Antimicrobial resistance, genetic resistance determinants for ceftriaxone and molecular epidemiology of Neisseria gonorrhoeae isolates in Nanjing, China

Journal of Antimicrobial Chemotherapy

Volumn 69, Issue 11, 2014, Pages 2959-2965

  Chen, Shao Chun ^a   Yin, Yue Ping ^a   Dai, Xiu Qin ^a   Unemo, Magnus ^b   Chen, Xiang Sheng ^a  

^a CHINESE CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

^b ÖREBRO UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Gonorrhoea; mtrR; NG MAST; penA; porB; Treatment

Indexed keywords

AZITHROMYCIN; CEFTRIAXONE; CIPROFLOXACIN; SPECTINOMYCIN; TETRACYCLINE; ANTIINFECTIVE AGENT;

ADOLESCENT; ADULT; AGAR DILUTION; AGED; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIUM ISOLATE; CHINA; FEMALE; GENE SEQUENCE; GENETIC RESISTANCE; HUMAN; MAJOR CLINICAL STUDY; MALE; MOLECULAR EPIDEMIOLOGY; NEISSERIA GONORRHOEAE; NONHUMAN; SEQUENCE ANALYSIS; VERY ELDERLY; DRUG EFFECTS; EPIDEMIOLOGY; GENETICS; ISOLATION AND PURIFICATION; MIDDLE AGED; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; ANTI-BACTERIAL AGENTS; ANTI-INFECTIVE AGENTS; CEFTRIAXONE; CHINA; DRUG RESISTANCE, BACTERIAL; HUMANS; MALE; MIDDLE AGED; MOLECULAR EPIDEMIOLOGY; NEISSERIA GONORRHOEAE; YOUNG ADULT;

EID: 84924042491     PISSN: 03057453     EISSN: 14602091     Source Type: Journal    
DOI: 10.1093/jac/dku245     Document Type: Article

References (48)

1. WHO. Global Incidence and Prevalence of Selected Curable Sexually Transmitted Infections-2008. Geneva: WHO. http://www.who.int/reproductivehealth/publications/rtis/2008_STI_estimates.pdf (28 May 2014, date last accessed).
2. Chinese CDC. Reports From National STI Surveillance System in China-2012. Nanjing: Chinese CDC. http://www.ncstdc.org/upfiles/201303/20130319152506703.pdf (28 May 2014, date last accessed).
3. Cohen MS. Classical sexually transmitted diseases drive the spread of HIV-1: back to the future. J Infect Dis 2012; 206: 1-2.
4. Unemo M, Nicholas RA. Emergence of multidrug-resistant, extensively drug-resistant and untreatable gonorrhea. Future Microbiol 2012; 7: 1401-22.
5. Unemo M, Shafer WM. Antibiotic resistance in Neisseria gonorrhoeae: origin, evolution, and lessons learned for the future. Ann N Y Acad Sci 2011; 1230: E19-28.
6. Lewis DA. Global resistance of Neisseria gonorrhoeae: when theory becomes reality. Curr Opin Infect Dis 2014; 27: 62-7.
7. Tapsall JW, Ndowa F, Lewis DA et al. Meeting the public health challenge of multidrug-and extensively drug-resistant Neisseria gonorrhoeae. Expert Rev Anti Infect Ther 2009; 7: 821-34.
8. Stoltey JE, Barry PM. The use of cephalosporins for gonorrhea: an update on the rising problem of resistance. Expert Opin Pharmacother 2012; 13: 1411-20.
9. Kirkcaldy RD, Ballard RC, Dowell D. Gonococcal resistance: are cephalosporins next? Curr Infect Dis Rep 2011; 13: 196-204.
10. Yokoi S, Deguchi T, Ozawa Tet al. Threat to cefixime treatment for gonorrhea. Emerg Infect Dis 2007; 13: 1275-7.
11. Unemo M, Golparian D, Syversen G et al. Two cases of verified clinical failures using internationally recommended first-line cefixime for gonorrhoea treatment, Norway, 2010. Euro Surveill 2010; 15: pii=19721.
12. Ison CA, Hussey J, Sankar KN et al. Gonorrhoea treatment failures to cefixime and azithromycin in England, 2010. Euro Surveill 2011; 16: pii=19833.
13. Unemo M, Golparian D, Stary A et al. First Neisseria gonorrhoeae strain with resistance to cefixime causing gonorrhoea treatment failure in Austria, 2011. Euro Surveill 2011; 16: pii=19998.
14. Unemo M, Golparian D, Nicholas R et al. High-level cefixime-and ceftriaxone-resistant Neisseria gonorrhoeae in France: novel penA mosaic allele in a successful international clone causes treatment failure. Antimicrobial Agents Chemother 2012; 56: 1273-80.
15. Allen VG, Mitterni L, Seah C et al. Neisseria gonorrhoeae treatment failure and susceptibility to cefixime in Toronto, Canada. JAMA 2013; 309: 163-70.
16. Lewis DA, Sriruttan C, Müller EE et al. Phenotypic and genetic characterization of the first two cases of extended-spectrum-cephalosporinresistant Neisseria gonorrhoeae infection in South Africa and association with cefixime treatment failure. J Antimicrob Chemother 2013; 68: 1267-70.
17. Japanese Society of Sexually Transmitted Infection. Gonococcal infection. Sexually transmitted infections, diagnosis and treatment guidelines 2011. Jpn J Sex Transm Dis 2011; 22 Suppl 1: 52-9. In Japanese.
18. CDC. Update to CDC's Sexually Transmitted Diseases Treatment Guidelines, 2010: oral cephalosporins no longer a recommended treatment for gonococcal infections. MMWR Morb Mortal Wkly Rep 2012; 61: 590-4.
19. Bignell C, Unemo M. 2012 European guideline on the diagnosis and treatment of gonorrhoea in adults. Int J STD AIDS 2013; 24: 85-92.
20. Ohnishi M, Saika T, Hoshina S et al. Ceftriaxone-resistant Neisseria gonorrhoeae, Japan. Emerg Infect Dis 2011; 17: 148-9.
21. Ohnishi M, Golparian D, Shimuta 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.
22. Tapsall J, Read P, Carmody C et al. Two cases of failed ceftriaxone treatment in pharyngeal gonorrhoea verified by molecular microbiological methods. J Med Microbiol 2009; 58: 683-7.
23. Chen MY, Stevens K, Tideman R et al. Failure of 500mg of ceftriaxone to eradicate pharyngeal gonorrhoea, Australia. J Antimicrob Chemother 2013; 68: 1445-7.
24. Read PJ, Limnios EA, McNulty A et al. One confirmed and one suspected case of pharyngeal gonorrhoea treatment failure following 500 mg ceftriaxone in Sydney, Australia. Sex Health 2013; 10: 460-2.
25. 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.
26. Unemo M, Golparian D, Potocnik M et al. Treatment failure of pharyngeal gonorrhoea with internationally recommended first-line ceftriaxone verified in Slovenia, September 2011. Euro Surveill 2012; 17: pii=20200.
27. Camara J, Serra J, Ayats J et al. Molecular characterization of two highlevel ceftriaxone-resistant Neisseria gonorrhoeae isolates detected in Catalonia, Spain. J Antimicrob Chemother 2012; 67: 1858-60.
28. Wang Q, Zhang G. Guidelines for Diagnosis and Treatment of Sexually Transmitted Diseases. Shanghai: Shanghai Science and Technology Press, 2007.
29. Martin I, Ison CA, Aanensen DM et al. Rapid sequence-based identification of gonococcal transmission clusters in a large metropolitan area. J Infect Dis 2004; 189: 1497-505.
30. Unemo M, Dillon JA. Review and international recommendation of methods for typing Neisseria gonorrhoeae isolates and their implications for improved knowledge of gonococcal epidemiology, treatment, and biology. Clin Microbiol Rev 2011; 24: 447-58.
31. Unemo M, Ballard R, Ison C et al. (Editors) Laboratory Diagnosis of Sexually Transmitted Infections, Including Human Immunodeficiency Virus. Geneva: WHO, 2013. http://apps.who.int/iris/bitstream/10665/85343/1/9789241505840_eng.pdf (28 May 2014, date last accessed).
32. Unemo M, Fasth O, Fredlund H et al. Phenotypic and genetic characterization of the 2008 WHO Neisseria gonorrhoeae reference strain panel intended for global quality assurance and quality control of gonococcal antimicrobial resistance surveillance for public health purposes. J Antimicrob Chemother 2009; 63: 1142-51.
33. Liao M, Gu WM, Yang Y et al. Analysis of mutations in multiple loci of Neisseria gonorrhoeae isolates reveals effects of PIB, PBP2 and MtrR on reduced susceptibility to ceftriaxone. J Antimicrob Chemother 2011; 66: 1016-23.
34. Chen SC, Yin YP, Dai XQ et al. Prevalence and molecular epidemiological typing of penicillinase-producing Neisseria gonorrhoeae and their blaTEM-135 gene variants in Nanjing, China. Sex Transm Dis 2013; 40: 872-6.
35. Lee SG, Lee H, Jeong SH et al. Various penA mutations together with mtrR, porB and ponA mutations in Neisseria gonorrhoeae isolates with reduced susceptibility to cefixime or ceftriaxone. J Antimicrob Chemother 2010; 65: 669-75.
36. Zhao S, Duncan M, Tomberg J et al. Genetics of chromosomally mediated intermediate resistance to ceftriaxone and cefixime in Neisseria gonorrhoeae. Antimicrob Agents Chemother 2009; 53: 3744-51.
37. Tapsall JW, Ray S, Limnios A. Characteristics and population dynamics of mosaic penA allele-containing Neisseria gonorrhoeae isolates collected in Sydney, Australia, in 2007-2008. Antimicrob Agents Chemother 2010; 54: 554-6.
38. Tomberg J, Unemo M, Davies C et al. Molecular and structural analysis of mosaic variants of penicillin-binding protein 2 conferring decreased susceptibility to expanded-spectrum cephalosporins in Neisseria gonorrhoeae: role of epistatic mutations. Biochemistry 2010; 49: 8062-70.
39. Whiley DM, Goire N, Lambert SB et al. Reduced susceptibility to ceftriaxone in Neisseria gonorrhoeae is associated with mutations G542S, P551S and P551L in the gonococcal penicillin-binding protein 2. J Antimicrob Chemother 2010; 65: 1615-8.
40. Ohneck EA, Zalucki YM, Johnson PJ et al. A novel mechanism of highlevel, broad-spectrum antibiotic resistance caused by a single base pair change in Neisseria gonorrhoeae. MBio 2011; 2: e00187-11.
41. Tapsall JW. Implications of current recommendations for thirdgeneration cephalosporin use in the WHOWestern Pacific Region following the emergence of multiresistant gonococci. Sex Transm Infect 2009; 85: 256-8.
42. Lahra MM. Annual report of the Australian Gonococcal Surveillance Programme, 2011. Commun Dis Intell Q Rep 2012; 36: E166-73.
43. Shimuta K, Unemo M, Nakayama S et al. Antimicrobial resistance and molecular typing of Neisseria gonorrhoeae isolates in Kyoto and Osaka, Japan in 2010-2012-intensified surveillance after identification of the first high-level ceftriaxone resistant strain H041. Antimicrob Agents Chemotherapy 2013; 57: 5225-32.
44. Tanaka M, Shimojima M, Saika Tet al. Nationwide antimicrobial susceptibility survey of Neisseria gonorrhoeae isolates in Japan. Kansenshogaku Zasshi 2011; 85: 360-5. In Japanese.
45. Huang CT, Yen MY, Wong WW et al. Characteristics and dissemination of mosaic penicillin-binding protein 2-harboring multidrugresistant Neisseria gonorrhoeae isolates with reduced cephalosporin susceptibility in northern Taiwan. Antimicrob Agents Chemother 2010; 54: 4893-5.
46. Bauer HM, Mark KE, Samuel M et al. Prevalence of and associated risk factors for fluoroquinolone-resistant Neisseria gonorrhoeae in California, 2000-2003. Clin Infect Dis 2005; 41: 795-803.
47. Jeverica S, Golparian D, MaticicMet al. Phenotypic and molecular characterization of Neisseria gonorrhoeae isolates fromSlovenia, 2006-12: rise and fall of the multidrug-resistant NG-MAST genogroup 1407 clone?. J Antimicrob Chemother 2014; 69: 1517-25.
48. Tomberg J, Unemo M, Ohnishi M et al. Identification of amino acids conferring high-level resistance to expanded-spectrum cephalosporins in the penA gene from Neisseria gonorrhoeae strain H041. Antimicrob Agents Chemother 2013; 57: 3029-36.