Genomic epidemiology and evolution of <i>Bordetella pertussis</i> under the vaccination pressure of acellular vaccines in Beijing, China, 2020–2023

Pertussis (or whooping cough) has experienced a global resurgence despite widespread vaccine efforts. In China, the incidence of pertussis has rapidly increased, particularly following the COVID-19 pandemic. Whole-genome sequencing analysis was performed on 60 <i>Bordetella pertussis</i> strains isolated in Beijing from 2020-2023, and the sequences were compared with those of 635 strains from China and 943 strains from other countries. In this study, the genetic evolution of <i>B. pertussis</i> was investigated, focusing on key virulence genes (<i>ptxP</i>, <i>ptxA</i>, <i>prn</i>, <i>fim2</i>, <i>fim3</i>, <i>tcfA</i>) and the resistance-related locus A2047 across different periods and regions. The dominant antigen genotype among the 60 isolates was <i>ptxP3</i>/<i>prn2</i>/<i>ptxA1</i>/<i>fim2-1</i>/<i>fim3-1</i>/<i>tcfA2</i> (88.3%), differing from the prevalent genotype <i>ptxP-1/prn-1/ptxA-1</i> in Beijing prior to 2019 and the vaccine strain genotype <i>ptxP-1</i>/<i>prn-1</i>/<i>ptxA-2</i>/<i>fim2-1</i>/<i>fim3-1</i>/<i>tcfA2</i>. Evolutionary analysis revealed significant genetic shifts associated with the introduction of vaccines, particularly acellular vaccines. Initially, the prevalent genotypes included <i>ptxP-1</i>, <i>prn-1</i>, <i>ptxA-2</i>, <i>fim2-2</i>, and <i>fim3-2</i>. However, currently, <i>ptxP-3</i>, <i>prn-2</i> and <i>ptxA-1</i> have become predominant globally, indicating vaccine-induced selection pressure. Additionally, all 60 isolated strains (100%) presented the A2047G mutation associated with erythromycin resistance, of which <i>ptxP3</i> accounted for 91.7%. Macrolide-resistant <i>Bordetella pertussis</i> (MRBP) is widespread in China, and the prevalence of <i>ptxP3-</i>MRBP may be increasing. The significant changes of dominance of subtypes in Beijing in recent years underscore the need for continuous surveillance and adaptation of pertussis vaccination strategies.