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

Journal of Antimicrobial Chemotherapy

Volumn 63, Issue 6, 2009, Pages 1142-1151

  Unemo, Magnus ^a   Fasth, Oskar ^a   Fredlund, Hans ^a   Limnios, Athena ^b   Tapsall, John ^b  

^a ÖREBRO UNIVERSITY HOSPITAL   (Sweden)

^b PRINCE OF WALES HOSPITAL   (Australia)

Author keywords

2008 World Health Organization reference strains; Antimicrobial resistance testing and surveillance; Genotypic characterization; Quality assurance and quality control

Indexed keywords

AMPICILLIN; AZITHROMYCIN; CEFIXIME; CEFTRIAXONE; CEFUROXIME; CIPROFLOXACIN; ERTAPENEM; ERYTHROMYCIN; GENTAMICIN; KANAMYCIN; PENICILLIN G; QUINOLINE DERIVED ANTIINFECTIVE AGENT; RIFAMPICIN; SPECTINOMYCIN; TETRACYCLINE;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL STRAIN; BACTERIUM IDENTIFICATION; CONTROLLED STUDY; DNA POLYMORPHISM; GENETIC VARIABILITY; GENOME ANALYSIS; GENOTYPE; GONORRHEA; IMMUNOSURVEILLANCE; MULTILOCUS SEQUENCE TYPING; NEISSERIA GONORRHOEAE; NONHUMAN; PHENOTYPE; PUBLIC HEALTH; QUALITY CONTROL; SEROTYPE; STRAIN IDENTIFICATION; VALIDATION PROCESS; WORLD HEALTH ORGANIZATION;

ANTIGENS, BACTERIAL; AUSTRALIA; BACTERIAL TYPING TECHNIQUES; DNA, BACTERIAL; HUMANS; MICROBIAL SENSITIVITY TESTS; NEISSERIA GONORRHOEAE; PHOSPHOTRANSFERASES (CARBOXYL GROUP ACCEPTOR); PLASMIDS; QUALITY ASSURANCE, HEALTH CARE; QUALITY CONTROL; REFERENCE STANDARDS; SEQUENCE ANALYSIS, DNA; SEROTYPING;

EID: 65749101194     PISSN: 03057453     EISSN: 14602091     Source Type: Journal    
DOI: 10.1093/jac/dkp098     Document Type: Article

References (57)

1. Reyn A, Bentzon MW, Thayer JD et al. Results of comparative experiments using different methods for determining the sensitivity of Neisseria gonorrhoeae. Bull WHO 1965; 32: 477-502.
2. Australian Gonococcal Surveillance Programme. Use of a quality assurance scheme in a long-term multi-centric study of antimicrobial susceptibility in Neisseria gonorrhoeae. Genitourin Med 1990; 66: 8-13.
3. Australian Gonococcal Surveillance Program. Annual report of the Australian Gonococcal Surveillance Programme, 2007. Commun Dis Intell 2008; 32: 227-31.
4. WHO Western Pacific Region Gonococcal Antimicrobial Resistance Surveillance Programme. Surveillance of antimicrobial resistance of Neisseria gonorrhoeae in the WHO Western Pacific region, 1992-1994. Genitourin Med 1997; 73: 355-61.
5. WHO Western Pacific Gonococcal Antimicrobial Surveillance Programme. Surveillance of antibiotic resistance in Neisseria gonorrhoeae in the WHO Western Pacific Region, 2006. Commun Dis Intell 2008; 32: 48-51.
6. Lo JYC, Ho KM, Leung AOC et al. Ceftibuten resistance and treatment failure in gonococcal infection. Antimicrob Agents Chemother 2008; 52: 3564-7.
7. Lindberg R, Fredlund H, Nicholas R et al. 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.
8. Tapsall JW, Dillon J-A, Ison CA et al. Development of an expanded WHO control panel of Neisseria gonorrhoeae for use in surveillance of gonococcal antimicrobial resistance. 16th International Pathogenic Neisseria Conference 2008, 7-12 September 2008, Rotterdam, The Netherlands. Abstract O18, p. 34. Congress Care, IPNC, 2008.
9. Yokoi S, Deguchi T, Ozawa T et al. Threat to cefixime treatment for gonorrhea. Emerg Infect Dis 2007; 13: 1275-7.
10. Workowski KA, Berman SM, Douglas JM Jr. Emerging antimicrobial resistance in Neisseria gonorrhoeae: Urgent need to strengthen prevention strategies. Ann Intern Med 2008; 148: 606-13.
11. Deguchi T, Yasuda M. Lack of nationwide surveillance of antimicrobial resistance in Neisseria gonorrhoeae in Japan. Ann Intern Med 2008; 149: 363-4.
12. CDC. Sexually Transmitted Disease Surveillance 2006 Supplement: Gonococcal Isolate Surveillance Project (GISP) Annual Report 2006. CDC, Atlanta, GA, 2008.
13. GRASP Steering Group. The Gonococcal Resistance to Antimicrobials Surveillance Programme (GRASP) Year 2007 Report. London: Health Protection Agency 2008. http://www.hpa.org.uk (16 February 2009, date last accessed).
14. Kubanova A, Frigo N, Kubanov A et al. National surveillance of antimicrobial susceptibility in Neisseria gonorrhoeae in 2005-2006 and recommendations of first-line antimicrobial drugs for gonorrhoea treatment in Russia. Sex Transm Infect 2008; 84: 285-9.
15. Martin IM, Hoffman S, Ison CA; ESSTI Network. European Surveillance of Sexually Transmitted Infections (ESSTI): The first combined antimicrobial susceptibility data for Neisseria gonorrhoeae in Western Europe. J Antimicrob Chemother 2006; 58: 587-93.
16. Tapsall JW. Antibiotic Resistance in Neisseria gonorrhoeae. Geneva: World Health Organization, 2001. WHO document WHO/CDS/DRS/2001.3.
17. Gharizadeh B, Akhras M, Unemo M et al. Detection of gyrA mutations associated with ciprofloxacin resistance in Neisseria gonorrhoeae by rapid and reliable pre-programmed short DNA sequencing. Int J Antimicrob Agents 2005; 26: 486-90.
18. Unemo M, Olcén P, Fredlund H et al. Real-time PCR and subsequent pyrosequencing for screening of penAmosaic alleles and prediction of reduced susceptibility to expanded-spectrum cephalosporins in Neisseria gonorrhoeae. APMIS 2008; 116: 1004-8.
19. Whiley DM, Bates J, Limnios A et al. Use of a novel screening PCR indicates presence of Neisseria gonorrhoeae isolates with a mosaic penA gene sequence in Australia. Pathology 2007; 39: 445-6.
20. WHO GASP Document. Rationale and applications for the current (2008) WHO panel of Neisseria gonorrhoeae for antimicrobial resistance surveillance for public health purposes, and instructions for their use. Technical document D007-0408-1#1. WHO Collaborating Centre for STD, Sydney, 2008.
21. Unemo M, Olcén P, Berglund T et al. Molecular epidemiology of Neisseria gonorrhoeae: Sequence analysis of the porB gene confirms presence of two circulating strains. J Clin Microbiol 2002; 40: 3741-9.
22. Carifo K, Catlin BW. Neisseria gonorrhoeae auxotyping: differentiation of clinical isolates based on growth responses on chemically defined media. Appl Microbiol 1973; 26: 223-30.
23. Unemo M, Sjöstrand A, Akhras M et al. Molecular characterisation of Neisseria gonorrhoeae identifies transmission and resistance of one ciprofloxacin resistant strain. APMIS 2007; 115: 231-41.
24. Limnios EA, Nguyen NL, Ray S et al. Dynamics of appearance and expansion of a prolyliminopeptidase-negative subtype among Neisseria gonorrhoeae isolates collected in Sydney, Australia, from 2002 to 2005. J Clin Microbiol 2006; 44: 1400-4.
25. Berglund T, Unemo M, Olcén P et al. One year of Neisseria gonorrhoeae isolates in Sweden: The prevalence study of antibiotic susceptibility shows relation to the geographic area of exposure. Int J STD AIDS 2002; 13: 109-14.
26. Van Dyck E, Meheus AZ, Piot P, eds. Gonorrhoea. In: Laboratory Diagnosis of Sexually Transmitted Diseases. Geneva: World Health Organization, 1999; 1-21.
27. Joesoef MR, Knapp JS, Idajadi A et al. Antimicrobial susceptibilities of Neisseria gonorrhoeae strains isolated in Surabaya, Indonesia. Antimicrob Agents Chemother 1994; 38: 2530-3.
28. Turner A, Gough KR, Leeming JP. Molecular epidemiology of tetM genes in Neisseria gonorrhoeae. Sex Transm Infect 1999; 75: 60-6.
29. Palmer HM, Leeming JP, Turner A. A multiplex polymerase chain reaction to differentiate β-lactamase plasmids of Neisseria gonorrhoeae. J Antimicrob Chemother 2000; 45: 777-82.
30. Tanaka M, Nakayama H, Huruya K et al. Analysis of mutations within multiple genes associated with resistance in a clinical isolate of Neisseria gonorrhoeae with reduced ceftriaxone susceptibility that shows a multidrug-resistant phenotype. Int J Antimicrob Agents 2006; 27: 20-6.
31. Mavroidi A, Tzouvelekis LS, Kyriakis KP et al. Multidrug-resistant strains of Neisseria gonorrhoeae in Greece. Antimicrob Agents Chemother 2001; 45: 2651-4.
32. Ropp PA, Hu M, Olesky M et al. Mutations in ponA, the gene encoding penicillin-binding protein 1, and a novel locus, penC, are required for high-level chromosomally mediated penicillin resistance in Neisseria gonorrhoeae. Antimicrob Agents Chemother 2002; 46 769-77.
33. Hellmark B, Söderquist B, Unemo M. Simultaneous species identification and detection of rifampicin resistance in staphylococci by sequencing of the rpoB gene. Eur J Clin Microbiol Infect Dis 2009; 28: 183-90.
34. Martin IMC, Ison CA, Aanensen DM et al. Rapid sequence-based identification of gonococcal transmission clusters in a large metropolitan area. J Infect Dis 2004; 189: 497-505.
35. Thulin S, Olcén P, Fredlund H et al. Total variation in the penA gene of Neisseria meningitidis: Correlation between susceptibility to β-lactam antibiotics and penA gene heterogeneity. Antimicrob Agents Chemother 2006; 50: 3317-24.
36. Unemo M, Norlén O, Fredlund H. The porA pseudogene of Neisseria gonorrhoeae - low level of genetic polymorphism and a few, mainly identical, inactivating mutations. APMIS 2005; 113: 410-9.
37. Unemo M, Palmer HM, Blackmore T et al. Global transmission of prolyliminopeptidase (PIP)-negative Neisseria gonorrhoeae strains - implications for changes in diagnostic strategies? Sex Transm Infect 2007; 83: 47-51.
38. Ito M, Deguchi T, Mizutani KS et al. Emergence and spread of Neisseria gonorrhoeae clinical isolates harboring mosaic-like structure of penicillin-binding protein 2 in Central Japan. Antimicrob Agents Chemother 2005; 49: 137-43.
39. Takahata S, Senju N, Osaki Y et al. Amino acid substitutions of mosaic penicillin-binding protein 2 associated with reduced susceptibility to cefixime in clinical isolates of Neisseria gonorrhoeae. Antimicrob Agents Chemother 2006; 50: 3638-45.
40. Osaka K, Takakura T, Narukawa K et al. Analysis of amino acid sequences of penicillin-binding protein 2 in clinical isolates of Neisseria gonorrhoeae with reduced susceptibility to cefixime and ceftriaxone. J Infect Chemother 2008; 14: 195-203.
41. Whiley DM, Limnios EA, Ray S et al. Diversity of penA alterations and subtypes in Neisseria gonorrhoeae strains from Sydney, Australia, that are less susceptible to ceftriaxone. Antimicrob Agents Chemother 2007; 51: 3111-6.
42. Daly CC, Hoffman I, Hobbs M et al. Development of an antimicrobial susceptibility surveillance system for Neisseria gonorrhoeae in Malawi: Comparison of methods. J Clin Microbiol 1997; 35: 2985-8.
43. Sutrisna A, Soebjakto O, Wignall FS et al. Increasing resistance to ciprofloxacin and other antibiotics in Neisseria gonorrhoeae from East Java and Papua, Indonesia in 2004 - implications for treatment. Int J STD AIDS 2006; 17: 810-2.
44. Livermore DM, Alexander S, Marsden B et al. Activity of ertapenem against Neisseria gonorrhoeae. J Antimicrob Chemother 2004; 54 280-1.
45. Cao V, Ratsima E, Van Tri D et al. Antimicrobial susceptibility of Neisseria gonorrhoeae strains isolated in 2004-2006 in Bangui, Central African Republic; Yaounde, Cameroon; Atananarivo, Madagascar; and Ho Chi Minh Ville and Nha Trang, Vietnam. Sex Transm Dis 2008; 31: 941-5.
46. Shafer WM, Folster JP. Towards an understanding of chromosomally mediated penicillin resistance in Neisseria gonorrhoeae: Evidence for a porin-efflux pump collaboration. J Bacteriol 2006; 188 2297-9.
47. Zarantonelli L, Borthagaray G, Lee EH et al. Decreased azithromycin susceptibility of Neisseria gonorrhoeae due to mtrR mutations. Antimicrob Agents Chemother 1999; 43: 2468-72.
48. Johnson SR, Sandul AL, Parekh M et al. Mutations causing in vitro resistance to azithromycin in Neisseria gonorrhoeae. Int J Antimicrob Agents 2003; 21: 414-9.
49. Nicholas RA, Zhao S, Tomberg J et al. Genetics of intermediate susceptibility to expanded-spectrum cephalosporins in Neisseria gonorrhoeae. 16th International Pathogenic Neisseria Conference 2008, 7-12 September 2008, Rotterdam, The Netherlands. Abstract P054, p. 133. Congress Care, IPNC, 2008.
50. Deguchi T, Yasuda M, Nakano M et al. Quinolone-resistant Neisseria gonorrhoeae: Correlation of alterations in the GyrA subunit of DNA gyrase and the ParC subunit of topoisomerase IV with antimicrobial susceptibility profiles. Antimicrob Agents Chemother 1996; 40: 1020-3.
51. Lindbäck E, Rahman M, Jalal S et al. Mutations in gyrA, gyrB, parC, and parE in quinolone-resistant strains of Neisseria gonorrhoeae. APMIS 2002; 110: 651-7.
52. Lindbäck E, Islam S, Unemo M et al. Transformation of ciprofloxacin-resistant Neisseria gonorrhoeae gyrA, parE and porB1b genes. Int J Antimicrob Agents 2006; 28: 206-11.
53. Nolte O, Müller M, Reitz S et al. Description of new mutations in the rpoB gene in rifampicin-resistant Neisseria meningitidis selected in vitro in a stepwise manner. J Med Microbiol 2003; 52: 1077-81.
54. Galimand M, Gerbaud G, Courvalin P. Spectinomycin resistance in Neisseria spp. due to mutations in 16S rRNA. Antimicrob Agents Chemother 2000; 44: 1365-6.
55. Hu M, Nandi S, Davies C et al. High-level chromosomally mediated tetracycline resistance in Neisseria gonorrhoeae results from a point mutation in the rpsJ gene encoding ribosomal protein S10 in combination with the mtrR and penB resistance determinants. Antimicrob Agents Chemother 2005; 49: 4327-34.
56. Ng L-K, Martin I, Liu G et al. Mutation in 23S rRNA associated with macrolide resistance in Neisseria gonorrhoeae. Antimicrob Agents Chemother 2002; 46: 3020-5.
57. Cousin SL Jr, Whittington WL, Roberts MC. Acquired macrolide resistance genes and the 1 bp deletion in the mtrR promoter in Neisseria gonorrhoeae. J Antimicrob Chemother 2003; 51: 131-3.