Molecular epidemiology and genomic features of Bordetella parapertussis in Shanghai, China, 2017-2022

Pan Fu; Yijia Li; Jie Qin; Li Xie; Chao Yang; Chuanqing Wang

doi:10.3389/fmicb.2024.1428766

Molecular epidemiology and genomic features of Bordetella parapertussis in Shanghai, China, 2017-2022

Front Microbiol. 2024 Jul 9:15:1428766. doi: 10.3389/fmicb.2024.1428766. eCollection 2024.

Authors

Pan Fu^#^{1

2}, Yijia Li^#¹, Jie Qin¹, Li Xie³, Chao Yang³, Chuanqing Wang^{1

2}

Affiliations

¹ Laboratory of Microbiology, Department of Clinical Laboratory, Children's Hospital of Fudan University, National Children's Medical Center, Shanghai, China.
² Nosocomial Infection Control Department, Children's Hospital of Fudan University, National Children's Medical Center, Shanghai, China.
³ CAS Key Laboratory of Molecular Virology and Immunology, The Center for Microbes, Development and Health, Shanghai Institute of Immunity and Infection, Chinese Academy of Sciences, Shanghai, China.

^# Contributed equally.

Abstract

Background: Pertussis is a highly contagious respiratory illness mainly caused by Bordetella pertussis (BP). Bordetella parapertussis (BPP) can induce symptoms compatible with pertussis, but has been underdiagnosed and underreported. The current pertussis vaccines offer low protection against BPP. Herein, we aim to reveal the epidemiology and genomic evolution of BPP in Shanghai, China.

Methods: Children diagnosed with BPP infection from January 2017 to December 2022 in Shanghai, China were enrolled. We performed antimicrobial susceptibility testing (AST), multiple locus variable-number tandem repeat analysis (MLVA), and whole genome sequencing (WGS) analysis. A total of 260 international BPP genomes were chosen for comparison to investigate the genomic diversity and phylogenetic characteristics of Chinese strains within a global context.

Results: Sixty patients were diagnosed with BPP infection by culture, with the positive ratio of 3.5‰ (60/17337) for BPP in nasopharyngeal swap samples. The average age of patients was 4.5 ± 0.3 years. BPPs contained four MLVA types including MT6 (65.0%), MT4 (26.7%), untype-1 (6.7%) and MT5 (1.7%), and none of strains showed resistance to macrolides. All strains carried virulence genotype of ptxP37/ptxA13/ptxB3/ptxC3/ptxD3/ptxE3/fim2-2/fim3-10. MT4 and MT5 strains carried prn54, whereas MT6 and untype-1 BPPs expressed prn101. We identified two outbreaks after 2020 caused by MT4 and MT6 strains, each corresponding to distinct WGS-based phylogenetic lineages. The MT4-lineage is estimated to have originated around 1991 and has since spread globally, being introduced to China between 2005 and 2010. In contrast, the MT6-lineage was exclusively identified in China and is inferred to have originated around 2002.

Conclusion: We revealed the genomic diversity of BPPs circulating in Shanghai, China, and reported the outbreaks of MT6 and MT4 BPPs after 2020. This is the first report on the emergence and regional outbreak of MT6 BPPs in the world, indicating that continuous surveillance on BPPs are thus required.

Keywords: Bordetella parapertussis; China; MT4; MT6; children.

Grants and funding

The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. This work was supported by grants from the National Natural Science Foundation of China (grant no. 82202567) and the Shanghai municipal three-year action plan for strengthening the construction of the public health system (2023–2025) GWVI-2.1.2.