Molecular epidemiology of the Bacillus anthracis isolates collected throughout Turkey from 1983 to 2011

  • R. Durmaz
  • M. Doganay
  • M. Sahin
  • D. Percin
  • M. K. Karahocagil
  • U. Kayabas
  • B. Otlu
  • A. Karagoz
  • F. Buyuk
  • O. Celebi
  • Z. Ozturk
  • M. Ertek
  • Anthrax Study Group


The main perspective of this study was to determine cross-transmissions amongst anthrax cases and provide detailed information regarding the genotypes of Bacillus anthracis isolates circulating in Turkey. A total of 251 B. anthracis isolates were obtained from human (93 isolates), animal (155 isolates), and environmental (three isolates) samples in various provinces of Turkey. All isolates were susceptible to quinolones, vancomycin, tigecycline, and linezolid, but not to ceftriaxone. Excluding human isolates, one of the animal isolates was found to be resistant to penicillin, erythromycin, and doxycycline. Multiple-locus variable-number tandem repeats analysis including 8 loci (MLVA8) revealed 12 genotypes, in which genotype 43 was observed at the highest frequency (41.8 %), followed by genotype 35 (25.5 %) and genotype 27 (10.4 %). Major subtype A3.a was the predominant cluster, including 86.8 % of the isolates. The MLVA25 analysis for the 251 isolates yielded 62 different genotypes, 33 of which had only one isolate, while the remaining 29 genotypes had 2 to 43 isolates, with a total of 218 isolates (86.9 %). These findings indicate very high cross-transmission rates within anthrax cases in Turkey. The genotypes diagnosed in Turkey are populated in the A major cluster. Penicillin prescribed as the first-choice antibiotic for the treatment of anthrax is still effective.

Supplementary material

10096_2012_1628_MOESM1_ESM.docx (144 kb)
Additional File 1This file contains a dendrogram of the 62 different MLVA25 genotypes of the 251 Bacillus anthracis isolates from Turkey. (DOCX 144 kb)


  1. 1.
    Schmid G, Kaufmann A (2002) Anthrax in Europe: its epidemiology, clinical characteristics, and role in bioterrorism. Clin Microbiol Infect 8:479–488PubMedCrossRefGoogle Scholar
  2. 2.
    Turnbull PCB, Böhm R, Cosivi O, Doganay M, Hugh-Jones ME, Joshi DD, Lalitha MK, de Vos V (1998) Guidelines for the surveillance and control of anthrax in humans and animals, 3rd edn. World Health Organization (WHO), GenevaGoogle Scholar
  3. 3.
    Centers for Disease Control and Prevention (CDC) Q & A: anthrax and animal hide drums. Available online at:
  4. 4.
    Sweeney DA, Hicks CW, Cui X, Li Y, Eichacker PQ (2011) Anthrax infection. Am J Respir Crit Care Med 184(12):1333–1341PubMedCrossRefGoogle Scholar
  5. 5.
    Doganay M, Metan G (2009) Human anthrax in Turkey from 1990 to 2007. Vector Borne Zoonotic Dis 9(2):131–140PubMedCrossRefGoogle Scholar
  6. 6.
  7. 7.
    Turkish Ministry of Health, Basic Health Services General Directorate, Department of Zoonotic Diseases. Available online at: Accessed 1 May 2012
  8. 8.
    Kaya A, Tasyaran MA, Erol S, Ozkurt Z, Ozkan B (2002) Anthrax in adults and children: a review of 132 cases in Turkey. Eur J Clin Microbiol Infect Dis 21:258–261PubMedCrossRefGoogle Scholar
  9. 9.
    Ozkurt Z, Parlak M, Tastan R, Dinler U, Saglam YS, Ozyurek SF (2005) Anthrax in eastern Turkey, 1992–2004. Emerg Infect Dis 11(12):1939–1941PubMedCrossRefGoogle Scholar
  10. 10.
    Ertek M (2011) Current situation of anthrax in Turkey. ANKEM Derg 25(Suppl 2):88–91Google Scholar
  11. 11.
    World Organisation for Animal Health (OIE). Annual animal disease status. Available online at:
  12. 12.
    Keim P, Price LB, Klevytska AM, Smith KL, Schupp JM, Okinaka R, Jackson PJ, Hugh-Jones ME (2000) Multiple-locus variable-number tandem repeat analysis reveals genetic relationships within Bacillus anthracis. J Bacteriol 182:2928–2936PubMedCrossRefGoogle Scholar
  13. 13.
    Keim P, Van Ert MN, Pearson T, Vogler AJ, Huynh LY, Wagner DM (2004) Anthrax molecular epidemiology and forensics: using the appropriate marker for different evolutionary scales. Infect Genet Evol 4:205–213PubMedCrossRefGoogle Scholar
  14. 14.
    Lista F, Faggioni G, Valjevac S, Ciammaruconi A, Vaissaire J, le Doujet C, Gorgé O, De Santis R, Carattoli A, Ciervo A, Fasanella A, Orsini F, D’Amelio R, Pourcel C, Cassone A, Vergnaud G (2006) Genotyping of Bacillus anthracis strains based on automated capillary 25-loci multiple locus variable-number tandem repeats analysis. BMC Microbiol 6:33. doi:10.1186/1471-2180-6-33 PubMedCrossRefGoogle Scholar
  15. 15.
    Merabishvili M, Natidze M, Rigvava S, Brusetti L, Raddadi N, Borin S, Chanishvili N, Tediashvili M, Sharp R, Barbeschi M, Visca P, Daffonchio D (2006) Diversity of Bacillus anthracis strains in Georgia and of vaccine strains from the Former Soviet Union. Appl Environ Microbiol 72(8):5631–5536PubMedCrossRefGoogle Scholar
  16. 16.
    Ryu C, Lee K, Hawng HJ, Yoo CK, Seong WK, Oh HB (2005) Molecular characterization of Korean Bacillus anthracis isolates by amplified fragment length polymorphism analysis and multilocus variable-number tandem repeat analysis. Appl Environ Microbiol 71:4664–4671PubMedCrossRefGoogle Scholar
  17. 17.
    Simonson TS, Okinaka RT, Wang B, Easterday WR, Huynh L, U’Ren JM, Dukerich M, Zanecki SR, Kenefic LJ, Beaudry J, Schupp JM, Pearson T, Wagner DM, Hoffmaster A, Ravel J, Keim P (2009) Bacillus anthracis in China and its relationship to worldwide lineages. BMC Microbiol 9:71. doi:10.1186/1471-2180-9-71 PubMedCrossRefGoogle Scholar
  18. 18.
    Ortatatli M, Karagoz A, Percin D, Kenar L, Kilic S, Durmaz R (2012) Antimicrobial susceptibility and molecular subtyping of 55 Turkish Bacillus anthracis strains using 25-loci multiple-locus VNTR analysis. Comp Immunol Microbiol Infect Dis 2012 Mar 22. [Epub ahead of print]Google Scholar
  19. 19.
    Mohammed MJ, Marston CK, Popovic T, Weyant RS, Tenover FC (2002) Antimicrobial susceptibility testing of Bacillus anthracis: comparison of results obtained by using the National Committee for Clinical Laboratory Standards broth microdilution reference and Etest agar gradient diffusion methods. J Clin Microbiol 40:1902–1907PubMedCrossRefGoogle Scholar
  20. 20.
    Doganay M (2003) Anthrax. In: Cohen J, Powderly WG (eds) Infectious diseases, vol 2, 2nd edn. American Society for Microbiology Press, Washington, pp 1257–1261Google Scholar
  21. 21.
    Esel D, Doganay M, Sumerkan B (2003) Antimicrobial susceptibilities of 40 isolates of Bacillus anthracis isolated in Turkey. Int J Antimicrob Agents 22(1):70–72PubMedCrossRefGoogle Scholar
  22. 22.
    Luna VA, King DS, Gulledge J, Cannons AC, Amuso PT, Cattani J (2007) Susceptibility of Bacillus anthracis, Bacillus cereus, Bacillus mycoides, Bacillus pseudomycoides and Bacillus thuringiensis to 24 antimicrobials using Sensititre automated microbroth dilution and Etest agar gradient diffusion methods. J Antimicrob Chemother 60(3):555–567PubMedCrossRefGoogle Scholar
  23. 23.
    Cavallo JD, Ramisse F, Girardet M, Vaissaire J, Mock M, Hernandez E (2002) Antibiotic susceptibilities of 96 isolates of Bacillus anthracis isolated in France between 1994 and 2000. Antimicrob Agents Chemother 46(7):2307–2309PubMedCrossRefGoogle Scholar
  24. 24.
    Odendaal MW, Pieterson PM, de Vos V, Botha AD (1991) The antibiotic sensitivity patterns of Bacillus anthracis isolated from the Kruger National Park. Onderstepoort J Vet Res 58(1):17–19PubMedGoogle Scholar
  25. 25.
    Doganay M, Aydın N (1991) Antimicrobial susceptibility of Bacillus anthracis. Scand J Infect Dis 23(3):333–335PubMedCrossRefGoogle Scholar
  26. 26.
    Aikembayev AM, Lukhnova L, Temiraliyeva G, Meka-Mechenko T, Pazylov Y, Zakaryan S, Denissov G, Easterday WR, Van Ert MN, Keim P, Francesconi SC, Blackburn JK, Hugh-Jones M, Hadfield T (2010) Historical distribution and molecular diversity of Bacillus anthracis, Kazakhstan. Emerg Infect Dis 16(5):789–796PubMedCrossRefGoogle Scholar
  27. 27.
    Antwerpen M, Ilin D, Georgieva E, Meyer H, Savov E, Frangoulidis D (2011) MLVA and SNP analysis identified a unique genetic cluster in Bulgarian Bacillus anthracis strains. Eur J Clin Microbiol Infect Dis 30(7):923–930PubMedCrossRefGoogle Scholar
  28. 28.
    Fasanella A, Van Ert M, Altamura SA, Garofolo G, Buonavoglia C, Leori G, Huynh L, Zanecki S, Keim P (2005) Molecular diversity of Bacillus anthracis in Italy. J Clin Microbiol 43(7):3398–3401PubMedCrossRefGoogle Scholar
  29. 29.
    Okutani A, Tungalag H, Boldbaatar B, Yamada A, Tserennorov D, Otgonchimeg I, Erdenebat A, Otgonbaatar D, Inoue S (2011) Molecular epidemiological study of Bacillus anthracis isolated in Mongolia by multiple-locus variable-number tandem-repeat analysis for 8 loci (MLVA-8). Jpn J Infect Dis 64(4):345–348PubMedGoogle Scholar
  30. 30.
    Merabishvili M, Natidze M, Rigvava S, Brusetti L, Raddadi N, Borin S, Chanishvili N, Tediashvili M, Sharp R, Barbeschi M, Visca P, Daffonchio D (2006) Diversity of Bacillus anthracis strains in Georgia and of vaccine strains from the former Soviet Union. Appl Environ Microbiol 72(8):5631–5636PubMedCrossRefGoogle Scholar
  31. 31.
    Pilo P, Perreten V, Frey J (2008) Molecular epidemiology of Bacillus anthracis: determining the correct origin. Appl Environ Microbiol 74(9):2928–2931PubMedCrossRefGoogle Scholar
  32. 32.
    Fasanella A, Garofolo G, Galante D, Quaranta V, Palazzo L, Lista F, Adone R, Jones MH (2010) Severe anthrax outbreaks in Italy in 2004: considerations on factors involved in the spread of infection. New Microbiol 33(1):83–86PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • R. Durmaz
    • 1
    • 2
  • M. Doganay
    • 3
  • M. Sahin
    • 4
  • D. Percin
    • 5
  • M. K. Karahocagil
    • 6
  • U. Kayabas
    • 7
  • B. Otlu
    • 8
  • A. Karagoz
    • 2
  • F. Buyuk
    • 4
  • O. Celebi
    • 4
  • Z. Ozturk
    • 9
  • M. Ertek
    • 10
  • Anthrax Study Group
  1. 1.Department of Clinical Microbiology, Medical FacultyKirikkale UniversityKirikkaleTurkey
  2. 2.Molecular Microbiology Research and Application LaboratoryRefik Saydam National Public Health AgencyAnkaraTurkey
  3. 3.Department of Infectious Disease, Medical FacultyErciyes UniversityKayseriTurkey
  4. 4.Department of Microbiology, Veterinary FacultyKafkas UniversityKarsTurkey
  5. 5.Department of Clinical Microbiology, Medical FacultyErciyes UniversityKayseriTurkey
  6. 6.Department of Infectious Disease, Medical Faculty100 Yil UniversityVanTurkey
  7. 7.Department of Infectious Disease, Medical FacultyInonu UniversityMalatyaTurkey
  8. 8.Department of Clinical Microbiology, Medical FacultyInonu UniversityMalatyaTurkey
  9. 9.Department of Infectious Disease, Medical FacultyAtatürk UniversityErzurumTurkey
  10. 10.Refik Saydam National Public Health AgencyAnkaraTurkey

Personalised recommendations