Genomic epidemiology of Neisseria gonorrhoeae in Shenzhen, China, during 2019-2020: increased spread of ceftriaxone-resistant isolates brings insights for strengthening public health responses

The antimicrobial resistance (AMR) in gonorrhea poses global threat of increasing public health concern. In response to this concern, molecular surveillance has been widely utilized to detail the changes in the evolution and distribution of Neisseria gonorrhoeae during AMR transmission. In this study, we performed a comprehensive molecular surveillance of 664 N. gonorrhoeae isolates collected in Shenzhen, one of the cities with the largest mobile population in China, 2019-2020. In 2020, ceftriaxone showed an unprecedented high resistance rate of 24.87%, and 67.83% of the ceftriaxone-resistant (Cro-R) isolates harbored a nonmosaic penA allele. The Cro-R isolates with nonmosaic penA alleles showed a tremendous increasing trend from 0.00% in 2014 to 20.45% in 2020, which proves the need for monitoring nonmosaic penA-related resistance. Importantly, genotyping indicated that multilocus sequence typing ST11231 (35.71%) had a notable rate of ceftriaxone resistance, which might become the focus of future surveillance. Whole-genome sequencing analysis showed that the internationally spreading FC428 clones have circulated in Shenzhen region with typical ceftriaxone resistance (MIC >= 0.5 mg/L) maintained. Our surveillance combined with genomic analysis provides current information to update gonorrhea management guidelines and emphasizes that continuous AMR surveillance for N. gonorrhoeae is essential. IMPORTANCE We conducted a comprehensive molecular epidemiology analysis for antimicrobial-resistant Neisseria gonorrhoeae in Shenzhen during 2019-2020, which provided important data for personalized treatment and adjustment of monitoring strategy. Briefly, the proportion of ceftriaxone-resistant (Cro-R) isolates reached a stunning prevalence rate of 24.87% in 2020. A typical increment of Cro-R isolates with nonmosaic penA alleles proves the necessity of monitoring nonmosaic AMR mechanism and involving it into developing molecular detection methods. Whole-genome sequencing analysis showed that the international spreading FC428 clone has been circulating in Shenzhen with typical ceftriaxone resistance (MIC >= 0.5 mg/L) maintained. In summary, we conducted a comprehensive epidemiology study, providing significant data for therapy management. Our results not only improve the understanding of the distribution and transmission of AMR in N. gonorrhoeae but also provide effective AMR data for improving surveillance strategies in China.

Automated summary

The study conducted comprehensive molecular surveillance of antimicrobial-resistant Neisseria gonorrhoeae in Shenzhen from 2019 to 2020, providing important data for personalized treatment and adjustment of monitoring strategies. The resistance rate of ceftriaxone reached a stunning 24.87% in 2020. The increasing trend of ceftriaxone-resistant isolates with nonmosaic penA alleles highlights the need to monitor nonmosaic antimicrobial resistance mechanisms and develop molecular detection methods. Whole-genome sequencing analysis revealed the circulation of the internationally spreading FC428 clone with typical ceftriaxone resistance in the Shenzhen region. In summary, this comprehensive epidemiological study provides significant data for therapy management and improves surveillance strategies in China.