Journal List > Ann Clin Microbiol > v.16(4) > 1078483

Kim, Seo, Kim, Lee, Lee, Lee, and Chong: Antimicrobial Resistance and Molecular Epidemiologic Characteristics of Neisseria gonorrhoeae Isolated from Korea in 2013

초록

Background

Antimicrobial resistance of Neisseria gonorrhoeae has become a serious problem world-wide, and ceftriaxone non-susceptible isolates have been recently reported from Japan and Europe. In this study, we evaluated the antimicrobial susceptibil-ities and molecular epidemiological characteristics of isolates from Korea in 2013.

Methods

Sixty strains of N. gonorrhoeae were collected from Korean patients and prostitutes. Antimicrobial susceptibility was tested by the agar dilution and disk diffusion methods. N. gonorrhoeae multiantigen sequence typing (NG-MAST) was performed in order to determine the molecular epidemiologic relatedness.

Results

All of isolates were non-susceptible to pen-icillin G and tetracycline, and the rate of ciprofloxacin- resistant isolates was 95% in 2013. The MICs of ceftriaxone were within the susceptible range for all isolates, but one isolate non-susceptible to cefixime (MIC=0.5 μ g/mL) was encountered. The isolates with decreased susceptibility (MIC≤0.12 μ g/mL) to cefixime or ceftriaxone accounted for 10% and 14% of the isolates tested, respectively. In NG-MAST analysis, 40 different STs were encountered among the 59 isolates. Isolates that belonged to tbpB110 showed higher cefixime and ceftriaxone MICs (0.12-0.5 μ g/ mL) as well as cefixime resistance.

Conclusion

Most of the N. gonorrhoeae isolates showed susceptibility to spectinomycin and cephalosporins. Due to the emergence of isolates that are non-sus-ceptible to cefixime and the prevalence of isolates with the tbpB110 allele belonging to ST1407, which cause cefixime and ceftriaxone treatment failure in successful global clones of N. gonorrhoeae, a continuous nationwide antimicrobial surveillance program is required to monitor the emergence of cephalospor-in resistance in N. gonorrhoeae.

REFERENCES

1.Centers for Disease Control and Prevention. Sexually transmitted diseases surveillance 2011. http://www.cdc.gov/std/stats11/Surv2011.pdf/[Online. (last visited on 29 October 2013).
3.Lee H., Suh Y., Kim HM., Lee Y., Chung KT., Lee YS, et al. Antimicrobial susceptibility of Neisseria gonorrhoeae isolated in Korea in 2008. Korean J Clin Microbiol. 2009. 12(S1):S115.
4.Antimicrobial susceptibility of Neisseria gonorrhoeae isolated in Korea in 2009. Korean J Clin Microbiol. 2010. 13(S1):S88.
5.Korea Centers for Disease Control and Prevention, Management guidelines for sexually transmitted disease. Seoul: Korea Centers for Disease Control and Prevention;2007.
6.Korea Centers for Disease Control and Prevention, and Korean Association of Urogenital Tract Infection and Inflammation. Korean guideline for sexually transmitted disease. Seoul: Inomax Co.;2011.
7.Yong D., Kim TS., Choi JR., Yum JH., Lee K., Chong Y, et al. Epidemiological characteristics and molecular basis of fluoroquino-lone-resistant Neisseria gonorrhoeae strains isolated in Korea and nearby countries. J Antimicrob Chemother. 2004. 54:451–5.
8.Ohnishi M., Saika T., Hoshina S., Iwasaku K., Nakayama S., Watanabe H, et al. Ceftriaxone-resistant Neisseria gonorrhoeae, Japan. Emerg Infect Dis. 2011. 17:148–9.
9.Ohnishi M., Golparian D., Shimuta K., Saika T., Hoshina S., Iwasaku K, et al. Is Neisseria gonorrhoeae initiating a future era of untreatable gonorrhea?: detailed characterization of the first strain with high-level resistance to ceftriaxone. Antimicrob Agents Chemother. 2011. 55:3538–45.
10.Unemo M., Golparian D., Nicholas R., Ohnishi M., Gallay A., Sednaoui P. High-level cefixime- and ceftriaxone-resistant Neisseria gonorrhoeae in France: novel penA mosaic allele in a successful international clone causes treatment failure. Antimicrob Agents Chemother. 2012. 56:1273–80.
11.Cámara J., Serra J., Ayats J., Bastida T., Carnicer-Pont D., Andreu A, et al. Molecular characterization of two high-level ceftriaxone-resistant Neisseria gonorrhoeae isolates detected in Catalonia, Spain. J Antimicrob Chemother. 2012. 67:1858–60.
12.Cockerill FR. Performance Standards for Antimicrobial Susceptibility Testing: Twenty-third Informational Supplement. Document M100-S23. Wayne, PA; Clinical and Laboratory Standards Institute. 2013.
13.Bell SM, editor. Antibiotic Susceptibility Testing by the CDS Method. A Manual for Medical and Veterinary Laboratories 2009. 5th ed.
14.EUCAST. The European Committee on Antimicrobial Susceptibility Testing - EUCAST 2013. http://www.eucast.org/[Online. (last visited on 29 October 2013).
15.Kam KM., Lo KK., Ho NK., Cheung MM. Rapid decline in penicillinase-producing Neisseria gonorrhoeae in Hong Kong associated with emerging 4-fluoroquinolone resistance. Genitourin Med. 1995. 71:141–4.
16.Nakayama S., Tribuddharat C., Prombhul S., Shimuta K., Srifuengfung S., Unemo M, et al. Molecular analyses of TEM genes and their corresponding penicillinase-producing Neisseria gonorrhoeae isolates in Bangkok, Thailand. Antimicrob Agents Chemother. 2012. 56:916–20.
17.Kim HJ., Soe YH., Lee HM., Lee KW., Chong YS. Antimicrobial resistance and molecular epidemiologic characteristics of Neisseria gonorrhoeae recently isolated from Korea. Poster Presentation E-152. International Interscience Conference on Infection and Chemotherapy. 2013. 94.
18.Tapsall J., Read P., Carmody C., Bourne C., Ray S., Limnios A, et al. Two cases of failed ceftriaxone treatment in pharyngeal gonorrhoea verified by molecular microbiological methods. J Med Microbiol. 2009. 58:683–7.
crossref
19.Allen VG., Mitterni L., Seah C., Rebbapragada A., Martin IE., Lee C, et al. Neisseria gonorrhoeae treatment failure and susceptibility to cefixime in Toronto, Canada. JAMA. 2013. 309:163–70.
20.Ameyama S., Onodera S., Takahata M., Minami S., Maki N., Endo K, et al. Mosaic-like structure of penicillin-binding protein 2 Gene (penA) in clinical isolates of Neisseria gonorrhoeae with reduced susceptibility to cefixime. Antimicrob Agents Chemother. 2002. 46:3744–9.
21.Lindberg R., Fredlund H., Nicholas R., Unemo M. Neisseria gonorrhoeae isolates with reduced susceptibility to cefixime and ceftriaxone: association with genetic polymorphisms in penA, mtrR, porB1b, and ponA. Antimicrob Agents Chemother. 2007. 51:2117–22.
22.Singh AE., Gratrix J., Read R., Lovgren M., Drews SJ., Romanowski B, et al. Neisseria gonorrhoeae multiantigen sequence typing is beneficial in further characterizing gonococcal populations in Alberta, Canada. Sex Transm Dis. 2013. 40:744–50.
23.Shimuta K., Unemo M., Nakayama S., Morita-Ishihara T., Dorin M., Kawahata T, et al. Antibiotic-Resistant Gonorrhea Study Group. Antimicrobial resistance and molecular typing of Neisseria gonorrhoeae isolates in Kyoto and Osaka, Japan, 2010 to 2012: intensi-fied surveillance after identification of the first strain (H041) with high-level ceftriaxone resistance. Antimicrob Agents Chemother. 2013. 57:5225–32.
crossref
24.Kirkcaldy RD., Zaidi A., Hook EW 3rd., Holmes KK., Soge O., del Rio C, et al. Neisseria gonorrhoeae antimicrobial resistance among men who have sex with men and men who have sex exclusively with women: the Gonococcal Isolate Surveillance Project, 2005-2010. Ann Intern Med. 2013. 158:321–8.
25.Ison CA., Hussey J., Sankar KN., Evans J., Alexander S. Gonorrhoea treatment failures to cefixime and azithromycin in England, 2010. Euro Surveill 201116. pii: 19833.
26.Allen VG., Mitterni L., Seah C., Rebbapragada A., Martin IE., Lee C, et al. Neisseria gonorrhoeae treatment failure and susceptibility to cefixime in Toronto, Canada. JAMA. 2013. 309:163–70.
27.Unemo M., Golparian D., Hestner A. Ceftriaxone treatment failure of pharyngeal gonorrhoea verified by international recommendations, Sweden, July 2010. Euro Surveill. 2011. 16:pii: 19792.
crossref

Table 1.
Antimicrobial susceptibility of Neisseria gonorrhoeae isolates tested by diskdiffusion
Antimicrobial agents (Dosage) % of isolates with (N=60)
Susceptible Intermediate e NS Resistant
Penicillin G (10 U) 0 42   58
Spectinomycin (100 μ g) 100 0   0
Ceftriaxone (0.5 μ g) 50   50  
Ceftriaxone (30 μ g) 75   25  
Cefixime (5 μ g) 75   25  
Cefpodoxime (10 μ g) 82   18  
Cefotaxime (30 μ g) 70   30  
Tetracycline (30 μ g) 0 5   95
Ciprofloxacin (5 μ g) 5 2   93
Nalidixic acid (30 μ g) 7   93  
Azithromycin (15 μ g) 98   2  

Australiancriteria (CDS) were applied. CLSI criteria were applied for the other antimicrobial agents;

Not susceptible.

Table 2.
Antimicrobial susceptibility of Neisseria gonorrhoeae isolates tested by agar dilution
Antimicrobial agents MIC (μ g/mL) % of isolates with (N=59)
Range 50% 90% S I R
Penicillin G 0.12-128 1 4 0 75 25
Ceftriaxone ≤0.008-0.25 0.015 0.12 100 0 0
Cefixime ≤0.008-0.5 0.015 0.12 98 2 0
Cefpodoxime ≤0.008-4 0.06 0.5 92 8 0
Spectinomycin ≤16-32 32 32 100 0 0
Gentamicin ≤2-8 8 8 NA NA NA
Tetracycline ≤0.12-64 2 16 5 44 51
Ciprofloxacin ≤0.008-32 4 16 3 2 95
Azithromycin ≤0.06-2 0.12 0.5 85 13 2

EUCAST breakpoints were applied;

Not susceptible.

Abbreviations: S, susceptible; I, intermediate; R, resistant; NA, not applicable.

Table 3.
Number of isolates according to multiantigen sequence typing
Sequence type No. of isolates (N=59) s porB tbpB Region
ST6734 10 4,016 33 S, I, G, C, J
ST8043 5 206 455 I, G
ST9675 3 4,801 33 S
ST228 2 23 27 G, J
ST2066 2 1,042 328 I, W
ST2958 2 1,785 110 S, G
ST3968 2 2,409 21 I
ST9673 2 1,416 328 S, J
Other 31     S, I, G, W, C, J

New ST identified in this study;

ST205 (porB164 tbpB4), ST278(porB4 tbpB27), ST807 (porB37 tbpB27), ST1670 (porB23 tbpB1674)*, ST3435 (porB1053 tbpB21), ST4502 (porB1785 tbpB21), ST4764(porB2874 tbpB21), ST5699 (porB580 tbpB328), ST7132 (porB4270 tbpB129), ST7548 (porB4530 tbpB21), ST7684 (porB4618 tbpB21), ST7686 (porB4620 tbpB21), ST7688 (porB23 tbpB21), ST8160(porB4892 tbpB563), ST8181 (porB4872 tbpB33), ST8561 (porB101 tbpB29), ST9667 (porB4 tbpB677)*, ST9668 (porB5700 tbpB33)*, ST9669 (porB5701 tbpB110

)*, ST9671 (porB4016 tbpB862)*, ST 9672 (porB258 tbpB862)*, ST9674 (porB5702 tbpB455)*, ST9676(porB5703 tbpB186)*, ST9677 (porB5704 tbpB21)*, ST9678 (porB37 tbpB455)*, ST9679 (porB543 tbpB1692)*, ST9680 (porB5705 tbpB4)*, ST9681 (porB5706 tbpB4)*, ST9682 (porB5707 tbpB1336)*, ST9683(porB5708 tbpB21)*, ST9684 (porB5709 tbpB21)*;

The same tbpB type of ST1407.

Abbreviations: S, Seoul; I, Incheon; G, Gyeonggi; W, Wonju; C, Chungbuk; J, Junbuk.

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