Antimicrobial resistance of Neisseria gonorrhoeae isolates in south-west Germany, 2004 to 2015: increasing minimal inhibitory concentrations of tetracycline but no resistance to third-generation cephalosporins

Increasing antimicrobial resistance of Neisseria gonorrhoeae, 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 N. gonorrhoeae 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.

[1]  M. Unemo,et al.  Detailed characterization of the first high-level azithromycin-resistant Neisseria gonorrhoeae cases in Ireland. , 2015, The Journal of antimicrobial chemotherapy.

[2]  M. Pandori,et al.  Fluoroquinolone Resistance in Neisseria gonorrhoeae After Cessation of Ciprofloxacin Usage in San Francisco: Using Molecular Typing to Investigate Strain Turnover , 2015, Sexually transmitted diseases.

[3]  A. Amato-Gauci,et al.  Risk Factors for Antimicrobial-Resistant Neisseria gonorrhoeae in Europe , 2014, Sexually transmitted diseases.

[4]  M. Unemo,et al.  Emerging cephalosporin and multidrug-resistant gonorrhoea in Europe. , 2014, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[5]  B. Berçot,et al.  High-level azithromycin-resistant Neisseria gonorrhoeae clinical isolate in France, March 2014. , 2014, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[6]  T. Wichelhaus,et al.  Antimicrobial susceptibility and molecular epidemiology of Neisseria gonorrhoeae in Germany. , 2014, International journal of medical microbiology : IJMM.

[7]  M. Unemo,et al.  Antimicrobial Resistance in Neisseria gonorrhoeae in the 21st Century: Past, Evolution, and Future , 2014, Clinical Microbiology Reviews.

[8]  R. Kirkcaldy,et al.  Ciprofloxacin Resistance and Gonorrhea Incidence Rates in 17 Cities, United States, 1991–2006 , 2014, Emerging infectious diseases.

[9]  D. Lewis Global resistance of Neisseria gonorrhoeae: when theory becomes reality , 2014, Current opinion in infectious diseases.

[10]  Xiangsheng Chen,et al.  Worldwide Susceptibility Rates of Neisseria gonorrhoeae Isolates to Cefixime and Cefpodoxime: A Systematic Review and Meta-Analysis , 2014, PloS one.

[11]  M. Unemo,et al.  The European Gonococcal Antimicrobial Surveillance Programme (Euro-GASP)—a sentinel approach in the European Union (EU)/European Economic Area (EEA) , 2013, Sexually Transmitted Infections.

[12]  M. Unemo,et al.  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? , 2013, Antimicrobial Agents and Chemotherapy.

[13]  K. Holmes,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 , 2013, Annals of Internal Medicine.

[14]  S. Abraham,et al.  Gonorrhea: Data on antibiotic resistance and accompanying infections at the University Hospital Dresden over a 10‐year time period , 2013, Journal der Deutschen Dermatologischen Gesellschaft = Journal of the German Society of Dermatology : JDDG.

[15]  M. Unemo,et al.  2012 European guideline on the diagnosis and treatment of gonorrhoea in adults , 2013, International journal of STD & AIDS.

[16]  M. Yasuda,et al.  Nationwide surveillance of the antimicrobial susceptibility of Neisseria gonorrhoeae from male urethritis in Japan , 2013, Journal of infection and chemotherapy : official journal of the Japan Society of Chemotherapy.

[17]  J. Papp,et al.  Update to CDC's Sexually transmitted diseases treatment guidelines, 2010: oral cephalosporins no longer a recommended treatment for gonococcal infections. , 2012, MMWR. Morbidity and mortality weekly report.

[18]  V. Bremer,et al.  Syphilis on the rise again in Germany--results from surveillance data for 2011. , 2012, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[19]  M. Unemo,et al.  Recent trends in gonorrhoea and syphilis epidemiology in Sweden: 2007 to 2011. , 2012, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[20]  C. Ison,et al.  Rapid increase in gonorrhoea and syphilis diagnoses in England in 2011. , 2012, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[21]  J. Rowley,et al.  Global incidence and prevalence of selected curable sexually transmitted infections: 2008 , 2012 .

[22]  A Stary,et al.  First Neisseria gonorrhoeae strain with resistance to cefixime causing gonorrhoea treatment failure in Austria, 2011. , 2011, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[23]  M. Unemo,et al.  The European gonococcal antimicrobial surveillance programme, 2009. , 2011, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[24]  M. Unemo,et al.  The Russian gonococcal antimicrobial susceptibility programme (RU-GASP)--national resistance prevalence in 2007 and 2008, and trends during 2005-2008. , 2010, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[25]  M. V. van Veen,et al.  Increasing trend in gonococcal resistance to ciprofloxacin in The Netherlands, 2006–8 , 2009, Sexually Transmitted Infections.

[26]  R. Howe,et al.  Emergence of high-level azithromycin resistance in Neisseria gonorrhoeae in England and Wales. , 2009, The Journal of antimicrobial chemotherapy.

[27]  P. Stefanelli,et al.  Azithromycin-resistant Neisseria gonorrhoeae strains recently isolated in Italy. , 2009, The Journal of antimicrobial chemotherapy.

[28]  H. Palmer,et al.  Emergence and spread of azithromycin-resistant Neisseria gonorrhoeae in Scotland. , 2008, The Journal of antimicrobial chemotherapy.

[29]  S. Chisholm,et al.  Emergence of high-level azithromycin resistance in Neisseria gonorrhoeae in England and Wales. , 2008, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[30]  C. Ison,et al.  European Surveillance of Sexually Transmitted Infections (ESSTI): the first combined antimicrobial susceptibility data for Neisseria gonorrhoeae in Western Europe. , 2006, The Journal of antimicrobial chemotherapy.

[31]  M. Enders,et al.  Antimicrobial resistance of Neisseria gonorrhoeae isolates from the Stuttgart and Heidelberg areas of southern Germany , 2006, European Journal of Clinical Microbiology and Infectious Diseases.

[32]  D. Katzenstein,et al.  Antimicrobial resistance in gonococci isolated from patients and from commercial sex workers in Harare, Zimbabwe. , 1997, International journal of antimicrobial agents.

[33]  E. Sandström,et al.  Treatment of pharyngeal gonorrhea due to beta-lactamase-producing gonococci. , 1982, The British journal of venereal diseases.