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Genomic analysis of Brucella isolates from animals and humans, Türkiye, 2010 to 2020
- Kadir Akar1,* , Hanka Brangsch2,* , Tariq Jamil2 , Gülseren Yıldız Öz3 , Emin Ayhan Baklan3 , Buket Eroğlu3 , Eray Atıl3 , Sevil Erdenlig Gürbilek 4 , Oktay Keskin4 , Osman Yaşar Tel4 , Ayfer Güllü Yücetepe4 , Vassilios Sandalakis5 , Evridiki Boukouvala6 , Anna Psaroulaki5 , Ashraf A Abd El Tawab7 , Falk Melzer2 , Mathias W Pletz8 , Heinrich Neubauer2 , Gamal Wareth2,8
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View Affiliations Hide AffiliationsAffiliations: 1 Department of Microbiology, Faculty of Veterinary Medicine, Van Yuzuncu Yıl University, Van, Türkiye 2 Institute of Bacterial Infections and Zoonoses, Friedrich-Loeffler-Institut, Jena, Germany 3 National Reference Laboratory (NRL) for Brucellosis, Pendik Veterinary Control Institute, Istanbul, Türkiye 4 Microbiology Department, Faculty of Veterinary Medicine, University of Harran, Şanlıurfa, Türkiye 5 Department of Clinical Microbiology and Microbial Pathogenesis, School of Medicine, University of Crete, Heraklion, Greece 6 Hellenic Agricultural Organization-DIMITRA, Veterinary Research Institute, Thessaloniki, Greece 7 Department of Bacteriology, Immunology and Mycology, Faculty of Veterinary Medicine, Benha University, Moshtohor, Toukh, Egypt 8 Institute of Infectious Diseases and Infection Control, Jena University Hospital, Jena, Germany* These authors contributed equally to the work and share first authorship.Correspondence:Gamal Warethgamal.wareth fli.de
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Citation style for this article: Akar Kadir, Brangsch Hanka, Jamil Tariq, Yıldız Öz Gülseren , Baklan Emin Ayhan, Eroğlu Buket, Atıl Eray, Erdenlig Gürbilek Sevil, Keskin Oktay, Tel Osman Yaşar, Yücetepe Ayfer Güllü, Sandalakis Vassilios, Boukouvala Evridiki, Psaroulaki Anna, Abd El Tawab Ashraf A, Melzer Falk, Pletz Mathias W, Neubauer Heinrich, Wareth Gamal. Genomic analysis of Brucella isolates from animals and humans, Türkiye, 2010 to 2020. Euro Surveill. 2024;29(38):pii=2400105. https://doi.org/10.2807/1560-7917.ES.2024.29.38.2400105 Received: 14 Feb 2024; Accepted: 22 Apr 2024
Abstract
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.
We aimed at investigating genomic differences of Brucella isolates from animals and humans in Türkiye.
We used whole genome sequencing (WGS) to assess the genetic diversity of Brucella 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.
Of the 106 Turkish Brucella isolates included, 57 were B. abortus and 49 were B. melitensis. One B. melitensis and two B. abortus isolates were identified as vaccine strains. Most (n = 55) B. abortus isolates clustered in three major branches, with no spatial discernible pattern. Of the B. melitensis 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.
Several B. melitensis and B. abortus 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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References
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
Alton GG, Jones LM, Angus R, Verger J. Techniques for the brucellosis laboratory. Paris: Institut National de la Recherche Agronomique (INRA); 1988.
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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.
-
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.
-
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.
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
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