Molecular characterization and antimicrobial susceptibility for 62 isolates of Bordetella pertussis from children

Front Microbiol. 2024 Dec 11:15:1498638. doi: 10.3389/fmicb.2024.1498638. eCollection 2024.

Abstract

Background: Pertussis is a highly contagious respiratory disease caused by Bordetella pertussis (BP). Despite global control of pertussis cases through the Expanded Programme on Immunization (EPI), there has been a significant increase in the incidence of pertussis in recent years, characterized by a "resurgence" in developed countries with high immunization rates as well as a comparable reemergence in certain areas of China. We aim to explore the genotypes and antimicrobial susceptibility of circulating BP from children in Hebei.

Study design: Children diagnosed with BP infection from 2019 to 2020 in Hebei, China were enrolled. We performed antimicrobial susceptibility testing (AST), whole-genome sequencing (WGS) analysis, single nucleotide polymorphism (SNP) detection, mltilocus sequence typing (MLST), multilocus antigen sequence typing (MAST), multilevel genome typing (MGT). A total of 313 international BP genomes were selected for comparison to examine the genomic diversity and evolutionary traits of Chinese strains within a global framework.

Results: Sixty-two individuals were identified with BP infection via culture, yielding a positive rate of 15.62% (62/397) for BP. Two phylogenetic groups were identified, each carrying a dominating genotype. The two vaccine strains, CS and Tohama I, exhibited a distant relationship to these two groups. This study identified 56 erythromycin-resistant isolates, 55 azithromycin-resistant isolates, 58 sulfamethoxazole-sensitive isolates, and 53 cefotaxime-sensitive isolates. All BP isolates were sensitive to levofloxacin, amoxicillin, ceftriaxone, and meropenem. Meanwhile, all erythromycin-resistant strains, which belonged to lineage I and MGT2 sequence type 7 (ST7), shared the ptxP1 gene and contained the 23S rRNA A2047G mutation. The major MAST was prn1/ptxP1/ptxA1/fim3-1/fim2-1 (75.81%). All 62 BP strains were divided into 1, 2, 3, 14, and 52 types at the MGT1, MGT2, MGT3, MGT4, and MGT5 levels, respectively.

Conclusion: This work showed that there may be a link between antimicrobial resistance and alterations in specific molecular types, and the isolates showed a clear change when compared with the vaccine strain and that selection pressure from both antibiotics and immunization may be responsible for driving Chinese BP evolution, and necessitate a reevaluation of the immunization strategy and the development of novel vaccines in China to halt the resurgence and medication resistance of pertussis.

Keywords: Bordetella pertussis; China; children; erythromycin resistance; ptxP1.

Grants and funding

The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. This study was supported by grants from the Hebei Provincial Health Commission Project (20210177), People’s Republic of China.