Abstract
ObjectivesChina has experienced a notable upsurge in pertussis cases post-COVID-19, alongside an age shift to older children, increased vaccine escape, and a notable rise in the prevalence of macrolide-resistant Bordetella pertussis (MRBP). Here, we present a genomic epidemiological investigation of these events. MethodsWe performed a retrospective observational study using culture-positive B. pertussis isolated in Shanghai, China between 2016 and 2024. We analysed strain and pertussis epidemiology dynamics by integrating whole-genome sequencing of 723 strains with antimicrobial susceptibility, transcriptomic profile, and clinical data. We compared the genome sequences of Shanghai strains with 6450 Chinese and global strains. ResultsFrom pre-COVID-19 (before December 2019) to post-COVID-19, patients shifted from predominantly infants (90%, 397/442) to a higher proportion of infections in older children (infant: 16%, 132/844), with the share of vaccinated individuals surging from 31% (107/340) to 88% (664/756). The MRBP prevalence increased from 60% (267/447) to 98% (830/845). The emergence and expansion of a ptxP3-lineage macrolide-resistant clone, MR-MT28, which is uniquely capable of causing substantial infections among older children and vaccinated individuals, was temporally strongly associated with the pertussis upsurge and epidemiological transition. While MR-MT28 showed increased expression of genes encoding pertussis toxin, it was associated with significantly milder clinical symtoms and a lower hospitalization rate. MR-MT28 likely originated in China around 2016, after acquiring several key mutations including a novel prn150 allele, and has been detected across multiple regions in China. Additionally, 26% (50/195) of MR-MT28 has evolved into predicted PRN-deficient strains, with an IS481 insertion being the predominant mechanism. ConclusionsWe report that the post-COVID-19 upsurge of pertussis in China is associated with ptxP3-MR-MT28, and provide evidence that pathogen evolution is likely the primary factor driving pertussis upsurge, age shift and vaccine escape. MR-MT28 poses a high risk of global spread and warrants global surveillance.
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