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Volume 27, Number 11—November 2021
Research

Multidrug-Resistant Methicillin-Resistant Staphylococcus aureus Associated with Bacteremia and Monocyte Evasion, Rio de Janeiro, Brazil

Alice Slotfeldt Viana1, Ana Maria Nunes Botelho12, Ahmed M. Moustafa1, Craig L.K. Boge, Adriana Lucia Pires Ferreira, Maria Cícera da Silva Carvalho, Márcia Aparecida Guimarães, Bruno de Souza Scramignon Costa3, Marcos Corrêa de Mattos, Sabrina Pires Maciel, Juliana Echevarria-Lima, Apurva Narechania, Kelsey O’Brien, Chanelle Ryan, Jeffrey S. Gerber, Bernadete Teixeira Ferreira Carvalho, Agnes Marie Sá Figueiredo4, and Paul J. Planet4Comments to Author 
Author affiliations: Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil (A.S. Viana, A.M.N. Botelho, A.L.P. Ferreira, M.C.S. Carvalho, M.A. Guimarães, B.S.S. Costa, M.C. Mattos, S.P. Maciel, J. Echevarria-Lima, B.T.F. Carvalho, A.M.S. Figueiredo); Children’s Hospital of Philadelphia, Philadelphia, Pennsylvania, USA (A.M. Moustafa, C.L.K. Boge, K. O’Brien, C. Ryan, J.S. Gerber, P.J. Planet); Diagnósticos da América S.A., Duque de Caxias, Brazil (A.L.P. Ferreira); American Museum of Natural History, New York, New York, USA (A. Narechania, P.J. Planet); University of Pennsylvania, Philadelphia (J.S. Gerber, P.J. Planet)

Main Article

Figure 1

Maximum-likelihood phylogenetic tree of 179 methicillin-resistant Staphylococcus aureus CC5 isolates from Rio de Janeiro, Brazil, 2014–2017 (red text) and 482 reference genomes (7). Red branches indicate the Rio de Janeiro clone of the lineage ST105(CC5)-SCCmecII-t002. Scale indicates substitutions per site. CC, clonal complex; SCC, staphylococcal chromosome cassette; ST, sequence type.

Figure 1. Maximum-likelihood phylogenetic tree of 179 methicillin-resistant Staphylococcus aureus CC5 isolates from Rio de Janeiro, Brazil, 2014–2017 (red text) and 482 reference genomes (7). Red branches indicate the Rio de Janeiro clone of the lineage ST105(CC5)-SCCmecII-t002. Scale indicates substitutions per site. CC, clonal complex; SCC, staphylococcal chromosome cassette; ST, sequence type.

Main Article

References
  1. Figueiredo  AMS, Ferreira  FA. The multifaceted resources and microevolution of the successful human and animal pathogen methicillin-resistant Staphylococcus aureus. Mem Inst Oswaldo Cruz. 2014;109:265–78. DOIPubMedGoogle Scholar
  2. Planet  PJ, Narechania  A, Chen  L, Mathema  B, Boundy  S, Archer  G, et al. Architecture of a species: phylogenomics of Staphylococcus aureus. Trends Microbiol. 2017;25:153–66. DOIPubMedGoogle Scholar
  3. Teixeira  LA, Resende  CA, Ormonde  LR, Rosenbaum  R, Figueiredo  AM, de Lencastre  H, et al. Geographic spread of epidemic multiresistant Staphylococcus aureus clone in Brazil. J Clin Microbiol. 1995;33:2400–4. DOIPubMedGoogle Scholar
  4. Silva-Carvalho  MC, Bonelli  RR, Souza  RR, Moreira  S, dos Santos  LCG, de Souza Conceição  M, et al. Emergence of multiresistant variants of the community-acquired methicillin-resistant Staphylococcus aureus lineage ST1-SCCmecIV in 2 hospitals in Rio de Janeiro, Brazil. Diagn Microbiol Infect Dis. 2009;65:300–5. DOIPubMedGoogle Scholar
  5. Chamon  RC, Ribeiro  SD, da Costa  TM, Nouér  SA, Dos Santos  KRN. Complete substitution of the Brazilian endemic clone by other methicillin-resistant Staphylococcus aureus lineages in two public hospitals in Rio de Janeiro, Brazil. Braz J Infect Dis. 2017;21:185–9. DOIPubMedGoogle Scholar
  6. Zuma  AVP, Lima  DF, Assef  APDC, Marques  EA, Leão  RS. Molecular characterization of methicillin-resistant Staphylococcus aureus isolated from blood in Rio de Janeiro displaying susceptibility profiles to non-β-lactam antibiotics. Braz J Microbiol. 2017;48:237–41. DOIPubMedGoogle Scholar
  7. Caiaffa-Filho  HH, Trindade  PA, Gabriela da Cunha  P, Alencar  CS, Prado  GVB, Rossi  F, et al. Methicillin-resistant Staphylococcus aureus carrying SCCmec type II was more frequent than the Brazilian endemic clone as a cause of nosocomial bacteremia. Diagn Microbiol Infect Dis. 2013;76:518–20. DOIPubMedGoogle Scholar
  8. Challagundla  L, Reyes  J, Rafiqullah  I, Sordelli  DO, Echaniz-Aviles  G, Velazquez-Meza  ME, et al. Phylogenomic classification and the evolution of clonal complex 5 methicillin-resistant Staphylococcus aureus in the Western Hemisphere. Front Microbiol. 2018;9:1901. DOIPubMedGoogle Scholar
  9. Arias  CA, Reyes  J, Carvajal  LP, Rincon  S, Diaz  L, Panesso  D, et al. A prospective cohort multicenter study of molecular epidemiology and phylogenomics of Staphylococcus aureus bacteremia in nine Latin American countries [Erratum in: Antimicrob Agents Chemother. 2017;61:e00095–18]. Antimicrob Agents Chemother. 2017;61:17. DOIGoogle Scholar
  10. Cockfield  JD, Pathak  S, Edgeworth  JD, Lindsay  JA. Rapid determination of hospital-acquired meticillin-resistant Staphylococcus aureus lineages. J Med Microbiol. 2007;56:614–9. DOIPubMedGoogle Scholar
  11. Milheiriço  C, Oliveira  DC, de Lencastre  H. Update to the multiplex PCR strategy for assignment of mec element types in Staphylococcus aureus [Erratum in: Antimicrob Agents Chemother. 2007;51:4537]. Antimicrob Agents Chemother. 2007;51:3374–7.DOIPubMedGoogle Scholar
  12. Beltrame  CO, Botelho  AMN, Silva-Carvalho  MC, Souza  RR, Bonelli  RR, Ramundo  MS, et al. Restriction modification (RM) tests associated to additional molecular markers for screening prevalent MRSA clones in Brazil. Eur J Clin Microbiol Infect Dis. 2012;31:2011–6. DOIPubMedGoogle Scholar
  13. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing: 28th informational supplement (M100-S28). Wayne (PA): The Institute; 2018.
  14. Zerbino  DR, Birney  E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 2008;18:821–9. DOIPubMedGoogle Scholar
  15. 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;19:455–77. DOIPubMedGoogle Scholar
  16. Stamatakis  A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312–3. DOIPubMedGoogle Scholar
  17. Ondov  BD, Starrett  GJ, Sappington  A, Kostic  A, Koren  S, Buck  CB, et al. Mash Screen: high-throughput sequence containment estimation for genome discovery. Genome Biol. 2019;20:232. DOIPubMedGoogle Scholar
  18. Moustafa  AM, Planet  PJ. WhatsGNU: a tool for identifying proteomic novelty. Genome Biol. 2020;21:58. DOIPubMedGoogle Scholar
  19. Didelot  X, Wilson  DJ. ClonalFrameML: efficient inference of recombination in whole bacterial genomes. PLOS Comput Biol. 2015;11:e1004041. DOIPubMedGoogle Scholar
  20. Bouckaert  R, Vaughan  TG, Barido-Sottani  J, Duchêne  S, Fourment  M, Gavryushkina  A, et al. BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLOS Comput Biol. 2019;15:e1006650. DOIPubMedGoogle Scholar
  21. Rambaut  A, Lam  TT, Max Carvalho  L, Pybus  OG. Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen). Virus Evol. 2016;2:vew007. DOIPubMedGoogle Scholar
  22. Aswani  V, Najar  F, Pantrangi  M, Mau  B, Schwan  WR, Shukla  SK. Virulence factor landscape of a Staphylococcus aureus sequence type 45 strain, MCRF184. BMC Genomics. 2019;20:123. DOIPubMedGoogle Scholar
  23. Novick  RP, Ram  G. Staphylococcal pathogenicity islands-movers and shakers in the genomic firmament. Curr Opin Microbiol. 2017;38:197–204. DOIPubMedGoogle Scholar
  24. Melehani  JH, James  DBA, DuMont  AL, Torres  VJ, Duncan  JA. Staphylococcus aureus leukocidin A/B (LukAB) kills human monocytes via host NLRP3 and ASC when extracellular, but not intracellular. PLoS Pathog. 2015;11:e1004970. DOIPubMedGoogle Scholar
  25. Panesso  D, Planet  PJ, Diaz  L, Hugonnet  JE, Tran  TT, Narechania  A, et al. Methicillin-susceptible, vancomycin-resistant Staphylococcus aureus, Brazil. Emerg Infect Dis. 2015;21:1844–8. DOIPubMedGoogle Scholar
  26. Sá-Leão  R, Santos Sanches  I, Dias  D, Peres  I, Barros  RM, de Lencastre  H. Detection of an archaic clone of Staphylococcus aureus with low-level resistance to methicillin in a pediatric hospital in Portugal and in international samples: relics of a formerly widely disseminated strain? J Clin Microbiol. 1999;37:1913–20. DOIPubMedGoogle Scholar
  27. Rokney  A, Baum  M, Ben-Shimol  S, Sagi  O, Anuka  E, Agmon  V, et al. Dissemination of the methicillin-resistant Staphylococcus aureus pediatric clone (ST5-T002-IV-PVL+) as a major cause of community-associated staphylococcal infections in Bedouin children, southern Israel. Pediatr Infect Dis J. 2019;38:230–5. DOIPubMedGoogle Scholar
  28. DeLeo  FR, Kennedy  AD, Chen  L, Bubeck Wardenburg  J, Kobayashi  SD, Mathema  B, et al. Molecular differentiation of historic phage-type 80/81 and contemporary epidemic Staphylococcus aureus. Proc Natl Acad Sci U S A. 2011;108:18091–6. DOIPubMedGoogle Scholar
  29. Ramundo  MS, Beltrame  CO, Botelho  AMN, Coelho  LR, Silva-Carvalho  MC, Ferreira-Carvalho  BT, et al. A unique SaeS allele overrides cell-density dependent expression of saeR and lukSF-PV in the ST30-SCCmecIV lineage of CA-MRSA. Int J Med Microbiol. 2016;306:367–80. DOIPubMedGoogle Scholar
  30. Roberts  RB, Chung  M, de Lencastre  H, Hargrave  J, Tomasz  A, Nicolau  DP, et al.; Tri-State MRSA Collaborative Study Group. Distribution of methicillin-resistant Staphylococcus aureus clones among health care facilities in Connecticut, New Jersey, and Pennsylvania. Microb Drug Resist. 2000;6:245–51. DOIPubMedGoogle Scholar
  31. Planet  PJ. Life after USA300: the rise and fall of a superbug. J Infect Dis. 2017;215(suppl_1):S71–7. DOIPubMedGoogle Scholar
  32. Carrel  M, Perencevich  EN, David  MZ. USA300 methicillin-resistant Staphylococcus aureus, United States, 2000–2013. Emerg Infect Dis. 2015;21:1973–80. DOIPubMedGoogle Scholar
  33. Almeida  ST, Nunes  S, Paulo  ACS, Faria  NA, de Lencastre  H, Sá-Leão  R. Prevalence, risk factors, and epidemiology of methicillin-resistant Staphylococcus aureus carried by adults over 60 years of age. Eur J Clin Microbiol Infect Dis. 2015;34:593–600. DOIPubMedGoogle Scholar
  34. Verghese  B, Schwalm  ND III, Dudley  EG, Knabel  SJ. A combined multi-virulence-locus sequence typing and Staphylococcal Cassette Chromosome mec typing scheme possesses enhanced discriminatory power for genotyping MRSA. Infect Genet Evol. 2012;12:1816–21. DOIPubMedGoogle Scholar
  35. Blanc  DS, Petignat  C, Wenger  A, Kuhn  G, Vallet  Y, Fracheboud  D, et al. Changing molecular epidemiology of methicillin-resistant Staphylococcus aureus in a small geographic area over an eight-year period. J Clin Microbiol. 2007;45:3729–36. DOIPubMedGoogle Scholar
  36. Faria  NA, Miragaia  M, de Lencastre  H; Multi Laboratory Project Collaborators. Massive dissemination of methicillin resistant Staphylococcus aureus in bloodstream infections in a high MRSA prevalence country: establishment and diversification of EMRSA-15. Microb Drug Resist. 2013;19:483–90. DOIPubMedGoogle Scholar
  37. Melo-Cristino  J, Resina  C, Manuel  V, Lito  L, Ramirez  M. First case of infection with vancomycin-resistant Staphylococcus aureus in Europe. Lancet. 2013;382:205. DOIPubMedGoogle Scholar
  38. Sullivan  MJ, Altman  DR, Chacko  KI, Ciferri  B, Webster  E, Pak  TR, et al. A complete genome screening program of clinical methicillin-resistant Staphylococcus aureus isolates identifies the origin and progression of a neonatal intensive care unit outbreak. J Clin Microbiol. 2019;57:e01261–19. DOIPubMedGoogle Scholar
  39. Iregui  A, Khan  Z, Malik  S, Landman  D, Quale  J. Emergence of delafloxacin-resistant Staphylococcus aureus in Brooklyn, New York. Clin Infect Dis. 2020;70:1758–60. DOIPubMedGoogle Scholar
  40. Omoe  K, Imanishi  K, Hu  D-L, Kato  H, Fugane  Y, Abe  Y, et al. Characterization of novel staphylococcal enterotoxin-like toxin type P. Infect Immun. 2005;73:5540–6. DOIPubMedGoogle Scholar
  41. Zdzalik  M, Kalinska  M, Wysocka  M, Stec-Niemczyk  J, Cichon  P, Stach  N, et al. Biochemical and structural characterization of SplD protease from Staphylococcus aureus. PLoS One. 2013;8:e76812. DOIPubMedGoogle Scholar
  42. Flannagan  RS, Heit  B, Heinrichs  DE. Antimicrobial mechanisms of macrophages and the immune evasion strategies of Staphylococcus aureus. Pathogens. 2015;4:826–68. DOIPubMedGoogle Scholar
  43. Le Pabic  H, Germain-Amiot  N, Bordeau  V, Felden  B. A bacterial regulatory RNA attenuates virulence, spread and human host cell phagocytosis. Nucleic Acids Res. 2015;43:9232–48. DOIPubMedGoogle Scholar

Main Article

1These first authors contributed equally to this article.

2Current affiliation: Fluminense Federal University, Niteroi, Brazil.

3Current affiliation: Fundação Oswaldo Cruz, Rio de Janeiro, Brazil.

4These authors were co–principal investigators.

Page created: August 16, 2021
Page updated: October 19, 2021
Page reviewed: October 19, 2021
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