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SDG 3: STI

Abstract

Background

The global dissemination of ceftriaxone-resistant FC428-like strains poses a public health concern. To assess and follow their spread, establishing effective antimicrobial resistance (AMR) surveillance systems is essential.

Aim

This study aimed to track ceftriaxone-resistant FC428-like strains in parts of China, using a molecular screening tool.

Methods

Samples were collected from Sichuan, Zhejiang, Shanghai, and Guangdong provinces between 2019 and 2021. We employed a rapid molecular tool − the high-resolution melting analysis-based FC428 (HRM-FC428) assay, to screen for FC428-like strains. All FC428-like strains detected were further characterised by genotyping and PCR-sequencing.

Results

Of 1,042 tested samples, 44 harboured the -60.001 allele linked to ceftriaxone resistance, revealing a 4.2% prevalence of FC428-like strains. The HRM-FC428 assay additionally uncovered six strains with mosaic -195.001 or -232.001 alleles, both bearing the A311V mutation, a ceftriaxone resistance marker. During the study, the prevalence of FC428-like strains among overall samples appeared to increase, with rates of 2.8% (11/395) in 2019, 4.2% (16/378) in 2020, and 6.3% (17/269) in 2021. Some strains’ sequence types (ST)s were identified across provinces (e.g. ST1903, ST1600) and most strains (24/44) were ST1903, an ST also reported in other regions/countries, suggesting local evolution and global transmission.

Conclusion

Our work underscores the value of culture-independent antimicrobial resistance monitoring and validates the use of molecular diagnostic tools, like the HRM-FC428 assay for this purpose. This study offers insights into the complex landscape of ceftriaxone-resistant , emphasising the importance of continued surveillance and global collaboration to mitigate this growing public health threat.

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This work is licensed under a Creative Commons Attribution 4.0 International License.
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2025-02-13
2025-02-15
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References

  1. World Health Organization (WHO). Multi-drug resistant gonorrhoea. Geneva: WHO; 2024. Available from: https://www.who.int/news-room/fact-sheets/detail/multi-drug-resistant-gonorrhoea
  2. 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 
  3. Allan-Blitz LT, Adamson PC, Klausner JD. Resistance-Guided Therapy for Neisseria gonorrhoeae. Clin Infect Dis. 2022;75(9):1655-60.  https://doi.org/10.1093/cid/ciac371  PMID: 35818315 
  4. Lee K, Nakayama SI, Osawa K, Yoshida H, Arakawa S, Furubayashi KI, et al. Clonal expansion and spread of the ceftriaxone-resistant Neisseria gonorrhoeae strain FC428, identified in Japan in 2015, and closely related isolates. J Antimicrob Chemother. 2019;74(7):1812-9.  https://doi.org/10.1093/jac/dkz129  PMID: 31002306 
  5. Eyre DW, Town K, Street T, Barker L, Sanderson N, Cole MJ, et al. Detection in the United Kingdom of the Neisseria gonorrhoeae FC428 clone, with ceftriaxone resistance and intermediate resistance to azithromycin, October to December 2018. Euro Surveill. 2019;24(10):1900147.  https://doi.org/10.2807/1560-7917.ES.2019.24.10.1900147  PMID: 30862336 
  6. Yuan Q, Li Y, Xiu L, Zhang C, Fu Y, Jiang C, et al. Identification of multidrug-resistant Neisseria gonorrhoeae isolates with combined resistance to both ceftriaxone and azithromycin, China, 2017-2018. Emerg Microbes Infect. 2019;8(1):1546-9.  https://doi.org/10.1080/22221751.2019.1681242  PMID: 31661379 
  7. Xiu L, Wang L, Li Y, Hu L, Huang J, Yong G, et al. Multicentre Clinical Evaluation of a Molecular Diagnostic Assay to Identify Neisseria gonorrhoeae Infection and Detect Antimicrobial Resistance. Int J Antimicrob Agents. 2023;61(5):106785.  https://doi.org/10.1016/j.ijantimicag.2023.106785  PMID: 36918087 
  8. 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;76(4):936-9.  https://doi.org/10.1093/jac/dkaa526  PMID: 33406237 
  9. Tickner JA, Lahra MM, Whiley DM. The need for a commercial test using the penA60 allele to identify ceftriaxone-resistant Neisseria gonorrhoeae. Lancet Infect Dis. 2022;22(9):1271-2.  https://doi.org/10.1016/S1473-3099(22)00520-5  PMID: 35961361 
  10. Kersh EN, Pham CD, Papp JR, Myers R, Steece R, Kubin G, et al. Expanding U.S. Laboratory Capacity for Neisseria gonorrhoeae Antimicrobial Susceptibility Testing and Whole-Genome Sequencing through the CDC’s Antibiotic Resistance Laboratory Network. J Clin Microbiol. 2020;58(4):e01461-19.  https://doi.org/10.1128/JCM.01461-19  PMID: 32024723 
  11. 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 
  12. Whiley DM, Mhango L, Jennison AV, Nimmo G, Lahra MM. Direct Detection of penA Gene Associated with Ceftriaxone-Resistant Neisseria gonorrhoeae FC428 Strain by Using PCR. Emerg Infect Dis. 2018;24(8):1573-5.  https://doi.org/10.3201/eid2408.180295  PMID: 30016236 
  13. Shimuta K, Igawa G, Yasuda M, Deguchi T, Nakayama SI, Ohnishi M. A real-time PCR assay for detecting a penA mutation associated with ceftriaxone resistance in Neisseria gonorrhoeae. J Glob Antimicrob Resist. 2019;19:46-9.  https://doi.org/10.1016/j.jgar.2019.02.011  PMID: 30825697 
  14. Li Y, Xiu L, Liu J, Zhang C, Wang F, Yin Y, et al. A multiplex assay for characterization of antimicrobial resistance in Neisseria gonorrhoeae using multi-PCR coupled with mass spectrometry. J Antimicrob Chemother. 2020;75(10):2817-25.  https://doi.org/10.1093/jac/dkaa269  PMID: 32688393 
  15. Sanderson ND, Swann J, Barker L, Kavanagh J, Hoosdally S, Crook D, et al. , GonFast Investigators Group. High precision Neisseria gonorrhoeae variant and antimicrobial resistance calling from metagenomic Nanopore sequencing. Genome Res. 2020;30(9):1354-63.  https://doi.org/10.1101/gr.262865.120  PMID: 32873606 
  16. Zhang C, Xiu L, Li Y, Sun L, Li Y, Zeng Y, et al. Multiplex PCR and Nanopore Sequencing of Genes Associated with Antimicrobial Resistance in Neisseria gonorrhoeae Directly from Clinical Samples. Clin Chem. 2021;67(4):610-20 https://doi.org/10.1093/clinchem/hvaa306  PMID: 33367585 
  17. Xiu L, Zhang C, Li Y, Wang F, Peng J. High-resolution melting analysis for rapid detection of the internationally spreading ceftriaxone-resistant Neisseria gonorrhoeae FC428 clone. J Antimicrob Chemother. 2020;75(1):106-9.  https://doi.org/10.1093/jac/dkz395  PMID: 31834402 
  18. Xiu L, Yuan Q, Li Y, Zhang C, Tang L, Peng J. Emergence of ceftriaxone-resistant Neisseria gonorrhoeae strains harbouring a novel mosaic penA gene in China. J Antimicrob Chemother. 2020;75(4):907-10.  https://doi.org/10.1093/jac/dkz530  PMID: 31899504 
  19. 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;75(3):566-70.  https://doi.org/10.1093/jac/dkz471  PMID: 31713620 
  20. Clinical and Laboratory Standards Institute (CLSI). Performance standards for antimicrobial susceptibility testing. 32nd edition. CLSI: United States; 2022.
  21. European Committee on Antimicrobial Susceptibility Testing (EUCAST). Clinical breakpoints - breakpoints and guidance, version 14. Växjö: EUCAST; 2017. Available from: https://www.eucast.org/clinical_breakpoints
  22. Wang D, Li Y, Zhang C, Zeng Y, Peng J, Wang F. Genomic epidemiology of Neisseria gonorrhoeae in Shenzhen, China, during 2019-2020: increased spread of ceftriaxone-resistant isolates brings insights for strengthening public health responses. Microbiol Spectr. 2023;11(5):e0172823.  https://doi.org/10.1128/spectrum.01728-23  PMID: 37732794 
  23. Wang D, Wang Y, Li Y, Xiu L, Yong G, Yang Y, et al. Identification of ceftriaxone-resistant Neisseria gonorrhoeae FC428 clone and isolates harboring a novel mosaic penA gene in Chengdu in 2019-2020. Ann Clin Microbiol Antimicrob. 2023;22(1):73.  https://doi.org/10.1186/s12941-023-00614-x  PMID: 37592240 
  24. Xiu L, Zhang L, Peng J. Surge in ceftriaxone-resistant Neisseria gonorrhoeae FC428-like strains, Asia-Pacific Region, 2015-2022. Emerg Infect Dis. 2024;30(8):1683-6.  https://doi.org/10.3201/eid3008.240139  PMID: 39043453 
  25. Schmerer MW, Abrams AJ, Seby S, Thomas JC 4th, Cartee J, Lucking S, et al. . Genomic Characterization of Neisseria gonorrhoeae Strains from 2016 U.S. Sentinel Surveillance Displaying Reduced Susceptibility to Azithromycin. Antimicrob Agents Chemother. 2020;64(5):e02420-19.  https://doi.org/10.1128/AAC.02420-19  PMID: 32071056 
  26. Lahra MM, Ryder N, Whiley DM. A new multidrug-resistant strain of Neisseria gonorrhoeae in Australia. N Engl J Med. 2014;371(19):1850-1.  https://doi.org/10.1056/NEJMc1408109  PMID: 25372111 
  27. Sánchez-Busó L, Yeats CA, Taylor B, Goater RJ, Underwood A, Abudahab K, et al. A community-driven resource for genomic epidemiology and antimicrobial resistance prediction of Neisseria gonorrhoeae at Pathogenwatch. Genome Med. 2021;13(1):61.  https://doi.org/10.1186/s13073-021-00858-2  PMID: 33875000 
  28. Tang Y, Liu X, Chen W, Luo X, Zhuang P, Li R, et al. Antimicrobial Resistance Profiling and Genome Analysis of the penA-60.001 Neisseria gonorrhoeae Clinical Isolates in China in 2021. J Infect Dis. 2023;228(6):792-9.  https://doi.org/10.1093/infdis/jiad258  PMID: 37462263 
  29. Zhao Y, Le W, Genco CA, Rice PA, Su X. Increase in Multidrug Resistant Neisseria gonorrhoeae FC428-Like Isolates Harboring the Mosaic penA 60.001 Gene, in Nanjing, China (2017-2020). Infect Drug Resist. 2023;16:4053-64.  https://doi.org/10.2147/IDR.S408896  PMID: 37383603 
  30. Lahra MM, Martin I, Demczuk W, Jennison AV, Lee KI, Nakayama SI, et al. Cooperative Recognition of Internationally Disseminated Ceftriaxone-Resistant Neisseria gonorrhoeae Strain. Emerg Infect Dis. 2018;24(4):735-40.  https://doi.org/10.3201/eid2404.171873  PMID: 29553335 
  31. Poncin T, Fouere S, Braille A, Camelena F, Agsous M, Bebear C, et al. Multidrug-resistant Neisseria gonorrhoeae failing treatment with ceftriaxone and doxycycline in France, November 2017. Euro Surveill. 2018;23(21):1800264.  https://doi.org/10.2807/1560-7917.ES.2018.23.21.1800264  PMID: 29845928 
  32. Berenger BM, Demczuk W, Gratrix J, Pabbaraju K, Smyczek P, Martin I. Genetic Characterization and Enhanced Surveillance of Ceftriaxone-Resistant Neisseria gonorrhoeae Strain, Alberta, Canada, 2018. Emerg Infect Dis. 2019;25(9):1660-7.  https://doi.org/10.3201/eid2509.190407  PMID: 31407661 
  33. Chen SC, Yuan LF, Zhu XY, van der Veen S, Yin YP. Sustained transmission of the ceftriaxone-resistant Neisseria gonorrhoeae FC428 clone in China. J Antimicrob Chemother. 2020;75(9):2499-502.  https://doi.org/10.1093/jac/dkaa196  PMID: 32473014 
  34. Peng JP, Yin YP, Chen SC, Yang J, Dai XQ, Zheng HP, et al. A Whole-genome Sequencing Analysis of Neisseria gonorrhoeae Isolates in China: An Observational Study. EClinicalMedicine. 2019;7:47-54.  https://doi.org/10.1016/j.eclinm.2019.01.010  PMID: 31193648 
  35. Salmerón P, Buckley C, Arando M, Alcoceba E, Romero B, Clavo P, et al. Genome-based epidemiology and antimicrobial resistance of Neisseria gonorrhoeae in Spain: A prospective multicentre study. J Eur Acad Dermatol Venereol. 2023;37(12):2575-82.  https://doi.org/10.1111/jdv.19458  PMID: 37620291 
  36. Demczuk W, Martin I, Sawatzky P, Allen V, Lefebvre B, Hoang L, et al. Equations To Predict Antimicrobial MICs in Neisseria gonorrhoeae Using Molecular Antimicrobial Resistance Determinants. Antimicrob Agents Chemother. 2020;64(3):e02005-19.  https://doi.org/10.1128/AAC.02005-19  PMID: 31871081 
  37. Donà V, Low N, Golparian D, Unemo M. Recent advances in the development and use of molecular tests to predict antimicrobial resistance in Neisseria gonorrhoeae. Expert Rev Mol Diagn. 2017;17(9):845-59.  https://doi.org/10.1080/14737159.2017.1360137  PMID: 28741392 
Molecular screening to track ceftriaxone-resistant FC428-like Neisseria gonorrhoeae strains’ dissemination in four provinces of China, 2019 to 2021
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Leshan+Xiu&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Xiu Leshan</a>, <a href="/search?value1=Liqin+Wang&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Wang Liqin</a>, <a href="/search?value1=Yamei+Li&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Li Yamei</a>, <a href="/search?value1=Lihua+Hu&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Hu Lihua</a>, <a href="/search?value1=Jia+Huang&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Huang Jia</a>, <a href="/search?value1=Gang+Yong&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Yong Gang</a>, <a href="/search?value1=Youwei+Wang&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Wang Youwei</a>, <a href="/search?value1=Wenling+Cao&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Cao Wenling</a>, <a href="/search?value1=Yang+Yang&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Yang Yang</a>, <a href="/search?value1=Weiming+Gu&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Gu Weiming</a>, <a href="/search?value1=Junping+Peng&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Peng Junping</a></span>. Molecular screening to track ceftriaxone-resistant FC428-like Neisseria gonorrhoeae strains’ dissemination in four provinces of China, 2019 to 2021. <a href="/content/ecdc">Euro Surveill.</a> 2025;30(6):pii=2400166. <a href="https://doi.org/10.2807/1560-7917.ES.2025.30.6.2400166" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2025.30.6.2400166</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 18 Mar 2024;&nbsp;&nbsp; <span class="generated">Accepted</span>: 31 Jul 2024 </span> </p>
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