Resistance Patterns of Neisseria gonorrhoeae in PLHIV: A Cross-Sectional Study from the Republic of Cyprus, 2015–2023
Abstract
:1. Introduction
2. Methods
3. Results
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- World Health Organization. Gonorrhoea (Neisseria gonorrhoeae infection) [Internet]. 2023. Available online: https://www.who.int/news-room/fact-sheets/detail/gonorrhoea-(neisseria-gonorrhoeae-infection)#:~:text=In%202020%2C%20WHO%20estimated%2082.4,people%20in%20high%20burden%20countries (accessed on 21 February 2024).
- European Centre for Disease Prevention and Control. Gonorrhoea—Annual Epidemiological Report for 2022; European Centre for Disease Prevention and Control: Stockholm, Sweden, 2024. [Google Scholar]
- European Centre for Disease Prevention and Control. Factsheet About Gonorrhoea; European Centre for Disease Prevention and Control: Solna, Sweden, 2010. [Google Scholar]
- Suay-García, B.; Pérez-Gracia, M.T. Drug-resistant Neisseria gonorrhoeae: Latest developments. Eur. J. Clin. Microbiol. Infect. Dis. 2017, 36, 1065–1071. [Google Scholar] [CrossRef] [PubMed]
- Unemo, M. Current and future antimicrobial treatment of gonorrhoea—The rapidly evolving Neisseria gonorrhoeae continues to challenge. BMC Infect. Dis. 2015, 15, 364. [Google Scholar] [CrossRef] [PubMed]
- Cole, M.; Day, M.; Unemo, M.; Jacobsson, S.; Spiteri, G. Response Plan to Control and Manage the Threat of Multi- and Extensively Drug-Resistant Gonorrhoea in Europe—2019 Update; European Centre for Disease Prevention and Control: Solna, Sweden, 2019. [Google Scholar]
- Lahra, M.M.; Martin, I.; Demczuk, W.; Jennison, A.V.; Lee, K.I.; Nakayama, S.I.; Lefebvre, B.; Longtin, J.; Ward, A.; Mulvey, M.R.; et al. Cooperative Recognition of Internationally Disseminated Ceftriaxone-Resistant Neisseria gonorrhoeae Strain. Emerg. Infect. Dis. 2018, 24, 735. [Google Scholar] [CrossRef] [PubMed]
- Vegvari, C.; Grad, Y.H.; White, P.J.; Didelot, X.; Whittles, L.K.; Scangarella-Oman, N.E.; Mitrani-Gold, F.S.; Dumont, E.; Perry, C.R.; Gilchrist, K.; et al. Using rapid point-of-care tests to inform antibiotic choice to mitigate drug resistance in gonorrhoea. Eurosurveillance 2020, 25, 1900210. [Google Scholar] [CrossRef] [PubMed]
- Ison, C.A.; Deal, C.; Unemo, M. Current and future treatment options for gonorrhoea. Sex. Transm. Infect. 2013, 89 (Suppl. S4), iv52–iv56. [Google Scholar] [CrossRef] [PubMed]
- Unemo, M.; Ross, J.; Serwin, A.; Gomberg, M.; Cusini, M.; Jensen, J. 2020 European guideline for the diagnosis and treatment of gonorrhoea in adults. Int. J. STD AIDS 2020. [Google Scholar] [CrossRef] [PubMed]
- Day, M.; Jacobsson, S.; Unemo, M.; Cole, M. Gonococcal Antimicrobial Susceptibility Surveillance in the European Union/European Economic Area—Summary of Results for 2020; European Centre for Disease Prevention and Control: Stockholm, Sweden, 2022. [Google Scholar]
- World Health Organisation [Internet]. Multi-Drug Resistant Gonorrhoea; World Health Organisation: Geneva, Switzerland, 2023. [Google Scholar]
- Bodoev, I.N.; Il’ina, E.N. Molecular mechanisms of formation of drug resistance in Neisseria gonorrhoeae: History and prospects. Mol. Genet. Microbiol. Virol. 2015, 30, 132–140. [Google Scholar] [CrossRef]
- Unemo, M.; del Rio, C.; Shafer, W.M. Antimicrobial Resistance Expressed by Neisseria gonorrhoeae: A Major Global Public Health Problem in the 21st Century. Microbiol. Spectr. 2016, 4, 18. [Google Scholar] [CrossRef] [PubMed]
- Unemo, M.; Shafer, W.M. Antimicrobial Resistance in Neisseria gonorrhoeae in the 21st Century: Past, Evolution, and Future. Clin. Microbiol. Rev. 2014, 27, 587–613. [Google Scholar] [CrossRef] [PubMed]
- Hook, E.W.; Kirkcaldy, R.D. A Brief History of Evolving Diagnostics and Therapy for Gonorrhea: Lessons Learned. Clin. Infect. Dis. 2018, 67, 1294–1299. [Google Scholar] [CrossRef] [PubMed]
- Yang, F.; Yan, J. Antibiotic Resistance and Treatment Options for Multidrug-Resistant Gonorrhea. Infect. Microbes Dis. 2020, 2, 67–76. [Google Scholar] [CrossRef]
- Pantaleo, G.; Fauci, A.S. Immunopathogenesis of HIV Infection. Annu. Rev. Microbiol. 1996, 50, 825–854. [Google Scholar] [CrossRef] [PubMed]
- Ison, C.A.; Dillon, J.A.R.; Tapsall, J.W. The epidemiology of global antibiotic resistance among Neisseria gonorrhoeae and Haemophilus ducreyi. Lancet 1998, 351, S8–S11. [Google Scholar] [CrossRef] [PubMed]
- Olaru, I.D.; Tacconelli, E.; Yeung, S.; Ferrand, R.A.; Stabler, R.A.; Hopkins, H.; Aiken, A.M.; Kranzer, K. The association between antimicrobial resistance and HIV infection: A systematic review and meta-analysis. Clin. Microbiol. Infect. 2021, 27, 846–853. [Google Scholar] [CrossRef] [PubMed]
- Aryal, S. Martin Lewis Agar- Composition, Principle, Preparation, Results, Uses; Microbe Notes: Kathmandu, Nepal, 2022. [Google Scholar]
- Takei, M.; Yamaguchi, Y.; Fukuda, H.; Yasuda, M.; Deguchi, T. Cultivation of Neisseria gonorrhoeae in Liquid Media and Determination of Its In Vitro Susceptibilities to Quinolones. J. Clin. Microbiol. 2005, 43, 4321–4327. [Google Scholar] [CrossRef] [PubMed]
- European Committee on Antimicrobial Susceptibility Testing. Clinical Breakpoints—Breakpoints and Guidance; European Committee on Antimicrobial Susceptibility Testing: Växjö, Sweden, 2025. [Google Scholar]
- Herrero, M.; Broner, S.; Cruells, A.; Esteve, S.; Ferré, L.; Mendioroz, J.; Jané, M.; Ciruela, P. Epidemiology and antimicrobial resistance profile of Neisseria gonorrhoeae in Catalonia, Spain, 2016–2019. Eur. J. Clin. Microbiol. Infect. Dis. 2023, 42, 883–893. [Google Scholar] [CrossRef] [PubMed]
- Workowski, K.A. Sexually Transmitted Infections Treatment Guidelines, 2021 [Internet]; Gonococcal Infections Among Adolescents and Adults; CDC: Atlanta, GA, USA, 2022. [Google Scholar]
- Unemo, M.; Jacobsson, S. Gonococcal Antimicrobial Susceptibility Surveillance in Europe. Available online: www.ecdc.europa.eu (accessed on 3 June 2025).
- Rob, F.; Klubalová, B.; Nyčová, E.; Hercogová, J.; Unemo, M. Gentamicin 240 mg plus azithromycin 2 g vs. ceftriaxone 500 mg plus azithromycin 2 g for treatment of rectal and pharyngeal gonorrhoea: A randomized controlled trial. Clin. Microbiol. Infect. 2020, 26, 207–212. [Google Scholar] [CrossRef] [PubMed]
- Geusau, A.; Chromy, D.; Heissenberger, D.; Lippert, K.; Eder, C.; Heger, F.; Indra, A.; Willinger, B.; Pleininger, S. Resistance profiles of Neisseria gonorrhoeae isolates in Vienna, Austria: A phenotypic and genetic characterization from 2013 to 2020. Int. J. Antimicrob. Agents 2022, 60, 106656. [Google Scholar] [CrossRef] [PubMed]
- Jacobsson, S.; Cole, M.J.; Schröder, D.; Jansen van Rensburg, M.; Day, M.; Ködmön, C.; Unemo, M.; Pleininger, S.; Schindler, S.; El-Khatib, Z.; et al. Antimicrobial resistance in Neisseria gonorrhoeae and its risk groups in 23 European countries in 2022 within the European Gonococcal Antimicrobial Surveillance Programme (Euro-GASP): A retrospective observational study. Lancet Reg. Health-Eur. 2025, 54, 101318. [Google Scholar] [CrossRef]
2015 | 2016 | 2017 | 2018 | 2019 | 2020 | 2021 | 2022 | 2023 | Total | |
---|---|---|---|---|---|---|---|---|---|---|
No. of N. gonorrhoeae isolates | 1 | 3 | 3 | 3 | 6 | 15 | 5 | 6 | 3 | 45 |
Total patients at Gregorios clinic | 568 | 657 | 741 | 836 | 968 | 1076 | 1162 | 1040 | 1168 | 8216 |
Characteristics | Number | % (95%CI) |
---|---|---|
Male | 39 | 100.0 |
Female | 0 | 0 |
Age in years (mean ± SD) | 38.5 ± 9.7 | |
Sexual orientation | ||
Bisexual | 4 | 10.2 (0.3–24) |
Heterosexual | 3 | 7.7 (0.2–21) |
MSM | 32 | 82.1 (66–92) |
Nationality | ||
Bulgarian | 1 | 2.6 (0–13) |
Cameroonian | 3 | 7.7 (0.2–21) |
Cypriot | 30 | 76.9 (61–89) |
Georgian | 1 | 2.6 (0–13) |
German | 1 | 2.6 (0–13) |
Greek | 1 | 2.6 (0–13) |
Liberian | 1 | 2.6(0–13) |
Ukrainian | 1 | 2.6 (0–13) |
Educational level | ||
Secondary | 9 | 23.1 (11–39) |
Tertiary | 29 | 74.4 (58–87) |
Unknown | 1 | 2.6 (0–13) |
History of previous STI | ||
No | 17 | 44.0 (28–60) |
Yes | 22 | 56.0 (40–72) |
Hepatitis B | 2 | 9.1 (1.1–29) |
Hepatitis B and Chlamydia | 1 | 4.5 (0.1–23) |
Syphilis | 16 | 72.7 (50–89) |
Syphilis and Chlamydia | 2 | 9.1 (1.1–29) |
Syphilis and HPV | 1 | 4.5 (0.1–23) |
Site of isolation (Swab N = 45) | ||
Pharynx | 9 | 20.0 (9.6–35) |
Pharynx, Urethra, Rectum | 2 | 4.4 (0.5–15) |
Rectum | 13 | 28.9 (16–44) |
Urethra | 21 | 46.7 (32–62) |
2015 | 2016 | 2017 | 2018 | 2019 | 2020 | 2021 | 2022 | 2023 | Total | |
---|---|---|---|---|---|---|---|---|---|---|
N | N | N | N | N | N | N | N | N | N (%, 95%CI) | |
AMPICILLIN | ||||||||||
R | 1 | 1 | 1 | 3 (75, 19–99) | ||||||
S | 1 | 1 (25, 1–81) | ||||||||
AZTREONAM | ||||||||||
R | 0 (0, 0–98) | |||||||||
S | 1 | 1 (100, 3–100) | ||||||||
CEFEPIME | ||||||||||
R | 0 (0, 0–46) | |||||||||
S | 1 | 2 | 1 | 2 | 6 (100, 54–100) | |||||
CEFOTAXIME | ||||||||||
R | 1 | 1 (7, 0.2–34) | ||||||||
S | 2 | 2 | 1 | 1 | 1 | 3 | 3 | 13 (93, 66–100) | ||
CEFTAZIDIME | ||||||||||
R | 0 (0) | |||||||||
S | 1 | 1 | 2 (100, 16–100) | |||||||
CEFTRIAXONE | ||||||||||
R | 1 | 1 (3, 0.1–14) | ||||||||
S | 1 | 3 | 2 | 3 | 5 | 15 | 4 | 2 | 35 (97, 85–100) | |
CEFUROXIME | ||||||||||
R | 1 | 1 (6, 0.1–29) | ||||||||
S | 1 | 3 | 1 | 3 | 6 | 2 | 16 (94, 71–100) | |||
CIPROFLOXACIN | ||||||||||
R | 1 | 1 | 1 | 2 | 1 | 1 | 7 (39, 17–64) | |||
S | 2 | 1 | 2 | 3 | 1 | 2 | 11 (61, 36–83) | |||
ERYTHROMYCIN | ||||||||||
R | 3 | 1 | 4 (13, 3.5–29) | |||||||
S | 2 | 6 | 12 | 4 | 4 | 28 (87, 71–96) | ||||
GENTAMICIN | ||||||||||
R | 7 | 5 | 5 | 17 (77, 55–92) | ||||||
S | 2 | 3 | 5 (23, 7.8–45) | |||||||
OFLOXACIN | ||||||||||
R | 1 | 1 | 1 | 3 (50, 12–88) | ||||||
S | 1 | 1 | 1 | 3 (50, 12–88) | ||||||
PENICILLIN G | ||||||||||
R | 2 | 1 | 1 | 1 | 1 | 6 (15, 5.9–31) | ||||
S | 1 | 1 | 3 | 4 | 14 | 4 | 4 | 31 (79, 64–91) | ||
I | 2 | 2 (5, 0.6–17) | ||||||||
TETRACYCLINE | ||||||||||
R | 3 | 2 | 1 | 1 | 7 (39, 17–64) | |||||
S | 1 | 3 | 6 | 1 | 11 (61, 36–83) | |||||
2015 | 2016 | 2017 | 2018 | 2019 | 2020 | 2021 | 2022 | 2023 | Total | |
N (%) | N (%) | N (%) | N (%) | N (%) | N (%) | N (%) | N (%) | N (%) | N (%) | |
No resistance | 3 (100) | 4 (67) | 7 (47) | 1 (17) | 2 (67) | 17 (38, 24–53) | ||||
Resistance to 1 antibiotic | 1 (33) | 2 (67) | 1 (17) | 5 (33) | 4 (80) | 2 (33) | 1 (33) | 16 (36, 22–51) | ||
Resistance to >1 antibiotics | 1 (100) | 2 (67) | 1 (33) | 1 (17) | 3 (20) | 1 (20) | 3 (50) | 12 (27, 15–42) |
Simple Liner Regression | Multiple Liner Regression | |||
---|---|---|---|---|
Variable | Coefficient | p-Value | Coefficient | p-Value |
Age (continuous) | −0.03 | 0.141 | −0.03 | 0.210 |
Cyprus nationality | 0.28 | 0.567 | 0.58 | 0.233 |
Sexual orientation | ||||
Heterosexual | Ref | |||
Bisexual | 0.33 | 0.740 | 0.48 | 0.647 |
MSM | 0.49 | 0.534 | 0.56 | 0.457 |
Year of culture (continuous) | −0.09 | 0.388 | - | - |
Culture site | ||||
Pharynx | −0.75 | 0.093 | - | - |
Rectum | −0.27 | 0.517 | - | - |
Urethra | 0.57 | 0.136 | - | - |
History of previous STI | 0.93 | 0.016 | 1.2 | 0.004 |
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Takos, M.; Siakallis, G.; Quattrocchi, A.; Alexandrou, M.; Papadamou, P.; Panagiotou, L.; Alon-Ellenbogen, D. Resistance Patterns of Neisseria gonorrhoeae in PLHIV: A Cross-Sectional Study from the Republic of Cyprus, 2015–2023. Antibiotics 2025, 14, 589. https://doi.org/10.3390/antibiotics14060589
Takos M, Siakallis G, Quattrocchi A, Alexandrou M, Papadamou P, Panagiotou L, Alon-Ellenbogen D. Resistance Patterns of Neisseria gonorrhoeae in PLHIV: A Cross-Sectional Study from the Republic of Cyprus, 2015–2023. Antibiotics. 2025; 14(6):589. https://doi.org/10.3390/antibiotics14060589
Chicago/Turabian StyleTakos, Michaela, George Siakallis, Annalisa Quattrocchi, Maria Alexandrou, Panagiota Papadamou, Loukia Panagiotou, and Danny Alon-Ellenbogen. 2025. "Resistance Patterns of Neisseria gonorrhoeae in PLHIV: A Cross-Sectional Study from the Republic of Cyprus, 2015–2023" Antibiotics 14, no. 6: 589. https://doi.org/10.3390/antibiotics14060589
APA StyleTakos, M., Siakallis, G., Quattrocchi, A., Alexandrou, M., Papadamou, P., Panagiotou, L., & Alon-Ellenbogen, D. (2025). Resistance Patterns of Neisseria gonorrhoeae in PLHIV: A Cross-Sectional Study from the Republic of Cyprus, 2015–2023. Antibiotics, 14(6), 589. https://doi.org/10.3390/antibiotics14060589