Skip to main content
Top
Published in: BMC Infectious Diseases 1/2014

Open Access 01-12-2014 | Research article

Antimicrobial susceptibility/resistance and genetic characteristics of Neisseria gonorrhoeaeisolates from Poland, 2010-2012

Authors: Beata Mlynarczyk-Bonikowska, Agnieszka Beata Serwin, Daniel Golparian, Szymon Walter de Walthoffen, Slawomir Majewski, Marta Koper, Magdalena Malejczyk, Marius Domeika, Magnus Unemo

Published in: BMC Infectious Diseases | Issue 1/2014

Login to get access

Abstract

Background

In Poland, gonorrhoea has been a mandatorily reported infection since 1948, however, the reported incidences are likely underestimated. No antimicrobial resistance (AMR) data for Neisseria gonorrhoeae has been internationally reported in nearly four decades, and data concerning genetic characteristics of N. gonorrhoeae are totally lacking. The aims of this study were to investigate the AMR to previously and currently recommended gonorrhoea treatment options, the main genetic resistance determinant (penA) for extended-spectrum cephalosporins (ESCs), and genotypic distribution of N. gonorrhoeae isolates in Poland in 2010-2012.

Methods

N. gonorrhoeae isolates cultured in 2010 (n = 28), 2011 (n = 92) and 2012 (n = 108) in Warsaw and Bialystok, Poland, were examined using antimicrobial susceptibility testing (Etest), pyrosequencing of penA and N. gonorrhoeae multi-antigen sequence typing (NG-MAST).

Results

The proportions of N. gonorrhoeae isolates showing resistance were as follows: ciprofloxacin 61%, tetracycline 43%, penicillin G 22%, and azithromycin 8.8%. No isolates resistant to ceftriaxone, cefixime or spectinomycin were found. However, the proportion of isolates with an ESC MIC = 0.125 mg/L, i.e. at the resistance breakpoint, increased significantly from none in 2010 to 9.3% and 19% in 2012 for ceftriaxone and cefixime, respectively. Furthermore, 3.1% of the isolates showed multidrug resistance, i.e., resistance to ciprofloxacin, penicillin G, azithromycin, and decreased susceptibility to cefixime (MIC = 0.125 mg/L). Seventy-six isolates (33%) possessed a penA mosaic allele and 14 isolates (6.1%) contained an A501V/T alteration in penicillin-binding protein 2. NG-MAST ST1407 (n = 58, 25% of isolates) was the most prevalent ST, which significantly increased from 2010 (n = 0) to 2012 (n = 46; 43%).

Conclusions

In Poland, the diversified gonococcal population displayed a high resistance to most antimicrobials internationally previously recommended for gonorrhoea treatment and decreasing susceptibility to the currently recommended ESCs. The decreasing susceptibility to ESCs was mostly due to the introduction of the internationally spread multidrug-resistant NG-MAST ST1407 in 2011. It is essential to promptly revise the gonorrhoea treatment guidelines, improve the gonorrhoea laboratory diagnostics, and implement quality assured surveillance of gonococcal AMR (ideally also treatment failures) in Poland.
Appendix
Available only for authorised users
Literature
3.
go back to reference Tapsall JW, Ndowa F, Lewis DA, et al: Meeting the public health challenge of multidrug-and extensively drug-resistant Neisseria gonorrhoeae. Expert Rev Anti Infect Ther. 2009, 7: 821-834. 10.1586/eri.09.63.CrossRefPubMed Tapsall JW, Ndowa F, Lewis DA, et al: Meeting the public health challenge of multidrug-and extensively drug-resistant Neisseria gonorrhoeae. Expert Rev Anti Infect Ther. 2009, 7: 821-834. 10.1586/eri.09.63.CrossRefPubMed
4.
go back to reference Lewis DA: The gonococcus fights back: is this time a knock out?. Sex Transm Infect. 2010, 86: 415-421. 10.1136/sti.2010.042648.CrossRefPubMed Lewis DA: The gonococcus fights back: is this time a knock out?. Sex Transm Infect. 2010, 86: 415-421. 10.1136/sti.2010.042648.CrossRefPubMed
5.
go back to reference Unemo M, Nicholas RA: Emergence of multi-drug resistant, extensively drug-resistant and untreatable gonorrhea. Future Microbiol. 2012, 7: 1401-1422. 10.2217/fmb.12.117.CrossRefPubMedPubMedCentral Unemo M, Nicholas RA: Emergence of multi-drug resistant, extensively drug-resistant and untreatable gonorrhea. Future Microbiol. 2012, 7: 1401-1422. 10.2217/fmb.12.117.CrossRefPubMedPubMedCentral
6.
go back to reference Tapsall J: Antimicrobial resistance in Neisseria gonorrhoeae. WHO/CDS/DRS/2001.3:16. 2001, Geneva: World Health Organisation (WHO) Tapsall J: Antimicrobial resistance in Neisseria gonorrhoeae. WHO/CDS/DRS/2001.3:16. 2001, Geneva: World Health Organisation (WHO)
7.
9.
go back to reference Unemo M, Golparian D, Nicholas R, et al: 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: 1273-1280. 10.1128/AAC.05760-11.CrossRefPubMedPubMedCentral Unemo M, Golparian D, Nicholas R, et al: 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: 1273-1280. 10.1128/AAC.05760-11.CrossRefPubMedPubMedCentral
12.
go back to reference Lewis DA, Sriruttan C, Müller EE, et al: 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: 1267-1270. 10.1093/jac/dkt034.CrossRefPubMed Lewis DA, Sriruttan C, Müller EE, et al: 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: 1267-1270. 10.1093/jac/dkt034.CrossRefPubMed
13.
go back to reference Allen VG, Mitterni L, Seah C, et al: Neisseria gonorrhoeae treatment failure and susceptibility to cefixime in Toronto, Canada. JAMA. 2013, 309: 163-170. 10.1001/jama.2012.176575.CrossRefPubMed Allen VG, Mitterni L, Seah C, et al: Neisseria gonorrhoeae treatment failure and susceptibility to cefixime in Toronto, Canada. JAMA. 2013, 309: 163-170. 10.1001/jama.2012.176575.CrossRefPubMed
14.
go back to reference Tapsall J, Read P, Carmody C, et al: Two cases of failed ceftriaxone treatment in pharyngeal gonorrhoea verified by molecular microbiological methods. J Med Microbiol. 2009, 58: 683-687. 10.1099/jmm.0.007641-0.CrossRefPubMed Tapsall J, Read P, Carmody C, et al: Two cases of failed ceftriaxone treatment in pharyngeal gonorrhoea verified by molecular microbiological methods. J Med Microbiol. 2009, 58: 683-687. 10.1099/jmm.0.007641-0.CrossRefPubMed
17.
go back to reference Ohnishi M, Golparian D, Shimuta K, et al: 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: 3538-3545. 10.1128/AAC.00325-11.CrossRefPubMedPubMedCentral Ohnishi M, Golparian D, Shimuta K, et al: 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: 3538-3545. 10.1128/AAC.00325-11.CrossRefPubMedPubMedCentral
18.
go back to reference Chen YM, Stevens K, Tideman R, et al: Failure of ceftriaxone 500 mg to eradicate pharyngeal gonorrhoea, Australia. J Antimicrob Chemother. 2013, 68: 1445-1447. 10.1093/jac/dkt017.CrossRef Chen YM, Stevens K, Tideman R, et al: Failure of ceftriaxone 500 mg to eradicate pharyngeal gonorrhoea, Australia. J Antimicrob Chemother. 2013, 68: 1445-1447. 10.1093/jac/dkt017.CrossRef
19.
go back to reference Cámara J, Serra J, Ayats J, et al: Molecular characterization of two high-level ceftriaxone-resistant Neisseria gonorrhoeae isolates detected in Catalonia, Spain. J Antimicrob Chemother. 2012, 67: 1858-1860. 10.1093/jac/dks162.CrossRefPubMed Cámara J, Serra J, Ayats J, et al: Molecular characterization of two high-level ceftriaxone-resistant Neisseria gonorrhoeae isolates detected in Catalonia, Spain. J Antimicrob Chemother. 2012, 67: 1858-1860. 10.1093/jac/dks162.CrossRefPubMed
23.
go back to reference Bignell C, Unemo M, on behalf of the European STI Guidelines Editorial Board: European guideline on the diagnosis and treatment of gonorrhoea in adults. Int J STD AIDS. 2013, 24: 85-92. 10.1177/0956462412472837.CrossRefPubMed Bignell C, Unemo M, on behalf of the European STI Guidelines Editorial Board: European guideline on the diagnosis and treatment of gonorrhoea in adults. Int J STD AIDS. 2013, 24: 85-92. 10.1177/0956462412472837.CrossRefPubMed
24.
go back to reference Ameyama S, Onodera S, Takahata M, et al: 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: 3744-3749. 10.1128/AAC.46.12.3744-3749.2002.CrossRefPubMedPubMedCentral Ameyama S, Onodera S, Takahata M, et al: 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: 3744-3749. 10.1128/AAC.46.12.3744-3749.2002.CrossRefPubMedPubMedCentral
25.
go back to reference Ito M, Deguchi T, Mizutani KS, et al: 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: 137-143. 10.1128/AAC.49.1.137-143.2005.CrossRefPubMedPubMedCentral Ito M, Deguchi T, Mizutani KS, et al: 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: 137-143. 10.1128/AAC.49.1.137-143.2005.CrossRefPubMedPubMedCentral
26.
go back to reference Lee SG, Lee H, Jeong SH, et al: Various penA mutations together with mtrR, porB and ponA mutations in Neisseria gonorrhoeae isolates with reduced susceptibility to cefixime or ceftriaxone. J Antimicrob Chemother. 2010, 65: 669-675. 10.1093/jac/dkp505.CrossRefPubMedPubMedCentral Lee SG, Lee H, Jeong SH, et al: Various penA mutations together with mtrR, porB and ponA mutations in Neisseria gonorrhoeae isolates with reduced susceptibility to cefixime or ceftriaxone. J Antimicrob Chemother. 2010, 65: 669-675. 10.1093/jac/dkp505.CrossRefPubMedPubMedCentral
27.
go back to reference Osaka K, Takakura T, Narukawa K, et al: Analysis of amino acid sequences of penicillin-binding protein 2 in clinical isolates of Neisseria gonorrhoeae with reduced susceptibility to cefixime and ceftriaxone. J Infect Chemother. 2008, 14: 195-203. 10.1007/s10156-008-0610-7.CrossRefPubMed Osaka K, Takakura T, Narukawa K, et al: Analysis of amino acid sequences of penicillin-binding protein 2 in clinical isolates of Neisseria gonorrhoeae with reduced susceptibility to cefixime and ceftriaxone. J Infect Chemother. 2008, 14: 195-203. 10.1007/s10156-008-0610-7.CrossRefPubMed
28.
go back to reference Takahata S, Senju N, Osaki Y, et al: 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: 3638-3645. 10.1128/AAC.00626-06.CrossRefPubMedPubMedCentral Takahata S, Senju N, Osaki Y, et al: 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: 3638-3645. 10.1128/AAC.00626-06.CrossRefPubMedPubMedCentral
29.
go back to reference Tomberg J, Unemo M, Davies C, et al: 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: 8062-8070. 10.1021/bi101167x.CrossRefPubMedPubMedCentral Tomberg J, Unemo M, Davies C, et al: 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: 8062-8070. 10.1021/bi101167x.CrossRefPubMedPubMedCentral
30.
go back to reference Zhao S, Duncan M, Tomberg J, et al: Genetics of chromosomally mediated intermediate resistance to ceftriaxone and cefixime in Neisseria gonorrhoeae. Antimicrob Agents Chemother. 2009, 53: 3744-3751. 10.1128/AAC.00304-09.CrossRefPubMedPubMedCentral Zhao S, Duncan M, Tomberg J, et al: Genetics of chromosomally mediated intermediate resistance to ceftriaxone and cefixime in Neisseria gonorrhoeae. Antimicrob Agents Chemother. 2009, 53: 3744-3751. 10.1128/AAC.00304-09.CrossRefPubMedPubMedCentral
31.
go back to reference Unemo M, Dillon JA: Review and international recommendation of methods for typing Neisseria gonorrhoeae isolates and their implications for improved knowledge of gonococcal epidemiology, treatment, and biology. Clin Microbiol Rev. 2011, 24: 447-458. 10.1128/CMR.00040-10.CrossRefPubMedPubMedCentral Unemo M, Dillon JA: Review and international recommendation of methods for typing Neisseria gonorrhoeae isolates and their implications for improved knowledge of gonococcal epidemiology, treatment, and biology. Clin Microbiol Rev. 2011, 24: 447-458. 10.1128/CMR.00040-10.CrossRefPubMedPubMedCentral
32.
go back to reference Majewski S, Rudnicka I, Dajek Z: Zapalenia cewki moczowej i narządu rodnego in: Postępowanie w przypadku rozpoznania chorób przenoszonych drogą płciową: Czelej. 2000, Lublin, 5-8. In Polish, 1, In Polish Majewski S, Rudnicka I, Dajek Z: Zapalenia cewki moczowej i narządu rodnego in: Postępowanie w przypadku rozpoznania chorób przenoszonych drogą płciową: Czelej. 2000, Lublin, 5-8. In Polish, 1, In Polish
33.
go back to reference Jablonska S, Majewski S: Choroby przenoszone droga płciowa. Choroby skóry i choroby przenoszone drogą plciowa. 2010, Polish: PZWL Warsaw, 457-507. Jablonska S, Majewski S: Choroby przenoszone droga płciowa. Choroby skóry i choroby przenoszone drogą plciowa. 2010, Polish: PZWL Warsaw, 457-507.
34.
go back to reference Hoffmann B, Monsiorska-Borowska Z, Araszkiewicz M, et al: Assessment of sensitivity to penicillin and other antibiotics in Neisseria gonorrhoeae in Poland in 1973. Pol Tyg Lek. 1974, 29: 1151-1154. In PolishPubMed Hoffmann B, Monsiorska-Borowska Z, Araszkiewicz M, et al: Assessment of sensitivity to penicillin and other antibiotics in Neisseria gonorrhoeae in Poland in 1973. Pol Tyg Lek. 1974, 29: 1151-1154. In PolishPubMed
35.
go back to reference Michalska-Trenkner E, Dratwiński Z, Wiewiórkowska L: Drug resistance of Neisseria gonorrhoeae in the Gdansk Province. Przegl Dermatol. 1975, 62: 377-382. In PolishPubMed Michalska-Trenkner E, Dratwiński Z, Wiewiórkowska L: Drug resistance of Neisseria gonorrhoeae in the Gdansk Province. Przegl Dermatol. 1975, 62: 377-382. In PolishPubMed
36.
go back to reference Stapinski A, Mroczkowski TF, Dajek Z, et al: 1st cases of gonorrhea caused by penicillinase-producing Neisseria gonorrhoeae in Poland. Przegl Dermatol. 1979, 66: 487-494. In PolishPubMed Stapinski A, Mroczkowski TF, Dajek Z, et al: 1st cases of gonorrhea caused by penicillinase-producing Neisseria gonorrhoeae in Poland. Przegl Dermatol. 1979, 66: 487-494. In PolishPubMed
37.
go back to reference Mlynarczyk-Bonikowska B, Przedpelska G, Malejczyk M, et al: Penicillinase production by Neisseria gonorrhoeae strains isolated from the patients of Dermatology and Wenerology Clinic, Warsaw Medical University in 2006–2009. Med Dosw Mikrobiol. 2011, 63: 115-120. In PolishPubMed Mlynarczyk-Bonikowska B, Przedpelska G, Malejczyk M, et al: Penicillinase production by Neisseria gonorrhoeae strains isolated from the patients of Dermatology and Wenerology Clinic, Warsaw Medical University in 2006–2009. Med Dosw Mikrobiol. 2011, 63: 115-120. In PolishPubMed
38.
go back to reference Linda H, Dzierzanowska D, Bramska S: Studies on the effectiveness of cephalosporins against Neisseria gonorrhoeae. Przegl Dermatol. 1979, 66: 685-688. In PolishPubMed Linda H, Dzierzanowska D, Bramska S: Studies on the effectiveness of cephalosporins against Neisseria gonorrhoeae. Przegl Dermatol. 1979, 66: 685-688. In PolishPubMed
39.
go back to reference Tapsall JW, Cheng JK: Rapid identification of pathogenic species of Neisseria by carbohydrate degradation tests: importance of glucose in media used for preparation of inocula. Br J Ven Dis. 1981, 57: 249-252. Tapsall JW, Cheng JK: Rapid identification of pathogenic species of Neisseria by carbohydrate degradation tests: importance of glucose in media used for preparation of inocula. Br J Ven Dis. 1981, 57: 249-252.
40.
go back to reference Unemo M, Olcen P, Berglund T, et al: Molecular epidemiology of Neisseria gonorrhoeae: sequence analysis of the porB gene confirms presence of two circulating strains. J Clin Microbiol. 2002, 40: 3741-3749. 10.1128/JCM.40.10.3741-3749.2002.CrossRefPubMedPubMedCentral Unemo M, Olcen P, Berglund T, et al: Molecular epidemiology of Neisseria gonorrhoeae: sequence analysis of the porB gene confirms presence of two circulating strains. J Clin Microbiol. 2002, 40: 3741-3749. 10.1128/JCM.40.10.3741-3749.2002.CrossRefPubMedPubMedCentral
41.
go back to reference Unemo M, Fasth O, Fredlund H, et al: 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. 2009, 63: 1142-1151. 10.1093/jac/dkp098.CrossRefPubMed Unemo M, Fasth O, Fredlund H, et al: 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. 2009, 63: 1142-1151. 10.1093/jac/dkp098.CrossRefPubMed
42.
go back to reference Martin IM, Ison CA, Aanensen DM, et al: Rapid sequence-based identification of gonococcal transmission clusters in a large metropolitan area. J Infect Dis. 2004, 189: 1497-1505. 10.1086/383047.CrossRefPubMed Martin IM, Ison CA, Aanensen DM, et al: Rapid sequence-based identification of gonococcal transmission clusters in a large metropolitan area. J Infect Dis. 2004, 189: 1497-1505. 10.1086/383047.CrossRefPubMed
43.
go back to reference Unemo M, Olcén P, Fredlund H, et al: 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: 1004-1008. 10.1111/j.1600-0463.2008.01062.x.CrossRefPubMed Unemo M, Olcén P, Fredlund H, et al: 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: 1004-1008. 10.1111/j.1600-0463.2008.01062.x.CrossRefPubMed
44.
go back to reference Deguchi T, Yasuda M, Yokoi S, et al: Treatment of uncomplicated gonococcal urethritis by double-dosing of 200 mg cefixime at a 6-h interval. J Infect Chemother. 2003, 9: 35-39. 10.1007/s10156-002-0204-8.CrossRefPubMed Deguchi T, Yasuda M, Yokoi S, et al: Treatment of uncomplicated gonococcal urethritis by double-dosing of 200 mg cefixime at a 6-h interval. J Infect Chemother. 2003, 9: 35-39. 10.1007/s10156-002-0204-8.CrossRefPubMed
Metadata
Title
Antimicrobial susceptibility/resistance and genetic characteristics of Neisseria gonorrhoeaeisolates from Poland, 2010-2012
Authors
Beata Mlynarczyk-Bonikowska
Agnieszka Beata Serwin
Daniel Golparian
Szymon Walter de Walthoffen
Slawomir Majewski
Marta Koper
Magdalena Malejczyk
Marius Domeika
Magnus Unemo
Publication date
01-12-2014
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2014
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/1471-2334-14-65

Other articles of this Issue 1/2014

BMC Infectious Diseases 1/2014 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.