Molecular analysis of antimicrobial resistance mechanisms in Neisseria gonorrhoeae isolates from Ontario, Canada

Antimicrobial Agents and Chemotherapy

Volumn 55, Issue 2, 2011, Pages 703-712

  Allen, Vanessa G ^a,b   Farrell, David J ^a,b   Rebbapragada, Anuradha ^a,b   Tan, Jingyuan ^a   Tijet, Nathalie ^a   Perusini, Stephen J ^a   Towns, Lynn ^a   Lo, Stephen ^a   Low, Donald E ^a,b,c   Melano, Roberto G ^a,b,c  

^a PUBLIC HEALTH ONTARIO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c MOUNT SINAI HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AZITHROMYCIN; BACTERIAL PROTEIN; CEFTRIAXONE; CIPROFLOXACIN; ERYTHROMYCIN; MULTIDRUG RESISTANCE PROTEIN; PENICILLIN G; RIBOSOME PROTEIN; SPECTINOMYCIN; TETRACYCLINE;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL GENETICS; BACTERIAL STRAIN; BACTERIUM ISOLATE; CANADA; CLINICAL ASSESSMENT; GENE MUTATION; GENETIC ANALYSIS; MULTIDRUG RESISTANCE; NEISSERIA GONORRHOEAE; NONHUMAN; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; CEFIXIME; CEFTRIAXONE; CEPHALOSPORINS; DNA, BACTERIAL; DRUG RESISTANCE, BACTERIAL; GONORRHEA; HUMANS; MICROBIAL SENSITIVITY TESTS; MOLECULAR SEQUENCE DATA; NEISSERIA GONORRHOEAE; ONTARIO; PENICILLIN-BINDING PROTEINS; POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA;

EID: 78751680159     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00788-10     Document Type: Article

References (62)

1. Akasaka, S., et al. 2001. Emergence of cephems and aztreonam high-resistant Neisseria gonorrhoeae that does not produce β-lactamase. J. Infect. Chemother. 7:49-50.
2. Alcalá, B., et al. 2003. Molecular characterization of ciprofloxacin resistance of gonococcal strains in Spain. Sex. Transm. Dis. 30:395-398.
3. Ameyama, S., et al. 2002. Mosaic-like structure of penicillin binding protein 2 gene (penA) in clinical isolates of Neisseria gonorrhoeae with reduced susceptibility to cefixime. Antimicrob. Agents Chemother. 46:3744-3749.
4. Bala, M., K. Ray, and S. Kumari. 2003. Alarming increase in ciprofloxacin and penicillin-resistant Neisseria gonorrhoeae isolates in New Delhi, India. Sex. Transm. Dis. 30:523-525.
5. Belland, R. J., S. G. Morrison, C. Ison, and W. M. Huang. 1994. Neisseria gonorrhoeae acquires mutations in analogous regions of gyrA and parC in fluoroquinolone-resistant isolates. Mol. Microbiol. 14:371-380.
6. Centers for Disease Control and Prevention. 2006. Update to CDC's sexually transmitted diseases guidelines, 2006. MMWR Morb. Mortal. Wkly. Rep. 55:1-94. http://www.cdc.gov/std/treatment/2006/rr5511.pdf.
7. Centers for Disease Control and Prevention. 2007. Update to CDC's sexually transmitted diseases treatment guidelines, 2006: fluoroquinolones no longer recommended for treatment of gonococcal infections. MMWR Morb. Mortal. Wkly. Rep. 56:332-336. http://www.cdc.gov/std/treatment/2006/GonUpdateApril2007. pdf.
8. Chen, P., et al. 2008. High prevalence of mutations in the quinolone resistance-determining region and Mtrr loci in Neisseria gonorrhoeae isolated in a tertiary hospital in Southern Taiwan, abstr. C2-3905. Abstr. 48th Intersci. Conf. Antimicrob. Agents Chemother. American Society for Microbiology, Washington, DC.
9. Chisholm, S. A., et al. 2009. Emergence of high-level azithromycin resistance in Neisseria gonorrhoeae in England and Wales. J. Antimicrob. Chemother. 64:353-358.
10. Clinical and Laboratory Standards Institute. 2008. Performance standards for antimicrobial susceptibility testing, 18th informational supplement. CLSI document M100-S18. Clinical and Laboratory Standards Institute, Wayne, PA.
11. Cousin, S., Jr., W. L. H. Whittington, and M. C. Roberts. 2003. Acquired macrolide resistance genes in pathogenic Neisseria spp. isolated between 1940 and 1987. Antimicrob. Agents Chemother. 47:3877-3880.
12. Cousin, S., Jr., W. L. H. Whittington, and M. C. Roberts. 2003. Acquired macrolide resistance genes and the 1 bp deletion in the mtrR promoter in Neisseria gonorrhoeae. J. Antimicrob. Chemother. 51:131-133.
13. Dan, M., F. Poch, and B. Sheinberg. 2002. High prevalence of high-level ciprofloxacin resistance in Neisseria gonorrhoeae in Tel Aviv, Israel: correlation with response to therapy. Antimicrob. Agents Chemother. 46:1671-1673.
14. Dillon, J. A., et al. 2001. Reduced susceptibility to azithromycin and high percentages of penicillin and tetracycline resistance in Neisseria gonorrhoeae isolates from Manaus, Brazil, 1998. Sex. Transm. Dis. 28:521-526.
15. European Committee on Antimicrobial Susceptibility Testing. 2009. EUCAST clinical MIC breakpoints - macrolides (v1.4). http://www.srga.org/eucastwt/ MICTAB/MICmacrolides.html.
16. Farrell, D. J., et al. 2003. Macrolide resistance by ribosomal mutation in clinical isolates of Streptococcus pneumoniae from the PROTEKT 1999-2000 study. Antimicrob. Agents Chemother. 47:1777-1783.
17. Farrell, D. J., J. Shackcloth, K. A. Barbadora, and M. D. Green. 2006. Streptococcus pyogenes isolates with high-level macrolide resistance and reduced susceptibility to telithromycin associated with 23S rRNA mutations. Antimicrob. Agents Chemother. 50:817-818.
18. Galarza, P. G., et al. 2009. Emergence of high level azithromycin- resistant Neisseria gonorrhoeae strain isolated in Argentina. Sex. Transm. Dis. 36:787-788.
19. Galarza, P. G., et al. 2010. New mutation in 23S rRNA gene associated with high level of azithromycin resistance in Neisseria gonorrhoeae. Antimicrob. Agents Chemother. 54:1652-1653.
20. Galimand, M., G. Gerbaud, and P. Courvalin. 2000. Spectinomycin resistance in Neisseria spp. due to mutations in 16S rRNA. Antimicrob. Agents Chemother. 44:1365-1366.
21. Gill, M. J., et al. 1998. Gonococcal resistance to beta-lactams and tetracycline involves mutation in loop 3 of the porin encoded at the penB locus. Antimicrob. Agents Chemother. 42:2799-2803.
22. Hu, M., S. Nandi, C. Davies, and R. A. Nicholas. 2005. 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. 49:4327-4334.
23. Ilina, E. N., et al. 2008. Relation between genetic markers of drug resistance and susceptibility profile of clinical Neisseria gonorrhoeae strains. Antimicrob. Agents Chemother. 52:2175-2182.
24. Ito, M., et al. 2004. Remarkable increase in central Japan in 2001-2002 of Neisseria gonorrhoeae isolates with decreased susceptibility to penicillin, tetracycline, oral cephalosporins, and fluoroquinolones. Antimicrob. Agents Chemother. 48:3185-3187.
25. Ito, M., et al. 2005. Emergence and spread of Neisseria gonorrhoeae clinical isolates harboring mosaic-like structure of penicillin-binding protein 2 in central Japan. Antimicrob. Agents Chemother. 49:137-143.
26. Lee, S. G., et al. 2010. Various penA mutations together with mtrR, porB and ponA mutations in Neisseria gonorrhoeae isolates with reduced susceptibility to cefixime or ceftriaxone. J. Antimicrob. Chemother. 65:669-675.
27. Lindberg, R., H. Fredlund, R. Nicholas, and M. Unemo. 2007. Neisseria gonorrhoeae isolates with reduced susceptibility to cefixime and ceftriaxone: association with genetic polymorphisms in penA, mtrR, porB1b, and ponA. Antimicrob. Agents Chemother. 51:2117-2122.
28. Lo, J. Y., et al. 2008. Ceftibuten resistance and treatment failure of Neisseria gonorrhoeae infection. Antimicrob. Agents Chemother. 52:3564-3567.
29. Lucas, C. E., J. T. Balthazar, K. E. Hagman, and W. M. Shafer. 1997. The MtrR repressor binds the DNA sequence between the mtrR and mtrC genes of Neisseria gonorrhoeae. J. Bacteriol. 179:4123-4128.
30. Luna, V. A., S. Cousin, Jr., W. L. Whittington, and M. C. Roberts. 2000. Identification of the conjugative mef gene in clinical Acinetobacter junii and Neisseria gonorrhoeae isolates. Antimicrob. Agents Chemother. 44:2503-2506.
31. Martin, I. M., C. A. Ison, D. M. Aanensen, K. A. Fenton, and B. G. Spratt. 2004. Rapid sequence-based identification of gonococcal transmission clusters in a large metropolitan area. J. Infect. Dis. 189:1497-1505.
32. McLean, C. A., et al. 2004. The emergence of Neisseria gonorrhoeae with decreased susceptibility to azithromycin in Kansas City, Missouri, 1999 to 2000. Sex. Transm. Dis. 31:73-78.
33. Morse, S. A., S. R. Johnson, J. W. Biddle, and M. C. Roberts. 1986. High-level tetracycline resistance in Neisseria gonorrhoeae is the result of acquisition of streptococcal tetM determinant. Antimicrob. Agents Chemother. 30:664-670.
34. Ng, L. K., I. Martin, G. Liu, and L. Bryden. 2002. Mutations in 23S rRNA associated with macrolide resistance in Neisseria gonorrhoeae. Antimicrob. Agents Chemother. 46:3020-3025.
35. Ohnishi, M., et al. 2010. Spread of a chromosomal cefixime-resistant penA gene among different Neisseria gonorrhoeae lineages. Antimicrob. Agents Chemother. 54:1060-1067.
36. Olesky, M., M. Hobbs, and R. A. Nicholas. 2002. Identification and analysis of amino acid mutations in porin IB that mediate intermediate-level resistance to penicillin and tetracycline in Neisseria gonorrhoeae. Antimicrob. Agents Chemother. 46:2811-2820.
37. Olesky, M., R. L. Rosenberg, and R. A. Nicholas. 2006. Porin-mediated antibiotic resistance in Neisseria gonorrhoeae: ion, solute, and antibiotic permeation through PIB proteins with penB mutations. J. Bacteriol. 188:2300-2308.
38. Ota, K. V., et al. 2009. Prevalence of and risk factors for quinolone-resistant Neisseria gonorrhoeae infection in Ontario. CMAJ 180:287-290.
39. Pandori, M., et al. 2009. Mosaic penicillin-binding protein 2 in Neisseria gonorrhoeae isolates collected in 2008 in San Francisco, California. Antimicrob. Agents Chemother. 53:4032-4034.
40. Palmer, H. M., H. Young, A. Winter, and J. Dave. 2008. Emergence and spread of azithromycin-resistant Neisseria gonorrhoeae in Scotland. J. Antimicrob. Chemother. 624:490-494.
41. Public Health Agency of Canada. 2008. Reported cases of notifiable STI from January 1 to December 31, 2007 and January 1 to December 31, 2008 and corresponding rates for 2007 and 2008. The Agency, Ottawa, Canada. http://origin.qa.phac-aspc.gc.ca/std-mts/stdcases-casmts/cases-cas-08-eng.php.
42. Public Health Agency of Canada. 2008. Gonococcal infections. The Agency, Ottawa, Canada. http://www.phac-aspc.gc.ca/std-mts/sti-2006/pdf/506-Gonococcal- Infections.pdf.
43. Roberts, M. C., et al. 1999. Erythromycin-resistant Neisseria gonorrhoeae and oral commensal Neisseria spp. carry known rRNA methylase genes. Antimicrob. Agents Chemother. 43:1367-1372.
44. Ropp, P. A., M. Hu, M. Olesky, and R. A. Nicholas. 2002. 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. 46:769-777.
45. Shafer, W. M., et al. 2001. Genetic organization and regulation of antimicrobial efflux systems possessed by Neisseria gonorrhoeae and Neisseria meningitidis. J. Mol. Microbiol. Biotechnol. 3:219-224.
46. Starnino, S., and P. Stefanelli on behalf of the Neisseria gonorrhoeae Italian Study Group. 2009. Azithromycin-resistant Neisseria gonorrhoeae strains recently isolated in Italy. J. Antimicrob. Chemother. 63:1200-1204.
47. Sutcliffe, J., T. Grebe, A. Tait-Kamradt, and L. Wondrack. 1996. Detection of erythromycin-resistant determinants by PCR. Antimicrob. Agents Chemother. 40:2562-2566.
48. Takahata, S., N. Senju, Y. Osaki, T. Yoshida, and T. Ida. 2006. Amino acid substitutions in mosaic penicillin-binding protein 2 associated with reduced susceptibility to cefixime in clinical isolates of Neisseria gonorrhoeae. Antimicrob. Agents Chemother. 50:3638-3645.
49. Tanaka, M., et al. 1998. Analysis of quinolone resistance mechanisms in Neisseria gonorrhoeae isolates in vitro. Sex. Transm. Dis. 74:59-62.
50. Tapsall, J. W. 2009. Neisseria gonorrhoeae and emerging resistance to extended spectrum cephalosporins. Curr. Opin. Infect. Dis. 22:87-91.
51. Trees, D. L., et al. 1999. Alterations within the quinolone resistance-determining regions of GyrA and ParC of Neisseria gonorrhoeae isolated in the Far East and the United States. Int. J. Antimicrob. Agents 12:325-332.
52. Unemo, M., O. Fasth, H. Fredlund, A. Limnios, and J. Tapsall. 2009. 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. 63:1142-1151.
53. Wang, G. E., and D. E. Taylor. 1998. Site-specific mutations in the 23S rRNA gene of Helicobacter pylori confer two types of resistance to macrolidelincosamide-streptogramin B antibiotics. Antimicrob. Agents Chemother. 42:1952-1958.
54. Wang, S. A., et al. 2003. Multidrug-resistant Neisseria gonorrhoeae with decreased susceptibility to cefixime - Hawaii, 2001. Clin. Infect. Dis. 15:849-852.
55. Warner, D. M., W. M. Shafer, and A. E. Jerse. 2008. Clinically relevant mutations that cause derepression of the Neisseria gonorrhoeae MtrC-MtrD-MtrE efflux pump system confer different levels of antimicrobial resistance and in vivo fitness. Mol. Microbiol. 70:462-478.
56. Whiley, D. M., E. A. Limnios, S. Ray, T. P. Sloots, and J. W. Tapsall. 2007. Diversity of penA alterations and subtypes in Neisseria gonorrhoeae strains from Sydney, Australia, that are less susceptible to ceftriaxone. Antimicrob. Agents Chemother. 51:3111-3116.
57. World Health Organization. 2003. Surveillance of antibiotic resistance in Neisseria gonorrhoeae in the WHO Western Pacific Region, 2002. Commun. Dis. Intell. 27:488-491.
58. World Health Organization. 2004. Increases in fluoroquinolone-resistant Neisseria gonorrhoeae among men who have sex with men - United States, 2003, and revised recommendations for gonorrhea treatment. MMWR Morb. Mortal. Wkly. Rep. 53:335-338.
59. Yokoi, S., et al. 2007. Threat to cefixime treatment for gonorrhea. Emerg. Infect. Dis. 13:1275-1277.
60. Zarantonelli, L., G. Borthagaray, E. Lee, and W. M. Shafer. 1999. Decreased azithromycin susceptibility of Neisseria gonorrhoeae due to mtrR mutations. Antimicrob. Agents Chemother. 43:2468-2472.
61. Zhao, S., D. M. Tabiason, M. Hu, H. S. Seifert, and R. A. Nicholas. 2005. The penC mutation conferring antibiotic resistance in Neisseria gonorrhoeae arises from a mutation in the PilQ secretin that interferes with multimer stability. Mol. Microbiol. 57:1238-1251.
62. Zhao, S., et al. 2009. Genetics of chromosomally mediated intermediate resistance to ceftriaxone and cefixime in Neisseria gonorrhoeae. Antimicrob. Agents Chemother. 53:3744-3751.