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Increasing antimicrobial resistance of , particularly to third-generation cephalosporins, has been reported in many countries. We examined the susceptibility (determined by Etest and evaluated using the breakpoints of the European Committee on Antimicrobial Susceptibility Testing) of 434 isolates collected from 107 female and 327 male patients in Stuttgart, south-west Germany, between 2004 and 2015. During the study period, high proportions of isolates were resistant to ciprofloxacin (70.3%), tetracycline (48.4%; increasing from 27.5% in 2004/2005 to 57.7% in 2014/2015; p = 0.0002) and penicillin (25.6%). The proportion of isolates resistant to azithromycin was low (5.5%) but tended to increase (p = 0.08). No resistance and stable minimum inhibitory concentrations were found for cefixime, ceftriaxone, and spectinomycin. High-level resistance was found for ciprofloxacin (39.6%) and tetracycline (20.0%) but not for azithromycin; 16.3% of the isolates produced betalactamase. Thus, cephalosporins can still be used for the treatment of gonorrhoea in the study area. To avoid further increasing resistance to azithromycin, its usage should be limited to patients allergic to cephalosporins, or (in combination with cephalosporins) to patients for whom no susceptibility testing could be performed or those co-infected with chlamydiae.


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  1. World Health Organization (WHO). Global incidence and prevalence of selected curable sexually transmitted infections—2008. Geneva: WHO; 2012. Available from: http://www.who.int/reproductivehealth/publications/rtis/stisestimates/en/
  2. Unemo M, Shafer WM. Antimicrobial resistance in Neisseria gonorrhoeae in the 21st century: past, evolution, and future. Clin Microbiol Rev. 2014;27(3):587-613.  https://doi.org/10.1128/CMR.00010-14  PMID: 24982323 
  3. Lewis DA. Global resistance of Neisseria gonorrhoeae: when theory becomes reality. Curr Opin Infect Dis. 2014;27(1):62-7.  https://doi.org/10.1097/QCO.0000000000000025  PMID: 24275696 
  4. Centers for Disease Control and Prevention (CDC). Update to CDC’s Sexually transmitted diseases treatment guidelines, 2010: oral cephalosporins no longer a recommended treatment for gonococcal infections. MMWR Morb Mortal Wkly Rep. 2012;61(31):590-4. PMID: 22874837 
  5. Bignell C, Unemo MEuropean STI Guidelines Editorial Board. 2012 European guideline on the diagnosis and treatment of gonorrhoea in adults. Int J STD AIDS. 2013;24(2):85-92.  https://doi.org/10.1177/0956462412472837  PMID: 24400344 
  6. Martin IM, Hoffmann S, Ison CA. ESSTI Network. European Surveillance of Sexually Transmitted Infections (ESSTI): the first combined antimicrobial susceptibility data for Neisseria gonorrhoeae in Western Europe. J Antimicrob Chemother. 2006;58(3):587-93.  https://doi.org/10.1093/jac/dkl265  PMID: 16816397 
  7. Cole MJ, Unemo M, Hoffmann S, Chisholm SA, Ison CA, van de Laar MJ. The European gonococcal antimicrobial surveillance programme, 2009. Euro Surveill. 2011;16(42):19995. PMID: 22027378 
  8. Cole MJ, Spiteri G, Chisholm SA, Hoffmann S, Ison CA, Unemo M, et al. Emerging cephalosporin and multidrug-resistant gonorrhoea in Europe. Euro Surveill. 2014;19(45):20955.  https://doi.org/10.2807/1560-7917.ES2014.19.45.20955  PMID: 25411689 
  9. Abraham S, Poehlmann C, Spornraft-Ragaller P. Gonorrhea: Data on antibiotic resistance and accompanying infections at the University Hospital Dresden over a 10-year time period. J Dtsch Dermatol Ges. 2013;11(3):241-9. PMID: 23194411 
  10. Horn NN, Kresken M, Körber-Irrgang B, Göttig S, Wichelhaus C, Wichelhaus TA. Working Party Antimicrobial Resistance of the Paul Ehrlich Society for Chemotherapy. Antimicrobial susceptibility and molecular epidemiology of Neisseria gonorrhoeae in Germany. Int J Med Microbiol. 2014;304(5-6):586-91. https://doi.org/10.1016/j.ijmm.2014.04.001  PMID: 24801146 
  11. Enders M, Turnwald-Maschler A, Regnath T. Antimicrobial resistance of Neisseria gonorrhoeae isolates from the Stuttgart and Heidelberg areas of southern Germany. Eur J Clin Microbiol Infect Dis. 2006;25(5):318-22. https://doi.org/10.1007/s10096-006-0134-y  PMID: 16733613 
  12. 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. 2011;16(43):19998.  PMID: 22085601 
  13. Cole MJ, Spiteri G, Town K, Unemo M, Hoffmann S, Chisholm SA, et al. Euro-GASP Network. Risk factors for antimicrobial-resistant Neisseria gonorrhoeae in Europe. Sex Transm Dis. 2014;41(12):723-9.  https://doi.org/10.1097/OLQ.0000000000000185  PMID: 25581808 
  14. Yu RX, Yin Y, Wang GQ, Chen SC, Zheng BJ, Dai XQ, et al. Worldwide susceptibility rates of Neisseria gonorrhoeae isolates to cefixime and cefpodoxime: a systematic review and meta-analysis. PLoS One. 2014;9(1):e87849.  https://doi.org/10.1371/journal.pone.0087849  PMID: 24498212 
  15. EUCAST. Breakpoint tables for interpretation of MICs and zone diameters. Version 5.0, 2015. Available from: http://www.eucast.org
  16. Clinical and Laboratory Standards Institute (CLSI). Performance standards for antimicrobial susceptibility testing; twenty-third informational supplement. CLSI document M100-S23. Wayne, PA: CLSI: 2013.
  17. Palmer HM, Young H, Winter A, Dave J. Emergence and spread of azithromycin-resistant Neisseria gonorrhoeae in Scotland. J Antimicrob Chemother. 2008;62(3):490-4.  https://doi.org/10.1093/jac/dkn235  PMID: 18552343 
  18. Chisholm SA, Neal TJ, Alawattegama AB, Birley HD, Howe RA, Ison CA. Emergence of high-level azithromycin resistance in Neisseria gonorrhoeae in England and Wales. J Antimicrob Chemother. 2009;64(2):353-8.  https://doi.org/10.1093/jac/dkp188  PMID: 19468025 
  19. Starnino S, Stefanelli P. Neisseria gonorrhoeae Italian Study Group. Azithromycin-resistant Neisseria gonorrhoeae strains recently isolated in Italy. J Antimicrob Chemother. 2009;63(6):1200-4.  https://doi.org/10.1093/jac/dkp118  PMID: 19357159 
  20. Unemo M, Golparian D, Hellmark B. First three Neisseria gonorrhoeae isolates with high-level resistance to azithromycin in Sweden: a threat to currently available dual-antimicrobial regimens for treatment of gonorrhea? Antimicrob Agents Chemother. 2014;58(1):624-5.  https://doi.org/10.1128/AAC.02093-13  PMID: 24189248 
  21. Berçot B, Belkacem A, Goubard A, Mougari F, Sednaoui P, La Ruche G, et al. High-level azithromycin-resistant Neisseria gonorrhoeae clinical isolate in France, March 2014. Euro Surveill. 2014;19(44):20951.  https://doi.org/10.2807/1560-7917.ES2014.19.44.20951  PMID: 25394255 
  22. Lynagh Y, Mac Aogáin M, Walsh A, Rogers TR, Unemo M, Crowley B. Detailed characterization of the first high-level azithromycin-resistant Neisseria gonorrhoeae cases in Ireland. J Antimicrob Chemother. 2015;70(8):2411-3.  https://doi.org/10.1093/jac/dkv106  PMID: 25907073 
  23. Espinosa K, Park JA, Gerrity JJ, Buono S, Shearer A, Dick C, et al. Fluoroquinolone resistance in Neisseria gonorrhoeae after cessation of ciprofloxacin usage in San Francisco: using molecular typing to investigate strain turnover. Sex Transm Dis. 2015;42(2):57-63.  https://doi.org/10.1097/OLQ.0000000000000233  PMID: 25585061 
  24. Hamasuna R, Yasuda M, Ishikawa K, Uehara S, Takahashi S, Hayami H, et al. Nationwide surveillance of the antimicrobial susceptibility of Neisseria gonorrhoeae from male urethritis in Japan. J Infect Chemother. 2013;19(4):571-8.  https://doi.org/10.1007/s10156-013-0637-2  PMID: 23813093 
  25. Federal Office of Consumer Protection and Food Safety. Paul-Ehrlich-Gesellschaft für Chemotherapie e.V., Infectiology Freiburg, eds. GERMAP 2012 – Report on the consumption of antimicrobials and the spread of antimicrobial resistance in human and veterinary medicine in Germany. Rheinbach: Antiinfectives Intelligence; 2014. Available from: http://www.bvl.bund.de/SharedDocs/Downloads/08_PresseInfothek/Germap_2012_en.pdf?__blob=publicationFile&v=3
  26. Velicko I, Unemo M. Recent trends in gonorrhoea and syphilis epidemiology in Sweden: 2007 to 2011. Euro Surveill. 2012;17(29):20223. PMID: 22835468 
  27. Savage EJ, Marsh K, Duffell S, Ison CA, Zaman A, Hughes G. Rapid increase in gonorrhoea and syphilis diagnoses in England in 2011. Euro Surveill. 2012;17(29):22224. PMID: 22835469 
  28. Bremer V, Marcus U, Hamouda O. Syphilis on the rise again in Germany--results from surveillance data for 2011. Euro Surveill. 2012;17(29):20222. PMID: 22835467 
  29. Chesson HW, Kirkcaldy RD, Gift TL, Owusu-Edusei K Jr, Weinstock HS. Ciprofloxacin resistance and gonorrhea incidence rates in 17 cities, United States, 1991-2006. Emerg Infect Dis. 2014;20(4):612-9.  https://doi.org/10.3201/eid2004.131288  PMID: 24655615 
  30. Kubanova A, Frigo N, Kubanov A, Sidorenko S, Lesnaya I, Polevshikova S, et al. The Russian gonococcal antimicrobial susceptibility programme (RU-GASP)--national resistance prevalence in 2007 and 2008, and trends during 2005-2008. Euro Surveill. 2010;15(14):19533. PMID: 20394716 
  31. Lindberg M, Ringertz O, Sandström E. Treatment of pharyngeal gonorrhea due to beta-lactamase-producing gonococci. Br J Vener Dis. 1982;58(2):101-4. PMID: 6461385 
  32. Koedijk FD, van Veen MG, de Neeling AJ, Linde GB, van der Sande MA. Increasing trend in gonococcal resistance to ciprofloxacin in The Netherlands, 2006-8. Sex Transm Infect. 2010;86(1):41-5.  https://doi.org/10.1136/sti.2009.037135  PMID: 19703843 
  33. Kirkcaldy RD, Zaidi A, Hook EW 3rd, Holmes KK, Soge O, del Rio C, et al. Neisseria gonorrhoeae antimicrobial resistance among men who have sex with men and men who have sex exclusively with women: the Gonococcal Isolate Surveillance Project, 2005-2010. Ann Intern Med. 2013;158(5 Pt 1):321-8.  https://doi.org/10.7326/0003-4819-158-5-201303050-00004  PMID: 23460055 
  34. Mason PR, Gwanzura L, Latif AS, Marowa E, Ray S, Katzenstein DA. Antimicrobial resistance in gonococci isolated from patients and from commercial sex workers in Harare, Zimbabwe. Int J Antimicrob Agents. 1997;9(3):175-9.  https://doi.org/10.1016/S0924-8579(97)00052-6  PMID: 9552714 

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