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Clinical and molecular epidemiology of ciprofloxacin-susceptible MRSA encoding PVL in England and Wales

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Abstract

We aimed to enhance our case ascertainment of meticillin-resistant Staphylococcus aureus encoding Panton-Valentine leucocidin (PVL-MRSA), determine the patient demographic, risk factor and disease associations, and define the clonal diversity amongst isolates referred to the UK Health Protection Agency’s Staphylococcus Reference Unit. PVL-MRSA collected during 2005–6 from community-based and hospitalised patients located across England and Wales were identified by polymerase chain reaction (PCR). Representative geographically and temporally unrelated isolates were characterised via toxin gene profiling, SCCmec, spa and agr typing, multilocus sequence typing (MLST) and minimum inhibitory concentration (MIC) determinations. PVL-MRSA were identified from 275 patients. Affected individuals were <1 to 95 years of age (mean 30, median 27 years). Forty-five isolates were from 18 household or community-based clusters and 23 isolates were from outbreaks in healthcare settings. Overall, 58% (n = 161) had skin and soft tissue infections and 9% (n = 25) presented with or developed more serious disease, including eight patients (3%) with necrotising pneumonia, five of whom subsequently died. PVL-MRSA were genetically diverse and harboured SCCmecIV or VT/VII. Representatives of MLST clonal complexes (CCs) 8, 30 and 80 were identified the most often. The 275 PVL-MRSA included internationally disseminated community-associated MRSA (CA-MRSA) strains, as well as other minor lineages, and were associated with typical risk factors and disease presentations.

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References

  1. Johnson AP, Aucken HM, Cavendish S et al (2001) Dominance of EMRSA-15 and -16 among MRSA causing nosocomial bacteraemia in the UK: analysis of isolates from the European Antimicrobial Resistance Surveillance System (EARSS). J Antimicrob Chemother 48:143–144. doi:10.1093/jac/48.1.143

    Article  PubMed  CAS  Google Scholar 

  2. Oliveira D, Santos-Sanches I, Mato R et al (1998) Virtually all methicillin-resistant Staphylococcus aureus (MRSA) infections in the largest Portuguese teaching hospital are caused by two internationally spread multiresistant strains: the ‘Iberian’ and the ‘Brazilian’ clones of MRSA. Clin Microbiol Infect 4:373–384. doi:10.1111/j.1469-0691.1998.tb00081.x

    Article  PubMed  CAS  Google Scholar 

  3. Tenover FC, McAllister S, Fosheim G et al (2008) Characterization of Staphylococcus aureus isolates from nasal cultures collected from individuals in the United States in 2001 to 2004. J Clin Microbiol 46:2837–2841. doi:10.1128/JCM.00480-08

    Article  CAS  Google Scholar 

  4. Diederen BM, Kluytmans JA (2006) The emergence of infections with community-associated methicillin resistant Staphylococcus aureus. J Infect 52:157–168. doi:10.1016/j.jinf.2005.09.001

    Article  PubMed  CAS  Google Scholar 

  5. David MZ, Glikman D, Crawford SE et al (2008) What is community-associated methicillin-resistant Staphylococcus aureus? J Infect Dis 197:1235–1243. doi:10.1086/533502

    Article  PubMed  Google Scholar 

  6. Han LL, McDougal LK, Gorwitz RJ et al (2007) High frequencies of clindamycin and tetracycline resistance in methicillin-resistant Staphylococcus aureus pulsed-field type USA300 isolates collected at a Boston ambulatory health center. J Clin Microbiol 45:1350–1352. doi:10.1128/JCM.02274-06

    Article  PubMed  CAS  Google Scholar 

  7. Wang R, Braughton KR, Kretschmer D et al (2007) Identification of novel cytolytic peptides as key virulence determinants for community-associated MRSA. Nat Med 13:1510–1514. doi:10.1038/nm1656

    Article  PubMed  CAS  Google Scholar 

  8. Diep BA, Sensabaugh GF, Somboona NS et al (2004) Widespread skin and soft-tissue infections due to two methicillin-resistant Staphylococcus aureus strains harboring the genes for Panton-Valentine leucocidin. J Clin Microbiol 42:2080–2084. doi:10.1128/JCM.42.5.2080-2084.2004

    Article  PubMed  Google Scholar 

  9. Vandenesch F, Naimi T, Enright MC et al (2003) Community-acquired methicillin-resistant Staphylococcus aureus carrying Panton-Valentine leukocidin genes: worldwide emergence. Emerg Infect Dis 9:978–984

    PubMed  Google Scholar 

  10. Prevost G, Couppie P, Prevost P et al (1995) Epidemiological data on Staphylococcus aureus strains producing synergohymenotropic toxins. J Med Microbiol 42:237–245

    Article  PubMed  CAS  Google Scholar 

  11. Voyich JM, Otto M, Mathema B et al (2006) Is Panton-Valentine leukocidin the major virulence determinant in community-associated methicillin-resistant Staphylococcus aureus disease? J Infect Dis 194:1761–1770. doi:10.1086/509506

    Article  PubMed  CAS  Google Scholar 

  12. Labandeira-Rey M, Couzon F, Boisset S et al (2007) Staphylococcus aureus Panton-Valentine leukocidin causes necrotizing pneumonia. Science 315:1130–1133. doi:10.1126/science.1137165

    Article  PubMed  CAS  Google Scholar 

  13. Morgan MS (2007) Diagnosis and treatment of Panton-Valentine leukocidin (PVL)-associated staphylococcal pneumonia. Int J Antimicrob Agents 30:289–296. doi:10.1016/j.ijantimicag.2007.04.019

    Article  PubMed  CAS  Google Scholar 

  14. Udo EE, Pearman JW, Grubb WB (1993) Genetic analysis of community isolates of methicillin-resistant Staphylococcus aureus in Western Australia. J Hosp Infect 25:97–108. doi:10.1016/0195-6701(93)90100-E

    Article  PubMed  CAS  Google Scholar 

  15. Berglund C, Mölling P, Sjöberg L et al (2005) Multilocus sequence typing of methicillin-resistant Staphylococcus aureus from an area of low endemicity by real-time PCR. J Clin Microbiol 43:4448–4454. doi:10.1128/JCM.43.9.4448-4454.2005

    Article  PubMed  CAS  Google Scholar 

  16. Denis O, Deplano A, De Beenhouwer H et al (2005) Polyclonal emergence and importation of community-acquired methicillin-resistant Staphylococcus aureus strains harbouring Panton-Valentine leucocidin genes in Belgium. J Antimicrob Chemother 56:1103–1106. doi:10.1093/jac/dki379

    Article  PubMed  CAS  Google Scholar 

  17. Müller-Premru M, Strommenger B, Alikadic N et al (2005) New strains of community-acquired methicillin-resistant Staphylococcus aureus with Panton-Valentine leukocidin causing an outbreak of severe soft tissue infection in a football team. Eur J Clin Microbiol Infect Dis 24:848–850. doi:10.1007/s10096-005-0048-0

    Article  PubMed  Google Scholar 

  18. Witte W, Braulke C, Cuny C et al (2005) Emergence of methicillin-resistant Staphylococcus aureus with Panton-Valentine leukocidin genes in central Europe. Eur J Clin Microbiol Infect Dis 24:1–5. doi:10.1007/s10096-004-1262-x

    Article  PubMed  CAS  Google Scholar 

  19. King MD, Humphrey BJ, Wang YF et al (2006) Emergence of community-acquired methicillin-resistant Staphylococcus aureus USA 300 clone as the predominant cause of skin and soft-tissue infections. Ann Intern Med 144:309–317

    PubMed  Google Scholar 

  20. Kourbatova EV, Halvosa JS, King MD et al (2005) Emergence of community-associated methicillin-resistant Staphylococcus aureus USA 300 clone as a cause of health care-associated infections among patients with prosthetic joint infections. Am J Infect Control 33:385–391. doi:10.1016/j.ajic.2005.06.006

    Article  PubMed  Google Scholar 

  21. Seybold U, Kourbatova EV, Johnson JG et al (2006) Emergence of community-associated methicillin-resistant Staphylococcus aureus USA300 genotype as a major cause of health care-associated blood stream infections. Clin Infect Dis 42:647–656. doi:10.1086/499815

    Article  PubMed  CAS  Google Scholar 

  22. Guidance on the diagnosis and management of PVL-associated Staphylococcus aureus infections (PVL-SA) in England. Health Protection Agency. 7th November 2008. Available online at: http://www.hpa.org.uk/web/HPAwebFile/HPAweb_C/1226478464166

  23. Andrews JM; BSAC Working Party on Susceptibility Testing (2008) BSAC standardized disc susceptibility testing method (version 7). J Antimicrob Chemother 62:256–278. doi:10.1093/jac/dkn194

    Article  PubMed  CAS  Google Scholar 

  24. Holmes A, Ganner M, McGuane S et al (2005) Staphylococcus aureus isolates carrying Panton-Valentine leucocidin genes in England and Wales: frequency, characterization, and association with clinical disease. J Clin Microbiol 43:2384–2390. doi:10.1128/JCM.43.5.2384-2390.2005

    Article  PubMed  CAS  Google Scholar 

  25. Milheiriço C, Oliveira DC, de Lencastre H (2007) Update to the multiplex PCR strategy for assignment of mec element types in Staphylococcus aureus. Antimicrob Agents Chemother 51:3374–3377. doi:10.1128/AAC.00275-07

    Article  PubMed  CAS  Google Scholar 

  26. Milheiriço C, Oliveira DC, de Lencastre H (2007) Multiplex PCR strategy for subtyping the staphylococcal cassette chromosome mec type IV in methicillin-resistant Staphylococcus aureus: ‘SCCmec IV multiplex’. J Antimicrob Chemother 60:42–48. doi:10.1093/jac/dkm112

    Article  PubMed  CAS  Google Scholar 

  27. Kondo Y, Ito T, Ma XX et al (2007) Combination of multiplex PCRs for staphylococcal cassette chromosome mec type assignment: rapid identification system for mec, ccr, and major differences in junkyard regions. Antimicrob Agents Chemother 51:264–274. doi:10.1128/AAC.00165-06

    Article  PubMed  CAS  Google Scholar 

  28. Ito T, Katayama Y, Asada K et al (2001) Structural comparison of three types of staphylococcal cassette chromosome mec integrated in the chromosome in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 45:1323–1336. doi:10.1128/AAC.45.5.1323-1336.2001

    Article  PubMed  CAS  Google Scholar 

  29. Ito T, Ma XX, Takeuchi F et al (2004) Novel type V staphylococcal cassette chromosome mec driven by a novel cassette chromosome recombinase, ccrC. Antimicrob Agents Chemother 48:2637–2651. doi:10.1128/AAC.48.7.2637-2651.2004

    Article  PubMed  CAS  Google Scholar 

  30. Takano T, Higuchi W, Otsuka T et al (2008) Novel characteristics of community-acquired methicillin-resistant Staphylococcus aureus strains belonging to multilocus sequence type 59 in Taiwan. Antimicrob Agents Chemother 52:837–845. doi:10.1128/AAC.01001-07

    Article  PubMed  CAS  Google Scholar 

  31. Harmsen D, Claus H, Witte W et al (2003) Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management. J Clin Microbiol 41:5442–5448. doi:10.1128/JCM.41.12.5442-5448.2003

    Article  PubMed  CAS  Google Scholar 

  32. Enright MC, Day NP, Davies CE et al (2000) Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol 38:1008–1015

    PubMed  CAS  Google Scholar 

  33. Strommenger B, Kettlitz C, Weniger T et al (2006) Assignment of Staphylococcus isolates to groups by spa typing, SmaI macrorestriction analysis, and multilocus sequence typing. J Clin Microbiol 44:2533–2540. doi:10.1128/JCM.00420-06

    Article  PubMed  CAS  Google Scholar 

  34. Communicable Disease Report Weekly. Health Protection Agency. 17th March 2005. Available online at: http://www.hpa.org.uk/cdr/archives/2005/cdr1105.pdf

  35. Interim guidance on diagnosis and management of PVL-associated Staphylococcal infections in the UK. Health Protection Agency. 13th March 2007. Available online at: http://www.dh.gov.uk/en/AboutUs/MinistersAndDepartmentLeaders/ChiefMedicalOfficer/Features/DH_4133761

  36. Update CMO 45. Chief Medical Officer. Winter 2006. Available online at: http://www.dh.gov.uk/en/Publicationsandstatistics/Lettersandcirculars/CMOupdate/DH_062990

  37. Zetola N, Francis JS, Nuermberger EL et al (2005) Community-acquired meticillin-resistant Staphylococcus aureus: an emerging threat. Lancet Infect Dis 5:275–286. doi:10.1016/S1473-3099(05)70112-2

    Article  PubMed  Google Scholar 

  38. Beam JW, Buckley B (2006) Community-acquired methicillin-resistant Staphylococcus aureus: prevalence and risk factors. J Athl Train 41:337–340

    PubMed  Google Scholar 

  39. Francois P, Harbarth S, Huyghe A et al (2008) Methicillin-resistant Staphylococcus aureus, Geneva, Switzerland, 1993–2005. Emerg Infect Dis 14:304–307. doi:10.3201/eid1402.070229

    Article  PubMed  Google Scholar 

  40. Helgason KO, Jones ME, Edwards G (2008) Panton-valentine leukocidin-positive Staphylococcus aureus and foreign travel. J Clin Microbiol 46:832–833. doi:10.1128/JCM.02154-07

    Article  PubMed  Google Scholar 

  41. Ellington MJ, Yearwood L, Ganner M et al (2008) Distribution of the ACME-arcA gene among methicillin-resistant Staphylococcus aureus from England and Wales. J Antimicrob Chemother 61:73–77. doi:10.1093/jac/dkm422

    Article  PubMed  CAS  Google Scholar 

  42. Witte W, Strommenger B, Cuny C et al (2007) Methicillin-resistant Staphylococcus aureus containing the Panton-Valentine leucocidin gene in Germany in 2005 and 2006. J Antimicrob Chemother 60:1258–1263. doi:10.1093/jac/dkm384

    Article  PubMed  CAS  Google Scholar 

  43. Linde H, Wagenlehner F, Strommenger B et al (2005) Healthcare-associated outbreaks and community-acquired infections due to MRSA carrying the Panton-Valentine leucocidin gene in southeastern Germany. Eur J Clin Microbiol Infect Dis 24:419–422. doi:10.1007/s10096-005-1341-7

    Article  PubMed  CAS  Google Scholar 

  44. Chen CJ, Su LH, Chiu CH et al (2007) Clinical features and molecular characteristics of invasive community-acquired methicillin-resistant Staphylococcus aureus infections in Taiwanese children. Diagn Microbiol Infect Dis 59:287–293. doi:10.1016/j.diagmicrobio.2007.05.015

    Article  PubMed  CAS  Google Scholar 

  45. Ho PL, Chuang SK, Choi YF et al (2008) Community-associated methicillin-resistant and methicillin-sensitive Staphylococcus aureus: skin and soft tissue infections in Hong Kong. Diagn Microbiol Infect Dis 61:245–250

    Article  PubMed  CAS  Google Scholar 

  46. Fang H, Hedin G, Li G et al (2008) Genetic diversity of community-associated methicillin-resistant Staphylococcus aureus in southern Stockholm, 2000–2005. Clin Microbiol Infect 14:370–376. doi:10.1111/j.1469-0691.2007.01941.x

    Article  PubMed  CAS  Google Scholar 

  47. Yu F, Chen Z, Liu C et al (2008) Prevalence of Staphylococcus aureus carrying Panton-Valentine leukocidin genes among isolates from hospitalised patients in China. Clin Microbiol Infect 14:381–384

    Article  Google Scholar 

  48. Witte W, Mielke M (2007) Community MRSA. Zentralbl Chir 132:124–129. doi:10.1055/s-2007-960652

    Article  PubMed  CAS  Google Scholar 

  49. Wannet WJ, Heck ME, Pluister GN et al (2004) Panton-Valentine leukocidin positive MRSA in 2003: the Dutch situation. Euro Surveill 9:28–29

    PubMed  CAS  Google Scholar 

  50. Boyle-Vavra S, Ereshefsky B, Wang CC et al (2005) Successful multiresistant community-associated methicillin-resistant Staphylococcus aureus lineage from Taipei, Taiwan, that carries either the novel Staphylococcal chromosome cassette mec (SCCmec) type VT or SCCmec type IV. J Clin Microbiol 43:4719–4730. doi:10.1128/JCM.43.9.4719-4730.2005

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

The authors would like to thank the microbiologists and HPUs across England and Wales. Additional thanks go to Clare Martin for providing database support and Marjorie Ganner for providing data entry and technical assistance.

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Ellington, M.J., Perry, C., Ganner, M. et al. Clinical and molecular epidemiology of ciprofloxacin-susceptible MRSA encoding PVL in England and Wales. Eur J Clin Microbiol Infect Dis 28, 1113–1121 (2009). https://doi.org/10.1007/s10096-009-0757-x

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