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Systematic Review Open Access
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Abstract

Background

Epidemiology of (NG) infection remains inadequately understood.

Aim

We aimed to characterise NG epidemiology in Europe.

Methods

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.

Results

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.

Conclusions

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.

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2024-02-29
2024-04-27
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2024.29.9.2300226
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References

  1. 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 
  2. 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 
  3. Neslon K. E., Williams CM. Infectious disease Epidemiology: Theory and Practice. Second Edition ed. Sudbury, Massachussets: Jones and Bartlett Publishers; 2007.
  4. 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.
  5. 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 
  6. 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 
  7. 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.
  8. 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.
  9. World Health Organization (WHO). Global health sector strategy on sexually transmitted infections 2016-2021: toward ending STIs. Geneva: WHO; 2016. Available from: https://www.who.int/publications/i/item/WHO-RHR-16.09
  10. 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.
  11. 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 
  12. 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 
  13. 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 
  14. 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 
  15. 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 
  16. 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.
  17. 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.
  18. 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 
  19. 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 
  20. 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 
  21. 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 
  22. 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 
  23. 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 
  24. 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 
  25. 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 
  26. 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 
  27. 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 
  28. 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 
  29. 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 
  30. 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 
  31. 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 
  32. Higgins JPT, Green S. Cochrane Collaboration. Cochrane handbook for systematic reviews of interventions. Chichester, England; Hoboken, NJ: Wiley-Blackwell; 2008. xxi, 649 p. p.
  33. 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 
  34. 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 
  35. World Health Organization (WHO). Countries. Geneva: WHO. [Accessed: 19 Jan 2023]. Available from: https://www.who.int/countries
  36. 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 
  37. 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 
  38. 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 
  39. 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 
  40. 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 
  41. Borenstein M, Hedges LV, Higgins JP, Rothstein HR. Introduction to meta-analysis: John Wiley & Sons; 2021.
  42. 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 
  43. 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 
  44. 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 
  45. RStudio Team. RStudio: integrated development for R. RStudio, Inc., Boston, MA. Available from: http://www.rstudio.com/.
  46. 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
  47. Stata Corporation LLC. Stata statistical software: release 14. College Station, TX, USA.2015. Available from: www.https://www.stata.com/stata14/
  48. 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 
  49. 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 
  50. 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 
  51. 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 
  52. 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 
  53. 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 
  54. 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 
  55. 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 
  56. Lewis D. Gonorrhoea resistance among men who have sex with men: what's oral sex got to do with it?: Taylor & Francis; 2013.
  57. 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 
  58. 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 
  59. 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 
  60. 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 
  61. 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 
  62. 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 
  63. 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 
  64. 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 
  65. 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 
  66. 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 
  67. 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 
  68. 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 
  69. 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/
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