Genomic Epidemiology and Evolutionary Dynamics of Bordetella pertussis: A Comparative Study Between China and Global Strains (2018-2024).

OBJECTIVES: To elucidate the global origins, evolutionary trajectory, and adaptive strategies of the MT28-ptxP3 macrolide-resistant Bordetella pertussis (MRBP) lineage driving the recent resurgence. METHODS: We integrated long-term epidemiological surveillance data from Shenzhen (2013-2024) with comparative genomic analysis of 632 isolates (2018-2024), including early international MT28 strains from the USA, Japan, Austria, and Vietnam. MLVA and SNP-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 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 towards adolescents (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.