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Surveillance Open Access
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Abstract

Background

Gonococcal antimicrobial resistance is emerging worldwide and is monitored in the Netherlands in 18 of 24 Sexual Health Centres (SHC).

Aim

To report trends, predictors and regional variation of gonococcal azithromycin resistance (AZI-R, minimum inhibitory concentration (MIC) > 1 mg/L) and ceftriaxone decreased susceptibility (CEF-DS, MIC > 0.032 mg/L) in 2013–2019.

Methods

SHC reported data on individual characteristics, sexually transmitted infection diagnoses, and susceptibility testing (MIC, measured by Etest). We used multilevel logistic regression analysis to identify AZI-R/CEF-DS predictors, correcting for SHC region. Population differences’ effect on regional variance of AZI-R and CEF-DS was assessed with a separate multilevel model.

Results

The study included 13,172 isolates, predominantly (n = 9,751; 74%) from men who have sex with men (MSM). Between 2013 and 2019, annual proportions of AZI-R isolates appeared to increase from 2.8% (37/1,304) to 9.3% (210/2,264), while those of CEF-DS seemed to decrease from 7.0% (91/1,306) to 2.9% (65/2,276). Among SHC regions, 0.0‒16.9% isolates were AZI-R and 0.0−7.0% CEF-DS; population characteristics could not explain regional variance. Pharyngeal strain origin and consultation year were significantly associated with AZI-R and CEF-DS for MSM, women, and heterosexual men. Among women and heterosexual men ≥ 4 partners was associated with CEF-DS, and ≥ 10 with AZI-R.

Conclusions

No resistance or decreasing susceptibility was found for CEF, the first line gonorrhoea treatment in the Netherlands. Similar to trends worldwide, AZI-R appeared to increase. Regional differences between SHC support nationwide surveillance with regional-level reporting. The increased risk of resistance/decreased susceptibility in pharyngeal strains underlines the importance of including extragenital infections in gonococcal resistance surveillance.

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2022-08-25
2024-10-31
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2022.27.34.2200081
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References

  1. Staritsky LE, Van Aar F, Visser M, Op de Coul E, Heijne JC, Götz HM, et al. Sexually Transmitted Infections in the Netherlands in 2019. Bilthoven: National Institute for Public Health and the Environment, 2020.
  2. European Centre for Disease Prevention and Control (ECDC). Gonococcal antimicrobial susceptibility surveillance in Europe, 2015. Stockholm: ECDC; 2017. Available from: https://www.ecdc.europa.eu/en/publications-data/gonococcal-antimicrobial-susceptibility-surveillance-europe-2015
  3. Koedijk FD, van Veen MG, de Neeling AJ, Linde GB, van der Sande MA. Increasing trend in gonococcal resistance to ciprofloxacin in The Netherlands, 2006-8. Sex Transm Infect. 2010;86(1):41-5.  https://doi.org/10.1136/sti.2009.037135  PMID: 19703843 
  4. Whiley DM, Jennison A, Pearson J, Lahra MM. Genetic characterisation of Neisseria gonorrhoeae resistant to both ceftriaxone and azithromycin. Lancet Infect Dis. 2018;18(7):717-8.  https://doi.org/10.1016/S1473-3099(18)30340-2  PMID: 29976521 
  5. Eyre DW, Sanderson ND, Lord E, Regisford-Reimmer N, Chau K, Barker L, et al. Gonorrhoea treatment failure caused by a Neisseria gonorrhoeae strain with combined ceftriaxone and high-level azithromycin resistance, England, February 2018. Euro Surveill. 2018;23(27).  https://doi.org/10.2807/1560-7917.ES.2018.23.27.1800323  PMID: 29991383 
  6. World Health Organization (WHO). WHO guidelines for the treatment of Neisseria gonorrhoeae. Geneva: WHO, 2016.
  7. European Centre for Disease Prevention and Control (ECDC). Response plan to control and manage the threat of multi- and extensively drug-resistant gonorrhoea in Europe – 2019 update. Stockholm: ECDC; 2019.
  8. Hofstraat SH, Götz HM, van Dam AP, van der Sande MA, van Benthem BH. Trends and determinants of antimicrobial susceptibility of Neisseria gonorrhoeae in the Netherlands, 2007 to 2015. Euro Surveill. 2018;23(36).  https://doi.org/10.2807/1560-7917.ES.2018.23.36.1700565  PMID: 30205870 
  9. European Committee on Antimicrobial Susceptibility Testing (EUCAST). Breakpoint tables for interpretation of MICs and zone diameters. Secondary Breakpoint tables for interpretation of MICs and zone diameters. Version 12.0, 1-1-2022; 2022. Växjö: EUCAST; 2022. Available from: http://eucast.org/clinical_breakpoints/
  10. European Committee on Antimicrobial Susceptibility Testing (EUCAST). Data from the EUCAST MIC distribution website. [Accessed 18 Aug 2022]. Available from: https://mic.eucast.org/
  11. National Institute for Public Health and Environment (RIVM). Landenlijst soa-endemische landen SOAP. [Country list endemic countries for sexually transmitted diseases]. Bilthoven: RIVM. [Accessed 18 Aug 2022]. Available from: https://www.rivm.nl/documenten/landenlijst-soa-endemische-landen-soap
  12. Merlo J, Chaix B, Ohlsson H, Beckman A, Johnell K, Hjerpe P, et al. A brief conceptual tutorial of multilevel analysis in social epidemiology: using measures of clustering in multilevel logistic regression to investigate contextual phenomena. J Epidemiol Community Health. 2006;60(4):290-7.  https://doi.org/10.1136/jech.2004.029454  PMID: 16537344 
  13. Day MJ, Jacobsson S, Spiteri G, Kulishev C, Sajedi N, Woodford N, et al. , Euro-GASP network. Significant increase in azithromycin "resistance" and susceptibility to ceftriaxone and cefixime in Neisseria gonorrhoeae isolates in 26 European countries, 2019. BMC Infect Dis. 2022;22(1):524.  https://doi.org/10.1186/s12879-022-07509-w  PMID: 35672671 
  14. George CRR, Enriquez RP, Gatus BJ, Whiley DM, Lo YR, Ishikawa N, et al. Systematic review and survey of Neisseria gonorrhoeae ceftriaxone and azithromycin susceptibility data in the Asia Pacific, 2011 to 2016. PLoS One. 2019;14(4):e0213312.  https://doi.org/10.1371/journal.pone.0213312  PMID: 30943199 
  15. Lahra MM, Shoushtari M, George CRR, Armstrong BH, Hogan TR. National Neisseria Network, Australia. Australian Gonococcal Surveillance Programme Annual Report, 2019. Commun Dis Intell (2018). 2020;44 http://dx.doi.org/10.33321/cdi.2020.44.58  PMID: 32664831 
  16. Centers for Disease Control and Prevention (CDC). Sexually Transmitted Disease Surveillance 2019. Atlanta: U.S. Department of Health and Human Services; 2021. Available from: https://www.cdc.gov/std/statistics/2019/default.htm
  17. UK Health Security Agency. Antimicrobial resistance in Neisseria gonorrhoeae in England and Wales. Key findings from the Gonococcal Resitance to Antimicrobials Surveillance Programme (GRASP 2020). London: UK Health Security Agency; 2021.
  18. de Laat MM, Wind CM, Bruisten SM, Dierdorp M, de Vries HJC, Schim van der Loeff MF, et al. Ceftriaxone Reduced Susceptible Neisseria gonorrhoeae in the Netherlands, 2009 to 2017: From PenA Mosaicism to A501T/V Nonmosaicism. Sex Transm Dis. 2019;46(9):594-601.  https://doi.org/10.1097/OLQ.0000000000001031  PMID: 31415041 
  19. Wind CM, Bruisten SM, Schim van der Loeff MF, Dierdorp M, de Vries HJC, van Dam AP. A Case-Control Study of Molecular Epidemiology in Relation to Azithromycin Resistance in Neisseria gonorrhoeae Isolates Collected in Amsterdam, the Netherlands, between 2008 and 2015. Antimicrob Agents Chemother. 2017;61(6):e02374-16.  https://doi.org/10.1128/AAC.02374-16  PMID: 28373191 
  20. de Korne-Elenbaas J, Bruisten SM, de Vries HJC, Van Dam AP. Emergence of a Neisseria gonorrhoeae clone with reduced cephalosporin susceptibility between 2014 and 2019 in Amsterdam, The Netherlands, revealed by genomic population analysis. J Antimicrob Chemother. 2021;76(7):1759-68.  https://doi.org/10.1093/jac/dkab082  PMID: 33739419 
  21. Unemo M, Ross J, Serwin A, Gomberg M, Cusini M, Jensen J. Background review for the ‘2020 European guideline for the diagnosis and treatment of gonorrhoea in adults’. Int J STD AIDS. 2021; 32(2):108-126.  https://doi.org/10.1177/0956462420948739  PMID: 33323071 
  22. Barbee LA, Golden MR. Editorial Commentary: When to Perform a Test of Cure for Gonorrhea: Controversies and Evolving Data. Clin Infect Dis. 2016;62(11):1356-9.  https://doi.org/10.1093/cid/ciw142  PMID: 26962080 
  23. Abraha M, Egli-Gany D, Low N. Epidemiological, behavioural, and clinical factors associated with antimicrobial-resistant gonorrhoea: a review. F1000 Res. 2018;7:400.  https://doi.org/10.12688/f1000research.13600.1  PMID: 29636908 
  24. Risley CL, Ward H, Choudhury B, Bishop CJ, Fenton KA, Spratt BG, et al. Geographical and demographic clustering of gonorrhoea in London. Sex Transm Infect. 2007;83(6):481-7.  https://doi.org/10.1136/sti.2007.026021  PMID: 17702771 
  25. Le Polain De Waroux O, Harris RJ, Hughes G, Crook PD. The epidemiology of gonorrhoea in London: a Bayesian spatial modelling approach. Epidemiol Infect. 2014;142(1):211-20.  https://doi.org/10.1017/S0950268813000745  PMID: 23561246 
  26. Town K, Harris S, Sánchez-Busó L, Cole MJ, Pitt R, Fifer H, et al. Genomic and Phenotypic Variability in Neisseria gonorrhoeae Antimicrobial Susceptibility, England. Emerg Infect Dis. 2020;26(3):505-15.  https://doi.org/10.3201/eid2603.190732  PMID: 32091356 
  27. Hernando Rovirola C, Spiteri G, Sabidó M, Montoliu A, Gonzalez V, Casabona J, et al. Antimicrobial resistance in Neisseria gonorrhoeae isolates from foreign-born population in the European Gonococcal Antimicrobial Surveillance Programme. Sex Transm Infect. 2020;96(3):204-10.  https://doi.org/10.1136/sextrans-2018-053912  PMID: 32019895 
  28. Williamson DA, Fairley CK, Howden BP, Chen MY, Stevens K, De Petra V, et al. Trends and Risk Factors for Antimicrobial-Resistant Neisseria gonorrhoeae, Melbourne, Australia, 2007 to 2018. Antimicrob Agents Chemother. 2019;63(10):e01221-19.  https://doi.org/10.1128/AAC.01221-19  PMID: 31383663 
  29. Kenyon C, Buyze J, Spiteri G, Cole MJ, Unemo M. Population-Level Antimicrobial Consumption Is Associated With Decreased Antimicrobial Susceptibility in Neisseria gonorrhoeae in 24 European Countries: An Ecological Analysis. J Infect Dis. 2020;221(7):1107-16. PMID: 30957153 
  30. Fifer H, Saunders J, Soni S, Sadiq ST, FitzGerald M. 2018 UK national guideline for the management of infection with Neisseria gonorrhoeae. Int J STD AIDS. 2020;31(1):4-15.  https://doi.org/10.1177/0956462419886775  PMID: 31870237 
  31. St Cyr S, Barbee L, Workowski KA, Bachmann LH, Pham C, Schlanger K, et al. Update to CDC’s Treatment Guidelines for Gonococcal Infection, 2020. MMWR Morb Mortal Wkly Rep. 2020;69(50):1911-6.  https://doi.org/10.15585/mmwr.mm6950a6  PMID: 33332296 
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