Abstract
The genus Bartonella comprises emerging bacteria that affect humans and other mammals worldwide. Felids represent an important reservoir for several Bartonella species. Domestic cats are the main reservoir of Bartonella henselae, the agent of cat scratch disease (CSD). It can be transmitted directly by scratches and bites from infected cats and via cat fleas. This study aims to investigate the circulation of Bartonella spp. in free-ranging Neotropical wild felids from Southern Brazil using serological and molecular methods. In this study, 53 live-trapped free-ranging wild felids were sampled, 39 Leopardus geoffroyi and 14 Leopardus wiedii, from five municipalities in the Rio Grande, do Sul state, southern Brazil. All captured animals were clinically healthy. Two blood samples of L. geoffroyi were positive, by PCR, for the presence of B. henselae DNA. Conversely, none of L. wiedii blood samples were positive when tested using PCR. Indirect immunofluorescence assay (IFA) showed that 28% of serum samples of wild felids were reactive (seropositive) for B. henselae by immunofluorescence, with titers ranging from 64 to 256. The results presented here provide the first evidence of a Bartonella-enzootic cycle involving L. geoffroyi and L. wiedii, which may account for the spillover of the emerging zoonotic pathogen B. henselae for the indigenous fauna in Southern Brazil.
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Data availability statement
The data that support the findings of this study are available from the corresponding author upon reasonable request.
References
Tompkins DM, Carver S, Jones ME, Krkošek M, Skerratt LF (2015) Emerging infectious diseases of wildlife: a critical perspective. Trends Parasitol 31(4):149–159. https://doi.org/10.1016/j.pt.2015.01.007
Gilbertson ML, Carver S, VandeWoude S, Crooks KR, Lappin MR, Craft ME (2016) Is pathogen exposure spatially autocorrelated? Patterns of pathogens in puma (Puma concolor) and bobcat (Lynx rufus). Ecosphere 7(11):01558. https://doi.org/10.1002/ecs2.1558
Murray M (1999) The parasites, predators, places and people I have known: a great adventure. Vet Parasitol 81(2):149–158. https://doi.org/10.1016/s0304-4017(98)00242-8
Aguirre AA, Tabor GM (2008) Global factors driving emerging infectious diseases. Ann N Y Acad Sci 1149:1–3. https://doi.org/10.1196/annals.1428.052
Woodford MH (2009) Veterinary aspects of ecological monitoring: the natural history of emerging infectious diseases of humans, domestic animals and wildlife. Trop Anim Health Prod 41(7):1023–1033. https://doi.org/10.1007/s11250-008-9269-4
Keesing F, Belden LK, Daszak P, Dobson A, Harvell CD, Holt RD, Hudson P, Jolles A, Jones KE, Mitchell CE, Myers SS, Bogich T, Ostfeld RS (2010) Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468(7324):647–652. https://doi.org/10.1038/nature09575
Thompson RA (2013) Parasite zoonoses and wildlife: one health, spillover and human activity. Int J Parasitol 43(12–13):1079–1088. https://doi.org/10.1016/j.ijpara.2013.06.007
Overbeck GE, Müller SC, Fidelis A, Pfadenhauer J, Pillar VD, Blanco CC et al (2007) Brazil's neglected biome: the South Brazilian Campos. Perspect Plant Ecol Evol Syst 9(2):101–116. https://doi.org/10.1016/j.ppees.2007.07.005
Roesch LFW, Vieira FCB, Pereira VA, Schunemann AL, Teixeira IF, Senna AJT, Stefenon VM (2009) The Brazilian pampa: a fragile biome. Diversity 1(2):182–198. https://doi.org/10.3390/d1020182
Trigo TC, Manoel LdeFR, Kasper CB(2013a) in Mamiferos do Rio Grande so Sul. Weber MDM, Roman C, Cáceres NC. Carnívoros Continentais Pp Em: Mamíferos do Rio Grande do Sul. UFSM
Trigo T, Schneider A, Lehugeur L, Silveira L, Freitas TO, Eizirik E (2013b) Molecular data reveal complex hybridization and a cryptic species of Neotropical wild cat. Curr Biol 23(24):2528–2533. https://doi.org/10.1016/j.cub.2013.10.046
Queirolo D (2016) Diversidade e padrões de distribuição de mamíferos dos campos do Uruguai e sul do Brasil. Bol Soc Zool Uruguay 25:92–247
Peters FB, Mazim FD, Favarini MO, Oliveira T, G. (2017) Leopardus pardalis (Linnaeus, 1758) (Carnivora, Felidae) nos campos do extremo sul do Brasil: expansão ou recolonização do Pampa? Rev Bras Zoociências 18(3):51–60
Kitchener AC, Breitenmoser-Würsten C, Eizirik E, Gentry A, Werdelin L, Wilting A, et al (2017) A revised taxonomy of the Felidae: the final report of the Cat Classification Task Force of the IUCN Cat Specialist Group. Cat News
Dall'Agnol B, Souza UA, Weck B, Trigo TC, Jardim MMA, Costa FB, Labruna MB, Peters FB, Favarini MO, Mazim FD, Ferreira CAS, Reck J (2018) Rickettsia parkeri in free-ranging wild canids from Brazilian Pampa. Transbound Emerg Dis 65(2):224–230. https://doi.org/10.1111/tbed.12743
Souza VK, Dall’Agnol B, Souza UA, Webster A, Peters FB, Favarini MO et al (2019) Detection of Rangelia vitalii (Piroplasmida: Babesiidae) in asymptomatic free-ranging wild canids from the Pampa biome, Brazil. Parasitol Res 118(4):1337–1342. https://doi.org/10.1007/s00436-019-06245-6
Dubey JP, Lappin MR, Kwok OC, Mofya S, Chikweto A, Baffa A et al (2009) Seroprevalence of Toxoplasma gondii and concurrent Bartonella spp., feline immunodeficiency virus, and feline leukemia virus infections in cats from Grenada, West Indies. J Parasitol 95(5):1129–1133. https://doi.org/10.1645/GE-2114.1
Chomel BB, Kikuchi Y, Martenson JS, Roelke-Parker ME, Chang CC, Kasten RW, Foley JE, Laudre J, Murphy K, Swift PK, Kramer VL, O’brien SJ (2004) Seroprevalence of Bartonella infection in American free-ranging and captive pumas (Felis concolor) and bobcats (Lynx rufus). Vet Res 35(2):233–241. https://doi.org/10.1051/vetres:2004001
Filoni C, Catão-Dias JL, Bay G, Durigon EL, Jorge RSP, Lutz H, Hofmann-Lehmann R (2006) First evidence of feline herpesvirus, calicivirus, parvovirus, and Ehrlichia exposure in Brazilian free-ranging felids. J Wildl Dis 42(2):470–477. https://doi.org/10.7589/0090-3558-42.2.470
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, de Carvalho VM, Coutinho SD’A, Lutz H, Hofmann-Lehmann R (2012) Surveillance using serological and molecular methods for the detection of infectious agents in captive Brazilian neotropic and exotic felids. J Vet Diagn Investig 24(1):166–173. https://doi.org/10.1177/1040638711407684
Breitschwerdt EB, Kordick DL (2000) Bartonella infection in animals: carriership, reservoir potential, pathogenicity, and zoonotic potential for human infection. Clin Microbiol Rev 13(3):428–438. https://doi.org/10.1128/cmr.13.3.428-438.2000
Chomel BB, Kasten RW, Sykes JE, Boulouis HJ, Breitschwerdt EB (2003) Clinical impact of persistent Bartonella bacteremia in humans and animals. Ann N Y Acad Sci 990(1):267–278. https://doi.org/10.1111/j.1749-6632.2003.tb07376.x
Chomel BB, Boulouis HJ, Maruyama S, Breitschwerdt EB (2006) Bartonella spp. in pets and effect on human health. Emerg Infect Dis 12(3):389. https://doi.org/10.3201/eid1203.050931
Vayssier-Taussat M, Le Rhun D, Bonnet S, Cotté V (2009) Insights in Bartonella host specificity. Ann N Y Acad Sci 1166:127–132. https://doi.org/10.1111/j.1749-6632.2009.04531.x
André MR, Denardi NCB, de Sousa KCM, Gonçalves LR, Henrique PC, Ontivero CRGR et al (2014) Arthropod-borne pathogens circulating in free-roaming domestic cats in a zoo environment in Brazil. Ticks Tick Borne Dis 5(5):545–551. https://doi.org/10.1016/j.ttbdis.2014.03.011
Guimarães AMS, Brandão PE, Moraes W, Kiihl S, Santos LC, Filoni C et al (2010) Detection of Bartonella spp. in neotropical felids and evaluation of risk factors and hematological abnormalities associated with infection. Vet Microbiol 142(3–4):346–351. https://doi.org/10.1016/j.vetmic.2009.10.002
Pitassi LH, de Paiva Diniz PP, Scorpio DG, Drummond MR, Lania BG et al (2015) Bartonella spp. bacteremia in blood donors from Campinas, Brazil. PLoS Negl Trop Dis 9(1):e0003467. https://doi.org/10.1371/journal.pntd.0003467
Sambrook J, Russel DW (2006) Molecular cloning: a laboratory manual3rd edn, Cold Spring Harbor
Johnson G, Ayers M, McClure SCC, Richardson SE, Tellier R (2003) Detection and identification of Bartonella species pathogenic for humans by PCR amplification targeting the riboflavin synthase gene (ribC). J Clin Microbiol 41(3):1069–1072. https://doi.org/10.1128/jcm.41.3.1069-1072.2003
Norman AF, Regnery R, Jameson P, Greene C, Krause DC (1995) Differentiation of Bartonella-like isolates at the species level by PCR-restriction fragment length polymorphism in the citrate synthase gene. J Clin Microbiol 33(7):1797–1803
Kumar S, Stecher G, Tamura K et al (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Lamas CC, Mares-Guia MA, Rozental T, Moreira N, Favacho AR, Barreira J et al (2010) Bartonella spp. infection in HIV positive individuals, their pets and ectoparasites in Rio de Janeiro, Brazil: serological and molecular study. Acta Trop 115(1–2):137–141. https://doi.org/10.1016/j.actatropica.2010.02.015
Lantos PM, Maggi RG, Ferguson B, Varkey J, Park LP, Breitschwerdt EB, Woods CW (2014) Detection of Bartonella species in the blood of veterinarians and veterinary technicians: a newly recognized occupational hazard? Vector Borne Zoonotic Dis 14(8):563–570. https://doi.org/10.1089/vbz.2013.1512
Kosoy M, Goodrich I (2019) Comparative ecology of Bartonella and Brucella infections in wild carnivores. Front Vet Sci 5:322. https://doi.org/10.3389/fvets.2018.00322
Molia S, Kasten RW, Stuckey MJ, Boulouis HJ, Allen J, Borgo GM et al (2016) Isolation of Bartonella henselae, Bartonella koehlerae subsp. koehlerae, Bartonella koehlerae subsp. bothieri and a new subspecies of B. koehlerae from free-ranging lions (Panthera leo) from South Africa, cheetahs (Acinonyx jubatus) from Namibia and captive cheetahs from California. Epidemiol Infect 144(15):3237–3243. https://doi.org/10.1017/S0950268816001394
Pretorius AM, Kuyl JM, Isherwood DR, Birtles RJ (2004) Bartonella henselae in African lion, South Africa. Emerg Infect Dis 10(12):2257–2258. https://doi.org/10.3201/eid1012.031054
Molia S, Chomel BB, Kasten RW, Leutenegger CM, Steele BR, Marker L, Martenson JS, Keet DF, Bengis RG, Peterson RP, Munson L, O’Brien SJ (2004) Prevalence of Bartonella infection in wild African lions (Panthera leo) and cheetahs (Acinonyx jubatus). Vet Microbiol 100(1–2):31–41. https://doi.org/10.1016/j.vetmic.2004.01.007
Yamamoto K, Chomel BB, Lowenstine LJ, Kikuchi Y, Phillips LG, Barr BC, Swift PK, Jones KR, Riley SPD, Kasten RW, Foley JE, Pedersen NC (1998) Bartonella henselae antibody prevalence in free-ranging and captive wild felids from California. J Wildl Dis 34(1):56–63. https://doi.org/10.7589/0090-3558-34.1.56
Rotstein DS, Taylor SK, Bradley J, Breitschwerdt EB (2000) Prevalence of Bartonella henselae antibody in Florida panthers. J Wildl Dis 36(1):157–160. https://doi.org/10.7589/0090-3558-36.1.157
Mazim FD, Oliveira TG, Soares JBG (2004) Unusual spot patterns in the population of Geoffroy’s cat from southern Brazil: evidence of hybridization with the little spotted cat. Cat News 40:22–23
Tirelli FP, Mazim FD, Crawshaw PG, Albano AP, Espinosa C, Queirolo D et al (2019) Density and spatio-temporal behaviour of Geoffroy’s cats in a human-dominated landscape of southern Brazil. Mamm Biol 99(1):128–135. https://doi.org/10.1016/j.mambio.2019.11.003
Peters FB, Mazim FD, Favarini MO, Soares JBG, de Oliveira TG (2016) Caça preventiva ou retaliativa de felinos por humanos no extremo sul do Brasil Pp. 311–326. En: Castaño-Uribe, C., C. A. Lasso, R. Hoogesteijn, A. Diaz-Pulido y E. Payán (Editores). II. Conflictos entre felinos y humanos en América Latina. Serie Editorial Fauna Silvestre Neotropical. Instituto de Investigación de Recursos Biológicos Alexander von Humboldt (IAvH), Bogotá, D C, Colombia
Espinosa CC, Trigo TC, Tirelli FP, da Silva LG, Eizirik E, Queirolo D, Mazim FD, Peters FB, Favarini MO, de Freitas TRO (2018) Geographic distribution modeling of the Margay (Leopardus wiedii) and jaguarundi (Puma yagouaroundi): a comparative assessment. J Mammal 99(1):252–262. https://doi.org/10.1093/jmammal/gyx152
Staggemeier R, Venker CA, Klein DH, Petry M, Spilki FR, Cantarelli VV (2010) Prevalence of Bartonella henselae and Bartonella clarridgeiae in cats in the south of Brazil: a molecular study. Mem Inst Oswaldo Cruz 105(7):873–878. https://doi.org/10.1590/S0074-02762010000700006
Malheiros J, Costa MM, Do Amaral RB, de Sousa KCM, André MR et al (2016) Identification of vector-borne pathogens in dogs and cats from Southern Brazil. Ticks Tick Borne Dis 7(5):893–900. https://doi.org/10.1016/j.ttbdis.2016.04.007
Guptill L, Slater L, Wu CC, Lin TL, Glickman LT, Welch DF, HogenEsch H (1997) Experimental infection of young specific pathogen-free cats with Bartonella henselae. J Infect Dis 176(1):206–216. https://doi.org/10.1086/514026
Acknowledgments
This work was supported by the Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul (FAPERGS), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Projeto RS Biodiversidade, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), and INCT Entomologia Molecular.
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The authors confirm that the ethical policies of the journal, as noted on the journal’s author guidelines page, have been adhered to and the appropriate ethical review committee approval has been received (CEUA-IPVDF). All the Brazilian National Council on Animal Experimentation (Conselho Nacional de Controle de Experimentação Animal, CONCEA) guidelines for the Care and Use of Laboratory Animals were followed. The study protocol was approved by our Committee for Animal Care and Experimentation (CEUA/IPVDF 28/2014 and PUCRS), ComPesq/UFRGS (37536), and the Brazilian Ministry of the Environment (permit SISBIO 47357-3, SISBIO-56373-1 and SISBIO-36803).
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Souza, U.A., Webster, A., Dall’Agnol, B. et al. Molecular and Serological Survey of the Cat-Scratch Disease Agent (Bartonella henselae) in Free-Ranging Leopardus geoffroyi and Leopardus wiedii (Carnivora: Felidae) From Pampa Biome, Brazil. Microb Ecol 81, 483–492 (2021). https://doi.org/10.1007/s00248-020-01601-x
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DOI: https://doi.org/10.1007/s00248-020-01601-x