American Association of Zoo Veterinarians Infectious Disease Committee Manual 2013 CYTAUXZOONOSIS

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Tobias Mathews
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1 Animal Group(s) Affected Felids, wild and domestic Transmission Tick-borne (Amblyomma americanum and Dermacentor variabilis) Clinical Signs Domestic cats and some exotic felids: some cats develop no clinical signs while others may develop high fever, lethargy, dyspnea, depression, dehydration, anorexia, anemia, hepatosplenomegaly, and/or jaundice; others die acutely. Exotic felids often show no clinical signs. Severity Treatment Prevention and Control Non-clinical or mild to severe including death; could depend on numerous factors such as species of felid, strain or genotype of parasite, or other unknown factors. Mortality is generally high even with treatment. A combination of atovaquone and azithromycin seems to have the highest success rates. Supportive care also should be provided. Avoid contact with ticks by keeping cats indoors. Outside cats should have effective acaricides applied. No vaccine available. Zoonotic Fact Sheet compiled by: Michael J. Yabsley Sheet completed on: 1 August 2013 Fact Sheet Reviewed by: Adam Birkenheuer; Meredith M. Clancy Susceptible animal groups: Felids. Cytauxzoon felis has been reported from domestic cats, bobcats (Lynx rufus), puma (Puma concolor), and captive exotic felids (e.g., tigers [Panthera tigris]). C. manul infects the Pallas cat. Cytauxzoon spp., some genetically similar to C. felis, have been reported from domestic cats and numerous free-ranging and/or captive exotic felids in South America and Europe. Causative organism: Cytauxzoon spp. are Apicomplexan parasites in the Order Piroplasmida, which are related to important human and veterinary pathogens in the genera Babesia and Theileria spp. In the US, C. felis is the causative agent of cytauxzoonosis in domestic cats and some exotic felids. Bobcats, and other wild felids (e.g., cougars), are the natural reservoir but chronically infected domestic cats can serve as a source of infection for ticks. Outside of the US, other species or genetic variants of C. felis infect wild and domestic felids; however, clinical cytauxzoonosis is rare. Zoonotic potential: None Distribution: C. felis has been reported from numerous states in the eastern US but is likely found throughout the range of the vector(s) and the main wildlife reservoir (bobcats). Other species of Cytauxzoon have been reported in parts of South America, Europe and Asia. Some of the Cytauxzoon likely represent novel species or have been described as separate species (e.g., C. manul), but recent genetic data indicates that Cytauxzoon from Brazil is closely related to C. felis from the US. Exotic felids kept in enclosures that allow tick exposure within the natural range of any Cytauxzoon spp. are at risk of infection. Incubation period: C. felis can typically be detected in erythrocytes of infected cats approximately 1-3 weeks after an infected tick bite. Clinical signs typically occur 5-16 days after infected tick bite. Clinical signs: Domestic cats: The majority of domestic cats develop severe clinical disease but some never develop clinical signs, but remain chronic carriers. Those with clinical signs may develop high fever, lethargy, dyspnea, depression, dehydration, anorexia, anemia, hepatosplenomegaly, and/or jaundice. Captive wild/exotic felids: Development of clinical signs is highly variable and may depend on felid species, No

2 strain of parasite, or some other factor. Fatal cases have been reported in a tiger housed in Florida and lions in Brazil; however, asymptomatic infections have been detected in tigers in US and ocelots (Leopardus pardalis), oncilla (L. tigrinus), jaguar (Panthera onca), and puma in Brazil. Wild felids (natural reservoirs): Wild reservoir species rarely develop clinical signs but very rare acute mortality has been reported among young bobcats. In addition, three infected cougar in the US developed a transient anemia and increased serum bilirubin concentrations and increased alanine aminotransferase and aspartate aminotransferase activities soon after infection; however, all recovered rapidly without treatment. Clinical pathological, gross, and histopathological findings: Parasitemia of C. felis on blood smears is generally low (<5%), even for clinically ill felids. Leukopenia or pancytopenia may be present as well as thrombocytopenia and normocytic, normochromic anemia. Gross lesions are typically severe as death occurs due to severe occlusions of vessels by developing parasites. Felids may have pale or icteric mucous membranes, petechiae and ecchymoses in the lung, heart, lymph nodes and on mucous membranes, splenomegaly, lymphadenomegaly, and hydropericardium. Numerous large schizonts will be noted in the cytoplasm of infected macrophages that often occlude the lumens of numerous vessels of many tissues, especially the lungs. Despite the large numbers and size of schizonts, a lack of inflammatory reaction generally is present. Diagnosis: Piroplasms may be detected in stained thin blood smears if sufficiently high parasitemias are present; however, subclinical chronic carriers generally have very low parasitemias. Although feline babesiosis has not been reported in domestic cats in the US, C. felis trophozoites are morphologically similar to other small piroplasms so PCR testing is necessary to definitive identify C. felis. If possible, a fine needle aspiration of a peripheral lymph node, spleen, or liver should be performed to identify schizonts in macrophages. These intracellular schizonts are not found in babesiosis cases so can be used to definitively identify Cytauxzoon infections. Several PCR protocols have been developed for the detection of C. felis. If PCR assays are not specific to C. felis, amplicons should be sequenced to confirm identification as other piroplasms can infect felids, especially wild felids. Material required for laboratory analysis: Thin blood smears fixed and stained for detection of piroplasms and anticoagulated whole blood (for PCR testing and preparation of thin blood smears). Formalin fixed needle biopsies of tissues for histologic evaluation for schizonts. Relevant diagnostic laboratories: Many diagnostic laboratories have PCR based assays for C. felis. Treatment: Despite treatment, mortality rates can be high. The greatest success has been obtained using atovaquone (15 mg/kg, PO, tid for 10 days) and azithromycin (10 mg/kg, PO, sid for 10 days) with supportive care (fluid therapy and heparin). Limited success has been obtained using imidocarb and diminazene diaceturate while even less success has been obtained using parvaquone, buparvaquone, trimethoprim/sulfadiazine, and sodium thiacetarsamide. Prevention and control: Because Cytauxzoon is tick-borne, limiting exposure of felids to ticks is necessary to prevent transmission. For domestic cats, the best prevention is to keep cats indoors. For exotic or wild felids or domestic cats that are allowed outdoors, an effective acaracide or acaricide-treated collar should be used to prevent or limit tick infestation. If possible, tick checks can also decrease risk by finding and removing ticks prior to transmission. Habitat modification can also be used around a premise to decrease local habits for ticks which should decrease tick infestation rates of animals. Suggested disinfectant for housing facilities: Prevent tick-exposure Notification: None Measures required under the Animal Disease Surveillance Plan: None Measures required for introducing animals to infected animal: This parasite is tick-borne so direct contact between animals is not a risk factor for infection. However, tick prevention should be implemented. Conditions for restoring disease-free status after an outbreak: Not applicable

3 Experts who may be consulted: Michael J. Yabsley, MS, PhD, FRES Associate Professor University of Georgia Athens, Georgia (706) Adam Birkenheuer, DVM., PhD, DACVIM Associate Professor North Carolina State University Raleigh, NC (919) Leah A. Cohn, DVM, PhD, DACVIM Professor University of Missouri Columbia, MO (573) References: 1. Birkenheuer, A.J., H.S. Marr, C. Warren, A.E. Acton, E.M. Mucker, J.G. Humphreys, and M.D. Tucker Cytauxzoon felis infections are present in bobcats (Lynx rufus) in a region where cytauxzoonosis is not recognized in domestic cats. Vet. Parasitol. 153(1-2): Birkenheuer, A.J., J.A. Le, A.M. Valenzisi, M.D. Tucker, M.G. Levy, and E.B. Breitschwerdt Cytauxzoon felis infection in cats in the mid-atlantic states: 34 cases ( ). J. Am. Vet. Med. Assoc. 228(4): Brown, H.M., J.M. Lockhart, K.S. Latimer, and D.S. Peterson Identification and genetic characterization of Cytauxzoon felis in asymptomatic domestic cats and bobcats. Vet. Parasitol. 172(3-4): Brown, H.M., S.M. Modaresi, J.L. Cook, K.S. Latimer, and D.S. Peterson Genetic variability of archived Cytauxzoon felis histologic specimens from domestic cats in Georgia, J. Vet. Diagn. Invest. 21(4): Brown, H.M., R.D. Berghaus, K.S. Latimer, J.O. Britt, P.M. Rakich, and D.S. Peterson Genetic variability of Cytauxzoon felis from 88 infected domestic cats in Arkansas and Georgia. J. Vet. Diagn. Invest. 21(1): Brown, H.M., K.S. Latimer, L.E. Erikson, M.E. Cashwell, J.O. Britt, and D.S. Peterson Detection of persistent Cytauxzoon felis infection by polymerase chain reaction in three asymptomatic domestic cats. J. Vet. Diagn. Invest. 20(4): Carli, E., M. Trotta, R. Chinelli, M. Drigo, L. Sinigoi, P. Tosolini, T. Furlanello, A. Millotti, M. Caldin, and L. Solano-Gallego Cytauxzoon sp. infection in the first endemic focus described in domestic cats in Europe. Vet. Parasitol. 183(3-4):

4 8. Cohn, L.A., A.J. Birkenheuer, J.D. Brunker, E.R. Ratcliff, and A.W. Craig Efficacy of atovaquone and azithromycin or imidocarb dipropionate in cats with acute cytauxzoonosis. J. Vet. Intern. Med. 25(1): Filoni, C., J.L. Catão-Dias, V. Cattori, B. Willi, M.L. Meli, S.H. Corrêa, M.C. Marques, C.H. Adania, J.C. Silva, M.F. Marvulo, J.S. Ferreira Neto, E.L. Durigon, V.M. de Carvalho, S.D. Coutinho, H. Lutz, and R. Hofmann-Lehmann Surveillance using serological and molecular methods for the detection of infectious agents in captive Brazilian neotropic and exotic felids. J. Vet. Diagn. Invest. 24(1): Garner, M.M., N.P. Lung, S. Citino, E.C. Greiner, J.W. Harvey, and B.L. Homer Fatal cytauxzoonosis in a captive-reared white tiger (Panthera tigris). Vet. Pathol. Jan;33(1): Hoover, J.P., D.B. Walker, and J.D. Hedges Cytauxzoonosis in cats: eight cases ( ). J. Am. Vet. Med. Assoc. 205(3): Haber, M.D., M.D. Tucker, H.S. Marr, J.K. Levy, J. Burgess, M.R. Lappin, and A.J. Birkenheuer The detection of Cytauxzoon felis in apparently healthy free-roaming cats in the USA. Vet. Parasitol. 146(3-4): Harvey, J.W., M.R. Dunbar, T.M. Norton, and M.J. Yabsley Laboratory findings in acute Cytauxzoon felis infection in cougars (Puma concolor couguar) in Florida. J. Zoo Wildl. Med. 38(2): Lewis, K.M., L.A. Cohn, M.E. Downey, M.S. Whitney, and A.J. Birkenheuer Evaluation of Cytauxzoon felis infection status in captive-born wild felids housed in an area endemic for the pathogen. J. Am. Vet. Med. Assoc. 241(8): Maia, L.M., M. Cerqueira Ade, D. de Barros Macieira, A.M. de Souza, N.S. Moreira, A.V. da Silva, J.B. Messick, R.F. Ferreira, and N.R. Almosny Cytauxzoon felis and 'Candidatus Mycoplasma haemominutum' coinfection in a Brazilian domestic cat (Felis catus). Rev. Bras. Parasitol. Vet. 22(2): Meinkoth, J., A.A. Kocan, L. Whitworth, G. Murphy, J.C. Fox, and J.P. Woods Cats surviving natural infection with Cytauxzoon felis: 18 cases ( ). J. Vet. Intern. Med. 14(5): Peixoto, P.V., C.O. Soares, A. Scofield, C.D. Santiago, T.N. França, and S.S. Barros Fatal cytauxzoonosis in captive-reared lions in Brazil. Vet. Parasitol. 145(3-4): Reichard, M.V., J.H. Meinkoth, A.C. Edwards, T.A. Snider, K.M. Kocan, E.F. Blouin, and S.E. Little Transmission of Cytauxzoon felis to a domestic cat by Amblyomma americanum. Vet. Parasitol. 161(1-2): Reichard, M.V., A.C. Edwards, J.H. Meinkoth, T.A.Snider, K.R. Meinkoth, R.E. Heinz, and S.E. Little Confirmation of Amblyomma americanum (Acari: Ixodidae) as a vector for Cytauxzoon felis (Piroplasmorida: Theileriidae) to domestic cats. J. Med. Entomol. 47(5): Reichard, M.V., K.A. Baum, S.C. Cadenhead, and T.A. Snider Temporal occurrence and environmental risk factors associated with cytauxzoonosis in domestic cats. Vet. Parasitol. 152(3-4): Schreeg, M.E., H.S. Marr, J. Tarigo, L.A. Cohn, M.G. Levy, and A.J. Birkenheuer Pharmacogenomics of Cytauxzoon felis cytochrome b: implications for atovaquone and azithromycin therapy in domestic cats with cytauxzoonosis. J. Clin. Microbiol. In press 22. Shock, B.C., A.J. Birkenheuer, L.L. Patton, C. Olfenbuttel, J. Beringer, D.M. Grove, M. Peek, J.W. Butfiloski, D.W. Hughes, J.M. Lockhart, M.W. Cunningham, H.M. Brown, D.S. Peterson, and M.J. Yabsley Variation in the ITS-1 and ITS-2 rrna genomic regions of Cytauxzoon felis from bobcats and pumas in the eastern United States and comparison with sequences from domestic cats. Vet. Parasitol. 190(1-2):

5 23. Shock, B.C., S.M. Murphy, L.L. Patton, P.M. Shock, C. Olfenbuttel, J. Beringer, S. Prange, D.M. Grove, M. Peek, J.W. Butfiloski, D.W. Hughes, J.M. Lockhart, S.N. Bevins, S. VandeWoude, K.R. Crooks, V.F. Nettles, H.M. Brown, D.S. Peterson, and M.J. Yabsley Distribution and prevalence of Cytauxzoon felis in bobcats (Lynx rufus), the natural reservoir, and other wild felids in thirteen states. Vet. Parasitol. 175(3-4): Yabsley, M.J., S.M. Murphy, and M.W. Cunningham. 2006, Molecular detection and characterization of Cytauxzoon felis and a Babesia species in cougars from Florida. J. Wildl. Dis. 42(2):

This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and

This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and education use, including for instruction at the authors institution