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Virology Journal
Published in: Virology Journal 1/2017

Open Access 01-12-2017 | Research

Putative progressive and abortive feline leukemia virus infection outcomes in captive jaguarundis (Puma yagouaroundi)

Authors: Claudia Filoni, A. Katrin Helfer-Hungerbuehler, José Luiz Catão-Dias, Mara Cristina Marques, Luciana Neves Torres, Manfred Reinacher, Regina Hofmann-Lehmann

Published in: Virology Journal | Issue 1/2017

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Abstract

Background

Feline leukemia virus (FeLV) is an exogenous gammaretrovirus of domestic cats (Felis catus) and some wild felids. The outcomes of FeLV infection in domestic cats vary according to host susceptibility, virus strain, and infectious challenge dose. Jaguarundis (Puma yagouaroundi) are small wild felids from South and Central America. We previously reported on FeLV infections in jaguarundis. We hypothesized here that the outcomes of FeLV infection in P. yagouaroundi mimic those observed in domestic cats. The aim of this study was to investigate the population of jaguarundis at Fundação Parque Zoológico de São Paulo for natural FeLV infection and resulting outcomes.

Methods

We investigated the jaguarundis using serological and molecular methods and monitored them for FeLV-related diseases for 5 years. We retrieved relevant biological and clinical information for the entire population of 23 jaguarundis held at zoo. Post-mortem findings from necropsies were recorded and histopathological and immunohistopathological analyses were performed. Sequencing and phylogenetic analyses were performed for FeLV-positive samples. For sample prevalence, 95% confidence intervals (CI) were calculated. Fisher’s exact test was used to compare frequencies between infected and uninfected animals. P-values <0.05 were considered significant.

Results

In total, we detected evidence of FeLV exposure in four out of 23 animals (17%; 95% CI 5–39%). No endogenous FeLV (enFeLV) sequences were detected. An intestinal B-cell lymphoma in one jaguarundi was not associated with FeLV. Two jaguarundis presented FeLV test results consistent with an abortive FeLV infection with seroconversion, and two other jaguarundis had results consistent with a progressive infection and potentially FeLV-associated clinical disorders and post-mortem changes. Phylogenetic analysis of env revealed the presence of FeLV-A, a common origin of the virus in both animals (100% identity) and the closest similarity to FeLV-FAIDS and FeLV-3281 (98.4% identity), originally isolated from cats in the USA.

Conclusions

We found evidence of progressive and abortive FeLV infection outcomes in jaguarundis, and domestic cats were probably the source of infection in these jaguarundis.
Literature
1.
2.
Adania CH, Silva JCR, Felippe PAN. Carnivora – Felidae (Onça, Suçuarana, Jaguatirica e Gato-do-Mato). In: Cubas ZS, Silva JCR, Catão-Dias JL, editors. Tratado de animais selvagens: medicina veterinária. São Paulo: Roca; 2014. p. 779–818.
3.
Hoover EA, Mullins JI. Feline leukemia virus infection and diseases. J Am Vet Med Assoc. 1991;199:1287–97.PubMed
4.
5.
Francis DP, Essex M, Hardy WD. Excretion of feline leukaemia virus by naturally infected pet cats. Nature. 1977;269:252–4.CrossRefPubMed
6.
Gomes-Keller MA, Tandon R, Gönczi E, Meli ML, Hofmann-Lehmann R, Lutz H. Shedding of feline leukemia virus RNA in saliva is a consistent feature in viremic cats. Vet Microbiol. 2006;112:11–21.CrossRefPubMed
7.
Gomes-Keller MA, Gönczi E, Grenacher B, Tandon R, Hofman-Lehmann R, Lutz H. Fecal shedding of infectious feline leukemia virus and its nucleic acids: a transmission potential. Vet Microbiol. 2009;134:208–17.CrossRefPubMed
8.
Reinacher M. Diseases associated with spontaneous feline leukemia virus (FeLV) infection in cats. Vet Immunol Immunopathol. 1989;21:85–95.CrossRefPubMed
9.
Driciru M, Siefert L, Prager KC, Dubovi E, Sande R, Princee F, Friday T, Munson L. A serosurvey of viral infections in lions (Panthera leo), from queen Elizabeth National Park, Uganda. J Wildl Dis. 2006;42:667–71.CrossRefPubMed
10.
Thalwitzer S, Wachter B, Robert N, Wibbelt G, Müller T, Lonzer J, Meli ML, Bay G, Hofer H, Lutz H. Seroprevalences to viral pathogens in free-ranging and captive cheetahs (Acinonyx jubatus) on Namibian Farmland. Clin Vaccine Immunol. 2010;17:232–8.CrossRefPubMed
11.
Ostrowski S, Van Vuuren M, Lenain DM, Durand A. A serologic survey of wild felids from central west Saudi Arabia. J Wildl Dis. 2003;39:696–701.CrossRefPubMed
12.
Filoni C, Adania CH, Durigon EL, Catão-Dias JL. Serosurvey for feline leukemia virus and lentiviruses in captive small neotropic felids in São Paulo state, Brazil. J Zoo Wildl Med. 2003;34:65–8.
13.
Hofmann-Lehmann R, Fehr D, Grob M, Elgizoli M, Packer C, Martenson JS, O’Brien SJ, Lutz H. Prevalence of antibodies to feline parvovirus, calicivirus, herpesvirus, coronavirus, and immunodeficiency virus and of feline leukemia virus antigen and the interrelationship of these viral infections in free-ranging lions in East Africa. Clin Diag Lab Immunol. 1996;3:554–62.
14.
15.
Leutenegger CM, Mislin CN, Sigrist B, Ehrengruber MU, Hofmann-Lehmann R, Lutz H. Viral infections in free-living populations of the European wildcat. J Wildl Dis. 1999;35:678–86.CrossRefPubMed
16.
Daniels MJ, Golder MC, Jarrett O, MacDonald DW. Feline viruses in wildcats from Scotland. J Wildl Dis. 1999;35:121–4.CrossRefPubMed
17.
Fromont E, Sager A, Léger F, Bourguemestre F, Jouquelet E, Stahl P, Pontier D, Artois M. Prevalence and pathogenicity of retroviruses in wildcats in France. Vet Rec. 2000;146:317–9.CrossRefPubMed
18.
Meli ML, Cattori V, Martínez F, López G, Vargas A, Palomares F, López-Bao JV, Hofmann-Lehmann R, Lutz H. Feline leukemia virus and other pathogens as important threats to the survival of the critically endangered Iberian lynx (Lynx pardinus). PLoS One. 2009;4(3):e4744. https://​doi.​org/​10.​1371/​journal.​pone.​0004744.
19.
Marina ML, Cattori V, Martínez F, López G, Vargas A, Palomares F, López-Bao JV, Hofmann-Lehmann R, Lutz H. Feline leukemia virus infection: a threat for the survival of the critically endangered Iberian lynx (Lynx pardinus). Vet Immunol Immunopathol. 2010;134:61–7.CrossRef
20.
Cunningham MW, Brown MA, Shindle DB, Terrell SP, Hayes KA, Ferree BC, McBride RT, Blankenship EL, Jansen D, Citino SB, Roelke ME, Kiltie RA, Troyer JL, O’Brien SJ. Epizootiology and management of feline leukemia virus in the Florida puma. J Wildl Dis. 2008;44:537–52.
21.
Brown MA, Cunningham MW, Roca AL, Troyer JL, Johnson WE, O’Brien SJ. Genetic characterization of feline leukemia virus from Florida panthers. Emerg Infect Dis. 2008;14:252–9.CrossRefPubMedPubMedCentral
22.
Guimaraes AMS, Brandão PE, de Moraes W, Cubas ZS, Santos LC, Villarreal LYB, Robes RR, Coelho FM, Resende M, Santos RCF, Oliveira RC, Yamaguti M, Marques LM, Neto RL, Buzinhani M, Marques R, Messick JB, Biondo AW, Timenetsky J. Survey of feline leukemia virus and feline coronaviruses in captive neotropical wild felids from southern Brazil. J Zoo Wildl Med. 2009;40:360–4.CrossRefPubMed
23.
Filoni C, Catão-Dias JL, Cattori V, Willi B, Meli ML, Corrêa SHR, Marques MC, Adania CH, Silva JCR, Marvulo MFV, Neto JSF, Durigon EL, Carvalho VM, Coutinho SD, Lutz H, Hofmann-Lehmann R. Surveillance using serological and molecular methods for the detection of infectious agents in captive Brazilian neotropic and exotic felids. J Vet Diagn Investig. 2012;24:166–73.CrossRef
24.
Filoni C, Catão-Dias JL, Bay G, Durigon EL, Jorge RS, Lutz H, Hofmann-Lehmann R. First evidence of feline herpesvirus, calicivirus, parvovirus, and Ehrlichia exposure in Brazilian free-ranging felids. J Wildl Dis. 2006;42:470–7.CrossRefPubMed
25.
Hofmann-Lehmann R, Cattori V, Tandon R, Boretti FS, Meli ML, Riond B, Lutz H. How molecular methods change our views of FeLV infection and vaccination. Vet Immunol Immunopathol. 2008;123:119–123.
26.
Hofmann-Lehmann R, Cattori V, Tandon R, Boretti FS, Meli ML, Riond B, Pepin AC, Willi B, Ossent P, Lutz H. Vaccination against the feline leukaemia virus: outcome and response categories and long-term follow-up. Vaccine. 2007;25:5531–9.CrossRefPubMed
27.
Major A, Cattori V, Boenzli E, Riond B, Ossent P, Meli ML, Hofmann-Lehmann R, Lutz H. Exposure of cats to low doses of FeLV: seroconversion as the sole parameter of infection. Vet Res. 2010;41:17.CrossRefPubMed
28.
Torres AN, Mathiason CK, Hoover EA. Re-examination of feline leukemia virus: host relationships using real-time PCR. Virology. 2005;332:272–83.CrossRefPubMed
29.
Cattori V, Pepin AC, Tandon R, Riond B, Meli ML, Willi B, Lutz H, Hofmann-Lehmann R. Real-time PCR investigation of feline leukemia virus proviral and viral RNA loads in leukocyte subsets. Vet Immunol Immunopathol. 2008;123:124–8.CrossRefPubMed
30.
Tandon R, Cattori V, Gomes-Keller MA, Meli ML, Golder MC, Lutz H, Hofmann-Lehmann R. Quantitation of feline leukaemia virus viral and proviral loads by TaqMan real-time polymerase chain reaction. J Virol Methods. 2005;130:124–32.CrossRefPubMed
31.
Pepin AC, Tandon R, Cattori V, Niederer E, Riond B, Willi B, Lutz H, Hofmann-Lehmann R. Cellular segregation of feline leukemia provirus and viral RNA in leukocyte subsets of long-term experimentally infected cats. Virus Res. 2007;127:9–16.CrossRefPubMed
32.
Boenzli E, Hadorn M, Hartnack S, Huder J, Hofmann-Lehmann R, Lutz H. Detection of antibodies to the feline leukemia virus (FeLV) transmembrane protein p15E: an alternative approach for serological FeLV detection based on antibodies to p15E. J Clin Microbiol. 2014;52:2046–52.
33.
Nesina S, Helfer-Hungerbuehler AK, Riond B, Boretti FS, Willi B, Meli ML, Grest P, Hofmann-Lehmann R. Retroviral DNA - the Silent Winner: Blood Transfusion Containing Latent Feline Leukemia Provirus Causes Infection and Disease in Naïve recipient cats. Retrovirology 12. BioMed Central. 2015;105 https://​doi.​org/​10.​1186/​s12977-015-0231-z.
34.
Hsu SM, Raine L, Fanger H. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem. 1981;29:577–80.CrossRefPubMed
35.
Kipar A, Kremendahl J, Grant CK, von Bothmer I, Reinacher M. Expression of viral proteins in feline leukemia virus-associated enteritis. Vet Pathol. 2000;37:129–36.CrossRefPubMed
36.
37.
38.
Leutenegger CM, Mislin CN, Sigrist B, Ehrengruber MU, Hofmann-Lehmann R, Lutz H. Quantitative real-time PCR for the measurement of feline cytokine mRNA. Vet Immunol Immunopathol. 1999;71:291–305.CrossRefPubMed
39.
Sheets RL, Pandey R, Jen WC, Roy-Burman P. Recombinant feline leukemia virus genes detected in naturally occurring feline lymphosarcomas. J Virol. 1993;67:3118–25.PubMedPubMedCentral
40.
Mathes LE, Pandey R, Chakrabarti R, Hofman FM, Hayes KA, Stromberg P, Roy-Burman P. Pathogenicity of a subgroup C feline leukemia virus (FeLV) is augmented when administered in association with certain FeLV recombinants. Virology. 1994;198:185–95.CrossRefPubMed
41.
Lutz H, Arnold P, Hübscher U, Egberink H, Pedersen N, Horzinek MC. Specificity assessment of feline T-lymphotropic lentivirus serology. Zentralbl Veterinarmed B. 1988;35:773–8.PubMed
42.
Allenspach K, Amacker M, Leutenegger CM, Hottiger M, Hofmann-Lehmann R, Hübscher U, Pistello M, Lutz H. Quantification of proviral FIV DNA using competitive PCR. Schweiz Arch Tierheilkd. 1996;138:87–92.PubMed
43.
Klein D, Leutenegger CM, Bahula C, Gold P, Hofmann-Lehmann R, Salmons B, Lutz H, Gunzburg WH. Influence of preassay and sequence variations on viral load determination by a multiplex real-time reverse transcriptase-polymerase chain reaction for feline immunodeficiency virus. J Acquir Immune Defic Syndr. 2001;26:8–20.CrossRefPubMed
44.
Tandon R, Cattori V, Willi B, Lutz H, Hofmann-Lehmann R. Association between endogenous feline leukemia virus loads and exogenous feline leukemia virus infection in domestic cats. Virus Res. 2008;135:136–43.CrossRefPubMed
45.
46.
Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994;22:4673–80.CrossRefPubMedPubMedCentral
47.
Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4:406–25.PubMed
48.
Nei M, Kumar S. Phylogenetic inference: maximum parsimony methods. In: Nei M, Kumar S, editors. Molecular evolution and Phylogenetics. New York: Oxford University Press Inc.; 2000.
49.
Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution. 1985;39:783–91.CrossRefPubMed
50.
Hofmann-Lehmann R, Huder JB, Gruber S, Boretti F, Sigrist B, Lutz H. Feline leukaemia provirus load during the course of experimental infection and in naturally infected cats. J Gen Virol. 2001;82:1589–96.CrossRefPubMed
51.
Helfer-Hungerbuehler AK, Widmer S, Kessler Y, Riond B, Boretti FS, Grest P, Lutz H, Hofmann-Lehmann R. Long-term follow up of feline leukemia virus infection and characterization of viral RNA loads using molecular methods in tissues of cats with different infection outcomes. Virus Res. 2015;197:137–50.CrossRefPubMed
52.
Johnson WE, Eizirik E, Pecon-Slattery J, Murphy WJ, Antunes A, Teeling E, O’Brien SJ. The late Miocene radiation of modern Felidae: a genetic assessment. Science. 2006;311:73–7.CrossRefPubMed
53.
Hartmann K. Clinical aspects of feline immunodeficiency and feline leukemia virus infection. Vet Immunol Immunopathol. 2011;143:190–201.CrossRefPubMed
54.
Marker L, Munson L, Basson PA, Quackenbush S. Multicentric T-cell lymphoma associated with feline leukemia virus infection in a captive Namibian cheetah (Acinonyx jubatus). J Wildl Dis. 2003;39:690–5.CrossRefPubMed
55.
Harrison TM, McKnight CA, Sikarskie JG, Kitchell BE, Garner MM, Raymond JT, Fitzgerald SD, Valli VE, Agnew D, Kiupel M. Malignant lymphoma in African lions (Panthera leo). Vet Pathol. 2010;47:952–7.CrossRefPubMed
56.
Kaye S, Wang W, Miller C, McLuckie A, Beatty JA, Grant CK, VandeWoude S, Bielefeldt-Ohmann H. Role of feline immunodeficiency virus in lymphomagenesis - going alone or colluding? ILAR J. 2016;57:24–33.CrossRefPubMed
57.
Helfer-Hungerbuehler AK, Cattori V, Bachler B, Hartnack S, Riond B, Ossent P, Lutz H, Hofmann-Lehmann R. Quantification and molecular characterization of the feline leukemia virus A receptor. Infect Genet Evol. 2011;11:1940–50.CrossRef
58.
59.
Coelho FM, Bomfim MR, de Andrade CF, Ribeiro NA, Luppi MM, Costa EA, Oliveira ME, da Fonseca FG, Resende M. Naturally occurring feline leukemia virus subgroup A and B infections in urban domestic cats. J Gen Virol. 2008;89:2799–805.CrossRefPubMed
60.
Hoover EA, Mullins JI, Quackenbush SL, Gasper PW. Experimental transmission and pathogenesis of immunodeficiency syndrome in cats. Blood. 1987;70:1880–92.PubMed
61.
Donahue PR, Hoover EA, Beltz GA, Riedel N, Hirsch VM, Overbaugh J, Mullins JI. Strong sequence conservation among horizontally transmissible, minimally pathogenic feline leukemia viruses. J Virol. 1988;62:722–31.PubMedPubMedCentral
62.
Simon F, Cassaro K, Quillen P. Small felid breeding project at Sao Paulo zoo. Int Zoo Yearb. 1997;35:159–64.CrossRef
63.
Chandhasin C, Coan PN, Levy LS. Subtle mutational changes in the SU protein of a natural feline leukemia virus subgroup A isolate alter disease spectrum. J Virol. 2005;79:1351–60.CrossRefPubMedPubMedCentral
64.
Lehmann R, Franchini M, Aubert A, Wolfensberger C, Cronier J, Lutz H. Vaccination of cats experimentally infected with feline immunodeficiency virus, using a recombinant feline leukemia virus vaccine. J Am Vet Med Assoc. 1991;199:1446–52.PubMed
65.
Hofmann-Lehmann R, Holznagel E, Aubert A, Ossent P, Reinacher M, Lutz H. Recombinant FeLV vaccine: long-term protection and effect on course and outcome of FIV infection. Vet Immunol Immunopathol. 1995;46:127–37.CrossRefPubMed
66.
Lutz H, Pedersen NC, Durbin R, Theilen GH. Monoclonal antibodies to three epitopic regions of feline leukemia virus p27 and their use in enzyme-linked immunosorbent assay of p27. J Immunol Methods. 1983;56:209–20.CrossRefPubMed
Metadata
Title
Putative progressive and abortive feline leukemia virus infection outcomes in captive jaguarundis (Puma yagouaroundi)
Authors
Claudia Filoni
A. Katrin Helfer-Hungerbuehler
José Luiz Catão-Dias
Mara Cristina Marques
Luciana Neves Torres
Manfred Reinacher
Regina Hofmann-Lehmann
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2017
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-017-0889-z

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