Plasmid-encoded transferable mecb-mediated methicillin resistance in staphylococcus aureus

Emerging Infectious Diseases

Volumn 24, Issue 2, 2018, Pages 242-248

  Becker, Karsten ^a   van Alen, Sarah ^a   Idelevich, Evgeny A ^a   Schleimer, Nina ^a   Seggewiß, Jochen ^a   Mellmann, Alexander ^a   Kaspar, Ursula ^a   Peters, Georg ^a,b  

^a UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^b CiM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOGLYCOSIDE; BETA LACTAM; DIETHYLENE GLYCOL MONOMETHYL ETHER; MACROLIDE; R FACTOR; TETRACYCLINE DERIVATIVE; BACTERIAL PROTEIN;

AACA APHD GENE; AADK GENE; ANTIBIOTIC SENSITIVITY; APHA GENE; ARTICLE; BACTERIAL GENE; ERMB GENE; GENE SEQUENCE; HUMAN; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MECA GENE; MECB GENE; MECC GENE; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MICROARRAY ANALYSIS; MULTIDRUG RESISTANCE; MULTILOCUS SEQUENCE TYPING; PHENOTYPE; PLASMID; POLYMERASE CHAIN REACTION; REGULATOR GENE; STAPHYLOCOCCUS INFECTION; TETS GENE; WHOLE GENOME SEQUENCING; AGED; GENETICS; HORIZONTAL GENE TRANSFER; MALE; METHICILLIN RESISTANCE;

AGED; BACTERIAL PROTEINS; GENE TRANSFER, HORIZONTAL; HUMANS; MALE; METHICILLIN RESISTANCE; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; PLASMIDS;

EID: 85040932169     PISSN: 10806040     EISSN: 10806059     Source Type: Journal    
DOI: 10.3201/eid2402.171074     Document Type: Article

References (48)

1. deKraker ME, Davey PG, Grundmann H; BURDEN study group. Mortality and hospital stay associated with resistant Staphylococcus aureus and Escherichia coli bacteremia: estimating the burden of antibiotic resistance in Europe. PLoS Med. 2011;8:e1001104. http://dx.doi.org/10.1371/journal.pmed.1001104
2. Lee BY, Singh A, David MZ, Bartsch SM, Slayton RB, Huang SS, et al. The economic burden of community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA). Clin Microbiol Infect. 2013;19:528-36. http://dx.doi.org/10.1111/j.1469-0691.2012.03914.x
3. Becker K, Heilmann C, Peters G. Coagulase-negative staphylococci. Clin Microbiol Rev. 2014;27:870-926. http://dx.doi.org/10.1128/CMR.00109-13
4. Tong SY, Davis JS, Eichenberger E, Holland TL, Fowler VG Jr. Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management. Clin Microbiol Rev. 2015;28:603-61. http://dx.doi.org/10.1128/CMR.00134-14
5. Johnson AP. Methicillin-resistant Staphylococcus aureus: the European landscape. J Antimicrob Chemother. 2011;66(Suppl 4):iv43-8. http://dx.doi.org/10.1093/jac/dkr076
6. Chambers HF, Deleo FR. Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat Rev Microbiol. 2009;7:629-41. http://dx.doi.org/10.1038/nrmicro2200
7. Harris SR, Feil EJ, Holden MT, Quail MA, Nickerson EK, Chantratita N, et al. Evolution of MRSA during hospital transmission and intercontinental spread. Science. 2010;327:469-74. http://dx.doi.org/10.1126/science.1182395
8. Becker K, Ballhausen B, Kahl BC, Köck R. The clinical impact of livestock-associated methicillin-resistant Staphylococcus aureus of the clonal complex 398 for humans. Vet Microbiol. 2017;200:33-8. http://dx.doi.org/10.1016/j.vetmic.2015.11.013
9. Jevons MP. “Celbenin”-resistant staphylococci. BMJ. 1961;1:124-5. http://dx.doi.org/10.1136/bmj.1.5219.124-a
10. Peacock SJ, Paterson GK. Mechanisms of methicillin resistance in Staphylococcus aureus. Annu Rev Biochem. 2015;84:577-601. http://dx.doi.org/10.1146/annurev-biochem-060614-034516
11. Becker K, Ballhausen B, Köck R, Kriegeskorte A. Methicillin resistance in Staphylococcus isolates: the “mec alphabet” with specific consideration of mecC, a mec homolog associated with zoonotic S. aureus lineages. Int J Med Microbiol. 2014;304:794-804. http://dx.doi.org/10.1016/j.ijmm.2014.06.007
12. Shore AC, Deasy EC, Slickers P, Brennan G, O’Connell B, Monecke S, et al. Detection of staphylococcal cassette chromosome mec type XI carrying highly divergent mecA, mecI, mecR1, blaZ, and ccr genes in human clinical isolates of clonal complex 130 methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother. 2011;55:3765-73. http://dx.doi.org/10.1128/AAC.00187-11
13. García-Álvarez L, Holden MT, Lindsay H, Webb CR, Brown DF, Curran MD, et al. Meticillin-resistant Staphylococcus aureus with a novel mecA homologue in human and bovine populations in the UK and Denmark: a descriptive study. Lancet Infect Dis. 2011;11:595-603. http://dx.doi.org/10.1016/S1473-3099(11)70126-8
14. Beck WD, Berger-Bächi B, Kayser FH. Additional DNA in methicillin-resistant Staphylococcus aureus and molecular cloning of mec-specific DNA. J Bacteriol. 1986;165:373-8. http://dx.doi.org/10.1128/jb.165.2.373-378.1986
15. Baba T, Kuwahara-Arai K, Uchiyama I, Takeuchi F, Ito T, Hiramatsu K. Complete genome sequence of Macrococcus caseolyticus strain JCSCS5402, reflecting the ancestral genome of the human-pathogenic staphylococci. J Bacteriol. 2009;191:1180-90. http://dx.doi.org/10.1128/JB.01058-08
16. Tsubakishita S, Kuwahara-Arai K, Baba T, Hiramatsu K. Staphylococcal cassette chromosome mec-like element in Macrococcus caseolyticus. Antimicrob Agents Chemother. 2010;54:1469-75. http://dx.doi.org/10.1128/AAC.00575-09
17. Schwendener S, Cotting K, Perreten V. Novel methicillin resistance gene mecD in clinical Macrococcus caseolyticus strains from bovine and canine sources. Sci Rep. 2017;7:43797. http://dx.doi.org/10.1038/srep43797
18. Köck R, Werner P, Friedrich AW, Fegeler C, Becker K, Bindewald O, et al. Persistence of nasal colonization with human pathogenic bacteria and associated antimicrobial resistance in the German general population. New Microbes New Infect. 2016;9:24-34. http://dx.doi.org/10.1016/j.nmni.2015.11.004
19. Lowy FD. Antimicrobial resistance: the example of Staphylococcus aureus. J Clin Invest. 2003;111:1265-73. http://dx.doi.org/10.1172/JCI18535
20. Stojanov M, Moreillon P, Sakwinska O. Excision of staphylococcal cassette chromosome mec in methicillin-resistant Staphylococcus aureus assessed by quantitative PCR. BMC Res Notes. 2015;8:828. http://dx.doi.org/10.1186/s13104-015-1815-3
21. Borg MA, Hulscher M, Scicluna EA, Richards J, Azanowsky JM, Xuereb D, et al. Prevention of meticillin-resistant Staphylococcus aureus bloodstream infections in European hospitals: moving beyond policies. J Hosp Infect. 2014;87:203-11. http://dx.doi.org/10.1016/j.jhin.2014.05.003
22. Jurke A, Köck R, Becker K, Thole S, Hendrix R, Rossen J, et al. Reduction of the nosocomial meticillin-resistant Staphylococcus aureus incidence density by a region-wide search and follow-strategy in forty German hospitals of the EUREGIO, 2009 to 2011. Euro Surveill. 2013;18:20579. http://dx.doi.org/10.2807/1560-7917.ES2013.18.36.20579
23. Liu P, Wu Z, Xue H, Zhao X. Antibiotics trigger initiation of SCCmec transfer by inducing SOS responses. Nucleic Acids Res. 2017;45:3944-52. http://dx.doi.org/10.1093/nar/gkx153
24. Humphreys H, Becker K, Dohmen PM, Petrosillo N, Spencer M, van Rijen M, et al. Staphylococcus aureus and surgical site infections: benefits of screening and decolonization before surgery. J Hosp Infect. 2016;94:295-304. http://dx.doi.org/10.1016/j.jhin.2016.06.011
25. Mellmann A, Friedrich AW, Rosenkötter N, Rothgänger J, Karch H, Reintjes R, et al. Automated DNA sequence-based early warning system for the detection of methicillin-resistant Staphylococcus aureus outbreaks. PLoS Med. 2006;3:e33. http://dx.doi.org/10.1371/journal.pmed.0030033
26. Enright MC, Day NP, Davies CE, Peacock SJ, Spratt BG. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol. 2000;38:1008-15.
27. Becker K, Pagnier I, Schuhen B, Wenzelburger F, Friedrich AW, Kipp F, et al. Does nasal cocolonization by methicillin-resistant coagulase-negative staphylococci and methicillin-susceptible Staphylococcus aureus strains occur frequently enough to represent a risk of false-positive methicillin-resistant S. aureus determinations by molecular methods? J Clin Microbiol. 2006;44:229-31. http://dx.doi.org/10.1128/JCM.44.1.229-231.2006
28. Kriegeskorte A, Ballhausen B, Idelevich EA, Köck R, Friedrich AW, Karch H, et al. Human MRSA isolates with novel genetic homolog, Germany. Emerg Infect Dis. 2012;18:1016-8. http://dx.doi.org/10.3201/eid1806.110910
29. Murakami K, Minamide W, Wada K, Nakamura E, Teraoka H, Watanabe S. Identification of methicillin-resistant strains of staphylococci by polymerase chain reaction. J Clin Microbiol. 1991;29:2240-4.
30. Peters G, Becker K. Epidemiology, control and treatment of methicillin-resistant Staphylococcus aureus. Drugs. 1996;52(Suppl 2):50-4. http://dx.doi.org/10.2165/00003495-199600522-00011
31. Idelevich EA, Schaumburg F, Knaack D, Scherzinger AS, Mutter W, Peters G, et al. The recombinant bacteriophage endolysin HY-133 exhibits in vitro activity against different african clonal lineages of the Staphylococcus aureus complex, including Staphylococcus schweitzeri. Antimicrob Agents Chemother. 2016;60:2551-3. http://dx.doi.org/10.1128/AAC.02859-15
32. Idelevich EA, von Eiff C, Friedrich AW, Iannelli D, Xia G, Peters G, et al. In vitro activity against Staphylococcus aureus of a novel antimicrobial agent, PRF-119, a recombinant chimeric bacteriophage endolysin. Antimicrob Agents Chemother. 2011;55:4416-9. http://dx.doi.org/10.1128/AAC.00217-11
33. Meyer F, Goesmann A, McHardy AC, Bartels D, Bekel T, Clausen J, et al. GenDB—an open source genome annotation system for prokaryote genomes. Nucleic Acids Res. 2003;31:2187-95. http://dx.doi.org/10.1093/nar/gkg312
34. Zhang Z, Schwartz S, Wagner L, Miller W. A greedy algorithm for aligning DNA sequences. J Comput Biol. 2000;7:203-14. http://dx.doi.org/10.1089/10665270050081478
35. Nübel U, Roumagnac P, Feldkamp M, Song JH, Ko KS, Huang YC, et al. Frequent emergence and limited geographic dispersal of methicillin-resistant Staphylococcus aureus. Proc Natl Acad Sci U S A. 2008;105:14130-5. http://dx.doi.org/10.1073/pnas.0804178105
36. Becker K, Schaumburg F, Fegeler C, Friedrich AW, Köck R; Prevalence of Multiresistant Microorganisms PMM Study. Staphylococcus aureus from the German general population is highly diverse. Int J Med Microbiol. 2017;307:21-7. http://dx.doi.org/10.1016/j.ijmm.2016.11.007
37. Monecke S, Coombs G, Shore AC, Coleman DC, Akpaka P, Borg M, et al. A field guide to pandemic, epidemic and sporadic clones of methicillin-resistant Staphylococcus aureus. PLoS One. 2011;6:e17936. http://dx.doi.org/10.1371/journal.pone.0017936
38. Lanza VF, Tedim AP, Martínez JL, Baquero F, Coque TM. The plasmidome of Firmicutes: impact on the emergence and the spread of resistance to antimicrobials. Microbiol Spectr. 2015;3:PLAS-0039-2014. http://dx.doi.org/10.1128/microbiolspec.PLAS-0039-2014
39. Gómez-Sanz E, Schwendener S, Thomann A, Gobeli Brawand S, Perreten V. First staphylococcal cassette chromosome mec containing a mecB-carrying gene complex independent of transposon Tn6045 in a Macrococcus caseolyticus isolate from a canine infection. Antimicrob Agents Chemother. 2015;59:4577-83. http://dx.doi.org/10.1128/AAC.05064-14
40. Harrison EM, Paterson GK, Holden MT, Larsen J, Stegger M, Larsen AR, et al. Whole genome sequencing identifies zoonotic transmission of MRSA isolates with the novel mecA homologue mecC. EMBO Mol Med. 2013;5:509-15. http://dx.doi.org/10.1002/emmm.201202413
41. Larsen J, Clasen J, Hansen JE, Paulander W, Petersen A, Larsen AR, et al. Copresence of tet(K) and tet(M) in livestock-associated methicillin-resistant Staphylococcus aureus clonal complex 398 is associated with increased fitness during exposure to sublethal concentrations of tetracycline. Antimicrob Agents Chemother. 2016;60:4401-3. http://dx.doi.org/10.1128/AAC.00426-16
42. Ramsay JP, Kwong SM, Murphy RJ, Yui Eto K, Price KJ, Nguyen QT, et al. An updated view of plasmid conjugation and mobilization in Staphylococcus. Mob Genet Elements. 2016;6:e1208317. http://dx.doi.org/10.1080/2159256X.2016.1208317
43. McCarthy AJ, Lindsay JA. The distribution of plasmids that carry virulence and resistance genes in Staphylococcus aureus is lineage associated. BMC Microbiol. 2012;12:104. http://dx.doi.org/10.1186/1471-2180-12-104
44. Shearer JE, Wireman J, Hostetler J, Forberger H, Borman J, Gill J, et al. Major families of multiresistant plasmids from geographically and epidemiologically diverse staphylococci. G3 (Bethesda). 2011;1:581-91. http://dx.doi.org/10.1534/g3.111.000760
45. Chan LC, Basuino L, Diep B, Hamilton S, Chatterjee SS, Chambers HF. Ceftobiprole-and ceftaroline-resistant methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother. 2015;59:2960-3. http://dx.doi.org/10.1128/AAC.05004-14
46. Schaumburg F, Peters G, Alabi A, Becker K, Idelevich EA. Missense mutations of PBP2a are associated with reduced susceptibility to ceftaroline and ceftobiprole in African MRSA. J Antimicrob Chemother. 2016;71:41-4. http://dx.doi.org/10.1093/jac/dkv325
47. Farrell DJ, Castanheira M, Mendes RE, Sader HS, Jones RN. In vitro activity of ceftaroline against multidrug-resistant Staphylococcus aureus and Streptococcus pneumoniae: a review of published studies and the AWARE Surveillance Program (2008-2010). Clin Infect Dis. 2012;55(Suppl 3):S206-14. http://dx.doi.org/10.1093/cid/cis563
48. Zhang H, Xiao M, Kong F, O’Sullivan MV, Mao LL, Zhao HR, et al. A multicentre study of meticillin-resistant Staphylococcus aureus in acute bacterial skin and skin-structure infections in China: susceptibility to ceftaroline and molecular epidemiology. Int J Antimicrob Agents. 2015;45:347-50. http://dx.doi.org/10.1016/j.ijantimicag.2014.12.014