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Abstract
Serological methods for the epidemiological study of Streptococcus pyogenes, such as T-, or M-typing, were replaced by emm typing in the 2000s. The frequency of emm types may differ according to geographical area and study period. Erythromycin resistance rates and the prevalence of erythromycin-resistant phenotypes in several countries are surveyed, and common emm genotypes associated with erythromycin resistance are described for each country. There is no correlation between erythromycin resistance and macrolide use in Korea. S. pyogenes is thought to cause severe illness, such as streptococcal toxic shock syndrome (STSS) and necrotizing fasciitis. The mortality rate of STSS is about 50%, and there have been several hundred victims of STSS in Japan in the last 2 decades. The resistance rate to macrolides peaked at 50% in 2002, and currently, ＜10% of strains exhibit macrolide resistance in Korea. However, the erythromycin resistance rate recently exceeded 90% in China. Considering increases of travel between neighboring countries, a vigilant survey to monitor these highly virulent and antibiotic-resistant strains is necessary.
REFERENCES
1. Markowitz M and Kaplan EL. Reappearance of rheumatic fever. Adv Pediatr. 1989; 36:39–65.
2. Johnson DR, Stevens DL, Kaplan EL. Epidemiologic analysis of group A streptococcal serotypes associated with severe systemic infections, rheumatic fever, or uncomplicated pharyngitis. J Infect Dis. 1992; 166:374–82.
3. Stevens DL. Streptococcal toxic shock syndrome. Clin Microbiol Infect. 2002; 8:133–6.
4. Nakashima K, Ichiyama S, Iinuma Y, Hasegawa Y, Ohta M, Ooe K, et al. A clinical and bacteriologic investigation of invasive streptococcal infections in Japan on the basis of serotypes, toxin production, and genomic DNA fingerprints. Clin Infect Dis. 1997; 25:260–6.
5. McNeil SA, Halperin SA, Langley JM, Smith B, Warren A, Sharratt GP, et al. Safety and immunogenicity of 26-valent group a streptococcus vaccine in healthy adult volunteers. Clin Infect Dis. 2005; 41:1114–22.
6. Gerber MA. Treatment failures and carriers: perception or problems? Pediatr Infect Dis J. 1994; 13:576–9.
7. Cockerill FR 3rd, MacDonald KL, Thompson RL, Roberson F, Kohner PC, Besser-Wiek J, et al. An outbreak of invasive group A streptococcal disease associated with high carriage rates of the invasive clone among school-aged children. JAMA. 1997; 277:38–43.
8. Kim SJ. Bacteriologic characteristics and serotypings of Streptococcus pyogenes isolated from throats of school children. Yonsei Med J. 2000; 41:56–60.
9. Johnson DR and Kaplan EL. Microtechnique for serum opacity factor characterization of group A streptococci adaptable to the use of human sera. J Clin Microbiol. 1988; 26:2025–30.
10. Kim S and Lee NY. Epidemiological usefulness of anti-opacity factor antibody screening in schoolchildren. J Clin Microbiol. 2001; 39:1316–8.
11. Beall B, Facklam R, Thompson T. Sequencing emm-specific PCR products for routine and accurate typing of group A streptococci. J Clin Microbiol. 1996; 34:953–8.
12. Koh EH, Maeng KY, Kim S, Jeong HJ, Lee NY. A decrease in erythromycin resistance rate of Streptococcus pyogenes in 2004 in Jinju. Korean J Clin Microbiol. 2006; 9:51–7.
13. Yi YH, Choi JH, Lee HK, Lee KJ, Bae SM, Yu JY, et al. Characterization of erythromycin resistance of Streptococcus pyogenes isolated from pharyngitis patients in Korea. Jpn J Infect Dis. 2006; 59:192–4.
14. Creti R, Imperi M, Baldassarri L, Pataracchia M, Recchia S, Alfarone G, et al. emm Types, virulence factors, and antibiotic resistance of invasive Streptococcus pyogenes isolates from Italy: What has changed in 11 years? J Clin Microbiol. 2007; 45:2249–56.
15. Choi EH. Emergence of macrolide resistance and clinical use of macrolide antimicrobials in children. Korean J Pediatr. 2008; 51:1031–7.
16. Cha S, Lee H, Lee K, Hwang K, Bae S, Lee Y. The emergence of erythromycin-resistant Streptococcus pyogenes in Seoul, Korea. J Infect Chemother. 2001; 7:81–6.
17. Kim S and Lee NY. Epidemiology and antibiotic resistance of group A streptococci isolated from healthy schoolchildren in Korea. J Antimicrob Chemother. 2004; 54:447–50.
18. Chong YS, Lee KW, Kown OH, Park HS. Antimicrobial susceptibility of Streptococcus pyogenes and Streptococcus agalactiae. J Korean Soc Chemother. 1994; 12:111–5.
19. Uh Y, Jang IH, Hwang GY, Lee MK, Yoon KJ, Kim HY. Antimicrobial susceptibility patterns and macrolide resistance genes of beta-hemolytic streptococci in Korea. Antimicrob Agents Chemother. 2004; 48:2716–8.
20. Bae SY, Kim JS, Kwon JA, Yoon SY, Lim CS, Lee KN, et al. Phenotypes and genotypes of macrolide-resistant Streptococcus pyogenes isolated in Seoul, Korea. J Med Microbiol. 2007; 56:229–35.
21. Chan JC, Chu YW, Chu MY, Cheung TK, Lo JY. Epidemiological analysis of Streptococcus pyogenes infections in Hong Kong. Pathology. 2009; 41:681–6.
22. Feng L, Lin H, Ma Y, Yang Y, Zheng Y, Fu Z, et al. Macrolide-resistant Streptococcus pyogenes from Chinese pediatric patients in association with Tn916 transposons family over a 16-year period. Diagn Microbiol Infect Dis. 2010; 67:369–75.
23. Green MD, Beall B, Marcon MJ, Allen CH, Bradley JS, Dashefsky B, et al. Multicentre surveillance of the prevalence and molecular epidemiology of macrolide resistance among pharyngeal isolates of group A streptococci in the USA. J Antimicrob Chemother. 2006; 57:1240–3.
24. Richter SS, Heilmann KP, Beekmann SE, Miller NJ, Miller AL, Rice CL, et al. Macrolide-resistant Streptococcus pyogenes in the United States, 2002-2003. Clin Infect Dis. 2005; 41:599–608.
25. Ardanuy C, Domenech A, Rolo D, Calatayud L, Tubau F, Ayats J, et al. Molecular characterization of macrolide- and multidrug-resistant Streptococcus pyogenes isolated from adult patients in Barcelona, Spain (1993-2008). J Antimicrob Chemother. 2010; 65:634–43.
26. Pérez-Trallero E, Montes M, Orden B, Tamayo E, García-Arenzana JM, Marimón JM. Phenotypic and genotypic characterization of Streptococcus pyogenes isolates displaying the MLSB phenotype of macrolide resistance in Spain, 1999 to 2005. Antimicrob Agents Chemother. 2007; 51:1228–33.
27. Zampaloni C, Cappelletti P, Prenna M, Vitali LA, Ripa S. emm Gene distribution among erythromycin-resistant and -susceptible Italian isolates of Streptococcus pyogenes. J Clin Microbiol. 2003; 41:1307–10.
28. Michos AG, Bakoula CG, Braoudaki M, Koutouzi FI, Roma ES, Pangalis A, et al. Macrolide resistance in Streptococcus pyogenes: prevalence, resistance determinants, and emm types. Diagn Microbiol Infect Dis. 2009; 64:295–9.
29. Fujita K, Murono K, Yoshikawa M, Murai T. Decline of erythromycin resistance of group A streptococci in Japan. Pediatr Infect Dis J. 1994; 13:1075–8.
30. Bass JW, Weisse ME, Plymyer MR, Murphy S, Eberly BJ. Decline of erythromycin resistance of group A beta-hemolytic streptococci in Japan. Comparison with worldwide reports. Arch Pediatr Adolesc Med. 1994; 148:67–71.
31. Bergman M, Huikko S, Pihlajamäki M, Laippala P, Palva E, Huovinen P, et al. Finnish Study Group for Antimicrobial Resistance (FiRe Network). Effect of macrolide consumption on erythromycin resistance in Streptococcus pyogenes in Finland in 1997-2001. Clin Infect Dis. 2004; 38:1251–6.
32. Koh E and Kim S. Decline in erythromycin resistance in group A streptococci from acute pharyngitis due to changes in the emm genotypes rather than restriction of antibiotic use. Korean J Lab Med. 2010; 30:485–90.
33. Oliver MA, García-Delafuente C, Cano ME, Pérez-Hernández F, Martínez-Martínez L, Albertí S. Rapid decrease in the prevalence of macrolide-resistant group A streptococci due to the appearance of two epidemic clones in Cantabria (Spain). J Antimicrob Chemother. 2007; 60:450–2.
34. Albertí S, García-Rey C, Domínguez MA, Aguilar L, Cercenado E, Gobernado M, et al. Spanish Surviellance Group for Respiratory Pathogens. Survey of emm gene sequences from pharyngeal Streptococcus pyogenes isolates collected in Spain and their relationship with erythromycin susceptibility. J Clin Microbiol. 2003; 41:2385–90.
35. Horn DL, Zabriskie JB, Austrian R, Cleary PP, Ferretti JJ, Fischetti VA, et al. Why have group A streptococci remained susceptible to penicillin? Report on a symposium. Clin Infect Dis. 1998; 26:1341–5.
Table 1.
Erythromycin resistance rates and predominant phenotypes of Streptococcus pyogenes in the last 20 years
| Country | Period | N | Erythromycin resistance rates | Predominant phenotypes | Reference |
|---|---|---|---|---|---|
| Korea | 2002 | 98 | 51.0% | cMLSB (61.2%) | 17 |
| Korea | 2004 | 328 | 9.8% | cMLSB (87.5%) | 12 |
| Korea | 1990-2000 | 143 | 16.1% | MLSB∗ (65%) | 19 |
| Korea | 1998-2003 | 615 | 20.5% | M (45%), cMLSB (42%) | 13 |
| Korea | 1998 | 92 | 41.3% | Not specified | 16 |
| Korea | 1980-1992 | 59 | 2.0% | Not specified | 18 |
| Korea | 1997-2003 | 222 | 23.0% | iMLSB (51%), cMLSB (31%) | 20 |
| Hong Kong | 2005-2008 | 281 | 25.6% | Not specified | 21 |
| China | 1993-1994 | 137 | 79.7% | cMLSB (90%) | 22 |
| China | 2005-2008 | 319 | 94.0% | cMLSB (99%) | 22 |
| USA | 2002-2003 | 1,885 | 6.8% | iMLSB (47%), M (44%) | 24 |
| USA | 2002-2003 | 2,797 | 6.1% | M (62%) | 23 |
| Italy | 1994-1996 | 118 | 26.5% | cMLSB (＞80%) | 14 |
| Spain | 1999-2005 | 17,232 | 21.3% | M (＞80%) before 2003; cMLSB (∼50%) in 2003-2005 | 26 |
| Spain | 2001-2004 | 146 | 34.2% | MLSB (∼70%) | 25 |
| Spain | 2007-2008 | 108 | 7.4% | MLSB (∼70%) | 25 |
| Greece | 2003-2006 | 1,160 | 14.9% | M (54%), iMLSB (40%) | 28 |
Table 2.
Association of emm genotypes and erythromycin-resistant phenotypes of Streptococcus pyogenes
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