Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-26T22:49:18.343Z Has data issue: false hasContentIssue false

Detection of Bartonella spp. in wild carnivores, hyraxes, hedgehog and rodents from Israel

Published online by Cambridge University Press:  13 April 2016

ODELYA MARCIANO
Affiliation:
Koret School of Veterinary Medicine, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, P.O. Box 12, Rehovot 76100, Israel
RICARDO GUTIÉRREZ
Affiliation:
Koret School of Veterinary Medicine, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, P.O. Box 12, Rehovot 76100, Israel
DANNY MORICK
Affiliation:
Koret School of Veterinary Medicine, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, P.O. Box 12, Rehovot 76100, Israel
RONI KING
Affiliation:
Nature Parks Authority, Jerusalem, Israel
YAARIT NACHUM-BIALA
Affiliation:
Koret School of Veterinary Medicine, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, P.O. Box 12, Rehovot 76100, Israel
GAD BANETH
Affiliation:
Koret School of Veterinary Medicine, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, P.O. Box 12, Rehovot 76100, Israel
SHIMON HARRUS*
Affiliation:
Koret School of Veterinary Medicine, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, P.O. Box 12, Rehovot 76100, Israel
*
*Corresponding author: Koret School of Veterinary Medicine, The Hebrew University of Jerusalem, P.O. Box 12, Rehovot 76100, Israel. E-mail: [email protected]

Summary

Bartonella infection was explored in wild animals from Israel. Golden jackals (Canis aureus), red foxes (Vulpes vulpes), rock hyraxes (Procavia capensis), southern white-breasted hedgehogs (Erinaceus concolor), social voles (Microtus socialis), Tristram's jirds (Meriones tristrami), Cairo spiny mice (Acomys cahirinus), house mice (Mus musculus) and Indian crested porcupines (Hystrix indica) were sampled and screened by molecular and isolation methods. Bartonella-DNA was detected in 46 animals: 9/70 (13%) golden jackals, 2/11 (18%) red foxes, 3/35 (9%) rock hyraxes, 1/3 (33%) southern white-breasted hedgehogs, 5/57 (9%) Cairo spiny mice, 25/43 (58%) Tristram's jirds and 1/6 (16%) house mice. Bartonella rochalimae and B. rochalimae-like were widespread among jackals, foxes, hyraxes and jirds. This report represents the first detection of this zoonotic Bartonella sp. in rock hyraxes and golden jackals. Moreover, DNA of Bartonella vinsonii subsp. berkhoffii, Bartonella acomydis, Candidatus Bartonella merieuxii and other uncharacterized genotypes were identified. Three different Bartonella strains were isolated from Tristram's jirds, and several genotypes were molecularly detected from these animals. Furthermore, this study reports the first detection of Bartonella infection in a southern hedgehog. Our study indicates that infection with zoonotic and other Bartonella species is widespread among wild animals and stresses their potential threat to public health.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

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, 34623468.CrossRefGoogle ScholarPubMed
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, 891897.Google Scholar
Birtles, R. J., Harrison, T. G., Saunders, N. A. and Molyneux, D. H. (1995). Proposals to unify the genera Grahamella and Bartonella, with descriptions of Bartonella talpae comb. nov., Bartonella peromysci comb. nov., and three new species, Bartonella grahamii sp. nov., Bartonella taylorii sp. nov., and Bartonella doshiae sp. nov. International Journal of Systematic Bacteriology 45, 18.Google Scholar
Brenner, E. C., Chomel, B. B., Singhasivanon, O. U., Namekata, D. Y., Kasten, R. W., Kass, P. H., Cortes-Vecino, J. A., Gennari, S. M., Rajapakse, R. P., Huong, L. T. and Dubey, J. P. (2013). Bartonella infection in urban and rural dogs from the tropics: Brazil, Colombia, Sri Lanka and Vietnam. Epidemiology and Infection 141, 5461.CrossRefGoogle Scholar
Buffet, J. P., Marsot, M., Vaumourin, E., Gasqui, P., Masseglia, S., Marcheteau, E., Huet, D., Chapuis, J. L., Pisanu, B., Ferquel, E., Halos, L., Vourc'h, G. and Vayssier-Taussat, M. (2012). Co-infection of Borrelia afzelii and Bartonella spp. in bank voles from a suburban forest. Comparative Immunology, Microbiology and Infectious Diseases 35, 583589.Google Scholar
Buffet, J. P., Kosoy, M. and Vayssier-Taussat, M. (2013). Natural history of Bartonella-infecting rodents in light of new knowledge on genomics, diversity and evolution. Future Microbiology 8, 11171128.Google Scholar
Chomel, B. B. and Kasten, R. W. (2010). Bartonellosis, an increasingly recognized zoonosis. Journal of Applied Microbiology 109, 743750.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Chomel, B. B., McMillan-Cole, A. C., Kasten, R. W., Stuckey, M. J., Sato, S., Maruyama, S., Diniz, P. P. and Breitschwerdt, E. B. (2012). Candidatus Bartonella merieuxii, a potential new zoonotic Bartonella species in Canids from Iraq. PLoS Neglected Tropical Diseases 6, e1843.CrossRefGoogle ScholarPubMed
Daly, J. S., Worthington, M. G., Brenner, D. J., Moss, C. W., Hollis, D. G., Weyant, R. S., Steigerwalt, A. G., Weaver, R. E., Daneshvar, M. I. and O'Connor, S. P. (1993). Rochalimaea elizabethae sp. nov. isolated from a patient with endocarditis. Journal of Clinical Microbiology 31, 872881.Google Scholar
Diaz, M. H., Bai, Y., Malania, L., Winchell, J. M. and Kosoy, M. Y. (2012). Development of a novel genus-specific real-time PCR assay for detection and differentiation of Bartonella species and genotypes. Journal of Clinical Microbiology 50, 16451649.Google Scholar
Diniz, P. P., Billeter, S. A., Otranto, D., De Caprariis, D., Petanides, T., Mylonakis, M. E., Koutinas, A. F. and Breitschwerdt, E. B. (2009). Molecular documentation of Bartonella infection in dogs in Greece and Italy. Journal of Clinical Microbiology 47, 15651567.CrossRefGoogle Scholar
Eremeeva, M. E., Gerns, H. L., Lydy, S. L., Goo, J. S., Ryan, E. T., Mathew, S. S., Ferraro, M. J., Holden, J. M., Nicholson, W. L., Dasch, G. A. and Koehler, J. E. (2007). Bacteremia, fever, and splenomegaly caused by a newly recognized Bartonella species. New England Journal of Medicine 356, 23812387.Google Scholar
Gerrikagoitia, X., Gil, H., Garcia-Esteban, C., Anda, P., Juste, R. A. and Barral, M. (2012). Presence of Bartonella species in wild carnivores of northern Spain. Applied and Environmental Microbiology 78, 885888.Google Scholar
Gundi, V. A., Taylor, C., Raoult, D. and La Scola, B. (2009). Bartonella rattaustraliani sp. nov., Bartonella queenslandensis sp. nov. and Bartonella coopersplainsensis sp. nov., identified in Australian rats. International Journal of Systematic and Evolutionary Microbiology 59, 29562961.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, 857864.CrossRefGoogle ScholarPubMed
Gutiérrez, R., Cohen, L., Morick, D., Mumcuoglu, K. Y., Harrus, S. and Gottlieb, Y. (2014 a). Identification of different Bartonella species in the cattle tail louse (Haematopinus quadripertusus) and in cattle blood. Applied and Environmental Microbiology 80, 54775483.CrossRefGoogle ScholarPubMed
Gutiérrez, R., Morick, D., Cohen, C., Hawlena, H. and Harrus, S. (2014 b). The effect of ecological and temporal factors on the composition of Bartonella infection in rodents and their fleas. ISME Journal 8, 15981608.Google Scholar
Gutiérrez, R., Krasnov, B., Morick, D., Gottlieb, Y., Khokhlova, I. S. and Harrus, S. (2015 a). Bartonella infection in rodents and their flea ectoparasites: an overview. Vector Borne and Zoonotic Diseases 15, 2739.CrossRefGoogle ScholarPubMed
Gutiérrez, R., Nachum-Biala, Y. and Harrus, S. (2015 b). Relationship between the Presence of Bartonella Species and Bacterial Loads in Cats and Cat Fleas (Ctenocephalides felis) under Natural Conditions. Applied and Environmental Microbiology 81, 56135621.CrossRefGoogle ScholarPubMed
Harrus, S., Bar-Gal, G. K., Golan, A., Elazari-Volcani, R., Kosoy, M. Y., Morick, D., Avidor, B. and Baneth, G. (2009). Isolation and genetic characterization of a Bartonella strain closely related to Bartonella tribocorum and Bartonella elizabethae in Israeli commensal rats. American Journal of Tropical Medicine and Hygiene 81, 5558.CrossRefGoogle ScholarPubMed
Henn, J. B., Gabriel, M. W., Kasten, R. W., Brown, R. N., Theis, J. H., Foley, J. E. and Chomel, B. B. (2007). Gray foxes (Urocyon cinereoargenteus) as a potential reservoir of a Bartonella clarridgeiae-like bacterium and domestic dogs as part of a sentinel system for surveillance of zoonotic arthropod-borne pathogens in northern California. Journal of Clinical Microbiology 45, 24112418.Google Scholar
Henn, J. B., Chomel, B. B., Boulouis, H. J., Kasten, R. W., Murray, W. J., Bar-Gal, G. K., King, R., Courreau, J. F. and Baneth, G. (2009 a). Bartonella rochalimae in raccoons, coyotes, and red foxes. Emerging Infectious Diseases 15, 19841987.Google Scholar
Henn, J. B., Gabriel, M. W., Kasten, R. W., Brown, R. N., Koehler, J. E., MacDonald, K. A., Kittleson, M. D., Thomas, W. P. and Chomel, B. B. (2009 b). Infective endocarditis in a dog and the phylogenetic relationship of the associated ‘Bartonella rochalimae’ strain with isolates from dogs, gray foxes, and a human. Journal of Clinical Microbiology 47, 787790.Google Scholar
Holmberg, M., Mills, J. N., McGill, S., Benjamin, G. and Ellis, B. A. (2003). Bartonella infection in sylvatic small mammals of central Sweden. Epidemiology and Infection 130, 149157.Google Scholar
Hoss, M. and Paabo, S. (1993). DNA extraction from Pleistocene bones by a silica-based purification method. Nucleic Acids Research 21, 39133914.Google Scholar
Inoue, K., Maruyama, S., Kabeya, H., Hagiya, K., Izumi, Y., Une, Y. and Yoshikawa, Y. (2009). Exotic small mammals as potential reservoirs of zoonotic Bartonella spp. Emerging Infectious Diseases 15, 526532.Google Scholar
Inoue, K., Kabeya, H., Shiratori, H., Ueda, K., Kosoy, M. Y., Chomel, B. B., Boulouis, H. J. and Maruyama, S. (2010). Bartonella japonica sp. nov. and Bartonella silvatica sp. nov., isolated from Apodemus mice. International Journal of Systematic and Evolutionary Microbiology 60, 759763.Google Scholar
Jaffe, C. L., Baneth, G., Abdeen, Z. A., Schlein, Y. and Warburg, A. (2004). Leishmaniasis in Israel and the Palestinian Authority. Trends in Parasitology 20, 328332.CrossRefGoogle ScholarPubMed
Kosoy, M., Hayman, D. T. S. and Chan, K.-S. (2012). Bartonella bacteria in nature: where does population variability end and a species start? Infection, Genetics and Evolution: Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases 12, 894904.Google Scholar
Kosoy, M. Y., Regnery, R. L., Tzianabos, T., Marston, E. L., Jones, D. C., Green, D., Maupin, G. O., Olson, J. G. and Childs, J. E. (1997). Distribution, diversity, and host specificity of Bartonella in rodents from the Southeastern United States. American Journal of Tropical Medicine and Hygiene 57, 578588.Google Scholar
Lin, J. W., Chen, C. Y., Chen, W. C., Chomel, B. B. and Chang, C. C. (2008). Isolation of Bartonella species from rodents in Taiwan including a strain closely related to ‘Bartonella rochalimae’ from Rattus norvegicus . Journal of Medical Microbiology 57, 14961501.CrossRefGoogle ScholarPubMed
Maggi, R. G. and Breitschwerdt, E. B. (2005). Potential limitations of the 16S-23S rRNA intergenic region for molecular detection of Bartonella species. Journal of Clinical Microbiology 43, 11711176.Google Scholar
Morick, D., Baneth, G., Avidor, B., Kosoy, M. Y., Mumcuoglu, K. Y., Mintz, D., Eyal, O., Goethe, R., Mietze, A., Shpigel, N. and Harrus, S. (2009). Detection of Bartonella spp. in wild rodents in Israel using HRM real-time PCR. Veterinary Microbiology 139, 293297.Google Scholar
Morick, D., Krasnov, B. R., Khokhlova, I. S., Shenbrot, G. I., Kosoy, M. Y. and Harrus, S. (2010). Bartonella genotypes in fleas (Insecta: Siphonaptera) collected from rodents in the Negev desert, Israel. Applied and Environmental Microbiology 76, 68646869.Google Scholar
Morick, D., Krasnov, B. R., Khokhlova, I. S., Gottlieb, Y. and Harrus, S. (2011). Investigation of Bartonella acquisition and transmission in Xenopsylla ramesis fleas (Siphonaptera: Pulicidae). Molecular Ecology 20, 28642870.Google Scholar
Nasereddin, A., Risheq, A., Harrus, S., Azmi, K., Ereqat, S., Baneth, G., Salant, H., Mumcuoglu, K. Y. and Abdeen, Z. (2014). Bartonella species in fleas from Palestinian territories: prevalence and genetic diversity. Journal of Vector Ecology: Journal of the Society for Vector Ecology 39, 261270.CrossRefGoogle ScholarPubMed
Ohad, D. G., Morick, D., Avidor, B. and Harrus, S. (2010). Molecular detection of Bartonella henselae and Bartonella koehlerae from aortic valves of Boxer dogs with infective endocarditis. Veterinary Microbiology 141, 182185.Google Scholar
Rasis, M., Rudoler, N., Schwartz, D. and Giladi, M. (2014). Bartonella dromedarii sp. nov. isolated from domesticated camels (Camelus dromedarius) in Israel. Vector Borne and Zoonotic Diseases 14, 775782.Google Scholar
Riess, T., Dietrich, F., Schmidt, K. V., Kaiser, P. O., Schwarz, H., Schafer, A. and Kempf, V. A. J. (2008). Analysis of a novel insect cell culture medium-based growth medium for Bartonella species. Applied and Environmental Microbiology 74, 52245227.CrossRefGoogle ScholarPubMed
Rudoler, N., Rasis, M., Sharir, B., Novikov, A., Shapira, G. and Giladi, M. (2014). First description of Bartonella bovis in cattle herds in Israel. Veterinary Microbiology 173, 110117.Google Scholar
Sato, S., Kabeya, H., Miura, T., Suzuki, K., Bai, Y., Kosoy, M., Sentsui, H., Kariwa, H. and Maruyama, S. (2012). Isolation and phylogenetic analysis of Bartonella species from wild carnivores of the suborder Caniformia in Japan. Veterinary Microbiology 161, 130136.Google Scholar
Sato, S., Kabeya, H., Fujinaga, Y., Inoue, K., Une, Y., Yoshikawa, Y. and Maruyama, S. (2013). Bartonella jaculi sp. nov., Bartonella callosciuri sp. nov., Bartonella pachyuromydis sp. nov. and Bartonella acomydis sp. nov., isolated from wild Rodentia. International Journal of Systematic and Evolutionary Microbiology 63, 17341740.Google Scholar
Schaefer, J. D., Kasten, R. W., Coonan, T. J., Clifford, D. L. and Chomel, B. B. (2011). Isolation or detection of Bartonella vinsonii subspecies berkhoffii and Bartonella rochalimae in the endangered island foxes (Urocyon littoralis). Veterinary Microbiology 154, 135139.CrossRefGoogle ScholarPubMed
Sofer, S., Gutiérrez, R., Morick, D., Mumcuoglu, K. Y. and Harrus, S. (2015). Molecular detection of zoonotic bartonellae (B. henselae, B. elizabethae and B. rochalimae) in fleas collected from dogs in Israel. Medical and Veterinary Entomology 29, 344348.CrossRefGoogle Scholar
Strauss-Ayali, D., Jaffe, C. L., Burshtain, O., Gonen, L. and Baneth, G. (2004). Polymerase chain reaction using noninvasively obtained samples, for the detection of Leishmania infantum DNA in dogs. Journal of Infectious Diseases 189, 17291733.Google Scholar
Svobodova, M., Votypka, J., Peckova, J., Dvorak, V., Nasereddin, A., Baneth, G., Sztern, J., Kravchenko, V., Orr, A., Meir, D., Schnur, L. F., Volf, P. and Warburg, A. (2006). Distinct transmission cycles of Leishmania tropica in 2 adjacent foci, Northern Israel. Emerging Infectious Diseases 12, 18601868.Google Scholar
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 27312739.Google Scholar
Valentine, K. H., Harms, C. A., Cadenas, M. B., Birkenheuer, A. J., Marr, H. S., Braun-McNeill, J., Maggi, R. G. and Breitschwerdt, E. B. (2007). Bartonella DNA in loggerhead sea turtles. Emerging Infectious Diseases 13, 949950.Google Scholar
Vayssier-Taussat, M., Le Rhun, D., Bonnet, S. and Cotte, V. (2009). Insights in Bartonella host specificity. Annals of the New York Academy of Sciences 1166, 127132.CrossRefGoogle ScholarPubMed
Welch, D. F., Carroll, K. C., Hofmeister, E. K., Persing, D. H., Robison, D. A., Steigerwalt, A. G. and Brenner, D. J. (1999). Isolation of a new subspecies, Bartonella vinsonii subsp. arupensis, from a cattle rancher: identity with isolates found in conjunction with Borrelia burgdorferi and Babesia microti among naturally infected mice. Journal of Clinical Microbiology 37, 25982601.Google Scholar
Supplementary material: File

Marciano supplementary material

Tables S1-S2

Download Marciano supplementary material(File)
File 23.5 KB