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Abstract

Background

Brucellosis is a bacterial zoonosis causing severe illness in humans and animals and leading to economic losses in the livestock production in Türkiye and other endemic countries.

Aim

We aimed at investigating genomic differences of isolates from animals and humans in Türkiye.

Methods

We used whole genome sequencing (WGS) to assess the genetic diversity of isolates from 41 provinces in Türkiye and compared with isolates from other countries. We applied allele-based typing and core genome single nucleotide polymorphism (cgSNP) determination.

Results

Of the 106 Turkish isolates included, 57 were and 49 were . One and two isolates were identified as vaccine strains. Most (n = 55) isolates clustered in three major branches, with no spatial discernible pattern. Of the isolates 48 were assigned to the Eastern Mediterranean lineage with no discernible patterns between host species, location and sampling date. The Turkish isolates clustered with isolates from neighbouring countries such as Greece and Syria, but some also with isolates from human patients in European countries, like Germany, Norway and Sweden, suggesting that the source may be travel-related.

Conclusion

Several and lineages are circulating in Türkiye. To decrease the prevalence and prevent brucellosis in animals and humans, stricter control measures are needed, particularly in areas where humans and animals have close contact. Furthermore, illegal transportation of animals across borders should be more closely controlled and regulated.

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2024-09-19
2024-09-27
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References

  1. Qureshi KA, Parvez A, Fahmy NA, Abdel Hady BH, Kumar S, Ganguly A, et al. Brucellosis: epidemiology, pathogenesis, diagnosis and treatment-a comprehensive review. Ann Med. 2023;55(2):2295398.  https://doi.org/10.1080/07853890.2023.2295398  PMID: 38165919 
  2. Pappas G, Panagopoulou P, Christou L, Akritidis N. Brucella as a biological weapon. Cell Mol Life Sci. 2006;63(19-20):2229-36.  https://doi.org/10.1007/s00018-006-6311-4  PMID: 16964579 
  3. De Massis F, Zilli K, Di Donato G, Nuvoloni R, Pelini S, Sacchini L, et al. Distribution of Brucella field strains isolated from livestock, wildlife populations, and humans in Italy from 2007 to 2015. PLoS One. 2019;14(3):e0213689.  https://doi.org/10.1371/journal.pone.0213689  PMID: 30901346 
  4. Pappas G, Papadimitriou P, Akritidis N, Christou L, Tsianos EV. The new global map of human brucellosis. Lancet Infect Dis. 2006;6(2):91-9.  https://doi.org/10.1016/S1473-3099(06)70382-6  PMID: 16439329 
  5. Bagheri Nejad R, Krecek RC, Khalaf OH, Hailat N, Arenas-Gamboa AM. Brucellosis in the Middle East: Current situation and a pathway forward. PLoS Negl Trop Dis. 2020;14(5):e0008071.  https://doi.org/10.1371/journal.pntd.0008071  PMID: 32437346 
  6. Laine CG, Johnson VE, Scott HM, Arenas-Gamboa AM. Global estimate of human brucellosis incidence. Emerg Infect Dis. 2023;29(9):1789-97.  https://doi.org/10.3201/eid2909.230052  PMID: 37610167 
  7. Elrashedy A, Gaafar M, Mousa W, Nayel M, Salama A, Zaghawa A, et al. Immune response and recent advances in diagnosis and control of brucellosis. Ger J Vet Res.2022;2(1):10-24.  https://doi.org/10.51585/gjvr.2022.1.0033 
  8. Johansen TB, Scheffer L, Jensen VK, Bohlin J, Feruglio SL. Whole-genome sequencing and antimicrobial resistance in Brucella melitensis from a Norwegian perspective. Sci Rep. 2018;8(1):8538.  https://doi.org/10.1038/s41598-018-26906-3  PMID: 29867163 
  9. Georgi E, Walter MC, Pfalzgraf MT, Northoff BH, Holdt LM, Scholz HC, et al. Whole genome sequencing of Brucella melitensis isolated from 57 patients in Germany reveals high diversity in strains from Middle East. PLoS One. 2017;12(4):e0175425.  https://doi.org/10.1371/journal.pone.0175425  PMID: 28388689 
  10. Yumuk Z, O’Callaghan D. Brucellosis in Turkey -- an overview. Int J Infect Dis. 2012;16(4):e228-35.  https://doi.org/10.1016/j.ijid.2011.12.011  PMID: 22333223 
  11. Vancelik S, Guraksin A, Ayyildiz A. Seroprevalence of human brucellosis in rural endemic areas in eastern Turkey. Trop Doct. 2008;38(1):42-3.  https://doi.org/10.1258/td.2007.060004  PMID: 18302867 
  12. Cetinkol Y, Enginyurt Ö, Çelebi B, Yıldırım AA, Çankaya S, Aktepe OC. Investigation of zoonotic infections in risk groups in Ordu University Hospital, Turkey. Niger J Clin Pract. 2017;20(1):6-11.  https://doi.org/10.4103/1119-3077.181395  PMID: 27958239 
  13. Akar K, Tatar F, Schmoock G, Wareth G, Neubauer H, Erganis O. Tracking the diversity and Mediterranean lineage of Brucella melitensis isolates from different animal species in Turkey using MLVA-16 genotyping. Ger J Vet Res.2022;2(1):25-30.  https://doi.org/10.51585/gjvr.2022.1.0037 
  14. Cross AR, Baldwin VM, Roy S, Essex-Lopresti AE, Prior JL, Harmer NJ. Zoonoses under our noses. Microbes Infect. 2019;21(1):10-9.  https://doi.org/10.1016/j.micinf.2018.06.001  PMID: 29913297 
  15. Khatibi M, Abdulaliyev G, Azimov A, Ismailova R, Ibrahimov S, Shikhiyev M, et al. Working towards development of a sustainable brucellosis control programme, the Azerbaijan example. Res Vet Sci. 2021;137:252-61.  https://doi.org/10.1016/j.rvsc.2021.05.014  PMID: 34049112 
  16. Hull NC, Schumaker BA. Comparisons of brucellosis between human and veterinary medicine. Infect Ecol Epidemiol. 2018;8(1):1500846.  https://doi.org/10.1080/20008686.2018.1500846  PMID: 30083304 
  17. European Food Safety Authority (EFSA)European Centre for Disease Prevention and Control (ECDC). The European Union One Health 2022 Zoonoses Report. EFSA J. 2023;21(12):e8442.  https://doi.org/10.2903/j.efsa.2023.8442  PMID: 38089471 
  18. Garofolo G, Di Giannatale E, De Massis F, Zilli K, Ancora M, Cammà C, et al. Investigating genetic diversity of Brucella abortus and Brucella melitensis in Italy with MLVA-16. Infect Genet Evol. 2013;19:59-70.  https://doi.org/10.1016/j.meegid.2013.06.021  PMID: 23831636 
  19. Vergnaud G, Hauck Y, Christiany D, Daoud B, Pourcel C, Jacques I, et al. Genotypic expansion within the population structure of classical Brucella species revealed by MLVA16 typing of 1404 Brucella isolates from different animal and geographic origins, 1974-2006. Front Microbiol. 2018;9:1545.  https://doi.org/10.3389/fmicb.2018.01545  PMID: 30050522 
  20. Akar K, Erganis O. Evaluation of the genetic profiles of Brucella melitensis strain from Turkey using multilocus variable number tandem repeat analysis (MLVA) and multilocus sequence typing (MLST) techniques. Vet Microbiol. 2022;269:109423.  https://doi.org/10.1016/j.vetmic.2022.109423  PMID: 35462118 
  21. Scholz HC, Vergnaud G. Molecular characterisation of Brucella species. Rev Sci Tech. 2013;32(1):149-62.  https://doi.org/10.20506/rst.32.1.2189  PMID: 23837373 
  22. Foster G, Osterman BS, Godfroid J, Jacques I, Cloeckaert A. Brucella ceti sp. nov. and Brucella pinnipedialis sp. nov. for Brucella strains with cetaceans and seals as their preferred hosts. Int J Syst Evol Microbiol. 2007;57(Pt 11):2688-93.  https://doi.org/10.1099/ijs.0.65269-0  PMID: 17978241 
  23. Holzer K, El-Diasty M, Wareth G, Abdel-Hamid NH, Hamdy MER, Moustafa SA, et al. Tracking the distribution of Brucella abortus in Egypt based on core genome SNP analysis and in silico MLVA-16. Microorganisms. 2021;9(9):1942.  https://doi.org/10.3390/microorganisms9091942  PMID: 34576838 
  24. Brangsch H, Sandalakis V, Babetsa M, Boukouvala E, Ntoula A, Makridaki E, et al. Genotype diversity of brucellosis agents isolated from humans and animals in Greece based on whole-genome sequencing. BMC Infect Dis. 2023;23(1):529.  https://doi.org/10.1186/s12879-023-08518-z  PMID: 37580676 
  25. Akar K, Erganis O. Evaluation of the genetic profiles of Brucella melitensis strain from Turkey using multilocus variable number tandem repeat analysis (MLVA) and multilocus sequence typing (MLST) techniques. Vet Microbiol. 2022;269:109423.  https://doi.org/10.1016/j.vetmic.2022.109423 
  26. Alton GG, Jones LM, Angus R, Verger J. Techniques for the brucellosis laboratory. Paris: Institut National de la Recherche Agronomique (INRA); 1988.
  27. Bricker BJ, Halling SM. Enhancement of the Brucella AMOS PCR assay for differentiation of Brucella abortus vaccine strains S19 and RB51. J Clin Microbiol. 1995;33(6):1640-2.  https://doi.org/10.1128/jcm.33.6.1640-1642.1995  PMID: 7650203 
  28. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19(5):455-77.  https://doi.org/10.1089/cmb.2012.0021  PMID: 22506599 
  29. Wood DE, Lu J, Langmead B. Improved metagenomic analysis with Kraken 2. Genome Biol. 2019;20(1):257.  https://doi.org/10.1186/s13059-019-1891-0  PMID: 31779668 
  30. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics. 2013;29(8):1072-5.  https://doi.org/10.1093/bioinformatics/btt086  PMID: 23422339 
  31. Whatmore AM, Perrett LL, MacMillan AP. Characterisation of the genetic diversity of Brucella by multilocus sequencing. BMC Microbiol. 2007;7(1):34.  https://doi.org/10.1186/1471-2180-7-34  PMID: 17448232 
  32. Jolley KA, Bray JE, Maiden MCJ. Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications. Wellcome Open Res. 2018;3:124.  https://doi.org/10.12688/wellcomeopenres.14826.1  PMID: 30345391 
  33. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30(9):1312-3.  https://doi.org/10.1093/bioinformatics/btu033  PMID: 24451623 
  34. Tan KK, Tan YC, Chang LY, Lee KW, Nore SS, Yee WY, et al. Full genome SNP-based phylogenetic analysis reveals the origin and global spread of Brucella melitensis. BMC Genomics. 2015;16(1):93.  https://doi.org/10.1186/s12864-015-1294-x  PMID: 25888205 
  35. Argimón S, Abudahab K, Goater RJE, Fedosejev A, Bhai J, Glasner C, et al. Microreact: visualizing and sharing data for genomic epidemiology and phylogeography. Microb Genom. 2016;2(11):e000093.  https://doi.org/10.1099/mgen.0.000093  PMID: 28348833 
  36. Akar K, Tatar F, Schmoock G, Wareth G, Neubauer H, Erganiş O. Tracking the diversity and Mediterranean lineage of Brucella melitensis isolates from different animal species in Turkey using MLVA-16 genotyping. Ger J Vet Res.2022;2(1):25-30.  https://doi.org/10.51585/gjvr.2022.1.0037 
  37. Pelerito A, Nunes A, Grilo T, Isidro J, Silva C, Ferreira AC, et al. Genetic characterization of Brucella spp.: whole genome sequencing-based approach for the determination of multiple locus variable number tandem repeat profiles. Front Microbiol. 2021;12:740068.  https://doi.org/10.3389/fmicb.2021.740068  PMID: 34867857 
  38. Pearson T, Busch JD, Ravel J, Read TD, Rhoton SD, U’Ren JM, et al. Phylogenetic discovery bias in Bacillus anthracis using single-nucleotide polymorphisms from whole-genome sequencing. Proc Natl Acad Sci USA. 2004;101(37):13536-41.  https://doi.org/10.1073/pnas.0403844101  PMID: 15347815 
  39. Uysal Y. Field experience with Rev.1 vaccine in Turkey. Alfort: FAO/WHO/OIE Round Table on the use of Rev.1 Vaccine in Small Ruminants and Cattle; 1995. Available from: https://www.fao.org/4/ai494e/ai494e00.pdf
  40. Blasco JM, Moreno E, Moriyón I. Efficacy of Brucella abortus S19 and RB51 vaccine strains: A systematic review and meta-analysis. Transbound Emerg Dis. 2022;69(4):1670-3.  https://doi.org/10.1111/tbed.14440  PMID: 34964556 
  41. Daskiran I, Savas T, Koyuncu M, Koluman N, Keskin M, Esenbuga N, et al. Goat production systems of Turkey: nomadic to industrial. Small Rumin Res. 2018;163:15-20.  https://doi.org/10.1016/j.smallrumres.2017.10.001 
  42. Gürbilek SE, Baklan EA, Sağlam G, Karagül MS, Saytekin AM. Conventional and molecular identification of Brucella isolates from livestock in Turkey. Ankara Univ Vet Fak Derg. 2022;69(3):297-302.  https://doi.org/10.33988/auvfd.796785 
  43. Wareth G, El-Diasty M, Melzer F, Schmoock G, Moustafa SA, El-Beskawy M, et al. MLVA-16 Genotyping of Brucella abortus and Brucella melitensis isolates from different animal species in Egypt: geographical relatedness and the Mediterranean lineage. Pathogens. 2020;9(6):498.  https://doi.org/10.3390/pathogens9060498  PMID: 32580472 
  44. İkikat Tümer E, Ağır HB, Aydoğan İ. Evaluating technical efficiency of hair goat farms in Turkey: the case of Mersin Province. Trop Anim Health Prod. 2020;52(6):3707-12.  https://doi.org/10.1007/s11250-020-02407-2  PMID: 33026611 
  45. Akbay C, Akdoğan F. Structure of dairy cattle holdings and market supply of milk: the case of İzmir Province, Turkey. Turk J Agric Res.2020;7(3):287-95.
  46. Tuncay RM, Sancak YC. Presence of Listeria monocytogenes in herby cheese and determination of their susceptibility to antibiotics. Van Vet J.2018;29(3):169-73.
  47. Altun SK, Yiğin A, Gürbilek SE, Gürbüz S, Demirci M, Keskin O, et al. An enzyme-linked immunosorbent assay for Brucella specific antibody and real-time PCR for detecting Brucella spp. in milk and cheese in Şanliurfa, Turkey. Pak Vet J. 2017;37(1):39-42.
  48. Taha H, Smith C, Durham J, Reid S. Identification of a One Health intervention for brucellosis in Jordan using system dynamics modelling. Systems (Basel). 2023;11(11):542.  https://doi.org/10.3390/systems11110542 
  49. Gurbilek SE, Karagul MS, Saytekin AM, Baklan EA, Saglam G. Investigating field efficacy and safety of conjunctival Brucella abortus S19 vaccine in cattle. Agric Sci Dig. 2022;43(4):556-61.  https://doi.org/10.18805/ag.DF-393 
  50. Gurbilek SE, Karagul MS, Saytekin AM, Baklan EA, Saglam G. Investıgatıng the serologıcal response and safety of Brucella melıtensıs rev.1 conjunctıval vaccıne ın small rumınants. Slovak J Anim Sci. 2023;56(1):30-7.  https://doi.org/10.36547/sjas.793 
  51. Hikal AF, Wareth G, Khan A. Brucellosis: why is it eradicated from domestic livestock in the United States but not in the Nile River Basin countries? Ger J Microbiol.2023;3(2):19-25.  https://doi.org/10.51585/gjm.2023.2.0026 
  52. Cekanac R, Mladenović J, Ristanović E, Lazić S. Epidemiological characteristics of brucellosis in Serbia, 1980-2008. Croat Med J. 2010;51(4):337-44.  https://doi.org/10.3325/cmj.2010.51.337  PMID: 20718087 
  53. Guler S, Kokoglu OF, Ucmak H, Gul M, Ozden S, Ozkan F. Human brucellosis in Turkey: different clinical presentations. J Infect Dev Ctries. 2014;8(5):581-8.  https://doi.org/10.3855/jidc.3510  PMID: 24820461 
  54. Bingöl KK. İstanbul ve Şanlıurfa'da satışa sunulan urfa peynirlerinin koagülaz pozitif staphylococcus aureus yönüyle karşılaştırılması. [Comparison of Urfa cheeses sold in Istanbul and Şanlıurfa in terms of coagulase positive Staphylococcus aureus]. Istanbul: İstanbul Medipol Üniversitesi Sağlık Bilimleri Enstitüsü; 2016.Turkish. Available from: https://acikerisim.medipol.edu.tr/xmlui/handle/20.500.12511/6859
  55. Namiduru M, Gungor K, Dikensoy O, Baydar I, Ekinci E, Karaoglan I, et al. Epidemiological, clinical and laboratory features of brucellosis: a prospective evaluation of 120 adult patients. Int J Clin Pract. 2003;57(1):20-4.  https://doi.org/10.1111/j.1742-1241.2003.tb11391.x  PMID: 12587937 
  56. Tanir G, Tufekci SB, Tuygun N. Presentation, complications, and treatment outcome of brucellosis in Turkish children. Pediatr Int. 2009;51(1):114-9.  https://doi.org/10.1111/j.1442-200X.2008.02661.x  PMID: 19371290 
Genomic analysis of Brucella isolates from animals and humans, Türkiye, 2010 to 2020
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Kadir+Akar&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Akar Kadir</a>, <a href="/search?value1=Hanka+Brangsch&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Brangsch Hanka</a>, <a href="/search?value1=Tariq+Jamil&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Jamil Tariq</a>, <a href="/search?value1=G%C3%BClseren++Y%C4%B1ld%C4%B1z+%C3%96z&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Yıldız Öz Gülseren </a>, <a href="/search?value1=Emin+Ayhan+Baklan&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Baklan Emin Ayhan</a>, <a href="/search?value1=Buket+Ero%C4%9Flu&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Eroğlu Buket</a>, <a href="/search?value1=Eray+At%C4%B1l&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Atıl Eray</a>, <a href="/search?value1=Sevil+Erdenlig+G%C3%BCrbilek&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Erdenlig Gürbilek Sevil</a>, <a href="/search?value1=Oktay+Keskin&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Keskin Oktay</a>, <a href="/search?value1=Osman+Ya%C5%9Far+Tel&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Tel Osman Yaşar</a>, <a href="/search?value1=Ayfer+G%C3%BCll%C3%BC+Y%C3%BCcetepe&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Yücetepe Ayfer Güllü</a>, <a href="/search?value1=Vassilios+Sandalakis&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Sandalakis Vassilios</a>, <a href="/search?value1=Evridiki+Boukouvala&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Boukouvala Evridiki</a>, <a href="/search?value1=Anna+Psaroulaki&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Psaroulaki Anna</a>, <a href="/search?value1=Ashraf+A+Abd+El+Tawab&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Abd El Tawab Ashraf A</a>, <a href="/search?value1=Falk+Melzer&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Melzer Falk</a>, <a href="/search?value1=Mathias+W+Pletz&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Pletz Mathias W</a>, <a href="/search?value1=Heinrich+Neubauer&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Neubauer Heinrich</a>, <a href="/search?value1=Gamal+Wareth&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Wareth Gamal</a></span>. Genomic analysis of Brucella isolates from animals and humans, Türkiye, 2010 to 2020. <a href="/content/ecdc">Euro Surveill.</a> 2024;29(38):pii=2400105. <a href="https://doi.org/10.2807/1560-7917.ES.2024.29.38.2400105" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2024.29.38.2400105</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 14 Feb 2024;&nbsp;&nbsp; <span class="generated">Accepted</span>: 22 Apr 2024 </span> </p>
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