Cryptic resistance in Staphylococcus aureus: A risk for the treatment of skin infection?

Current Opinion in Infectious Diseases

Volumn 27, Issue 2, 2014, Pages 130-136

  Saeed, Kordo ^a   Marsh, Peter ^a   Ahmad, Nusreen ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

cryptic resistance; heteroresistant vancomycin intermediate S. aureus; MecC; oxacillin susceptible meticillin resistant S. aureus; small colony variants

Indexed keywords

CLINDAMYCIN; VANCOMYCIN;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; BACTERIUM COLONY; HUMAN; INFECTION RISK; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; NONHUMAN; REVIEW; SOFT TISSUE INFECTION; STAPHYLOCOCCAL SKIN INFECTION; STAPHYLOCOCCUS AUREUS;

ANTI-BACTERIAL AGENTS; DRUG RESISTANCE, MICROBIAL; HUMANS; SKIN DISEASES, BACTERIAL; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS;

EID: 84896707288     PISSN: 09517375     EISSN: 14736527     Source Type: Journal    
DOI: 10.1097/QCO.0000000000000046     Document Type: Review

References (74)

1. Garau J, Ostermann H, Medina J, et al. Current management of patients hospitalized with complicated skin and soft tissue infections across Europe (2010- 2011): assessment of clinical practice patterns and real-life effectiveness of antibiotics from the REACH study. Clin Microbiol Infect 2013; 19:E377-E385.
2. Jensen SO, Lyon BR. Genetics of antimicrobial resistance in Staphylococcus aureus. Future Microbiol 2009; 4:565-582.
3. Dryden M. Complicated skin and soft tissue infection. J Antimicrob Chemother 2010; 65 (Suppl 3):iii35-iii44.
4. Pantosti A, Sanchini A, Monaco M. Mechanisms of antibiotic resistance in Staphylococcus aureus. Future Microbiol 2007; 2:323-334.
5. Chambers HF. Methicillin resistance in staphylococci: molecular and biochemical basis and clinical implications. Clin Microbiol Rev 1997; 10: 781.
6. de Lencastre H, Tomasz A. Reassessment of the number of auxiliary genes essential for expression of high-level methicillin resistance in Staphylococcus aureus. Antimicrob Agents Chemother 1994; 38:2590.
7. Berger-Bächi B. Expression of resistance to methicillin. Trends Microbiol 1994; 2:389.
8. Cavassini M, Wenger A, Jaton K, et al. Evaluation of MRSA-screen, a simple anti-PBP 2a slide latex agglutination kit, for rapid detection of methicillin resistance in Staphylococcus aureus. J ClinMicrobiol 1999; 37:1591-1594.
9. Murakami K, Minamide W, Wada K, et al. Identification of methicillin-resistant strains of staphylococci by polymerase chain reaction. J Clin Microbiol 1991; 29:2240-2244.
10. Sakoulas G, Gold HS, Venkataraman L, et al. Methicillin-resistant Staphylococcus aureus: comparison of susceptibility testing methods and analysis of mecA-positive susceptible strains. J Clin Microbiol 2001; 39:3946-3951.
11. van Griethuysen A, Pouw M, van Leeuwen N, et al. Rapid slide latex agglutination test for detection of methicillin resistance in Staphylococcus aureus. J Clin Microbiol 1999; 37:2789-2792.
12. Saeed K, Dryden M, Parnaby R. Oxacillin-susceptible MRSA, the emerging MRSA clone in the UK? J Hosp Infect 2010; 76:267-268.
13. Saeed K, Green S, Ahmed N, Dryden M. Oxacillin-susceptible meticillinresistant Staphylococcus aureus: an emerging threat for UK hospitals? Poster presentation No. 16 at the Health Protection Agency Annual Conference; 13-14 September 2011; Warwick, UK. https://www.hpa-events.org.uk/hpa/frontend/ reg/titem.csp?pageID=62084&eventID=127&eventID=127. [Accessed 22 October 2013].
14. Anil Kumar V, Steffy K, Chatterjee M. Detection of oxacillin-susceptible mecA-positive Staphylococcus aureus isolates by use of chromogenic medium MRSA ID. J Clin Microbiol 2013; 51:318-319.
15. Arabela Cuirolo A, Canigia LF, Gardella N, et al. Oxacillin- and cefoxitinsusceptible meticillin-resistant Staphylococcus aureus (MRSA). Int J Antimicrob Agents 2011; 37:178-179.
16. Ikonomidis A, Michail G, Vasdeki A, et al. In vitro and in vivo evaluations of oxacillin efficiency against mecA-positive oxacillin-susceptible Staphylococcus aureus. Antimicrob Agents Chemother 2008; 52:3905-3908.
17. Ito T, Hiramatsu K, Tomasz A, et al. Guidelines for reporting novel mecA gene homologues. Antimicrob Agents Chemother 2012; 56:4997-4999.
18. García-Álvarez L, Holden MTG, Lindsay H, 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.
19. Edward JP, Cartwrighta BC, Gavin K, et al. Use of Vitek 2 antimicrobial susceptibility profile to identify MECC in methicillin-resistant Staphylococcus aureus. J Clin Microbiol 2013; 51:2732-2734.
20. García-Garrote F, Cercenado E, Marín M, et al. Methicillin-resistant Staphylococcus aureus carrying the mecC gene: emergence in Spain and report of a fatal case of bacteraemia. J Antimicrob Chemother 2014; 69:45-50.
21. Cuny C, Layer F, Strommenger B, Witte W. Rare occurrence of methicillinresistant Staphylococcus aureus CC130 with a novel mecA homologue in humans in Germany. PLoS ONE 2011; 6:e24360.
22. Paterson GK, Larsen AR, Robb A, et al. The newly described mecA homologue, mecA(LGA251), is present in methicillin-resistant Staphylococcus aureus isolates from a diverse range of host species. J Antimicrob Chemother 2012; 67:2809-2813.
23. Pichon B, Hill R, Laurent F, et al. Development of a real-time quadruplex PCR assay for simultaneous detection of nuc, Panton Valentine leucocidin (PVL), mecA and homologue mecA(LGA251). J Antimicrob Chemother 2012; 67:2338-2341.
24. Stegger M, Andersen PS, Kearns A, et al. Rapid detection, differentiation and typing of methicillin-resistant Staphylococcus aureus harbouring either mecA or the new mecA homologue mecA(LGA251). Clin Microbiol Infect 2012; 18:395-400.
25. Sabat AJ, Koksal M, Akkerboom V, et al. Detection of new methicillin-resistant Staphylococcus aureus strains that carry a novel genetic homologue and important virulence determinants. J Clin Microbiol 2012; 50:3374-3377.
26. Shore AC, Deasy EC, Slickers P, 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 methicillinresistant Staphylococcus aureus. Antimicrob Agents Chemother 2011; 55:3765-3773.
27. Laurent F, Chardon H, Haenni M, et al. MRSA harboring mecA variant gene mecC, France. Emerg Infect Dis 2012; 18:1465-1467.
28. Hellman J, Olsson-Liljequist B. A report on Swedish antibiotic utilisation and resistance in human medicine. Solna, Sweden: Swedish Institute for Communicable Disease Control; 2012. www.smi.se/publikationer or www. sva.se. [Accessed on 12 October 2013]
29. Schaumburg F, Köck R, Mellmann A, et al. Population dynamics among methicillin-resistant Staphylococcus aureus isolates in Germany during a 6-year period. J Clin Microbiol 2012; 50:3186-3192.
30. Basset P, Prod'hom G, Senn L, et al. Very low prevalence of meticillinresistant Staphylococcus aureus carrying the mecC gene in western Switzerland. J Hosp Infect 2013; 83:257-259.
31. Medhus A, Slettemeas JS, Marstein L, et al. Methicillin-resistant Staphylococcus aureus with the novel mecC gene variant isolated from a cat suffering from chronic conjunctivitis. J Antimicrob Chemother 2013; 68:968-969.
32. Monecke S, Gavier-Widen D, Mattsson R, et al. Detection of mecC-positive Staphylococcus aureus (CC130-MRSA-XI) in diseased European Hedgehogs (Erinaceus europaeus) in Sweden. PLoS ONE 2013; 8:e66166.
33. Harrison EM, Paterson GK, Holden MTG, et al. Whole genome sequencing identifies zoonotic transmission of MRSA isolates with the novel mecA homologue mecC. EMBO Mol Med 2013; 5:509-515.
34. Petersen A, Stegger M, Heltberg O, et al. Epidemiology of methicillin-resistant Staphylococcus aureus carrying the novel mecC gene in Denmark corroborates a zoonotic reservoir with transmission to humans. Clin Microbiol Infect 2013; 19:E16-22.
35. Chang S, Sievert DM, Hageman JC, et al. Infection with vancomycin resistant Staphylococcus aureus containing the vanA resistance gene. N Engl J Med 2003; 348:1342-1347.
36. Hiramatsu K, Aritaka N, Hanaki H, et al. Dissemination in Japanese hospitals of strains of Staphylococcus aureus heterogeneously resistant to vancomycin. Lancet 1997; 350:1670-1673.
37. Hiramatsu K, Hanaki H, Ino T, et al. Methicillin-resistant Staphylococcus aureus clinical strain with reduced vancomycin susceptibility. J Antimicrob Chemother 1997; 40:135.
38. Wootton M, Howe RA, Hillman R, et al. A modified population analysis profile (PAP) method to detect hetero-resistance to vancomycin in Staphylococcus aureus in a UK hospital. J Antimicrob Chemother 2001; 47:399-403.
39. Tenover FC, Moellering RC Jr. The rationale for revising the Clinical and Laboratory Standards Institute vancomycin minimal inhibitory concentration interpretive criteria for Staphylococcus aureus. Clin Infect Dis 2007; 44: 1208.
40. Wong SS, Ho PL, Woo PC, Yuen KY. Bacteremia caused by staphylococci with inducible vancomycin heteroresistance. Clin Infect Dis 1999; 29:760.
41. Charles PG, Ward PB, Johnson PD, et al. Clinical features associated with bacteremia due to heterogeneous vancomycin intermediate Staphylococcus aureus. Clin Infect Dis 2004; 38:448-451.
42. Howden BP, Ward PB, Charles PG, et al. Treatment outcomes for serious infections caused by methicillin-resistant Staphylococcus aureus with reduced vancomycin susceptibility. Clin Infect Dis 2004; 38:521-528.
43. Musta AC, Riederer K, Shemes S, et al. Vancomycin MIC plus heteroresistance and outcome of methicillin-resistant Staphylococcus aureus bacteremia: trends over 11 years. J Clin Microbiol 2009; 47:1640-1644.
44. Fridkin SK, Hageman J, McDougal LK, et al. Epidemiological and microbiological characterization of infections caused by Staphylococcus aureus with reduced susceptibility to vancomycin, United States, 1997-2001. Clin Infect Dis 2003; 36:429-439.
45. Horne KC, Howden BP, Grabsch EA, et al. Prospective comparison of the clinical impacts of heterogeneous vancomycin-intermediate methicillinresistant Staphylococcus aureus (MRSA) and vancomycin susceptible MRSA. Antimicrob Agents Chemother 2009; 53:3447-3452.
46. Price J, Atkinson S, Llewelyn M, Paul J. Paradoxical relationship between the clinical outcome of Staphylococcus aureus bacteremia and the minimum inhibitory concentration of vancomycin. Clin Infect Dis 2009; 48:997-998.
47. Soriano A, Marco F, Martinez JA, et al. Influence of vancomycin minimum inhibitory concentration on the treatment of methicillin-resistant Staphylococcus aureus bacteremia. Clin Infect Dis 2008; 46:193-200.
48. van Hal SJ, Paterson DL. Systematic review and meta-analysis of the significance of heterogeneous vancomycin-intermediate Staphylococcus aureus isolates. Antimicrob Agents Chemother 2011; 55:405-410.
49. van Hal SJ, Lodise TP, Paterson DL. The clinical significance of vancomycin minimum inhibitory concentration in Staphylococcus aureus infections: a systematic review and meta-analysis. Clin Infect Dis 2012; 54:755-771.
50. Howden BP, Smith DJ, Mansell A, et al. Different bacterial gene expression patterns and attenuated host immune responses are associated with the evolution of low-level vancomycin resistance during persistent methicillinresistant Staphylococcus aureus bacteraemia. BMC Microbiol 2008; 8:39.
51. Cui L, Tominaga E, Neoh HM, et al. Correlation between reduced daptomycin susceptibility and vancomycin resistance in vancomycin intermediate Staphylococcus aureus. Antimicrob Agents Chemother 2006; 50:1079-1082.
52. Sakoulas G, Alder J, Thauvin-Eliopoulos C, et al. Induction of daptomycin heterogeneous susceptibility in Staphylococcus aureus by exposure to vancomycin. Antimicrob Agents Chemother 2006; 50:1581-1585.
53. Sader HS, Becker HK, Moet GJ, Jones RN. Antimicrobial activity of daptomycin tested against Staphylococcus aureus with vancomycin MIC of 2 microg/mL isolated in the United States and European hospitals (2006-2008). Diagn Microbiol Infect Dis 2010; 66:329-331.
54. von Eiff C, Peters G, Becker K. The small colony variant (SCV) concept: the role of staphylococcal SCVs in persistent infections. Injury 2006; 37 (Suppl 2):S26-S33.
55. Proctor RA, von Eiff C, Kahl BC, et al. Small colony variants: a pathogenic form of bacteria that facilitates persistent and recurrent infections. Nat Rev Microbiol 2006; 4:295-305.
56. Gao W, Chua K, Davies JK, et al. Two novel point mutations in clinical Staphylococcus aureus reduce linezolid susceptibility and switch on the stringent response to promote persistent infection. PLoS Pathog 2010; 6:e1000944.
57. von Eiff C. Staphylococcus aureus small colony variants: a challenge to microbiologists and clinicians. Int J Antimicrob Agents 2008; 31:507-510.
58. Proctor RA, van Langevelde P, Kristjansson M, et al. Persistent and relapsing infections associated with small-colony variants of Staphylococcus aureus. Clin Infect Dis 1995; 20:95-102.
59. Edwards AM. Phenotype switching is a natural consequence of Staphylococcus aureus replication. J Bacteriol 2012; 194:5404-5412.
60. Wolter DJ, Emerson JC, McNamara S, et al. Staphylococcus aureus smallcolony variants are independently associated with worse lung disease in children with cystic fibrosis. Clin Infect Dis 2013; 57:384-391.
61. Chuard C, Vaudaux PE, Proctor RA, et al. Decreased susceptibility to antibiotic killing of a stable small colony variant of Staphylococcus aureus in fluid phase and on fibronectin-coated surfaces. J Antimicrob Chemother 1997; 39:603-608.
62. Garcia LG, Lemaire S, Kahl BC, et al. Intracellular forms of menadionedependent small-colony variants of methicillin-resistant Staphylococcus aureus are hypersusceptible to b-lactams in a THP-1 cell model due to cooperation between vacuolar acidic pH and oxidant species. J Antimicrob Chemother 2012; 67:2873-2881.
63. Garcia LG, Lemaire S, Kahl BC, et al. Antibiotic activity against small-colony variants of Staphylococcus aureus: review of in vitro, animal and clinical data. J Antimicrob Chemother 2013; 68:1455-1464.
64. Hamblin MR, Hasan T. Photodynamic therapy: a new antimicrobial approach to infectious disease? Photochem Photobiol Sci 2004; 3:436-450.
65. Tubby S, Wilson M, Wright JA, et al. Staphylococcus aureus small colony variants are susceptible to light activated antimicrobial agents. BMC Microbiol 2013; 13:201.
66. Lewis JS, Jorgensen JH. Inducible clindamycin resistance in staphylococci: should clinicians and microbiologists be concerned? Clin Infect Dis 2005; 40:280-285.
67. Liu C, Bayer A, Cosgrove SE, et al. Clinical practice guidelines by the Infectious Diseases Society of America for the treatment of methicillinresistant Staphylococcus aureus infections in adults and children. Clin Infect Dis 2011; 52:e18-e55.
68. Labreche MJ, Lee GC, Attridge RT, et al. Treatment failure and costs in patients with methicillin-resistant Staphylococcus aureus (MRSA) skin and soft tissue infections: a South Texas Ambulatory Research Network (STARNet) Study. J Am Board Fam Med 2013; 26:508-517.
69. Soriano A, Martinez JA, Mensa J, et al. Pathogenic significance of methicillin resistance for patients with Staphylococcus aureus bacteremia. Clin Infect Dis 2000; 30:368-373.
70. Melzer M, Eykyn SJ, Gransden WR, Chinn S. Is methicillin-resistant Staphylococcus aureus more virulent than methicillin-susceptible S. aureus? A comparative cohort study of British patients with nosocomial infection and bacteremia. Clin Infect Dis 2003; 37:1453-1460.
71. Kumar A, Roberts D, Wood KE, et al. Duration of hypotension before initiation of effective antimicrobial therapy is the critical determinant of survival in human septic shock. Crit Care Med 2006; 34:1589-1596.
72. Frei CR, Miller ML, Lewis JS, et al. Trimethoprim-sulfamethoxazole or clindamycin for community-associated MRSA (CA-MRSA) skin infections. J Am Board Fam Med 2010; 23:714-719.
73. Menzin J, Marton JP, Meyers JL, et al. Inpatient treatment patterns, outcomes, and costs of skin and skin structure infections because of Staphylococcus aureus. Am J Infect Control 2009; 38:44-49.
74. Kumar K, Chopra S. New drugs for methicillin-resistant Staphylococcus aureus: an update. J Antimicrob Chemother 2013; 68:1465-1470.