Bartonella species in wild small mammals in Western Black Sea Region of Turkey

Bekir Çelebı; Alper Karagöz; Mehmet Ali Öktem; Ahmet Çarhan; Ferhat Matur; Nuri Kaan Özkazanç; Cahit Babür; Selçuk Kılıç; Mustafa Sözen; Ahmet Karataş; Rıza Durmaz

doi:10.1501/Vetfak_0000002678

Letter to Editor

Bartonella species in wild small mammals in Western Black Sea Region of Turkey

Year 2015, , 183 - 187, 01.09.2015

Bekir Çelebı Alper Karagöz Mehmet Ali Öktem Ahmet Çarhan Ferhat Matur Nuri Kaan Özkazanç Cahit Babür Selçuk Kılıç Mustafa Sözen Ahmet Karataş Rıza Durmaz

https://doi.org/10.1501/Vetfak_0000002678

Cited By: 12

Abstract

The species within the genus Bartonella are intracellular bacteria causing long-lasting bacteremia in humans and animals. In this study, Bartonella spp. in 173 small mammals, which were Apodemus flavicollis, A. witherbyi, A. uralensis, A. mystacinus, Myodes glareolus, Crocidura suaveolens, Rattus rattus and Rattus norvegicus species captured from Western Black Sea Region of Turkey, were investigated by blood culture and molecular methods. The positivity of Bartonella was 63.6% (110/173) by blood culture of small mammalian. The gltA gene regions for the isolated strains were identified by DNA sequencing analysis. Isolates were identified as Bartonella taylorii, B. birtlesii, B. coopersplainsensis and a zoonotic B. grahamii

Keywords

Bartonella, blood culture, gltA, PCR, rodent

References

Bermond D, Heller R, Barrat F, Delacour G, Dehio C, Alliot A, Monteil H, Chomel B, Boulouis HJ, Piémont Y. (2000): Bartonella birtlesii sp. nov., isolated from small mammals (Apodemus spp.). Int J Syst Evol Microbiol. 6: 1973-9.
Birtles RJ, Harrison TG, Saunders NA, Molyneux DH. (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. Int J Syst Bacteriol. 45: 1-8.
Birtles RJ, Harrison TG, Molyneux DH. (1994): Grahamella in small woodland mammals in the U.K.: isolation, prevalence and host specificity. Ann Trop Med Parasitol. 88: 317-27.
Boulouis HJ, Chang CC, Henn JB, Kasten RW, Chomel BB. (2005): Factors associated with the rapid emergence of zoonotic Bartonella infections. Vet Res. 36: 383-410.
Çelebi B. (2008): Bartonella henselae and its infections. Mikrobiyol Bul. 42: 163-75.
Celebi B, Kilic S, Aydin N, Tarhan G, Carhan A, Babur C. (2009): Investigation of Bartonella henselae in cats in Ankara, Turkey. Zoonoses Public Health. 56: 169-75.
Celebi B, Carhan A, Kilic S, Babur C. (2010): Detection and genetic diversity of Bartonella vinsonii subsp. berkhoffii strains isolated from dogs in Ankara, Turkey. J Vet Med Sci. 72: 969-73.
Chomel, B. B., H. J. Boulouis, and E. B. Breitschwerdt, (2004): Cat scratch disease and other zoonotic Bartonella infections. J. Am. Vet. Med. Assoc. 224, 1270–1279.
Daly, J.S., Worthington, M.G., Brenner, D.J., Moss, C.W., Rochalimaea elizabethae sp. nov. isolated from a patient with endocarditis. J Clin Microbiol. 31: 872–81.
Engbaek K, Lawson PA.(2004): Identification of Bartonella species in rodents, shrews and cats in Denmark: detection of two B. henselae variants, one in cats and the other in the long-tailed field mouse. APMIS. 112: 336-41.
Fenollar, F., Sire, S. and Raoult, D. (2005). Bartonella vinsonii subsp. arupensis as an agent of blood culture– negative endocarditis in a human. J Clin Microbiol 43: 945–7.
Gil H, García-Esteban C, Barandika JF, Peig J, Toledo A, Escudero R, Jado I, Rodríguez-Vargas M, García- Amil C, Lobo B, Roales P, Rodríguez-Moreno I, Olmeda AS, García-Pérez AL, Anda. P. (2010): Variability of Bartonella genotypes among small mammals in Spain. Appl Environ Microbiol. 76: 8062-70.
Gundi, V.A., Taylo,r C., Raoult, D. and La Scola, B. (2009): Bartonella rattaustraliani sp. nov., Bartonella queenslandensis coopersplainsensis sp. nov., identified in Australian rats. Int J Syst Evol Microbiol. 59: 2956-61. Bartonella
Holmberg M, Mills JN, McGill S, Benjamin G, Ellis BA.(2003): Bartonella infection in sylvatic small mammals of central Sweden. Epidemiol Infect. 130: 149-57.
Iralu J, Bai Y, Crook L, Tempest B, Simpson G, Mckenzie T, Koster F. (2006): Rodent-associated Bartonella febrile illness, Southwestern United States. Emerg Infect Dis. 12: 1081-6.
Jiyipong, T., Jittapalapong, S., Morand, S., Raoult, D., Rolain, J.M. (2012): Prevalence and genetic diversity of Bartonella spp. In small mammals from Southeastern Asia. Appl Environ Microbiol. 78: 8463-6.
Karagoz, A., Celebi, B., Simsek, H., Taner, M., Kilic, S., Durmaz, R. and Ertek,M. (2013): Detection of Bartonella spp. in field mice (Microtus socialis) by culture and PCR. Ankara Üniv Vet Fak Derg. 60: 235-239,
Kerkhoff FT, Bergmans AM, van Der Zee A, Rothova A. (1999): Demonstration of Bartonella grahamii DNA in ocular fluids of a patient with neuroretinitis. J Clin Microbiol. 37: 4034-8.
Kilic, S., Celebi, B., Acar, B., Atas, M. (2013): In vitro susceptibility of isolates of Francisella tularensis from Turkey. Scand J Infect Dis. 45: 337-41.
Knap N, Duh D, Birtles R, Trilar T, Petrovec M, Avsic- Zupanc T. (2007): Molecular detection of Bartonella species infecting rodents in Slovenia. FEMS Immunol Med Microbiol. 50: 45-50.
Kosoy, M., Murray, M., Gilmore, R.D., Bai, Y. and Gage, K.L. (2003): Bartonella strains from ground squirrels are identical to Bartonella washoensis isolated from a human patient. J Clin Microbiol 41: 645–50.
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: 1797-803.
Oktem IM, Uyar Y, Dincer E, Gozalan A, Schlegel M, Babur C, Celebi B, Sozen M, Karatas A, Ozkazanc NK, (2014): Dobrava-Belgrade virus in Apodemus flavicollis and A. uralensis mice, Turkey. Emerg Infect Dis. 20: 121- 5.
Reis C, Cote M, Le Rhun D, Lecuelle B, Levin ML, Vayssier-Taussat M, Bonnet SI. (2011): Vector competence of the tick Ixodes ricinus for transmission of Bartonella birtlesii. PLoS Negl Trop Dis. 5: 1186.
Scola, B., Zeaiter, Z., Khamis, A. and Raoult, D. (2003): Gene-sequence-based criteria for species definition in bacteriology: the Bartonella paradigm. Trends Microbiol. 11: 318–321.
Tea A, Alexiou-Daniel S, Papoutsi A, Papa A, Antoniadis A. (2004): Bartonella species isolated from rodents, Greece. Emerg Infect Dis. 10: 963-4
Tsai, Y.L., Chuang, S.T., Chang, C.C., Kass, P.H. and Chomel, B.B. (2010): Bartonella species in small mammals and their ectoparasites in Taiwan. Am J Trop Med Hyg. 83: 917-23.
Welch DF, Carroll KC, Hofmeister EK, Persing DH, Robison DA, Steigerwalt AG, Brenner DJ. (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. J Clin Microbiol.37: 2598-601.
Welc-Faleciak R, Paziewska A, Bajer A, Behnke JM, Siński E. (2008): Bartonella spp. infection in rodents from different habitats in the Mazury Lake District, Northeast Poland. Vector Borne Zoonotic Dis. 8: 467-74.

Batı Karadeniz Bölgesinde yabani küçük memelilerde Bartonella türleri

Year 2015, , 183 - 187, 01.09.2015

Bekir Çelebı Alper Karagöz Mehmet Ali Öktem Ahmet Çarhan Ferhat Matur Nuri Kaan Özkazanç Cahit Babür Selçuk Kılıç Mustafa Sözen Ahmet Karataş Rıza Durmaz

https://doi.org/10.1501/Vetfak_0000002678

Cited By: 12

Abstract

Bartonella genusundaki türler insanlarda ve hayvanlarda uzun süreli bakteriyemiye neden olan hücre içi bakterilerdir. Bu çalışmada Batı Karadeniz Bölgesi’nde yakalanan Apodemus flavicollis, A. witherbyi, A. uralensis, A. mystacinus, Myodes glareolus, Crocidura suaveolens, Rattus rattus ve Rattus norvegicus türlerinin dahil olduğu 173 küçük memelide, kan kültürü ve moleküler yöntemlerle Bartonella türleri araştırıldı. Bartonella pozitifliği küçük memelilerde kan kültürü ile %63.6 (110/173) bulundu. Kültürde izole edilen Bartonella suşlarının, sitrat sentez gen bölgesi (gltA) DNA dizi analizi ile tür tanımlamaları yapıldı. İzolatlar Bartonella taylorii, B. birtlesii, B. coopersplainsensis ve zoonotik bir tür olan B. grahamii olarak tanımlandı

Keywords

Bartonella, gltA, kan kültürü, PCR, rodent

References

Bermond D, Heller R, Barrat F, Delacour G, Dehio C, Alliot A, Monteil H, Chomel B, Boulouis HJ, Piémont Y. (2000): Bartonella birtlesii sp. nov., isolated from small mammals (Apodemus spp.). Int J Syst Evol Microbiol. 6: 1973-9.
Birtles RJ, Harrison TG, Saunders NA, Molyneux DH. (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. Int J Syst Bacteriol. 45: 1-8.
Birtles RJ, Harrison TG, Molyneux DH. (1994): Grahamella in small woodland mammals in the U.K.: isolation, prevalence and host specificity. Ann Trop Med Parasitol. 88: 317-27.
Boulouis HJ, Chang CC, Henn JB, Kasten RW, Chomel BB. (2005): Factors associated with the rapid emergence of zoonotic Bartonella infections. Vet Res. 36: 383-410.
Çelebi B. (2008): Bartonella henselae and its infections. Mikrobiyol Bul. 42: 163-75.
Celebi B, Kilic S, Aydin N, Tarhan G, Carhan A, Babur C. (2009): Investigation of Bartonella henselae in cats in Ankara, Turkey. Zoonoses Public Health. 56: 169-75.
Celebi B, Carhan A, Kilic S, Babur C. (2010): Detection and genetic diversity of Bartonella vinsonii subsp. berkhoffii strains isolated from dogs in Ankara, Turkey. J Vet Med Sci. 72: 969-73.
Chomel, B. B., H. J. Boulouis, and E. B. Breitschwerdt, (2004): Cat scratch disease and other zoonotic Bartonella infections. J. Am. Vet. Med. Assoc. 224, 1270–1279.
Daly, J.S., Worthington, M.G., Brenner, D.J., Moss, C.W., Rochalimaea elizabethae sp. nov. isolated from a patient with endocarditis. J Clin Microbiol. 31: 872–81.
Engbaek K, Lawson PA.(2004): Identification of Bartonella species in rodents, shrews and cats in Denmark: detection of two B. henselae variants, one in cats and the other in the long-tailed field mouse. APMIS. 112: 336-41.
Fenollar, F., Sire, S. and Raoult, D. (2005). Bartonella vinsonii subsp. arupensis as an agent of blood culture– negative endocarditis in a human. J Clin Microbiol 43: 945–7.
Gil H, García-Esteban C, Barandika JF, Peig J, Toledo A, Escudero R, Jado I, Rodríguez-Vargas M, García- Amil C, Lobo B, Roales P, Rodríguez-Moreno I, Olmeda AS, García-Pérez AL, Anda. P. (2010): Variability of Bartonella genotypes among small mammals in Spain. Appl Environ Microbiol. 76: 8062-70.
Gundi, V.A., Taylo,r C., Raoult, D. and La Scola, B. (2009): Bartonella rattaustraliani sp. nov., Bartonella queenslandensis coopersplainsensis sp. nov., identified in Australian rats. Int J Syst Evol Microbiol. 59: 2956-61. Bartonella
Holmberg M, Mills JN, McGill S, Benjamin G, Ellis BA.(2003): Bartonella infection in sylvatic small mammals of central Sweden. Epidemiol Infect. 130: 149-57.
Iralu J, Bai Y, Crook L, Tempest B, Simpson G, Mckenzie T, Koster F. (2006): Rodent-associated Bartonella febrile illness, Southwestern United States. Emerg Infect Dis. 12: 1081-6.
Jiyipong, T., Jittapalapong, S., Morand, S., Raoult, D., Rolain, J.M. (2012): Prevalence and genetic diversity of Bartonella spp. In small mammals from Southeastern Asia. Appl Environ Microbiol. 78: 8463-6.
Karagoz, A., Celebi, B., Simsek, H., Taner, M., Kilic, S., Durmaz, R. and Ertek,M. (2013): Detection of Bartonella spp. in field mice (Microtus socialis) by culture and PCR. Ankara Üniv Vet Fak Derg. 60: 235-239,
Kerkhoff FT, Bergmans AM, van Der Zee A, Rothova A. (1999): Demonstration of Bartonella grahamii DNA in ocular fluids of a patient with neuroretinitis. J Clin Microbiol. 37: 4034-8.
Kilic, S., Celebi, B., Acar, B., Atas, M. (2013): In vitro susceptibility of isolates of Francisella tularensis from Turkey. Scand J Infect Dis. 45: 337-41.
Knap N, Duh D, Birtles R, Trilar T, Petrovec M, Avsic- Zupanc T. (2007): Molecular detection of Bartonella species infecting rodents in Slovenia. FEMS Immunol Med Microbiol. 50: 45-50.
Kosoy, M., Murray, M., Gilmore, R.D., Bai, Y. and Gage, K.L. (2003): Bartonella strains from ground squirrels are identical to Bartonella washoensis isolated from a human patient. J Clin Microbiol 41: 645–50.
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: 1797-803.
Oktem IM, Uyar Y, Dincer E, Gozalan A, Schlegel M, Babur C, Celebi B, Sozen M, Karatas A, Ozkazanc NK, (2014): Dobrava-Belgrade virus in Apodemus flavicollis and A. uralensis mice, Turkey. Emerg Infect Dis. 20: 121- 5.
Reis C, Cote M, Le Rhun D, Lecuelle B, Levin ML, Vayssier-Taussat M, Bonnet SI. (2011): Vector competence of the tick Ixodes ricinus for transmission of Bartonella birtlesii. PLoS Negl Trop Dis. 5: 1186.
Scola, B., Zeaiter, Z., Khamis, A. and Raoult, D. (2003): Gene-sequence-based criteria for species definition in bacteriology: the Bartonella paradigm. Trends Microbiol. 11: 318–321.
Tea A, Alexiou-Daniel S, Papoutsi A, Papa A, Antoniadis A. (2004): Bartonella species isolated from rodents, Greece. Emerg Infect Dis. 10: 963-4
Tsai, Y.L., Chuang, S.T., Chang, C.C., Kass, P.H. and Chomel, B.B. (2010): Bartonella species in small mammals and their ectoparasites in Taiwan. Am J Trop Med Hyg. 83: 917-23.
Welch DF, Carroll KC, Hofmeister EK, Persing DH, Robison DA, Steigerwalt AG, Brenner DJ. (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. J Clin Microbiol.37: 2598-601.
Welc-Faleciak R, Paziewska A, Bajer A, Behnke JM, Siński E. (2008): Bartonella spp. infection in rodents from different habitats in the Mazury Lake District, Northeast Poland. Vector Borne Zoonotic Dis. 8: 467-74.

There are 29 citations in total.

Details

Primary Language	English
Subjects	Veterinary Surgery
Other ID	JA72JT36JY
Journal Section	Research Article
Authors	Bekir Çelebı Alper Karagöz Mehmet Ali Öktem Ahmet Çarhan Ferhat Matur Nuri Kaan Özkazanç Cahit Babür Selçuk Kılıç Mustafa Sözen Ahmet Karataş Rıza Durmaz
Publication Date	September 1, 2015
Published in Issue	Year 2015

Cite

APA	Çelebı, B., Karagöz, A., Öktem, M. A., Çarhan, A., et al. (2015). Bartonella species in wild small mammals in Western Black Sea Region of Turkey. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 62(3), 183-187. https://doi.org/10.1501/Vetfak_0000002678
AMA	Çelebı B, Karagöz A, Öktem MA, Çarhan A, Matur F, Özkazanç NK, Babür C, Kılıç S, Sözen M, Karataş A, Durmaz R. Bartonella species in wild small mammals in Western Black Sea Region of Turkey. Ankara Univ Vet Fak Derg. September 2015;62(3):183-187. doi:10.1501/Vetfak_0000002678
Chicago	Çelebı, Bekir, Alper Karagöz, Mehmet Ali Öktem, Ahmet Çarhan, Ferhat Matur, Nuri Kaan Özkazanç, Cahit Babür, Selçuk Kılıç, Mustafa Sözen, Ahmet Karataş, and Rıza Durmaz. “Bartonella Species in Wild Small Mammals in Western Black Sea Region of Turkey”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 62, no. 3 (September 2015): 183-87. https://doi.org/10.1501/Vetfak_0000002678.
EndNote	Çelebı B, Karagöz A, Öktem MA, Çarhan A, Matur F, Özkazanç NK, Babür C, Kılıç S, Sözen M, Karataş A, Durmaz R (September 1, 2015) Bartonella species in wild small mammals in Western Black Sea Region of Turkey. Ankara Üniversitesi Veteriner Fakültesi Dergisi 62 3 183–187.
IEEE	B. Çelebı, “Bartonella species in wild small mammals in Western Black Sea Region of Turkey”, Ankara Univ Vet Fak Derg, vol. 62, no. 3, pp. 183–187, 2015, doi: 10.1501/Vetfak_0000002678.
ISNAD	Çelebı, Bekir et al. “Bartonella Species in Wild Small Mammals in Western Black Sea Region of Turkey”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 62/3 (September 2015), 183-187. https://doi.org/10.1501/Vetfak_0000002678.
JAMA	Çelebı B, Karagöz A, Öktem MA, Çarhan A, Matur F, Özkazanç NK, Babür C, Kılıç S, Sözen M, Karataş A, Durmaz R. Bartonella species in wild small mammals in Western Black Sea Region of Turkey. Ankara Univ Vet Fak Derg. 2015;62:183–187.
MLA	Çelebı, Bekir et al. “Bartonella Species in Wild Small Mammals in Western Black Sea Region of Turkey”. Ankara Üniversitesi Veteriner Fakültesi Dergisi, vol. 62, no. 3, 2015, pp. 183-7, doi:10.1501/Vetfak_0000002678.
Vancouver	Çelebı B, Karagöz A, Öktem MA, Çarhan A, Matur F, Özkazanç NK, Babür C, Kılıç S, Sözen M, Karataş A, Durmaz R. Bartonella species in wild small mammals in Western Black Sea Region of Turkey. Ankara Univ Vet Fak Derg. 2015;62(3):183-7.