Genomic epidemiology and evolutionary dynamics of Bordetella pertussis: A comparative study between China and Global Strains (2018-2024).

OBJECTIVES

This study aimed to elucidate the global origins, evolutionary trajectory, and adaptive strategies of the MT28-ptxP3 macrolide-resistant Bordetella pertussis lineage driving the recent resurgence.

METHODS

We integrated long-term epidemiologic surveillance data from Shenzhen (2013-2024) with comparative genomic analysis of 632 isolates (2018-2024), including early international MT28 strains from the United States, Japan, Austria, and Vietnam. Multilocus variable-number tandem-repeat analysis and single-nucleotide polymorphism-based phylogenetics were used to define population structure and evolutionary dynamics.

RESULTS

The study revealed a dramatic clonal replacement: the MT28 lineage surged from 6.5% in 2018 to 89.4% in 2024 (P <0.001), establishing dominance. Phylogenetic analysis traced the global seeding of the MT28 backbone to the USA in 2018 and Japan/Austria in 2019. These early strains lacked the 23S ribosomal RNA (rRNA) A2047G mutation, suggesting that the recent resurgence may be due to the localized fixation of resistance within this lineage. This genotype-phenotype convergence provided a decisive fitness advantage in an antibiotic-rich environment. Epidemiologically, this expansion coincided with a significant shift in infection burden toward adolescents (age 7-15 years), indicating effective transmission in populations with waning vaccine-induced immunity.

CONCLUSIONS

The 2024 resurgence in China is linked to the localized fixation of macrolide resistance within the globally dispersed MT28 lineage. Its evolution, combining resistance, hyper-virulence, and vaccine escape (prn deficiency), highlights the urgent need for revisions in global antibiotic stewardship and vaccination strategies.