | NLM | Turabian | Vancouver |
Attachments
| Download file | FP_068_010_Suppl.pdf File size: 240.91 kB |
References
- Altreuther G., Borgsteede F.H.M., Buch J., Charles S.D., Cruthers L., Epe C., Young D.R., Krieger K.J. 2005: Efficacy of a topically administered combination of emodepside and praziquantel against mature and immature Ancylostoma tubaeforme in domestic cats. Parasitol. Res. 97: S51-S57.
Go to original source...
Go to PubMed... - Antolová D., Reiterová K., Stanko M., Zalesny G., Frièová J., Dvoro¾òáková E. 2013: Small mammals: paratenic hosts for species of Toxocara in eastern Slovakia. J. Helminthol. 87: 52-58.
Go to original source...
Go to PubMed... - Baneth G., Thamsborg S.M., Otranto D., Guillot J., Blaga R., Deplazes P., Solano-Gallego L. 2016: Major parasitic zoonoses associated with dogs and cats in Europe. J. Comp. Pathol. 155: S54-S74.
Go to original source...
Go to PubMed... - Barton K. 2019: Multi-Model Inference. R package version 1.43.6. https://CRAN.R-project.org/package=MuMIn
- Barutzki D., Schaper R. 2003: Endoparasites in dogs and cats in Germany 1999-2002. Parasitol Res. 90: S148-S150.
Go to original source...
Go to PubMed... - Becker A.C., Rohen M., Epe C., Schnieder T. 2012: Prevalence of endoparasites in stray and fostered dogs and cats in northern Germany. Parasitol Res. 111: 849-857.
Go to original source...
Go to PubMed... - Beugnet F., Bourdeau P., Chalvet-Monfray K., Cozma V., Farkas R., Guillot J., Halos L., Joachim A., Losson B., Miró G., Otranto D., Renaud M., Rinaldi L. 2014: Parasites of domestic owned cats in Europe: co-infestations and risk factors. Parasit. Vectors 7: 291.
Go to original source...
Go to PubMed... - Blasco X., Salas A., Manuelian C.L., Torre C., Ortuño A. 2017: Intestinal parasitic infection in multi-cat shelters in catalonia. Refu. Vet. 72: 16-21.
- Brooks E.M., Kristensen K., Benthem J. K., Magnusson A., Berg W.C., Nielsen A., Skaug J.H., Maechler M., Bolker M.B. 2017: glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R Journal 9: 378-400.
Go to original source... - Burnham K.P., Anderson D.R. (Eds.) 2004: Model Selection and Multimodel Inference. Springer, New York, 515 pp.
Go to original source... - Cacciò S., Pinter E., Fantini R., Mezzaroma I., Pozio E. 2002: Human Infection with Cryptosporidium felis: case report and literature review. Emerg. Infect. Dis. 8: 85-86.
Go to original source...
Go to PubMed... - Capári B., Hamel D., Visser M., Winter R., Pfister K., Rehbein S. 2013: Parasitic infections of domestic cats, Felis catus, in western Hungary. Vet. Parasitol. 192: 33-42.
Go to original source...
Go to PubMed... - Chalkowski K., Wilson A.E., Lepczyk C.A., Zohdy S. 2019: Who let the cats out? A global meta-analysis on risk of parasitic infection in indoor versus outdoor domestic cats (Felis catus). Biol. Lett. 15: 20180840.
Go to original source...
Go to PubMed... - Coati N., Schnieder T., Epe C. 2004: Vertical transmission of Toxocara cati Schrank 1788 (Anisakidae) in the cat. Parasitol. Res. 92: 142-146.
Go to original source...
Go to PubMed... - Dabritz H.A., Conrad P.A. 2010: Cats and Toxoplasma: implications for public health. Zoonoses Public Health 57: 34-52.
Go to original source...
Go to PubMed... - Deksne G., Petrusēvièa A., Kirju¹ina M. 2013: Seroprevalence and factors associated with Toxoplasma gondii infection in domestic cats from urban areas in Latvia. J. Parasitol. 99: 48-50.
Go to original source...
Go to PubMed... - Deplazes P., Hegglin D., Gloor S., Romig T. 2004: Wilderness in the city: the urbanization of Echinococcus multilocularis. Trends Parasitol. 20: 77-84.
Go to original source...
Go to PubMed... - Deplazes P., van Knapen F., Schweiger A., Overgaauw P.A.M. 2011: Role of pet dogs and cats in the transmission of helminthic zoonoses in Europe, with a focus on echinococcosis and toxocarosis. Vet. Parasitol. 182: 41-53.
Go to original source...
Go to PubMed... - Despommier D. 2003: Toxocariasis: clinical aspects, epidemiology, medical ecology, and molecular aspects. Clin. Microbiol. Rev. 16: 265-272.
Go to original source...
Go to PubMed... - Dubey J.P. 1995: Duration of immunity to shedding of Toxoplasma gondii oocysts by cats. J. Parasitol. 81: 410.
Go to original source...
Go to PubMed... - Dubey J. 2010: Toxoplasmosis of Animals and Humans. Second Edition. CRC Press, Boca Raton, 313 pp.
- Dubey J.P. 2018: A review of Cystoisospora felis and C. rivolta-induced coccidiosis in cats. Vet. Parasitol. 263: 34-48.
Go to original source...
Go to PubMed... - Dyachenko V., Pantchev N., Gawlowska S., Vrhovec M.G., Bauer C. 2008: Echinococcus multilocularis infections in domestic dogs and cats from Germany and other European countries. Vet. Parasitol. 157: 244-253.
Go to original source...
Go to PubMed... - Ekanayake S., Warnasuriya N.D., Samarakoon P.S., Abewickrama H., Kuruppuarachchi N.D., Dissanaike A.S. 1999: An unusual 'infection' of a child in Sri Lanka, with Taenia taeniaeformis of the cat. Ann. Trop. Med. Parasitol. 93: 869-873.
Go to original source...
Go to PubMed... - ESCCAP: Control of Intestinal Protozoa in Dogs and Cats. 2018. European Scientific Counsel Companion Animal Parasites. Second Edition. Malvern Hills Science Park, Malvern, 22 pp.
- ESCCAP: Worm Control in Dogs and Cats. 2017. European Scientific Counsel Companion Animal Parasites. Third Edition. Malvern Hills Science Park, Malvern, 41 pp.
- ESCCAP: Worm Control in Dogs and Cats. 2020. European Scientific Counsel Companion Animal Parasites. Sixth Edition. Malvern Hills Science Park, Malvern, 42 pp.
- Fayer R., Morgan U., Upton S.J. 2000: Epidemiology of Cryptosporidium: transmission, detection and identification. Int. J. Parasitol. 30: 1305-1322.
Go to original source...
Go to PubMed... - Gates M.C., Nolan T.J. 2009: Endoparasite prevalence and recurrence across different age groups of dogs and cats. Vet. Parasitol. 166: 153-158.
Go to original source...
Go to PubMed... - Gracenea M., Gómez M., Torres J. 2009: Prevalence of intestinal parasites in shelter dogs and cats in the metropolitan area of Barcelona (Spain). Acta Parasitol. 54: 73-77.
Go to original source... - Greenwood J.S. 2020. Protozoan Parasites of Veterinary importance. 2020: http://people.upei.ca/sgreenwood/html/protozoa.html
- Heinze G., Ploner M. 2018: logistf: Firth's Bias-Reduced Logistic Regression. R package version 1.23. https://CRAN.R-project.org/package=logistf
- Heyworth M.F. 2016: Giardia duodenalis genetic assemblages and hosts. Parasite 23: 13.
Go to original source...
Go to PubMed... - Jokelainen P., Simola O., Rantanen E., Näreaho A., Lohi H., Sukura A. 2012: Feline toxoplasmosis in Finland: cross-sectional epidemiological study and case series study. J. Vet. Diagn. Invest. 24: 1115-1124.
Go to original source...
Go to PubMed... - Jokelainen P., Velström K., Lassen B. 2015: Seroprevalence of Toxoplasma gondii in free-ranging wild boars hunted for human consumption in Estonia. Acta Vet. Scand. 57: 42.
Go to original source...
Go to PubMed... - Kapel C.M.O., Torgerson P.R., Thompson R.C.A., Deplazes P. 2006: Reproductive potential of Echinococcus multilocularis in experimentally infected foxes, dogs, raccoon dogs and cats. Int. J. Parasitol. 36: 79-86.
Go to original source...
Go to PubMed... - Karamon J., Sroka J., D±browska J., Bilska-Zaj±c E., Zdybel J., Kochanowski M., Ró¿ycki M., Cencek T. 2019: First report of Echinococcus multilocularis in cats in Poland: a monitoring study in cats and dogs from a rural area and animal shelter in a highly endemic region. Parasit. Vectors 12: 313.
Go to original source...
Go to PubMed... - Khatat S., Rosenberg D., Benchekroun G., Polack B. 2016: Lungworm Eucoleus aerophilus (Capillaria aerophila ) infection in a feline immunodeficiency virus-positive cat in France. JFMS Open Rep. 2: 1-5.
Go to original source...
Go to PubMed... - Knapp J., Giraudoux P., Combes B., Umhang G., Boué F., Said-Ali Z., Aknouche S., Garcia C., Vacheyrou M., Laboissière A., Raton V., Comte S., Favier S., Demerson J.-M., Caillot C., Millon L., Raoul F. 2018: Rural and urban distribution of wild and domestic carnivore stools in the context of Echinococcus multilocularis environmental exposure. Int. J. Parasitol. 48: 937-946.
Go to original source...
Go to PubMed... - Kostopoulou D., Claerebout E., Arvanitis D., Ligda P., Voutzourakis N., Casaert S., Sotiraki S. 2017: Abundance, zoonotic potential and risk factors of intestinal parasitism amongst dog and cat populations: the scenario of Crete, Greece. Parasit. Vectors 10: 43.
Go to original source...
Go to PubMed... - Lalo¹eviæ D., Stanojev-Jovanoviæ D., Lalo¹eviæ V., Pozio E., Klem I. 2008: Pulmonary capillariasis miming bronchial carcinoma. Am. J. Trop. Med. Hyg. 78: 14-16.
Go to original source... - Lassen B., Janson M., Viltrop A., Neare K., Hütt P., Golovljova I., Tummeleht L., Jokelainen P. 2016: Serological evidence of exposure to globally relevant zoonotic parasites in the estonian population. PLoS One 11: e0164142.
Go to original source...
Go to PubMed... - Laurimaa, L., Davison, J., Plumer, L., Süld, K., Oja, R., Moks, E., Keis, M., Hindrikson, M., Kinkar L., Laurimäe T., Abner J., Remm J., Anijalg P., Saarma U. 2015a: Noninvasive detection of Echinococcus multilocularis tapeworm in urban area, Estonia. Emerg. Infect. Dis. 21: 163-164.
Go to original source...
Go to PubMed... - Laurimaa L., Davison J., Süld K., Plumer L., Oja R., Moks E., Keis M., Hindrikson M., Kinkar L., Laurimäe T., Abner J., Remm J., Anijalg P., Saarma U. 2015b: First report of highly pathogenic Echinococcus granulosus genotype G1 in dogs in a European urban environment. Parasit. Vectors 8: 182.
Go to original source...
Go to PubMed... - Laurimaa L., Moks E., Soe E., Valdmann H., Saarma U. 2016a: Echinococcus multilocularis and other zoonotic parasites in red foxes in Estonia. Parasitology 143: 1450-1458.
Go to original source...
Go to PubMed... - Laurimaa L., Süld K., Davison J., Moks E., Valdmann H., Saarma U. 2016b: Alien species and their zoonotic parasites in native and introduced ranges: The raccoon dog example. Vet. Parasitol. 219: 24-33.
Go to original source...
Go to PubMed... - Laurimaa L., Süld K., Moks E., Valdmann H., Umhang G., Knapp J., Saarma U. 2015c: First report of the zoonotic tapeworm Echinococcus multilocularis in raccoon dogs in Estonia, and comparisons with other countries in Europe. Vet. Parasitol. 212: 200-205.
Go to original source...
Go to PubMed... - Lefkaditis M., Paºtiu A., Rodi-Buriel A., Sossidou A., Panorias A., Eleftheriadis T., Cozma V., Mihalca A. 2014: Helminth burden in stray cats from Thessaloniki, Greece. Helminthologia 51: 73-76.
Go to original source... - Leoni F., Gallimore C.I., Green J., McLauchlin J. 2003: Molecular epidemiological analysis of Cryptosporidium isolates from humans and animals by using a heteroduplex mobility assay and nucleic acid sequencing based on a small double-stranded RNA element. J. Clin. Microbiol. 41: 981-992.
Go to original source...
Go to PubMed... - Loftin C.M., Donnett U.B., Schneider L.G., Varela-Stokes A.S. 2019: Prevalence of endoparasites in northern Mississippi shelter cats. Vet. Parasitol. Reg. Stud. Reports 18: 100322.
Go to original source...
Go to PubMed... - McGlade T.R., Robertson I.D., Elliot A.D., Read C., Thompson R.C.A. 2003: Gastrointestinal parasites of domestic cats in Perth, Western Australia. Vet. Parasitol. 117: 251-262.
Go to original source...
Go to PubMed... - Mircean V., Titilincu A., Vasile C. 2010: Prevalence of endoparasites in household cat (Felis catus) populations from Transylvania (Romania) and association with risk factors. Vet. Parasitol. 171: 163-166.
Go to original source...
Go to PubMed... - Moks E., Jõgisalu I., Saarma U., Talvik H., Järvis T., Valdmann H. 2006: Helminthological survey of wolf (Canis lupus) in Estonia, with an emphasis on the occurrence of Echinococcus granulosus. J. Wildl. Dis. 42: 359-365.
Go to original source...
Go to PubMed... - Moks E., Saarma U., Valdmann H. 2005: Echinococcus multilocularis in Estonia. Emerg. Infect. Dis. 11: 1973-1974.
Go to original source...
Go to PubMed... - Must K., Lassen B., Jokelainen P. 2015: Seroprevalence of and risk factors for Toxoplasma gondii infection in cats in Estonia. Vector Borne Zoonotic Dis. 15: 597-601.
Go to original source...
Go to PubMed... - Näreaho A., Puomio J., Saarinen K., Jokelainen P., Juselius T., Sukura A. 2012: Feline intestinal parasites in Finland: prevalence, risk factors and anthelmintic treatment practices. J. Feline Med. Surg. 14: 378-383.
Go to original source...
Go to PubMed... - Nijsse R., Ploeger H.W., Wagenaar J.A., Mughini-Gras L. 2016: Prevalence and risk factors for patent Toxocara infections in cats and cat owners' attitude towards deworming. Parasitol Res. 115: 4519-4525.
Go to original source...
Go to PubMed... - Otranto D., Cantacessi C., Pfeffer M., Dantas-Torres F., Brianti E., Deplazes P., Genchi C., Guberti V., Capelli G. 2015: The role of wild canids and felids in spreading parasites to dogs and cats in Europe. Vet. Parasitol. 213: 12-23.
Go to original source...
Go to PubMed... - Overgaauw P.A.M., van Zutphen L., Hoek D., Yaya F.O., Roelfsema J., Pinelli E., van Knapen F., Kortbeek L.M. 2009: Zoonotic parasites in fecal samples and fur from dogs and cats in The Netherlands. Vet. Parasitol. 163: 115-122.
Go to original source...
Go to PubMed... - Palmer C.S., Thompson R.C.A., Traub R.J., Rees R., Robertson I.D. 2008: National study of the gastrointestinal parasites of dogs and cats in Australia. Vet. Parasitol. 151: 181-190.
Go to original source...
Go to PubMed... - Pavlásek I., Ryan U. 2007: The first finding of a natural infection of Cryptosporidium muris in a cat. Vet. Parasitol. 144: 349-352.
Go to original source...
Go to PubMed... - Plumer L., Davison J., Saarma U. 2014: Rapid urbanization of red foxes in Estonia: distribution, behaviour, attacks on domestic animals, and health-risks related to zoonotic diseases. PLoS One 9: e115124.
Go to original source...
Go to PubMed... - R Core Team 2020: R: A language and environment for statistical computing. R foundation for statistical computing, Vienna. https://www.r-project.org/
- Remes N., Kärssin A., Must K., Tagel M., Lassen B., Jokelainen P. 2018: Toxoplasma gondii seroprevalence in free-ranging moose (Alces alces) hunted for human consumption in Estonia: indicator host species for environmental Toxoplasma gondii oocyst contamination. Vet. Parasitol. Reg. Stud. Reports 11: 6-11.
Go to original source...
Go to PubMed... - Roepstorff A., Nansen P. 1998: The Epidemiology, Diagnosis and Control of Helminth Parasites of Swine, FAO Animal Health Manual. Food and Agriculture Organization of the United Nations, Rome, 171 pp.
- Rossin A., Malizia A.I., Denegri G.M. 2004: The role of the subterranean rodent Ctenomys talarum (Rodentia: Octodontidae) in the life cycle of Taenia taeniaeformis (Cestoda: Taeniidae) in urban environments. Vet. Parasitol. 122: 27-33.
Go to original source...
Go to PubMed... - Saarma U., Jõgisalu I., Moks E., Varcasia A., Lavikainen A., Oksanen A., Simsek S., Andresiuk V., Denegri G., González L.M., Ferrer E., Gárate T., Rinaldi L., Maravilla P. 2009: A novel phylogeny for the genus Echinococcus, based on nuclear data, challenges relationships based on mitochondrial evidence. Parasitology 136: 317-328.
Go to original source...
Go to PubMed... - Schurer J.M., McKenzie C., Dowling P.M., Bouchard E., Jenkins E.J. 2015: Parasite control in Canadian companion animal shelters and a cost-comparison of anthelmintics. Can. Vet. J. 56: 964-970.
Go to PubMed... - Schurer J.M., Ndao M., Skinner S., Irvine J., Elmore S.A., Epp T., Jenkins E.J. 2013: Parasitic zoonoses: one health surveillance in northern Saskatchewan. PLoS Negl. Trop. Dis. 7: e2141.
Go to original source...
Go to PubMed... - Spain C.V., Scarlett J.M., Wade S.E., McDonough P. 2001: Prevalence of enteric zoonotic agents in cats less than 1 year old in central New York State. J. Vet. Intern. Med. 15: 33-38.
Go to original source...
Go to PubMed... - Strube C., Heuer L., Janecek E. 2013: Toxocara spp. infections in paratenic hosts. Vet. Parasitol. 193: 375-389.
Go to original source...
Go to PubMed... - Suzuki J., Murata R., Kobayashi S., Sadamasu K., Kai A., Takeuchi T. 2011: Risk of human infection with Giardia duodenalis from cats in Japan and genotyping of the isolates to assess the route of infection in cats. Parasitology 138: 493-500.
Go to original source...
Go to PubMed... - Talvik H., Moks E., Mägi E., Järvis T., Miller I. 2006: Distribution of Toxocara infection in the environment and in definitive and paratenic hosts in Estonia. Acta Vet. Hung. 54: 399-406.
Go to original source...
Go to PubMed... - Tartu Animal Shelter 2019: Statistics of Tartu Animal Shelter 2019. https://www.loomadevarjupaik.eu/en/varjupaik/statistika.
- Tokiwa T., Ohnuki A., Kubota R., Tamukai K., Ike K. 2018: Morphological and molecular characterization of Cystoisospora sp. from Asian small-clawed otters Aonyx cinereus. Int. J. Parasitol. Parasit. Wildl. 7: 268-273.
Go to original source...
Go to PubMed... - Tull A., Moks E., Laurimaa L., Keis M., Süld K. 2020: Endoparasite infection hotspots in Estonian urban areas. J. Helminthol. 94: 1-9.
Go to original source...
Go to PubMed... - Tzannes S., Batchelor D.J., Graham P.A., Pinchbeck G.L., Wastling J., German A.J. 2008: Prevalence of Cryptosporidium, Giardia and Isospora species infections in pet cats with clinical signs of gastrointestinal disease. J. Feline Med. Surg. 10: 1-8.
Go to original source...
Go to PubMed... - Valdmann H., Moks E., Talvik H. 2004: Helminth fauna of Eurasian lynx (Lynx lynx) in Estonia. J. Wildl. Dis. 40: 356-360.
Go to original source...
Go to PubMed... - Villeneuve A., Polley L., Jenkins E., Schurer J., Gilleard J., Kutz S., Conboy G., Benoit D., Seewald W., Gagné F. 2015: Parasite prevalence in fecal samples from shelter dogs and cats across the Canadian provinces. Parasit. Vectors 8: 281.
Go to original source...
Go to PubMed... - Vuitton D.A., Zhou H., Bresson-Hadni S., Wang Q., Piarroux M., Raoul F., Giraudoux P. 2003: Epidemiology of alveolar echinococcosis with particular reference to China and Europe. Parasitology 127: S87-S107.
Go to original source...
Go to PubMed... - Wyrosdick H.M., Chapman A., Martinez J., Schaefer, J.J. 2017: Parasite prevalence survey in shelter cats in Citrus County, Florida. Vet. Parasitol. Reg. Stud. Reports. 10: 20-24.
Go to original source...
Go to PubMed... - Zottler E.-M., Bieri M., Basso W., Schnyder M. 2019: Intestinal parasites and lungworms in stray, shelter and privately owned cats of Switzerland. Parasitol. Int. 69: 75-81.
Go to original source...
Go to PubMed...


