Antimicrobial resistance in Neisseria gonorrhoeae isolates from foreign-born population in the European Gonococcal Antimicrobial Surveillance Programme

Cristina Hernando Rovirola, Gianfranco Spiteri, Meritxell Sabidó, Alexandra Montoliu, Victoria Gonzalez, Jordi Casabona, Michelle Jayne Cole, Teymur Noori, Magnus Unemo, Cristina Hernando Rovirola, Gianfranco Spiteri, Meritxell Sabidó, Alexandra Montoliu, Victoria Gonzalez, Jordi Casabona, Michelle Jayne Cole, Teymur Noori, Magnus Unemo

Abstract

Objectives: International spread has contributed substantially to the high prevalence of antimicrobial resistant (AMR) Neisseria gonorrhoeae infections worldwide. We compared the prevalence of AMR gonococcal isolates among native persons to foreign-born (reporting country different from country of birth) persons, and describe the epidemiological and clinical characteristics of foreign-born patients and their associations to AMR.

Methods: We analysed isolates and patient data reported to the European Gonococcal Antimicrobial Surveillance Programme (Euro-GASP) 2010-2014 (n=9529).

Results: Forty-three per cent of isolates had known country of birth and 17.2% of these were from persons born abroad. Almost 50% of foreign-born were from the WHO European Region (13.1% from non-European Union [EU] and the European Economic Area [EEA] countries). Compared with isolates from natives, isolates from foreign-born had a similar level (p>0.05) of azithromycin resistance (7.5% vs 7.2%), ciprofloxacin resistance (50.0% vs 46.3%) and of decreased susceptibility to ceftriaxone (1.9% vs 2.8%); a lower rate of cefixime resistance (5.7% vs 3.6%, p=0.02), and a higher proportion of isolates producing penicillinase (8.4% vs 11.7%, p=0.02). Among isolates from persons born outside EU/EEA, the level of decreased susceptibility to ceftriaxone was higher (1.8% vs 3.5%, p=0.02), particularly in those from the WHO Eastern Mediterranean Region and non-EU/EEA WHO European countries (1.9% vs 9.6% and 8.7%, respectively, p<0.01). In multivariable analysis, foreign-born patients with AMR isolates were more likely to be from non-EU/EEA WHO European countries (adjusted OR [aOR]: 3.2, 95% CI 1.8 to 5.8), WHO Eastern Mediterranean countries (aOR: 1.8, 95% CI 1.1 to 3.3) and heterosexual males (aOR: 1.8, 95% CI 1.2 to 2.7).

Conclusions: Importation of AMR strains remains an important threat in the EU/EEA. Research to improve understanding of sexual networks within foreign born and sexual tourism populations could help to inform effective tailor-made interventions. The Euro-GASP demonstrates the public health value of quality-assured surveillance of gonococcal AMR and the need for strengthened AMR surveillance, particularly in the non-EU/EEA WHO European Region.

Keywords: Euro-GASP; Europe; antimicrobial resistance; ceftriaxone; gonorrhoea; migrants; surveillance; treatment.

Conflict of interest statement

Competing interests: None declared.

© Author(s) (or their employer(s)) 2020. Re-use permitted under CC BY-NC. No commercial re-use. See rights and permissions. Published by BMJ.

References

    1. Bignell C, Unemo M. European guideline on the diagnosis and treatment of gonorrhoea in adults. Int J STD AIDS 2012;2013:85–92.
    1. Unemo M, Shafer WM. Antimicrobial resistance in Neisseria gonorrhoeae in the 21st century: past, evolution, and future. Clin Microbiol Rev 2014;27:587–613. 10.1128/CMR.00010-14
    1. European Centre for Disease Prevention and Control (ECDC) Response plan to control and manage the threat of multidrug-resistant gonorrhoea in Europe. Stockholm, 2012. Available: [Accessed 7 Nov 2018].
    1. Lebedzeu F, Golparian D, Titov L, et al. . Antimicrobial susceptibility/resistance and NG-MAST characterisation of Neisseria gonorrhoeae in Belarus, eastern Europe, 2010–2013. BMC Infect Dis 2015;15 10.1186/s12879-015-0755-9
    1. Kubanova A, Kubanov A, Frigo N, et al. . Russian gonococcal antimicrobial susceptibility programme (RU-GASP) – resistance in Neisseria gonorrhoeae during 2009–2012 and NG-MAST genotypes in 2011 and 2012. BMC Infect Dis 2014;14 10.1186/1471-2334-14-342
    1. Cole MJ, Spiteri G, Jacobsson S, et al. . Overall low extended-spectrum cephalosporin resistance but high azithromycin resistance in Neisseria gonorrhoeae in 24 European countries, 2015. BMC Infect Dis 2017;17 10.1186/s12879-017-2707-z
    1. Wi T, Lahra MM, Ndowa F, et al. . Antimicrobial resistance in Neisseria gonorrhoeae: Global surveillance and a call for international collaborative action. PLoS Med 2017;14:e1002344 10.1371/journal.pmed.1002344
    1. Unemo M. Current and future antimicrobial treatment of gonorrhoea – the rapidly evolving Neisseria gonorrhoeae continues to challenge. BMC Infect Dis 2015;15 10.1186/s12879-015-1029-2
    1. World Health Organization (WHO) WHO guidelines for the treatment of Neisseria gonorrhoeae. Geneva, 2016. Available: [Accessed 7 Nov 2018].
    1. Lahra MM, Martin I, Demczuk W, et al. . Cooperative Recognition of Internationally Disseminated Ceftriaxone-Resistant Neisseria gonorrhoeae Strain. Emerg Infect Dis 2018;24 10.3201/eid2404.171873
    1. Fifer H, Natarajan U, Jones L, et al. . Failure of dual antimicrobial therapy in treatment of gonorrhea. N Engl J Med 2016;374:2504–6. 10.1056/NEJMc1512757
    1. Eyre DW, Sanderson ND, Lord E, 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 10.2807/1560-7917.ES.2018.23.27.1800323
    1. Whiley DM, Jennison A, Pearson J, et al. . Genetic characterisation of Neisseria gonorrhoeae resistant to both ceftriaxone and azithromycin. Lancet Infect Dis 2018;18:717–8. 10.1016/S1473-3099(18)30340-2
    1. World Health Organization (WHO) Global action plan to control the spread and impact of antimicrobial resistance in Neisseria gonorrhoeae. Geneva, 2012. Available: [Accessed 7 Nov 2018].
    1. Simon J, Kiss N, Łaszewska A. Public health aspects of migrant health: a review of the evidence on health status for labour migrants in the European region. Copenhagen: who regional office for Europe, 2015. Available: [Accessed 7 Nov 2018].
    1. EUROSTAT Your key to European statistics. [Internet]. Available: [Accessed 7 Nov 2018].
    1. Suk JE, Semenza JC. Future infectious disease threats to Europe. Am J Public Health 2011;101:2068–79. 10.2105/AJPH.2011.300181
    1. Smith E. Sexually transmitted infections among immigrants in Denmark. Is it a problem?]. UgeskrLaeger 2000;162:6237–40. In Danish.
    1. Kyriakis KP, Hadjivassiliou M, Paparizos VA, et al. . Incidence determinants of gonorrhea, chlamydial genital infection, syphilis and chancroid in attendees at a sexually transmitted disease clinic in Athens, Greece. Int J Dermatol 2003;42:876–81. 10.1046/j.1365-4362.2003.01737.x
    1. European Centre for Disease Prevention and Control (ECDC) Assessing the burden of key infectious diseases affecting migrant populations in the EU/EEA. Stockholm, 2014. Available: [Accessed 7 Nov 2018].
    1. European Centre for Disease Prevention and Control (ECDC) Gonococcal antimicrobial susceptibility surveillance in Europe, 2014. Stockholm, 2016. Available: [Accessed 7 Nov 2018].
    1. IOM Glossary on migration. International migration law series. Geneva, 2011. Available: [Accessed 7 Nov 2018].
    1. Unemo M, Golparian D, Sánchez-Busó L, et al. . The novel 2016 WHO Neisseria gonorrhoeae reference strains for global quality assurance of laboratory investigations: phenotypic, genetic and reference genome characterization. J Antimicrob Chemother 2016;71:3096–108. 10.1093/jac/dkw288
    1. The European committee on antimicrobial susceptibility testing Breakpoint tables for interpretation of MICs and zone diameters. version 8.1, 2018. Available: [Accessed 7 Nov 2018].
    1. Jeverica S, Golparian D, Matičič M, et al. . Phenotypic and molecular characterization of Neisseria gonorrhoeae isolates from Slovenia, 2006-12: rise and fall of the multidrug-resistant NG-MAST genogroup 1407 clone? J Antimicrob Chemother 2014;69:1517–25. 10.1093/jac/dku026
    1. 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;9:35–9. 10.1007/s10156-002-0204-8
    1. Harris SR, Cole MJ, Spiteri G, et al. . Public health surveillance of multidrug-resistant clones of Neisseria gonorrhoeae in Europe: a genomic survey. Lancet Infect Dis 2018;18:758–68. 10.1016/S1473-3099(18)30225-1
    1. Demczuk W, Lynch T, Martin I, et al. . Whole-genome phylogenomic heterogeneity of Neisseria gonorrhoeae isolates with decreased cephalosporin susceptibility collected in Canada between 1989 and 2013. J Clin Microbiol 2015;53:191–200. 10.1128/JCM.02589-14
    1. Grad YH, Harris SR, Kirkcaldy RD, et al. . Genomic Epidemiology of gonococcal resistance to extended-spectrum cephalosporins, macrolides, and fluoroquinolones in the United States, 2000–2013. J Infect Dis 2016;214:1579–87. 10.1093/infdis/jiw420
    1. MacPherson DW, Gushulak BD, Baine WB, et al. . Population mobility, globalization, and antimicrobial drug resistance. Emerg Infect Dis 2009;15:1727–32. 10.3201/eid1511.090419

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