Neisseria gonorrhoeae 2008
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1 Magnus Unemo Date: Page 1 of 7 Neisseria gonorrhoeae 2008 Annual report regarding serological characterisation and antibiotic susceptibility of Swedish Neisseria gonorrhoeae strains In 2008, 523 Swedish N. gonorrhoeae (GC) isolates from 447 clinical gonorrhoea cases were submitted for complete characterisation to the National Reference Laboratory for Pathogenic Neisseria (an external body of the Swedish Institute for Infectious Disease Control [SMI]), Department of Laboratory Medicine, Section Clinical Microbiology, Örebro University Hospital, Örebro, Sweden or to the Division of Clinical Bacteriology, Department of Laboratory Medicine, Karolinska University Hospital Huddinge, Stockholm, Sweden. In total, 447 different GC strains from 434 patients were identified. Thus, five patients were infected with two different strains on the same occasion and 13 were infected on two different occasions (same strain [n=5] and different strains [n=8]) during the year. Of the 523 characterised GC isolates, 293 were cultured from urethra or cervix, 82 from pharynx, 79 from rectum, five from other locations (eye [n=4] or abscess [n=1]), and 64 specimens were unspecified. All the 447 different GC strains are presented in Table I. In 2008, 725 gonorrhoea cases were notified, in accordance with the Swedish Communicable Diseases Act, SMI, Solna, Sweden. Notably, the number of notified gonorrhoea cases in Sweden has increased. For comparison, 642 cases were notified in Most of the cases were identified in the three largest counties of Sweden, which comprise the cities Stockholm, Gothenburg, and Malmoe, respectively. The proportion of patients infected abroad was 32% and Thailand was the predominant country for exposure. Of all the gonorrhoea cases (n=725), 60% were heterosexually acquired, 34% were homosexually acquired, and in 6%, the transmission route was not described or other route (personal communication, Inga Velicko, epidemiologist, SMI). The GC isolates from 447 gonorrhoea cases, which were submitted for complete characterisation, represented 62% of the notified cases. Age and gender In 439 of the gonorrhoea cases (n=447), the age of the patient was depicted. The mean age of all cases was 30 years and the median age was 28 years (in 2007, 32 years and 30 years, respectively). In 443 of the cases (79 women and 364 men, gender ratio 1:4.6), the gender of the patient was described or possible to determine. The ranges of the ages were 14 to 68 years and 15 to 44 years for the men and women, respectively. The mean age of the women was 24 years and the median age 21 years (in 2007, 29 years and 24 years, respectively). The mean Address: National Reference Laboratory for Pathogenic Neisseria Department of Laboratory Medicine, Clinical Microbiology Örebro University Hospital SE Örebro Sweden Telephone: Fax: magnus.unemo@orebroll.se
2 Page 2 of 7 age of the men was 32 years and the median age 29 years (in 2007, 33 years and 31 years, respectively). Serological characterisation Of the different GC strains (n=447), 76 strains were assigned serogroup WI (PorB1a) and 371 strains were determined as serogroup WII/III (PorB1b). In Table I, the serogroup distribution, serovar distribution (PhadeBact GC Serovar Test, Bactus AB; 1) and specimens for all the different strains submitted to the National Reference Laboratory for Pathogenic Neisseria, Örebro or to the laboratory in Huddinge are described. On request also the Genetic Systems monoclonal antibodies can be used. Antibiotic susceptibility The susceptibility of all isolates to ampicillin, cefixime, ceftriaxone, azithromycin, ciprofloxacin, and spectinomycin was analyzed using the Etest method (AB Biodisk, Solna, Sweden) on GC Medium Base agar (supplemented with 1% haemoglobin and 1% IsoVitaleX). Breakpoints for susceptibility (S), intermediate susceptibility (I), and resistance have been determined by the Reference Laboratory and Swedish Reference Group on Antibiotics (2). At the Reference Laboratory, the susceptibility to ciprofloxacin was also determined with Nalidixic acid discs (30 µg) on IsoSensitest Agar supplemented with 5% defibrinated horse blood and 20 mg/l β-nicotinamide adenine dinucleotide (NAD). β- lactamase production was analysed using Nitrocefin discs. Of the 447 GC strains, 127 (28%) were β-lactamase producing, i.e. PPNG. A high level of intermediate susceptibility and resistance to traditional antibiotics used for treatment of gonorrhoea, i.e. ampicillin and ciprofloxacin, was identified. All the ciprofloxacin resistant strains were also identified with Nalidixic acid discs. All the 447 strains were fully susceptible to spectinomycin. However, one strain (0.2%) showed a reduced susceptibility to ceftriaxone (MIC=0.19 mg/l). Nineteen strains (4%) displayed an intermediate susceptibility to cefixime, however, no resistant isolates were identified. Forty-four strains (10%) showed an intermediate susceptibility and fourteen strains (3%) were resistant to azithromycin. No obvious correlation between antibiotic susceptibility and any individual serovar was possible to identify, however, many of the serovars were only represented by occasional strains. In Table II, the antibiotic susceptibility of Swedish GC strains from 2002 to 2008 is summarised. Swedish N. gonorrhoeae strains submitted for characterisation in 2008 were: representing 62% of the notified gonorrhoea cases. Most of the gonorrhoea cases were identified in the three largest counties of Sweden, which comprise the cities Stockholm, Gothenburg, and Malmoe, respectively. mainly (83%) determined as serogroup WII/III (PorB1b).
3 Page 3 of 7 predominated by the serovars Bropyst (n=114), Arst (n=60), and Bpyut (n=58), Table I. β-lactamase producing in 28% (PPNG strains) of the cases, Table II. to a higher level, i.e. 13%, showing an intermediate susceptibility or resistance to azithromycin (in 2007, 7%), Table II. to a higher level, i.e. 4%, showing an intermediate susceptibility or resistance to cefixime (in 2007, 1%), Table II. For the first time, an isolate displaying intermediate susceptibility/resistance to ceftriaxone, using the current SIR-breakpoints, was identified in Sweden, Table II. to a very high level showing an intermediate susceptibility or resistance to ciprofloxacin (64%), Table II. Overall, ceftriaxone, cefixime, spectinomycin, or in some occasional cases, such as after performed in vitro susceptibility testing and with concurrent Chlamydia trachomatis infection, azithromycin is the recommended first choice of antibiotic for the treatment if the results from the antibiotic susceptibility testing is pending (from a microbiological point of view). Notable in 2008 As previously described in the annual reports from the Reference Laboratory, an increased awareness of prolyliminopeptidase (PIP)-negative GC strains that are difficult to identify using commercial biochemical kits (3, 4) has to be emphasised. A more or less global transmission of one PIP-negative GC strain and its genetically highly related subtypes has been described but also other PIP-negative strains are circulating in many countries (4). This stresses the need of using additional methods, e.g. antigenic/serological methods such as coagglutination (PorB protein) or DNA/RNA-based methods, for species confirmation. However, a soon finalised study examining the prevalence and characteristics of PIP-negative GC isolates in Sweden during indicates that these isolates are relatively rare in Sweden. For effective treatment of gonorrhoea it is crucial to locally, nationally, and internationally monitor the GC antibiotic resistance (AMR), which is a major concern globally. In Sweden, it is recommended that all GC isolates are analyzed regarding their antibiotic susceptibility. In 2009, for enhanced quality assurance of the resistance testing the newly characterised and designated 2008 WHO N. gonorrhoeae reference strains (5), intended for global quality assurance and control of GC AMR, will be implemented. Furthermore, it is crucial to increase the knowledge regarding the genetic basis for resistance to most antibiotics as well as to develop genetic assays for antimicrobial resistance screening for GC (6-9). An increased number of Swedish laboratories show interest to use commercial nucleic acid amplification tests (NAATs) for routine diagnosis of gonorrhoea. This is mainly not recommended due to the lack of AMR testing as well as the suboptimal specificity, causing very low positive predictive values, of nearly all GC NAATs. Accordingly, the choice of an effective GC NAAT and the need of confirmatory testing using other method, i.e. culture or
4 Page 4 of 7 NAAT detecting other genetic target, are crucial to stress. The Reference Laboratory uses highly sensitive and specific single- and dual-target GC NAATs for confirmation of samples positive in the commercial NAATs (10-12). In special epidemiological situations and/or for research purposes, the Reference Laboratory performs genetic characterisation of GC strains. Pulsed-field gel electrophoresis (PFGE) (3, 4, 6, 13, 14) and/or sequencing of the porb gene (1, 3, 4, 5-8, 13-16) and the tbpb gene (1, 4, 5-8, 14) are effective genetic methods for epidemiological characterisation of GC strains. The epidemiological and/or scientifical questions asked in relation to each project have to guide the use of appropriate method(s). In the future, the Reference Laboratory will hopefully afford to genetically characterise all Swedish GC isolates. Örebro Magnus Unemo, Per Olcén, Paula Mölling, Hans Fredlund, and co-workers at the National Reference Laboratory for Pathogenic Neisseria (an external body of the Swedish Institute for Infectious Disease Control [SMI]), Department of Laboratory Medicine, Section Clinical Microbiology, Örebro University Hospital, Örebro, Sweden. Betina Colucci, Eva-Lena Ericson, and co-workers at the Division of Clinical Bacteriology, Department of Laboratory Medicine, Karolinska University Hospital Huddinge, Stockholm, Sweden.
5 Page 5 of 7 References 1. Olsen B, Hadad R, Fredlund H, and Unemo M. The Neisseria gonorrhoeae population in Sweden during 2005 phenotypes, genotypes and antibiotic resistance. APMIS 2008;116: The Swedish Reference Group for Antibiotics (SRGA) and its subcommittee on Methodology (SRGA- M) ( 3. Fjeldsøe-Nielsen H, Unemo M, Fredlund H, Hjort SV, Berthelsen LM, Palmer HM, and Friis-Möller A. Phenotypic and genotypic characterisation of prolyliminopeptidase-negative Neisseria gonorrhoeae isolates in Denmark. Eur J Clin Microbiol Infect Dis 2005;24: Unemo M, Palmer HM, Blackmore T, Herrera G, Fredlund H, Limnios A, Nguyen N, and Tapsall J. Global transmission of prolyliminopeptidase (PIP)-negative Neisseria gonorrhoeae strains - implications for changes in diagnostic strategies? Sex Transm Infect 2007;83: Unemo M, Fasth O, Fredlund H, Limnios A, Tapsall J. Phenotypic and genetic characterization of the 2008 WHO Neisseria gonorrhoeae reference strain panel intended for global quality assurance and quality control of gonococcal antimicrobial resistance surveillance for public health purposes. J Antimicrob Chemother Mar 24. [Epub ahead of print] 6. Lundbäck D, Fredlund H, Berglund T, Wretlind B, and Unemo M. Molecular epidemiology of Neisseria gonorrhoeae identification of the first presumed Swedish transmission chain of an azithromycin resistant strain. APMIS 2006;114: Lindberg R, Fredlund H, Nicholas R, and 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: Unemo M, Sjöstrand A, Akhras M, Gharizadeh B, Lindbäck E, Pourmand N, Wretlind B, and Fredlund H. Molecular characterization of Neisseria gonorrhoeae identifies transmission and resistance of one ciprofloxacin-resistant strain. APMIS 2007;115: Unemo M, Olcén P, Fredlund H, Thulin S. Real-time PCR and subsequent pyrosequencing for screening of pena mosaic alleles and prediction of reduced susceptibility to expanded-spectrum cephalosporins in Neisseria gonorrhoeae. APMIS 2008;116: Hjelmevoll SO, Olsen ME, Sollid JU, Haaheim H, Unemo M, Skogen V. A fast real-time polymerase chain reaction method for sensitive and specific detection of the Neisseria gonorrhoeae pora pseudogene. J Mol Diagn 2006;8: Hjelmevoll SO, Olsen ME, Sollid JU, Haaheim H, Melby KK, Moi H, Unemo M, Skogen V. Clinical validation of a real-time polymerase chain reaction detection of Neisseria gonorrheae pora pseudogene versus culture techniques. Sex Transm Dis 2008;35: Goire N, Nissen MD, LeCornec GM, Sloots TP, Whiley DM. A duplex Neisseria gonorrhoeae realtime polymerase chain reaction assay targeting the gonococcal pora pseudogene and multicopy opa genes. Diagn Microbiol Infect Dis 2008;61: Unemo M. Genotypic and phenotypic characterisation of Neisseria gonorrhoeae. Linköping University Medical Dissertations no. 828, Fredlund H, Falk L, Jurstrand M, and Unemo M. Molecular genetic methods for diagnosis and characterisation of Chlamydia trachomatis and Neisseria gonorrhoeae: impact on epidemiological surveillance and interventions. APMIS 2004;112: Unemo M, Olcèn P, Albert J, and Fredlund H. Comparison of serologic and genetic porb-based typing of Neisseria gonorrhoeae: consequences for future characterization. J Clin Microbiol 2003;41: Unemo M, Olcén P, Jonasson J, and Fredlund H. Molecular typing of Neisseria gonorrhoeae by pyrosequencing of highly polymorphic segments of the porb gene. J Clin Microbiol 2004;42:
6 Page 6 of 7 Table I. Serogroup distribution, serovar distribution and specimens for different N. gonorrhoeae strains (n=447) submitted to the National Reference Laboratory for Pathogenic Neisseria, Örebro or to the Karolinska University Hospital Huddinge, Sweden in Serogroup Serovar Urethra Cervix Pharynx Unspecified or Rectum other specimens a Total WI Arst Arost WII/III Bropyst Bpyut Bropst Brpyust Bropyt Bopyt Bpyvut Bropyvst Bropt Bpyst Brpyut Bropys Bryus Bpyust Bryut Bopt Bopyst Bropyust Brpyvust Bryu Other serovars b Total a Other specimens were eye (n=4) and abscess (n=1). b Serovars that were identified in less than three cases fall (Aost, Aot, Ar, Arot, Ars, Ast, Boput, Bopyust, Bpvst, Bpyt, Bpyus, Broput, Bropyus, Bropyut, Bropyvt, Brout, Broyt, Brpst, Brpyst, Brpyt, Brpyvut, Byus).
7 Page 7 of 7 Table II. Percentages of Swedish N. gonorrhoeae strains comprising β-lactamase production, intermediate susceptibility or resistance in (n=120) 2003 (n=130) 2004 (n=149) 2005 (n=497) # 2006 (n=352) # 2007 (n=406) # 2008 (n=447) # β-lactamase production Ampicillin *, ** MIC > > <1 0 Cefixime > > Ceftriaxone > <1 Azithromycin > > Ciprofloxacin > <1 <1 <1 > Spectinomycin > # From 2005, all strains submitted to the National Reference Laboratory for Pathogenic Neisseria, Örebro, Sweden and to the Karolinska University Hospital Huddinge, Stockholm, Sweden are presented. * Minimum inhibitory concentration (MIC) in mg/l. ** PPNG strains are not included; 2002 (n=73), 2003 (n=102), 2004 (n=110), 2005 (n=384), 2006 (n=248), 2007 (n=285), and 2008 (n=320). Report sent to: Swedish Institute of Infectious Disease Control, att: Annika Linde, Margareta Löfdahl, Anders Blaxhult, Inga Velicko, Magnus Thore, Lars Engstrand Swedish National Institute of Public Health, att: Gunilla Rådö European Centre for Disease Prevention and Control (ECDC), att: Zsuzsanna Jakab, Johan Giesecke, Karl Ekdahl, Marita van der Laar Eastern European Sexual and Reproductive Health Network, att: Marius Domeika WHO Collaborating Centre for STD, Sydney, Australia, att: John Tapsall WHO Headquarter, Geneva, Switzerland, att: Francis Ndowa Sexually Transmitted Bacterial Reference Laboratory, HPA, London, UK, att: Catherine Ison Centers for Disease Control and Prevention (CDC), att: Ronald Ballard
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