Skip to main content
SpringerLink
Log in

Antibiotic Resistance in Neisseria

  • Chapter
  • First Online:
Antimicrobial Drug Resistance

Abstract

Antibiotic resistance represents a substantial threat in the treatment and control of Neisseria gonorrhoeae. Exhibiting high transformability, resistance mechanisms have spread rapidly throughout the species, resulting in the development of clinically significant resistance to every class of antibiotics used in the treatment of gonorrheal disease. Resistance to third-generation cephalosporins, the only remaining class suitable as a single-dose single-agent therapy, has developed, and effective treatment regimens vary depending on the geographic origin of infection. Ongoing surveillance programs are essential for identifying and limiting the emergence of cephalosporin- and multidrug-resistant gonococci in the future, a problem which to a lesser extent threatens the closely related pathogen, N. meningitidis.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 229.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 299.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 299.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  1. Hook III EW, Handsfield HH. Gonococcal infections in the adult. In: Holmes KK, Sparling PF, Stamm WE, et al., editors. Sexually transmitted diseases. 4th ed. New York: McGraw-Hill; 2008.

    Google Scholar 

  2. Hynes NA, Rompalo AM. Gonococcal infection in women. In: Goldman MB, Troisi R, Rexrode KM, editors. Women and health. 2nd ed. London: Academic; 2013.

    Google Scholar 

  3. Cohen MS. Sexually transmitted diseases enhance HIV transmission: no longer a hypothesis. Lancet. 1998;351 Suppl 3:5–7.

    Article  PubMed  Google Scholar 

  4. World Health Organization. Global incidence and prevalence of selected curable sexually transmitted infections—2008. Geneva: World Health Organization; 2012.

    Google Scholar 

  5. Public Health England. Sexually transmitted infections and chlamydia screening in England, 2014. Infection Report, vol. 9. London: Public Health England; 2015.

    Google Scholar 

  6. Centers for Disease Control and Prevention. Sexually transmitted disease surveillance 2012. Atlanta: Centers for Disease Control and Prevention; 2013.

    Google Scholar 

  7. Centers for Disease Control and Prevention, Donovan B, Bodsworth NJ, Rohrsheim R, McNulty A, Tapsall JW, Martin IM, Ison CA, Waugh MA, Holtgrave DR, Crosby RA, Walker CK, Sweet RL, Laga M, Manoka A, Kivuvu M, Malele B, Tuliza M, Nzila N, Goeman J, Behets F, Batter V, Alary M, et al. Increases in fluoroquinolone-resistant Neisseria gonorrhoeae among men who have sex with men--United States, 2003, and revised recommendations for gonorrhea treatment, 2004. MMWR Morb Mortal Wkly Rep. 2004;53(16):335–8. doi:10.2147/IJWH.S13427.

    Google Scholar 

  8. Donovan B, Bodsworth NJ, Rohrsheim R, McNulty A, Tapsall JW. Increasing gonorrhoea reports—not only in London. Lancet. 2000;355(9218):1908. doi:10.1016/s0140-6736(05)73352-3.

    Article  CAS  PubMed  Google Scholar 

  9. Martin IM, Ison CA. Rise in gonorrhoea in London, UK. London Gonococcal Working Group. Lancet. 2000;355(9204):623.

    Article  CAS  PubMed  Google Scholar 

  10. Waugh MA. Task force for the urgent response to the epidemics of sexually transmitted diseases in eastern Europe and central Asia. Sex Transm Infect. 1999;75(1):72–3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Holtgrave DR, Crosby RA. Social capital, poverty, and income inequality as predictors of gonorrhoea, syphilis, chlamydia and AIDS case rates in the United States. Sex Transm Infect. 2003;79(1):62–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Walker CK, Sweet RL. Gonorrhea infection in women: prevalence, effects, screening, and management. Int J Womens Health. 2011;3:197–206. doi:10.2147/ijwh.s13427.

    PubMed  PubMed Central  Google Scholar 

  13. Sparling PF, Handsfield HH. Neisseria gonorrhoeae. In: Mandell GL, Bennett JE, editors. Principles and practice of infectious diseases, 8th ed. Philadelphia: Churchill Livingstone; 2000. p. 2242–58.

    Google Scholar 

  14. Laga M, Manoka A, Kivuvu M, Malele B, Tuliza M, Nzila N, Goeman J, Behets F, Batter V, Alary M, et al. Non-ulcerative sexually transmitted diseases as risk factors for HIV-1 transmission in women: results from a cohort study. AIDS. 1993;7(1):95–102.

    Article  CAS  PubMed  Google Scholar 

  15. Cohen MS, Hoffman IF, Royce RA, Kazembe P, Dyer JR, Daly CC, Zimba D, Vernazza PL, Maida M, Fiscus SA, Eron Jr JJ, AIDSCAP Malawi Research Group. Reduction of concentration of HIV-1 in semen after treatment of urethritis: implications for prevention of sexual transmission of HIV-1. Lancet. 1997;349(9069):1868–73.

    Article  CAS  PubMed  Google Scholar 

  16. Tapsall JW. Antimicrobial resistance in Neisseria gonorrhoeae. Geneva: World Health Organization; 2001.

    Google Scholar 

  17. World Health Organization. Global action plan to control the spread and impact of antimicrobial resistance in Neisseria gonorrhoeae. Geneva: World Health Organization; 2012.

    Google Scholar 

  18. Haizlip J, Isbey SF, Hamilton HA, Jerse AE, Leone PA, Davis RH, Cohen MS. Time required for elimination of Neisseria gonorrhoeae from the urogenital tract in men with symptomatic urethritis: comparison of oral and intramuscular single-dose therapy. Sex Transm Dis. 1995;22(3):145–8.

    Article  CAS  PubMed  Google Scholar 

  19. Holmes KK, Johnson DW, Floyd TM. Studies of venereal disease. I. Probenecid-procaine penicillin G combination and tetracycline hydrochloride in the treatment of “penicillin-resistant” gonorrhea in men. J Am Med Assoc. 1967;202(6):461–73.

    Article  CAS  Google Scholar 

  20. Cannon JG, Sparling PF. The genetics of the gonococcus. Annu Rev Microbiol. 1984;38:111–33. doi:10.1146/annurev.mi.38.100184.000551.

    Article  CAS  PubMed  Google Scholar 

  21. Fussenegger M, Rudel T, Barten R, Ryll R, Meyer TF. Transformation competence and type-4 pilus biogenesis in Neisseria gonorrhoeae—a review. Gene. 1997;192(1):125–34.

    Article  CAS  PubMed  Google Scholar 

  22. Hamilton HL, Dillard JP. Natural transformation of Neisseria gonorrhoeae: from DNA donation to homologous recombination. Mol Microbiol. 2006;59(2):376–85. doi:10.1111/j.1365-2958.2005.04964.x.

    Article  CAS  PubMed  Google Scholar 

  23. Barry PM, Klausner JD. The use of cephalosporins for gonorrhea: the impending problem of resistance. Expert Opin Pharmacother. 2009;10(4):555–77. doi:10.1517/14656560902731993.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Lewis DA. Global resistance of Neisseria gonorrhoeae: when theory becomes reality. Curr Opin Infect Dis. 2014;27(1):62–7. doi:10.1097/qco.0000000000000025.

    Article  CAS  PubMed  Google Scholar 

  25. Patel AL, Chaudhry U, Sachdev D, Sachdeva PN, Bala M, Saluja D. An insight into the drug resistance profile and mechanism of drug resistance in Neisseria gonorrhoeae. Indian J Med Res. 2011;134:419–31.

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Reyn A, Korner B, Bentzon MW. Effects of penicillin, streptomycin, and tetracycline on N. gonorrhoeae isolated in 1944 and in 1957. Br J Vener Dis. 1958;34(4):227–39.

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Allen VG, Mitterni L, Seah C, Rebbapragada A, Martin IE, Lee C, Siebert H, Towns L, Melano RG, Low DE. Neisseria gonorrhoeae treatment failure and susceptibility to cefixime in Toronto, Canada. J Am Med Assoc. 2013;309(2):163–70. doi:10.1001/jama.2012.176575.

    Article  CAS  Google Scholar 

  28. Camara J, Serra J, Ayats J, Bastida T, Carnicer-Pont D, Andreu A, Ardanuy C. Molecular characterization of two high-level ceftriaxone-resistant Neisseria gonorrhoeae isolates detected in Catalonia, Spain. J Antimicrob Chemother. 2012;67(8):1858–60. doi:10.1093/jac/dks162.

    Article  CAS  PubMed  Google Scholar 

  29. Ison CA, Hussey J, Sankar KN, Evans J, Alexander S. Gonorrhoea treatment failures to cefixime and azithromycin in England, 2010. Euro Surveill. 2011;16(14):7–10.

    Google Scholar 

  30. Lewis DA, Sriruttan C, Muller EE, Golparian D, Gumede L, Fick D, de Wet J, Maseko V, Coetzee J, Unemo M. Phenotypic and genetic characterization of the first two cases of extended-spectrum-cephalosporin-resistant Neisseria gonorrhoeae infection in South Africa and association with cefixime treatment failure. J Antimicrob Chemother. 2013;68(6):1267–70. doi:10.1093/jac/dkt034.

    Article  CAS  PubMed  Google Scholar 

  31. Chen MY, Stevens K, Tideman R, Zaia A, Tomita T, Fairley CK, Lahra M, Whiley D, Hogg G. Failure of 500 mg of ceftriaxone to eradicate pharyngeal gonorrhoea, Australia. J Antimicrob Chemother. 2013;68(6):1445–7. doi:10.1093/jac/dkt017.

    Article  CAS  Google Scholar 

  32. Ohnishi M, Golparian D, Shimuta K, Saika T, Hoshina S, Iwasaku K, Nakayama S, Kitawaki J, Unemo M. 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(7):3538–45. doi:10.1128/aac.00325-11.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. 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(3):1273–80. doi:10.1128/aac.05760-11.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Unemo M, Golparian D, Stary A, Eigentler A. First Neisseria gonorrhoeae strain with resistance to cefixime causing gonorrhoea treatment failure in Austria, 2011. Euro Surveill. 2011b;16(43): pii: 19998.

    Google Scholar 

  35. Unemo M, Golparian D, Syversen G, Vestrheim DF, Moi H. Two cases of verified clinical failures using internationally recommended first-line cefixime for gonorrhoea treatment, Norway, 2010. Euro Surveill. 2010;15(47): pii: 19721.

    Google Scholar 

  36. Yokoi S, Deguchi T, Ozawa T, Yasuda M, Ito S, Kubota Y, Tamaki M, Maeda S. Threat to cefixime treatment for gonorrhea. Emerg Infect Dis. 2007;13(8):1275–7. doi:10.3201/eid1308.060948.

    PubMed  PubMed Central  Google Scholar 

  37. Laga M. Epidemiology and control of sexually transmitted diseases in developing countries. Sex Transm Dis. 1994;21 Suppl 2:S45–50.

    CAS  PubMed  Google Scholar 

  38. Abellanosa I, Nichter M. Antibiotic prophylaxis among commercial sex workers in Cebu City, Philippines. Patterns of use and perceptions of efficacy. Sex Transm Dis. 1996;23(5):407–12.

    Article  CAS  PubMed  Google Scholar 

  39. Adu-Sarkodie YA. Antimicrobial self medication in patients attending a sexually transmitted diseases clinic. Int J STD AIDS. 1997;8(7):456–8.

    Article  CAS  PubMed  Google Scholar 

  40. Taylor RB, Shakoor O, Behrens RH. Drug quality, a contributor to drug resistance? Lancet. 1995;346(8967):122.

    Article  CAS  PubMed  Google Scholar 

  41. Van der Veen F, Fransen L. Drugs for STD management in developing countries: choice, procurement, cost, and financing. Sex Transm Infect. 1998;74 Suppl 1:S166–74.

    PubMed  Google Scholar 

  42. Johnson SR, Morse SA. Antibiotic resistance in Neisseria gonorrhoeae: genetics and mechanisms of resistance. Sex Transm Dis. 1988;15(4):217–24.

    Article  CAS  PubMed  Google Scholar 

  43. Sparling PF. Antibiotic resistance in Neisseria gonorrhoeae. Med Clin North Am. 1972;56(5):1133–44.

    Article  CAS  PubMed  Google Scholar 

  44. Ropp PA, Hu M, Olesky M, Nicholas RA. 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(3):769–77.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Dougherty TJ. Involvement of a change in penicillin target and peptidoglycan structure in low-level resistance to beta-lactam antibiotics in Neisseria gonorrhoeae. Antimicrob Agents Chemother. 1985;28(1):90–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Sparling PF, Sarubbi Jr FA, Blackman E. Inheritance of low-level resistance to penicillin, tetracycline, and chloramphenicol in Neisseria gonorrhoeae. J Bacteriol. 1975;124(2):740–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Guymon LF, Sparling PF. Altered crystal violet permeability and lytic behavior in antibiotic-resistant and -sensitive mutants of Neisseria gonorrhoeae. J Bacteriol. 1975;124(2):757–63.

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Hagman KE, Pan W, Spratt BG, Balthazar JT, Judd RC, Shafer WM. Resistance of Neisseria gonorrhoeae to antimicrobial hydrophobic agents is modulated by the mtrRCDE efflux system. Microbiology. 1995;141(Pt. 3):611–22. doi:10.1099/13500872-141-3-611.

    Article  CAS  PubMed  Google Scholar 

  49. Gill MJ, Simjee S, Al-Hattawi K, Robertson BD, Easmon CS, Ison CA. Gonococcal resistance to beta-lactams and tetracycline involves mutation in loop 3 of the porin encoded at the penB locus. Antimicrob Agents Chemother. 1998;42(11):2799–803.

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Olesky M, Hobbs M, Nicholas RA. 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. 2002;46(9):2811–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Olesky M, Zhao S, Rosenberg RL, Nicholas RA. Porin-mediated antibiotic resistance in Neisseria gonorrhoeae: ion, solute, and antibiotic permeation through PIB proteins with penB mutations. J Bacteriol. 2006;188(7):2300–8. doi:10.1128/jb.188.7.2300-2308.2006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Zhao S, Tobiason DM, Hu M, Seifert HS, Nicholas RA. The penC mutation conferring antibiotic resistance in Neisseria gonorrhoeae arises from a mutation in the PilQ secretin that interferes with multimer stability. Mol Microbiol. 2005;57(5):1238–51. doi:10.1111/j.1365-2958.2005.04752.x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Ison CA. Antimicrobial agents and gonorrhoea: therapeutic choice, resistance and susceptibility testing. Genitourin Med. 1996;72(4):253–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Bygdeman SM. Polyclonal and mnoclonal antibodies applied to the epidemiology of gonococcal infection. In: Young H, McMillan A, editors. Immunologic diagnosis of sexually transmitted diseases. New York: Marcel Dekker; 1988. p. 117–65.

    Google Scholar 

  55. Knapp JS, Bygdeman S, Sandstrom E, Holmes KK. Nomenclature for the serologic classification of Neisseria gonorrhoeae. In: Schoolnik G, Brooks GF, Falkow S, editors. The pathogenic Neisseriae. Washington, DC: American Society for Microbiology; 1985. p. 4–5.

    Google Scholar 

  56. Brunton JL, Clare D, Ehrman N, Meier MA. Evolution of antibiotic resistance plasmids in Neisseria gonorrhoeae and Haemophilus species. Clin Invest Med. 1983;6(3):221–8.

    CAS  PubMed  Google Scholar 

  57. Flett F, Humphreys GO, Saunders JR. Intraspecific and intergeneric mobilization of non-conjugative resistance plasmids by a 24.5 megadalton conjugative plasmid of Neisseria gonorrhoeae. J Gen Microbiol. 1981;125(1):123–9. doi:10.1099/00221287-125-1-123.

    CAS  PubMed  Google Scholar 

  58. Laufs R, Kaulfers PM, Jahn G, Teschner U. Molecular characterization of a small Haemophilus influenzae plasmid specifying beta-lactamase and its relationship to R factors from Neisseria gonorrhoeae. J Gen Microbiol. 1979;111(1):223–31. doi:10.1099/00221287-111-1-223.

    Article  CAS  PubMed  Google Scholar 

  59. Roberts M, Elwell LP, Falkow S. Molecular characterization of two beta-lactamase-specifying plasmids isolated from Neisseria gonorrhoeae. J Bacteriol. 1977;131(2):557–63.

    CAS  PubMed  PubMed Central  Google Scholar 

  60. van Embden JD, van Klingeren B, Dessens-Kroon M, van Wijngaarden LJ. Emergence in the Netherlands of penicillinase-producing gonococci carrying “Africa” plasmid in combination with transfer plasmid. Lancet. 1981;1(8226):938.

    Article  PubMed  Google Scholar 

  61. Phillips I. Beta-lactamase-producing, penicillin-resistant gonococcus. Lancet. 1976;2(7987):656–7.

    Article  CAS  PubMed  Google Scholar 

  62. Ashford WA, Golash RG, Hemming VG. Penicillinase-producing Neisseria gonorrhoeae. Lancet. 1976;2(7987):657–8.

    Article  CAS  PubMed  Google Scholar 

  63. Lim KB, Rajan VS, Giam YC, Lui EO, Sng EH, Yeo KL. Two dose Augmentin treatment of acute gonorrhoea in men. Br J Vener Dis. 1984;60(3):161–3.

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Lim KB, Thirumoorthy T, Lee CT, Sng EH, Tan T. Three regimens of procaine penicillin G, Augmentin, and probenecid compared for treating acute gonorrhoea in men. Genitourin Med. 1986;62(2):82–5.

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Tapsall JW, Phillips EA, Morris LM. Chromosomally mediated intrinsic resistance to penicillin of penicillinase producing strains of Neisseria gonorrhoeae isolated in Sydney: guide to treatment with Augmentin. Genitourin Med. 1987;63(5):305–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  66. Hu M, Nandi S, Davies C, Nicholas RA. 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(10):4327–34. doi:10.1128/aac.49.10.4327-4334.2005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Faruki H, Kohmescher RN, McKinney WP, Sparling PF. A community-based outbreak of infection with penicillin-resistant Neisseria gonorrhoeae not producing penicillinase (chromosomally mediated resistance). N Engl J Med. 1985;313(10):607–11. doi:10.1056/nejm198509053131004.

    Article  CAS  PubMed  Google Scholar 

  68. Morse SA, Johnson SR, Biddle JW, Roberts MC. High-level tetracycline resistance in Neisseria gonorrhoeae is result of acquisition of streptococcal tetM determinant. Antimicrob Agents Chemother. 1986;30(5):664–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Gascoyne-Binzi DM, Heritage J, Hawkey PM. Nucleotide sequences of the tet(M) genes from the American and Dutch type tetracycline resistance plasmids of Neisseria gonorrhoeae. J Antimicrob Chemother. 1993;32(5):667–76.

    Article  CAS  PubMed  Google Scholar 

  70. Turner A, Gough KR, Leeming JP. Molecular epidemiology of tetM genes in Neisseria gonorrhoeae. Sex Transm Infect. 1999;75(1):60–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Djajakusumah T, Sudigdoadi S, Meheus A, Van Dyck E. Plasmid patterns and antimicrobial susceptibilities of Neisseria gonorrhoeae in Bandung, Indonesia. Trans R Soc Trop Med Hyg. 1998;92(1):105–7.

    Article  CAS  PubMed  Google Scholar 

  72. Ison CA, Dillon JA, Tapsall JW. The epidemiology of global antibiotic resistance among Neisseria gonorrhoeae and Haemophilus ducreyi. Lancet. 1998;351 Suppl 3:8–11.

    Article  PubMed  Google Scholar 

  73. Van Dyck E, Crabbe F, Nzila N, Bogaerts J, Munyabikali JP, Ghys P, Diallo M, Laga M. Increasing resistance of Neisseria gonorrhoeae in west and central Africa. Consequence on therapy of gonococcal infection. Sex Transm Dis. 1997;24(1):32–7.

    Article  PubMed  Google Scholar 

  74. West B, Changalucha J, Grosskurth H, Mayaud P, Gabone RM, Ka-Gina G, Mabey D. Antimicrobial susceptibility, auxotype and plasmid content of Neisseria gonorrhoeae in northern Tanzania: emergence of high level plasmid mediated tetracycline resistance. Genitourin Med. 1995;71(1):9–12.

    CAS  PubMed  PubMed Central  Google Scholar 

  75. WHO Western Pacific Region Gonococcal Antimicrobial Surveillance Programme. Surveillance of antibiotic susceptibility of Neisseria gonorrhoeae in the WHO western Pacific region 1992–1994. Genitourin Med. 1997;73(5):355–61.

    Google Scholar 

  76. Ho RI, Lai PH, Corman L, Ho J, Morse SA. Comparison of dihydrofolate reductases from trimethoprim- and sulfonamide-resistant strains of Neisseria gonorrhoeae. Sex Transm Dis. 1978;5(2):43–50.

    Article  CAS  PubMed  Google Scholar 

  77. Tapsall JW. Antibiotic resistance in Neisseria gonorrhoeae. Clin Infect Dis. 2005;41 Suppl 4:S263–8. doi:10.1086/430787.

    Article  CAS  PubMed  Google Scholar 

  78. Moran JS, Zenilman JM. Therapy for gonococcal infections: options in 1989. Rev Infect Dis. 1990;12 Suppl 6:S633–44.

    Article  PubMed  Google Scholar 

  79. Dan M. The use of fluoroquinolones in gonorrhoea: the increasing problem of resistance. Expert Opin Pharmacother. 2004;5(4):829–54. doi:10.1517/14656566.5.4.829.

    Article  CAS  PubMed  Google Scholar 

  80. Ghanem KG, Giles JA, Zenilman JM. Fluoroquinolone-resistant Neisseria gonorrhoeae: the inevitable epidemic. Infect Dis Clin North Am. 2005;19(2):351–65. doi:10.1016/j.idc.2005.03.005.

    Article  PubMed  Google Scholar 

  81. Update to CDC’s sexually transmitted diseases treatment guidelines, 2006: fluoroquinolones no longer recommended for treatment of gonococcal infections. MMWR Morb Mortal Wkly Rep. 2007;56(14):332–6.

    Google Scholar 

  82. Belland RJ, Morrison SG, Ison C, Huang WM. Neisseria gonorrhoeae acquires mutations in analogous regions of gyrA and parC in fluoroquinolone-resistant isolates. Mol Microbiol. 1994;14(2):371–80.

    Article  CAS  PubMed  Google Scholar 

  83. Deguchi T, Saito I, Tanaka M, Sato K, Deguchi K, Yasuda M, Nakano M, Nishino Y, Kanematsu E, Ozeki S, Kawada Y. Fluoroquinolone treatment failure in gonorrhea. Emergence of a Neisseria gonorrhoeae strain with enhanced resistance to fluoroquinolones. Sex Transm Dis. 1997;24(5):247–50.

    Article  CAS  PubMed  Google Scholar 

  84. Giles JA, Falconio J, Yuenger JD, Zenilman JM, Dan M, Bash MC. Quinolone resistance-determining region mutations and por type of Neisseria gonorrhoeae isolates: resistance surveillance and typing by molecular methodologies. J Infect Dis. 2004;189(11):2085–93. doi:10.1086/386312.

    Google Scholar 

  85. Tanaka M, Nakayama H, Haraoka M, Nagafuji T, Saika T, Kobayashi I. Analysis of quinolone resistance mechanisms in a sparfloxacin-resistant clinical isolate of Neisseria gonorrhoeae. Sex Transm Dis. 1998;25(9):489–93.

    Article  CAS  PubMed  Google Scholar 

  86. Tanaka M, Sagiyama K, Haraoka M, Saika T, Kobayashi I, Naito S. Genotypic evolution in a quinolone-resistant Neisseria gonorrhoeae isolate from a patient with clinical failure of levofloxacin treatment. Urol Int. 1999;62(1):64–8.

    Article  CAS  PubMed  Google Scholar 

  87. Tanaka M, Sakuma S, Takahashi K, Nagahuzi T, Saika T, Kobayashi I, Kumazawa J. Analysis of quinolone resistance mechanisms in Neisseria gonorrhoeae isolates in vitro. Sex Transm Infect. 1998;74(1):59–62.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Trees DL, Sandul AL, Whittington WL, Knapp JS. Identification of novel mutation patterns in the parC gene of ciprofloxacin-resistant isolates of Neisseria gonorrhoeae. Antimicrob Agents Chemother. 1998;42(8):2103–5.

    CAS  PubMed  PubMed Central  Google Scholar 

  89. Dewi BE, Akira S, Hayashi H, Ba-Thein W. High occurrence of simultaneous mutations in target enzymes and MtrRCDE efflux system in quinolone-resistant Neisseria gonorrhoeae. Sex Transm Dis. 2004;31(6):353–9.

    Article  CAS  PubMed  Google Scholar 

  90. Knapp JS, Fox KK, Trees DL, Whittington WL. Fluoroquinolone resistance in Neisseria gonorrhoeae. Emerg Infect Dis. 1997;3(1):33–9. doi:10.3201/eid0301.970104.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Shultz TR, Tapsall JW, White PA. Correlation of in vitro susceptibilities to newer quinolones of naturally occurring quinolone-resistant Neisseria gonorrhoeae strains with changes in GyrA and ParC. Antimicrob Agents Chemother. 2001;45(3):734–8. doi:10.1128/aac.45.3.734-738.2001.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Ison CA, Bindayna KM, Woodford N, Gill MJ, Easmon CS. Penicillin and cephalosporin resistance in gonococci. Genitourin Med. 1990;66(5):351–6.

    CAS  PubMed  PubMed Central  Google Scholar 

  93. 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(6):2117–22. doi:10.1128/aac.01604-06.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Takahata S, Senju N, Osaki Y, Yoshida T, Ida T. Amino acid substitutions in mosaic penicillin-binding protein 2 associated with reduced susceptibility to cefixime in clinical isolates of Neisseria gonorrhoeae. Antimicrob Agents Chemother. 2006;50(11):3638–45. doi:10.1128/aac.00626-06.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Tanaka M, Nakayama H, Huruya K, Konomi I, Irie S, Kanayama A, Saika T, Kobayashi I. 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(1):20–6. doi:10.1016/j.ijantimicag.2005.08.021.

    Article  CAS  PubMed  Google Scholar 

  96. Whiley DM, Jacobsson S, Tapsall JW, Nissen MD, Sloots TP, Unemo M. 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. 2010;65(12):2543–7. doi:10.1093/jac/dkq377.

    Article  CAS  PubMed  Google Scholar 

  97. Rice RJ, Biddle JW, JeanLouis YA, DeWitt WE, Blount JH, Morse SA. Chromosomally mediated resistance in Neisseria gonorrhoeae in the United States: results of surveillance and reporting, 1983–1984. J Infect Dis. 1986;153(2):340–5.

    Article  CAS  PubMed  Google Scholar 

  98. Schwebke JR, Whittington W, Rice RJ, Handsfield HH, Hale J, Holmes KK. Trends in susceptibility of Neisseria gonorrhoeae to ceftriaxone from 1985 through 1991. Antimicrob Agents Chemother. 1995;39(4):917–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Tomberg J, Unemo M, Davies C, Nicholas RA. 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(37):8062–70. doi:10.1021/bi101167x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Bowler LD, Zhang QY, Riou JY, Spratt BG. Interspecies recombination between the penA genes of Neisseria meningitidis and commensal Neisseria species during the emergence of penicillin resistance in N. meningitidis: natural events and laboratory simulation. J Bacteriol. 1994;176(2):333–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Ameyama S, Onodera S, Takahata M, Minami S, Maki N, Endo K, Goto H, Suzuki H, Oishi Y. 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(12):3744–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Chen M, Guo Q, Wang Y, Zou Y, Wang G, Zhang X, Xu X, Zhao M, Hu F, Qu D, Chen M, Wang M. Shifts in the antibiotic susceptibility, serogroups, and clonal complexes of Neisseria meningitidis in Shanghai, China: a time trend analysis of the pre-quinolone and quinolone Eras. PLoS Med. 2015;12(6), e1001838. doi:10.1371/journal.pmed.1001838, discussion e1001838.

    Article  PubMed  PubMed Central  Google Scholar 

  103. 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(31):590–4.

    Google Scholar 

  104. Unemo M, Golparian D, Hestner A. Ceftriaxone treatment failure of pharyngeal gonorrhoea verified by international recommendations, Sweden, July 2010. Euro Surveill 2011a;16(6): pii: 19792.

    Google Scholar 

  105. Boslego JW, Tramont EC, Takafuji ET, Diniega BM, Mitchell BS, Small JW, Khan WN, Stein DC. Effect of spectinomycin use on the prevalence of spectinomycin-resistant and of penicillinase-producing Neisseria gonorrhoeae. N Engl J Med. 1987;317(5):272–8. doi:10.1056/nejm198707303170504.

    Article  CAS  PubMed  Google Scholar 

  106. Maness MJ, Foster GC, Sparling PF. Ribosomal resistance to streptomycin and spectinomycin in Neisseria gonorrhoeae. J Bacteriol. 1974;120(3):1293–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  107. Gil-Setas A, Navascues-Ortega A, Beristain X. Spectinomycin in the treatment of gonorrhoea. Euro Surveill. 2010;15(19):pii/19568; author reply pii/19569.

    Google Scholar 

  108. Dowell D, Kirkcaldy RD. Effectiveness of gentamicin for gonorrhoea treatment: systematic review and meta-analysis. Sex Transm Infect. 2012;88(8):589–94. doi:10.1136/sextrans-2012-050604.

    Article  PubMed  Google Scholar 

  109. Daly CC, Hoffman I, Hobbs M, Maida M, Zimba D, Davis R, Mughogho G, Cohen MS. Development of an antimicrobial susceptibility surveillance system for Neisseria gonorrhoeae in Malawi: comparison of methods. J Clin Microbiol. 1997;35(11):2985–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  110. Lkhamsuren E, Shultz TR, Limnios EA, Tapsall JW. The antibiotic susceptibility of Neisseria gonorrhoeae isolated in Ulaanbaatar, Mongolia. Sex Transm Infect. 2001;77(3):218–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Slaney L, Chubb H, Ronald A, Brunham R. In-vitro activity of azithromycin, erythromycin, ciprofloxacin and norfloxacin against Neisseria gonorrhoeae, Haemophilus ducreyi, and Chlamydia trachomatis. J Antimicrob Chemother. 1990;25(Suppl. A):1–5.

    Google Scholar 

  112. Chisholm SA, Dave J, Ison CA. High-level azithromycin resistance occurs in Neisseria gonorrhoeae as a result of a single point mutation in the 23S rRNA genes. Antimicrob Agents Chemother. 2010;54(9):3812–6. doi:10.1128/aac.00309-10.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Ehret JM, Nims LJ, Judson FN. A clinical isolate of Neisseria gonorrhoeae with in vitro resistance to erythromycin and decreased susceptibility to azithromycin. Sex Transm Dis. 1996;23(4):270–2.

    Article  CAS  PubMed  Google Scholar 

  114. Rouquette-Loughlin CE, Balthazar JT, Shafer WM. Characterization of the MacA-MacB efflux system in Neisseria gonorrhoeae. J Antimicrob Chemother. 2005;56(5):856–60. doi:10.1093/jac/dki333.

    Article  CAS  PubMed  Google Scholar 

  115. Steingrimsson O, Olafsson JH, Thorarinsson H, Ryan RW, Johnson RB, Tilton RC. Azithromycin in the treatment of sexually transmitted disease. J Antimicrob Chemother. 1990;25(Suppl. A):109–14.

    Google Scholar 

  116. Tapsall JW, Shultz TR, Limnios EA, Donovan B, Lum G, Mulhall BP. Failure of azithromycin therapy in gonorrhea and discorrelation with laboratory test parameters. Sex Transm Dis. 1998;25(10):505–8.

    Article  CAS  PubMed  Google Scholar 

  117. Young H, Moyes A, McMillan A. Azithromycin and erythromycin resistant Neisseria gonorrhoeae following treatment with azithromycin. Int J STD AIDS. 1997;8(5):299–302.

    Article  CAS  PubMed  Google Scholar 

  118. Kirkcaldy RD, Weinstock HS, Moore PC, Philip SS, Wiesenfeld HC, Papp JR, Kerndt PR, Johnson S, Ghanem KG, Hook 3rd EW. The efficacy and safety of gentamicin plus azithromycin and gemifloxacin plus azithromycin as treatment of uncomplicated gonorrhea. Clin Infect Dis. 2014;59(8):1083–91. doi:10.1093/cid/ciu521.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Bhalla P, Sethi K, Reddy BS, Mathur MD. Antimicrobial susceptibility and plasmid profile of Neisseria gonorrhoeae in India (New Delhi). Sex Transm Infect. 1998;74(3):210–2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Tapsall JW. Use of a quality assurance scheme in a long-term multicentric study of antibiotic susceptibility of Neisseria gonorrhoeae. Genitourin Med. 1990;66(1):8–13.

    CAS  PubMed  PubMed Central  Google Scholar 

  121. Lahra MM. Surveillance of antibiotic resistance in Neisseria gonorrhoeae in the WHO Western Pacific and South East Asian Regions, 2010. Commun Dis Intell Q Rep. 2012;36(1):95–100.

    PubMed  Google Scholar 

  122. Surveillance of antibiotic resistance in Neisseria gonorrhoeae in the World Health Organization Western Pacific Region, 2003. Commun Dis Intell Q Rep. 2005;29(1):62–4.

    Google Scholar 

  123. Deguchi T, Yasuda M, Nakano M, Kanematsu E, Ozeki S, Nishino Y, Ezaki T, Maeda S, Saito I, Kawada Y. Rapid screening of point mutations of the Neisseria gonorrhoeae parC gene associated with resistance to quinolones. J Clin Microbiol. 1997;35(4):948–50.

    CAS  PubMed  PubMed Central  Google Scholar 

  124. Deguchi T, Yasuda M, Nakano M, Ozeki S, Ezaki T, Maeda S, Saito I, Kawada Y. Rapid detection of point mutations of the Neisseria gonorrhoeae gyrA gene associated with decreased susceptibilities to quinolones. J Clin Microbiol. 1996;34(9):2255–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  125. Deguchi T, Yasuda M, Nakano M, Ozeki S, Kanematsu E, Kawada Y, Ezaki T, Saito I. Uncommon occurrence of mutations in the gyrB gene associated with quinolone resistance in clinical isolates of Neisseria gonorrhoeae. Antimicrob Agents Chemother. 1996;40(10):2437–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  126. Vernel-Pauillac F, Merien F. A novel real-time duplex PCR assay for detecting penA and ponA genotypes in Neisseria gonorrhoeae: Comparison with phenotypes determined by the E-test. Clin Chem. 2006;52(12):2294–6. doi:10.1373/clinchem.2006.075309.

    Article  CAS  PubMed  Google Scholar 

  127. Giles J, Hardick J, Yuenger J, Dan M, Reich K, Zenilman J. Use of applied biosystems 7900HT sequence detection system and Taqman assay for detection of quinolone-resistant Neisseria gonorrhoeae. J Clin Microbiol. 2004;42(7):3281–3. doi:10.1128/jcm.42.7.3281-3283.2004.

    Google Scholar 

  128. Kilmarx PH, Knapp JS, Xia M, St Louis ME, Neal SW, Sayers D, Doyle LJ, Roberts MC, Whittington WL. Intercity spread of gonococci with decreased susceptibility to fluoroquinolones: a unique focus in the United States. J Infect Dis. 1998;177(3):677–82.

    Article  CAS  PubMed  Google Scholar 

  129. van Klingeren B, Ansink-Schipper MC, Dessens-Kroon M, Verheuvel M. Relationship between auxotype, plasmid pattern and susceptibility to antibiotics in penicillinase-producing Neisseria gonorrhoeae. J Antimicrob Chemother. 1985;16(2):143–7.

    Article  PubMed  Google Scholar 

  130. Rothenberg R, Voigt R. Epidemiologic aspects of control of penicillinase-producing Neisseria gonorrhoeae. Sex Transm Dis. 1988;15(4):211–6.

    Article  CAS  PubMed  Google Scholar 

  131. Increases in fluoroquinolone-resistant Neisseria gonorrhoeae—Hawaii and California, 2001. MMWR Morb Mortal Wkly Rep. 2002;51(46):1041–4.

    Google Scholar 

  132. Surveillance of antibiotic resistance in Neisseria gonorrhoeae in the WHO Western Pacific Region, 2002. Commun Dis Intell Q Rep. 2003;27(4):488–91.

    Google Scholar 

  133. Tanaka M, Nakayama H, Haraoka M, Saika T. Antimicrobial resistance of Neisseria gonorrhoeae and high prevalence of ciprofloxacin-resistant isolates in Japan, 1993 to 1998. J Clin Microbiol. 2000;38(2):521–5.

    CAS  PubMed  PubMed Central  Google Scholar 

  134. Tapsall JW, Shultz TR, Phillips EA. Characteristics of Neisseria gonorrhoeae isolated in Australia showing decreased sensitivity to quinolone antibiotics. Pathology. 1992;24(1):27–31.

    Article  CAS  PubMed  Google Scholar 

  135. Trees DL, Sandul AL, Neal SW, Higa H, Knapp JS. Molecular epidemiology of Neisseria gonorrhoeae exhibiting decreased susceptibility and resistance to ciprofloxacin in Hawaii, 1991–1999. Sex Transm Dis. 2001;28(6):309–14.

    Article  CAS  PubMed  Google Scholar 

  136. Palmer HM, Leeming JP, Turner A. Investigation of an outbreak of ciprofloxacin-resistant Neisseria gonorrhoeae using a simplified opa-typing method. Epidemiol Infect. 2001;126(2):219–24.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Tapsall JW, Limnios EA, Shultz TR. Continuing evolution of the pattern of quinolone resistance in Neisseria gonorrhoeae isolated in Sydney, Australia. Sex Transm Dis. 1998;25(8):415–7.

    Article  CAS  PubMed  Google Scholar 

  138. Unemo M, Sjostrand A, Akhras M, Gharizadeh B, Lindback E, Pourmand N, Wretlind B, Fredlund H. Molecular characterization of Neisseria gonorrhoeae identifies transmission and resistance of one ciprofloxacin-resistant strain. APMIS. 2007;115(3):231–41. doi:10.1111/j.1600-0463.2007.apm_487.x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Yagupsky P, Schahar A, Peled N, Porat N, Trefler R, Dan M, Keness Y, Block C. Increasing incidence of gonorrhea in Israel associated with countrywide dissemination of a ciprofloxacin-resistant strain. Eur J Clin Microbiol Infect Dis. 2002;21(5):368–72. doi:10.1007/s10096-002-0717-1.

    Article  CAS  PubMed  Google Scholar 

  140. Bignell C, Fitzgerald M. UK national guideline for the management of gonorrhoea in adults, 2011. Int J STD AIDS. 2011;22(10):541–7. doi:10.1258/ijsa.2011.011267.

    Article  CAS  PubMed  Google Scholar 

  141. Bignell C, Unemo M. 2012 European guideline on the diagnosis and treatment of gonorrhoea in adults. Int J STD AIDS. 2013;24(2):85–92. doi:10.1177/0956462412472837.

    Article  CAS  PubMed  Google Scholar 

  142. Brooks B, Patel R. The 2012 International Union against Sexually Transmitted Infections European Collaborative Clinical Group report on the diagnosis and management of Neisseria gonorrhoeae infections in Europe. Int J STD AIDS. 2013;24(6):419–22. doi:10.1177/0956462413476269.

    Article  CAS  PubMed  Google Scholar 

  143. Tapsall JW, Limnios EA, Abu Bakar HM, Darussalam B, Ping YY, Buadromo EM, Kumar P, Singh S, Lo J, Bala M, Risbud A, Deguchi T, Tanaka M, Watanabe Y, Lee K, Chong Y, Noikaseumsy S, Phouthavane T, Sam IC, Tundev O, Lwin KM, Eh PH, Goarant C, Goursaud R, Bathgate T, Brokenshire M, Latorre L, Velemu E, Carlos C, Leano S, Telan EO, Goh SS, Koh ST, Ngan C, Tan AL, Mananwatte S, Piyanoot N, Lokpichat S, Sirivongranson P, Fakahau M, Sitanilei H, le Hung V. Surveillance of antibiotic resistance in Neisseria gonorrhoeae in the WHO Western Pacific and South East Asian regions, 2007–2008. Commun Dis Intell Q Rep. 2010;34(1):1–7.

    CAS  PubMed  Google Scholar 

  144. Workowski KA, Bolan GA, Centers for Disease C, Prevention. Sexually transmitted diseases treatment guidelines, 2015. MMWR Recomm Rep. 2015;64 (RR-03):1–137

    Google Scholar 

  145. World Health Organization. Guidelines for the management of sexually transmitted infections. Geneva: World Health Organization; 2003.

    Google Scholar 

  146. Backman M, Jacobson K, Ringertz S. The virgin population of Neisseria gonorrhoeae in Stockholm has decreased and antimicrobial resistance is increasing. Genitourin Med. 1995;71(4):234–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  147. Marrazzo JM. Sexual tourism: implications for travelers and the destination culture. Infect Dis Clin North Am. 2005;19(1):103–20. doi:10.1016/j.idc.2004.10.008.

    Article  PubMed  Google Scholar 

  148. Gorwitz RJ, Nakashima AK, Moran JS, Knapp JS, The Gonococcal Isolate Surveillance Project Study Group. Sentinel surveillance for antimicrobial resistance in Neisseria gonorrhoeae—United States, 1988–1991. MMWR CDC Surveill Summ. 1993;42(3):29–39.

    CAS  PubMed  Google Scholar 

  149. Ison CA, Town K, Obi C, Chisholm S, Hughes G, Livermore DM, Lowndes CM. Decreased susceptibility to cephalosporins among gonococci: data from the Gonococcal Resistance to Antimicrobials Surveillance Programme (GRASP) in England and Wales, 2007–2011. Lancet Infect Dis. 2013;13(9):762–8. doi:10.1016/s1473-3099(13)70143-9.

    Article  CAS  PubMed  Google Scholar 

  150. Lahra MM. Australian Gonococcal Surveillance Programme annual report, 2013. Commun Dis Intell Q Rep. 2015;39(1):E137–45.

    PubMed  Google Scholar 

  151. Members of the Australian Gonococcal Surveillance Programme. Penicillin sensitivity of gonococci in Australia: development of Australian gonococcal surveillance programme. Br J Vener Dis. 1984;60(4):226–30.

    Google Scholar 

  152. Paine TC, Fenton KA, Herring A, Turner A, Ison C, Martin I, Robinson A, Kinghorn G. GRASP: a new national sentinel surveillance initiative for monitoring gonococcal antimicrobial resistance in England and Wales. Sex Transm Infect. 2001;77(6):398–401.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Dillon JA, Li H, Sealy J, Ruben M, Prabhakar P. Antimicrobial susceptibility of Neisseria gonorrhoeae isolates from three Caribbean countries: Trinidad, Guyana, and St. Vincent Sex Transm Dis. 2001;28(9):508–14.

    Article  CAS  PubMed  Google Scholar 

  154. World Health Organization. Baseline report on global sexually transmitted infection surveillance 2012. World Health Organization; 2013.

    Google Scholar 

  155. World Health Organization. Progress report of the implementation of the global strategy for prevention and control of sexually transmitted infections: 2006–2015. Geneva: World Health Organization; 2015.

    Google Scholar 

  156. Mayaud P, Hawkes S, Mabey D. Advances in control of sexually transmitted diseases in developing countries. Lancet. 1998;351 Suppl 3:29–32.

    Article  PubMed  Google Scholar 

  157. Zenilman JM, Deal CD. Gonorrhea: epidemiology, control, and prevention. In: Stanberry LR, Bernstein DI, editors. Sexually transmitted diseases-vaccines, prevention and control. London: Academic; 2000. p. 369–85.

    Chapter  Google Scholar 

  158. Annual report of the Australian Gonococcal Surveillance Programme, 2004. Commun Dis Intell Q Rep. 2005;29(2):137–42.

    Google Scholar 

  159. Lyss SB, Kamb ML, Peterman TA, Moran JS, Newman DR, Bolan G, Douglas Jr JM, Iatesta M, Malotte CK, Zenilman JM, Ehret J, Gaydos C, Newhall WJ. Chlamydia trachomatis among patients infected with and treated for Neisseria gonorrhoeae in sexually transmitted disease clinics in the United States. Ann Intern Med. 2003;139(3):178–85.

    Article  PubMed  Google Scholar 

  160. Miller WC, Zenilman JM. Epidemiology of chlamydial infection, gonorrhea, and trichomoniasis in the United States—2005. Infect Dis Clin North Am. 2005;19(2):281–96. doi:10.1016/j.idc.2005.04.001.

    Article  PubMed  Google Scholar 

  161. Schachter J. Chlamydial infections (second of three parts). N Engl J Med. 1978;298(9):490–5. doi:10.1056/nejm197803022980905.

    Article  CAS  PubMed  Google Scholar 

  162. Harry C. The management of uncomplicated adult gonococcal infection: should test of cure still be routine in patients attending genitourinary medicine clinics? Int J STD AIDS. 2004;15(7):453–8. doi:10.1258/0956462041211252.

    Article  CAS  PubMed  Google Scholar 

  163. Tapsall JW, Limnios EA, Thacker C, Donovan B, Lynch SD, Kirby LJ, Wise KA, Carmody CJ. High-level quinolone resistance in Neisseria gonorrhoeae: a report of two cases. Sex Transm Dis. 1995;22(5):310–1.

    Article  CAS  PubMed  Google Scholar 

  164. Bignell CJ. BASHH guideline for gonorrhoea. Sex Transm Infect. 2004;80(5):330–1. doi:10.1136/sti.2004.012781.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  165. Handsfield HH, Dalu ZA, Martin DH, Douglas Jr JM, McCarty JM, Schlossberg D, Azithromycin Gonorrhea Study Group. Multicenter trial of single-dose azithromycin vs. ceftriaxone in the treatment of uncomplicated gonorrhea. Sex Transm Dis. 1994;21(2):107–11.

    Article  CAS  PubMed  Google Scholar 

  166. Dillon JA, Rubabaza JP, Benzaken AS, Sardinha JC, Li H, Bandeira MG, dos Santos Fernando Filho E. Reduced susceptibility to azithromycin and high percentages of penicillin and tetracycline resistance in Neisseria gonorrhoeae isolates from Manaus, Brazil, 1998. Sex Transm Dis. 2001;28(9):521–6.

    Article  CAS  PubMed  Google Scholar 

  167. Kamwendo F, Forslin L, Bodin L, Danielsson D. Decreasing incidences of gonorrhea- and chlamydia-associated acute pelvic inflammatory disease. A 25-year study from an urban area of central Sweden. Sex Transm Dis. 1996;23(5):384–91.

    Article  CAS  PubMed  Google Scholar 

  168. Kamwendo F, Forslin L, Bodin L, Danielsson D. Programmes to reduce pelvic inflammatory disease—the Swedish experience. Lancet. 1998;351 Suppl 3:25–8.

    Article  PubMed  Google Scholar 

  169. Kamwendo F, Forslin L, Bodin L, Danielsson D. Epidemiology of ectopic pregnancy during a 28 year period and the role of pelvic inflammatory disease. Sex Transm Infect. 2000;76(1):28–32.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  170. Over M, Piot P. Human immunodeficiency virus infection and other sexually transmitted diseases in developing countries: public health importance and priorities for resource allocation. J Infect Dis. 1996;174 Suppl 2:S162–75.

    Article  PubMed  Google Scholar 

  171. Grosskurth H, Mosha F, Todd J, Mwijarubi E, Klokke A, Senkoro K, Mayaud P, Changalucha J, Nicoll A, ka-Gina G, et al. Impact of improved treatment of sexually transmitted diseases on HIV infection in rural Tanzania: randomised controlled trial. Lancet. 1995;346(8974):530–6.

    Article  CAS  PubMed  Google Scholar 

  172. Simonsen GS, Tapsall JW, Allegranzi B, Talbot EA, Lazzari S. The antimicrobial resistance containment and surveillance approach—a public health tool. Bull World Health Organ. 2004;82(12):928–34.

    PubMed  Google Scholar 

  173. Increases in unsafe sex and rectal gonorrhea among men who have sex with men--San Francisco, California, 1994–1997. MMWR Morb Mortal Wkly Rep. 1999;48(3):45–8.

    Google Scholar 

  174. Katz AR, Lee MV, Ohye RG, Whiticar PM, Effler PV. Ciprofloxacin resistance in Neisseria gonorrhoeae: trends in Hawaii, 1997–2002. Lancet. 2003;362(9382):495. doi:10.1016/s0140-6736(03)14084-6.

    Article  PubMed  Google Scholar 

  175. Enhanced surveillance of epidemic meningococcal meningitis in Africa: a three-year experience. Wkly Epidemiol Rec. 2005;80(37):313–20.

    Google Scholar 

  176. Xie O, Pollard AJ, Mueller JE, Norheim G. Emergence of serogroup X meningococcal disease in Africa: need for a vaccine. Vaccine. 2013;31(27):2852–61. doi:10.1016/j.vaccine.2013.04.036.

    Article  PubMed  Google Scholar 

  177. Cohn AC, MacNeil JR, Harrison LH, Hatcher C, Theodore J, Schmidt M, Pondo T, Arnold KE, Baumbach J, Bennett N, Craig AS, Farley M, Gershman K, Petit S, Lynfield R, Reingold A, Schaffner W, Shutt KA, Zell ER, Mayer LW, Clark T, Stephens D, Messonnier NE. Changes in Neisseria meningitidis disease epidemiology in the United States, 1998–2007: implications for prevention of meningococcal disease. Clin Infect Dis. 2010;50(2):184–91. doi:10.1086/649209.

    Article  PubMed  Google Scholar 

  178. Ladhani SN, Flood JS, Ramsay ME, Campbell H, Gray SJ, Kaczmarski EB, Mallard RH, Guiver M, Newbold LS, Borrow R. Invasive meningococcal disease in England and Wales: implications for the introduction of new vaccines. Vaccine. 2012;30(24):3710–6. doi:10.1016/j.vaccine.2012.03.011.

    Article  PubMed  Google Scholar 

  179. Greenfield S, Sheehe PR, Feldman HA. Meningococcal carriage in a population of “normal” families. J Infect Dis. 1971;123(1):67–73.

    Article  CAS  PubMed  Google Scholar 

  180. Antignac A, Ducos-Galand M, Guiyoule A, Pires R, Alonso JM, Taha MK. Neisseria meningitidis strains isolated from invasive infections in France (1999–2002): phenotypes and antibiotic susceptibility patterns. Clin Infect Dis. 2003;37(7):912–20. doi:10.1086/377739.

    Article  PubMed  Google Scholar 

  181. Trotter CL, Fox AJ, Ramsay ME, Sadler F, Gray SJ, Mallard R, Kaczmarski EB. Fatal outcome from meningococcal disease—an association with meningococcal phenotype but not with reduced susceptibility to benzylpenicillin. J Med Microbiol. 2002;51(10):855–60. doi:10.1099/0022-1317-51-10-855.

    Article  CAS  PubMed  Google Scholar 

  182. Schwentker FF, Gelman S, Long PH. Landmark article April 24, 1937. The treatment of meningococcic meningitis with sulfanilamide. Preliminary report. By Francis F. Schwentker, Sidney Gelman, and Perrin H. Long. J Am Med Assoc. 1984;251(6):788–90.

    Article  CAS  Google Scholar 

  183. Meningococcal infections. In: Kimberlin DW, Brady MT, Jackson MA, Long SS, editors. Red book, 2015 Report of the Committee on Infectious Diseases, 30th ed. American Academy of Pediatrics Elk Grove Village; 2015. p. 547–58.

    Google Scholar 

  184. Nathan N, Borel T, Djibo A, Evans D, Djibo S, Corty JF, Guillerm M, Alberti KP, Pinoges L, Guerin PJ, Legros D. Ceftriaxone as effective as long-acting chloramphenicol in short-course treatment of meningococcal meningitis during epidemics: a randomised non-inferiority study. Lancet. 2005;366(9482):308–13. doi:10.1016/s0140-6736(05)66792-x.

    Article  CAS  PubMed  Google Scholar 

  185. Aguilera JF, Perrocheau A, Meffre C, Hahne S. Outbreak of serogroup W135 meningococcal disease after the Hajj pilgrimage, Europe, 2000. Emerg Infect Dis. 2002;8(8):761–7. doi:10.3201/eid0805.010422.

    Article  PubMed  PubMed Central  Google Scholar 

  186. Memish Z, Al Hakeem R, Al Neel O, Danis K, Jasir A, Eibach D. Laboratory-confirmed invasive meningococcal disease: effect of the Hajj vaccination policy, Saudi Arabia, 1995–2011. Euro Surveill. 2013;18(37).

    Google Scholar 

  187. Auckland C, Gray S, Borrow R, Andrews N, Goldblatt D, Ramsay M, Miller E. Clinical and immunologic risk factors for meningococcal C conjugate vaccine failure in the United Kingdom. J Infect Dis. 2006;194(12):1745–52. doi:10.1086/509619.

    Article  CAS  PubMed  Google Scholar 

  188. De Wals P, Trottier P, Pepin J. Relative efficacy of different immunization schedules for the prevention of serogroup C meningococcal disease: a model-based evaluation. Vaccine. 2006;24(17):3500–4. doi:10.1016/j.vaccine.2006.02.010.

    Article  PubMed  CAS  Google Scholar 

  189. Trotter CL, Andrews NJ, Kaczmarski EB, Miller E, Ramsay ME. Effectiveness of meningococcal serogroup C conjugate vaccine 4 years after introduction. Lancet. 2004;364(9431):365–7. doi:10.1016/s0140-6736(04)16725-1.

    Article  CAS  PubMed  Google Scholar 

  190. Frasch CE. Recent developments in Neisseria meningitidis group A conjugate vaccines. Expert Opin Biol Ther. 2005;5(2):273–80. doi:10.1517/14712598.5.2.273.

    Article  CAS  PubMed  Google Scholar 

  191. Kshirsagar N, Mur N, Thatte U, Gogtay N, Viviani S, Preziosi MP, Elie C, Findlow H, Carlone G, Borrow R, Parulekar V, Plikaytis B, Kulkarni P, Imbault N, LaForce FM. Safety, immunogenicity, and antibody persistence of a new meningococcal group A conjugate vaccine in healthy Indian adults. Vaccine. 2007;25 Suppl 1:A101–7. doi:10.1016/j.vaccine.2007.04.050.

    Article  CAS  PubMed  Google Scholar 

  192. Meyer SA, Kambou JL, Cohn A, Goodson JL, Flannery B, Medah I, Messonnier N, Novak R, Diomande F, Djingarey MH, Clark TA, Yameogo I, Fall A, Wannemuehler K. Serogroup A meningococcal conjugate (PsA-TT) vaccine coverage and measles vaccine coverage in Burkina Faso—implications for introduction of PsA-TT into the Expanded Programme on Immunization. Vaccine. 2015;33(12):1492–8. doi:10.1016/j.vaccine.2015.01.043.

    Article  CAS  PubMed  Google Scholar 

  193. Program for Appropriate Technology in Health. Meningitis Vaccine Project; 2003–2015.

    Google Scholar 

  194. Daugla DM, Gami JP, Gamougam K, Naibei N, Mbainadji L, Narbe M, Toralta J, Kodbesse B, Ngadoua C, Coldiron ME, Fermon F, Page AL, Djingarey MH, Hugonnet S, Harrison OB, Rebbetts LS, Tekletsion Y, Watkins ER, Hill D, Caugant DA, Chandramohan D, Hassan-King M, Manigart O, Nascimento M, Woukeu A, Trotter C, Stuart JM, Maiden MC, Greenwood BM. Effect of a serogroup A meningococcal conjugate vaccine (PsA-TT) on serogroup A meningococcal meningitis and carriage in Chad: a community study [corrected]. Lancet. 2014;383(9911):40–7. doi:10.1016/s0140-6736(13)61612-8.

    Article  CAS  PubMed  Google Scholar 

  195. Kristiansen PA, Ba AK, Ouedraogo AS, Sanou I, Ouedraogo R, Sangare L, Diomande F, Kandolo D, Saga IM, Misegades L, Clark TA, Preziosi MP, Caugant DA. Persistent low carriage of serogroup A Neisseria meningitidis two years after mass vaccination with the meningococcal conjugate vaccine, MenAfriVac. BMC Infect Dis. 2014;14:663. doi:10.1186/s12879-014-0663-4.

    Article  PubMed  PubMed Central  Google Scholar 

  196. Kristiansen PA, Diomande F, Ba AK, Sanou I, Ouedraogo AS, Ouedraogo R, Sangare L, Kandolo D, Ake F, Saga IM, Clark TA, Misegades L, Martin SW, Thomas JD, Tiendrebeogo SR, Hassan-King M, Djingarey MH, Messonnier NE, Preziosi MP, Laforce FM, Caugant DA. Impact of the serogroup A meningococcal conjugate vaccine, MenAfriVac, on carriage and herd immunity. Clin Infect Dis. 2013;56(3):354–63. doi:10.1093/cid/cis892.

    Article  CAS  PubMed  Google Scholar 

  197. Martin DR, Walker SJ, Baker MG, Lennon DR. New Zealand epidemic of meningococcal disease identified by a strain with phenotype B:4:P1.4. J Infect Dis. 1998;177(2):497–500.

    Article  CAS  PubMed  Google Scholar 

  198. Bjune G, Gronnesby JK, Hoiby EA, Closs O, Nokleby H. Results of an efficacy trial with an outer membrane vesicle vaccine against systemic serogroup B meningococcal disease in Norway. NIPH Ann. 1991;14(2):125–30 [discussion 130-122].

    CAS  PubMed  Google Scholar 

  199. Bjune G, Hoiby EA, Gronnesby JK, Arnesen O, Fredriksen JH, Halstensen A, Holten E, Lindbak AK, Nokleby H, Rosenqvist E, et al. Effect of outer membrane vesicle vaccine against group B meningococcal disease in Norway. Lancet. 1991;338(8775):1093–6.

    Article  CAS  PubMed  Google Scholar 

  200. Boslego J, Garcia J, Cruz C, Zollinger W, Brandt B, Ruiz S, Martinez M, Arthur J, Underwood P, Silva W, et al. Efficacy, safety, and immunogenicity of a meningococcal group B (15:P1.3) outer membrane protein vaccine in Iquique, Chile. Chilean National Committee for Meningococcal Disease. Vaccine. 1995;13(9):821–9.

    Article  CAS  PubMed  Google Scholar 

  201. Milagres LG, Ramos SR, Sacchi CT, Melles CE, Vieira VS, Sato H, Brito GS, Moraes JC, Frasch CE. Immune response of Brazilian children to a Neisseria meningitidis serogroup B outer membrane protein vaccine: comparison with efficacy. Infect Immun. 1994;62(10):4419–24.

    CAS  PubMed  PubMed Central  Google Scholar 

  202. Oster P, O’Hallahan J, Aaberge I, Tilman S, Ypma E, Martin D. Immunogenicity and safety of a strain-specific MenB OMV vaccine delivered to under 5-year olds in New Zealand. Vaccine. 2007;25(16):3075–9. doi:10.1016/j.vaccine.2007.01.023.

    Article  CAS  PubMed  Google Scholar 

  203. Sierra GV, Campa HC, Varcacel NM, Garcia IL, Izquierdo PL, Sotolongo PF, Casanueva GV, Rico CO, Rodriguez CR, Terry MH. Vaccine against group B Neisseria meningitidis: protection trial and mass vaccination results in Cuba. NIPH Ann. 1991;14(2):195–207 [discussion 208-110].

    CAS  PubMed  Google Scholar 

  204. Thornton V, Lennon D, Rasanathan K, O’Hallahan J, Oster P, Stewart J, Tilman S, Aaberge I, Feiring B, Nokleby H, Rosenqvist E, White K, Reid S, Mulholland K, Wakefield MJ, Martin D. Safety and immunogenicity of New Zealand strain meningococcal serogroup B OMV vaccine in healthy adults: beginning of epidemic control. Vaccine. 2006;24(9):1395–400. doi:10.1016/j.vaccine.2005.09.043.

    Article  CAS  PubMed  Google Scholar 

  205. Wong S, Lennon D, Jackson C, Stewart J, Reid S, Crengle S, Tilman S, Aaberge I, O’Hallahan J, Oster P, Mulholland K, Martin D. New Zealand epidemic strain meningococcal B outer membrane vesicle vaccine in children aged 16–24 months. Pediatr Infect Dis J. 2007;26(4):345–50. doi:10.1097/01.inf.0000258697.05341.2c.

    Article  PubMed  Google Scholar 

  206. Feavers I, Griffiths E, Baca-Estrada M, Knezevic I, Zhou T. WHO/Health Canada meeting on regulatory considerations for evaluation and licensing of new meningococcal Group B vaccines, Ottawa, Canada, 3–4 October 2011. Biologicals. 2012;40(6):507–16. doi:10.1016/j.biologicals.2012.09.008.

    Article  PubMed  Google Scholar 

  207. McQuaid F, Snape MD. Will booster doses be required for serogroup B meningococcal vaccine? Expert Rev Vaccines. 2014;13(3):313–5. doi:10.1586/14760584.2014.878654.

    Article  CAS  PubMed  Google Scholar 

  208. Poolman JT, Richmond P. Multivalent meningococcal serogroup B vaccines: challenges in predicting protection and measuring effectiveness. Expert Rev Vaccines. 2015;14(9):1277–87. doi:10.1586/14760584.2015.1071670.

    CAS  PubMed  Google Scholar 

  209. Snape MD, Saroey P, John TM, Robinson H, Kelly S, Gossger N, Yu LM, Wang H, Toneatto D, Dull PM, Pollard AJ. Persistence of bactericidal antibodies following early infant vaccination with a serogroup B meningococcal vaccine and immunogenicity of a preschool booster dose. CMAJ. 2013;185(15):E715–24. doi:10.1503/cmaj.130257.

    Article  PubMed  PubMed Central  Google Scholar 

  210. Tirani M, Meregaglia M, Melegaro A. Health and economic outcomes of introducing the new MenB vaccine (Bexsero) into the Italian routine infant immunisation programme. PLoS ONE. 2015;10(4), e0123383. doi:10.1371/journal.pone.0123383.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  211. Antignac A, Boneca IG, Rousselle JC, Namane A, Carlier JP, Vazquez JA, Fox A, Alonso JM, Taha MK. Correlation between alterations of the penicillin-binding protein 2 and modifications of the peptidoglycan structure in Neisseria meningitidis with reduced susceptibility to penicillin G. J Biol Chem. 2003;278(34):31529–35. doi:10.1074/jbc.M304607200.

    Article  CAS  PubMed  Google Scholar 

  212. Harcourt BH, Anderson RD, Wu HM, Cohn AC, MacNeil JR, Taylor TH, Wang X, Clark TA, Messonnier NE, Mayer LW. Population-based surveillance of Neisseria meningitidis antimicrobial resistance in the United States. Open Forum Infect Dis. 2015;2(3):ofv117. doi:10.1093/ofid/ofv117.

  213. Arreaza L, de La Fuente L, Vazquez JA. Antibiotic susceptibility patterns of Neisseria meningitidis isolates from patients and asymptomatic carriers. Antimicrob Agents Chemother. 2000;44(6):1705–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  214. Saez-Nieto JA, Lujan R, Berron S, Campos J, Vinas M, Fuste C, Vazquez JA, Zhang QY, Bowler LD, Martinez-Suarez JV, et al. Epidemiology and molecular basis of penicillin-resistant Neisseria meningitidis in Spain: a 5-year history (1985–1989). Clin Infect Dis. 1992;14(2):394–402.

    Article  CAS  PubMed  Google Scholar 

  215. Thulin S, Olcen P, Fredlund H, Unemo M. Total variation in the penA gene of Neisseria meningitidis: correlation between susceptibility to beta-lactam antibiotics and penA gene heterogeneity. Antimicrob Agents Chemother. 2006;50(10):3317–24. doi:10.1128/aac.00353-06.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  216. Orus P, Vinas M. Mechanisms other than penicillin-binding protein-2 alterations may contribute to moderate penicillin resistance in Neisseria meningitidis. Int J Antimicrob Agents. 2001;18(2):113–9.

    Article  CAS  PubMed  Google Scholar 

  217. Rouquette-Loughlin C, Dunham SA, Kuhn M, Balthazar JT, Shafer WM. The NorM efflux pump of Neisseria gonorrhoeae and Neisseria meningitidis recognizes antimicrobial cationic compounds. J Bacteriol. 2003;185(3):1101–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  218. Saez-Nieto JA, Fontanals D, Garcia de Jalon J, Martinez de Artola V, Pena P, Morera MA, Verdaguer R, Sanfeliu I, Belio-Blasco C, Perez-Saenz JL, et al. Isolation of Neisseria meningitidis strains with increase of penicillin minimal inhibitory concentrations. Epidemiol Infect. 1987;99(2):463–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  219. Vazquez JA, Enriquez R, Abad R, Alcala B, Salcedo C, Arreaza L. Antibiotic resistant meningococci in Europe: any need to act? FEMS Microbiol Rev. 2007;31(1):64–70. doi:10.1111/j.1574-6976.2006.00049.x.

    Article  CAS  PubMed  Google Scholar 

  220. Taha MK, Vazquez JA, Hong E, Bennett DE, Bertrand S, Bukovski S, Cafferkey MT, Carion F, Christensen JJ, Diggle M, Edwards G, Enriquez R, Fazio C, Frosch M, Heuberger S, Hoffmann S, Jolley KA, Kadlubowski M, Kechrid A, Kesanopoulos K, Kriz P, Lambertsen L, Levenet I, Musilek M, Paragi M, Saguer A, Skoczynska A, Stefanelli P, Thulin S, Tzanakaki G, Unemo M, Vogel U, Zarantonelli ML. Target gene sequencing to characterize the penicillin G susceptibility of Neisseria meningitidis. Antimicrob Agents Chemother. 2007;51(8):2784–92. doi:10.1128/aac.00412-07.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  221. Zarantonelli ML, Skoczynska A, Antignac A, El Ghachi M, Deghmane AE, Szatanik M, Mulet C, Werts C, Peduto L, d'Andon MF, Thouron F, Nato F, Lebourhis L, Philpott DJ, Girardin SE, Vives FL, Sansonetti P, Eberl G, Pedron T, Taha MK, Boneca IG. Penicillin resistance compromises Nod1-dependent proinflammatory activity and virulence fitness of neisseria meningitidis. Cell Host Microbe. 2013;13(6):735–45. doi:10.1016/j.chom.2013.04.016.

    Article  CAS  PubMed  Google Scholar 

  222. Tondella ML, Rosenstein NE, Mayer LW, Tenover FC, Stocker SA, Reeves MW, Popovic T. Lack of evidence for chloramphenicol resistance in Neisseria meningitidis, Africa. Emerg Infect Dis. 2001;7(1):163–4. doi:10.3201/eid0701.700163.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  223. Galimand M, Gerbaud G, Guibourdenche M, Riou JY, Courvalin P. High-level chloramphenicol resistance in Neisseria meningitidis. N Engl J Med. 1998;339(13):868–74. doi:10.1056/nejm199809243391302.

  224. Feldman HA. Sulfonamide-resistant meningococci. Annu Rev Med. 1967;18:495–506. doi:10.1146/annurev.me.18.020167.002431.

    Article  CAS  PubMed  Google Scholar 

  225. Kristiansen BE, Radstrom P, Jenkins A, Ask E, Facinelli B, Skold O. Cloning and characterization of a DNA fragment that confers sulfonamide resistance in a serogroup B, serotype 15 strain of Neisseria meningitidis. Antimicrob Agents Chemother. 1990;34(11):2277–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  226. Cooper ER, Ellison 3rd RT, Smith GS, Blaser MJ, Reller LB, Paisley JW. Rifampin-resistant meningococcal disease in a contact patient given prophylactic rifampin. J Pediatr. 1986;108(1):93–6.

    Article  CAS  PubMed  Google Scholar 

  227. Yagupsky P, Ashkenazi S, Block C. Rifampicin-resistant meningococci causing invasive disease and failure of chemoprophylaxis. Lancet. 1993;341(8853):1152–3.

    Article  CAS  PubMed  Google Scholar 

  228. Tapsall JW, Shultz T, Limnios E, Munro R, Mercer J, Porritt R, Griffith J, Hogg G, Lum G, Lawrence A, Hansman D, Collignon P, Southwell P, Ott K, Gardam M, Richardson CJ, Bates J, Murphy D, Smith H. Surveillance of antibiotic resistance in invasive isolates of Neisseria meningitidis in Australia 1994–1999. Pathology. 2001;33(3):359–61.

    Article  CAS  PubMed  Google Scholar 

  229. Rosenstein NE, Stocker SA, Popovic T, Tenover FC, Perkins BA. Antimicrobial resistance of Neisseria meningitidis in the United States, 1997. The Active Bacterial Core Surveillance (ABCs) Team. Clin Infect Dis. 2000;30(1):212–3. doi:10.1086/313599.

    Article  CAS  PubMed  Google Scholar 

  230. Delaune D, Andriamanantena D, Merens A, Viant E, Aoun O, Ceppa F, Taha MK, Rapp C. Management of a rifampicin-resistant meningococcal infection in a teenager. Infection. 2013;41(3):705–8. doi:10.1007/s15010-013-0418-y.

    Article  CAS  PubMed  Google Scholar 

  231. Mounchetrou Njoya I, Deghmane A, Taha M, Isnard H, Parent du Chatelet I. A cluster of meningococcal disease caused by rifampicin-resistant C meningococci in France, April 2012. Euro Surveill. 2012;17(34): pii: 20254.

    Google Scholar 

  232. Canica M, Dias R, Nunes B, Carvalho L, Ferreira E. Invasive culture-confirmed Neisseria meningitidis in Portugal: evaluation of serogroups in relation to different variables and antimicrobial susceptibility (2000–2001). J Med Microbiol. 2004;53(Pt 9):921–5. doi:10.1099/jmm.0.45556-0.

    Article  CAS  PubMed  Google Scholar 

  233. Ibarz-Pavon AB, Lemos AP, Gorla MC, Regueira M, Gabastou JM. Laboratory-based surveillance of Neisseria meningitidis isolates from disease cases in Latin American and Caribbean countries, SIREVA II 2006–2010. PLoS ONE. 2012;7(8), e44102. doi:10.1371/journal.pone.0044102.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  234. Jackson LA, Alexander ER, DeBolt CA, Swenson PD, Boase J, McDowell MG, Reeves MW, Wenger JD. Evaluation of the use of mass chemoprophylaxis during a school outbreak of enzyme type 5 serogroup B meningococcal disease. Pediatr Infect Dis J. 1996;15(11):992–8.

    Article  CAS  PubMed  Google Scholar 

  235. Alcala B, Salcedo C, de la Fuente L, Arreaza L, Uria MJ, Abad R, Enriquez R, Vazquez JA, Motge M, de Batlle J. Neisseria meningitidis showing decreased susceptibility to ciprofloxacin: first report in Spain. J Antimicrob Chemother. 2004;53(2):409. doi:10.1093/jac/dkh075.

    Article  CAS  PubMed  Google Scholar 

  236. Shultz TR, Tapsall JW, White PA, Newton PJ. An invasive isolate of Neisseria meningitidis showing decreased susceptibility to quinolones. Antimicrob Agents Chemother. 2000;44(4):1116.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  237. Emergence of fluoroquinolone-resistant Neisseria meningitidis--Minnesota and North Dakota, 2007–2008. MMWR Morb Mortal Wkly Rep. 2008;57(7):173–5.

    Google Scholar 

  238. Shultz TR, White PA, Tapsall JW. In vitro assessment of the further potential for development of fluoroquinolone resistance in Neisseria meningitidis. Antimicrob Agents Chemother. 2005;49(5):1753–60. doi:10.1128/aac.49.5.1753-1760.2005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  239. Luaces Cubells C, Garcia Garcia JJ, Roca Martinez J, Latorre Otin CL. Clinical data in children with meningococcal meningitis in a Spanish hospital. Acta Paediatr. 1997;86(1):26–9.

    Article  CAS  PubMed  Google Scholar 

  240. Turner PC, Southern KW, Spencer NJ, Pullen H. Treatment failure in meningococcal meningitis. Lancet. 1990;335(8691):732–3.

    Article  CAS  PubMed  Google Scholar 

  241. Bardi L, Badolati A, Corso A, Rossi MA. Failure of the treatment with penicillin in a case of Neisseria meningitidis meningitis. Medicina (B Aires). 1994;54(5 Pt 1):427–30.

    CAS  Google Scholar 

  242. Rainbow J, Cebelinski E, Bartkus J, Glennen A, Boxrud D, Lynfield R. Rifampin-resistant meningococcal disease. Emerg Infect Dis. 2005;11(6):977–9. doi:10.3201/eid1106.050143.

    Article  PubMed  PubMed Central  Google Scholar 

  243. Briggs S, Ellis-Pegler R, Roberts S, Thomas M, Woodhouse A. Short course intravenous benzylpenicillin treatment of adults with meningococcal disease. Intern Med J. 2004;34(7):383–7. doi:10.1111/j.1445-5994.2004.00601.x.

    Article  CAS  PubMed  Google Scholar 

  244. Brouqui P, Raoult D. Endocarditis due to rare and fastidious bacteria. Clin Microbiol Rev. 2001;14(1):177–207. doi:10.1128/cmr.14.1.177-207.2001.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  245. Haddow LJ, Mulgrew C, Ansari A, Miell J, Jackson G, Malnick H, Rao GG. Neisseria elongata endocarditis: case report and literature review. Clin Microbiol Infect. 2003;9(5):426–30.

    Article  CAS  PubMed  Google Scholar 

  246. Morla N, Guibourdenche M, Riou JY. Neisseria spp. and AIDS. J Clin Microbiol. 1992;30(9):2290–4.

    CAS  PubMed  PubMed Central  Google Scholar 

  247. Mastrantonio P, Stefanelli P, Fazio C, Sofia T, Neri A, La Rosa G, Marianelli C, Muscillo M, Caporali MG, Salmaso S. Serotype distribution, antibiotic susceptibility, and genetic relatedness of Neisseria meningitidis strains recently isolated in Italy. Clin Infect Dis. 2003;36(4):422–8. doi:10.1086/346154.

    Article  CAS  PubMed  Google Scholar 

  248. Orus P, Vinas M. Transfer of penicillin resistance between Neisseriae in microcosm. Microb Drug Resist. 2000;6(2):99–104. doi:10.1089/107662900419393.

    Article  CAS  PubMed  Google Scholar 

  249. Arreaza L, Salcedo C, Alcala B, Vazquez JA. What about antibiotic resistance in Neisseria lactamica? J Antimicrob Chemother. 2002;49(3):545–7.

    Article  CAS  PubMed  Google Scholar 

  250. Wu HM, Harcourt BH, Hatcher CP, Wei SC, Novak RT, Wang X, Juni BA, Glennen A, Boxrud DJ, Rainbow J, Schmink S, Mair RD, Theodore MJ, Sander MA, Miller TK, Kruger K, Cohn AC, Clark TA, Messonnier NE, Mayer LW, Lynfield R. Emergence of ciprofloxacin-resistant Neisseria meningitidis in North America. N Engl J Med. 2009;360(9):886–92. doi:10.1056/NEJMoa0806414.

    Article  CAS  PubMed  Google Scholar 

  251. Ito M, Deguchi T, Mizutani KS, Yasuda M, Yokoi S, Ito S, Takahashi Y, Ishihara S, Kawamura Y, Ezaki T. 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(1):137–43. doi:10.1128/AAC.49.1.137-143.2005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Office of Vaccines Research and Review, Center for Biologics Evaluation and Research, U.S. Food and Drug Administration, Bethesda, MD, USA

    Margaret C. Bash M.D., M.P.H. & Kathryn A. Matthias Ph.D.

  2. Department of Pediatrics, Uniformed Services University of the Health Sciences, Bethesda, MD, USA

    Margaret C. Bash M.D., M.P.H. & Kathryn A. Matthias Ph.D.

Authors
  1. Margaret C. Bash M.D., M.P.H.
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kathryn A. Matthias Ph.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Margaret C. Bash M.D., M.P.H. .

Editor information

Editors and Affiliations

  1. Treiber Therapeutics, Cambridge, Massachusetts, USA

    Douglas L. Mayers

  2. Wayne State University School of Medicine, Detroit Medical Center, Detroit, Michigan, USA

    Jack D. Sobel

  3. Canada Research Chair in Antimicrobial Resistance, Centre de recherche en Infectiologie, University of Laval, Quebec City, Canada

    Marc Ouellette

  4. Division of Infectious Diseases, University of Michigan Medical School, Ann Arbor, Michigan, USA

    Keith S. Kaye

  5. Infection Control and Prevention Unit of Infectious Diseases, Assaf Harofeh Medical Center, Sackler Faculty of Medicine, Tel-Aviv University, Tel Aviv, Israel

    Dror Marchaim

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Bash, M.C., Matthias, K.A. (2017). Antibiotic Resistance in Neisseria . In: Mayers, D., Sobel, J., Ouellette, M., Kaye, K., Marchaim, D. (eds) Antimicrobial Drug Resistance. Springer, Cham. https://doi.org/10.1007/978-3-319-47266-9_6

Download citation

Publish with us

Policies and ethics

Search

Navigation