Ann Clin Microbiol.  2016 Mar;19(1):13-19. 10.5145/ACM.2016.19.1.13.

Prevalence and Antimicrobial Susceptibility of Genital Mycoplasmataceae in Korean Women: Correlation between Phenotypic Test and Resistance Genes

• Chang J
• Yu JK
• Song C
• Park IY
• Park YJ

• KMID: 2160080
• DOI: http://doi.org/10.5145/ACM.2016.19.1.13

Abstract

BACKGROUND
While 7.6% of cultured genital Mycoplasmataceae was identified as Ureaplasma urealyticum, most of them were Ureaplasma parvum (80.3%). This is the first study differentiating between these two species. We investigated the prevalence and antimicrobial resistance of genital Mycoplasmataceae in Korean women.
METHODS
A total of 150 specimens submitted to the laboratory for culture of M. hominis and Ureaplasma spp. were included. Detection and antimicrobial susceptibility tests were performed with the Mycoplasma IST2 kit (bioMérieux, France). The identification of Ureaplasma spp. was performed by PCR, and mutations in drug resistance genes were investigated by PCR and sequencing.
RESULTS
In total, 66 specimens (44.0%) were positive for genital Mycoplasmatacea: U. parvum, 53 (80.3%); U. urealyticum, 5 (7.6%); M. hominis, 2 (3.0%); mixed infection, 6 (9.1%). Susceptibilities of Ureaplasma spp. to erythromycin, azithromycin, clarithromycin, and doxycycline were 86.0%, 80.7%, 98.2%, and 94.7%, respectively. The susceptibility of Ureaplasma spp. to ofloxacin and ciprofloxacin was 47.4% and 17.5%, respectively. The S83L mutation was found in the ParC subunit of the ofloxacin-resistant (5/7, 71.4%) and the ciprofloxacin-resistant isolates (7/14, 50.0%). One M. hominis isolate showed resistance to erythromycin, azithromycin, and clarithromycin but susceptibility to josamycin, pristinamycin, fluoroquinolones, and tetracyclines.
CONCLUSION
The prevalence of genital Mycoplasmataceae in Korean women was 44.0%; most of them were identified as U. parvum. As more than 10% of Ureaplasma spp. showed non-susceptibility to erythromycin and azithromycin (15.5%, 20.7%), a susceptibility test is needed prior to use of these antibiotics. Further study is needed about the clinical features of infections caused by U. urealyticum vs. U. parvum and their associated resistance mechanisms.

Keyword

Antimicrobial susceptibility; Mycoplasma IST2 kit; Ureaplasma parvum; Ureaplasma urealyticum

MeSH Terms

Anti-Bacterial Agents
Azithromycin
Ciprofloxacin
Clarithromycin
Coinfection
Doxycycline
Drug Resistance
Erythromycin
Female
Fluoroquinolones
Humans
Josamycin
Mycoplasma
Mycoplasmataceae*
Ofloxacin
Polymerase Chain Reaction
Prevalence*
Pristinamycin
Tetracyclines
Ureaplasma
Ureaplasma urealyticum
Anti-Bacterial Agents
Azithromycin
Ciprofloxacin
Clarithromycin
Doxycycline
Erythromycin
Fluoroquinolones
Josamycin
Ofloxacin
Pristinamycin
Tetracyclines

Figure

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  Fig. 1. Clostridium difficile isolates from unformed stool (CDI or colonization): Number and proportion of isolates (total 251 unduplicated isolates). Abbreviations: CDI, Clostridium difficile infection; HCFA-HO, healthcare facility-associated hospital onset; HCFA-CO, healthcare facility-associated community onset; CA, community-associated community onset.

Reference

References

1. Dubberke ER, Reske KA, Yan Y, Olsen MA, McDonald LC, Fraser VJ. Clostridium difficile–associated disease in a setting of endemicity: identification of novel risk factors. Clin Infect Dis. 2007; 45:1543–9.

2. Bignardi GE. Risk factors for Clostridium difficile infection. J Hosp Infect. 1998; 40:1–15.

3. Zilberberg MD, Shorr AF, Kollef MH. Increase in adult Clostridium difficile-related hospitalizations and case-fatality rate, United States, 2000–2005. Emerg Infect Dis. 2008; 14:929–31.

4. Centers for Disease Control and Prevention. Antibiotic resistance threats in the United States, 2013. http://www.cdc.gov/drugresistance/threat-report-2013/pdf/ar-threats-2013-508.pdf. [Online] (last visited on 15 March 2016).

5. Kim YS, Han DS, Kim YH, Kim WH, Kim JS, Kim HS, et al. Incidence and clinical features of Clostridium difficile infection in Korea: a nationwide study. Epidemiol Infect. 2013; 141:189–94.

6. Tan XQ, Verrall AJ, Jureen R, Riley TV, Collins DA, Lin RT, et al. The emergence of community-onset Clostridium difficile infection in a tertiary hospital in Singapore: a cause for concern. Int J Antimicrob Agents. 2014; 43:47–51.

7. Chitnis AS, Holzbauer SM, Belflower RM, Winston LG, Bamberg WM, Lyons C, et al. Epidemiology of community-associated Clostridium difficile infection, 2009 through 2011. JAMA Intern Med. 2013; 173:1359–67.

8. Gupta A and Khanna S. Community-acquired Clostridium difficile infection: an increasing public health threat. Infect Drug Resist. 2014; 7:63–72.

9. Choi HK, Kim KH, Lee SH, Lee SJ. Risk factors for recurrence of Clostridium difficile infection: effect of vancomycin-resistant enterococci colonization. J Korean Med Sci. 2011; 26:859–64.

10. Shin BM, Moon SJ, Kim YS, Shin WC, Yoo HM. Characterization of cases of Clostridium difficile infection (CDI) presenting at an emergency room: molecular and clinical features differentiate community-onset hospital-associated and community-associated CDI in a tertiary care hospital. J Clin Microbiol. 2011; 49:2161–5.

11. Cohen SH, Gerding DN, Johnson S, Kelly CP, Loo VG, McDonald LC, et al. Clinical practice guidelines for Clostridium difficile infection in adults: 2010 update by the society for healthcare epidemiology of America (SHEA) and the infectious diseases society of America (IDSA). Infect Control Hosp Epidemiol. 2010; 31:431–55.

12. Friedman ND, Kaye KS, Stout JE, McGarry SA, Trivette SL, Briggs JP, et al. Health care–associated bloodstream infections in adults: a reason to change the accepted definition of community-acquired infections. Ann Intern Med. 2002; 137:791–7.

13. Dubberke ER, Carling P, Carrico R, Donskey CJ, Loo VG, McDonald LC, et al. Strategies to prevent Clostridium difficile infections in acute care hospitals: 2014 Update. Infect Control Hosp Epidemiol. 2014; 35:628–45.

14. Bacci S, Mølbak K, Kjeldsen MK, Olsen KE. Binary toxin and death after Clostridium difficile infection. Emerg Infect Dis. 2011; 17:976–82.

15. Evans CT and Safdar N. Current trends in the epidemiology and outcomes of Clostridium difficile infection. Clin Infect Dis. 2015; 60(Suppl 2):S66–71.

16. Ogielska M, Lanotte P, Le Brun C, Valentin AS, Garot D, Tellier AC, et al. Emergence of community-acquired Clostridium difficile infection: the experience of a French hospital and review of the literature. Int J Infect Dis. 2015; 37:36–41.

17. Mori N and Aoki Y. Clinical characteristics and risk factors for community-acquired Clostridium difficile infection: A retrospective, case-control study in a tertiary care hospital in Japan. J Infect Chemother. 2015; 21:864–7.

18. Tan XQ, Verrall AJ, Jureen R, Riley TV, Collins DA, Lin RT, et al. The emergence of community-onset Clostridium difficile infection in a tertiary hospital in Singapore: a cause for concern. Int J Antimicrob Agents. 2014; 43:47–51.

19. Dantes R, Mu Y, Hicks LA, Cohen J, Bamberg W, Beldavs ZG, et al. Association between outpatient antibiotic prescribing practices and community-associated Clostridium difficile infection. Open Forum Infect Dis. 2015; 2:ofv113.

20. Clabots CR, Johnson S, Olson MM, Peterson LR, Gerding DN. Acquisition of Clostridium difficile by hospitalized patients: evidence for colonized new admissions as a source of infection. J Infect Dis. 1992; 166:561–7.

21. McFarland LV, Mulligan ME, Kwok RY, Stamm WE. Nosocomial acquisition of Clostridium difficile infection. N Engl J Med. 1989; 320:204–10.

22. Johnson S, Clabots CR, Linn FV, Olson MM, Peterson LR, Gerding DN. Nosocomial Clostridium difficile colonisation and disease. Lancet. 1990; 336:97–100.

23. Hung YP, Tsai PJ, Hung KH, Liu HC, Lee CI, Lin HJ, et al. Impact of toxigenic Clostridium difficile colonization and infection among hospitalized adults at a district hospital in southern Taiwan. PLoS One. 2012; 7:e42415.

24. Alcalá L, Reigadas E, Marín M, Martín A, Catalán P, Bouza E. Spanish Clostridium difficile Study Group. Impact of clinical awareness and diagnostic tests on the underdiagnosis of Clostridium difficile infection. Eur J Clin Microbiol Infect Dis. 2015; 34:1515–25.

25. Mohan SS, McDermott BP, Parchuri S, Cunha BA. Lack of value of repeat stool testing for Clostridium difficile toxin. Am J Med. 2006; 119:356. .e7–8.

26. Lo Vecchio A and Zacur GM. Clostridium difficile infection: an update on epidemiology, risk factors, and therapeutic options. Curr Opin Gastroenterol. 2012; 28:1–9.

27. Maroo S and Lamont JT. Recurrent Clostridium difficile. Gastroenterology. 2006; 130:1311–6.

28. Gerding DN, Johnson S, Rupnik M, Aktories K. Clostridium difficile binary toxin CDT: mechanism, epidemiology, and potential clinical importance. Gut Microbes. 2014; 5:15–27.