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Abstract

Carbapenem-resistant are prevalent in low- and middle-income countries such as Egypt, but little is known about the molecular epidemiology and mechanisms of resistance in these settings. Here, we characterize carbapenem-resistant from Alexandria, Egypt, and place it in a regional context. Fifty-four carbapenem-resistant isolates from Alexandria Main University Hospital (AMUH), Alexandria, Egypt, collected between 2010 and 2015 were genome sequenced using Illumina technology. Genomes were assembled and annotated. Genomes for 36 isolates from the Middle East region were downloaded from GenBank. The core-gene compliment was determined using Roary, and analyses of recombination were performed in Gubbins. Multilocus sequence typing (MLST) sequence type (ST) and antibiotic-resistance genes were identified. The majority of Egyptian isolates belonged to one of three major clades, corresponding to Pasteur MLST clonal complex (CC) 1, CC2 and ST158. Strains belonging to ST158 have been reported almost exclusively from North Africa, the Middle East and Pakistan, and may represent a region-specific lineage. All isolates carried an gene, six carried and one carried . The gene was located on a variety of different mobile elements, with Tn predominant in CC2 strains, and Tn predominant in other lineages. Of particular concern, in 8 of the 13 CC1 strains, the gene was located in a temperate bacteriophage phiOXA, previously identified only once before in a CC1 clone from the USA military. The carbapenem-resistant population in AMUH is very diverse, and indicates an endemic circulating population, including a region-specific lineage. A major mechanism for dissemination in CC1 isolates appears to be a bacteriophage, presenting new concerns about the ability of these carbapenemases to spread throughout the bacterial population.

Funding
This study was supported by the:
  • Newton Fund (Award Egyptian STDF project ID: 26235)
    • Principle Award Recipient: AlaaAbouelfetouh
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2022-02-01
2024-04-26
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References

  1. WHO Global Priority List of Antibiotic-Resistant Bacteria to Guide Research, Discovery, and Development of New Antibiotics Geneva: World Health Organization; 2017
    [Google Scholar]
  2. Antunes LCS, Visca P, Towner KJ. Acinetobacter baumannii: evolution of a global pathogen. Pathog Dis 2014; 71:292–301 [View Article] [PubMed]
    [Google Scholar]
  3. Rodríguez CH, Nastro M, Famiglietti A. Carbapenemases in Acinetobacter baumannii: review of their dissemination in Latin America. Rev Argent Microbiol 2018; 50:327–333 [View Article] [PubMed]
    [Google Scholar]
  4. Kempf M, Rolain JM. Emergence of resistance to carbapenems in Acinetobacter baumannii in Europe: clinical impact and therapeutic options. Int J Antimicrob Agents 2012; 39:105–114 [View Article] [PubMed]
    [Google Scholar]
  5. Hu F, Zhu D, Wang F, Wang M. Current status and trends of antibacterial resistance in China. Clin Infect Dis 2018; 67:S128–S134 [View Article] [PubMed]
    [Google Scholar]
  6. Hsu LY, Apisarnthanarak A, Khan E, Suwantarat N, Ghafur A et al. Carbapenem-resistant Acinetobacter baumannii and Enterobacteriaceae in South and Southeast Asia. Clin Microbiol Rev 2017; 30:1–22 [View Article] [PubMed]
    [Google Scholar]
  7. Kostyanev T, Vilken T, Lammens C, Timbermont L, Van’t Veen A et al. Detection and prevalence of carbapenem-resistant Gram-negative bacteria among European laboratories in the COMBACTE network: a COMBACTE LAB-Net survey. Int J Antimicrob Agents 2019; 53:268–274 [View Article] [PubMed]
    [Google Scholar]
  8. Moghnieh RA, Kanafani ZA, Tabaja HZ, Sharara SL, Awad LS et al. Epidemiology of common resistant bacterial pathogens in the countries of the Arab League. Lancet Infect Dis 2018; 18:e379–e394 [View Article] [PubMed]
    [Google Scholar]
  9. Potron A, Poirel L, Nordmann P. Emerging broad-spectrum resistance in Pseudomonas aeruginosa and Acinetobacter baumannii: mechanisms and epidemiology. Int J Antimicrob Agents 2015; 45:568–585 [View Article] [PubMed]
    [Google Scholar]
  10. Evans BA, Amyes SGB. OXA β-lactamases. Clin Microbiol Rev 2014; 27:241–263 [View Article] [PubMed]
    [Google Scholar]
  11. Naas T, Oueslati S, Bonnin RA, Dabos ML, Zavala A et al. Beta-lactamase database (BLDB) – structure and function. J Enzyme Inhib Med Chem 2017; 32:917–919 [View Article] [PubMed]
    [Google Scholar]
  12. Takebayashi Y, Findlay J, Heesom KJ, Warburton PJ, Avison MB et al. Variability in carbapenemase activity of intrinsic OxaAb (OXA-51-like) β-lactamase enzymes in Acinetobacter baumannii. J Antimicrob Chemother 2021; 76:587–595
    [Google Scholar]
  13. Turton JF, Ward ME, Woodford N, Kaufmann ME, Pike R et al. The role of ISAba1 in expression of OXA carbapenemase genes in Acinetobacter baumannii. FEMS Microbiol Lett 2006; 258:72–77 [View Article] [PubMed]
    [Google Scholar]
  14. Nigro SJ, Hall RM. Does the intrinsic oxaAb (blaOXA-51-like) gene of Acinetobacter baumannii confer resistance to carbapenems when activated by ISAba1?. J Antimicrob Chemother 2018; 73:3518–3520 [View Article] [PubMed]
    [Google Scholar]
  15. Higgins PG, Dammhayn C, Hackel M, Seifert H. Global spread of carbapenem-resistant Acinetobacter baumannii. J Antimicrob Chemother 2010; 65:233–238 [View Article] [PubMed]
    [Google Scholar]
  16. El-Sayed-Ahmed MAE-G, Amin MA, Tawakol WM, Loucif L, Bakour S et al. High prevalence of bla(NDM-1) carbapenemase-encoding gene and 16S rRNA armA methyltransferase gene among Acinetobacter baumannii clinical Isolates in Egypt. Antimicrob Agents Chemother 2015; 59:3602–3605 [View Article] [PubMed]
    [Google Scholar]
  17. Fouad M, Attia AS, Tawakkol WM, Hashem AM. Emergence of carbapenem-resistant Acinetobacter baumannii harboring the OXA-23 carbapenemase in intensive care units of Egyptian hospitals. Int J Infect Dis 2013; 17:e1252–4 [View Article] [PubMed]
    [Google Scholar]
  18. Al-Hassan L, Zafer MM, El-Mahallawy H. Multiple sequence types responsible for healthcare-associated Acinetobacter baumannii dissemination in a single centre in Egypt. BMC Infect Dis 2019; 19:829 [View Article] [PubMed]
    [Google Scholar]
  19. Zowawi HM, Sartor AL, Sidjabat HE, Balkhy HH, Walsh TR et al. Molecular epidemiology of carbapenem-resistant Acinetobacter baumannii isolates in the Gulf Cooperation Council States: dominance of OXA-23-type producers. J Clin Microbiol 2015; 53:896–903 [View Article] [PubMed]
    [Google Scholar]
  20. Nigro SJ, Hall RM. Structure and context of Acinetobacter transposons carrying the oxa23 carbapenemase gene. J Antimicrob Chemother 2016; 71:1135–1147 [View Article] [PubMed]
    [Google Scholar]
  21. Zarrilli R, Pournaras S, Giannouli M, Tsakris A. Global evolution of multidrug-resistant Acinetobacter baumannii clonal lineages. Int J Antimicrob Agents 2013; 41:11–19 [View Article] [PubMed]
    [Google Scholar]
  22. Diancourt L, Passet V, Nemec A, Dijkshoorn L, Brisse S. The population structure of Acinetobacter baumannii: expanding multiresistant clones from an ancestral susceptible genetic pool. PLoS One 2010; 5:e10034 [View Article] [PubMed]
    [Google Scholar]
  23. Bartual SG, Seifert H, Hippler C, Luzon MAD, Wisplinghoff H et al. Development of a multilocus sequence typing scheme for characterization of clinical isolates of Acinetobacter baumannii. J Clin Microbiol 2005; 43:4382–4390 [View Article] [PubMed]
    [Google Scholar]
  24. Gaiarsa S, Batisti Biffignandi G, Esposito EP, Castelli M, Jolley KA et al. Comparative analysis of the two Acinetobacter baumannii multilocus sequence typing (MLST) schemes. Front Microbiol 2019; 10:930 [View Article] [PubMed]
    [Google Scholar]
  25. Hamidian M, Nigro SJ. Emergence, molecular mechanisms and global spread of carbapenem-resistant Acinetobacter baumannii. Microb Genom 2019; 5:e000306 [View Article] [PubMed]
    [Google Scholar]
  26. Rodríguez CH, Balderrama Yarhui N, Nastro M, Nuñez Quezada T, Castro Cañarte G et al. Molecular epidemiology of carbapenem-resistant Acinetobacter baumannii in South America. J Med Microbiol 2016; 65:1088–1091 [View Article] [PubMed]
    [Google Scholar]
  27. Ghaith DM, Zafer MM, Al-Agamy MH, Alyamani EJ, Booq RY et al. The emergence of a novel sequence type of MDR Acinetobacter baumannii from the intensive care unit of an Egyptian tertiary care hospital. Ann Clin Microbiol Antimicrob 2017; 16:34 [View Article] [PubMed]
    [Google Scholar]
  28. Abouelfetouh A, Torky AS, Aboulmagd E. Phenotypic and genotypic characterization of carbapenem-resistant Acinetobacter baumannii isolates from Egypt. Antimicrob Resist Infect Control 2019; 8:185 [View Article] [PubMed]
    [Google Scholar]
  29. Abouelfetouh A, Torky AS, Aboulmagd E. Role of plasmid carrying blaNDM in mediating antibiotic resistance among Acinetobacter baumannii clinical isolates from Egypt. 3 Biotech 2020; 10:170 [View Article] [PubMed]
    [Google Scholar]
  30. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article] [PubMed]
    [Google Scholar]
  31. Wingett SW, Andrews S. FastQ Screen: a tool for multi-genome mapping and quality control. F1000Res 2018; 7:1338 [View Article] [PubMed]
    [Google Scholar]
  32. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article] [PubMed]
    [Google Scholar]
  33. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
    [Google Scholar]
  34. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 2013; 29:1072–1075 [View Article] [PubMed]
    [Google Scholar]
  35. Viale AM, Evans BA. Microevolution in the major outer membrane protein OmpA of Acinetobacter baumannii. Microb Genom 2020; 6:e000381 [View Article] [PubMed]
    [Google Scholar]
  36. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 2015; 31:3691–3693 [View Article] [PubMed]
    [Google Scholar]
  37. Price MN, Dehal PS, Arkin AP. FastTree 2 – approximately maximum-likelihood trees for large alignments. PLoS One 2010; 5:e9490 [View Article] [PubMed]
    [Google Scholar]
  38. Jironkin A, Al-Shahib A, Painset A, Underwood A, Kapatai G et al.PHEnix 1.3 ed; 2017
  39. Dallman T, Ashton P, Schafer U, Jironkin A, Painset A et al. SnapperDB: a database solution for routine sequencing analysis of bacterial isolates. Bioinformatics 2018; 34:3028–3029 [View Article] [PubMed]
    [Google Scholar]
  40. Croucher NJ, Page AJ, Connor TR, Delaney AJ, Keane JA et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res 2015; 43:e15 [View Article] [PubMed]
    [Google Scholar]
  41. Larsen MV, Cosentino S, Rasmussen S, Friis C, Hasman H et al. Multilocus sequence typing of total-genome-sequenced bacteria. J Clin Microbiol 2012; 50:1355–1361 [View Article] [PubMed]
    [Google Scholar]
  42. Hunt M, Mather AE, Sánchez-Busó L, Page AJ, Parkhill J et al. ARIBA: rapid antimicrobial resistance genotyping directly from sequencing reads. Microb Genom 2017; 3:e000131 [View Article] [PubMed]
    [Google Scholar]
  43. McArthur AG, Waglechner N, Nizam F, Yan A, Azad MA et al. The Comprehensive Antibiotic Resistance Database. Antimicrob Agents Chemother 2013; 57:3348–3357 [View Article] [PubMed]
    [Google Scholar]
  44. Inouye M, Dashnow H, Raven L-A, Schultz MB, Pope BJ et al. SRST2: rapid genomic surveillance for public health and hospital microbiology labs. Genome Med 2014; 6:11 [View Article] [PubMed]
    [Google Scholar]
  45. Abudahab K, Prada JM, Yang Z, Bentley SD, Croucher NJ et al. PANINI: pangenome neighbour identification for bacterial populations. Microb Genom 2019; 5:e000220 [View Article] [PubMed]
    [Google Scholar]
  46. Jones P, Binns D, Chang H-Y, Fraser M, Li W et al. InterProScan 5: genome-scale protein function classification. Bioinformatics 2014; 30:1236–1240 [View Article] [PubMed]
    [Google Scholar]
  47. Söding J, Biegert A, Lupas AN. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 2005; 33:W244–W248 [View Article] [PubMed]
    [Google Scholar]
  48. Lowe TM, Chan PP. tRNAscan-SE On-line: integrating search and context for analysis of transfer RNA genes. Nucleic Acids Res 2016; 44:W54–W57 [View Article] [PubMed]
    [Google Scholar]
  49. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 2011; 7:539 [View Article] [PubMed]
    [Google Scholar]
  50. Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 2015; 32:268–274 [View Article] [PubMed]
    [Google Scholar]
  51. Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 2017; 14:587–589 [View Article] [PubMed]
    [Google Scholar]
  52. Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS. UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol 2018; 35:518–522 [View Article] [PubMed]
    [Google Scholar]
  53. Okonechnikov K, Conesa A, García-Alcalde F. Qualimap 2: advanced multi-sample quality control for high-throughput sequencing data. Bioinformatics 2016; 32:292–294 [View Article] [PubMed]
    [Google Scholar]
  54. Héritier C, Poirel L, Nordmann P. Cephalosporinase over-expression resulting from insertion of ISAba1 in Acinetobacter baumannii. Clin Microbiol Infect 2006; 12:123–130 [View Article] [PubMed]
    [Google Scholar]
  55. Woodford N, Ellington MJ, Coelho JM, Turton JF, Ward ME et al. Multiplex PCR for genes encoding prevalent OXA carbapenemases in Acinetobacter spp. Int J Antimicrob Agents 2006; 27:351–353 [View Article] [PubMed]
    [Google Scholar]
  56. Sambrook J, Russell DW. Extraction of bacteriophage λ DNA from large-scale cultures using proteinase K and SDS. CSH Protoc 2006; 2006:pdb.prot3972 [View Article] [PubMed]
    [Google Scholar]
  57. Li H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv 20131303.3997
    [Google Scholar]
  58. Tomaschek F, Higgins PG, Stefanik D, Wisplinghoff H, Seifert H. Head-to-head comparison of two multi-locus sequence typing (MLST) schemes for characterization of Acinetobacter baumannii outbreak and sporadic isolates. PLoS One 2016; 11:e0153014 [View Article] [PubMed]
    [Google Scholar]
  59. Zander E, Nemec A, Seifert H, Higgins PG. Association between β-lactamase-encoding bla(OXA-51) variants and DiversiLab rep-PCR-based typing of Acinetobacter baumannii isolates. J Clin Microbiol 2012; 50:1900–1904 [View Article] [PubMed]
    [Google Scholar]
  60. Poirel L, Bonnin RA, Boulanger A, Schrenzel J, Kaase M et al. Tn125-related acquisition of blaNDM-like genes in Acinetobacter baumannii. Antimicrob Agents Chemother 2012; 56:1087–1089 [View Article] [PubMed]
    [Google Scholar]
  61. Bonnin RA, Poirel L, Naas T, Pirs M, Seme K et al. Dissemination of New Delhi metallo-β-lactamase-1-producing Acinetobacter baumannii in Europe. Clin Microbiol Infect 2012; 18:E362–E365 [View Article] [PubMed]
    [Google Scholar]
  62. Corvec S, Poirel L, Naas T, Drugeon H, Nordmann P. Genetics and expression of the carbapenem-hydrolyzing oxacillinase gene blaOXA-23 in Acinetobacter baumannii. Antimicrob Agents Chemother 2007; 51:1530–1533 [View Article] [PubMed]
    [Google Scholar]
  63. Gallagher LA, Ramage E, Weiss EJ, Radey M, Hayden HS et al. Resources for genetic and genomic analysis of emerging pathogen Acinetobacter baumannii. J Bacteriol 2015; 197:2027–2035 [View Article] [PubMed]
    [Google Scholar]
  64. Casjens SR, Grose JH. Contributions of P2- and P22-like prophages to understanding the enormous diversity and abundance of tailed bacteriophages. Virology 2016; 496:255–276 [View Article] [PubMed]
    [Google Scholar]
  65. Moraru C, Varsani A, Kropinski AM. VIRIDIC – a novel tool to calculate the intergenomic similarities of prokaryote-infecting viruses. Viruses 2020; 12:1268 [View Article]
    [Google Scholar]
  66. Adriaenssens E. How to name and classify your phage: an informal guide. Viruses 2017; 9:E70 [View Article] [PubMed]
    [Google Scholar]
  67. Al-Hassan L, El Mehallawy H, Amyes SGB. Diversity in Acinetobacter baumannii isolates from paediatric cancer patients in Egypt. Clin Microbiol Infect 2013; 19:1082–1088 [View Article] [PubMed]
    [Google Scholar]
  68. Karah N, Khalid F, Wai SN, Uhlin BE, Ahmad I. Molecular epidemiology and antimicrobial resistance features of Acinetobacter baumannii clinical isolates from Pakistan. Ann Clin Microbiol Antimicrob 2020; 19:2 [View Article] [PubMed]
    [Google Scholar]
  69. Evans BA, Hamouda A, Towner KJ, Amyes SGB. OXA-51-like beta-lactamases and their association with particular epidemic lineages of Acinetobacter baumannii. Clin Microbiol Infect 2008; 14:268–275 [View Article] [PubMed]
    [Google Scholar]
  70. Hamouda A, Evans BA, Towner KJ, Amyes SGB. Characterization of epidemiologically unrelated Acinetobacter baumannii isolates from four continents by use of multilocus sequence typing, pulsed-field gel electrophoresis, and sequence-based typing of bla(OXA-51-like) genes. J Clin Microbiol 2010; 48:2476–2483 [View Article] [PubMed]
    [Google Scholar]
  71. Stietz MS, Ramírez MS, Vilacoba E, Merkier AK, Limansky AS et al. Acinetobacter baumannii extensively drug resistant lineages in Buenos Aires hospitals differ from the international clones I-III. Infect Genet Evol 2013; 14:294–301 [View Article] [PubMed]
    [Google Scholar]
  72. Graña-Miraglia L, Evans BA, López-Jácome LE, Hernández-Durán M, Colín-Castro CA et al. Origin of OXA-23 variant OXA-239 from a recently emerged lineage of Acinetobacter baumannii international clone V. mSphere 2020; 5:e00801-19 [View Article] [PubMed]
    [Google Scholar]
  73. Karah N, Jolley KA, Hall RM, Uhlin BE. Database for the ampC alleles in Acinetobacter baumannii. PLoS One 2017; 12:e0176695 [View Article] [PubMed]
    [Google Scholar]
  74. Al-Agamy MH, Khalaf NG, Tawfick MM, Shibl AM, El Kholy A. Molecular characterization of carbapenem-insensitive Acinetobacter baumannii in Egypt. Int J Infect Dis 2014; 22:49–54 [View Article] [PubMed]
    [Google Scholar]
  75. Kaase M, Nordmann P, Wichelhaus TA, Gatermann SG, Bonnin RA et al. NDM-2 carbapenemase in Acinetobacter baumannii from Egypt. J Antimicrob Chemother 2011; 66:1260–1262 [View Article] [PubMed]
    [Google Scholar]
  76. Benmahmod AB, Said HS, Ibrahim RH. Prevalence and mechanisms of carbapenem resistance among. Microb Drug Resist 2019; 25:480–488 [View Article] [PubMed]
    [Google Scholar]
  77. Gomaa FAM, Helal ZH, Khan MI. High Prevalence of blaNDM-1, blaVIM, qacE, and qacEΔ1 genes and their association with decreased susceptibility to antibiotics and common hospital biocides in clinical isolates of Acinetobacter baumannii. Microorganisms 2017; 5:E18 [View Article] [PubMed]
    [Google Scholar]
  78. Adams-Haduch JM, Paterson DL, Sidjabat HE, Pasculle AW, Potoski BA et al. Genetic basis of multidrug resistance in Acinetobacter baumannii clinical isolates at a tertiary medical center in Pennsylvania. Antimicrob Agents Chemother 2008; 52:3837–3843 [View Article] [PubMed]
    [Google Scholar]
  79. Colomer-Lluch M, Imamovic L, Jofre J, Muniesa M. Bacteriophages carrying antibiotic resistance genes in fecal waste from cattle, pigs, and poultry. Antimicrob Agents Chemother 2011; 55:4908–4911 [View Article] [PubMed]
    [Google Scholar]
  80. Quirós P, Colomer-Lluch M, Martínez-Castillo A, Miró E, Argente M et al. Antibiotic resistance genes in the bacteriophage DNA fraction of human fecal samples. Antimicrob Agents Chemother 2014; 58:606–609 [View Article] [PubMed]
    [Google Scholar]
  81. Gómez-Gómez C, Blanco-Picazo P, Brown-Jaque M, Quirós P, Rodríguez-Rubio L et al. Infectious phage particles packaging antibiotic resistance genes found in meat products and chicken feces. Sci Rep 2019; 9:13281 [View Article] [PubMed]
    [Google Scholar]
  82. Enault F, Briet A, Bouteille L, Roux S, Sullivan MB et al. Phages rarely encode antibiotic resistance genes: a cautionary tale for virome analyses. ISME J 2017; 11:237–247 [View Article] [PubMed]
    [Google Scholar]
  83. Touchon M, Cury J, Yoon E-J, Krizova L, Cerqueira GC et al. The genomic diversification of the whole Acinetobacter genus: origins, mechanisms, and consequences. Genome Biol Evol 2014; 6:2866–2882 [View Article] [PubMed]
    [Google Scholar]
  84. Costa AR, Monteiro R, Azeredo J. Genomic analysis of Acinetobacter baumannii prophages reveals remarkable diversity and suggests profound impact on bacterial virulence and fitness. Sci Rep 2018; 8:15346 [View Article] [PubMed]
    [Google Scholar]
  85. López-Leal G, Santamaria RI, Cevallos , Gonzalez V, Castillo-Ramírez S. Prophages encode antibiotic resistance genes in Acinetobacter baumannii. Microb Drug Resist 2020; 26:1275–1277 [View Article]
    [Google Scholar]
  86. Wachino JI, Jin W, Kimura K, Arakawa Y. Intercellular transfer of chromosomal antimicrobial resistance genes between Acinetobacter baumannii strains mediated by prophages. Antimicrob Agents Chemother 2019; 63:e00334-19 [View Article] [PubMed]
    [Google Scholar]
  87. Kenyon JJ, Arbatsky NP, Shneider MM, Popova AV, Dmitrenok AS et al. The K46 and K5 capsular polysaccharides produced by Acinetobacter baumannii NIPH 329 and SDF have related structures and the side-chain non-ulosonic acids are 4-O-acetylated by phage-encoded O-acetyltransferases. PLoS One 2019; 14:e0218461 [View Article] [PubMed]
    [Google Scholar]
  88. Girlich D, Bonnin RA, Bogaerts P, De Laveleye M, Huang DT et al. Chromosomal amplification of the blaOXA-58 carbapenemase gene in a Proteus mirabilis clinical isolate. Antimicrob Agents Chemother 2017; 61:e01697-16 [View Article] [PubMed]
    [Google Scholar]
  89. Chan AP, Sutton G, DePew J, Krishnakumar R, Choi Y et al. A novel method of consensus pan-chromosome assembly and large-scale comparative analysis reveal the highly flexible pan-genome of Acinetobacter baumannii. Genome Biol 2015; 16:143 [View Article] [PubMed]
    [Google Scholar]
  90. Wibberg D, Salto IP, Eikmeyer FG, Maus I, Winkler A et al. Complete genome sequencing of Acinetobacter baumannii strain K50 discloses the large conjugative plasmid pK50a encoding carbapenemase OXA-23 and extended-spectrum β-lactamase GES-11. Antimicrob Agents Chemother 2018; 62:e00212-18 [View Article] [PubMed]
    [Google Scholar]
  91. Rafei R, Pailhoriès H, Hamze M, Eveillard M, Mallat H et al. Molecular epidemiology of Acinetobacter baumannii in different hospitals in Tripoli, Lebanon using bla(OXA-51-like) sequence based typing. BMC Microbiol 2015; 15:103 [View Article] [PubMed]
    [Google Scholar]
  92. Hammerum AM, Hansen F, Skov MN, Stegger M, Andersen PS et al. Investigation of a possible outbreak of carbapenem-resistant Acinetobacter baumannii in Odense, Denmark using PFGE, MLST and whole-genome-based SNPs. J Antimicrob Chemother 2015; 70:1965–1968 [View Article] [PubMed]
    [Google Scholar]
  93. Vali L, Dashti K, Opazo-Capurro AF, Dashti AA, Al Obaid K et al. Diversity of multi-drug resistant Acinetobacter baumannii population in a major hospital in Kuwait. Front Microbiol 2015; 6:743 [View Article] [PubMed]
    [Google Scholar]
  94. Castanheira M, Costello SE, Woosley LN, Deshpande LM, Davies TA et al. Evaluation of clonality and carbapenem resistance mechanisms among Acinetobacter baumannii-Acinetobacter calcoaceticus complex and Enterobacteriaceae isolates collected in European and Mediterranean countries and detection of two novel β-lactamases, GES-22 and VIM-35. Antimicrob Agents Chemother 2014; 58:7358–7366 [View Article] [PubMed]
    [Google Scholar]
  95. Bonnin RA, Rotimi VO, Al Hubail M, Gasiorowski E, Al Sweih N et al. Wide dissemination of GES-type carbapenemases in Acinetobacter baumannii isolates in Kuwait. Antimicrob Agents Chemother 2013; 57:183–188 [View Article] [PubMed]
    [Google Scholar]
  96. Mabrouk A, Grosso F, Botelho J, Achour W, Ben Hassen A et al. GES-14-producing Acinetobacter baumannii isolates in a neonatal intensive care unit in Tunisia are associated with a typical Middle East clone and a transferable plasmid. Antimicrob Agents Chemother 2017; 61:e00142-17 [View Article] [PubMed]
    [Google Scholar]
  97. Wang X, Qiao F, Yu R, Gao Y, Zong Z. Clonal diversity of Acinetobacter baumannii clinical isolates revealed by a snapshot study. BMC Microbiol 2013; 13:234 [View Article] [PubMed]
    [Google Scholar]
  98. Sullivan MJ, Petty NK, Beatson SA. Easyfig: a genome comparison visualizer. Bioinformatics 2011; 27:1009–1010 [View Article] [PubMed]
    [Google Scholar]
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