1887

Abstract

An epidemic of post-surgical wound infections, caused by a non-tuberculous mycobacterium, has been on-going in Brazil. It has been unclear whether one or multiple lineages are responsible and whether their wide geographical distribution across Brazil is due to spread from a single point source or is the result of human-mediated transmission. 188 isolates, collected from nine Brazilian states, were whole genome sequenced and analysed using phylogenetic and comparative genomic approaches. The isolates from Brazil formed a single clade, which was estimated to have emerged in 2003. We observed temporal and geographic structure within the lineage that enabled us to infer the movement of sub-lineages across Brazil. The genome size of the Brazilian lineage was reduced relative to most strains in the three subspecies of Mycobacterium abscessus and contained a novel plasmid, pMAB02, in addition to the previously described pMAB01 plasmid. One lineage, which emerged just prior to the initial outbreak, is responsible for the epidemic of post-surgical wound infections in Brazil. Phylogenetic analysis indicates that multiple transmission events led to its spread. The presence of a novel plasmid and the reduced genome size suggest that the lineage has undergone adaptation to the surgical niche.

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2017-05-03
2024-03-28
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References

  1. Tortoli E, Kohl TA, Brown-Elliott BA, Trovato A, Leão SC et al. Emended description of Mycobacterium abscessus, Mycobacterium abscessus subsp. abscessus and Mycobacterium abscessus subsp. bolletii and designation of Mycobacterium abscessus subsp. massiliense comb. nov. Int J Syst Evol Microbiol 2016; 66:4471–4479 [View Article][PubMed]
    [Google Scholar]
  2. Bryant JM, Grogono DM, Rodriguez-Rincon D, Everall I, Brown KP et al. Emergence and spread of a human-transmissible multidrug-resistant nontuberculous mycobacterium. Science 2016; 354:751–757 [View Article][PubMed]
    [Google Scholar]
  3. Aitken ML, Limaye A, Pottinger P, Whimbey E, Goss CH et al. Respiratory outbreak of Mycobacterium abscessus subspecies massiliense in a lung transplant and cystic fibrosis center. Am J Respir Crit Care Med 2012; 185:231–232 [View Article][PubMed]
    [Google Scholar]
  4. Bryant JM, Grogono DM, Greaves D, Foweraker J, Roddick I et al. Whole-genome sequencing to identify transmission of Mycobacterium abscessus between patients with cystic fibrosis: a retrospective cohort study. Lancet 2013; 381:1551–1560 [View Article][PubMed]
    [Google Scholar]
  5. Cheng A, Liu YC, Chen ML, Hung CC, Tsai YT et al. Extrapulmonary infections caused by a dominant strain of Mycobacterium massiliense (Mycobacterium abscessus subspecies bolletii). Clin Microbiol Infect 2013; 19:E473E482 [View Article][PubMed]
    [Google Scholar]
  6. Cheng A, Sheng WH, Huang YC, Sun HY, Tsai YT et al. Prolonged postprocedural outbreak of Mycobacterium massiliense infections associated with ultrasound transmission gel. Clin Microbiol Infect 2016; 22:382.e1–382.e11 [View Article]
    [Google Scholar]
  7. Viana-Niero C, Lima KV, Lopes ML, Rabello MC, Marsola LR et al. Molecular characterization of Mycobacterium massiliense and Mycobacterium bolletii in isolates collected from outbreaks of infections after laparoscopic surgeries and cosmetic procedures. J Clin Microbiol 2008; 46:850–855 [View Article][PubMed]
    [Google Scholar]
  8. Lorena NS, Pitombo MB, Côrtes PB, Maya MC, Silva MG et al. Mycobacterium massiliense BRA100 strain recovered from postsurgical infections: resistance to high concentrations of glutaraldehyde and alternative solutions for high level disinfection. Acta Cir Bras 2010; 25:455–459 [View Article][PubMed]
    [Google Scholar]
  9. Leão SC, Viana-Niero C, Matsumoto CK, Lima KV, Lopes ML et al. Epidemic of surgical-site infections by a single clone of rapidly growing mycobacteria in Brazil. Future Microbiol 2010; 5:971–980 [View Article][PubMed]
    [Google Scholar]
  10. Guimarães T, Chimara E, Do Prado GV, Ferrazoli L, Carvalho NG et al. Pseudooutbreak of rapidly growing mycobacteria due to Mycobacterium abscessus subsp bolletii in a digestive and respiratory endoscopy unit caused by the same clone as that of a countrywide outbreak. Am J Infect Control 2016; 44:e221e226 [View Article][PubMed]
    [Google Scholar]
  11. Cardoso AM, Martins de Sousa E, Viana-Niero C, Bonfim de Bortoli F, Pereira das Neves ZC et al. Emergence of nosocomial Mycobacterium massiliense infection in Goiás, Brazil. Microbes Infect 2008; 10:1552–1557 [View Article][PubMed]
    [Google Scholar]
  12. Duarte RS, Lourenço MC, Fonseca LS, Leão SC, Amorim EL et al. Epidemic of postsurgical infections caused by Mycobacterium massiliense . J Clin Microbiol 2009; 47:2149–2155 [View Article][PubMed]
    [Google Scholar]
  13. Monego F, Duarte RS, Nakatani SM, Araújo WN, Riediger IN et al. Molecular identification and typing of Mycobacterium massiliense isolated from postsurgical infections in Brazil. Braz J Infect Dis 2011; 15:436–441 [View Article][PubMed]
    [Google Scholar]
  14. Nunes S, Baethgen LF, Ribeiro MO, Cardoso CM, De Paris F et al. Outbreaks due to Mycobacterium abscessus subsp. bolletii in southern Brazil: persistence of a single clone from 2007 to 2011. J Med Microbiol 2014; 63:1288–1293 [View Article][PubMed]
    [Google Scholar]
  15. Leão SC, Matsumoto CK, Carneiro A, Ramos RT, Nogueira CL et al. The detection and sequencing of a broad-host-range conjugative IncP-1β plasmid in an epidemic strain of Mycobacterium abscessus subsp. bolletii . PLoS One 2013; 8:e60746 [View Article][PubMed]
    [Google Scholar]
  16. Shang S, Gibbs S, Henao-Tamayo M, Shanley CA, Mcdonnell G et al. Increased virulence of an epidemic strain of Mycobacterium massiliense in mice. PLoS One 2011; 6:e24726 [View Article][PubMed]
    [Google Scholar]
  17. Matsumoto CK, Chimara E, Bombarda S, Duarte RS, Leão SC. Diversity of pulsed-field gel electrophoresis patterns of Mycobacterium abscessus type 2 clinical isolates. J Clin Microbiol 2011; 49:62–68 [View Article][PubMed]
    [Google Scholar]
  18. Davidson RM, Hasan NA, de Moura VC, Duarte RS, Jackson M et al. Phylogenomics of Brazilian epidemic isolates of Mycobacterium abscessus subsp. bolletii reveals relationships of global outbreak strains. Infect Genet Evol 2013; 20:292–297 [View Article][PubMed]
    [Google Scholar]
  19. Tettelin H, Davidson RM, Agrawal S, Aitken ML, Shallom S et al. High-level relatedness among Mycobacterium abscessus subsp. massiliense strains from widely separated outbreaks. Emerg Infect Dis 2014; 20:364–371 [View Article][PubMed]
    [Google Scholar]
  20. Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 2008; 18:821–829 [View Article][PubMed]
    [Google Scholar]
  21. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article][PubMed]
    [Google Scholar]
  22. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M et al. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 2005; 21:3674–3676 [View Article][PubMed]
    [Google Scholar]
  23. Li H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv 20131–3
    [Google Scholar]
  24. Harris SR, Feil EJ, Holden MT, Quail MA, Nickerson EK et al. Evolution of MRSA during hospital transmission and intercontinental spread. Science 2010; 327:469–474 [View Article][PubMed]
    [Google Scholar]
  25. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article][PubMed]
    [Google Scholar]
  26. Francisco AP, Vaz C, Monteiro PT, Melo-Cristino J, Ramirez M et al. PHYLOViZ: phylogenetic inference and data visualization for sequence based typing methods. BMC Bioinformatics 2012; 13:87 [View Article][PubMed]
    [Google Scholar]
  27. 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]
  28. Page AJ, Taylor B, Delaney AJ, Soares J, Seemann T et al. SNP-sites: rapid efficient extraction of SNPs from multi-FASTA alignments. Microb Genom 2016; 2: [View Article][PubMed]
    [Google Scholar]
  29. Murray GG, Wang F, Harrison EM, Paterson GK, Mather AE et al. The effect of genetic structure on molecular dating and tests for temporal signal. Methods Ecol Evol 2016; 7:80–89 [View Article][PubMed]
    [Google Scholar]
  30. Drummond AJ, Rambaut A. BEAST: bayesian evolutionary analysis by sampling trees. BMC Evol Biol 2007; 7:214–218 [View Article][PubMed]
    [Google Scholar]
  31. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article][PubMed]
    [Google Scholar]
  32. Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG et al. ACT: the Artemis comparison tool. Bioinformatics 2005; 21:3422–3423 [View Article][PubMed]
    [Google Scholar]
  33. Dumas E, Christina Boritsch E, Vandenbogaert M, Rodríguez de La Vega RC, Thiberge JM et al. Mycobacterial pan-genome analysis suggests important role of plasmids in the radiation of type VII secretion systems. Genome Biol Evol 2016; 8:387–402 [View Article][PubMed]
    [Google Scholar]
  34. Ummels R, Abdallah AM, Kuiper V, Aâjoud A, Sparrius M et al. Identification of a novel conjugative plasmid in mycobacteria that requires both type IV and type VII secretion. MBio 2014; 5:e01744 [View Article][PubMed]
    [Google Scholar]
  35. Howard ST, Byrd TF, Lyons CR. A polymorphic region in Mycobacterium abscessus contains a novel insertion sequence element. Microbiology 2002; 148:2987–2996 [View Article][PubMed]
    [Google Scholar]
  36. Raiol T, Ribeiro GM, Maranhão AQ, Bocca AL, Silva-Pereira I et al. Complete genome sequence of Mycobacterium massiliense . J Bacteriol 2012; 194:5455 [View Article][PubMed]
    [Google Scholar]
  37. Cole ST, Eiglmeier K, Parkhill J, James KD, Thomson NR et al. Massive gene decay in the leprosy bacillus. Nature 2001; 409:1007–1011 [View Article][PubMed]
    [Google Scholar]
  38. Stinear TP, Seemann T, Pidot S, Frigui W, Reysset G et al. Reductive evolution and niche adaptation inferred from the genome of Mycobacterium ulcerans, the causative agent of Buruli ulcer . Genome Res 2007; 17:192–200 [View Article][PubMed]
    [Google Scholar]
  39. Okoro CK, Kingsley RA, Connor TR, Harris SR, Parry CM et al. Intracontinental spread of human invasive Salmonella Typhimurium pathovariants in sub-Saharan Africa. Nat Genet 2012; 44:1215–1221 [View Article][PubMed]
    [Google Scholar]
  40. Klemm EJ, Gkrania-Klotsas E, Hadfield J, Forbester JL, Harris SR et al. Emergence of host-adapted Salmonella Enteritidis through rapid evolution in an immunocompromised host. Nat Microbiol 2016; 1:15023 [View Article][PubMed]
    [Google Scholar]
  41. Svetlíková Z, Skovierová H, Niederweis M, Gaillard JL, Mcdonnell G et al. Role of porins in the susceptibility of Mycobacterium smegmatis and Mycobacterium chelonae to aldehyde-based disinfectants and drugs. Antimicrob Agents Chemother 2009; 53:4015–4018 [View Article][PubMed]
    [Google Scholar]
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