Reduced Vancomycin Susceptibility Found in Methicillin-Resistant and Methicillin-Sensitive Staphylococcus aureus Clinical Isolates in Northeast China

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Hu, Jian ^a,c   Ma, Xiao Xue ^a   Tian, Yuan ^a   Pang, Long ^a   Cui, Long Zhu ^b   Shang, Hong ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

^b KITASATO UNIVERSITY   (Japan)

^c Department of Clinical Laboratory   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CEFTOBIPROLE; CHLORAMPHENICOL; CIPROFLOXACIN; CLINDAMYCIN; COTRIMOXAZOLE; DAPTOMYCIN; ERYTHROMYCIN; GENTAMICIN; LEVOFLOXACIN; LINEZOLID; OXACILLIN; RIFAMPICIN; TEICOPLANIN; TETRACYCLINE; TIGECYCLINE; VANCOMYCIN;

ACCESSORY GENE REGULATOR GROUP II; ANTIBIOTIC SENSITIVITY; AREA UNDER THE CURVE; ARTICLE; AUTOLYSIS; BACTERIAL GENE; BACTERIAL GENETICS; BACTERIUM ADHERENCE; BACTERIUM CULTURE; BACTERIUM IDENTIFICATION; BACTERIUM ISOLATE; BIOFILM; BLOOD CULTURE; BODILY SECRETIONS; BROTH DILUTION; CHINA; CONTROLLED STUDY; DISK DIFFUSION; GENOTYPE; HUMAN; MAJOR CLINICAL STUDY; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; METHICILLIN SUSCEPTIBLE STAPHYLOCOCCUS AUREUS; MINIMUM INHIBITORY CONCENTRATION; MOLECULAR TYPING; NONHUMAN; PHENOTYPE; PREVALENCE; PUS; PVL GENE; RETROSPECTIVE STUDY; SCREENING; SPA GENE; SPUTUM CULTURE; STAPHYLOCOCCAL CASSETTE CHROMOSOME MEC TYPE II;

ANTI-BACTERIAL AGENTS; CHINA; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIAL SENSITIVITY TESTS; STAPHYLOCOCCUS AUREUS; VANCOMYCIN;

EID: 84884191446     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0073300     Document Type: Article

References (52)

1. Lowy FD, (2011) How Staphylococcus aureus adapts to its host. N Engl J Med 364: 1987-1990.
2. Richter SS, Satola SW, Crispel EK, Heilmann KP, Dohrn CL, et al. (2011) Detection of Staphylococcus aureus isolates with heterogeneous intermediate-level resistance to vancomycin in the United States. J Clin Microbiol 49: 4203-4207.
3. Kirby A, Graham R, Williams NJ, Wootton M, Broughton CM, et al. (2010) Staphylococcus aureus with reduced glycopeptide susceptibility in Liverpool, UK. J Antimicrob Chemother 65: 721-724.
4. Sun W, Chen H, Liu Y, Zhao C, Nichols WW, et al. (2009) Prevalence and characterization of heterogeneous vancomycin-intermediate Staphylococcus aureus isolates from 14 cities in China. Antimicrob Agents Chemother 53: 3642-3649.
5. Campanile F, Borbone S, Perez M, Bongiorno D, Cafiso V, et al. (2010) Heteroresistance to glycopeptides in Italian meticillin-resistant Staphylococcus aureus (MRSA) isolates. Int J Antimicrob Agents 36: 415-419.
6. Adam HJ, Louie L, Watt C, Gravel D, Bryce E, et al. (2010) Detection and characterization of heterogeneous vancomycin-intermediate Staphylococcus aureus isolates in Canada: results from the Canadian Nosocomial Infection Surveillance Program, 1995-2006. Antimicrob Agents Chemother 54: 945-949.
7. Hiramatsu K, Hanaki H, Ino T, Yabuta K, Oguri T, et al. (1997) Methicillin-resistant Staphylococcus aureus clinical strain with reduced vancomycin susceptibility. J Antimicrob Chemother 40: 135-136.
8. Hiramatsu K, Aritaka N, Hanaki H, Kawasaki S, Hosoda Y, et al. (1997) Dissemination in Japanese hospitals of strains of Staphylococcus aureus heterogeneously resistant to vancomycin. Lancet 350: 1670-1673.
9. Tenover FC, Moellering RC Jr, (2007) The rationale for revising the Clinical and Laboratory Standards Institute vancomycin minimal inhibitory concentration interpretive criteria for Staphylococcus aureus. Clin Infect Dis 44: 1208-1215.
10. Howden BP, Davies JK, Johnson PD, Stinear TP, Grayson ML, (2010) Reduced vancomycin susceptibility in Staphylococcus aureus, including vancomycin-intermediate and heterogeneous vancomycin-intermediate strains: resistance mechanisms, laboratory detection, and clinical implications. Clin Microbiol Rev 23: 99-139.
11. Clinical and Laboratory Standards Institute (CLSI) (2012) Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard-ninth edition. CLSI document M07-A9. WaynePA: CLSI.
12. Wootton M, MacGowan AP, Walsh TR, Howe RA, (2007) A multicenter study evaluating the current strategies for isolating Staphylococcus aureus strains with reduced susceptibility to glycopeptides. J Clin Microbiol 45: 329-332.
13. van Hal SJ, Wehrhahn MC, Barbagiannakos T, Mercer J, Chen D, et al. (2011) Performance of various testing methodologies for detection of heteroresistant vancomycin-intermediate Staphylococcus aureus in bloodstream isolates. J Clin Microbiol 49: 1489-1494.
14. Wootton M, Howe RA, Hillman R, Walsh TR, Bennett PM, et al. (2001) A modified population analysis profile (PAP) method to detect hetero-resistance to vancomycin in Staphylococcus aureus in a UK hospital. J Antimicrob Chemother 47: 399-403.
15. Burnham CA, Weber CJ, Dunne WM Jr, (2010) Novel screening agar for detection of vancomycin-nonsusceptible Staphylococcus aureus. J Clin Microbiol 48: 949-951.
16. Kosowska-Shick K, Ednie LM, McGhee P, Smith K, Todd CD, et al. (2008) Incidence and characteristics of vancomycin nonsusceptible strains of methicillin-resistant Staphylococcus aureus at Hershey Medical Center. Antimicrob Agents Chemother 52: 4510-4513.
17. Riederer K, Shemes S, Chase P, Musta A, Mar A, et al. (2011) Detection of intermediately vancomycin-susceptible and heterogeneous Staphylococcus aureus isolates: comparison of Etest and agar screening methods. J Clin Microbiol 49: 2147-2150.
18. Rybak MJ, Leonard SN, Rossi KL, Cheung CM, Sadar HS, et al. (2008) Characterization of vancomycin-heteroresistant Staphylococcus aureus from the metropolitan area of Detroit, Michigan, over a 22-year period (1986 to 2007). J Clin Microbiol 46: 2950-2954.
19. Kawaguchiya M, Urushibara N, Kuwahara O, Ito M, Mise K, et al. (2011) Molecular characteristics of community-acquired methicillin-resistant Staphylococcus aureus in Hokkaido, northern main island of Japan: identification of sequence types 6 and 59 Panton-Valentine leucocidin-positive community-acquired methicillin-resistant Staphylococcus aureus. Microb Drug Resist 17: 241-250.
20. Song JH, Hiramatsu K, Suh JY, Ko KS, Ito T, et al. (2004) Emergence in Asian countries of Staphylococcus aureus with reduced susceptibility to vancomycin. Antimicrob Agents Chemother 48: 4926-4928.
21. Howden BP, Johnson PD, Ward PB, Stinear TP, Davies JK, (2006) Isolates with low-level vancomycin resistance associated with persistent methicillin-resistant Staphylococcus aureus bacteremia. Antimicrob Agents Chemother 50: 3039-3047.
22. Garnier F, Chainier D, Walsh T, Karlsson A, Bolmstrǒm A, et al. (2006) A 1 year surveillance study of glycopeptide-intermediate Staphylococcus aureus strains in a French hospital. J Antimicrob Chemother 57: 146-149.
23. Li H, Zhao C, Chen H, Zhang F, He W, et al. (2013) Identification of Gene Clusters Associated with Host Adaptation and Antibiotic Resistance in Chinese Staphylococcus aureus Isolates by Microarray-Based Comparative Genomics. PLoS One 8: e53341.
24. Liu C, Chambers HF, (2003) Staphylococcus aureus with heterogeneous resistance to vancomycin: epidemiology, clinical significance, and critical assessment of diagnostic methods. Antimicrob Agents Chemother 47: 3040-3045.
25. Pillai SK, Wennersten C, Venkataraman L, Eliopoulos GM, Moellering RC Jr, et al. (2009) Development of Reduced Vancomycin Susceptibility in Methicillin-Susceptible Staphylococcus aureus. Clin Infect Dis 49: 1169-1174.
26. Ma XX, Sun DD, Hu J, Wang EH, Luo EJ, (2011) Epidemiological and molecular characterization of Staphylococcus haemolyticus strains, from a hematology ward, with decreased susceptibility to glycopeptides. Can J Microbiol 57: 476-484.
27. Ma XX, Wang EH, Liu Y, Luo EJ, (2011) Antibiotic susceptibility of coagulase-negative staphylococci (CoNS): emergence of teicoplaninnon-susceptible CoNS strains with inducible resistance to vancomycin. J Med Microbiol 60: 1661-1668.
28. Clinical and Laboratory Standards Institute (CLSI) (2012) Performance standards for antimicrobial susceptibility testing; twenty-second informational supplement. CLSI document M100-S22. WaynePA: CLSI.
29. Unal S, Hoskins J, Flokowitsch JE, Wu CY, Preston DA, et al. (1992) Detection of methicillin-resistant staphylococci by using the polymerase chain reaction. J Clin Microbiol 30: 1685-1691.
30. Aires-de-Sousa M, Boye K, de Lencastre H, Deplano A, Enright MC, et al. (2006) High Interlaboratory Reproducibility of DNA Sequence-Based Typing of Bacteria in a Multicenter Study. J Clin Microbiol 44: 619-621.
31. Enright MC, Day NP, 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.
32. Feil EJ, Li BC, Aanensen DM, Hanage WP, Spratt BG, (2004) Eburst: Inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J Bacteriol 186: 1518-1530.
33. Lina G, Boutite F, Tristan A, Bes M, Etienne J, et al. (2003) Bacterial competition for human nasal cavity colonization: role of Staphylococcal agr alleles. Appl Environ Microbiol 69: 18-23.
34. Kondo Y, Ito T, Ma XX, Watanabe S, Kreiswirth BN, 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.
35. Ma XX, Ito T, Kondo Y, Cho M, Yoshizawa Y, et al. (2008) Two Different Panton-Valentine Leukocidin Phage Lineages Predominate in Japan. J Clin Microbiol 46: 3246-3258.
36. Ma XX, Sun DD, Wang S, Wang ML, Li M, et al. (2011) Nasal carriage of methicillin-resistant Staphylococcus aureus among preclinical medical students: epidemiologic and molecular characteristics of methicillin-resistant S. aureus clones. Diagn Microbiol Infect Dis 70: 22-30.
37. Sakoulas G, Eliopoulos GM, Moellering RC Jr, Wennersten C, Venkataraman L, et al. (2002) Accessory gene regulator (agr) locus in geographically diverse Staphylococcus aureus isolates with reduced susceptibility to vancomycin. Antimicrob Agents Chemother 46: 1492-1502.
38. van Hal SJ, Paterson DL, (2011) Systematic review and meta-analysis of the significance of heterogeneous vancomycin-intermediate Staphylococcus aureus isolates. Antimicrob Agents Chemother 55: 405-410.
39. Maor Y, Hagin M, Belausov N, Keller N, Ben-David D, et al. (2009) Clinical features of heteroresistant vancomycin-intermediate Staphylococcus aureus bacteremia versus those of methicillin-resistant S. aureus bacteremia. J Infect Dis 199: 619-624.
40. Leonard SN, Rossi KL, Newton KL, Rybak MJ, (2009) Evaluation of the Etest GRD for the detection of Staphylococcus aureus with reduced susceptibility to glycopeptides. J Antimicrob Chemother 63: 489-492.
41. Musta AC, Riederer K, Shemes S, Chase P, Jose J, et al. (2009) Vancomycin MIC plus heteroresistance and outcome of methicillin-resistant Staphylococcus aureus bacteremia: trends over 11 years. J Clin Microbiol 47: 1640-1644.
42. Han JH, Edelstein PH, Lautenbach E, (2012) Reduced vancomycin susceptibility and staphylococcal cassette chromosome mec (SCCmec) type distribution in methicillin-resistant staphylococcus aureus bacteraemia. J Antimicrob Chemother 67: 2346-2349.
43. Davis SL, Rybak MJ, Amjad M, Kaatz GW, McKinnon PS, (2006) Characteristics of patients with healthcare-associated infection due to SCCmec type methicillin-resistant Staphylococcus aureus. Infect Control Hosp Epidemiol 27: 1025-1031.
44. Sakoulas G, Moellering RC Jr, Eliopoulos GM, (2006) Adaptation of methicillin-resistant Staphylococcus aureus in the face of vancomycin therapy. Clin Infect Dis 42: S40-50.
45. Howe RA, Monk A, Wootton M, Walsh TR, Enright MC, (2004) Vancomycin susceptibility within methicillin-resistant Staphylococcus aureus lineages. Emerg Infect Dis 10: 855-857.
46. Rijnders MI, Deurenberg RH, Boumans ML, Hoogkamp-Korstanje JA, Beisser PS, et al. (2009) Population structure of Staphylococcus aureus strains isolated from intensive care unit patients in the Netherlands over an 11-year period (1996 to 2006). J Clin Microbiol 47: 4090-4095.
47. Popovich KJ, Weinstein RA, (2009) The graying of methicillin-resistant Staphylococcus aureus. Infect Control Hosp Epidemiol 30: 9-12.
48. Graber CJ, Wong MK, Carleton HA, Perdreau-Remington F, Haller BL, et al. (2007) Intermediate vancomycin susceptibility in a community-associated MRSA clone. Emerg Infect Dis 13: 491-493.
49. Hageman JC, Patel J, Franklin P, Miscavish K, McDougal L, et al. (2008) Occurrence of a USA300 vancomycin-intermediate Staphylococcus aureus. Diagn Microbiol Infect Dis 62: 440-442.
50. Harigaya Y, Ngo D, Lesse AJ, Huang V, Tsuji BT, (2011) Characterization of heterogeneous vancomycin-intermediate resistance, MIC and accessory gene regulator (agr) dysfunction among clinical bloodstream isolates of staphyloccocus aureus. BMC Infect Dis 11: 287.
51. Fowler VG, Sakoulas G, McIntyre LM, Meka VG, Arbeit RD, et al. (2004) Persistent bacteremia due to methicillin-resistant Staphylococcus aureus infection is associated with agr dysfunction and low-level in vitro resistance to thrombin-induced platelet microbicidal protein. J Infect Dis 190: 1140-1149.
52. Ludwig F, Edwards B, Lawes T, Gould IM, (2012) Effects of storage on vancomycin and daptomycin MIC in susceptible blood isolates of methicillin-resistant Staphylococcus aureus. J Clin Microbiol 50: 3383-3387.