Skip to main content
NCBI home page
The Yale Journal of Biology and Medicine logoLink to The Yale Journal of Biology and Medicine
. 2022 Dec 22;95(4):465–478.

Global status of Azithromycin and Erythromycin Resistance Rates in Neisseria gonorrhoeae: A Systematic Review and Meta-analysis

Zhiwei Lu a,b, Danyal Abbasi Tadi c, Jinchao Fu d,*, Khalil Azizian e, Ebrahim Kouhsari f,g,*
PMCID: PMC9765340  PMID: 36568835

Abstract

Background: The widespread development of antibiotic resistance or decreased susceptibility in Neisseria gonorrhoeae (NG) infection is a global and significant human public health issue. Objectives: Therefore, this meta-analysis aimed to estimate worldwide resistance rates of NG to the azithromycin and erythromycin according to years, regions, and antimicrobial susceptibility testing (AST). Methods: We systematically searched the published studies in PubMed, Scopus, and Embase from 1988 to 2021. All analyses were conducted using Stata software. Results: The 134 reports included in the meta-analysis were performed in 51 countries and examined 165,172 NG isolates. Most of the included studies were from Asia (50 studies) and Europe (46 studies). In the metadata, the global prevalence over the past 30 years were 6% for azithromycin and 48% for erythromycin. There was substantial change in the prevalence of macrolides NG resistance over time (P <0.01). In this metadata, among 58 countries reporting resistance data for azithromycin, 17 (29.3%) countries reported that >5% of specimens had azithromycin resistance. Conclusions: The implications of this study emphasize the rigorous or improved antimicrobial stewardship, early diagnosis, contact tracing, and enhanced intensive global surveillance system are crucial for control of further spreading of gonococcal emergence of antimicrobial resistance (AMR).

Keywords: Animicrobial Resistance, Neisseria gonorrhoeae, antibiotic resistance, azithromycin, erythromycin, systematic review and meta-analysis

Introduction

Sexually transmitted infections (STIs) are a significant human health issue around the world [1,2]. Gonorrhea, as one of the most frequent bacterial STIs, continues to be a major threat to public health [3]. In 2020, the WHO estimated that there were 82.4 million (95% CI 47.7 million-130.4 million) new cases of gonorrhea among adolescents and adults. Antimicrobial resistance (AMR) in Neisseria gonorrhoeae (NG) is a developing clinical and public health challenge [3]. Emerging azithromycin-resistance among the NG reported in most countries which would lead to an increase in serious problems, including infertility, ectopic pregnancy, and increased transmission of HIV [4]. Thus, an effective and inexpensive anti-infective agent is a necessity to control gonorrhea. The aim of this meta-analysis is: (1) to assess the weighted pooled resistance rate (WPR: proportion of strains resistant to specific antibiotic agent) rates of NG to azithromycin and erythromycin according to years, regions, and antimicrobial susceptibility testing (AST).

Methods

This review is reported accordant with the Preferred Reporting Items for Systematic Reviews and Meta Analyses guidelines (PRISMA) [5].

Search Strategy and Study Selection

We systematically searched for studies in four international databases including PubMed, Scopus, and Embase (until August 2021) by utilizing the related keywords: (“Neisseria gonorrhoeae” OR “gonorrhoea” OR “Gonococcus”) AND (“antimicrobial resistance” OR “antibiotic resistance” OR “macrolides resistance” OR “azithromycin resistance” “erythromycin resistance”) in the Title/Abstract/Keywords fields. The search strategy was designed and conducted by study investigators.

Reference lists of all studies were also reviewed for any other related publication. The records found through database searching were merged and the duplicates were removed using EndNote X8 (Thomson Reuters, New York, NY, USA). One of the team researchers randomly assessed the search results and confirmed that no relevant study had been ignored. All these steps were done by the three authors and any disagreements about article selection were resolved through discussion, and a fourth author acted as arbiter.

Inclusion and Exclusion Criteria

The included articles met the following criteria: (1) original study that investigated NG AMR in human clinical isolates; (2) peer-reviewed articles published in English between January 1980 and August 2021; (3) sample size of NG isolates; (4) the methods used for resistance testing (MIC-based methods, disk diffusion, mix methods (both methods)); (5) reported the AMR rate in NG isolates following the criteria by the Clinical and Laboratory Standards Institute (CLSI) standards [6], European Committee on Antimicrobial Susceptibility Testing (EUCAST) [7], and/or the WHO WPR Resistance Surveillance Programme guidelines [8]. The clinical azithromycin resistant breakpoints were interpreted using the EUCAST (>0.5 µg/mL) and CLSI (epidemiological cutoff value ≥2.0 µg/mL). In 2019, EUCAST and CLSI excluded their clinical breakpoints for azithromycin and an epidemiological cutoff value (MIC >1 mg/L) has been used for the identification of non-susceptible isolates with determinants of azithromycin resistance [9]. Studies were excluded if they contained duplicate data or were overlapping articles, (2) animal research, reviews, meta-analysis and/or systematic review, conference abstracts, and macrolides resistance were not evidently described.

Data Extraction and Assessment of Study Quality

Data extracted from each included study was; author, study period, publication year, regions, sample size of NG isolates, sample size of macrolides resistant NG isolates, and AST (disk diffusion, agar dilution, microbroth dilution, E-test). The Newcastle-Ottawa scale (NOS) was adapted for cross-sectional studies for quality assessment [10]. NOS is based on a star scoring system, which a maximum of 8 (for cross-sectional studies) can be awarded to each study. Quality assessment was checked independently by two authors, and any disagreements were solved by the third. Studies that received a score of 6 or above were considered to be high quality.

Statistical Analysis

Cross-sectional articles presenting eligible information on macrolides susceptibility in NG isolates were pooled and analyzed based on random-effects model with Stata/SE software, v.17.1 (StataCorp, College Station, TX, USA). Freeman-Tukey double arcsine transformation was performed to estimate the WPR. The inconsistency across studies was examined by the forest plot as well as the I2 statistic. Values of I2 (25%, 50%, and 75%) were interpreted as the presence of low, medium, or high heterogeneity, respectively. So, the DerSimonian and Laird random effects models were used [11]. Macrolides resistance rate was expressed as percentage and 95% confidence interval (CI) basis. Publication bias was calculated using Egger’s test.

Study Outcomes

The primary outcome was the WPR rate of NG to azithromycin and erythromycin resistance. Subgroup analyses were then utilized by year publication (1988-2013, 2014-2018, and 2019-2021), (2) regions, (3) AST, and (4) interpretation of resistance (CLSI, EUCAST, and WHO).

Results

Results of the Systematic Literature Search

Initially, a total of 2,350 studies were identified. The full texts of the remaining 505 articles were reviewed. Ultimately, 134 studies were included [12-145] based on their irrelevance/duplication and the inclusion and exclusion criteria (Figure 1). The 134 reports included in the analysis were conducted in 51 countries, examined 165,172 NG isolates, and were published between 1988 and 2021. The main group of included articles (50 studies) were conducted from Asia and Europe (46 studies) (Table 1). The macrolides WPR rates and the subgroup analyses by year, continents, AST, and interpretation of resistance are shown in Table 1.

Figure 1.

Figure 1

Open in a new tab

Flow chart of study selection.

Table 1. Subgroup Analysis for Azithromycin and Erythromycin Resistance Rates.

Variables Number of Studies (n, N) Prevalence (%) of Resistance (95% CI) Heterogeneity (I2) (%) Egger test
Azithromycin 133 (6104, 165172) 6.00 (5.00-7.00) 98.76 <0.01
Publication date
 1988-2013 34 (409, 52191) 2.31 (1.40-3.40) 94.85
 2014-2018 46 (2018, 68318) 6.85 (4.62-9.46) 98.82
 2019-2021 53 (3677, 44013) 7.25 (5.62-9.06) 97.22
Continent
 North America 15 (819, 96842) 2.13 (1.10-3.43) 98.71
 Asia 49 (1945, 17500) 6.36 (4.07-9.07) 97.48
 Africa 15 (307, 2995) 5.28 (0.35-14.15) 98.32
 Europe 45 (2887, 45035) 5.88 (4.63-7.26) 96.19
 South America 8 (139, 1752) 9.27 (4.89-14.79) 90.68
 Oceania 1 (7, 398) 1.76 (0.71-3.59) 0.00
Interpretation of resistance
 CLSI 65 (1823, 112801) 4.00 (3.00-5.00) 98.20
 EUCAST 60 (3237, 44863) 7.00 (6.00-9.00) 96.64
 WHO 8 (1044, 6858) 8.00 (3.00-14.00) 98.23
AST
 MIC-based methods 116 (5772, 160099) 5.64 (4.46-6.93) 98.86
 Disk diffusion 10 (185, 2005) 9.24 (1.79-20.78) 94.38
 Mix methods 7 (147, 2418) 2.76 (0.376.80) 97.65
Erythromycin 16 (3010, 13161) 21 (13-29) 98.69 0.68
Publication date
 1988-2013 11 (1423, 8186) 17.16 (6.08-32.12) 98.37
 2014-2018 1 (18, 25) 72.00 (50.61-87.93) 0.00
 2019-2021 4 (1569, 4950) 21.50 (7.17-40.61) 97.74
Continent
 North America 4 (2713, 12123) 13.61 (6.01-23.62) 99.26
 Asia 3 (58, 176) 36.31 (0.00-93.16) -
 Africa 4 (62, 223) 23.74 (0.00-88.05) 99.00
 Europe 5 (177, 639) 17.52 (0.45-49.43) 98.68
 South America - -
Interpretation of resistance
 CLSI 10 (2791, 12527) 17.00 (9-26) 98.97
 EUCAST 5 (219, 558) 37.00 (13-64) 97.42
 WHO 1 (0, 76) 0.00 (0.00-2) -
AST
 MIC-based methods 1 (2, 12974) 24.11 (15.46-33.95) 98.92
 Disk diffusion 3 (18, 156) 12.58 (0.00-64.08) 0
 Mix methods 12 (2990, 31) 6.45 (0.79-21.42) 0
Open in a new tab

CI, confidence interval; n, number of events (drug resistance); N, total number of isolates from the included studies

Azithromycin Resistance

The susceptibility to azithromycin was determined in 133 studies included 165,172 NG isolates; the WPR was 6% (95% CI 5%-7%) with substantial heterogeneity (I2=98.76%; P=0.01) was observed between included studies (Table 1). Also, significant publication bias was detected (Egger rank correlation test, P <0.01). To analyze the trends for changes in the prevalence of azithromycin resistance in more recent years, we performed a subgroup analysis for three periods (1988-2013; 2014-2018; and 2019-2021) (Table 1, Figure 2). The subgroup analysis that compared the data from 1988-2013 (WPR 2.31%; 95% CI 1.40%-3.40%), 2014-2018 (WPR 6.85%; 95% CI 4.62%-9.46%), and 2019-2021 (WPR 7.25%; 95% CI 5.62%-9.06%) indicated an increase in the resistance rate. However, there was significant variation in the proportion of azithromycin resistance isolates over time (P <0.01). Among 51 countries reporting resistance data for azithromycin, 22 (43.13%) countries (China, Bangladesh, Brazil, Guyana, Cuba, Israel, Korea, Germany, Vietnam, Italy, Belarus, Norway, Hungary, Slovenia, Estonia, Poland, Spain, Iran, Argentina, Ethiopia, Ireland, and Côte d’Ivoire) reported that >5% of specimens had azithromycin resistance (Figures 3 and 4). There was a statistically significant difference in the azithromycin resistance rates between different continents (P <0.01); and this rate was higher in South America than Asia (9.2% vs. 6.3%), Europe (9.2% vs. 5.8%), Africa (9.2% vs. 5.3%), North America (9.2% vs. 2.1%,), and Oceania (9.2% vs. 1.7%) (Figure 4). No significant difference was found in the method used for AST and the interpretation of resistance (P=0.36).

Figure 2.

Figure 2

Open in a new tab

The prevalence of antibiotics weighted pooled resistance over years.

Figure 3.

Figure 3

Open in a new tab

Global map of reported weighted pooled resistance rates for (A) azithromycin and (B) erythromycin in the study.

Figure 4.

Figure 4

Open in a new tab

Forest plot for the summary of azithromycin and erythromycin WPRs by regions.

Erythromycin Resistance

The susceptibility to erythromycin was determined in 16 studies that included 13,161 NG isolates; the WPR was 21% (95% CI 13%-29%) with substantial heterogeneity (I2=98.69%, P< 0.01) was observed between included studies (Table 1). Also, no significant publication bias was detected (Egger rank correlation test, P=0.68). As shown in the Table 1 and Figure 2, the prevalence of erythromycin resistance notably increased from 17.16% (95% CI 6.08-32.12) of 18 strains 1988-2013 reaching 72% (95% CI 50.61-87.93) of 1,569 strains in 2014-2018. Regarding erythromycin resistance, a huge increase was noted from the earlier time period of 1988-2013 to 2014-2018, but this was based on a single study [146] with very few isolates. The frequency of erythromycin resistance during the years 2019-2021 represents a gradual increase over the years 1988-2013. However, there was significant variation in the proportion of erythromycin resistance isolates over time (P <0.01). Among 11 countries reporting resistance data for erythromycin, 4 (~22%) countries (Bangladesh, Nigeria, Denmark, and Belarus) reported that >25% of specimens had resistance. There was a no statistically significant difference in the erythromycin resistance rates between different continents (P=0.83). No significant difference was found in the method used for AST (P=0.08). No significant difference was found in the interpretation of resistance based on CLSI, EUCAST, and WHO (P=0.79).

Discussion

This metadata was conducted to study the prevalence of macrolides resistance in NG isolates around the world. It is proposed for the implication of continuous and robust monitoring of AMR of clinical NG isolates. NG AMR has become an important issue around the world in the past few decades [1,2]. In our metadata, the global WPRs over the past 30 years are higher than the 5% for azithromycin (6%) and erythromycin (21%). The WHO recommends that alternative agents should be used when NG AMR rate reaches a 5% threshold [147,148].

Ceftriaxone is the last choice for empirical first-line gonorrhea monotherapy in many countries [9]. However, emergence of decreased susceptibility or resistance to ceftriaxone have been stated globally. Currently most countries commonly suggest dual antimicrobial therapy (ceftriaxone 250-500mg plus azithromycin 1-2g) as empirical first-line gonorrhea treatment to prevent the emergence/accumulation of AMR [147]. However, as documented in the WHO’s global gonococcal AMR surveillance 2017-18, there are major gaps in NG AMR surveillance [149]. The emergence of azithromycin and/or ceftriaxone resistance has been developing rapidly, which raises significant global challenges over the continued efficacy of current gonorrhea treatments [150-153]. During 2018, the WHO Gonococcal AMR Surveillance Programme (WHO-GASP) reported data on azithromycin resistance in NG among 61 countries in WHO regions; 44 (72%) countries reported that > 5% of specimens had resistance [1,2,9]. In this metadata, among 58 countries reporting resistance data for azithromycin, 17 (29.3%) countries (China, Bangladesh, Japan, Korea, Italy, Slovenia, Portugal, Slovenia, Iran, Denmark, Spain, and Ethiopia) reported that > 5% of specimens had azithromycin resistance. The area discrepancies in azithromycin-resistance rate of NG isolates may result from gonorrhea control policy, antibiotic stewardship, the lack of an implementing response plans, antimicrobial misuse, and several AST methods. The selection and spread of azithromycin resistance are driven by unsuitable treatment of patients with suboptimal doses of azithromycin for gonococcal infection. Gonorrhea and AMR in NG are significant public health concerns globally, especially in Asian and European countries. In our metadata, the most reports were from Asia (50 reports) and Europe (46 studies) than on the other continents. Current evidence of AMR NG in Asian and European data supports rigorous monitoring of definite antibiotic policy, and active surveillance of infections. Furthermore, there is an alarm for the high prevalence (>10%) of azithromycin resistance in NG strains in China, Iran, Bangladesh, Myanmar, Vietnam, Norway, Ireland, Estonia, Hungary, and Slovenia. It is significant to appreciate the epidemiology of AMR in NG to inform treatment guidelines and prevention and control measures, in addition to wider gonorrhea prevention efforts.

This meta-analysis revealed a significant increase in the proportion of azithromycin resistance isolates over time, which is consistent with other reports [154,155]. Over the period, our findings showed that the trend of azithromycin resistance had increased from 1988-2013 to 2019-2021 (2.3% and 7.2%, respectively). Azithromycin resistance rate over times was increased as compared to erythromycin. The previous clinical and in vitro AMR data displayed early that erythromycin is not sufficiently effective for the treatment of gonorrhea [156,157]. So, due to the limited clinical effects of drugs (like; erythromycin) for the treatment of gonorrhea, currently most countries commonly suggest dual antimicrobial therapy (ceftriaxone 250-500mg plus azithromycin 1-2g) as empirical first-line gonorrhea treatment to prevent the emergence/accumulation of AMR [147]. The reason for the decrease in resistance to erythromycin in the past years is the lack of use of this drug in the treatment of gonorrhea.

The prevalence of azithromycin and erythromycin resistant NG isolates in South America (9.2%) and Asia (36.3%) is higher than in other continents. These results indicate that macrolides resistance patterns differed among geographic regions and in different periods.

Despite the significance of AST for clinical management of infection and AMR surveillance, the methodologies and breakpoints of the CLSI and EUCAST are used worldwide. Divergences in clinical breakpoints between CLSI and EUCAST considerably impact susceptibility interpretation of clinical isolates. This has implications not only for antibiograms at institutions switching between the two AST systems, but for broader AMR surveillance initiatives comparing data within and between countries using different systems or over the time period during which a shift in methodology is applied.

The creeping increase in the emergence of NG isolates with resistance to ceftriaxone plus azithromycin is a cause for a rising global challenge that necessitates further monitoring and investigation. The increase in emergence of reduced susceptibility or low- to high-level azithromycin resistance of NG strains has previously been reported to be related to mutational changes in the specific residues (the peptidyl-transferase loop) in domain V of the 23S rRNA, namely A2059G, C2611T, A2143G, A2058G, and multiple transferable resistance (Mtr) system as a tripartite efflux pump [158,159]. The main limitation of our review that is that we used collection date for data samples, rather than the publication date for analysis. The correct date of samples was not available or mentioned in all the included studies, so the authors performed the subgroup analysis by year published instead of the year of collection data of samples.

However, there were also several limitations of our meta-analysis to be addressed: (1) most of the included studies in this meta-analysis were conducted in European and Asian countries; (2); not including the strains identification code of NG in the included studies.

Conclusions

In this metadata, the global resistance prevalence was 6% for azithromycin and 48% for erythromycin. These are major insights into the epidemiological macrolides resistance pattern of NG over time and has highlighted the distribution of macrolides-resistant strains in continents/countries. The creeping increase in the emergence of NG isolates with resistance to ceftriaxone and/or azithromycin is a cause for a rising global challenge that necessitates robust monitoring and more investigation. The implications of this study emphasize the rigorous or improved antimicrobial stewardship, early diagnosis, contact tracing, and enhanced intensive global surveillance system are crucial for control of further spreading of gonococcal AMR.

Acknowledgments

This study (Grant number: 14-113102) was supported and approved by Golestan University of Medical Sciences (Gorgan, Iran) for which we are very grateful.

Glossary

NG

Neisseria gonorrhoeae

AST

antimicrobial susceptibility testing

AMR

antimicrobial resistance

WPR

weighted pooled resistance rate

CLSI

Clinical and Laboratory Standards Institute

EUCAST

European Committee on Antimicrobial Susceptibility Testing

Competing Interests

The authors have no relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript.

Author Contributions

ZL, DAT, JF contributed to the conception and design of the work. KA and EK contributed to design of the work, and final approval of the version to be published. ZL and JF contributed in drafting the work and revising it critically for important intellectual content. JF and EK contributed in revising the article and final approval of the version to be published.

Data availability statement

All the data in this review are included in the manuscript.

References

  1. Kirkcaldy RD, Weston E, Segurado AC, Hughes G. Epidemiology of gonorrhoea: a global perspective. Sex Health. 2019. Sep;16(5):401–11. 10.1071/SH19061 [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Unemo M, Golparian D, Eyre DW. Antimicrobial Resistance in Neisseria gonorrhoeae and Treatment of Gonorrhea. Methods Mol Biol. 2019;1997:37–58. 10.1007/978-1-4939-9496-0_3 [DOI] [PubMed] [Google Scholar]
  3. Multi-drug resistant gonorrhea: World Health Organization; 10 November 2021. Available from: https://www.who.int/news-room/fact-sheets/detail/multi-drug-resistant-gonorrhoea
  4. Derbie A, Mekonnen D, Woldeamanuel Y, Abebe T. Azithromycin resistant gonococci: a literature review. Antimicrob Resist Infect Control. 2020. Aug;9(1):138. 10.1186/s13756-020-00805-7 [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. 2009;6(7):e1000097. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Performance Standards for Antimicrobial Susceptibility Testing , CLSI supplement M100. CLSI; Clinical and Laboratory Standards Institute; 2022.
  7. The European Committee on Antimicrobial Susceptibility Testing. Breakpoint tables for interpretation of MICs and zone diameters. Version 12.0, 2022. http://www.eucast.org
  8. Ison CA, Town K, Obi C, Chisholm S, Hughes G, Livermore DM, et al. Decreased susceptibility to cephalosporins among gonococci: data from the Gonococcal Resistance to Antimicrobials Surveillance Programme (GRASP) in England and Wales, 2007–2011. Lancet Infect Dis. 2013;13(9):762-8. [DOI] [PubMed] [Google Scholar]
  9. Unemo M, Lahra MM, Escher M, Eremin S, Cole MJ, Galarza P, et al. WHO global antimicrobial resistance surveillance for Neisseria gonorrhoeae 2017–18: a retrospective observational study. 2021;2(11):e627-e36. [DOI] [PubMed] [Google Scholar]
  10. Newcastle O. Newcastle-Ottawa: Scale customized for cross-sectional studies. 2018.
  11. DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986. Sep;7(3):177–88. 10.1016/0197-2456(86)90046-2 [DOI] [PubMed] [Google Scholar]
  12. Adamson PC, Van Le H, Le HH, Le GM, Nguyen TV, Klausner JD. Trends in antimicrobial resistance in Neisseria gonorrhoeae in Hanoi, Vietnam, 2017-2019. BMC Infect Dis. 2020. Nov;20(1):809. 10.1186/s12879-020-05532-3 [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ahmed MU, Chawdhury FA, Hossain M, Sultan SZ, Alam M, Salahuddin G, et al. Monitoring antimicrobial susceptibility of Neisseria gonorrhoeae isolated from Bangladesh during 1997-2006: emergence and pattern of drug-resistant isolates. J Health Popul Nutr. 2010. Oct;28(5):443–9. 10.3329/jhpn.v28i5.6152 [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Alfsnes K, Eldholm V, Olsen AO, Brynildsrud OB, Bohlin J, Steinbakk M, et al. Genomic epidemiology and population structure of Neisseria gonorrhoeae in Norway, 2016-2017. Microb Genom. 2020. Apr;6(4):e000359. 10.1099/mgen.0.000359 [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Aniskevich A, Shimanskaya I, Boiko I, Golubovskaya T, Golparian D, Stanislavova I, et al. Antimicrobial resistance in Neisseria gonorrhoeae isolates and gonorrhea treatment in the Republic of Belarus, Eastern Europe, 2009–2019. BMC Infect Dis. 2021;21(1):1–9. 10.1186/s12879-021-06184-7 [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Attram N, Agbodzi B, Dela H, Behene E, Nyarko EO, Kyei NN, et al. Antimicrobial resistance (AMR) and molecular characterization of Neisseria gonorrhoeae in Ghana, 2012-2015. PLoS One. 2019. Oct;14(10):e0223598. 10.1371/journal.pone.0223598 [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Azizmohammadi S, Azizmohammadi S. Antimicrobial susceptibility pattern of Neisseria gonorrhoeae isolated from fertile and infertile women. Trop J Pharm Res. 2016;15(12):2653–7. 10.4314/tjpr.v15i12.17 [DOI] [Google Scholar]
  18. Bailey AL, Potter RF, Wallace MA, Johnson C, Dantas G, Burnham CA. Genotypic and Phenotypic Characterization of Antimicrobial Resistance in Neisseria gonorrhoeae: a Cross-Sectional Study of Isolates Recovered from Routine Urine Cultures in a High-Incidence Setting. MSphere. 2019. Jul;4(4):e00373–19. 10.1128/mSphere.00373-19 [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Bala M, Ray K, Gupta SM. Antimicrobial resistance pattern of Neisseria gonorrhoeae isolates from peripheral health centres and STD clinic attendees of a tertiary care centre in India. Int J STD AIDS. 2008. Jun;19(6):378–80. 10.1258/ijsa.2007.007226 [DOI] [PubMed] [Google Scholar]
  20. Barbee LA, Soge OO, Katz DA, Dombrowski JC, Holmes KK, Golden MR. Increases in Neisseria gonorrhoeae with reduced susceptibility to azithromycin among men who have sex with men in Seattle, King County, Washington, 2012–2016. Clin Infect Dis. 2018. Feb;66(5):712–8. 10.1093/cid/cix898 [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Barros Dos Santos KT, Skaf LB, Justo-da-Silva LH, Medeiros RC, Francisco Junior RD, Caniné MC, et al. Evidence for Clonally Associated Increasing Rates of Azithromycin Resistant Neisseria gonorrhoeae in Rio de Janeiro, Brazil. BioMed Res Int. 2019. Jan;2019:3180580. 10.1155/2019/3180580 [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Bazzo ML, Golfetto L, Gaspar PC, Pires AF, Ramos MC, Franchini M, et al. Brazilian-GASP Network. First nationwide antimicrobial susceptibility surveillance for Neisseria gonorrhoeae in Brazil, 2015-16. J Antimicrob Chemother. 2018. Jul;73(7):1854–61. 10.1093/jac/dky090 [DOI] [PubMed] [Google Scholar]
  23. Bharara T, Bhalla P, Rawat D, Garg VK, Sardana K, Chakravarti A. Rising trend of antimicrobial resistance among Neisseria gonorrhoeae isolates and the emergence of N. gonorrhoeae isolate with decreased susceptibility to ceftriaxone. Indian J Med Microbiol. 2015;33(1):39–42. 10.4103/0255-0857.148374 [DOI] [PubMed] [Google Scholar]
  24. Boiko I, Golparian D, Jacobsson S, Krynytska I, Frankenberg A, Shevchenko T, et al. Genomic epidemiology and antimicrobial resistance determinants of Neisseria gonorrhoeae isolates from Ukraine, 2013-2018. APMIS. 2020. Jul;128(7):465–75. 10.1111/apm.13060 [DOI] [PubMed] [Google Scholar]
  25. Boiko I, Golparian D, Krynytska I, Bezkorovaina H, Frankenberg A, Onuchyna M, et al. Antimicrobial susceptibility of Neisseria gonorrhoeae isolates and treatment of gonorrhoea patients in Ternopil and Dnipropetrovsk regions of Ukraine, 2013-2018. APMIS. 2019. Jul;127(7):503–9. 10.1111/apm.12948 [DOI] [PubMed] [Google Scholar]
  26. Brunner A, Nemes-Nikodem E, Jeney C, Szabo D, Marschalko M, Karpati S, et al. Emerging azithromycin-resistance among the Neisseria gonorrhoeae strains isolated in Hungary. Ann Clin Microbiol Antimicrob. 2016. Sep;15(1):53. 10.1186/s12941-016-0166-9 [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Brunner A, Nemes-Nikodem E, Mihalik N, Marschalko M, Karpati S, Ostorhazi E. Incidence and antimicrobial susceptibility of Neisseria gonorrhoeae isolates from patients attending the national Neisseria gonorrhoeae reference laboratory of Hungary. BMC Infect Dis. 2014. Aug;14(1):433. 10.1186/1471-2334-14-433 [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Buder S, Dudareva S, Jansen K, Loenenbach A, Nikisins S, Sailer A, et al. GORENET study group. Antimicrobial resistance of Neisseria gonorrhoeae in Germany: low levels of cephalosporin resistance, but high azithromycin resistance. BMC Infect Dis. 2018. Jan;18(1):44. 10.1186/s12879-018-2944-9 [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Calado J, Castro R, Lopes Â, Campos MJ, Rocha M, Pereira F. Antimicrobial resistance and molecular characteristics of Neisseria gonorrhoeae isolates from men who have sex with men. Int J Infect Dis. 2019. Feb;79:116–22. 10.1016/j.ijid.2018.10.030 [DOI] [PubMed] [Google Scholar]
  30. Carannante A, Ciammaruconi A, Vacca P, Anselmo A, Fillo S, Palozzi AM, et al. Genomic characterization of gonococci from different anatomic sites, Italy, 2007–2014. Microb Drug Resist. 2019. Nov;25(9):1316–24. 10.1089/mdr.2018.0371 [DOI] [PubMed] [Google Scholar]
  31. Cobo F, Cabezas-Fernández MT, Avivar C. Typing and antimicrobial susceptibility of 134 Neisseria gonorrhoeae strains from Southern Spain. Rev Esp Quimioter. 2019. Apr;32(2):114–20. [PMC free article] [PubMed] [Google Scholar]
  32. Cobo F, Cabezas-Fernández MT, Cabeza-Barrera MI. Antimicrobial susceptibility and typing of Neisseria gonorrhoeae strains from Southern Spain, 2012-2014. Enferm Infecc Microbiol Clin. 2016. Jan;34(1):3–7. 10.1016/j.eimc.2015.01.017 [DOI] [PubMed] [Google Scholar]
  33. Cole MJ, Spiteri G, Jacobsson S, Pitt R, Grigorjev V, Unemo M, Euro-GASP Network. Is the tide turning again for cephalosporin resistance in Neisseria gonorrhoeae in Europe? Results from the 2013 European surveillance. BMC Infect Dis. 2015. Aug;15(1):321. 10.1186/s12879-015-1013-x [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Costa LM, Pedroso ER, Vieira Neto V, Souza VC, Teixeira MJ. Antimicrobial susceptibility of Neisseria gonorrhoeae isolates from patients attending a public referral center for sexually transmitted diseases in Belo Horizonte, State of Minas Gerais, Brazil. Rev Soc Bras Med Trop. 2013;46(3):304–9. 10.1590/0037-8682-0009-2013 [DOI] [PubMed] [Google Scholar]
  35. Crucitti T, Belinga S, Fonkoua MC, Abanda M, Mbanzouen W, Sokeng E, et al. Sharp increase in ciprofloxacin resistance of Neisseria gonorrhoeae in Yaounde, Cameroon: analyses of a laboratory database period 2012-2018. Int J STD AIDS. 2020. May;31(6):579–86. 10.1177/0956462419897227 [DOI] [PubMed] [Google Scholar]
  36. Costa-Lourenço AP, Abrams AJ, Dos Santos KT, Argentino IC, Coelho-Souza T, Caniné MC, et al. Phylogeny and antimicrobial resistance in Neisseria gonorrhoeae isolates from Rio de Janeiro, Brazil. Infect Genet Evol. 2018. Mar;58:157–63. 10.1016/j.meegid.2017.12.003 [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Dan M, Mor Z, Gottliev S, Sheinberg B, Shohat T. Trends in antimicrobial susceptibility of Neisseria gonorrhoeae in Israel, 2002 to 2007, with special reference to fluoroquinolone resistance. Sex Transm Dis. 2010. Jul;37(7):451–3. 10.1097/OLQ.0b013e3181cfca06 [DOI] [PubMed] [Google Scholar]
  38. de Korne-Elenbaas J, Bruisten SM, de Vries HJ, 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. Jun;76(7):1759–68. 10.1093/jac/dkab082 [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Fuertes de Vega I, Baliu-Piqué C, Bosch Mestres J, Vergara Gómez A, Vallés X, Alsina Gibert M. Risk factors for antimicrobial-resistant Neisseria gonorrhoeae and characteristics of patients infected with gonorrhea. Enferm Infecc Microbiol Clin (Engl Ed). 2018. Mar;36(3):165–8. 10.1016/j.eimce.2016.11.007 [DOI] [PubMed] [Google Scholar]
  40. Dillon JA, Rubabaza JP, Benzaken AS, Sardinha JC, Li H, Bandeira MG, et al. Reduced susceptibility to azithromycin and high percentages of penicillin and tetracycline resistance in Neisseria gonorrhoeae isolates from Manaus, Brazil, 1998. Sex Transm Dis. 2001. Sep;28(9):521–6. 10.1097/00007435-200109000-00008 [DOI] [PubMed] [Google Scholar]
  41. Donegan EA, Wirawan DN, Muliawan P, Schachter J, Moncada J, Parekh M, et al. Fluoroquinolone-resistant Neisseria gonorrhoeae in Bali, Indonesia: 2004. Sex Transm Dis. 2006. Oct;33(10):625–9. 10.1097/01.olq.0000216012.83990.bd [DOI] [PubMed] [Google Scholar]
  42. Dong Y, Yang Y, Wang Y, Martin I, Demczuk W, Gu W. Shanghai Neisseria gonorrhoeae Isolates Exhibit Resistance to Extended-Spectrum Cephalosporins and Clonal Distribution. Front Microbiol. 2020. Oct;11:580399. 10.3389/fmicb.2020.580399 [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Ehinmidu J, Bolaji R, Adegboye E. Isolation and antibiotic susceptibility profile of Neisseria gonorrhoeae isolated from urine samples in Zara, Northern Nigeria. Journal of Phytomedicine and Therapeutics. 2004;9. [Google Scholar]
  44. Enders M, Turnwald-Maschler A, Regnath T. Antimicrobial resistance of Neisseria gonorrhoeae isolates from the Stuttgart and Heidelberg areas of southern Germany. Eur J Clin Microbiol Infect Dis. 2006. May;25(5):318–22. 10.1007/s10096-006-0134-y [DOI] [PubMed] [Google Scholar]
  45. Fentaw S, Abubeker R, Asamene N, Assefa M, Bekele Y, Tigabu E. Antimicrobial susceptibility profile of Gonococcal isolates obtained from men presenting with urethral discharge in Addis Ababa, Ethiopia: implications for national syndromic treatment guideline. PLoS One. 2020. Jun;15(6):e0233753. 10.1371/journal.pone.0233753 [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Ibargoyen García U, Nieto Toboso MC, Azpeitia EM, Imaz Perez M, Hernandez Ragpa L, Álava Menica JA, et al. Epidemiological surveillance study of gonococcal infection in Northern Spain. Enferm Infecc Microbiol Clin (Engl Ed). 2020. Feb;38(2):59–64. 10.1016/j.eimce.2019.05.005 [DOI] [PubMed] [Google Scholar]
  47. Gianecini R, Romero ML, Oviedo C, Vacchino M, Galarza P, Gonococcal Antimicrobial Susceptibility Surveillance Programme-Argentina Working G, Gonococcal Antimicrobial Susceptibility Surveillance Programme-Argentina (GASSP-AR) Working Group. Emergence and Spread of Neisseria gonorrhoeae Isolates With Decreased Susceptibility to Extended-Spectrum Cephalosporins in Argentina, 2009 to 2013. Sex Transm Dis. 2017. Jun;44(6):351–5. 10.1097/OLQ.0000000000000603 [DOI] [PubMed] [Google Scholar]
  48. Glazkova S, Golparian D, Titov L, Pankratova N, Suhabokava N, Shimanskaya I, et al. Antimicrobial susceptibility/resistance and molecular epidemiological characteristics of Neisseria gonorrhoeae in 2009 in Belarus. APMIS. 2011. Aug;119(8):537–42. 10.1111/j.1600-0463.2011.02770.x [DOI] [PubMed] [Google Scholar]
  49. Golparian D, Bazzo ML, Golfetto L, Gaspar PC, Schörner MA, Schwartz Benzaken A, et al. Brazilian-GASP Network. Genomic epidemiology of Neisseria gonorrhoeae elucidating the gonococcal antimicrobial resistance and lineages/sublineages across Brazil, 2015-16. J Antimicrob Chemother. 2020. Nov;75(11):3163–72. 10.1093/jac/dkaa318 [DOI] [PubMed] [Google Scholar]
  50. Golparian D, Brilene T, Laaring Y, Viktorova E, Johansson E, Domeika M, et al. First antimicrobial resistance data and genetic characteristics of Neisseria gonorrhoeae isolates from Estonia, 2009-2013. New Microbes New Infect. 2014. Sep;2(5):150–3. 10.1002/nmi2.57 [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Golparian D, Harris SR, Sánchez-Busó L, Hoffmann S, Shafer WM, Bentley SD, et al. Genomic evolution of Neisseria gonorrhoeae since the preantibiotic era (1928-2013): antimicrobial use/misuse selects for resistance and drives evolution. BMC Genomics. 2020. Feb;21(1):116. 10.1186/s12864-020-6511-6 [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Guerrero-Torres MD, Menéndez MB, Guerras CS, Tello E, Ballesteros J, Clavo P, et al. Epidemiology, molecular characterisation and antimicrobial susceptibility of Neisseria gonorrhoeae isolates in Madrid, Spain, in 2016. Epidemiol Infect. 2019. Sep;147:e274. 10.1017/S095026881900150X [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Hamasuna R, Yasuda M, Ishikawa K, Uehara S, Hayami H, Takahashi S, et al. The second nationwide surveillance of the antimicrobial susceptibility of Neisseria gonorrhoeae from male urethritis in Japan, 2012-2013. J Infect Chemother. 2015. May;21(5):340–5. 10.1016/j.jiac.2015.01.010 [DOI] [PubMed] [Google Scholar]
  54. Hamasuna R, Yasuda M, Ishikawa K, Uehara S, Takahashi S, Hayami H, et al. Nationwide surveillance of the antimicrobial susceptibility of Neisseria gonorrhoeae from male urethritis in Japan. J Infect Chemother. 2013. Aug;19(4):571–8. 10.1007/s10156-013-0637-2 [DOI] [PubMed] [Google Scholar]
  55. Harris SR, Cole MJ, Spiteri G, Sánchez-Busó L, Golparian D, Jacobsson S, et al. Euro-GASP study group. Public health surveillance of multidrug-resistant clones of Neisseria gonorrhoeae in Europe: a genomic survey. Lancet Infect Dis. 2018. Jul;18(7):758–68. 10.1016/S1473-3099(18)30225-1 [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Hjelmevoll SO, Golparian D, Dedi L, Skutlaberg DH, Haarr E, Christensen A, et al. Phenotypic and genotypic properties of Neisseria gonorrhoeae isolates in Norway in 2009: antimicrobial resistance warrants an immediate change in national management guidelines. Eur J Clin Microbiol Infect Dis. 2012. Jun;31(6):1181–6. 10.1007/s10096-011-1426-4 [DOI] [PubMed] [Google Scholar]
  57. 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. Sep;23(36):1700565. 10.2807/1560-7917.ES.2018.23.36.1700565 [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Holderman JL, Thomas JC 4th, Schlanger K, Black JM, Town K, St Cyr SB, et al. Sustained transmission of Neisseria gonorrhoeae with high-level resistance to azithromycin, in Indianapolis, Indiana, 2017–2018. Clin Infect Dis. 2021. Sep;73(5):808–15. 10.1093/cid/ciab132 [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Horn NN, Kresken M, Körber-Irrgang B, Göttig S, Wichelhaus C, Wichelhaus TA, Working Party Antimicrobial Resistance of the Paul Ehrlich Society for Chemotherapy. Antimicrobial susceptibility and molecular epidemiology of Neisseria gonorrhoeae in Germany. Int J Med Microbiol. 2014. Jul;304(5-6):586–91. 10.1016/j.ijmm.2014.04.001 [DOI] [PubMed] [Google Scholar]
  60. Hovhannisyan G, von Schoen-Angerer T, Babayan K, Fenichiu O, Gaboulaud V. Antimicrobial susceptibility of Neisseria gonorrheae strains in three regions of Armenia. Sex Transm Dis. 2007. Sep;34(9):686–8. 10.1097/01.olq.0000258433.36526.b5 [DOI] [PubMed] [Google Scholar]
  61. Ieven M, Van Looveren M, Sudigdoadi S, Rosana Y, Goossens W, Lammens C, et al. Antimicrobial susceptibilities of Neisseria gonorrhoeae strains isolated in Java, Indonesia. Sex Transm Dis. 2003. Jan;30(1):25–9. 10.1097/00007435-200301000-00006 [DOI] [PubMed] [Google Scholar]
  62. Jacobsson S, Cole MJ, Spiteri G, Day M, Unemo M, Euro-GASP Network. Associations between antimicrobial susceptibility/resistance of Neisseria gonorrhoeae isolates in European Union/European Economic Area and patients’ gender, sexual orientation and anatomical site of infection, 2009-2016. BMC Infect Dis. 2021. Mar;21(1):273. 10.1186/s12879-021-05931-0 [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Jean SS, Lu MC, Shi ZY, Tseng SH, Wu TS, Lu PL, et al. In vitro activity of ceftazidime-avibactam, ceftolozane-tazobactam, and other comparable agents against clinically important Gram-negative bacilli: results from the 2017 Surveillance of Multicenter Antimicrobial Resistance in Taiwan (SMART). Infect Drug Resist. 2018. Oct;11:1983–92. 10.2147/IDR.S175679 [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Jeverica S, Golparian D, Matičič M, Potočnik M, Mlakar B, Unemo M. 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. Jun;69(6):1517–25. 10.1093/jac/dku026 [DOI] [PubMed] [Google Scholar]
  65. Jiang FX, Lan Q, Le WJ, Su XH. Antimicrobial susceptibility of Neisseria gonorrhoeae isolates from Hefei (2014-2015): genetic characteristics of antimicrobial resistance. BMC Infect Dis. 2017. May;17(1):366. 10.1186/s12879-017-2472-z [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Joesoef MR, Knapp JS, Idajadi A, Linnan M, Barakbah Y, Kamboji A, et al. Antimicrobial susceptibilities of Neisseria gonorrhoeae strains isolated in Surabaya, Indonesia. Antimicrob Agents Chemother. 1994. Nov;38(11):2530–3. 10.1128/AAC.38.11.2530 [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Kam KM, Wong PW, Cheung MM, Ho NK, Lo KK. Quinolone-resistant Neisseria gonorrhoeae in Hong Kong. Sex Transm Dis. 1996;23(2):103–8. 10.1097/00007435-199603000-00003 [DOI] [PubMed] [Google Scholar]
  68. Karymbaeva S, Boiko I, Jacobsson S, Mamaeva G, Ibraeva A, Usupova D, et al. Antimicrobial resistance and molecular epidemiological typing of Neisseria gonorrhoeae isolates from Kyrgyzstan in Central Asia, 2012 and 2017. BMC Infect Dis. 2021. Jun;21(1):559. 10.1186/s12879-021-06262-w [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Khaki P, Bhalla P, Sharma P, Chawla R, Bhalla K. Epidemilogical analysis of Neisseria gonorrhoeae isolates by antimicrobial susceptibility testing, auxotyping and serotyping. Indian J Med Microbiol. 2007. Jul;25(3):225–9. 10.1016/S0255-0857(21)02110-1 [DOI] [PubMed] [Google Scholar]
  70. Khanam R, Ahmed D, Rahman M, Alam MS, Amin M, Khan SI, et al. Antimicrobial Susceptibility of Neisseria gonorrhoeae in Bangladesh (2014 Update). Antimicrob Agents Chemother. 2016. Jun;60(7):4418–9. 10.1128/AAC.00223-16 [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Kirkcaldy RD, Soge O, Papp JR, Hook EW 3rd, del Rio C, Kubin G, et al. Analysis of Neisseria gonorrhoeae azithromycin susceptibility in the United States by the Gonococcal Isolate Surveillance Project, 2005 to 2013. Antimicrob Agents Chemother. 2015. Feb;59(2):998–1003. 10.1128/AAC.04337-14 [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Kirkcaldy RD, Zaidi A, Hook EW 3rd, Holmes KK, Soge O, del Rio C, et al. Neisseria gonorrhoeae antimicrobial resistance among men who have sex with men and men who have sex exclusively with women: the Gonococcal Isolate Surveillance Project, 2005-2010. Ann Intern Med. 2013. Mar;158(5 Pt 1 5_Part_1):321–8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Kivata MW, Mbuchi M, Eyase FL, Bulimo WD, Kyanya CK, Oundo V, et al. gyrA and parC mutations in fluoroquinolone-resistant Neisseria gonorrhoeae isolates from Kenya. BMC Microbiol. 2019. Apr;19(1):76. 10.1186/s12866-019-1439-1 [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Kubanov A, Vorobyev D, Chestkov A, Leinsoo A, Shaskolskiy B, Dementieva E, et al. Molecular epidemiology of drug-resistant Neisseria gonorrhoeae in Russia (Current Status, 2015). BMC Infect Dis. 2016. Aug;16(1):389. 10.1186/s12879-016-1688-7 [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Kubanova A, Frigo N, Kubanov A, Sidorenko S, Lesnaya I, Polevshikova S, et al. The Russian gonococcal antimicrobial susceptibility programme (RU-GASP)—national resistance prevalence in 2007 and 2008, and trends during 2005-2008. Euro Surveill. 2010. Apr;15(14):19533. 10.2807/ese.15.14.19533-en [DOI] [PubMed] [Google Scholar]
  76. Kularatne R, Maseko V, Gumede L, Kufa T. Trends in Neisseria gonorrhoeae antimicrobial resistance over a ten-year surveillance period, Johannesburg, South Africa, 2008–2017. Antibiotics (Basel). 2018. Jul;7(3):58. 10.3390/antibiotics7030058 [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Kulkarni SV, Bala M, Muqeeth SA, Sasikala G, Nirmalkar AP, Thorat R, et al. Antibiotic susceptibility pattern of Neisseria gonorrhoeae strains isolated from five cities in India during 2013-2016. J Med Microbiol. 2018. Jan;67(1):22–8. 10.1099/jmm.0.000662 [DOI] [PubMed] [Google Scholar]
  78. Lagace-Wiens PR, Duncan S, Kimani J, Thiong’o A, Shafi J, McClelland S, et al. Emergence of fluoroquinolone resistance in Neisseria gonorrhoeae isolates from four clinics in three regions of Kenya. Sex Transm Dis. 2012. May;39(5):332–4. 10.1097/OLQ.0b013e318248a85f [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Lan PT, Golparian D, Ringlander J, Van Hung L, Van Thuong N, Unemo M. Genomic analysis and antimicrobial resistance of Neisseria gonorrhoeae isolates from Vietnam in 2011 and 2015-16. J Antimicrob Chemother. 2020. Jun;75(6):1432–8. 10.1093/jac/dkaa040 [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Le W, Su X, Lou X, Li X, Gong X, Wang B, et al. Susceptibility Trends of Zoliflodacin against Multidrug-Resistant Neisseria gonorrhoeae Clinical Isolates in Nanjing, China, 2014 to 2018. Antimicrob Agents Chemother. 2021. Feb;65(3):e00863–20. 10.1128/AAC.00863-20 [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Lebedzeu F, Golparian D, Titov L, Pankratava N, Glazkova S, Shimanskaya I, et al. Antimicrobial susceptibility/resistance and NG-MAST characterisation of Neisseria gonorrhoeae in Belarus, Eastern Europe, 2010-2013. BMC Infect Dis. 2015. Jan;15(1):29. 10.1186/s12879-015-0755-9 [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Lee H, Unemo M, Kim HJ, Seo Y, Lee K, Chong Y. Emergence of decreased susceptibility and resistance to extended-spectrum cephalosporins in Neisseria gonorrhoeae in Korea. J Antimicrob Chemother. 2015. Sep;70(9):2536–42. 10.1093/jac/dkv146 [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Lee RS, Seemann T, Heffernan H, Kwong JC, Gonçalves da Silva A, Carter GP, et al. Genomic epidemiology and antimicrobial resistance of Neisseria gonorrhoeae in New Zealand. J Antimicrob Chemother. 2018. Feb;73(2):353–64. 10.1093/jac/dkx405 [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. Li W, et al. Surveillance of antimicrobial susceptibilities of Neisseria gonorrhoeae from 2013 to 2015 in Guangxi Province, China. Japanese Journal of Infectious Diseases. JJID. 2017;2017:169. [DOI] [PubMed] [Google Scholar]
  85. Liu JW, Xu WQ, Zhu XY, Dai XQ, Chen SC, Han Y, et al. Gentamicin susceptibility of Neisseria gonorrhoeae isolates from 7 provinces in China. Infect Drug Resist. 2019. Aug;12:2471–6. 10.2147/IDR.S214059 [DOI] [PMC free article] [PubMed] [Google Scholar]
  86. Liu YH, Huang YT, Liao CH, Hsueh PR. Antimicrobial susceptibilities and molecular typing of Neisseria gonorrhoeae isolates at a medical centre in Taiwan, 2001-2013 with an emphasis on high rate of azithromycin resistance among the isolates. Int J Antimicrob Agents. 2018. May;51(5):768–74. 10.1016/j.ijantimicag.2018.01.024 [DOI] [PubMed] [Google Scholar]
  87. Liu YH, Wang YH, Liao CH, Hsueh PR. Emergence and Spread of Neisseria gonorrhoeae Strains with High-Level Resistance to Azithromycin in Taiwan from 2001 to 2018. Antimicrob Agents Chemother. 2019. Aug;63(9):e00773–19. 10.1128/AAC.00773-19 [DOI] [PMC free article] [PubMed] [Google Scholar]
  88. Lo JY, Ho KM, Lo AC. Surveillance of gonococcal antimicrobial susceptibility resulting in early detection of emerging resistance. J Antimicrob Chemother. 2012. Jun;67(6):1422–6. 10.1093/jac/dks036 [DOI] [PubMed] [Google Scholar]
  89. Loo VG, Simor AE, Jaeger R, Low DE. Survey of Neisseria gonorrhoeae antimicrobial susceptibility in Ontario. Can J Infect Dis. 1990;1(4):136–8. 10.1155/1990/739370 [DOI] [PMC free article] [PubMed] [Google Scholar]
  90. Mabonga E, Parkes-Ratanshi R, Riedel S, Nabweyambo S, Mbabazi O, Taylor C, et al. Complete ciprofloxacin resistance in gonococcal isolates in an urban Ugandan clinic: findings from a cross-sectional study. Int J STD AIDS. 2019. Mar;30(3):256–63. 10.1177/0956462418799017 [DOI] [PMC free article] [PubMed] [Google Scholar]
  91. Maduna LD, Kock MM, van der Veer BM, Radebe O, McIntyre J, van Alphen LB, et al. Antimicrobial Resistance of Neisseria gonorrhoeae Isolates from High-Risk Men in Johannesburg, South Africa. Antimicrob Agents Chemother. 2020. Oct;64(11):e00906–20. 10.1128/AAC.00906-20 [DOI] [PMC free article] [PubMed] [Google Scholar]
  92. Martin I, Sawatzky P, Allen V, Hoang L, Lefebvre B, Mina N, et al. Emergence and characterization of Neisseria gonorrhoeae isolates with decreased susceptibilities to ceftriaxone and cefixime in Canada: 2001-2010. Sex Transm Dis. 2012. Apr;39(4):316–23. 10.1097/OLQ.0b013e3182401b69 [DOI] [PubMed] [Google Scholar]
  93. Martin I, Sawatzky P, Allen V, Lefebvre B, Hoang L, Naidu P, et al. Multidrug-resistant and extensively drug-resistant Neisseria gonorrhoeae in Canada, 2012-2016. Can Commun Dis Rep. 2019. Feb;45(2-3):45–53. [DOI] [PMC free article] [PubMed] [Google Scholar]
  94. Martin I, Sawatzky P, Liu G, Allen V, Lefebvre B, Hoang L, et al. Antimicrobial susceptibilities and distribution of sequence types of Neisseria gonorrhoeae isolates in Canada: 2010. Can J Microbiol. 2013. Oct;59(10):671–8. 10.1139/cjm-2013-0357 [DOI] [PubMed] [Google Scholar]
  95. Martins RA, Cassu-Corsi D, Nodari CS, Cayô R, Natsumeda L, Streling AP, et al. Temporal evolution of antimicrobial resistance among Neisseria gonorrhoeae clinical isolates in the most populated South American Metropolitan Region. Mem Inst Oswaldo Cruz. 2019;114:e190079. 10.1590/0074-02760190079 [DOI] [PMC free article] [PubMed] [Google Scholar]
  96. Mehta SD, Maclean I, Ndinya-Achola JO, Moses S, Martin I, Ronald A, et al. Emergence of quinolone resistance and cephalosporin MIC creep in Neisseria gonorrhoeae isolates from a cohort of young men in Kisumu, Kenya, 2002 to 2009. Antimicrob Agents Chemother. 2011. Aug;55(8):3882–8. 10.1128/AAC.00155-11 [DOI] [PMC free article] [PubMed] [Google Scholar]
  97. Melendez JH, Hardick J, Barnes M, Page KR, Gaydos CA. Antimicrobial Susceptibility of Neisseria gonorrhoeae Isolates in Baltimore, Maryland, 2016: The Importance of Sentinel Surveillance in the Era of Multi-Drug-Resistant Gonorrhea. Antibiotics (Basel). 2018. Aug;7(3):77. 10.3390/antibiotics7030077 [DOI] [PMC free article] [PubMed] [Google Scholar]
  98. Mlynarczyk-Bonikowska B, Serwin AB, Golparian D, Walter de Walthoffen S, Majewski S, Koper M, et al. Antimicrobial susceptibility/resistance and genetic characteristics of Neisseria gonorrhoeae isolates from Poland, 2010-2012. BMC Infect Dis. 2014. Feb;14(1):65. 10.1186/1471-2334-14-65 [DOI] [PMC free article] [PubMed] [Google Scholar]
  99. Morris SR, Moore DF, Hannah PB, Wang SA, Wolfe J, Trees DL, et al. Strain typing and antimicrobial resistance of fluoroquinolone-resistant Neisseria gonorrhoeae causing a California infection outbreak. J Clin Microbiol. 2009. Sep;47(9):2944–9. 10.1128/JCM.01001-09 [DOI] [PMC free article] [PubMed] [Google Scholar]
  100. Nacht C, Agingu W, Otieno F, Odhiambo F, Mehta SD. Antimicrobial resistance patterns in Neisseria gonorrhoeae among male clients of a sexually transmitted infections clinic in Kisumu, Kenya. Int J STD AIDS. 2020. Jan;31(1):46–52. 10.1177/0956462419881087 [DOI] [PubMed] [Google Scholar]
  101. Naznin M, Salam MA, Hossain MZ, Alam MS. Current status of gonococcal antimicrobial susceptibility with special reference to Azithromycin and Ceftriaxone: report from a tertiary care hospital in Bangladesh. Pak J Med Sci. 2018;34(6):1397–401. 10.12669/pjms.346.16144 [DOI] [PMC free article] [PubMed] [Google Scholar]
  102. Nemes-Nikodém É, Brunner A, Pintér D, Mihalik N, Lengyel G, Marschalkó M, et al. Antimicrobial susceptibility and genotyping analysis of Hungarian Neisseria gonorrhoeae strains in 2013. Acta Microbiol Immunol Hung. 2014. Dec;61(4):435–45. 10.1556/amicr.61.2014.4.5 [DOI] [PubMed] [Google Scholar]
  103. Olsen B, Pham TL, Golparian D, Johansson E, Tran HK, Unemo M. Antimicrobial susceptibility and genetic characteristics of Neisseria gonorrhoeae isolates from Vietnam, 2011. BMC Infect Dis. 2013. Jan;13(1):40. 10.1186/1471-2334-13-40 [DOI] [PMC free article] [PubMed] [Google Scholar]
  104. Olsen B, Månsson F, Camara C, Monteiro M, Biai A, Alves A, et al. Phenotypic and genetic characterisation of bacterial sexually transmitted infections in Bissau, Guinea-Bissau, West Africa: a prospective cohort study. BMJ Open. 2012. Mar;2(2):e000636. 10.1136/bmjopen-2011-000636 [DOI] [PMC free article] [PubMed] [Google Scholar]
  105. Pinto M, Rodrigues JC, Matias R, Água-Doce I, Cordeiro D, Correia C, et al. Fifteen years of a nationwide culture collection of Neisseria gonorrhoeae antimicrobial resistance in Portugal. Eur J Clin Microbiol Infect Dis. 2020. Sep;39(9):1761–70. 10.1007/s10096-020-03907-7 [DOI] [PubMed] [Google Scholar]
  106. Qin X, Zhao Y, Chen W, Wu X, Tang S, Li G, et al. Changing antimicrobial susceptibility and molecular characterisation of Neisseria gonorrhoeae isolates in Guangdong, China: in a background of rapidly rising epidemic. Int J Antimicrob Agents. 2019. Dec;54(6):757–65. 10.1016/j.ijantimicag.2019.08.015 [DOI] [PMC free article] [PubMed] [Google Scholar]
  107. Queirós C, Borges da Costa J, Lito L, Filipe P, Melo Cristino J. Estudio retrospectivo acerca de la evolución y el desarrollo de resistencias antimicrobianas en casos diagnosticados de gonorrea en un hospital de nivel terciario en Portugal durante 10 años. Actas Dermosifiliogr (Engl Ed). 2020. Nov;111(9):761–7. 10.1016/j.ad.2020.08.010 [DOI] [PubMed] [Google Scholar]
  108. Rambaran S, Naidoo K, Dookie N, Moodley P, Sturm AW. Resistance Profile of Neisseria gonorrhoeae in KwaZulu-Natal, South Africa Questioning the Effect of the Currently Advocated Dual Therapy. Sex Transm Dis. 2019. Apr;46(4):266–70. 10.1097/OLQ.0000000000000961 [DOI] [PubMed] [Google Scholar]
  109. Regnath T, Mertes T, Ignatius R. Antimicrobial resistance of Neisseria gonorrhoeae isolates in south-west Germany, 2004 to 2015: increasing minimal inhibitory concentrations of tetracycline but no resistance to third-generation cephalosporins. Euro Surveill. 2016. Sep;21(36):30335. 10.2807/1560-7917.ES.2016.21.36.30335 [DOI] [PMC free article] [PubMed] [Google Scholar]
  110. Rice RJ, Knapp JS. Susceptibility of Neisseria gonorrhoeae associated with pelvic inflammatory disease to cefoxitin, ceftriaxone, clindamycin, gentamicin, doxycycline, azithromycin, and other antimicrobial agents. Antimicrob Agents Chemother. 1994. Jul;38(7):1688–91. 10.1128/AAC.38.7.1688 [DOI] [PMC free article] [PubMed] [Google Scholar]
  111. Ryan L, Golparian D, Fennelly N, Rose L, Walsh P, Lawlor B, et al. Antimicrobial resistance and molecular epidemiology using whole-genome sequencing of Neisseria gonorrhoeae in Ireland, 2014-2016: focus on extended-spectrum cephalosporins and azithromycin. Eur J Clin Microbiol Infect Dis. 2018. Sep;37(9):1661–72. 10.1007/s10096-018-3296-5 [DOI] [PubMed] [Google Scholar]
  112. Salmerón P, Viñado B, Arando M, Alcoceba E, Romero B, Menéndez B, et al. Neisseria gonorrhoeae antimicrobial resistance in Spain: a prospective multicentre study. J Antimicrob Chemother. 2021. May;76(6):1523–31. 10.1093/jac/dkab037 [DOI] [PubMed] [Google Scholar]
  113. Salmerón P, Viñado B, El Ouazzani R, Hernández M, Barbera MJ, Alberny M, et al. Antimicrobial susceptibility of Neisseria gonorrhoeae in Barcelona during a five-year period, 2013 to 2017. Euro Surveill. 2020. Oct;25(42):1900576. 10.2807/1560-7917.ES.2020.25.42.1900576 [DOI] [PMC free article] [PubMed] [Google Scholar]
  114. Serra-Pladevall J, Barberá MJ, Rodriguez S, Bartolomé-Comas R, Roig G, Juvé R, et al. Neisseria gonorrhoeae antimicrobial susceptibility in Barcelona: penA, ponA, mtrR, and porB mutations and NG-MAST sequence types associated with decreased susceptibility to cephalosporins. Eur J Clin Microbiol Infect Dis. 2016. Sep;35(9):1549–56. 10.1007/s10096-016-2696-7 [DOI] [PubMed] [Google Scholar]
  115. Sethi S, Golparian D, Bala M, Dorji D, Ibrahim M, Jabeen K, et al. Antimicrobial susceptibility and genetic characteristics of Neisseria gonorrhoeae isolates from India, Pakistan and Bhutan in 2007-2011. BMC Infect Dis. 2013. Jan;13(1):35. 10.1186/1471-2334-13-35 [DOI] [PMC free article] [PubMed] [Google Scholar]
  116. Shimuta K, Unemo M, Nakayama S, Morita-Ishihara T, Dorin M, Kawahata T, et al. Antibiotic-Resistant Gonorrhea Study Group. Antimicrobial resistance and molecular typing of Neisseria gonorrhoeae isolates in Kyoto and Osaka, Japan, 2010 to 2012: intensified surveillance after identification of the first strain (H041) with high-level ceftriaxone resistance. Antimicrob Agents Chemother. 2013. Nov;57(11):5225–32. 10.1128/AAC.01295-13 [DOI] [PMC free article] [PubMed] [Google Scholar]
  117. Sood S, Mahajan N, Verma R, Kar HK, Sharma VK. Emergence of decreased susceptibility to extended-spectrum cephalosporins in Neisseria gonorrhoeae in India. Natl Med J India. 2013;26(1):26–8. [PubMed] [Google Scholar]
  118. Sosa J, Ramirez-Arcos S, Ruben M, Li H, Llanes R, Llop A, et al. High percentages of resistance to tetracycline and penicillin and reduced susceptibility to azithromycin characterize the majority of strain types of Neisseria gonorrhoeae isolates in Cuba, 1995-1998. Sex Transm Dis. 2003. May;30(5):443–8. 10.1097/00007435-200305000-00012 [DOI] [PubMed] [Google Scholar]
  119. Starnino S, Suligoi B, Regine V, Bilek N, Stefanelli P, Dal Conte I, et al. Neisseria gonorrhoeae Italian Study Group. Phenotypic and genotypic characterization of Neisseria gonorrhoeae in parts of Italy: detection of a multiresistant cluster circulating in a heterosexual network. Clin Microbiol Infect. 2008. Oct;14(10):949–54. 10.1111/j.1469-0691.2008.02071.x [DOI] [PubMed] [Google Scholar]
  120. Takayama Y, Nakayama S, Shimuta K, Morita-Ishihara T, Ohnishi M. Characterization of azithromycin-resistant Neisseria gonorrhoeae isolated in Tokyo in 2005-2011. J Infect Chemother. 2014. May;20(5):339–41. 10.1016/j.jiac.2014.01.007 [DOI] [PubMed] [Google Scholar]
  121. Takuva S, Mugurungi O, Mutsvangwa J, Machiha A, Mupambo AC, Maseko V, et al. Etiology and antimicrobial susceptibility of pathogens responsible for urethral discharge among men in Harare, Zimbabwe. Sex Transm Dis. 2014. Dec;41(12):713–7. 10.1097/OLQ.0000000000000204 [DOI] [PubMed] [Google Scholar]
  122. Tanaka M, Furuya R, Irie S, Kanayama A, Kobayashi I. High Prevalence of Azithromycin-Resistant Neisseria gonorrhoeae Isolates With a Multidrug Resistance Phenotype in Fukuoka, Japan. Sex Transm Dis. 2015. Jun;42(6):337–41. 10.1097/OLQ.0000000000000279 [DOI] [PubMed] [Google Scholar]
  123. Tanaka M, Furuya R, Kobayashi I, Ohno A, Kanesaka I. Molecular characteristics and antimicrobial susceptibility of penicillinase-producing Neisseria gonorrhoeae isolates in Fukuoka, Japan, 1996-2018. J Glob Antimicrob Resist. 2021. Sep;26:45–51. 10.1016/j.jgar.2021.04.014 [DOI] [PubMed] [Google Scholar]
  124. Tanaka M, Koga Y, Nakayama H, Kanayama A, Kobayashi I, Saika T, et al. Antibiotic-resistant phenotypes and genotypes of Neisseria gonorrhoeae isolates in Japan: identification of strain clusters with multidrug-resistant phenotypes. Sex Transm Dis. 2011. Sep;38(9):871–5. 10.1097/OLQ.0b013e31821d0f98 [DOI] [PubMed] [Google Scholar]
  125. Tayimetha CY, Unemo M. Antimicrobial susceptibility of Neisseria gonorrhoeae isolates in Yaoundé, Cameroon from 2009 to 2014. Sex Transm Dis. 2018. Dec;45(12):e101–3. 10.1097/OLQ.0000000000000915 [DOI] [PubMed] [Google Scholar]
  126. Thakur SD, Levett PN, Horsman GB, Dillon JR. High levels of susceptibility to new and older antibiotics in Neisseria gonorrhoeae isolates from Saskatchewan (2003-15): time to consider point-of-care or molecular testing for precision treatment? J Antimicrob Chemother. 2018. Jan;73(1):118–25. 10.1093/jac/dkx333 [DOI] [PubMed] [Google Scholar]
  127. 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. Mar;26(3):505–15. 10.3201/eid2603.190732 [DOI] [PMC free article] [PubMed] [Google Scholar]
  128. Tribuddharat C, Pongpech P, Charoenwatanachokchai A, Lokpichart S, Srifuengfung S, Sonprasert S. Gonococcal Antimicrobial Susceptibility and the Prevalence of blaTEM-1 and blaTEM-135 Genes in Neisseria gonorrhoeae Isolates from Thailand. Jpn J Infect Dis. 2017. Mar;70(2):213–5. 10.7883/yoken.JJID.2016.209 [DOI] [PubMed] [Google Scholar]
  129. Tshokey T, Tshering T, Pradhan AR, Adhikari D, Sharma R, Gurung K, et al. Antibiotic resistance in Neisseria gonorrhoea and treatment outcomes of gonococcal urethritis suspected patients in two large hospitals in Bhutan, 2015. PLoS One. 2018. Aug;13(8):e0201721. 10.1371/journal.pone.0201721 [DOI] [PMC free article] [PubMed] [Google Scholar]
  130. Unemo M, Ahlstrand J, Sánchez-Busó L, Day M, Aanensen D, Golparian D, et al. European Collaborative Group. High susceptibility to zoliflodacin and conserved target (GyrB) for zoliflodacin among 1209 consecutive clinical Neisseria gonorrhoeae isolates from 25 European countries, 2018. J Antimicrob Chemother. 2021. Apr;76(5):1221–8. 10.1093/jac/dkab024 [DOI] [PubMed] [Google Scholar]
  131. Vandepitte J, Hughes P, Matovu G, Bukenya J, Grosskurth H, Lewis DA. High prevalence of ciprofloxacin-resistant gonorrhea among female sex workers in Kampala, Uganda (2008-2009). Sex Transm Dis. 2014. Apr;41(4):233–7. 10.1097/OLQ.0000000000000099 [DOI] [PubMed] [Google Scholar]
  132. Visser M, van Westreenen M, van Bergen J, van Benthem BH. Low gonorrhoea antimicrobial resistance and culture positivity rates in general practice: a pilot study. Sex Transm Infect. 2020. May;96(3):220–2. 10.1136/sextrans-2019-054006 [DOI] [PMC free article] [PubMed] [Google Scholar]
  133. Vorobieva V, Firsova N, Ababkova T, Leniv I, Haldorsen BC, Unemo M, et al. Antibiotic susceptibility of Neisseria gonorrhoeae in Arkhangelsk, Russia. Sex Transm Infect. 2007. Apr;83(2):133–5. 10.1136/sti.2006.021857 [DOI] [PMC free article] [PubMed] [Google Scholar]
  134. Wang F, Liu JW, Li YZ, Zhang LJ, Huang J, Chen XS, et al. Surveillance and molecular epidemiology of Neisseria gonorrhoeae isolates in Shenzhen, China, 2010-2017. J Glob Antimicrob Resist. 2020. Dec;23:269–74. 10.1016/j.jgar.2020.08.013 [DOI] [PubMed] [Google Scholar]
  135. West B, Changalucha J, Grosskurth H, Mayaud P, Gabone RM, Ka-Gina G, et al. Antimicrobial susceptibility, auxotype and plasmid content of Neisseria gonorrhoeae in northern Tanzania: emergence of high level plasmid mediated tetracycline resistance. Genitourin Med. 1995. Feb;71(1):9–12. 10.1136/sti.71.1.9 [DOI] [PMC free article] [PubMed] [Google Scholar]
  136. Wind CM, Schim van der Loeff MF, van Dam AP, de Vries HJ, van der Helm JJ. Trends in antimicrobial susceptibility for azithromycin and ceftriaxone in Neisseria gonorrhoeae isolates in Amsterdam, the Netherlands, between 2012 and 2015. Euro Surveill. 2017. Jan;22(1):30431. 10.2807/1560-7917.ES.2017.22.1.30431 [DOI] [PMC free article] [PubMed] [Google Scholar]
  137. Yan J, Chen Y, Yang F, Ling X, Jiang S, Zhao F, et al. High percentage of the ceftriaxone-resistant Neisseria gonorrhoeae FC428 clone among isolates from a single hospital in Hangzhou, China. J Antimicrob Chemother. 2021. Mar;76(4):936–9. 10.1093/jac/dkaa526 [DOI] [PubMed] [Google Scholar]
  138. Yan J, Xue J, Chen Y, Chen S, Wang Q, Zhang C, et al. Increasing prevalence of Neisseria gonorrhoeae with decreased susceptibility to ceftriaxone and resistance to azithromycin in Hangzhou, China (2015-17). J Antimicrob Chemother. 2019. Jan;74(1):29–37. [DOI] [PubMed] [Google Scholar]
  139. Yang Y, Yang Y, Martin I, Dong Y, Diao N, Wang Y, et al. NG-STAR genotypes are associated with MDR in Neisseria gonorrhoeae isolates collected in 2017 in Shanghai. J Antimicrob Chemother. 2020. Mar;75(3):566–70. 10.1093/jac/dkz471 [DOI] [PMC free article] [PubMed] [Google Scholar]
  140. Yéo A, Kouamé-Blavo B, Kouamé CE, Ouattara A, Yao AC, Gbedé BD, et al. Establishment of a Gonococcal Antimicrobial Surveillance Programme, in Accordance With World Health Organization Standards, in Côte d’Ivoire, Western Africa, 2014-2017. Sex Transm Dis. 2019. Mar;46(3):179–84. 10.1097/OLQ.0000000000000943 [DOI] [PubMed] [Google Scholar]
  141. Yin YP, Han Y, Dai XQ, Zheng HP, Chen SC, Zhu BY, et al. Susceptibility of Neisseria gonorrhoeae to azithromycin and ceftriaxone in China: A retrospective study of national surveillance data from 2013 to 2016. PLoS Med. 2018. Feb;15(2):e1002499. 10.1371/journal.pmed.1002499 [DOI] [PMC free article] [PubMed] [Google Scholar]
  142. Yuan LF, Yin YP, Dai XQ, Pearline RV, Xiang Z, Unemo M, et al. Resistance to azithromycin of Neisseria gonorrhoeae isolates from 2 cities in China. Sex Transm Dis. 2011. Aug;38(8):764–8. 10.1097/OLQ.0b013e318219cdb5 [DOI] [PubMed] [Google Scholar]
  143. Zheng XL, Xu WQ, Liu JW, Zhu XY, Chen SC, Han Y, et al. Evaluation of Drugs with Therapeutic Potential for Susceptibility of Neisseria gonorrhoeae Isolates from 8 Provinces in China from 2018. Infect Drug Resist. 2020. Dec;13:4475–86. 10.2147/IDR.S278020 [DOI] [PMC free article] [PubMed] [Google Scholar]
  144. Zheng Z, Liu L, Shen X, Yu J, Chen L, Zhan L, et al. Antimicrobial resistance and molecular characteristics among Neisseria gonorrhoeae clinical isolates in a Chinese tertiary hospital. Infect Drug Resist. 2019. Oct;12:3301–9. 10.2147/IDR.S221109 [DOI] [PMC free article] [PubMed] [Google Scholar]
  145. Zhu B, Hu Y, Zhou X, Liu K, Wen W, Hu Y. Retrospective Analysis of Drug Sensitivity of Neisseria gonorrhoeae in Teaching Hospitals of South China. Infect Drug Resist. 2021. Jun;14:2087–90. 10.2147/IDR.S317032 [DOI] [PMC free article] [PubMed] [Google Scholar]
  146. Naznin M, Salam MA, Hossain MZ, Alam MS. Current status of gonococcal antimicrobial susceptibility with special reference to Azithromycin and Ceftriaxone: report from a tertiary care hospital in Bangladesh. Pak J Med Sci. 2018;34(6):1397–401. 10.12669/pjms.346.16144 [DOI] [PMC free article] [PubMed] [Google Scholar]
  147. 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. Sep;16(5):412–25. 10.1071/SH19023 [DOI] [PMC free article] [PubMed] [Google Scholar]
  148. WHO. Global action plan to control the spread and impact of antimicrobial resistance in Neisseria gonorrhoeae. World Health Organization; 2012. [Google Scholar]
  149. WHO . Antimicrobial resistance global report on surveillance: 2014 summary. World Health Organization; 2014. [Google Scholar]
  150. Liang JY, Cao WL, Li XD, Bi C, Yang RD, Liang YH, et al. Azithromycin-resistant Neisseria gonorrhoeae isolates in Guangzhou, China (2009-2013): coevolution with decreased susceptibilities to ceftriaxone and genetic characteristics. BMC Infect Dis. 2016. Apr;16(1):152. 10.1186/s12879-016-1469-3 [DOI] [PMC free article] [PubMed] [Google Scholar]
  151. Unemo M. Current and future antimicrobial treatment of gonorrhoea - the rapidly evolving Neisseria gonorrhoeae continues to challenge. BMC Infect Dis. 2015. Aug;15(1):364. 10.1186/s12879-015-1029-2 [DOI] [PMC free article] [PubMed] [Google Scholar]
  152. Radovanovic M, Kekic D, Jovicevic M, Kabic J, Gajic I, Opavski N, et al. Current Susceptibility Surveillance and Distribution of Antimicrobial Resistance in N. gonorrheae within WHO Regions. Pathogens. 2022. Oct;11(11):1230. 10.3390/pathogens11111230 [DOI] [PMC free article] [PubMed] [Google Scholar]
  153. Shaskolskiy B, Kandinov I, Dementieva E, Gryadunov D. Antibiotic Resistance in Neisseria gonorrhoeae: Challenges in Research and Treatment. Microorganisms. 2022. Aug;10(9):1699. 10.3390/microorganisms10091699 [DOI] [PMC free article] [PubMed] [Google Scholar]
  154. Fletcher-Lartey S, Dronavalli M, Alexander K, Ghosh S, Boonwaat L, Thomas J, et al. Trends in Antimicrobial Resistance Patterns in Neisseria Gonorrhoeae in Australia and New Zealand: A Meta-analysis and Systematic Review. Antibiotics (Basel). 2019. Oct;8(4):191. 10.3390/antibiotics8040191 [DOI] [PMC free article] [PubMed] [Google Scholar]
  155. George CR, 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. Apr;14(4):e0213312. 10.1371/journal.pone.0213312 [DOI] [PMC free article] [PubMed] [Google Scholar]
  156. Brown ST, Pedersen HB, Holmes KK. Comparison of erythromycin base and estolate in gonococcal urethritis. JAMA. 1977. Sep;238(13):1371–3. 10.1001/jama.1977.03280140049015 [DOI] [PubMed] [Google Scholar]
  157. Lewis DA. The Gonococcus fights back: is this time a knock out? Sex Transm Infect. 2010 Nov;86(6):415-21. 2010;86(6):415-21. 10.1136/sti.2010.042648 [DOI] [PubMed]
  158. Laumen JG, Manoharan-Basil SS, Verhoeven E, Abdellati S, De Baetselier I, Crucitti T, et al. Molecular pathways to high-level azithromycin resistance in Neisseria gonorrhoeae. J Antimicrob Chemother. 2021. Jun;76(7):1752–8. 10.1093/jac/dkab084 [DOI] [PubMed] [Google Scholar]
  159. Młynarczyk-Bonikowska B, Majewska A, Malejczyk M, Młynarczyk G, Majewski S. Multiresistant Neisseria gonorrhoeae: a new threat in second decade of the XXI century. Med Microbiol Immunol (Berl). 2020. Apr;209(2):95–108. 10.1007/s00430-019-00651-4 [DOI] [PMC free article] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

All the data in this review are included in the manuscript.

Articles from The Yale Journal of Biology and Medicine are provided here courtesy of Yale Journal of Biology and Medicine

RESOURCES