Serotype, antibiotic susceptibility and whole-genome characterization of Streptococcus pneumoniae in all age groups living in Southwest China during 2018-2022

Chenglin Miao; Ziyi Yan; Chunmei Chen; Linghan Kuang; Keping Ao; Yingying Li; Jialu Li; Xiaocui Huang; Xinghua Zhu; Yijia Zhao; Yali Cui; Yongmei Jiang; Yi Xie

doi:10.3389/fmicb.2024.1342839

Serotype, antibiotic susceptibility and whole-genome characterization of Streptococcus pneumoniae in all age groups living in Southwest China during 2018-2022

Front Microbiol. 2024 Feb 1:15:1342839. doi: 10.3389/fmicb.2024.1342839. eCollection 2024.

Authors

Chenglin Miao^#¹, Ziyi Yan^#¹, Chunmei Chen^{2

3}, Linghan Kuang¹, Keping Ao⁴, Yingying Li^{1

5}, Jialu Li⁶, Xiaocui Huang⁷, Xinghua Zhu⁸, Yijia Zhao^{2

3}, Yali Cui^{1

2

3}, Yongmei Jiang^{1

9}, Yi Xie⁴

Affiliations

¹ Department of Laboratory Medicine, West China Second University Hospital, Sichuan University, Chengdu, Sichuan, China.
² Department of Laboratory Medicine, Meishan Women and Children's Hospital, Alliance Hospital of West China Second University Hospital, Sichuan University, Meishan, Sichuan, China.
³ Department of Laboratory Medicine, West China Second University Hospital (Tianfu), Sichuan University/Sichuan Provincial Children's Hospital, Meishan, Sichuan, China.
⁴ Department of Laboratory Medicine, West China Hospital, Sichuan University, Chengdu, Sichuan, China.
⁵ Department of Laboratory Medicine, Tibet Autonomous Region Women's and Children's Hospital, Lhasa, China.
⁶ Department of Obstetrics, Key Laboratory of Birth Defects and Related Disease of Women and Children of MOE, West China Second Hospital, Sichuan University, Chengdu, Sichuan, China.
⁷ Department of Laboratory Medicine, Chengdu Jinjiang District Maternal and Child Healthcare Hospital, Chengdu, Sichuan, China.
⁸ Department of Laboratory Medicine, The First People's Hospital of Longquanyi District, Chengdu, Sichuan, China.
⁹ Key Laboratory of Birth Defects and Related Diseases of Women and Children (Sichuan University), Ministry of Education, Chengdu, Sichuan, China.

^# Contributed equally.

Abstract

Background: Streptococcus pneumoniae is a common pathogen that colonizes the human upper respiratory tract, causing high morbidity and mortality worldwide. This study aimed to investigate the prevalence status of S. pneumoniae isolated from patients of all ages in Southwest China, including serotype, antibiotic susceptibility and other molecular characteristics, to provide a basis for clinical antibiotic usage and vaccine development.

Methods: This study was conducted from January 2018 to March 2022 at West China Hospital, West China Second University Hospital, First People's Hospital of Longquanyi District (West China Longquan Hospital), Meishan Women and Children's Hospital (Alliance Hospital of West China Second University Hospital) and Chengdu Jinjiang Hospital for Women and Children Health. Demographic and clinical characteristics of 263 pneumococcal disease (PD) all-age patients were collected and analyzed. The serotypes, sequence types (STs), and antibiotic resistance of the strains were determined by next-generation sequencing, sequence analysis and the microdilution broth method.

Results: The most common pneumococcal serotypes were 19F (17.87%), 19A (11.41%), 3 (8.75%), 23F (6.46%) and 6A (5.70%). Coverage rates for PCV10, PCV13, PCV15, PCV20 and PCV24 were 36.12, 61.98, 61.98, 63.12 and 64.26%, respectively. Prevalent STs were ST271 (12.55%), ST320 (11.79%), ST90 (4.18%), ST876 (4.18%) and ST11972 (3.42%). Penicillin-resistant S. pneumoniae (PRSP) accounted for 82.35 and 1.22% of meningitis and nonmeningitis PD cases, respectively. Resistance genes msrD (32.7%), mefA (32.7%), ermB (95.8%), tetM (97.3%) and catTC (7.6%) were found among 263 isolates. Most isolates showed high resistance to erythromycin (96.96%) and tetracycline (79.85%), with more than half being resistant to SXT (58.94%). A few isolates were resistant to AMX (9.89%), CTX (11.03%), MEN (9.13%), OFX (1.14%), LVX (1.14%) and MXF (0.38%). All isolates were susceptible to vancomycin and linezolid.

Conclusion: Our study provides reliable information, including the prevalence, molecular characterization and antimicrobial resistance of S. pneumoniae isolates causing pneumococcal diseases in Southwest China. The findings contribute to informed and clinical policy decisions for prevention and treatment.

Keywords: China; Streptococcus pneumoniae; antibiotic resistance; molecular characterization; serotype; whole-genome sequencing.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by the National Natural Science Foundation of China (No. 82300015), the Sichuan Science and Technology Program (Nos. 24NSFSC3511, 2023YFS0222, 2023YFS0223, and 2023NSFSC1699), the Cadres Healthcare Research Projects in Sichuan Province (No. 2021-1703), the Science and Technology Innovation Project of Maternal and Child Medicine in Sichuan Province (No. 21FX025) and the West China Second University Hospital (No. KL066). The funders had no role in the study design, data collection analysis, and interpretation of the data.