-
Epidemiology of gonorrhoea: systematic review, meta-analyses, and meta-regressions, World Health Organization European Region, 1949 to 2021
- Omar Chidiac1,* , Sawsan AlMukdad1,2,* , Manale Harfouche1,2,* , Emma Harding-Esch3 , Laith J Abu-Raddad1,2,4,5,6
-
View Affiliations Hide AffiliationsAffiliations: 1 Infectious Disease Epidemiology Group, Weill Cornell Medicine-Qatar, Cornell University, Qatar Foundation - Education City, Doha, Qatar 2 World Health Organization Collaborating Centre for Disease Epidemiology Analytics on HIV/AIDS, Sexually Transmitted Infections, and Viral Hepatitis, Weill Cornell Medicine–Qatar, Cornell University, Qatar Foundation – Education City, Doha, Qatar 3 Clinical Research Department, Faculty of Infectious and Tropical Diseases, London School of Hygiene & Tropical Medicine, London, UK 4 Department of Population Health Sciences, Weill Cornell Medicine, Cornell University, New York, New York, USA 5 Department of Public Health, College of Health Sciences, QU Health, Qatar University, Doha, Qatar 6 College of Health and Life Sciences, Hamad bin Khalifa University, Doha, Qatar * These authors contributed equally to this work and share first authorship.Laith J. Abu-Raddadlja2002 qatar-med.cornell.edu
-
View Citation Hide Citation
Citation style for this article: Chidiac Omar, AlMukdad Sawsan, Harfouche Manale, Harding-Esch Emma, Abu-Raddad Laith J. Epidemiology of gonorrhoea: systematic review, meta-analyses, and meta-regressions, World Health Organization European Region, 1949 to 2021. Euro Surveill. 2024;29(9):pii=2300226. https://doi.org/10.2807/1560-7917.ES.2024.29.9.2300226 Received: 20 Apr 2023; Accepted: 08 Nov 2023
Abstract
Epidemiology of Neisseria gonorrhoeae (NG) infection remains inadequately understood.
We aimed to characterise NG epidemiology in Europe.
We used Cochrane and PRISMA guidelines to systematically review, report, synthesise and analyse NG prevalence data from 1949 to 30 September 2021. Random-effects meta-analyses estimated pooled prevalence. Meta-regression analyses investigated associations and sources of heterogeneity.
The 844 included publications yielded 1,573 prevalence measures. Pooled prevalence of current urogenital infection was 1.0% (95% CI: 0.7–1.2%) among general populations, 3.2% (95% CI: 1.8–4.8%) among female sex workers, 4.9% (95% CI: 4.2–5.6%) among sexually transmitted infection clinic attendees and 12.1% (95% CI: 8.8–15.8%) among symptomatic men. Among men who have sex with men, pooled prevalence was 0.9% (95% CI: 0.5–1.4%), 5.6% (95% CI: 3.6–8.1%), and 3.8% (95% CI: 2.5–5.4%), respectively, for current urogenital, anorectal or oropharyngeal infection. Current urogenital, anorectal or oropharyngeal infection was 1.45-fold (95% CI: 1.19–1.77%), 2.75-fold (95% CI: 1.89–4.02%) and 2.64-fold (95% CI: 1.77–3.93%) higher among men than women. Current urogenital infection declined 0.97-fold (95% CI: 0.96–0.98%) yearly, but anorectal and oropharyngeal infection increased (1.02-fold; 95% CI: 1.01–1.04% and 1.02-fold; 95% CI: 1.00–1.04%), respectively.
Neisseria gonorrhoeae epidemiology in Europe has distinct and contrasting epidemiologies for vaginal sex transmission in heterosexual sex networks vs anal and oral sex transmission in MSM sexual networks. Increased transmission may facilitate drug-resistant strain emergence. Europe is far from achieving the World Health Organization target of 90% incidence reduction by 2030.
Article metrics loading...
Full text loading...
References
-
Kirkcaldy RD, Weston E, Segurado AC, Hughes G. Epidemiology of gonorrhoea: a global perspective. Sex Health. 2019;16(5):401-11. https://doi.org/10.1071/SH19061 PMID: 31505159
-
Unemo M, Seifert HS, Hook EW 3rd, Hawkes S, Ndowa F, Dillon JR. Gonorrhoea. Nat Rev Dis Primers. 2019;5(1):79. https://doi.org/10.1038/s41572-019-0128-6 PMID: 31754194
-
Neslon K. E., Williams CM. Infectious disease Epidemiology: Theory and Practice. Second Edition ed. Sudbury, Massachussets: Jones and Bartlett Publishers; 2007.
-
Centers for Disease Control and Prevention (CDC). Sexually Transmitted Diseases (STDs): Gonorrhoea - CDC Fact Sheet. Atlanta: CDC; 2022. [Accessed: 30 Mar 2023]. Available from: http://www.cdc.gov/std/gonorrhoea/stdfact-gonorrhoea.htm.
-
Chemaitelly H, Majed A, Abu-Hijleh F, Blondeel K, Matsaseng TC, Kiarie J, et al. Global epidemiology of Neisseria gonorrhoeae in infertile populations: systematic review, meta-analysis and metaregression. Sex Transm Infect. 2021;97(2):157-69. https://doi.org/10.1136/sextrans-2020-054515 PMID: 32423944
-
Rowley J, Vander Hoorn S, Korenromp E, Low N, Unemo M, Abu-Raddad LJ, et al. Chlamydia, gonorrhoea, trichomoniasis and syphilis: global prevalence and incidence estimates, 2016. Bull World Health Organ. 2019;97(8):548-562P. https://doi.org/10.2471/BLT.18.228486 PMID: 31384073
-
Centers for Disease Control and Prevention (CDC). Sexually Transmitted Disease Surveillance, 2019. Atlanta: CDC; 2021. Available from: https://www.cdc.gov/std/statistics/2019/std-surveillance-2019.pdf.
-
European Centre for Disease Prevention and Control (ECDC). Gonorrhoea Annual epidemiological report for 2018. Stockholm: ECDC; 2020. Available from: https://www.ecdc.europa.eu/en/all-topics-zgonorrhoeasurveillance-and-disease-data/annual-epidemiological-reports-gonorrhoea.
-
-
World Health Organization (WHO). Global health sector strategies on, respectively, HIV, viral hepatitis and sexually transmitted infections for the period 2022-2030. Geneva: WHO; 2022. Available from: https://www.who.int/publications/i/item/9789240053779.
-
Wi T, Lahra MM, Ndowa F, Bala M, Dillon JR, Ramon-Pardo P, et al. Antimicrobial resistance in Neisseria gonorrhoeae: Global surveillance and a call for international collaborative action. PLoS Med. 2017;14(7):e1002344. https://doi.org/10.1371/journal.pmed.1002344 PMID: 28686231
-
Lewis DA. Global resistance of Neisseria gonorrhoeae: when theory becomes reality. Curr Opin Infect Dis. 2014;27(1):62-7. https://doi.org/10.1097/QCO.0000000000000025 PMID: 24275696
-
Bolan GA, Sparling PF, Wasserheit JN. The emerging threat of untreatable gonococcal infection. N Engl J Med. 2012;366(6):485-7. https://doi.org/10.1056/NEJMp1112456 PMID: 22316442
-
Kirkcaldy RD, Harvey A, Papp JR, Del Rio C, Soge OO, Holmes KK, et al. Neisseria gonorrhoeae Antimicrobial Susceptibility Surveillance - The Gonococcal Isolate Surveillance Project, 27 Sites, United States, 2014. MMWR Surveill Summ. 2016;65(7):1-19. https://doi.org/10.15585/mmwr.ss6507a1 PMID: 27414503
-
Unemo M, Lahra MM, Cole M, Galarza P, Ndowa F, Martin I, et al. World Health Organization Global Gonococcal Antimicrobial Surveillance Program (WHO GASP): review of new data and evidence to inform international collaborative actions and research efforts. Sex Health. 2019;16(5):412-25. https://doi.org/10.1071/SH19023 PMID: 31437420
-
World Health Organization (WHO). Global priority list of antibiotic-resistant bacteria to guide research, discovery, and development of new antibiotics. Geneva: WHO; 2017. Available from: http://remed.org/wp-content/uploads/2017/03/lobal-priority-list-of-antibiotic-resistant-bacteria-2017.pdf.
-
World Health Organization (WHO). Global action plan to control the spread and impact of antimicrobial resistance in Neisseria gonorrhoeae. Geneva: WHO; 2012. Available from: https://apps.who.int/iris/bitstream/handle/10665/44863/9789241503501_eng.pdf?sequence=1.
-
Petousis-Harris H, Paynter J, Morgan J, Saxton P, McArdle B, Goodyear-Smith F, et al. Effectiveness of a group B outer membrane vesicle meningococcal vaccine against gonorrhoea in New Zealand: a retrospective case-control study. Lancet. 2017;390(10102):1603-10. https://doi.org/10.1016/S0140-6736(17)31449-6 PMID: 28705462
-
Semchenko EA, Tan A, Borrow R, Seib KL. The Serogroup B Meningococcal Vaccine Bexsero Elicits Antibodies to Neisseria gonorrhoeae. Clin Infect Dis. 2019;69(7):1101-11. https://doi.org/10.1093/cid/ciy1061 PMID: 30551148
-
Edwards JL, Jennings MP, Apicella MA, Seib KL. Is gonococcal disease preventable? The importance of understanding immunity and pathogenesis in vaccine development. Crit Rev Microbiol. 2016;42(6):928-41. https://doi.org/10.3109/1040841X.2015.1105782 PMID: 26805040
-
Edwards JL, Jennings MP, Seib KL. Neisseria gonorrhoeae vaccine development: hope on the horizon? Curr Opin Infect Dis. 2018;31(3):246-50. https://doi.org/10.1097/QCO.0000000000000450 PMID: 29601324
-
Chemaitelly H, Harfouche M, Blondeel K, Matsaseng TC, Kiarie J, Toskin I, et al. Global epidemiology of Neisseria gonorrhoeae in infertile populations: protocol for a systematic review. BMJ Open. 2019;9(5):e025808. https://doi.org/10.1136/bmjopen-2018-025808 PMID: 31122971
-
Smolak A, Chemaitelly H, Hermez JG, Low N, Abu-Raddad LJ. Epidemiology of Chlamydia trachomatis in the Middle East and north Africa: a systematic review, meta-analysis, and meta-regression. Lancet Glob Health. 2019;7(9):e1197-225. https://doi.org/10.1016/S2214-109X(19)30279-7 PMID: 31402004
-
Alareeki A, Osman AMM, Khandakji MN, Looker KJ, Harfouche M, Abu-Raddad LJ. Epidemiology of herpes simplex virus type 2 in Europe: systematic review, meta-analyses, and meta-regressions. Lancet Reg Health Eur. 2023;25:100558. https://doi.org/10.1016/j.lanepe.2022.100558 PMID: 36818238
-
AlMukdad S, Farooqui US, Harfouche M, Aldos L, Abu-Raddad LJ. Epidemiology of Herpes Simplex Virus Type 2 in Canada, Australia, and New Zealand: Systematic Review, Meta-Analyses, and Meta-Regressions. Sex Transm Dis. 2022;49(6):403-13. https://doi.org/10.1097/OLQ.0000000000001612 PMID: 35608096
-
AlMukdad S, Harfouche M, Wettstein A, Abu-Raddad LJ. Epidemiology of herpes simplex virus type 2 in Asia: A systematic review, meta-analysis, and meta-regression. Lancet Reg Health West Pac. 2021;12:100176. https://doi.org/10.1016/j.lanwpc.2021.100176 PMID: 34527970
-
Harfouche M, Abu-Hijleh FM, James C, Looker KJ, Abu-Raddad LJ. Epidemiology of herpes simplex virus type 2 in sub-Saharan Africa: Systematic review, meta-analyses, and meta-regressions. EClinicalMedicine. 2021;35:100876. https://doi.org/10.1016/j.eclinm.2021.100876 PMID: 34027335
-
Harfouche M, Alareeki A, Osman AMM, Alaama AS, Hermez JG, Abu-Raddad LJ. Epidemiology of herpes simplex virus type 2 in the Middle East and North Africa: Systematic review, meta-analyses, and meta-regressions. J Med Virol. 2023;95(3):e28603. https://doi.org/10.1002/jmv.28603 PMID: 36815489
-
Harfouche M, Maalmi H, Abu-Raddad LJ. Epidemiology of herpes simplex virus type 2 in Latin America and the Caribbean: systematic review, meta-analyses and metaregressions. Sex Transm Infect. 2021;97(7):490-500. https://doi.org/10.1136/sextrans-2021-054972 PMID: 34088792
-
Chemaitelly H, Weiss HA, Calvert C, Harfouche M, Abu-Raddad LJ. HIV epidemiology among female sex workers and their clients in the Middle East and North Africa: systematic review, meta-analyses, and meta-regressions. BMC Med. 2019;17(1):119. https://doi.org/10.1186/s12916-019-1349-y PMID: 31230594
-
Chemaitelly H, Weiss HA, Smolak A, Majed E, Abu-Raddad LJ. Epidemiology of Treponema pallidum, Chlamydia trachomatis, Neisseria gonorrhoeae, Trichomonas vaginalis, and herpes simplex virus type 2 among female sex workers in the Middle East and North Africa: systematic review and meta-analytics. J Glob Health. 2019;9(2):020408. https://doi.org/10.7189/jogh.09.020408 PMID: 31360448
-
Higgins JPT, Green S. Cochrane Collaboration. Cochrane handbook for systematic reviews of interventions. Chichester, England; Hoboken, NJ: Wiley-Blackwell; 2008. xxi, 649 p. p.
-
Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71. https://doi.org/10.1136/bmj.n71 PMID: 33782057
-
Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6(7):e1000097-6. https://doi.org/10.1371/journal.pmed.1000097 PMID: 19621072
-
World Health Organization (WHO). Countries. Geneva: WHO. [Accessed: 19 Jan 2023]. Available from: https://www.who.int/countries
-
World Atlas. Europe countries and regions. Available from: https://www.worldatlas.com/articles/the-four-european-regions-as-defined-by-the-united-nationsgeoscheme-for-europe.html.
-
El-Kettani A, Mahiané G, Bennani A, Abu-Raddad L, Smolak A, Rowley J, et al. Trends in adult Chlamydia and Gonorrhoea prevalence, incidence and urethral discharge case reporting in Morocco over 1995-2015—Estimates using the spectrum-sexually transmitted infection model. Sex Transm Dis. 2017;44(9):557-64. https://doi.org/10.1097/OLQ.0000000000000647 PMID: 28806354
-
Smolak A, Rowley J, Nagelkerke N, Kassebaum NJ, Chico RM, Korenromp EL, et al. Trends and predictors of syphilis prevalence in the general population: global pooled analyses of 1103 prevalence measures including 136 million syphilis tests. Clin Infect Dis. 2018;66(8):1184-91. https://doi.org/10.1093/cid/cix975 PMID: 29136161
-
Korenromp EL, Mahiané G, Rowley J, Nagelkerke N, Abu-Raddad L, Ndowa F, et al. Estimating prevalence trends in adult gonorrhoea and syphilis in low- and middle-income countries with the Spectrum-STI model: results for Zimbabwe and Morocco from 1995 to 2016. Sex Transm Infect. 2017;93(8):599-606. https://doi.org/10.1136/sextrans-2016-052953 PMID: 28325771
-
Hoy D, Brooks P, Woolf A, Blyth F, March L, Bain C, et al. Assessing risk of bias in prevalence studies: modification of an existing tool and evidence of interrater agreement. J Clin Epidemiol. 2012;65(9):934-9. https://doi.org/10.1016/j.jclinepi.2011.11.014 PMID: 22742910
-
Clopper CJ, Pearson ES. The use of confidence or fiducial limits illustrated in the case of the binomial. Biometrika. 1934;26(4):404-13. https://doi.org/10.1093/biomet/26.4.404
-
Borenstein M, Hedges LV, Higgins JP, Rothstein HR. Introduction to meta-analysis: John Wiley & Sons; 2021.
-
Freeman MF, Tukey JW. Transformations related to the angular and the square root. Ann Math Stat. 1950;21(4):607-11. https://doi.org/10.1214/aoms/1177729756
-
Schwarzer G, Chemaitelly H, Abu-Raddad LJ, Rücker G. Seriously misleading results using inverse of Freeman-Tukey double arcsine transformation in meta-analysis of single proportions. Res Synth Methods. 2019;10(3):476-83. https://doi.org/10.1002/jrsm.1348 PMID: 30945438
-
Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21(11):1539-58. https://doi.org/10.1002/sim.1186 PMID: 12111919
-
RStudio Team. RStudio: integrated development for R. RStudio, Inc., Boston, MA. Available from: http://www.rstudio.com/.
-
Schwarzer G. meta: An R package for meta-analysis. R News. 2007;7(3):40-5. Available from: https://cran.rstudio.org/doc/Rnews/Rnews_2007-3.pdf#page=40
-
Stata Corporation LLC. Stata statistical software: release 14. College Station, TX, USA.2015. Available from: www.https://www.stata.com/stata14/
-
Low N, Broutet N, Adu-Sarkodie Y, Barton P, Hossain M, Hawkes S. Global control of sexually transmitted infections. Lancet. 2006;368(9551):2001-16. https://doi.org/10.1016/S0140-6736(06)69482-8 PMID: 17141708
-
Smith JS, Robinson NJ. Age-specific prevalence of infection with herpes simplex virus types 2 and 1: a global review. J Infect Dis. 2002;186(s1) Suppl 1;S3-28. https://doi.org/10.1086/343739 PMID: 12353183
-
Hallett TB, Aberle-Grasse J, Bello G, Boulos LM, Cayemittes MP, Cheluget B, et al. Declines in HIV prevalence can be associated with changing sexual behaviour in Uganda, urban Kenya, Zimbabwe, and urban Haiti. Sex Transm Infect. 2006;82(Suppl 1) Suppl 1;i1-8. https://doi.org/10.1136/sti.2005.016014 PMID: 16581753
-
Awad SF, Abu-Raddad LJ. Could there have been substantial declines in sexual risk behavior across sub-Saharan Africa in the mid-1990s? Epidemics. 2014;8(0):9-17. https://doi.org/10.1016/j.epidem.2014.06.001 PMID: 25240899
-
Loeber O, Reuter S, Apter D, van der Doef S, Lazdane G, Pinter B. Aspects of sexuality education in Europe - definitions, differences and developments. Eur J Contracept Reprod Health Care. 2010;15(3):169-76. https://doi.org/10.3109/13625181003797280 PMID: 20465399
-
Wijesooriya NS, Rochat RW, Kamb ML, Turlapati P, Temmerman M, Broutet N, et al. Global burden of maternal and congenital syphilis in 2008 and 2012: a health systems modelling study. Lancet Glob Health. 2016;4(8):e525-33. https://doi.org/10.1016/S2214-109X(16)30135-8 PMID: 27443780
-
Unemo M, Jensen JS. Antimicrobial-resistant sexually transmitted infections: gonorrhoea and Mycoplasma genitalium. Nat Rev Urol. 2017;14(3):139-52. https://doi.org/10.1038/nrurol.2016.268 PMID: 28072403
-
Adamson PC, Klausner JD. The staying power of pharyngeal gonorrhea: implications for public health and antimicrobial resistance. Clin Infect Dis. 2021;73(4):583-5. https://doi.org/10.1093/cid/ciab074 PMID: 33508084
-
Lewis D. Gonorrhoea resistance among men who have sex with men: what's oral sex got to do with it?: Taylor & Francis; 2013.
-
Lewis DA. Will targeting oropharyngeal gonorrhoea delay the further emergence of drug-resistant Neisseria gonorrhoeae strains? Sex Transm Infect. 2015;91(4):234-7. https://doi.org/10.1136/sextrans-2014-051731 PMID: 25911525
-
Manavi K, Zafar F, Shahid H. Oropharyngeal gonorrhoea: rate of co-infection with sexually transmitted infection, antibiotic susceptibility and treatment outcome. Int J STD AIDS. 2010;21(2):138-40. https://doi.org/10.1258/ijsa.2009.009167 PMID: 19884359
-
Stolte G, Dukers NH, de Wit JB, Fennema H, Coutinho RA. A summary report from Amsterdam: increase in sexually transmitted diseases and risky sexual behaviour among homosexual men in relation to the introduction of new anti-HIV drugs. Euro Surveill. 2002;7(2):19-22. https://doi.org/10.2807/esm.07.02.00346-en PMID: 12631950
-
Dodds JP, Nardone A, Mercey DE, Johnson AM. Increase in high risk sexual behaviour among homosexual men, London 1996-8: cross sectional, questionnaire study. BMJ. 2000;320(7248):1510-1. https://doi.org/10.1136/bmj.320.7248.1510 PMID: 10834892
-
Pakianathan M, Whittaker W, Lee MJ, Avery J, Green S, Nathan B, et al. Chemsex and new HIV diagnosis in gay, bisexual and other men who have sex with men attending sexual health clinics. HIV Med. 2018;19(7):485-90. https://doi.org/10.1111/hiv.12629 PMID: 29790254
-
Tomkins A, George R, Kliner M. Sexualised drug taking among men who have sex with men: a systematic review. Perspect Public Health. 2019;139(1):23-33. https://doi.org/10.1177/1757913918778872 PMID: 29846139
-
Hegazi A, Lee MJ, Whittaker W, Green S, Simms R, Cutts R, et al. Chemsex and the city: sexualised substance use in gay bisexual and other men who have sex with men attending sexual health clinics. Int J STD AIDS. 2017;28(4):362-6. https://doi.org/10.1177/0956462416651229 PMID: 27178067
-
Guerra FM, Salway TJ, Beckett R, Friedman L, Buchan SA. Review of sexualized drug use associated with sexually transmitted and blood-borne infections in gay, bisexual and other men who have sex with men. Drug Alcohol Depend. 2020;216:108237. https://doi.org/10.1016/j.drugalcdep.2020.108237 PMID: 33091811
-
González-Baeza A, Dolengevich-Segal H, Pérez-Valero I, Cabello A, Téllez MJ, Sanz J, et al. Sexualized drug use (Chemsex) is associated with high-risk sexual behaviors and sexually transmitted infections in HIV-positive men who have sex with men: data from the U-SEX GESIDA 9416 study. AIDS Patient Care STDS. 2018;32(3):112-8. https://doi.org/10.1089/apc.2017.0263 PMID: 29620925
-
Ramchandani MS, Golden MR. Confronting rising STIs in the era of PrEP and treatment as prevention. Curr HIV/AIDS Rep. 2019;16(3):244-56. https://doi.org/10.1007/s11904-019-00446-5 PMID: 31183609
-
Kojima N, Davey DJ, Klausner JD. Pre-exposure prophylaxis for HIV infection and new sexually transmitted infections among men who have sex with men. AIDS. 2016;30(14):2251-2. https://doi.org/10.1097/QAD.0000000000001185 PMID: 27314179
-
Hunter JP, Saratzis A, Sutton AJ, Boucher RH, Sayers RD, Bown MJ. In meta-analyses of proportion studies, funnel plots were found to be an inaccurate method of assessing publication bias. J Clin Epidemiol. 2014;67(8):897-903. https://doi.org/10.1016/j.jclinepi.2014.03.003 PMID: 24794697
-
United Nations Department of Economic and Social Affairs. World Population Prospects, the 2022 Revision. 2022. Available from: https://population.un.org/wpp/Download/Standard/Population/
Data & Media loading...
Supplementary data
-
-
Supplement
-