Antimicrobial Agents and Chemotherapy, July 2004, p . 2716-2718, Vol . 48, No . 7

Antimicrobial Susceptibility Patterns and Macrolide Resistance Genes of ß-Hemolytic Streptococci in Korea

Young Uh,^1* In Ho Jang,¹ Gyu Yel Hwang,¹ Mi Kyung Lee,¹ Kap Jun Yoon,¹ and Hyo Youl Kim²

Departments of Laboratory Medicine,¹ Infectious Disease, Yonsei University Wonju College of Medicine, Wonju, South Korea²

Received 28 December 2003/ Returned for modification 29 January 2004/ Accepted 29 February 2004

A total of 540 strains of BHS were collected from clinical specimens between January 1990 and December 2000 at Wonju Christian Hospital, a 1,000-bed teaching hospital in South Korea . Multiple isolates from the same patient were avoided . The isolates were identified by standard methods . Beta-hemolytic strains with group F antigens were excluded . Susceptibility to penicillin G, erythromycin, clindamycin, tetracycline, ceftriaxone (Sigma Chemical Co., St . Louis, Mo.), vancomycin (Daewoong Lilly, Seoul, Korea), and chloramphenicol (Chongkundang, Seoul, Korea) was tested by the agar dilution method (14) . The resistance phenotypes of erythromycin-resistant (intermediate and resistant) isolates were determined by the double-disk test with erythromycin (15 µg) and clindamycin (2 µg) disks (17) . The presence of erm and mef class genes was determined by PCR amplification with previously described primers (11, 18) specific for erm(A) subclasses erm(TR), erm(B), erm(C), and mef(A) .

The overall resistance rates of BHS were found to be 80.0% for tetracycline, 22.8% for chloramphenicol, 20.2% for erythromycin, and 19.1% for clindamycin, whereas all isolates were susceptible to penicillin G, ceftriaxone, and vancomycin (Table 1) . The rates of resistance to erythromycin found in this study were as follows, in order of decreasing rank: S . agalactiae, 25.3%; S . pyogenes, 16.1%; group C streptococci, 9.1%; group G streptococci, 9.0% . S . agalactiae had the highest rate of clindamycin resistance (28.2%), followed by S . pyogenes (9.8%), group C streptococci (4.5%), and group G streptococci (1.5%) . Of 109 erythromycin-resistant BHS isolates, 63.3% had the cMLS_B phenotype (constitutive resistance to macrolide-lincosamide-streptogramin B [MLS_B]), 23.9% had the M phenotype, and 12.8% had the iMLS_B (inducible resistance to MLS_B) phenotype . With the exception of two isolates, all MLS_B-resistant strains carried the erm(B) gene (cMLS_B phenotype), the erm(A) subclass erm(TR) gene (iMLS_B phenotype), or the mef(A) gene (M phenotype) .

 
The erythromycin resistance rate of 20.2% (intermediate, 1.7%; resistant, 18.5%) in this study is similar to that reported in North America (18.6%) but higher than those in the Asia-Pacific region (10.9%), Europe (9.7%), and Latin America (2.7%) (7) . The resistance of BHS to clindamycin was significantly higher in this study (19.1%) than in North America (6.8%), the Asia-Pacific region (4.7%), Europe (4.7%), and Latin America (0.9%) (7) . Macrolide resistance among S . pyogenes isolates is an emerging concern . Erythromycin resistance among S . pyogenes isolates has remained variable but generally low in most countries . However, there have been reports from Japan in the 1970s (13) and more recently from Europe (2, 15) and Taiwan (8) of high percentages of isolates that are macrolide resistant . Erythromycin-resistant S . pyogenes was isolated for the first time in this study in 1994; after that time, the resistance rate ranged from 14.3 to 23.8% during the period of 1994 to 2000 . Although there are far fewer reports of antimicrobial resistance in S . agalactiae compared with S . pyogenes, the increasing isolation of erythromycin-resistant S . agalactiae has also become alarming (3) . Studies have documented that the erythromycin resistance rates for invasive S . agalactiae isolates during 1997 to 1999 were 14.3 and 25.4% in Canada and the United States, respectively (1) . Investigators in Taiwan reported that 46% of S . agalactiae isolates were resistant to erythromycin (9) . In this study, erythromycin-resistant S . agalactiae emerged in 1996; after that time, the resistance rate ranged from 18.7 to 40.0% during the period of 1996 to 2000 (Table 2) . Most studies reported rates of resistance to erythromycin higher than those of clindamycin (1, 3, 4, 6, 7, 19) . In contrast, the rate of resistance to clindamycin in our S . agalactiae isolates was higher than the rate of resistance to erythromycin . Among the BHS, S . agalactiae exhibited the highest rates of resistance to erythromycin, clindamycin, and tetracycline . Although the susceptibility data for group C and G BHS were sparse, our studies showed that all isolates were susceptible to penicillin G, ceftriaxone, and vancomycin and 90% of the isolates were susceptible to erythromycin and clindamycin . The rates of resistance to tetracycline and chloramphenicol were high for both group C and G streptococci .

 
It was noted that the prevalent phenotype of MLS_B resistance of BHS is serogroup dependent . A study conducted in North America found that rates of the M phenotype of group A and B streptococci were 91.4 and 59.1%, respectively (4) . In Europe, the distribution of frequencies of MLS_B resistance phenotypes and genotypes of S . pyogenes are quite different according to geographical location; e.g., in Spain, 89.5% of S . pyogenes isolates had the M phenotype (15); in Italy, 47.4% of S . pyogenes isolates had the cMLS_B phenotype (20); and in central and Eastern European countries, 60.5% of S . pyogenes isolates had the cMLS_B phenotype (12) . In Taiwan, 80.2% of erythromycin-resistant S . pyogenes isolates exhibited the M phenotype (8) . The predominant MLS_B resistance phenotype of S . agalactiae was cMLS_B in Spain (3) and Taiwan (9), whereas the M phenotype was prevalent in North America (4) . Kataja et al . (10) reported that nearly all (95%) of the erythromycin-resistant group C streptococcus isolates had the M phenotype, whereas 91% of the erythromycin-resistant group G streptococcus isolates had the iMLS_B phenotype . In our study, S . pyogenes isolates showed a nearly equal distribution of MLS_B resistance phenotypes (Table 3) . The prevalence rate of the cMLS_B resistance phenotype in S . agalactiae was much higher than in streptococci of other serogroups, and the M phenotype was more prevalent in group G streptococci .

 
We found that erythromycin and clindamycin resistance was relatively common, particularly among S . agalactiae; that the cMLS_B resistance phenotype was dominant among erythromycin-resistant BHS; and that rates of S . agalactiae resistance to erythromycin and clindamycin showed an increasing trend in Korea .

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