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Prevalence, hematological findings and genetic diversity of Bartonella spp. in domestic cats from Valdivia, Southern Chile

Published online by Cambridge University Press:  12 December 2016

ANANDA MÜLLER Open the ORCID record for ANANDA MÜLLER [Opens in a new window] ,
ROMINA WALKER ,
PEDRO BITTENCOURT ,
ROSANGELA ZACARIAS MACHADO ,
JYAN LUCAS BENEVENUTE ,
RENAN BRESSIANI DO AMARAL ,
LUIZ RICARDO GONÇALVES  and
MARCOS ROGÉRIO ANDRÉ
ANANDA MÜLLER*
Affiliation:
Facultad de Ciencias Veterinarias, Instituto de Ciencias Clínicas Veterinarias, Universidad Austral de Chile, Valdivia, Chile
ROMINA WALKER
Affiliation:
Facultad de Ciencias Veterinarias, Instituto de Ciencias Clínicas Veterinarias, Universidad Austral de Chile, Valdivia, Chile
PEDRO BITTENCOURT
Affiliation:
Facultad de Ciencias Veterinarias, Instituto de Ciencias Clínicas Veterinarias, Universidad Austral de Chile, Valdivia, Chile
ROSANGELA ZACARIAS MACHADO
Affiliation:
Departamento de Patologia Veterinária, Faculdade de Ciências Agrárias e Veterinárias, Universidade Estadual Paulista (FCAV/UNESP), Jaboticabal, SP, Brazil
JYAN LUCAS BENEVENUTE
Affiliation:
Departamento de Patologia Veterinária, Faculdade de Ciências Agrárias e Veterinárias, Universidade Estadual Paulista (FCAV/UNESP), Jaboticabal, SP, Brazil
RENAN BRESSIANI DO AMARAL
Affiliation:
Departamento de Patologia Veterinária, Faculdade de Ciências Agrárias e Veterinárias, Universidade Estadual Paulista (FCAV/UNESP), Jaboticabal, SP, Brazil
LUIZ RICARDO GONÇALVES
Affiliation:
Departamento de Patologia Veterinária, Faculdade de Ciências Agrárias e Veterinárias, Universidade Estadual Paulista (FCAV/UNESP), Jaboticabal, SP, Brazil
MARCOS ROGÉRIO ANDRÉ
Affiliation:
Departamento de Patologia Veterinária, Faculdade de Ciências Agrárias e Veterinárias, Universidade Estadual Paulista (FCAV/UNESP), Jaboticabal, SP, Brazil
*
*Corresponding author: A. Müller, Facultad de Ciencias Veterinarias, Instituto de Ciencias Clínicas Veterinarias, Universidad Austral de Chile, Veterinary Hospital UACh, PO Box 567, Valdivia, Chile. E-mail: ananda.muller@uach.cl
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Summary

The present study determined the prevalence, hematological findings and genetic diversity of Bartonella spp. in domestic cats from Valdivia, Southern Chile. A complete blood count and nuoG gene real-time quantitative PCR (qPCR) for Bartonella spp. were performed in 370 blood samples from cats in Valdivia, Southern Chile. nuoG qPCR-positive samples were submitted to conventional PCR for the gltA gene and sequencing for species differentiation and phylogenetic analysis. Alignment of gltA gene was used to calculate the nucleotide diversity, polymorphic level, number of variable sites and average number of nucleotide differences. Bartonella DNA prevalence in cats was 18·1% (67/370). Twenty-nine samples were sequenced with 62·0% (18/29) identified as Bartonella henselae, 34·4% (10/29) as Bartonella clarridgeiae, and 3·4% (1/29) as Bartonella koehlerae. Bartonella-positive cats had low DNA bacterial loads and their hematological parameters varied minimally. Each Bartonella species from Chile clustered together and with other Bartonella spp. described in cats worldwide. Bartonella henselae and B. clarridgeiae showed a low number of variable sites, haplotypes and nucleotide diversity. Bartonella clarridgeiae and B. koehlerae are reported for the first time in cats from Chile and South America, respectively.

Keywords

Bartonella henselaeBartonella clarridgeiaeBartonella koehleraecat scratch diseaseqPCRSouth America
Type
Research Article
Information
Parasitology , Volume 144 , Issue 6 , May 2017 , pp. 773 - 782
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Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

André, M. R., Baccarim Denardi, N. C., Marques de Sousa, K. C., Gonçalves, L. R., Henrique, P. C., Grosse Rossi Ontivero, C. R., Lima Gonzalez, I. H., Cabral Nery, C. V., Fernandes Chagas, C. R., Monticelli, C., Alexandre de Santis, A. C. G. and Machado, R. Z. (2014). Arthropod-borne pathogens circulating in free-roaming domestic cats in a zoo environment in Brazil. Ticks and Tick-borne Diseases 5, 545–551.Google Scholar
André, M. R., Dumler, J. S., Herrera, H. M., Goncalves, L. R., de Sousa, K. C., Scorpio, D. G., de Santis, A. C. G. A., Domingos, I. H., de Macedo, G. C. and Machado, R. Z. (2016). Assessment of a quantitative 5′ nuclease real-time polymerase chain reaction using the nicotinamide adenine dinucleotide dehydrogenase gamma subunit (nuoG) for Bartonella species in domiciled and stray cats in Brazil. Journal of Feline Medicine and Surgery 18, 783–790.Google Scholar
Arvand, M., Feil, E. J., Giladi, M., Boulouis, H. and Viezens, J. (2007). Multi-locus sequence typing of Bartonella henselae isolates from three continents reveals hypervirulent and feline-associated clones. PLoS ONE 2, e1346.Google Scholar
Avidor, B., Graidy, M., Efrat, G., Leibowitz, C., Shapira, G., Schattner, A., Zimhony, O. and Giladi, M. (2004). Bartonella koehlerae, a new cat-associated agent of culture-negative human endocarditis. Journal of Clinical Microbiology 42, 3462–3468.Google Scholar
Bai, Y., Rizzo, M. F., Alvarez, D., Moran, D., Peruski, L. F. and Kosoy, M. (2015). Coexistence of Bartonella henselae and B. clarridgeiae in populations of cats and their fleas in Guatemala. Journal of Vector Ecology 40, 327–332.Google Scholar
Bergh, K., Bevanger, L., Hanssen, I. and Loseth, K. (2002). Low prevalence of Bartonella henselae infections in Norwegian domestic and feral cats. APMIS 110, 309–314.Google Scholar
Billeter, S. A., Gundi, V. A. K. B., Rood, M. P. and Kosoy, M. Y. (2011). Molecular detection and identification of Bartonella species in Xenopsylla cheopis fleas (Siphonaptera: Pulicidae) collected from Rattus norvegicus rats in Los Angeles, California. Applied and Environmental Microbiology 77, 7850–7852.Google Scholar
Birtles, R. J. and Raoult, D. (1996). Comparison of partial citrate synthase gene (gltA) sequences for phylogenetic analysis of Bartonella species. International Journal of Systematic Bacteriology 46, 891–897.Google Scholar
Boulouis, H.-J., Chao-chin, C., Henn, J. B., Kasten, R. W. and Chomel, B. B. (2005). Factors associated with the rapid emergence of zoonotic Bartonella infections. Veterinary Research 36, 383–410.Google Scholar
Braga, M. do S. C. de O., de Paiva Diniz Diniz, P. P. V., André, M. R., de Bortoli, C. P. and Machado, R. Z. (2012). Molecular characterisation of Bartonella species in cats from São Luís, state of Maranhão, north-eastern Brazil. Memorias do Instituto Oswaldo Cruz 107, 772–777.Google Scholar
Breitschwerdt, E. B. (2008). Feline bartonellosis and cat scratch disease. Veterinary Immunology and Immunopathology 123, 167–171.Google Scholar
Breitschwerdt, E. B., Maggi, R. G., Mozayeni, B. R., Hegarty, B. C., Bradley, J. M. and Mascarelli, P. E. (2010 a). PCR amplification of Bartonella koehlerae from human blood and enrichment blood cultures. Parasites and Vectors 3, 1–9.Google Scholar
Breitschwerdt, E. B., Maggi, R. G., Chomel, B. B. and Lappin, M. R. (2010 b). Bartonellosis: an emerging infectious disease of zoonotic importance to animals and human beings. Journal of Veterinary Emergency and Critical Care 20, 8–30.Google Scholar
Bustin, S. A., Benes, V., Garson, J. A., Hellemans, J., Huggett, J., Kubista, M., Mueller, R., Nolan, T., Pfaffl, M. W. and Shipley, G. L. (2009). Special report the MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry 55, 611–622.Google Scholar
Chang, C., Chomel, B. B., Kasten, R. W., Tappero, J. W., Sanchez, M. A. and Koehler, J. E. (2002). Molecular epidemiology of Bartonella henselae infection in human immunodeficiency virus–infected patients and their cat contacts, using pulsed-field gel electrophoresis and genotyping. Journal of Infectious Diseases 186, 1733–1739.Google Scholar
Chomel, B. B. and Kasten, R. W. (2010). Bartonellosis, an increasingly recognized zoonosis. Journal of applied Mycrobiology 109, 743–750.Google Scholar
Chomel, B. B., Abbott, R. C., Kasten, R. W., Floyd-Hawkins, K. A., Kass, P. H., Glaser, C. A., Pedersen, N. C. and Koehler, J. E. (1995). Bartonella henselae prevalence in domestic cats in California: risk factors and association between bacteremia and antibody titers. Journal of Clinical Microbiology 33, 2445–2450.Google Scholar
Chomel, B. B., Carlos, E. T., Kasten, R. W., Yamamoto, K., Chang, C. C., Carlos, R. S., Abenes, M. V. and Pajares, C. M. (1999). Bartonella henselae and Bartonella clarridgeiae infection in domestic cats from The Philippines. American Journal of Tropical Medicine and Hygiene 60, 593–597.Google Scholar
Chomel, B. B., Boulouis, H. J. and Breitschwerdt, E. B. (2004). Cat scratch disease and other zoonotic Bartonella infections. Journal of the American Veterinary Medical Association 224, 1270–1279.Google Scholar
Chomel, B. B., Boulouis, H.-J., Breitschwerdt, E. B., Kasten, R. W., Vayssier-Taussat, M., Birtles, R. J., Koehler, J. E. and Dehio, C. (2009). Ecological fitness and strategies of adaptation of Bartonella species to their hosts and vectors. Veterinary Research 40, 29.Google Scholar
Cicuttin, G. L., Brambati, D. F., De Gennaro, M. F., Carmona, F., Isturiz, M. L., Pujol, L. E., Belerenian, G. C. and Gil, H. (2014). Bartonella spp. in cats from Buenos Aires, Argentina. Veterinary Microbiology 168, 225–228.Google Scholar
Crissiuma, A., Favacho, A., Gershony, L., Mendes-de-Almeida, F., Gomes, R., Rozental, T., Barreira, J., Lemos, E. and Labarthe, N. (2011). Prevalence of Bartonella species DNA and antibodies in cats (Felis catus) submitted to a spay/neuter program in Rio de Janeiro, Brazil. Journal of Feline Medicine and Surgery 13, 149–151.Google Scholar
de Bortoli, C., André, M., Seki, M., Pinto, A., Machado, S. Z. and Machado, R. Z. (2012). Detection of hemoplasma and Bartonella species and co-infection with retroviruses in cats subjected to a spaying/neutering program in Jaboticabal, SP, Brazil. Revista Brasileira de Parasitologia Veterinaria 21, 219–223.Google Scholar
Droz, S., Chi, B., Horn, E., Steigerwalt, A. G., Whitney, A. M. and Brenner, D. J. (1999). Bartonella koehlerae sp. nov., isolated from cats. Journal of Clinical Microbiology 37, 1117–1122.Google Scholar
Fard, M. R. N., Vahedi, S. M., Ashrafi, I., Alipour, F., Sharafi, G., Akbarein, H. and Aldavood, S. J. (2016). Molecular identification and phylogenic analysis of Bartonella henselae isolated from Iranian cats based on glt A gene. Veterinary Research Forum 7, 69–72.Google Scholar
Fenollar, F. and Raoult, D. (2004). Molecular genetic methods for the diagnosis of fastidious microorganisms. APMIS 112, 785–807.Google Scholar
Ferrés, G. M., Abarca, V. K., Prado, D. P., Montecinos, P. L., Navarrete, C. M. and Vial, C. P. A. (2006a). Prevalencia de anticuerpos contra Bartonella henselae en niños, en adolescentes y en una población de riesgo ocupacional en Chile. Revista médica de Chile 134, 863–867.Google Scholar
Ferrés, M., Abarca, K., Godoy, P., García, P., Palavecino, E., Méndez, G., Valdés, A., Ernst, S., Thibaut, J., Koberg, J., Chanqueo, L. and Vial, P. A. (2005). Presence of Bartonella henselae in cats: natural reservoir quantification and human exposition risk of this zoonoses in Chile. Revista médica de Chile 133, 1465–1471.Google Scholar
Ferrés, M., Abarca, V. K., Prado, D. P., Montecinos, P. L., Navarrete, C. M. and Vial, C. P. A. (2006b). Prevalencia de anticuerpos contra Bartonella henselae en niños, en adolescentes y en una población de riesgo ocupacional en Chile. Revista médica de Chile 134, 863–867.Google Scholar
Fleischman, D. A., Chomel, B. B., Kasten, R. W., Stuckey, M. J., Scarlet, J., Liu, H., Boulouis, H., Haddad, N. and Pedersen, N. (2015). Bartonella infection among cats adopted from a San Francisco Shelter, revisited. Applied and Environmental Microbiology 81, 6446–6450.Google Scholar
Guimaraes, A. M. S., Brandão, P. E., Moraes, W., Kiihl, S., Santos, L. C., Filoni, C., Cubas, Z. S., Robes, R. R., Marques, L. M., Neto, R. L., Yamaguti, M., Oliveira, R. C., Catão-Dias, J. L., Richtzenhain, L. J., Messick, J. B., Biondo, A. W. and Timenetsky, J. (2010). Detection of Bartonella spp. in neotropical felids and evaluation of risk factors and hematological abnormalities associated with infection. Veterinary Microbiology 142, 346–351.Google Scholar
Guptill, L., Wu, C., Hogenesch, H., Slater, L., Glickman, N.,Dunham, A., Syme, H. and Glickman, L. (2004). Prevalence, risk factors, and genetic diversity of Bartonella henselae infections in pet cats in four regions of the United States. Journal of Clinical Microbiology 42, 652–659.Google Scholar
Guptill, L., Slater, L., Wu, C. C., Lin, T. L., Glickman, L. T., Welch, D. F. and HogenEsch, H. (1997). Experimental infection of young specific pathogen-free cats with Bartonella henselae . Journal of Infectious Diseases 176, 206–216.Google Scholar
Gutiérrez, R., Morick, D., Gross, I., Winkler, R., Abdeen, Z. and Harrus, S. (2013). Bartonellae in domestic and stray cats from Israel: comparison of bacterial cultures and high-resolution melt real-time PCR as diagnostic methods. Vector-Borne and Zoonotic Diseases 13, 857–864.Google Scholar
Guy, L., Nystedt, B., Sun, Y., Näslund, K., Berglund, E. C. and Andersson, S. G. E. (2012). A genome-wide study of recombination rate variation in Bartonella henselae . BMC evolutionary Biology 12, 65.Google Scholar
Helps, C., Lait, P., Damhuis, A., Björnehammar, U., Bolta, D., Brovida, C., Chabanne, L., Egberink, H., Ferrand, G., Fontbonne, A., Pennisi, M. G., Gruffydd-Jones, T., Gunn-Moore, D., Hartmann, K., Lutz, H., Malandain, E., Möstl, K., Stengel, C., Harbour, D. A. and Graat, E. A. M. (2005). Factors associated with upper respiratory tract disease caused by feline herpesvirus, feline calicivirus, Chlamydophila felis and Bordetella bronchiseptica in cats: experience from 218 European catteries. Veterinary Record 156, 669–673.Google Scholar
Kordick, D. L., Brown, T. T., Shin, K. and Breitschwerdt, E. B. (1999). Clinical and pathologic evaluation of chronic Bartonella henselae or Bartonella clarridgeiae infection in cats. Journal of Clinical Microbiology 37, 1536–1547.Google Scholar
Levy, J. K., Crawford, P. C., Lappin, M. R., Dubovi, E. J., Levy, M. G., Alleman, R., Tucker, S. J. and Clifford, E. L. (2008). Infec tious diseases of dogs and cats on Isabel a Island, Galapagos. Journal of Veterinary Internal Medicine 22, 60–65.Google Scholar
Librado, P. and Rozas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformathics 25, 1451–1452.Google Scholar
Maggi, R. G., Duncan, A. W. and Breitschwerdt, E. B. (2005). Novel chemically modified liquid medium that will support the growth of seven Bartonella species. Journal of Clinical Microbiology 43, 2651–2655.Google Scholar
Maggi, R. G., Mascarelli, P. E., Pultorak, E. L., Hegarty, B. C., Bradley, J. M., Mozayeni, B. R. and Breitschwerdt, E. B. (2011). Bartonella spp. bacteremia in high-risk immunocompetent patients. Diagnostic Microbiology and Infectious Disease 71, 430–437.Google Scholar
Miceli, N. G., Gavioli, F. A., Gonçalves, L. R., André, M. R., Souza, V., Marques de Sousa, K. C. and Machado, R. Z. (2013). Molecular detection of feline arthropod-borne pathogens in cats in Cuiabá, state of Mato Grosso, central-western region of Brazil. Rev Bras Parasitol Vet 22, 385–390.Google Scholar
Miller, M. A., Pfeiffer, W. and Schwartz, T. (2010). Creating the CIPRES science gateway for inference of large phylogenetic trees. In Proceedings of the Gateway, Computing Environments Workshop (GCE), pp. 1–8. New Orleans, LA.Google Scholar
Mogollon-Pasapera, E., Otvos, L., Giordano, A. and Cassone, M. (2009). Bartonella: emerging pathogen or emerging awareness? International Journal of Infectious Diseases 13, 3–8.Google Scholar
O'Reilly, K. L., Bauer, R. W., Freeland, R. L., Foil, L. D., Hughes, K. J., Rohde, K. R., Roy, A. F., Stout, R. W. and Triche, P. C. (1999). Acute clinical disease in cats following infection with a pathogenic strain of Bartonella henselae (LSU16). Infection and immunity 67, 3066–3072.Google Scholar
Pérez, C., Maggi, R., Diniz, P. and Breitschwerdt, E. B. (2011). Molecular and serological diagnosis of Bartonella infection in 61 dogs from the United States. Journal of Veterinary Internal Medicine 25, 805–810.Google Scholar
Pérez-Martínez, L., Venzal, J. M., González-Acuña, D., Portillo, A., Blanco, J. R. and Oteo, J. A. (2009). Bartonella rochalimae and other Bartonella spp. in fleas, Chile. Emerging Infectious Diseases 15, 1150–1152.Google Scholar
Staggemeier, R., Venker, C. A., Klein, D. H., Petry, M., Spilki, F. R. and Cantarelli, V. V. (2010). Prevalence of Bartonella henselae and Bartonella clarridgeiae in cats in the south of Brazil: a molecular study. Memórias do Instituto Oswaldo Cruz 105, 873–878.Google Scholar
Statamakis, A., Hoover, P. and Rougemont, J. (2008). A rapid Bootstrap Algorithm for the RAxML Web Servers. Systematic Biology 57, 758–771.Google Scholar
Thrusfield, M. (2007). Veterinary Epidemiology, 3th Edn. Blackwell Science Ltd, UK.Google Scholar
Troncoso, I., Fischer, C., Arteaga, F., Espinoza, C., Azócar, T. and Abarca, K. (2016). Seroprevalencia de Bartonella henselae en personas con riesgo ocupacional. Revista Chilena de Infectología 33, 355–357.Google Scholar
Zaror, L., Ernst, S., Navarrete, M., Ballesteros, A., Boroschek, D., Ferres, M. and Thibaut, J. (2002). Archivos de medicina Detección serológica de Bartonella henselae en gatos en la ciudad de Valdivia, Chile Serologic detection of Bartonella henselae in cats in the city of Valdivia. Archivos de Medicina Veterinaria 1, 103–110.Google Scholar
Zuñiga, M. L. (2007). Características Demográficas de la población canina y Recuento de la población felina, en la Ciudad de Valdivia, Chile.Google Scholar