Clonal replacement of epidemic methicillin-resistant Staphylococcus aureus strains in a German University Hospital over a period of eleven years

PLoS ONE

Volumn 6, Issue 11, 2011, Pages

  Albrecht, Nicole ^a,b   Jatzwauk, Lutz ^c   Slickers, Peter ^d   Ehricht, Ralf ^d   Monecke, Stefan ^a,d  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b Hochschule Lausitz (FH) University of Applied Sciences   (Germany)

^c UNIVERSITY HOSPITAL CARL GUSTAV CARUS   (Germany)

^d Alere Technologies GmbH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADOLESCENT; ADULT; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL STRAIN; BACTERIUM IDENTIFICATION; BACTERIUM ISOLATE; CLONAL REPLACEMENT; CONTROLLED STUDY; DNA MICROARRAY; FEMALE; GENETIC RESISTANCE; GENOTYPE; GERMANY; HUMAN; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MICROARRAY ANALYSIS; MICROBIAL POPULATION DYNAMICS; MOUSE; NONHUMAN; POPULATION ABUNDANCE; TREND STUDY; UNIVERSITY HOSPITAL;

ADOLESCENT; ADULT; CHILD; CLONE CELLS; EPIDEMICS; FEMALE; GERMANY; HOSPITALS, UNIVERSITY; HUMANS; MALE; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MIDDLE AGED; STAPHYLOCOCCAL INFECTIONS; TIME FACTORS;

EID: 82355170967     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0028189     Document Type: Article

References (72)

1. Jevons MP, (1961) "Celbenin"-resistant Staphylococci. British Medical Journal 1: 1924-1925.
2. Hartman B, Tomasz A, (1981) Altered penicillin-binding proteins in methicillin-resistant strains of Staphylococcus aureus. Antimicrob Agents Chemother 19: 726-735.
3. IWG-SCC (2009) Classification of staphylococcal cassette chromosome mec (SCCmec): guidelines for reporting novel SCCmec elements. Antimicrob Agents Chemother 53: 4961-7.
4. Ito T, Katayama Y, Asada K, Mori N, Tsutsumimoto 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: 1323-36.
5. Hiramatsu K, Cui L, Kuroda M, Ito T, (2001) The emergence and evolution of methicillin-resistant Staphylococcus aureus. Trends in Microbiology 9: 486-493.
6. Ito T, Okuma K, Ma XX, Yuzawa H, Hiramatsu K, (2003) Insights on antibiotic resistance of Staphylococcus aureus from its whole genome: genomic island SCC. Drug Resist Updat 6: 41-52.
7. Ito T, Ma XX, Takeuchi F, Okuma K, Yuzawa H, et al. (2004) Novel type V staphylococcal cassette chromosome mec driven by a novel cassette chromosome recombinase, ccrC. Antimicrob Agents Chemother 48: 2637-51.
8. Grundmann H, Hori S, Winter B, Tami A, Austin DJ, (2002) Risk factors for the transmission of methicillin-resistant Staphylococcus aureus in an adult intensive care unit: fitting a model to the data. J Infect Dis 185: 481-8.
9. Vandenesch F, Naimi T, Enright MC, Lina G, Nimmo GR, et al. (2003) Community-acquired methicillin-resistant Staphylococcus aureus carrying Panton-Valentine leukocidin genes: worldwide emergence. Emerg Infect Dis 9: 978-84.
10. Van de Velde H, (1894) Etude sur le mécanisme de la virulence du Staphylocoque pyogène. La Cellule 10: 401-410.
11. Panton P, Valentine F, (1932) Staphylococcal toxin. Lancet 1: 506-508.
12. Voss A, Loeffen F, Bakker J, Klaassen C, Wulf M, (2005) Methicillin-resistant Staphylococcus aureus in pig farming. Emerg Infect Dis 11: 1965-6.
13. Huijsdens XW, van Dijke BJ, Spalburg E, van Santen-Verheuvel MG, Heck ME, et al. (2006) Community-acquired MRSA and pig-farming. Ann Clin Microbiol Antimicrob 5: 26.
14. van Loo I, Huijsdens X, Tiemersma E, de Neeling A, van de Sande-Bruinsma N, et al. (2007) Emergence of methicillin-resistant Staphylococcus aureus of animal origin in humans. Emerg Infect Dis 13: 1834-9.
15. Shore A, Rossney AS, Keane CT, Enright MC, Coleman DC, (2005) Seven novel variants of the staphylococcal chromosomal cassette mec in methicillin-resistant Staphylococcus aureus isolates from Ireland. Antimicrob Agents Chemother 49: 2070-83.
16. Rossney AS, Lawrence MJ, Morgan PM, Fitzgibbon MM, Shore A, et al. (2006) Epidemiological typing of MRSA isolates from blood cultures taken in Irish hospitals participating in the European Antimicrobial Resistance Surveillance System (1999-2003). Eur J Clin Microbiol Infect Dis 25: 79-89.
17. Shore AC, Rossney AS, Kinnevey PM, Brennan OM, Creamer E, et al. (2010) Enhanced discrimination of highly clonal ST22-methicillin-resistant Staphylococcus aureus IV isolates achieved by combining spa, dru, and pulsed-field gel electrophoresis typing data. J Clin Microbiol 48: 1839-52.
18. Amorim ML, Faria NA, Oliveira DC, Vasconcelos C, Cabeda JC, et al. (2007) Changes in the Clonal Nature and Antibiotic Resistance Profiles of Methicillin-Resistant Staphylococcus aureus Isolates Associated with Spread of the EMRSA-15 Clone in a Tertiary Care Portuguese Hospital. J Clin Microbiol 45: 2881-2888.
19. Amorim M, Aires de Sousa M, Sanches I, Sa-Leao R, Cabeda J, et al. (2002) Clonal and antibiotic resistance profiles of methicillin-resistant Staphylococcus aureus (MRSA) from a Portuguese hospital over time. Microb Drug Resist 8: 301-9.h
20. Aires de Sousa M, Correia B, de Lencastre H, (2008) Changing patterns in frequency of recovery of five methicillin-resistant Staphylococcus aureus clones in Portuguese hospitals: surveillance over a 16-year period. J Clin Microbiol 46: 2912-7.
21. Ma XX, Ito T, Chongtrakool P, Hiramatsu K, (2006) Predominance of clones carrying Panton-Valentine leukocidin genes among methicillin-resistant Staphylococcus aureus strains isolated in Japanese hospitals from 1979 to 1985. J Clin Microbiol 44: 4515-27.
22. Velazquez-Meza ME, Aires de Sousa M, Echaniz-Aviles G, Solorzano-Santos F, Miranda-Novales G, et al. (2004) Surveillance of methicillin-resistant Staphylococcus aureus in a pediatric hospital in Mexico City during a 7-year period (1997 to 2003): clonal evolution and impact of infection control. J Clin Microbiol 42: 3877-80.
23. Conceicao T, Aires-de-Sousa M, Fuzi M, Toth A, Paszti J, et al. (2007) Replacement of methicillin-resistant Staphylococcus aureus clones in Hungary over time: a 10-year surveillance study. Clin Microbiol Infect 13: 971-9.
24. Diep BA, Otto M, (2008) The role of virulence determinants in community-associated MRSA pathogenesis. Trends in Microbiology 16: 361-369.
25. Monecke S, Coombs G, Shore AC, Coleman DC, Akpaka P, et al. (2011) A Field Guide to Pandemic, Epidemic and Sporadic Clones of Methicillin-Resistant Staphylococcus aureus. PLoS ONE 6: e17936.
26. Tavares DA, Sa-Leao R, Miragaia M, de Lencastre H, (2010) Large screening of CA-MRSA among Staphylococcus aureus colonizing healthy young children living in two areas (urban and rural) of Portugal. BMC Infect Dis 10: 110.
27. Tenover FC, McAllister S, Fosheim G, McDougal LK, Carey RB, 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: 2837-41.
28. Ellington MJ, Ganner M, Warner M, Cookson BD, Kearns AM, (2010) Polyclonal multiply antibiotic-resistant methicillin-resistant Staphylococcus aureus with Panton-Valentine leucocidin in England. J Antimicrob Chemother 65: 46-50.
29. Dsouza N, Rodrigues C, Mehta A, (2010) Molecular characterization of Methicillin resistant Staphylococcus aureus (MRSA) with emergence of epidemic clones ST 22 and ST 772, in Mumbai, India. J Clin Microbiol 48: 1806-11.
30. Monecke S, Slickers P, Hotzel H, Richter-Huhn G, Pohle M, et al. (2006) Microarray-based characterisation of a Panton-Valentine leukocidin-positive community-acquired strain of methicillin-resistant Staphylococcus aureus. Clin Microbiol Infect 12: 718-728.
31. Conceicao T, Tavares A, Miragaia M, Hyde K, Aires-de-Sousa M, et al. (2010) Prevalence and clonality of methicillin-resistant Staphylococcus aureus (MRSA) in the Atlantic Azores islands: predominance of SCCmec types IV, V and VI. Eur J Clin Microbiol Infect Dis 29: 543-50.
32. Ellington MJ, Hope R, Livermore DM, Kearns AM, Henderson K, et al. (2010) Decline of EMRSA-16 amongst methicillin-resistant Staphylococcus aureus causing bacteraemias in the UK between 2001 and 2007. J Antimicrob Chemother 65: 446-8.
33. Scicluna E, Shore A, Thuermer A, Ehricht R, Slickers P, et al. (2010) Characterisation of MRSA from Malta and the description of a Maltese epidemic MRSA strain. Eur J Clin Microbiol Infect Dis 29: 163-170.
34. Witte W, Enright M, Schmitz FJ, Cuny C, Braulke C, et al. (2001) Characteristics of a new epidemic MRSA in Germany ancestral to United Kingdom EMRSA 15. Int J Med Microbiol 290: 677-82.
35. Witte W, (2005) The situation of MRSA in Germany: report from the national reference centre for Staphylococci [Zur MRSA-Situation in Deutschland im Jahr 2004: Bericht aus dem Nationalen Referenzzentrum für Staphylokokken]. Epidemiologisches Bulletin pp. 376-80.
36. Monecke S, Jatzwauk L, Weber S, Slickers P, Ehricht R, (2008) DNA Microarray based genotyping of MRSA strains from Eastern Saxony. Clin Microbiol Infect 14: 534-45.
37. Witte W, Braulke C, Heuck D, Cuny C, (2000) Methicillin resistant Staphylococcus aureus in German hospitals develop narrower patterns of antimicrobial resistance. Euro Surveill 5: 31-34.
38. Witte W, Heuck D, Braulke C, (2000) Tätigkeitsbericht des Nationalen Referenzzentrums für Staphylokokken im Jahr 1999. Bundesgesundheitsbl- Gesundheitsforsch- Gesundheitsschutz 43: 633-638.
39. Deurenberg RH, Nulens E, Valvatne H, Sebastian S, Driessen C, et al. (2009) Cross-border dissemination of methicillin-resistant Staphylococcus aureus, Euregio Meuse-Rhin region. Emerg Infect Dis 15: 727-34.
40. Witte W, Cuny C, Braulke C, Heuck D, Klare I, (1997) Widespread dissemination of epidemic MRSA in German hospitals. Euro Surveill 2: 25-28.
41. Campanile F, Bongiorno D, Borbone S, Stefani S, (2009) Hospital-associated methicillin-resistant Staphylococcus aureus (HA-MRSA) in Italy. Annals of Clinical Microbiology and Antimicrobials 8: 22.
42. Cuevas O, Cercenado E, Bouza E, Castellares C, Trincado P, et al. (2007) Molecular epidemiology of methicillin-resistant Staphylococcus aureus in Spain: a multicentre prevalence study (2002). Clin Microbiol Infect 13: 250-6.
43. Walther B, Monecke S, Ruscher C, Friedrich AW, Ehricht R, et al. (2009) Comparative molecular analysis substantiates a zoonotic potential of equine Methicillin-resistant Staphylococcus aureus (MRSA). J Clin Microbiol 47: 704-710.
44. Cuny C, Kuemmerle J, Stanek C, Willey B, Strommenger B, et al. (2006) Emergence of MRSA infections in horses in a veterinary hospital: strain characterisation and comparison with MRSA from humans. Euro Surveill 11: 44-7.
45. Smyth DS, McDougal LK, Gran FW, Manoharan A, Enright MC, et al. (2010) Population structure of a hybrid clonal group of methicillin-resistant Staphylococcus aureus, ST239-MRSA-III. PLoS One 5: e8582.
46. Melter O, Santos Sanches I, Schindler J, Aires de Sousa M, Mato R, et al. (1999) Methicillin-resistant Staphylococcus aureus clonal types in the Czech Republic. J Clin Microbiol 37: 2798-803.
47. Melter O, Aires de Sousa M, Urbaskova P, Jakubu V, Zemlickova H, et al. (2003) Update on the major clonal types of methicillin-resistant Staphylococcus aureus in the Czech Republic. J Clin Microbiol 41: 4998-5005.
48. Humphreys H, Carroll JD, Keane CT, Cafferkey MT, Pomeroy HM, et al. (1990) Importation of methicillin-resistant Staphylococcus aureus from Baghdad to Dublin and subsequent nosocomial spread. J Hosp Infect 15: 127-35.
49. Adler A, Givon-Lavi N, Moses AE, Block C, Dagan R, (2010) Carriage of community-associated methicillin-resistant Staphylococcus aureus in a cohort of infants in southern Israel: risk factors and molecular features. J Clin Microbiol 48: 531-8.
50. Bekkhoucha SN, Cady A, Gautier P, Itim F, Donnio PY, (2009) A portrait of Staphylococcus aureus from the other side of the Mediterranean Sea: molecular characteristics of isolates from Western Algeria. Eur J Clin Microbiol Infect Dis 28: 553-5.
51. Ben Nejma M, Mastouri M, Bel Hadj Jrad B, Nour M, (2008) Characterization of ST80 Panton-Valentine leukocidin-positive community-acquired methicillin-resistant Staphylococcus aureus clone in Tunisia. Diagn Microbiol Infect Dis.
52. Enany S, Yaoita E, Yoshida Y, Enany M, Yamamoto T, (2010) Molecular characterization of Panton-Valentine leukocidin-positive community-acquired methicillin-resistant Staphylococcus aureus isolates in Egypt. Microbiol Res 165: 152-162.
53. Tokajian ST, Khalil PA, Jabbour D, Rizk M, Farah MJ, et al. (2010) Molecular characterization of Staphylococcus aureus in Lebanon. Epidemiol Infect 138: 707-12.
54. Udo EE, O'Brien FG, Al-Sweih N, Noronha B, Matthew B, et al. (2008) Genetic lineages of community-associated methicillin-resistant Staphylococcus aureus in Kuwait hospitals. J Clin Microbiol 46: 3514-6.
55. Vourli S, Perimeni D, Makri A, Polemis M, Voyiatzi A, et al. (2005) Community acquired MRSA infections in a paediatric population in Greece. Euro Surveill 10: 78-9.
56. Moran GJ, Krishnadasan A, Gorwitz RJ, Fosheim GE, McDougal LK, et al. (2006) Methicillin-resistant S. aureus infections among patients in the emergency department. N Engl J Med 355: 666-74.
57. Tenover FC, McDougal LK, Goering RV, Killgore G, Projan SJ, et al. (2006) Characterization of a Strain of Community-Associated Methicillin-Resistant Staphylococcus aureus Widely Disseminated in the United States. J Clin Microbiol 44: 108-118.
58. Otter JA, Havill NL, Boyce JM, French GL, (2009) Comparison of community-associated methicillin-resistant Staphylococcus aureus from teaching hospitals in London and the USA, 2004-2006: where is USA300 in the UK? Eur J Clin Microbiol Infect Dis 28: 835-9.
59. Linde H, Wagenlehner F, Strommenger B, Drubel I, Tanzer J, 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: 419-22.
60. Tristan A, Bes M, Meugnier H, Lina G, Bozdogan B, et al. (2007) Global distribution of Panton-Valentine leukocidin--positive methicillin-resistant Staphylococcus aureus, 2006. Emerg Infect Dis 13: 594-600.
61. Maier J, Melzl H, Reischl U, Drubel I, Witte W, et al. (2005) Panton-Valentine leukocidin-positive methicillin-resistant Staphylococcus aureus in Germany associated with travel or foreign family origin. Eur J Clin Microbiol Infect Dis 24: 637-639.
62. Lee SM, Ender M, Adhikari R, Smith JMB, Berger-Bachi B, et al. (2007) Fitness cost of staphylococcal cassette chromosome mec in methicillin-resistant Staphylococcus aureus by way of continuous culture. Antimicrob Agents Chemother 51: 1497-1499.
63. Ender M, McCallum N, Adhikari R, Berger-Bachi B, (2004) Fitness Cost of SCCmec and Methicillin Resistance Levels in Staphylococcus aureus. Antimicrob Agents Chemother 48: 2295-2297.
64. Coombs GW, Pearson JC, O'Brien FG, Murray RJ, Grubb WB, et al. (2006) Methicillin-resistant Staphylococcus aureus clones, Western Australia. Emerg Infect Dis 12: 241-7.
65. Kupfer M, (2009) Epidemiologische Untersuchung zum Auftreten von Methicillin Resistenten Staphylococcus aureus (MRSA) im Universitätsklinikum Dresden in den Jahren 2001-2007. Faculty of Medicine Technical University of Dresden: Dresden.
66. Kupfer M, Jatzwauk L, Monecke S, Mobius J, Weusten A, (2010) MRSA in a large German University Hospital: Male gender is a significant risk factor for MRSA acquisition. GMS Krankenhhyg Interdiszip 5.
67. Huggan PJ, Wells JE, Browne M, Richardson A, Murdoch DR, et al. (2010) Population-based epidemiology of Staphylococcus aureus bloodstream infection in Canterbury, New Zealand. Internal Medicine Journal 40: 117-125.
68. Diep BA, Gill SR, Chang RF, Phan TH, Chen JH, et al. (2006) Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet 367: 731-9.
69. Barbier F, Lebeaux D, Hernandez D, Delannoy AS, Caro V, et al. (2011) High prevalence of the arginine catabolic mobile element in carriage isolates of methicillin-resistant Staphylococcus epidermidis. J Antimicrob Chemother 66: 29-36.
70. Miragaia M, de Lencastre H, Perdreau-Remington F, Chambers HF, Higashi J, et al. (2009) Genetic diversity of arginine catabolic mobile element in Staphylococcus epidermidis. PLoS One 4: e7722.
71. Monecke S, Slickers P, Ehricht R, (2008) Assignment of Staphylococcus aureus isolates to clonal complexes based on microarray analysis and pattern recognition. FEMS Immunol Med Microbiol 53: 237-251.
72. Enright MC, Day NPJ, Davies CE, Peacock SJ, Spratt BG, (2000) Multilocus Sequence Typing for Characterization of Methicillin-Resistant and Methicillin-Susceptible Clones of Staphylococcus aureus. J Clin Microbiol 38: 1008-1015.