Neisseria gonorrhoeae sequence typing for antimicrobial resistance, a novel antimicrobial resistance multilocus typing scheme for tracking global dissemination of N. Gonorrhoeae strains

Journal of Clinical Microbiology

Volumn 55, Issue 5, 2017, Pages 1454-1468

  Demczuk, W ^a   Sidhu, S ^a   Unemo, M ^b   Whiley, D M ^c   Allen, V G ^d   Dillon, J R ^e   Cole, M ^f   Seah, C ^d   Trembizki, E ^c   Trees, D L ^g   Kersh, E N ^g   Abrams, A J ^g   De Vries, H J C ^h,i   Van Dam, A P ^h,j   Medina, I ^a   Bharat, A ^a   Mulvey, M R ^a   Van Domselaar, G ^a   Martin, I ^a  

^a PUBLIC HEALTH AGENCY OF CANADA   (Canada)

^b ÖREBRO UNIVERSITY HOSPITAL   (Sweden)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d PUBLIC HEALTH ONTARIO   (Canada)

^e UNIVERSITY OF SASKATCHEWAN   (Canada)

^f PUBLIC HEALTH ENGLAND   (United Kingdom)

^g CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^h DEPARTMENT OF INFECTIOUS DISEASES   (Netherlands)

ⁱ UNIVERSITY OF AMSTERDAM   (Netherlands)

^j ONZE LIEVE VROUWE GASTHUIS   (Netherlands)

more..

Author keywords

Antimicrobial resistance; Molecular epidemiology; Neisseria gonorrhoeae; Sequence typing

Indexed keywords

AZITHROMYCIN; BACTERIAL RNA; CEFIXIME; CEFTRIAXONE; CEPHALOSPORIN; CIPROFLOXACIN; RNA 23S; ANTIINFECTIVE AGENT; CEPHALOSPORIN DERIVATIVE; QUINOLONE DERIVATIVE;

ALLELE; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL TRANSMISSION; DNA SEQUENCE; GENE LOCUS; GYRA GENE; INFORMATION PROCESSING; MTRR GENE; MULTILOCUS SEQUENCE TYPING; NEISSERIA GONORRHOEAE; NEISSERIA GONORRHOEAE SEQUENCE TYPING FOR ANTIMICROBIAL RESISTANCE; PARC GENE; PONA GENE; PORB GENE; PRIORITY JOURNAL; PROMOTER REGION; SOFTWARE; AMINO ACID SEQUENCE; CLASSIFICATION; DRUG EFFECTS; GENETICS; GONORRHEA; HUMAN; ISOLATION AND PURIFICATION; MICROBIOLOGY; MULTIDRUG RESISTANCE; PROCEDURES;

AMINO ACID SEQUENCE; ANTI-BACTERIAL AGENTS; AZITHROMYCIN; CEPHALOSPORINS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; FLUOROQUINOLONES; GONORRHEA; HUMANS; MULTILOCUS SEQUENCE TYPING; NEISSERIA GONORRHOEAE;

EID: 85018273210     PISSN: 00951137     EISSN: 1098660X     Source Type: Journal    
DOI: 10.1128/JCM.00100-17     Document Type: Article

References (47)

1. Newman L, Rowley J, Hoorn SV, Wijesooriya NS, Unemo M, Low N, Stevens G, Gottlieb S, Kiarie J, Temmerman M. 2015. Global estimates of the prevalence and incidence of four curable sexually transmitted infections in 2012 based on systematic review and global reporting. PLoS One 10:e0143304. https://doi.org/10.1371/journal.pone.0143304.
2. Lewis DA. 2010. The gonococcus fights back: is this time a knock out? Sex Transm Infect 86:415-421. https://doi.org/10.1136/sti.2010.042648.
3. Unemo M, Shafer WM. 2014. Antimicrobial resistance in Neisseria gonorrhoeae in the 21st century: past, evolution, and future. Clin Microbiol Rev 27:587-613. https://doi.org/10.1128/CMR.00010-14.
4. Allen VG, Mitterni L, Seah C, Rebbapragada A, Martin IE, Lee C, Siebert H, Towns L, Melano RG, Lowe DE. 2013. Neisseria gonorrhoeae treatment failure and susceptibility to cefixime in Toronto, Canada. JAMA 309: 163-170. https://doi.org/10.1001/jama.2012.176575.
5. Ison CA, Hussey J, Sankar KN, Evans J, Alexander S. 2011. Gonorrhoea treatment failures to cefixime and azithromycin in England, 2010. Euro Surveill 16(14):pii-19833. http://www.eurosurveillance.org/View Article.aspx?Articled-19833.
6. Lewis DA, Sriruttan C, Müller EE, Golparian D, Gumede L, Fick D, de Wet J, Maseko V, Coetzee J, Unemo M. 2013. Phenotypic and genetic characterization of the first two cases of extended-spectrum-cephalosporinresistant Neisseria gonorrhoeae infection in South Africa and association with cefixime treatment failure. J Antimicrob Chemother 68:1267-1270. https://doi.org/10.1093/jac/dkt034.
7. Unemo M, Golparian D, Stary A, Eigentler A. 2011. First Neisseria gonorrhoeae strain with resistance to cefixime causing gonorrhoea treatment failure in Austria, 2011. Euro Surveill 16(43):pii-19998. http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId-19998.
8. Unemo M, Golparian D, Syversen G, Vestrheim DF, Moi H. 2010. Two cases of verified clinical failures using internationally recommended first-line cefixime for gonorrhoea treatment, Norway, 2010. Euro Surveill 15(47): pii-19721. http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId-19721.
9. Ohnishi M, Golparian D, Shimuta K, Saika T, Hoshina S, Iwasaku K, Nakayama S, Kitawaki J, Unemo M. 2011. 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 55:3538-3545. https://doi.org/10.1128/AAC.00325-11.
10. Gratrix J, Bergman J, Egan C, Drews SJ, Read R, Singh AE. 2013. Retrospective review of pharyngeal gonorrhea treatment failures in Alberta, Canada. Sex Transm Dis 40:877-879. https://doi.org/10.1097/OLQ.0000000000000033.
11. Unemo M, Golparian D, Nicholas R, Ohnishi M, Gallay A, Sednaouie P. 2012. 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 56: 1273-1280. https://doi.org/10.1128/AAC.05760-11.
12. Allen VG, Seah C, Martin I, Melano RG. 2014. Azithromycin resistance is coevolving with reduced susceptibility to cephalosporins in Neisseria gonorrhoeae in Ontario, Canada. Antimicrob Agents Chemother 58: 2528-2534. https://doi.org/10.1128/AAC.02608-13.
13. Cole MJ, Spiteri G, Jacobsson S, Pitt R, Grigorjev V, Unemo M. 2015. Is the tide turning again for cephalosporin resistance in Neisseria gonorrhoeae in Europe? Results from the 2013 European surveillance. BMC Infect Dis 15:321. https://doi.org/10.1186/s12879-015-1013-x.
14. Unemo M, Golparian D, Shafer WM. 2014. Challenges with gonorrhea in the era of multi-drug and extensively drug resistance - are we on the right track? Expert Rev Anti Infect Ther 12:653-656. https://doi.org/10.1586/14787210.2014.906902.
15. Whiley DM, Goire N, Lahra MM, Donovan B, Limnios AE, Nissen MD, Sloots TP. 2012. The ticking time bomb: escalating antibiotic resistance in Neisseria gonorrhoeae is a public health disaster in waiting. J Antimicrob Chemother 67:2059-2061. https://doi.org/10.1093/jac/dks188.
16. Goire N, Lahra MM, Chen M, Donovan B, Fairley CK, Guy R, Kaldor J, Regan D, Ward J, Nissen MD, Sloots TP, Whiley DM. 2014. Molecular approaches to enhance surveillance of gonococcal antimicrobial resistance. Nat Rev Microbiol 12:223-229. https://doi.org/10.1038/nrmicro3217.
17. Ito M, Deguchi T, Mizutani KS, Yasuda M, Yokoi S, Ito SI, Takahashi Y, Ishihara S, Kawamura Y, Ezaki T. 2005. Emergence and spread of Neisseria gonorrhoeae clinical isolates harboring mosaic-like structure of penicillin-binding protein 2 in central Japan. Antimicrob Agents Chemother 49:137-143. https://doi.org/10.1128/AAC.49.1.137-143.2005.
18. Mavroidi A, Tzouvelekis LS, Kyriakis KP, Avgerinou H, Daniilidou M, Tzelepi E. 2001. Multidrug-resistant strains of Neisseria gonorrhoeae in Greece. Antimicrob Agents Chemother 45:2651-2654. https://doi.org/10.1128/AAC.45.9.2651-2654.2001.
19. Warner DM, Shafer WM, Jerse AE. 2008. Clinically relevant mutations that cause derepression of the Neisseria gonorrhoeae MtrC-MtrD-MtrE Efflux pump system confer different levels of antimicrobial resistance and in vivo fitness. Mol Microbiol 70:462-478. https://doi.org/10.1111/j.1365-2958.2008.06424.x.
20. Cousin SL, Jr, Whittington WLH, Roberts MC. 2003. Acquired macrolide resistance genes and the 1 bp deletion in the mtrR promoter in Neisseria gonorrhoeae. J Antimicrob Chemother 51:131-133. https://doi.org/10.1093/jac/dkg040.
21. Zarantonelli L, Borthagaray G, Lee EH, Shafer WM. 1999. Decreased azithromycin susceptibility of Neisseria gonorrhoeae due to mtrR mutations. Antimicrob Agents Chemother 43:2468-2472.
22. Martin IMC, Ison CA, Aanensen DM, Fenton KA, Spratt BG. 2004. Rapid sequence-based identification of gonococcal transmission clusters in a large metropolitan area. J Infect Dis 189:1497-1505. https://doi.org/10.1086/383047.
23. Lindberg R, Fredlund H, Nicholas R, Unemo M. 2007. Neisseria gonorrhoeae isolates with reduced susceptibility to cefixime and ceftriaxone: association with genetic polymorphisms in penA, mtrR, porB1b, and ponA. Antimicrob Agents Chemother 51:2117-2122. https://doi.org/10.1128/AAC.01604-06.
24. Olesky M, Hobbs M, Nicholas RA. 2002. Identification and analysis of amino acid mutations in porin IB that mediate intermediate-level resistance to penicillin and tetracycline in Neisseria gonorrhoeae. Antimicrob Agents Chemother 46:2811-2820. https://doi.org/10.1128/AAC.46.9.2811-2820.2002.
25. Olesky M, Zhao S, Rosenberg RL, Nicholas RA. 2006. Porin-mediated antibiotic resistance in Neisseria gonorrhoeae: ion, solute, and antibiotic permeation through PIB proteins with penB mutations. J Bacteriol 188: 2300-2308. https://doi.org/10.1128/JB.188.7.2300-2308.2006.
26. Ropp PA, Hu M, Olesky M, Nicholas RA. 2002. Mutations in ponA, the gene encoding penicillin-binding protein 1, and a novel locus, penC, are required for high-level chromosomally mediated penicillin resistance in Neisseria gonorrhoeae. Antimicrob Agents Chemother 46:769-777. https://doi.org/10.1128/AAC.46.3.769-777.2002.
27. Lindback E, Rahman M, Jalal S, Wretlind B. 2002. Mutations in gyrA, gyrB, parC, and parE in quinolone-resistant strains of Neisseria gonorrhoeae. APMIS 110:651-657. https://doi.org/10.1034/j.1600-0463.2002.1100909.x.
28. Ng LK, Martin I, Liu G, Bryden L. 2002. Mutation in 23S rRNA associated with macrolide resistance in Neisseria gonorrhoeae. Antimicrob Agents Chemother 46:3020-3025. https://doi.org/10.1128/AAC.46.9.3020-3025.2002.
29. Chisholm SA, Dave J, Ison CA. 2010. High-level azithromycin resistance occurs in Neisseria gonorrhoeae as a result of a single point mutation in the 23S rRNA genes. Antimicrob Agents Chemother 54:3812-3816. https://doi.org/10.1128/AAC.00309-10.
30. Thakur SD, Levett PN, Horsman GB, Dillon JR. 2014. Molecular epidemiology of Neisseria gonorrhoeae isolates from Saskatchewan, Canada: utility of NG-MAST in predicting antimicrobial susceptibility regionally. Sex Transm Infect 90:297-302. https://doi.org/10.1136/sextrans-2013-051229.
31. Thakur SD, Starnino S, Horsman GB, Levett PN, Dillon JR. 2014. Unique combined penA/mtrR/porB mutations and NG-MAST strain types associated with ceftriaxone and cefixime MIC increases in a 'susceptible' Neisseria gonorrhoeae population. J Antimicrob Chemother 69: 1510-1516. https://doi.org/10.1093/jac/dkt543.
32. Dillon JR, Rahman M, Yeung K. 1993. Discriminatory power of typing schemes based on Simpson's index of diversity for Neisseria gonorrhoeae. J Clin Microbiol 31:2831-2833.
33. Demczuk W, Lynch T, Martin I, Van Domselaar G, Graham M, Bharat A, Allen V, Hoang L, Lefebvre B, Tyrrell G, Horsman G, Haldane D, Garceau R, Wylie J, Wong T, Mulvey MR. 2015. Whole-genome phylogenomic heterogeneity of Neisseria gonorrhoeae isolates with decreased cephalosporin susceptibility collected in Canada between 1989 and 2013. J Clin Microbiol 53:191-200. https://doi.org/10.1128/JCM.02589-14.
34. Grad YH, Harris SR, Kirkcaldy RD, Green AG, Marks DS, Bentley SD, Trees D, Lipsitch M. 2016. Genomic epidemiology of gonococcal resistance to extended-spectrum cephalosporins, macrolides and fluoroquinolones in the United States, 2000-2013. J Infect Dis 214:1579-1587. https://doi.org/10.1093/infdis/jiw420.
35. Liao M, Gu WM, Yang Y, Dillon JA. 2011. Analysis of mutations in multiple loci of Neisseria gonorrhoeae isolates reveals effects of PIB, PBP2 and MtrR on reduced susceptibility to ceftriaxone. J Antimicrob Chemother 66:1016-1023. https://doi.org/10.1093/jac/dkr021.
36. Demczuk W, Martin I, Peterson S, Bharat A, Van Domselaar G, Graham M, Lefebvre B, Allen V, Hoang L, Tyrrell G, Horsman G, Wylie J, Haldane D, Archibald C, Wong T, Unemo M, Mulvey MR. 2016. Genomic epidemiology and molecular resistance mechanisms of azithromycin-resistant Neisseria gonorrhoeae in Canada from 1997 to 2014. J Clin Microbiol 54:1304-1313. https://doi.org/10.1128/JCM.03195-15.
37. Jacobsson S, Golparian D, Cole M, Spiteri G, Martin I, Bergheim T, Borrego MJ, Crowley B, Crucitti T, Van Dam AP, Hoffmann S, Jeverica S, Kohl P, Mlynarczyk-Bonikowska B, Pakarna G, Stary A, Stefanelli P, Pavlik P, Tzelepi E, Abad R, Harris SR, Unemo M. 2016. WGS analysis and molecular resistance mechanisms of azithromycin-resistant (MIC-2 mg/L) Neisseria gonorrhoeae isolates in Europe from 2009 to 2014. J Antimicrob Chemother 71: 3109-3116. https://doi.org/10.1093/jac/dkw279.
38. Unemo M, Golparian D, Sánchez-Busó L, Grad Y, Jacobsson S, Ohnishi M, Lahra MM, Limnios A, Sikora AE, Wi T, Harris SR. 2016. The novel 2016 WHO Neisseria gonorrhoeae reference strains for global quality assurance of laboratory investigations: phenotypic, genetic and reference genome characterization. J Antimicrob Chemother 71:3096-3108. https://doi.org/10.1093/jac/dkw288.
39. Clinical and Laboratory Standards Institute. 2016. Performance standards for antimicrobial susceptibility testing. Twenty-sixth informational supplement. CLSI document, approved standard M100-S26. Clinical and Laboratory Standards Institute, Wayne, PA.
40. Public Health Agency of Canada National Microbiology Laboratory. 2015. National surveillance of antimicrobial susceptibilities of Neisseria gonorrhoeae annual summary 2014. http://healthycanadians.gc.ca/publications/drugs-products-medicaments-produits/2014-neisseria/index-eng.php. Accessed 1 May 2016.
41. Francisco AP, Vaz C, Monteiro PT, Melo-Cristino J, Ramirez M, Carriço JA. 2012. PHYLOViZ: phylogenetic inference and data visualization for sequence based typing methods. BMC Bioinformatics 13:87. https://doi.org/10.1186/1471-2105-13-87.
42. Nascimento M, Sousa A, Ramirez M, Francisco AP, Carriço JA, Vaz C. 2017. PHYLOViZ 2.0: providing scalable data integration and visualization for multiple phylogenetic inference methods. Bioinformatics 33:128-129. https://doi.org/10.1093/bioinformatics/btw582.
43. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol 215:403-410. https://doi.org/10.1016/S0022-2836(05)80360-2.
44. Dean A, Sullivan K, Soe M. 2013. OpenEpi: Open Source Epidemiologic Statistics for Public Health version 3.01. http://www.openepi.com. Accessed 8 August 2014.
45. Hunter PR, Gaston MA. 1988. Numerical index of the discriminatory ability of typing systems: an application of Simpson's index of diversity. J Clin Microbiol 26:2465-2466.
46. Serviano A, Pinto FR, Ramirez M, Carriço JA. 2011. Adjusted Wallace coefficient as a measure of congruence between typing methods. J Clin Microbiol 49:3997-4000. https://doi.org/10.1128/JCM.00624-11.
47. Ng LK, Sawatzky P, Martin IE, Booth S. 2002. Characterization of ciprofloxacin resistance in Neisseria gonorrhoeae isolates in Canada. Sex Transm Dis 29:780-788. https://doi.org/10.1097/00007435-200212000-00008.