Gonococcal infections and emergence of gonococcal decreased susceptibility to cephalosporins in France, 2001 to 2012.

Resistance to cephalosporins may lead to untreatable gonococcal infections. We describe the results of the sentinel surveillance of gonococcal infections and the evolution of the resistance of Neisseria gonorrhoeae to antibiotics in France from 2001 to 2012. We also analyse the factors associated with decreased susceptibility to third generation cephalosporins. In France, surveillance of gonococcal infections is conducted through a network of voluntarily participating laboratories. Strains are sent to the national reference laboratory to determine the minimum inhibitory concentration (MIC) for six antibiotics. During the study period, the number of gonococcal infections increased steadily. The susceptibility of 8,649 strains was studied for this period. The proportion of strains with decreased susceptibility to cefixime (MIC>0.125 mg/L) quadrupled between 2011 (0.7%:10/1,521) and 2012 (3.0%: 33/1,093; p 0.125 mg/L for ceftriaxone. Decreased susceptibility to cephalosporins increased with older age and was more common in pharyngeal strains. Decreased susceptibility to cefixime may indicate that the national recommendation to use ceftriaxone as a first line treatment for cases of urethritis and cervicitis has not been fully implemented. Enhanced surveillance of pharyngeal strains is strongly suggested.

[1]  J. Wasserheit,et al.  The emerging threat of untreatable gonococcal infection. , 2012, The New England journal of medicine.

[2]  Josefina Ayats,et al.  Molecular characterization of two high-level ceftriaxone-resistant Neisseria gonorrhoeae isolates detected in Catalonia, Spain. , 2012, The Journal of antimicrobial chemotherapy.

[3]  A Coulter,et al.  Short form 36 (SF36) health survey questionnaire: normative data for adults of working age. , 1993, BMJ.

[4]  G Stanek,et al.  Lyme borreliosis: clinical case definitions for diagnosis and management in Europe. , 2011, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[5]  Qingxia Chen,et al.  Effectiveness of seasonal vaccine in preventing confirmed influenza-associated hospitalizations in community dwelling older adults. , 2011, The Journal of infectious diseases.

[6]  Kate E. Jones,et al.  Impacts of biodiversity on the emergence and transmission of infectious diseases , 2010, Nature.

[7]  R. F. S. C. G. J. D. N. C. Worsham,et al.  Resurgent bacterial sexually transmitted disease among men who have sex with men--King County, Washington, 1997-1999. , 1999, MMWR. Morbidity and mortality weekly report.

[8]  A. Halling,et al.  Increased incidence of Lyme borreliosis in southern Sweden following mild winters and during warm, humid summers , 2006, European Journal of Clinical Microbiology and Infectious Diseases.

[9]  U. Buchholz,et al.  Influenza vaccine effectiveness estimates in Europe in a season with three influenza type/subtypes circulating: the I-MOVE multicentre case-control study, influenza season 2012/13. , 2014, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[10]  B. Twisselmann,et al.  Surveillance of Lyme borreliosis in Germany, 1999 , 2001 .

[11]  S. Wisniewski,et al.  Interim Adjusted Estimates of Seasonal Influenza Vaccine Effectiveness — United States, February 2013 , 2013, MMWR. Morbidity and mortality weekly report.

[12]  W. Rakowicz,et al.  Lyme disease in the United Kingdom , 2013, Postgraduate Medical Journal.

[13]  Fabrice Carrat,et al.  INFLUENZA BURDEN OF ILLNESS: ESTIMATES FROM A NATIONAL PROSPECTIVE SURVEY OF HOUSEHOLD CONTACTS IN FRANCE , 2002, Archives of internal medicine.

[14]  M. Cartter,et al.  Effect of Surveillance Method on Reported Characteristics of Lyme Disease, Connecticut, 1996–2007 , 2012, Emerging infectious diseases.

[15]  E. Lindgren,et al.  Effects of Climate Change on Ticks and Tick-Borne Diseases in Europe , 2009, Interdisciplinary perspectives on infectious diseases.

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

[17]  U. Buchholz,et al.  Comparison of Shedding Characteristics of Seasonal Influenza Virus (Sub)Types and Influenza A(H1N1)pdm09; Germany, 2007–2011 , 2012, PloS one.

[18]  Anne Gallay,et al.  A survey of primary care physician practices in antibiotic prescribing for the treatment of uncomplicated male gonoccocal urethritis , 2011, BMC family practice.

[19]  D. Lipsker,et al.  How accurate is a clinical diagnosis of erythema chronicum migrans? Prospective study comparing the diagnostic accuracy of general practitioners and dermatologists in an area where lyme borreliosis is endemic. , 2004, Archives of dermatology.

[20]  A. N. Robertson,et al.  Effectiveness of seasonal 2012/13 vaccine in preventing laboratory-confirmed influenza infection in primary care in the United Kingdom: mid-season analysis 2012/13 , 2013 .

[21]  M. Meltzer,et al.  Economic Impact of Lyme Disease , 2006, Emerging infectious diseases.

[22]  P. Mead,et al.  Surveillance for Lyme disease--United States, 1992-2006. , 2008, Morbidity and mortality weekly report. Surveillance summaries.

[23]  J. Iredell,et al.  Rapid semi-automated quantitative multiplex tandem PCR (MT-PCR) assays for the differential diagnosis of influenza-like illness , 2010, BMC infectious diseases.

[24]  V. van Casteren,et al.  Incidence and management of presumption of Lyme borreliosis in Belgium: recent data from the sentinel network of general practitioners , 2012, European Journal of Clinical Microbiology and Infectious Diseases.

[25]  D. Skowronski,et al.  Low 2012–13 Influenza Vaccine Effectiveness Associated with Mutation in the Egg-Adapted H3N2 Vaccine Strain Not Antigenic Drift in Circulating Viruses , 2014, PloS one.

[26]  D. Whiley,et al.  Two cases of failed ceftriaxone treatment in pharyngeal gonorrhoea verified by molecular microbiological methods. , 2009, Journal of medical microbiology.

[27]  S. Lindstrom,et al.  Design and Performance of the CDC Real-Time Reverse Transcriptase PCR Swine Flu Panel for Detection of 2009 A (H1N1) Pandemic Influenza Virus , 2011, Journal of Clinical Microbiology.

[28]  Nicholas S. Kelley,et al.  Efficacy and effectiveness of influenza vaccines: a systematic review and meta-analysis. , 2012, The Lancet. Infectious diseases.

[29]  C. Semaille,et al.  Épidémiologie actuelle des infections sexuellement transmissibles bactériennes en France , 2013 .

[30]  A. Flahault,et al.  Virtual surveillance of communicable diseases: a 20-year experience in France , 2006, Statistical methods in medical research.

[31]  Makoto Ohnishi,et al.  Ceftriaxone-Resistant Neisseria gonorrhoeae, Japan , 2011, Emerging infectious diseases.

[32]  A. Flahault,et al.  Lyme disease in France: a primary care-based prospective study , 2005, Epidemiology and Infection.

[33]  J. Halperin,et al.  The clinical assessment, treatment, and prevention of lyme disease, human granulocytic anaplasmosis, and babesiosis: clinical practice guidelines by the Infectious Diseases Society of America. , 2006, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[34]  David N. Reshef,et al.  Factors Related to Increasing Prevalence of Resistance to Ciprofloxacin and Other Antimicrobial Drugs in Neisseria gonorrhoeae, United States , 2012, Emerging infectious diseases.

[35]  D. Livermore,et al.  Decreased susceptibility to cephalosporins among gonococci: data from the Gonococcal Resistance to Antimicrobials Surveillance Programme (GRASP) in England and Wales, 2007-2011. , 2013, The Lancet. Infectious diseases.

[36]  G. Poggensee,et al.  Epidemiological situation of Lyme borreliosis in Germany: Surveillance data from six Eastern German States, 2002 to 2006 , 2008, Parasitology Research.

[37]  J. Desenclos,et al.  Increase of Neisseria gonorrhoeae Ciprofloxacin Resistance in France in 2001–2003 , 2006, Sexually transmitted diseases.

[38]  P. Sednaoui,et al.  Gonorrhoea Surveillance System in France: 1986–2000 , 2004, Sexually transmitted diseases.

[39]  S. Subak,et al.  Effects of climate on variability in Lyme disease incidence in the northeastern United States. , 2003, American journal of epidemiology.

[40]  A. Nicoll,et al.  Are trends in HIV, gonorrhoea, and syphilis worsening in western Europe? , 2002, BMJ : British Medical Journal.

[41]  M. Unemo,et al.  Antibiotic resistance in Neisseria gonorrhoeae: origin, evolution, and lessons learned for the future , 2011, Annals of the New York Academy of Sciences.

[42]  M. Unemo,et al.  High-Level Cefixime- and Ceftriaxone-Resistant Neisseria gonorrhoeae in France: Novel penA Mosaic Allele in a Successful International Clone Causes Treatment Failure , 2011, Antimicrobial Agents and Chemotherapy.

[43]  J. Ioannidis,et al.  Effectiveness and harms of seasonal and pandemic influenza vaccines in children, adults and elderly , 2012, Human vaccines & immunotherapeutics.

[44]  M. Unemo,et al.  Two cases of verified clinical failures using internationally recommended first-line cefixime for gonorrhoea treatment, Norway, 2010. , 2010, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[45]  M. Yasuda,et al.  Threat to Cefixime Treatment for Gonorrhea , 2007, Emerging infectious diseases.

[46]  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.

[47]  M. Neteler,et al.  Lyme borreliosis in Europe. , 2011, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[48]  L. Stjernberg,et al.  Effect of gender on clinical and epidemiologic features of Lyme borreliosis. , 2007, Vector borne and zoonotic diseases.

[49]  I. Martin,et al.  Neisseria gonorrhoeae treatment failure and susceptibility to cefixime in Toronto, Canada. , 2013, JAMA.

[50]  I. Martin,et al.  Cephalosporin and Azithromycin Susceptibility in Neisseria gonorrhoeae Isolates by Site of Infection, British Columbia, 2006 to 2011 , 2013, Sexually transmitted diseases.

[51]  W. Paget,et al.  Trends in gonorrhoea in nine western European countries, 1991–6 , 2000, Sexually transmitted infections.

[52]  A. Valleron,et al.  Attitude of French general practitioners to the public health surveillance of communicable diseases. , 1995, International journal of epidemiology.

[53]  John W Tapsall,et al.  Antibiotic resistance in Neisseria gonorrhoeae. , 2005, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[54]  R. Webby,et al.  Implementing hospital-based surveillance for severe acute respiratory infections caused by influenza and other respiratory pathogens in New Zealand. , 2014, Western Pacific surveillance and response journal : WPSAR.

[55]  G. Hogg,et al.  Failure of 500 mg of ceftriaxone to eradicate pharyngeal gonorrhoea, Australia. , 2013, The Journal of antimicrobial chemotherapy.

[56]  G. Stanek,et al.  Epidemiology of European Lyme borreliosis. , 1998, Zentralblatt fur Bakteriologie : international journal of medical microbiology.

[57]  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.

[58]  V Demicheli,et al.  Assessment of the efficacy and effectiveness of influenza vaccines in healthy children: systematic review , 2005, The Lancet.

[59]  H. Wilking,et al.  Trends in surveillance data of human Lyme borreliosis from six federal states in eastern Germany, 2009-2012. , 2014, Ticks and tick-borne diseases.

[60]  J. Takkinen,et al.  Lyme borreliosis: Europe-wide coordinated surveillance and action needed? , 2006, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[61]  Michael Haber,et al.  The case test-negative design for studies of the effectiveness of influenza vaccine. , 2013, Vaccine.

[62]  Harish Nair,et al.  Global burden of respiratory infections due to seasonal influenza in young children: a systematic review and meta-analysis , 2011, The Lancet.

[63]  M. Unemo,et al.  Molecular epidemiological typing within the European Gonococcal Antimicrobial Resistance Surveillance Programme reveals predominance of a multidrug-resistant clone. , 2013, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.