Journal List > Korean J Clin Microbiol > v.11(2) > 1038155

Uh, Hwang, Jang, Kwon, Yoon, and Kim: Distributions of Macrolide-Lincosamide-Streptogramin B Resistance Phenotypes in Clinical Isolates of Staphylococi

Abstract

Background

Increased resistance rates to macrolide-lincosamide-streptogramin B (MLSB) antibiotics among clinical isolates of staphylococci are considered as a consequence of an expanded use of these antibiotics in the treatment of Gram-positive infections. The proportion of MLSB resistance phenotypes of staphylococci is quite different by geographical variations and study periods. The aim of the present study was to determine the distribution of MLSB resistance phenotypes among clinical isolates of staphylococci in a university hospital.

Methods

The MLSB resistance phenotypes of clinical isolates of staphylococci were investigated by the double-disk diffusion test using erythromycin and clindamycin disks.

Results

Of 7,916 isolates, 55.7% exhibited a constitutive resistance phenotype (cMLSB) whereas 8.1% expressed an inducible resistance phenotype (iMLSB). Among 3,419 coagulase-negative staphylococci (CNS), 32.6% and 10.0% exhibited cMLSB and iMLSB resist-ance phenotypes, respectively. Of 4,497 Staphylococcus aureus isolates, 73.1% and 6.8% were cMLSB and iMLSB resistance phenotypes, respectively. cMLSB was detected among 90.2% of methicillin-resistant S. aureus (MRSA), 46.5% of methicillin-resistant CNS (MRCNS), 3.2% of methicillin-susceptible CNS (MSCNS), and 2.2% of methicillin-susceptible S. aureus (MSSA). iMLSB was detected among 16.5% of MSSA, 11.5% of MRCNS, 6.7% of MSCNS, and 4.4% of MRSA.

Conclusion

MLSB resistance was more prevalent among S. aureus isolates than CNS strains. Although cMLSB was the most frequently detected resistance phenotype among the total staphylococcal isolates, methicillin-susceptible strains exhibited somewhat higher iMLSB resistance rates compared with methi-cillin-resistant strains.

References

1. Maltezou HC and Giamarelloub H. Community-acquired methicillin-resistant Staphylococcus aureus infections. Int J Antimicrob Agents. 2006; 27:87–96.
2. Lewis JS and Jorgensen JH. Inducible clindamycin resistance in staphylococci: should clinicians and microbiologists be concerned? Clin Infect Dis. 2005; 40:280–5.
3. National Committee for Clinical Laboratory Standards. Performance standards for antimicrobial susceptibility testing. fourteenth informational supplement. NCCLS document M100-S14. Wayne, PA; NCCLS. 2004.
4. Bacterial sensitivity test KB Disk Eiken operation manual. Eiken, Tokyo, Japan. 2003.
5. CDC. CDC web sites on infection control home. Community-associated MRSA information for clinicians.www.cdc.gov/nci-dod/dhqp/ar_mrsa_ca_clinicians.html. [Online] (updated on Febrary 2005).
6. Lim JA, Kwon AR, Kim SK, Chong Y, Lee K, Choi EC. Prevalence of resistance to macrolide, lincosamide and streptogramin antibiotics in Gram-positive cocci isolated in a Korean hospital. J Antimicrob Chemother. 2002; 49:489–95.
crossref
7. Nicola FG, McDougal LK, Biddle JW, Tenover FC. Characterization of erythromycin-resistant isolates of Staphylococcus aureus recovered in the United States from 1958 through 1969. Antimicrob Agents Chemother 1998 42:. 3024–7.
8. Schmitz FJ, Verhoef J, Fluit AC. Prevalence of resistance to MLS antibiotics in 20 European university hospitals participating in the European SENTRY surveillance programme. Sentry Participants Group. J Antimicrob Chemother. 1999; 43:783–92.
9. Chong Y, Lee K, et al. eds. New antimicrobial resistance and mechanisms of bacteria. 1st ed. Seoul; Seoheung Publishing Com-pany.,2002:. 181–97.
10. LaPlante KL, Leonard SN, Andes DR, Craig WA, Rybak MJ. Activities of clindamycin, daptomycin, doxycycline, linezolid, trimethoprim-sulfamethoxazole, and vancomycin against community-associated methicillin-resistant Staphylococcus aureus with inducible clindamycin resistance in murine thigh infection and in vitro pharmacodynamic models. Antimicrob Agents Chemother. 2008; 52:2156–62.
11. Westh H, Hougaard DM, Vuust J, Rosdahl VT. Prevalence of erm gene classes in erythromycin-resistant Staphylococcus aureus strains isolated between 1959 and 1988. Antimicrob Agents Chemother. 1995; 39:369–73.
crossref
12. Thakker-Varia S, Jenssen WD, Moon-McDermott L, Weinstein MP, Dubin DT. Molecular epidemiology of macrolides-lincosamides-streptogramin B resistance in Staphylococcus aureus and coagu-lase-negative staphylococci. Antimicrob Agents Chemother. 1987; 31:735–43.
crossref
13. Eady EA, Ross JI, Tipper JL, Walters CE, Cove JH, Noble WC. Distribution of genes encoding erythromycin ribosomal methylases and an erythromycin efflux pump in epidemiologically distinct groups of staphylococci. J Antimicrob Chemother. 1993; 31:211–7.
crossref
14. Cetin ES, Gunes H, Kaya S, Aridogan BC, Demirci M. Macrolide-lincosamide-streptogramin B resistance phenotypes in clinical staphylococcal isolates. Int J Antimicrob Agents. 2008; 31:364–8.
crossref
15. Kim JS, Kim HS, Song W, Cho HC, Lee KM, Kim EC. Antimicrobial resistance profiles of Staphylococcus aureus isolated in 13 Korean hospitals. Korean J Lab Med. 2004; 24:223–9.
16. Uh Y, Kim HY, et al. eds. Antimicrobial agents and antimicrobial susceptibility test. eds. 1st ed.Paju: Korean Studies Information Co., Ltd.;2006. p. 556–7.

Table 1.
Distribution of macrolide-lincosamide-streptogramin B (MLSB) resistance phenotypes of Staphylococcus species
Organisms MLSB No. (%) cMLSB No. (%) iMLSB No. (%) ERYSCLIR No. (%)
S. aureus        
MRSA (3626) 3431 (94.6) 3271 (90.2) 160 (4.4)0 4 (0.1)
MSSA (871) 163 (18.7) 19 (2.2)0 114 (16.5) 1 (0.1)
Subtotal (4497) 3594 (79.9) 3290 (73.1) 304 (6.8)0 5 (0.1)
CNS        
MRCNS (2322) 1347 (58.0) 1080 (46.5) 267(11.5) 44 (1.9)
MSCNS (1097) 109 (9.9)0 35 (3.2)0 74 (6.7)0 9 (0.8)
Subtotal (3419) 1456 (42.6) 1115 (32.6) 341 (10.0) 53 (1.6)
Total (7916) 5050 (63.8) 4405 (55.7) 645 (8.1)0 58 (0.7)

Abbreviations: cMLSB, constitutive MLSB resistance phenotype; iMLSB, inducible MLSB resistance phenotype; ERY

S CLI

R erythromycin-susceptible and clindamycin-resistant; MRSA, methicillin-resistant S. aureus; MSSA, methicillin-susceptible S. aureus; CNS, coagulase-negative staphylococci; MRCNS, methicillin-resistant CNS; MSCNS, methicillin-susceptible CNS.

Table 2.
Distributions of MLSB resistance phenotypes of Staphylococcus species according to patients' classification
Classification (No.) ERYSCLIS No. (%) cMLSB No. (%) iMLSB No. (%) ERYSCLIR No. (%)
Community-acquired        
MRSA (499) 95 (19.1) 324 (64.9) 79 (15.8) 1 (0.2)
MSSA (546) 459 (84.0) 8 (1.5) 78 (14.3) 1 (0.2)
Subtotal (1045) 554 (53.0) 332 (31.8) 157 (15.0) 2 (0.2)
MRCNS (1212) 651 (53.7) 349 (28.8) 192 (15.8) 20 (1.7)
MSCNS (810) 722 (89.1) 20 (2.5) 61 (7.5) 7 (0.9)
Subtotal (2022) 1373 (67.9) 369 (18.3) 253 (12.5) 27 (1.3)
Hospital-acquired
MRSA (3127) 96 (3.1) 2947 (94.2) 81 (2.6) 3 (0.1)
MSSA (325) 248 (76.3) 11 (3.4) 66 (20.3) 0 (0)
Subtotal (3452) 344 (9.9) 2958 (85.7) 147 (4.3) 3 (0.1)
MRCNS (1110) 280 (25.2) 731 (65.8) 75 (6.8) 24 (2.2)
MSCNS (287) 257 (89.6) 15 (5.2) 13 (4.5) 2 (0.7)
Subtotal (1397) 537 (38.4) 746 (53.4) 88 (6.3) 26 (1.9)

Abbreviations: ERY

S CLI

S erythromycin-susceptible and clindamycin-susceptible; Others, see Table 1.

Table 3.
Antibiotic susceptibilities of Staphylococcus aureus according to MLSB resistance phenotypes and patients' classification
Classification (No.) Tetracycline No. (%) TMP/SMX No. (%) Ciprofloxacin No. (%) Arbekacin No. (%)
Community-acquired
MRSA        
cMLSB 14 (4.3) 284 (87.7) 5 (1.5) 306 (94.4)
iMLSB ERYSCLIR 49 (62.0) 1 (100) 73 (92.4) 1 (100) 49 (62.0) 1 (100) 76 (96.2) 1 (100)
ERYSCLIS 83 (87.4) 91 (95.8) 84 (88.8) 91 (95.8)
Subtotal 147 (29.5) 449 (90.0) 139 (27.9) 474 (95.0)
MSSA
cMLSB 4 (50.0) 7 (87.5) 7 (87.5) 8 (100)
iMLSB 73 (93.6) 78 (100) 74 (94.9) 74 (94.9)
ERYSCLIR 0 (0) 1 (100) 0 (0) 1 (100)
ERYSCLIS 422 (91.9) 459 (100) 451 (98.3) 439 (95.6)
Subtotal 499 (91.4) 545 (99.8) 532 (97.4) 522 (95.6)
Hospital-acquired
MRSA        
cMLSB 270 (9.2) 2808 (95.3) 13 (0.4) 2748 (93.2)
iMLSB 47 (58.0) 71 (87.7) 46 (56.8) 78 (96.3)
ERYSCLIR 1 (33.3) 0 (0) 0 (0) 3 (100)
ERYSCLIS 90 (93.8) 93 (96.9) 84 (87.5) 93 (96.9)
Subtotal 408 (13.0) 2972 (95.0) 143 (4.6) 2922 (93.4)
MSSA
cMLSB 7 (63.6) 10 (90.9) 6 (54.5) 11 (100)
iMLSB 64 (97.0) 66 (100) 65 (98.5) 63 (95.5)
ERYSCLIS 233 (94.0) 247 (99.6) 239 (96.4) 239 (96.4)
Subtotal 304 (93.5) 323 (99.4) 310 (95.4) 313 (96.5)

Abbreviations: TMP/SMX, trimethoprim/sulfamethoxazole; Others, see Table 1 and Table 2.

Table 4.
Prevalence of MLSB resistance phenotypes of methicillin-resistant Staphylococcus aureus according to isolation years and patients' classification
Classification No. (%) by year
2005 2006 2007 2008
Community-acquired
cMLSB 31 (38.7) 254 (37.6) 284 (41.5) 104 (38.4)
iMLSB 16 (20.0) 118 (17.5) 102 (14.9) 35 (12.9)
ERYSCLIR 1 (1.3)0 12 (1.8)0 5 (0.7)0 3 (1.1)0
ERYSCLIS 32 (40.0) 291 (43.1) 294 (42.9)0 129 (47.6)
Subtotal 80 (100) 675 (100) 685 (100) 271 (100)
Hospital-acquired
cMLSB 236 (89.3) 1198 (85.4) 1609 (87.2) 635 (87.5)
iMLSB 11 (4.2)0 66 (4.7)0 59 (3.2)0 20 (2.8)0
ERYSCLIR 1 (0.4)0 4 (0.3)0 14 (0.8)0 8 (1.1)0
ERYSCLIS 16 (6.1)0 135 (9.6)0 162 (8.8)0 63 (8.7)0
Subtotal 264 (100)0 1403 (100) 1844 (100) 726 (100)

Abbreviations: see Table 1 and Table 2.

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