Dissemination of Neisseria Gonorrhoeae with Decreased Susceptibility to Extended-spectrum Cephalosporins in Southern China, 2021: a Genome-wide Surveillance from 20 Cities

Overview

Journal Ann Clin Microbiol Antimicrob

Publisher Biomed Central

Specialties Infectious Diseases
Microbiology

Date 2023 May 17

PMID 37198645

Authors

Yiwen Liao

Qinghui Xie

Xiaoxiao Li

Xiaona Yin

Xingzhong Wu

Mingjing Liu

Yuying Pan

Lihong Zeng

Jianjiang Yang

Zhanqin Feng

Xiaolin Qin

Heping Zheng

Affiliations

Soon will be listed here.

Abstract

Background: Antimicrobial resistance (AMR) of untreatable gonococcal infection is an emerging threat, especially in Guangdong, a prosperous province in Southern China.

Methods: N.gonorrhoeae was isolated from 20 cities in Guangdong and determined antimicrobial susceptibility. Through whole-genome sequencing (WGS), multilocus sequence typing (MLST), N.gonorrhoeae multiantigen sequence typing (NG-MAST), and N.gonorrhoeae sequence typing for antimicrobial resistance (NG-STAR) were obtained based on the PubMLST database ( https://pubmlst.org/ ). Phylogenetic analysis was used for dissemination and tracking analysis.

Results: Antimicrobial susceptibility was performed on 347 isolates, and 50 isolates were identified as decreased susceptibility (DS) to cephalosporins. Of which 16.0% (8/50) were ceftriaxone DS, 38.0% (19/50) were cefixime DS, and 46.0% (23/50) were both ceftriaxone and cefixime DS. In all, the dual-resistant rate of the cephalosporin-DS isolates was 96.0% for penicillin and 98.0% for tetracycline-resistant, and 10.0% (5/50) were resistant to azithromycin. All cephalosporin-DS isolates were resistant to ciprofloxacin but sensitive to spectinomycin. The predominant MLSTs were ST7363 (16%, 8/50), ST1903 (14%, 7/50), ST1901 (12%, 6/50), and ST7365 (10%, 5/50). Besides some isolates that failed genotyping (NA), NG-STAR ST1143 (n = 6) and NG-MAST ST17748 (n = 4) were the most prevalent. Twelve isolates with mosaic penA-60.001 allele retained the most elevated cephalosporin MIC (Minimum Inhibitory Concentration). Phylogenetic analysis revealed that epidemic penA-60.001 clones, either domestic or foreign, had spread to nine cities in Guangdong, and 9/12 clones were from the Pearl River Delta region.

Conclusions: N. gonorrhoeae with cephalosporins-DS was extensively disseminated in Guangdong, Southern China, requiring strict surveillance.

Citing Articles

Emerging epidemic of the Africa-type plasmid in penicillinase-producing in Guangdong, China, 2013-2022.

Qin X, Chen Y, Wu X, Chen W, Xue Y, Huang J Emerg Microbes Infect. 2024; 14(1):2440489.

PMID: 39648890 PMC: 11703304. DOI: 10.1080/22221751.2024.2440489.

Multigeographic clinical assessment of a molecular diagnostic assay for detection of key codons to predict decreased susceptibility or resistance to cephalosporins in .

Wang L, Li Y, Xiu L, Hu L, Huang J, Yong G Antimicrob Agents Chemother. 2024; 68(12):e0116524.

PMID: 39470197 PMC: 11620283. DOI: 10.1128/aac.01165-24.

Rolling the evolutionary dice: commensals as proxies for elucidating the underpinnings of antibiotic resistance mechanisms and evolution in human pathogens.

Frost K, Charron-Smith S, Cotsonas T, Dimartino D, Eisenhart R, Everingham E Microbiol Spectr. 2024; 12(2):e0350723.

PMID: 38179941 PMC: 10871548. DOI: 10.1128/spectrum.03507-23.

Identification of ceftriaxone-resistant Neisseria gonorrhoeae FC428 clone and isolates harboring a novel mosaic penA gene in Chengdu in 2019-2020.

Wang D, Wang Y, Li Y, Xiu L, Yong G, Yang Y Ann Clin Microbiol Antimicrob. 2023; 22(1):73.

PMID: 37592240 PMC: 10436653. DOI: 10.1186/s12941-023-00614-x.

References

Eyre D, Sanderson N, Lord E, Regisford-Reimmer N, Chau K, Barker L . Gonorrhoea treatment failure caused by a strain with combined ceftriaxone and high-level azithromycin resistance, England, February 2018. Euro Surveill. 2018; 23(27). PMC: 6152157. DOI: 10.2807/1560-7917.ES.2018.23.27.1800323. View

Stamatakis A . RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014; 30(9):1312-3. PMC: 3998144. DOI: 10.1093/bioinformatics/btu033. View

Wang H, Wang Y, Yong G, Li X, Yu L, Ma S . Emergence and genomic characterization of the ceftriaxone-resistant Neisseria gonorrhoeae FC428 clone in Chengdu, China. J Antimicrob Chemother. 2020; 75(9):2495-2498. DOI: 10.1093/jac/dkaa123. View

Li Y, Li Y, Xiu L, Zeng Y, Zhang C, Sun L . Typing of isolates in Shenzhen, China from 2014-2018 reveals the shift of genotypes associated with antimicrobial resistance. Antimicrob Agents Chemother. 2021; 65(5). PMC: 8092899. DOI: 10.1128/AAC.02311-20. View

Unemo M, Shafer W . Antimicrobial resistance in Neisseria gonorrhoeae in the 21st century: past, evolution, and future. Clin Microbiol Rev. 2014; 27(3):587-613. PMC: 4135894. DOI: 10.1128/CMR.00010-14. View

Huang D, Wang J, Yang T . Mapping the Spatial-Temporal Distribution and Migration Patterns of Men Who Have Sex with Men in Mainland China: A Web-Based Study. Int J Environ Res Public Health. 2020; 17(5). PMC: 7084445. DOI: 10.3390/ijerph17051469. View

Lee H, Suh Y, Lee S, Kim Y, Han M, Bae H . Emergence and Spread of Cephalosporin-Resistant Neisseria gonorrhoeae with Mosaic penA Alleles, South Korea, 2012-2017. Emerg Infect Dis. 2019; 25(3):416-424. PMC: 6390772. DOI: 10.3201/eid2503.181503. View

Shimuta K, Watanabe Y, Nakayama S, Morita-Ishihara T, Kuroki T, Unemo M . Emergence and evolution of internationally disseminated cephalosporin-resistant Neisseria gonorrhoeae clones from 1995 to 2005 in Japan. BMC Infect Dis. 2015; 15:378. PMC: 4574456. DOI: 10.1186/s12879-015-1110-x. View

Peng J, Yin Y, Chen S, Yang J, Dai X, Zheng H . A Whole-genome Sequencing Analysis of Isolates in China: An Observational Study. EClinicalMedicine. 2019; 7:47-54. PMC: 6537553. DOI: 10.1016/j.eclinm.2019.01.010. View

10.

Kirkcaldy R, Hook 3rd E, Soge O, Del Rio C, Kubin G, Zenilman J . Trends in Neisseria gonorrhoeae Susceptibility to Cephalosporins in the United States, 2006-2014. JAMA. 2015; 314(17):1869-71. PMC: 4788090. DOI: 10.1001/jama.2015.10347. View

11.

Unemo M, Del Rio C, Shafer W . Antimicrobial Resistance Expressed by Neisseria gonorrhoeae: A Major Global Public Health Problem in the 21st Century. Microbiol Spectr. 2016; 4(3). PMC: 4920088. DOI: 10.1128/microbiolspec.EI10-0009-2015. View

12.

Yuan Q, Li Y, Xiu L, Zhang C, Fu Y, Jiang C . Identification of multidrug-resistant isolates with combined resistance to both ceftriaxone and azithromycin, China, 2017-2018. Emerg Microbes Infect. 2019; 8(1):1546-1549. PMC: 6830194. DOI: 10.1080/22221751.2019.1681242. View

13.

Yin Y, Han Y, Dai X, Zheng H, Chen S, Zhu B . Susceptibility of Neisseria gonorrhoeae to azithromycin and ceftriaxone in China: A retrospective study of national surveillance data from 2013 to 2016. PLoS Med. 2018; 15(2):e1002499. PMC: 5800545. DOI: 10.1371/journal.pmed.1002499. View

14.

Nakayama S, Shimuta K, Furubayashi K, Kawahata T, Unemo M, Ohnishi M . New Ceftriaxone- and Multidrug-Resistant Neisseria gonorrhoeae Strain with a Novel Mosaic penA Gene Isolated in Japan. Antimicrob Agents Chemother. 2016; 60(7):4339-41. PMC: 4914677. DOI: 10.1128/AAC.00504-16. View

15.

Whiley D, Jennison A, Pearson J, Lahra M . Genetic characterisation of Neisseria gonorrhoeae resistant to both ceftriaxone and azithromycin. Lancet Infect Dis. 2018; 18(7):717-718. DOI: 10.1016/S1473-3099(18)30340-2. View

16.

Lee K, Nakayama S, Osawa K, Yoshida H, Arakawa S, Furubayashi K . 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):1812-1819. DOI: 10.1093/jac/dkz129. View

17.

Pleininger S, Indra A, Golparian D, Heger F, Schindler S, Jacobsson S . Extensively drug-resistant (XDR) causing possible gonorrhoea treatment failure with ceftriaxone plus azithromycin in Austria, April 2022. Euro Surveill. 2022; 27(24). PMC: 9205165. DOI: 10.2807/1560-7917.ES.2022.27.24.2200455. View

18.

Katz A . Ceftriaxone-Resistant Neisseria gonorrhoeae, Canada, 2017. Emerg Infect Dis. 2017; 24(3). PMC: 5824665. DOI: 10.3201/eid2403.171892. View

19.

Zhang L, Zhang C, Zeng Y, Li Y, Huang S, Wang F . Emergence and Characterization of a Ceftriaxone-Resistant FC428 Clone Evolving Moderate-Level Resistance to Azithromycin in Shenzhen, China. Infect Drug Resist. 2021; 14:4271-4276. PMC: 8541749. DOI: 10.2147/IDR.S336212. View

20.

McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A . The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010; 20(9):1297-303. PMC: 2928508. DOI: 10.1101/gr.107524.110. View