Review and international recommendation of methods for typing neisseria gonorrhoeae isolates and their implications for improved knowledge of gonococcal epidemiology, treatment, and biology

Clinical Microbiology Reviews

Volumn 24, Issue 3, 2011, Pages 447-458

  Unemo, Magnus ^a   Dillon, Jo Anne R ^b  

^a ÖREBRO UNIVERSITY HOSPITAL   (Sweden)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL RNA; PLASMID DNA; RIBOSOME RNA; TRANSFERRIN;

ANTIBIOTIC SENSITIVITY; ARTICLE; AUXOTYPING; BACTERIAL GENE; BACTERIAL GENETICS; BACTERIUM EXAMINATION; BACTERIUM ISOLATION; DNA SEQUENCE; GENE LOCUS; GONORRHEA; MICROBIAL DIVERSITY; MOLECULAR EPIDEMIOLOGY; MOLECULAR EVOLUTION; MULTILOCUS SEQUENCE TYPING; NEISSERIA GONORRHOEAE; NEISSERIA GONORRHOEAE MULTIANTIGEN SEQUENCE TYPING; NONHUMAN; OPA TYPING; PHENOTYPE; POLYMERASE CHAIN REACTION; PORB GENE; PULSED FIELD GEL ELECTROPHORESIS; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; RIBOTYPING; SEROTYPE;

BACTERIAL TYPING TECHNIQUES; DNA, BACTERIAL; GONORRHEA; HUMANS; MULTILOCUS SEQUENCE TYPING; NEISSERIA GONORRHOEAE;

NEISSERIA GONORRHOEAE;

EID: 79960146321     PISSN: 08938512     EISSN: 10986618     Source Type: Journal    
DOI: 10.1128/CMR.00040-10     Document Type: Article

References (201)

1. Abu-Rajab, K., et al. 2009. To what extent does Neisseria gonorrhoeae multiantigen sequence typing of gonococcal isolates support information derived from patient interviews? Int. J. STD AIDS 20:414-417.
2. Achtman, M., et al. 1999. Yersinia pestis, the cause of the plague, is a recently emerged clone of Yersinia pseudotuberculosis. Proc. Natl. Acad. Sci. U. S. A. 96:14043-14048.
3. Azariah, S., and N. Perkins. 2007. Risk factors and characteristics of patients with gonorrhoea presenting to Auckland Sexual Health Service, New Zealand. N. Z. Med. J. 120:U2491.
4. Baehr, W., E. C. Gotschlich, and P. J. Hitchcock. 1989. The virulence associated gonococcal H.8 gene encodes 14 tandemly repeated pentapeptides. Mol. Microbiol. 3:49-55.
5. Barry, P. M., and J. D. Klausner. 2009. The use of cephalosporins for gonorrhea: the impending problem of resistance. Expert Opin. Pharmacother. 10:555-577.
6. Bash, M. C., et al. 2005. por variable-region typing by DNA probe hybridization is broadly applicable to epidemiologic studies of Neisseria gonorrhoeae. J. Clin. Microbiol. 43:1522-1530.
7. Bennett, J. S., et al. 2007. Species status of Neisseria gonorrhoeae: evolutionary and epidemiological inferences from multilocus sequence typing. BMC. Biol. 5:35.
8. Bilek, N., C. A. Ison, and B. G. Spratt. 2009. Relative contributions of recombination and mutation to the diversification of the opa gene repertoire of Neisseria gonorrhoeae. J. Bacteriol. 191:1878-1890.
9. Bilek, N., et al. 2007. Concordance between Neisseria gonorrhoeae genotypes recovered from known sexual contacts. J. Clin. Microbiol. 45:3564-3567.
10. Booth, S. A., M. A. Drebot, I. E. Martin, and L. K. Ng. 2003. Design of oligonucleotide arrays to detect point mutations: molecular typing of antibiotic resistant strains of Neisseria gonorrhoeae and hantavirus infected deer mice. Mol. Cell Probes 17:77-84.
11. Brunham, R. C., F. A. Plummer, and R. S. Stephens. 1993. Bacterial antigenic variation, host immune response, and pathogen-host coevolution. Infect. Immun. 61:2273-2276.
12. Butt, N. J., M. Virji, F. Vayreda, P. R. Lambden, and J. E. Heckels. 1990. Gonococcal outer-membrane protein PIB: comparative sequence analysis and localization of epitopes which are recognized by type-specific and cross-reacting monoclonal antibodies. J. Gen. Microbiol. 136:2165-2172.
13. Buvé, A., C. Gourbin, and M. Laga. 2008. Gender perspectives and sexually transmitted diseases, p. 151-164. In K. K. Holmes, P. F. Sparling, W. E. Stamm, P. Piot, J. N. Wasserheit, L. Corey, M. S. Cohen, and D. H. Watts (ed.), Sexually transmitted diseases, 4th ed. McGraw-Hill, New York, NY.
14. Camarena, J. J., et al. 1995. DNA amplification fingerprinting for subtyping Neisseria gonorrhoeae strains. Sex. Transm. Dis. 22:128-136.
15. Carballo, M., and J. R. Dillon. 1992. Evaluation of an enzyme immunoassay and a modified coagglutination assay for typing gonococcal isolates with monoclonal antibodies. Sex. Transm. Dis. 19:219-224.
16. Carballo, M., L.-K. Ng, and J. R. Dillon. 1994. Detection of the tetM determinant in Neisseria gonorrhoeae using a non-radioactively labeled oligonucleotide probe. Mol. Cell Probes 8:205-208.
17. Carifo, K., and B. W. Catlin. 1973. Neisseria gonorrhoeae auxotyping: ifferentiation of clinical isolates based on growth responses on chemically defined media. Appl. Microbiol. 26:223-230.
18. Catlin, B. W. 1973. Nutritional profiles of Neisseria gonorrhoeae, Neisseria meningitidis and Neisseria lactamica in chemical defined media and the use of growth requirements for gonococcal typing. J. Infect. Dis. 128:178-194.
19. Chen, H., et al. 2008. Typing of Neisseria gonorrhoeae Opa and NG-MAST gene of 12 pairs of sexual contact gonorrhea patients in China. J. Huazhong Univ. Sci. Technolog. Med. Sci. 28:472-475.
20. Chen, Q., et al. 2007. Opa typing of Neisseria gonorrhoeae strains isolated from patients attending sexually transmitted disease clinics in China. Sex. Transm. Dis. 34:967-973.
21. 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.
22. Choudhury, B., et al. 2006. Identification of individuals with gonorrhoea within sexual networks: a population-based study. Lancet 368:139-146.
23. Chow, V. T. K., Q. C. Lau, and C. L. Poh. 1994. Mapping of serovar-specific monoclonal antibody epitopes by DNA and amino acid sequence analysis of Neisseria gonorrhoeae outer membrane protein IB strains. Immun. Infect. Dis. 4:202-206.
24. Cooke, S. J., H. de la Paz, C. L. Poh, C. A. Ison, and J. E. Heckels. 1997. Variation within serovars of Neisseria gonorrhoeae detected by structural analysis of outer-membrane protein PIB and by pulsed-field gel electrophoresis. Microbiology 143:1415-1422.
25. Cooke, S. J., K. Jolley, C. A. Ison, H. Young, and J. E. Heckels. 1998. Naturally occurring isolates of Neisseria gonorrhoeae; which display anomalous serovar properties, express PIA/PIB hybrid porins, deletions in PIB or novel PIA molecules. FEMS. Microbiol. Lett. 162:75-82.
26. Corkill, J. E., et al. 2003. Molecular epidemiology of endemic ciprofloxacinresistant Neisseria gonorrhoeae in Liverpool. Int. J. STD AIDS 14:379-385.
27. De Jongh, M., Y. Dangor, C. A. Ison, and A. A. Hoosen. 2008. Neisseria gonorrhoeae multi-antigen sequence typing (NG-MAST) of ciprofloxacin resistant isolates of Pretoria, South Africa. J. Clin. Pathol. 61:686-687.
28. De la Fuente, L., and J. A. Vazquez. 1992. Analysis of genetic variability of penicillinase non-producing Neisseria gonorrhoeae strains with different levels of susceptibility to penicillin. J. Med. Microbiol. 37:96-99.
29. De la Fuente, L., and J. A. Vazquez. 1991. Multilocus enzyme analysis of African type penicillinase producing Neisseria gonorrhoeae (PPNG) strains isolated in Spain. Sex. Transm. Dis. 18:150-152.
30. De Mattia, A., et al. 2006. The use of combination subtyping in the forensic evaluation of a three-year-old girl with gonorrhea. Pediatr. Infect. Dis. J. 25:461-463.
31. Dillon, J. R. 1994. Molecular epidemiology of antibiotic resistant Neisseria gonorrhoeae. Ann. Inst. Pasteur Actual. 5:148-156.
32. Dillon, J. R., and F. Pagotto. 1999. Importance of drug resistance in gonococci: from mechanisms to monitoring. Curr. Opin. Infect. Dis. 12:35-40.
33. Dillon, J. R., and K.-H. Yeung. 1989. Beta-lactamase plasmids and chromosomally mediated antibiotic resistance in pathogenic Neisseria species. Clin. Microbiol. Rev. 2:S125-S133.
34. Dillon, J. R., and M. Carballo. 1990. Molecular epidemiology and novel auxotype/serovar/plasmid content combinations in tetracycline-resistant Neisseria gonorrhoeae (TRNG) isolated in Canada. Can. J. Microbiol. 36: 64-67.
35. Dillon, J. R., and M. Pauzé. 1981. Relationship between plasmid content and auxotype in Neisseria gonorrhoeae isolates. Infect. Immun. 33:625-628.
36. Dillon, J. R., H. Li, K. Yeung, and T. A. Aman. 1999. A PCR assay for discriminating Neisseria gonorrhoeae β-lactamase-producing plasmids. Mol. Cell Probes 13:89-92.
37. Dillon, J. R., M. Carballo, S. D. King, and A. R. Brathwaite. 1987. Auxotype, plasmid content and serovars of gonococcal isolates (PPNG and non-PPNG) from Jamaica. Genitourin. Med. 63:233-238.
38. Dillon, J. R., M. Pauzé, and A. G. Jessamine. 1981. Epidemiology and biology of penicillinase-producing Neisseria gonorrhoeae isolated in Canada (1976 to September 1980). Can. Med. Assoc. J. 125:851-855.
39. Dillon, J. R., M. Pauzé, and K.-H. Yeung. 1986. Molecular and epidemiological analysis of penicillinase producing strains of Neisseria gonorrhoeae isolated in Canada 1976-84: evolution of new auxotypes and beta-lactamase encoding plasmids. Genitourin. Med. 62:151-157.
40. + phenotype. Lancet i:103-104.
41. Dillon, J. R., M. Rahman, and K.-H. Yeung. 1993. Discriminatory power of typing schemes based on Simpsons's index of diversity for Neisseria gonorrhoeae. J. Clin. Microbiol. 31:2831-2833.
42. Dillon, J. R., P. Duck, and D. Y. Thomas. 1981. Molecular and phenotypic characterization of penicillinase-producing Neisseria gonorrhoeae from Canadian sources. Antimicrob. Agents Chemother. 19:952-957.
43. Dillon, J. R., S. Bygdeman, and E. Sandström. 1987. Serological ecology of Neisseria gonorrhoeae (PPNG and non-PPNG) isolated in Canada. Genitourin. Med. 63:160-168.
44. Dunning Hotopp, J. C., et al. 2006. Comparative genomics of Neisseria meningitidis: core genome, islands of horizontal transfer and pathogenspecific genes. Microbiology 152:3733-3749.
45. Enright, M. C., and B. G. Spratt. 1999. Multilocus sequence typing. Trends Microbiol. 7:482-487.
46. Falk, E. S., et al. 1984. Restriction endonuclease fingerprinting of chromosomal DNA of Neisseria gonorrhoeae. Acta Pathol. Microbiol. Immunol. Scand. B 92:271-278.
47. Falk, E. S., et al. 1988. Genotypes and phenotypes of beta-lactamase producing strains of Neisseria gonorrhoeae from African countries. Genitourin. Med. 64:226-232.
48. Fernandez Cobo, M., et al. 1999. Characterization of an outbreak of tetMcontaining Neisseria gonorrhoeae in Argentina. Int. J. STD AIDS 10:169-173.
49. Fernando, I., H. M. Palmer, and H. Young. 2009. Characteristics of patients infected with common Neisseria gonorrhoeae NG-MAST sequence type strains presenting at the Edinburgh genitourinary medicine clinic. Sex. Transm. Infect. 85:443-446.
50. Fjeldsøe-Nielsen, H., et al. 2005. Phenotypic and genotypic characterization of prolyliminopeptidase-negative Neisseria gonorrhoeae isolates in Denmark. Eur. J. Clin. Microbiol. Infect. Dis. 24:280-283.
51. Florindo, C., et al. 2010. Genotypes and antimicrobial-resistant phenotypes of Neisseria gonorrhoeae in Portugal (2004-2009). Sex. Transm. Infect. 86: 449-453.
52. Fredlund, H., L. Falk, M. Jurstrand, and M. Unemo. 2004. Molecular genetic methods for diagnosis and characterisation of Chlamydia trachomatis and Neisseria gonorrhoeae: impact on epidemiological surveillance and interventions. APMIS 112:771-784.
53. Fudyk, T. C., et al. 1999. Genetic diversity and mosaicism at the por locus of Neisseria gonorrhoeae. J. Bacteriol. 181:5591-5599.
54. Galarza, P. G., et al. 2009. Emergence of high level azithromycin-resistant Neisseria gonorrhoeae strain isolated in Argentina. Sex. Transm. Dis. 36:787-788.
55. Galvin, S. R., and M. S. Cohen. 2004. The role of sexually transmitted diseases in HIV transmission. Nat. Rev. Microbiol. 2:33-42.
56. Garvin, L. E., et al. 2008. Phenotypic and genotypic analyses of Neisseria gonorrhoeae isolates that express frequently recovered PorB PIA variable region types suggest that certain P1a porin sequences confer a selective advantage for urogenital tract infection. Infect. Immun. 76:3700-3709.
57. Gascoyne-Binzi, D. M., J. Heritage, and P. M. Hawkey. 1993. Nucleotide sequences of the tet(M) genes from the American and Dutch type tetracycline resistance plasmids of Neisseria gonorrhoeae. J. Antimicrob. Chemother. 32:667-676.
58. Giles, J. A., et al. 2004. Quinolone resistance-determining region mutations and por type of Neisseria gonorrhoeae isolates: resistance surveillance and typing by molecular methodologies. J. Infect. Dis. 189:2085-2093.
59. Gill, M. J. 1991. Serotyping Neisseria gonorrhoeae: a report of the Fourth International Workshop. Genitourin. Med. 67:53-57.
60. Golparian, D., B. Hellmark, H. Fredlund, and M. Unemo. 2010. Emergence, spread and characteristics of Neisseria gonorrhoeae isolates with in vitro decreased susceptibility and resistance to extended-spectrum cephalosporins in Sweden. Sex. Transm. Infect. 86:454-460.
61. Greco, V., L.-K. Ng, R. Catana, H. Li, and J. R. Dillon. 2003. Molecular epidemiology of Neisseria gonorrhoeae isolates with tetracycline resistance in Canada: temporal and geographical trends and prevalence from 1986 to 1997. Microb. Drug Resist. 9:353-360.
62. Gürtler, V., and V. A. Stanisich. 1996. New approaches to typing and identification of bacteria using the 16S-23S rDNA spacer region. Microbiology 142:3-16.
63. Gutjahr, T. S., M. O'Rourke, C. A. Ison, and B. G. Spratt. 1997. Arginine-, hypoxanthine-, uracil-requiring isolates of Neisseria gonorrhoeae are a clonal lineage with a non-clonal population. Microbiology 143:633-640.
64. Harris, S. R., et al. 2010. Evolution of MRSA during hospital transmission and intercontinental spread. Science 327:469-474.
65. Hendry, A. T., and I. O. Stewart. 1979. Auxanographic grouping and typing of Neisseria gonorrhoeae. Can. J. Microbiol. 25:512-521.
66. Heymans, R., L. M. Schouls, H. G. van der Heide, M. F. van der Loeff, and S. M. Bruisten. 2011. Multiple-locus variable-number tandem repeat analysis of Neisseria gonorrhoeae. J. Clin. Microbiol. 49:354-363.
67. Hobbs, M. M., et al. 1999. Molecular typing of Neisseria gonorrhoeae causing repeated infections: evolution of porin during passage within a community. J. Infect. Dis. 179:371-381.
68. Hook, E. W., and H. H. Handsfield. 2008. Gonococcal infections in the adult, p. 627-646. In K. K. Holmes, P. F. Sparling, W. E. Stamm, P. Piot, J. N. Wasserheit, L. Corey, M. S. Cohen, and D. H. Watts (ed.), Sexually transmitted diseases, 4th ed. McGraw-Hill, New York, NY.
69. Reference deleted.
70. Hunter, P. R., and M. A. Gaston. 1988. Numerical index of the discriminatory ability of typing systems: an application of Simpson's index of diversity. J. Clin. Microbiol. 26:2465-2466.
71. Ilina, E. N., N. Y. Oparina, E. A. Shitikov, A. D. Borovskaya, and V. M. Govorun. 2010. Molecular surveillance of clinical Neisseria gonorrhoeae isolates in Russia. J. Clin. Microbiol. 48:3681-3689.
72. Ison, C. A., L. Whitaker, and A. Renton. 1992. Concordance of auxotype/serovar classes of Neisseria gonorrhoeae between sexual contacts. Epidemiol. Infect. 109:265-271.
73. Ison, C. A., et al. 2003. International comparison of molecular typing methods for Neisseria gonorrhoeae, abstr. 364. Abstr. 15th Int. Soc. Sex. Transm. Dis. Res. Congr., Ottawa, Canada.
74. Ison, C. A., J. R. Dillon, and J. W. Tapsall. 1998. The epidemiology of global antibiotic resistance among Neisseria gonorrhoeae and Haemophilus ducreyi. Lancet 351(Suppl. III):8-11.
75. Johansson, E., H. Fredlund, and M. Unemo. 2009. Prevalence, phenotypic and genetic characteristics of prolyliminopeptidase-negative Neisseria gonorrhoeae isolates in Sweden during 2000-2007. APMIS 117:900-904.
76. Khaki, P., et al. 2009. Molecular typing of Neisseria gonorrhoeae isolates by Opa-typing and ribotyping in New Delhi, India. Int. J. Microbiol. 2009: 934823.
77. Kidgell, C., et al. 2002. Salmonella typhi, the causative agent of typhoid fever, is approximately 50,000 years old. Infect. Genet. Evol. 2:39-45.
78. Knapp, J. S., M. R. Tam, R. C. Nowinski, K. K. Holmes, and E. G. Sandström. 1984. Serological classification of Neisseria gonorrhoeae with use of monoclonal antibodies to gonococcal outer membrane protein I. J. Infect. Dis. 150:44-48.
79. Komolafe, A. J., H. Sugunendran, and J. E. Corkill. 2004. Gonorrhoea: test of cure for sensitive bacteria? Use of genotyping to disprove treatment failure. Int. J. STD AIDS 15:212.
80. Lawung, R., et al. 2010. Antibiograms and randomly amplified polymorphic DNA-polymerase chain reactions (RAPD-PCR) as epidemiological markers of gonorrhea. J. Clin. Lab. Anal. 24:31-37.
81. 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.
82. Li, H., and J. R. Dillon. 1995. Utility of ribotyping, restriction endonuclease analysis and pulsed field gel electrophoresis to discriminate between isolates of Neisseria gonorrhoeae of serovar 1A-2 which require arginine, hypoxanthine and uracil for growth. J. Med. Microbiol. 43:208-215.
83. Liao, M., et al. 2008. Clusters of circulating Neisseria gonorrhoeae strains and association with antimicrobial resistance in Shanghai. J. Antimicrob. Chemother. 61:478-487.
84. Liao, M., H. Li, K. Bell, N. F. Eng, and J. R. Dillon. 2005. Comparison of ribotyping, pulse field gel electrophoresis and genetic typing to discriminate gonococcal strains associated with either outbreak clusters or random isolates with IB-5 and IB-7, abstr. WP-005. Abstr. 16th Biennial Meet. Int. Soc. Sex. Transm. Dis. Res., Amsterdam, Netherlands.
85. Liao, M., et al. 2009. Comparison of Neisseria gonorrhoeae multiantigen sequence typing and porB sequence analysis for identification of clusters of N. gonorrhoeae isolates. J. Clin. Microbiol. 47:489-491.
86. 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.
87. Ling, A. E., et al. 2007. Evaluation of PorB variable region typing of Neisseria gonorrhoeae using PCR-ELISA in samples collected from men who have sex with men. J. Clin. Lab. Anal. 21:237-243.
88. Lo, J. Y., et al. 2008. Ceftibuten resistance and treatment failure of Neisseria gonorrhoeae infection. Antimicrob. Agents Chemother. 52:3564-3567.
89. Lundbäck, D., H. Fredlund, T. Berglund, B. Wretlind, and M. Unemo. 2006. Molecular epidemiology of Neisseria gonorrhoeae-identification of the first presumed Swedish transmission chain of an azithromycin-resistant strain. APMIS 114:67-71.
90. Lynn, F., et al. 2005. Genetic typing of the porin protein of Neisseria gonorrhoeae from clinical noncultured samples for strain characterization and identification of mixed gonococcal infections. J. Clin. Microbiol. 43:368-375.
91. Maiden, M. C., et al. 1998. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc. Natl. Acad. Sci. U. S. A. 95:3140-3145.
92. Margos, G., et al. 2008. MLST of housekeeping genes captures geographic population structure and suggests a European origin of Borrelia burgdorferi. Proc. Natl. Acad. Sci. U. S. A. 105:8730-8735.
93. Márquez, C., J. R. Dillon, V. Rodríguez, and G. Borthagaray. 2002. Detection of a novel tetM determinant in tetracycline-resistant Neisseria gonorrhoeae from Uruguay, 1996-1999. Sex. Transm. Dis. 29:792-797.
94. Marquez, C., et al. 1996. The first molecular characterization of tetracycline- resistant Neisseria gonorrhoeae from Uruguay. J. Antimicrob. Chemother. 37:839-841.
95. Martin, I. M., A. Ghani, G. Bell, G. Kinghorn, and C. A. Ison. 2003. Persistence of two genotypes of Neisseria gonorrhoeae during transmission. J. Clin. Microbiol. 41:5609-5614.
96. Martin, I. M., and C. A. Ison. 2003. Detection of mixed infection of Neisseria gonorrhoeae. Sex. Transm. Infect. 79:56-58.
97. Martin, I. M., C. A. Ison, D. M. Aanensen, K. A. Fenton, and B. G. Spratt. 2005. Changing epidemiologic profile of quinolone-resistant Neisseria gonorrhoeae in London. J. Infect. Dis. 192:1191-1195.
98. 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.
99. Martin, I. M., et al. 2007. Non-cultural detection and molecular genotyping of Neisseria gonorrhoeae from a piece of clothing. J. Med. Microbiol. 56: 487-490.
100. Maynard Smith, J., N. H. Smith, M. O'Rourke, and B. G. Spratt. 1993. How clonal are bacteria? Proc. Natl. Acad. Sci. U. S. A. 90:4384-4388.
101. McKnew, D. L., F. Lynn, J. M. Zenilman, and M. C. Bash. 2003. Porin variation among clinical isolates of Neisseria gonorrhoeae over a 10-year period, as determined by por variable region typing. J. Infect. Dis. 187:1213-1222.
102. Mee, B. J., H. Thomas, S. J. Cooke, P. R. Lambden, and J. E. Heckels. 1993. Structural comparison and epitope analysis of outer-membrane protein PIA from strains of Neisseria gonorrhoeae with differing serovars specificities. J. Gen. Microbiol. 139:2613-2620.
103. Monfort, L., et al. 2009. First Neisseria gonorrhoeae genotyping analysis in France: identification of a strain cluster with reduced susceptibility to ceftriaxone J. Clin. Microbiol. 47:3540-3545.
104. Moodley, P., I. M. Martin, C. A. Ison, and A. W. Sturm. 2002. Typing of Neisseria gonorrhoeae reveals rapid reinfection in rural South Africa. J. Clin. Microbiol. 40:4567-4570.
105. Moodley, P., I. M. Martin, K. Pillay, C. A. Ison, and A. W. Sturm. 2006. Molecular epidemiology of recently emergent ciprofloxacin-resistant Neisseria gonorrhoeae in South Africa. Sex. Transm. Dis. 33:357-360.
106. Morris, A. K., H. M. Palmer, and H. Young. 2008. Opa-typing can identify epidemiologically distinct subgroups within Neisseria gonorrhoeae multiantigen sequence type (NG-MAST) clusters. Epidemiol. Infect. 136:417-420.
107. Morris, S. R., et al. 2009. Strain typing and antimicrobial resistance of fluoroquinolone-resistant Neisseria gonorrhoeae causing a California infection outbreak. J. Clin. Microbiol. 47:2944-2949.
108. Morris, S. R., et al. 2008. Using strain typing to characterise a fluoroquinolone- resistant Neisseria gonorrhoeae transmission network in southern California. Sex. Transm. Infect. 84:290-291.
109. Morse, S. A., and C. M. Beck-Sague. 1999. Gonorrhoea, p. 151-174. In P. J. Hitchcock, H. T. MacKay, J. N. Wasserheit, and R. Binder (ed.), Sexually transmitted diseases and adverse outcomes of pregnancy. ASM Press, Washington, DC.
110. Morse, S. A., S. R. Johnson, J. W. Biddle, and M. C. Roberts. 1986. High-level tetracycline resistance in Neisseria gonorrhoeae is result of acquisition of streptococcal tetM determinant. Antimicrob. Agents Chemother. 30:664-670.
111. Ng, L. K., A. Lau, I. Martin, and R. Tsang. 2006. Characterization of proline, citrulline, and uracil auxotrophic plasmid-carrying Neisseria gonorrhoeae strains in Canada, 1993-2003. Sex. Transm. Dis. 33:688-690.
112. Ng, L. K., and J. R. Dillon. 1993. Typing by serovar, antibiogram, plasmid content, riboprobing, and isoenzyme typing to determine whether Neisseria gonorrhoeae isolates requiring proline, citrulline, and uracil for growth are clonal. J. Clin. Microbiol. 31:1555-1561.
113. Ng, L.-K., M. Carballo, and J.-A. R. Dillon. 1995. Differentiation of Neisseria gonorrhoeae isolates requiring proline, citrulline, and uracil by plasmid content, serotyping, and pulsed-field gel electrophoresis. J. Clin. Microbiol. 33:1039-1041.
114. Ng, L. K., et al. 2006. Auxotype classifications of Neisseria gonorrhoeae represent the overall genetic content of individual strains, abstr. P2.2.06. Abstr. 15th Int. Pathogenic Neisseria Conf., Cairns, Australia.
115. Ng, L. K., P. Sawatzky, I. E. Martin, and S. Booth. 2002. Characterization of ciprofloxacin resistance in Neisseria gonorrhoeae isolates in Canada. Sex. Transm. Dis. 29:780-788.
116. Ohnishi, M., et al. 2010. Spread of a chromosomal cefixime-resistant penA gene among different Neisseria gonorrhoeae lineages. Antimicrob. Agents Chemother. 54:1060-1067.
117. Olsen, B., R. Hadad, H. Fredlund, and M. Unemo. 2008. The Neisseria gonorrhoeae population in Sweden during 2005-phenotypes, genotypes and antibiotic resistance. APMIS 116:181-189.
118. O'Rourke, M., and B. G. Spratt. 1994. Further evidence for the non-clonal population structure of Neisseria gonorrhoeae: extensive genetic diversity within isolates of the same electrophoretic type. Microbiology 140:1285-1290.
119. O'Rourke, M., and E. Stevens. 1993. Genetic structure of Neisseria gonorrhoeae populations: a non-clonal pathogen. J. Gen. Microbiol. 139:2603-2611.
120. O'Rourke, M., C. A. Ison, A. M. Renton, and B. G. Spratt. 1995. Opatyping: a high-resolution tool for studying the epidemiology of gonorrhoea. Mol. Microbiol. 17:865-875.
121. Ota, K. V., et al. 2009. Incidence and treatment outcomes of pharyngeal Neisseria gonorrhoeae and Chlamydia trachomatis infections in men who have sex with men: a 13-year retrospective cohort study. Clin. Infect. Dis. 48:1237-1243.
122. Pagotto, F., et al. 2000. Sequence analysis of the family of penicillinaseproducing plasmids of Neisseria gonorrhoeae based on DNA sequencing. Plasmid 43:24-34.
123. Palmer, H. M., and C. Arnold. 2001. Genotyping Neisseria gonorrhoeae using fluorescent amplified fragment length polymorphism analysis. J. Clin. Microbiol. 39:2325-2329.
124. Palmer, H. M., and H. Young. 2006. Dramatic increase in a single genotype of TRNG ciprofloxacin-resistant Neisseria gonorrhoeae isolates in men who have sex with men. Int. J. STD AIDS 17:254-256.
125. Palmer, H. M., H. Young, A. Winter, and J. Dave. 2008. Emergence and spread of azithromycin-resistant Neisseria gonorrhoeae in Scotland. J. Antimicrob. Chemother. 62:490-494.
126. Palmer, H. M., H. Young, C. Graham, and J. Dave. 2008. Prediction of antibiotic resistance using Neisseria gonorrhoeae multi-antigen sequence typing. Sex. Transm. Infect. 84:280-284.
127. Palmer, H. M., H. Young, I. M. Martin, C. A. Ison, and B. G. Spratt. 2005. The epidemiology of ciprofloxacin resistant isolates of Neisseria gonorrhoeae in Scotland 2002: a comparison of phenotypic and genotypic analysis. Sex. Transm. Infect. 81:403-407.
128. Palmer, H. M., J. P. Leeming, and A. Turner. 2000. A multiplex polymerase chain reaction to differentiate beta-lactamase plasmids of Neisseria gonorrhoeae. J. Antimicrob. Chemother. 45:777-782.
129. Palmer, H. M., J. P. Leeming, and A. Turner. 2001. Investigation of an outbreak of ciprofloxacin-resistant Neisseria gonorrhoeae using a simplified opa-typing method. Epidemiol. Infect. 126:219-224.
130. 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.
131. Pérez-Losada, M., K. A. Crandall, J. Zenilman, and R. P. Viscidi. 2007. Temporal trends in gonococcal population genetics in a high prevalence urban community. Infect. Genet. Evol. 7:271-278.
132. Pérez-Losada, M., et al. 2007. Distinguishing importation from diversification of quinolone-resistant Neisseria gonorrhoeae by molecular evolutionary analysis. BMC. Evol. Biol. 7:84.
133. Pérez-Losada, M., R. P. Viscidi, J. C. Demma, J. Zenilman, and K. A. Crandall. 2005. Population genetics of Neisseria gonorrhoeae in a highprevalence community using a hypervariable outer membrane porB and 13 slowly evolving housekeeping genes. Mol. Biol. Evol. 22:1887-1902.
134. Poh, C. L., and Q. C. Lau. 1993. Subtyping of Neisseria gonorrhoeae auxotype- serovar groups by pulsed-field gel electrophoresis. J. Med. Microbiol. 38:366-370.
135. Poh, C. L., G. K. Loh, and J. W. Tapsall. 1995. Resolution of clonal subgroups among Neisseria gonorrhoeae IB-2 and IB-6 serovars by pulsedfield gel electrophoresis. Genitourin. Med. 71:145-149.
136. Poh, C. L., J. C. Ocampo, and G. K. Loh. 1992. Genetic relationships among Neisseria gonorrhoeae serovars analysed by multilocus enzyme electrophoresis. Epidemiol. Infect. 108:31-38.
137. Poh, C. L., Q. C. Lau, and V. T. K. Chow. 1995. Differentiation of Neisseria gonorrhoeae IB-3 and IB-7 serovars by direct sequencing of protein IB gene and pulsed-field gel electrophoresis. J. Med. Microbiol. 43:201-207.
138. Poh, C. L., V. Ramachandran, and J. W. Tapsall. 1996. Genetic diversity of Neisseria gonorrhoeae IB-2 and IB-6 isolates revealed by whole-cell repetitive element sequence-based PCR. J. Clin. Microbiol. 34:292-295.
139. Posada, D., K. A. Crandall, M. Nguyen, J. C. Demma, and R. P. Viscidi. 2000. Population genetics of the porB gene of Neisseria gonorrhoeae: different dynamics in different homology groups. Mol. Biol. Evol. 17:423-436.
140. Risley, C. L., et al. 2007. Geographical and demographic clustering of gonorrhoea in London. Sex. Transm. Infect. 83:481-487.
141. Sandström, E., and D. Danielsson. 1980. Serology of Neisseria gonorrhoeae. Classification by co-agglutination. Acta Pathol. Microbiol. Scand. B 88:27-38.
142. Sandström, E., and S. Bygdeman. 1987. Serological classification of Neisseria gonorrhoeae. Clinical and epidemiological applications. Antonie Van Leeuwenhoek 53:375-380.
143. Sandström, E., et al. 1985. Evaluation of a new set of Neisseria gonorrhoeae serogroup W-specific monoclonal antibodies for serovar determination, p. 26-30. In G. K. Schoolnik et al. (ed.), The pathogenic neisseriae. American Society for Microbiology, Washington, DC.
144. Schwartz, D. C., and C. R. Cantor. 1984. Separation of yeast chromosomesized DNAs by pulsed gradient gel electrophoresis. Cell 37:67-75.
145. Selander, R. K., et al. 1986. Methods of multilocus enzyme electrophoresis for bacterial population genetics and systematics. Appl. Environ. Microbiol. 51:873-884.
146. Reference deleted.
147. Smith, N. H., E. C. Holmes, G. M. Donovan, G. A. Carpenter, and B. G. Spratt. 1999. Networks and groups within the genus Neisseria: analysis of argF, recA, rho, and 16S rRNA sequences from human Neisseria species. Mol. Biol. Evol. 16:773-783.
148. Smith, N. H., J. Maynard Smith, and B. G. Spratt. 1995. Sequence evolution of the porB gene of Neisseria gonorrhoeae and Neisseria meningitidis: evidence of positive Darwinian selection. Mol. Biol. Evol. 12:363-370.
149. Snyder, L. A., and N. J. Saunders. 2006. The majority of genes in the pathogenic Neisseria species are present in non-pathogenic Neisseria lactamica, including those designated as 'virulence genes'. BMC Genomics 7:128.
150. Snyder, L. A., J. K. Davies, and N. J. Saunders. 2004. Microarray genomotyping of key experimental strains of Neisseria gonorrhoeae reveals gene complement diversity and five new neisserial genes associated with minimal mobile elements. BMC Genomics 5:23.
151. Spaargaren, J., J. Stoof, H. Fennema, R. Coutinho, and P. Savelkoul. 2001. Amplified fragment length polymorphism fingerprinting for identification of a core group of Neisseria gonorrhoeae transmitters in the population attending a clinic for treatment of sexually transmitted diseases in Amsterdam, The Netherlands. J. Clin. Microbiol. 39:2335-2337.
152. Sparling, P. F. 2008. Biology of Neisseria gonorrhoeae, p. 607-626. In K. K. Holmes, P. F. Sparling, W. E. Stamm, P. Piot, J. N. Wasserheit, L. Corey, M. S. Cohen, and D. H. Watts (ed.), Sexually transmitted diseases, 4th ed. McGraw-Hill, New York, NY.
153. Spratt, B. G., and M. C. Maiden. 1999. Bacterial population genetics, evolution and epidemiology. Philos. Trans. R. Soc. Lond. B Biol. Sci. 354:701-710.
154. Sreevatsan, S., et al. 1997. Restricted structural gene polymorphism in the Mycobacterium tuberculosis complex indicates evolutionarily recent global dissemination. Proc. Natl. Acad. Sci. U. S. A. 94:9869-9874.
155. Starnino, S., P. Stefanelli, and Neisseria gonorrhoeae Italian Study Group. 2009. Azithromycin-resistant Neisseria gonorrhoeae strains recently isolated in Italy. J. Antimicrob. Chemother. 63:1200-1204.
156. Starnino, S., A. Neri, P. Stefanelli, and Neisseria gonorrhoeae Italian Study Group. 2008. Molecular analysis of tetracycline-resistant gonococci: rapid detection of resistant genotypes using a real-time PCR assay. FEMS. Microbiol. Lett. 286:16-23.
157. Starnino, S., et al. 2010. Trend of ciprofloxacin resistance in Neisseria gonorrhoeae strains isolated in Italy and analysis of the molecular determinants. Diagn. Microbiol. Infect. Dis. 67:350-354.
158. Starnino, S., B. Suligoi, V. Regine, N. Bilek, P. Stefanelli, Neisseria gonorrhoeae Italian Study Group, et al. 2008. Phenotypic and genotypic characterization of Neisseria gonorrhoeae in parts of Italy: detection of a multiresistant cluster circulating in a heterosexual network. Clin. Microbiol. Infect. 14:949-954.
159. Tam, M. R., et al. 1982. Serological classification of Neisseria gonorrhoeae with monoclonal antibodies. Infect. Immun. 36:1042-1053.
160. Tapsall, J. 2001. Antimicrobial resistance in Neisseria gonorrhoeae. World Health Organization (WHO) report. WHO/CDS/CSR/DSR/2001.3. World Health Organization, Geneva, Switzerland.
161. Tapsall, J., D. Whiley, and T. Sloots. 2006. Applications of molecular testing in clinical laboratories for the diagnosis and control of gonorrhea. Future Microbiol. 1:317-324.
162. Tapsall, J. W., F. Ndowa, D. A. Lewis, and M. Unemo. 2009. Meeting the public health challenge of multidrug- and extensively drug-resistant Neisseria gonorrhoeae. Expert Rev. Anti Infect. Ther. 7:821-834.
163. Tapsall, J., et al. 2009. Two cases of failed ceftriaxone treatment in pharyngeal gonorrhoea verified by molecular microbiological methods. J. Med. Microbiol. 58:683-687.
164. Tapsall, J. W., S. Ray, and A. Limnios. 2010. Characteristics and population dynamics of mosaic penA allele-containing Neisseria gonorrhoeae isolates collected in Sydney, Australia, in 2007-2008. Antimicrob. Agents Chemother. 54:554-556.
165. Tazi, L., et al. 2010. Population dynamics of Neisseria gonorrhoeae in Shanghai, China: a comparative study. BMC Infect. Dis. 10:13.
166. Thompson, D. K., C. D. Deal, C. A. Ison, J. M. Zenilman, and M. C. Bash. 2000. A typing system for Neisseria gonorrhoeae based on biotinylated oligonucleotide probes to PIB gene variable regions. J. Infect. Dis. 181: 1652-1660.
167. Todd, K., et al. 2007. Using epidemiological and molecular methods to investigate an outbreak of gonorrhoea associated with heterosexual contact in Newcastle, NSW, Australia. Sex. Health 4:233-236.
168. Trees, D. L., A. J. Schultz, and J. S. Knapp. 2000. Use of the neisserial lipoprotein (Lip) for subtyping Neisseria gonorrhoeae. J. Clin. Microbiol. 38:2914-2916.
169. Trees, D. L., A. L. Sandul, S. W. Neal, H. Higa, and J. S. Knapp. 2001. Molecular epidemiology of Neisseria gonorrhoeae exhibiting decreased susceptibility and resistance to ciprofloxacin in Hawaii, 1991-1999. Sex. Transm. Dis. 28:309-314.
170. Trees, D. L., et al. 2002. Multiclonal increase in ciprofloxacin-resistant Neisseria gonorrhoeae, Thailand, 1998-1999. Sex. Transm. Dis. 29:668-673.
171. Turner, A., K. R. Gough, and J. P. Leeming. 1999. Molecular epidemiology of tetM genes in Neisseria gonorrhoeae. Sex. Transm. Infect. 75:60-66.
172. Tzelepi, E., et al. 2010. Changing figures of antimicrobial susceptibility and serovar distribution in Neisseria gonorrhoeae isolated in Greece. Sex. Transm. Dis. 37:115-120.
173. Tzelepi, E., et al. 2008. Cluster of multidrug-resistant Neisseria gonorrhoeae with reduced susceptibility to the newer cephalosporins in Northern Greece. J. Antimicrob. Chemother. 62:637-639.
174. Unemo, M., et al. 2007. Molecular characterization of Neisseria gonorrhoeae identifies transmission and resistance of one ciprofloxacin-resistant strain. APMIS 115:231-241.
175. Unemo, M., D. Golparian, G. Syversen, D. F. Vestrheim, and H. Moi. 2010. Two cases of verified clinical failures using internationally recommended first-line cefixime for gonorrhoea treatment, Norway, 2010. Euro Surveill. 15:pii: 19721.
176. Unemo, M., et al. 2007. Global transmission of prolyliminopeptidase (PIP)- negative Neisseria gonorrhoeae strains-implications for changes in diagnostic strategies? Sex. Transm. Infect. 83:47-51.
177. 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.
178. Unemo, M., P. Olcén, J. Albert, and H. Fredlund. 2003. Comparison of serologic and genetic porB-based typing of Neisseria gonorrhoeae: consequences for future characterization. J. Clin. Microbiol. 41:4141-4147.
179. Unemo, M., P. Olcén, J. Jonasson, and H. Fredlund. 2004. Molecular typing of Neisseria gonorrhoeae isolates by pyrosequencing of highly polymorphic segments of the porB gene. J. Clin. Microbiol. 42:2926-2934.
180. Unemo, M., P. Olcén, T. Berglund, J. Albert, and H. Fredlund. 2002. Molecular epidemiology of Neisseria gonorrhoeae: sequence analysis of the porB gene confirms presence of two circulating strains. J. Clin. Microbiol. 40:3741-3749.
181. Unemo, M., T. Berglund, P. Olcén, and H. Fredlund. 2002. Pulsed-field gel electrophoresis as an epidemiologic tool for Neisseria gonorrhoeae: identification of clusters within serovars. Sex. Transm. Dis. 29:25-31.
182. Unemo, M., et al. 2007. Neisseria gonorrhoeae population in Arkhangelsk, Russia: phenotypic and genotypic heterogeneity. Clin. Microbiol. Infect. 13:873-878.
183. Urwin, R., and M. C. J. Maiden. 2003. Multi-locus sequence typing: a tool for global epidemiology. Trends Microbiol. 11:479-487.
184. van Looveren, M., et al. 1999. Evaluation of the discriminatory power of typing methods for Neisseria gonorrhoeae. J. Clin. Microbiol. 37:2183-2188.
185. Vickerman, P., R. W. Peeling, C. Watts, and D. Mabey. 2005. Detection of gonococcal infection: pros and cons of a rapid test. Mol. Diagn. 9:175-179.
186. Vidovic, S., G. Horsman, and J. R. Dillon. 2010. Novel gonococcal multilocus sequence typing (MLST) scheme suitable for short- and long-term molecular epidemiology studies, abstr. OE34. Abstr. 17th Int. Pathogenic Neisseria Conf., Banff, Alberta, Canada.
187. Viscidi, R. P., and J. C. Demma. 2003. Genetic diversity of Neisseria gonorrhoeae housekeeping genes. J. Clin. Microbiol. 41:197-204.
188. Viscidi, R. P., J. C. Demma, J. Gu, and J. Zenilman. 2000. Comparison of sequencing of the por gene and typing of the opa gene for discrimination of Neisseria gonorrhoeae strains from sexual contacts. J. Clin. Microbiol. 38: 4430-4438.
189. Vollrath, D., and R. W. Davis. 1987. Resolution of DNA molecules greater than 5 megabases by contour-clamped homogeneous electric fields. Nucleic Acids Res. 15:7865-7876.
190. Wallace, R. F., X. Collins, B. B. Diena, and J. R. Dillon. 1978. Auxonographic typing of Neisseria gonorrhoeae strains. Lab. Centre Dis. Control Newsl. 2:17-20.
191. Ward, H., et al. 2000. A prospective social and molecular investigation of gonococcal transmission. Lancet 356:1812-1817.
192. 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.
193. Whiley, D. M., et al. 2010. Neisseria gonorrhoeae multi-antigen sequence typing using non-cultured clinical specimens. Sex. Transm. Infect. 86:51-55.
194. Whiley, D. M., et al. 2010. Alterations of the pilQ gene in Neisseria gonorrhoeae are unlikely contributors to decreased susceptibility to ceftriaxone and cefixime in clinical gonococcal strains. J. Antimicrob. Chemother. 65: 2543-2547.
195. Wong, W. W., et al. 2008. Molecular epidemiological identification of Neisseria gonorrhoeae clonal clusters with distinct susceptibility profiles associated with specific groups at high risk of contracting human immunodeficiency virus and syphilis. J. Clin. Microbiol. 46:3931-3934.
196. Woods, J. P., S. M. Spinola, S. M. Strobel, and J. G. Cannon. 1989. Conserved lipoprotein H. 8 of pathogenic Neisseria consists entirely of pentapeptide repeats. Mol. Microbiol. 3:43-48.
197. World Health Organization. 2011. Prevalence and incidence in 2005 of selected sexually transmitted infections: methods and results. World Health Organization, Geneva, Switzerland.
198. Xia, M., et al. 1996. Neisseria gonorrhoeae with decreased susceptibility to ciprofloxacin: pulsed-field gel electrophoresis typing of strains from North America, Hawaii, and the Philippines. Antimicrob. Agents Chemother. 40:2439-2440.
199. Xia, M., W. L. Whittington, K. K. Holmes, F. A. Plummer, and M. C. Roberts. 1995. Pulsed-field gel electrophoresis for genomic analysis of Neisseria gonorrhoeae. J. Infect. Dis. 171:455-458.
200. Yeung, K. H., and J. R. Dillon. 1988. Construction of miniplasmids from the 7.2 and 5.1 kb penicillinase producing plasmids of N. gonorrhoeae reveals two replication regions. Plasmid 20:232-240.
201. Young, H., A. Moyes, I. B. Tait, A. C. McCartney, and G. Gallacher. 1990. Non-typable quinolone-resistant gonococci. Lancet 335:604.