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Clonal replacement by a P1-1/ST3 lineage in pediatric Mycoplasma pneumoniae, Jinan, China, 2021-2024
Ming Fang1, Xiao Wang2, Xiaolin Yu1
1Shandong Center for Disease Control and Prevention, Shandong Province Key Laboratory of Intelligent Monitoring, Early Warning, and Prevention of Infectious Diseases, Jinan, China.
Introduction:
After a prolonged lull during COVID-19 non-pharmaceutical interventions, Mycoplasma pneumoniae activity re-emerged in 2023 in multiple regions; in China this occurred against a backdrop of very high macrolide resistance. We conducted a retrospective single-center study of pediatric M. pneumoniae pneumonia in Jinan, comparing a pre-resurgence period (2021) with 2023-2024.
Methods:
Clinical data were linked to whole-genome sequencing of 227 cultured isolates. We assessed lineage composition and relatedness using core-genome phylogenetics and SNP-threshold networks, and compared diversity and pan-genome functional profiles across major clades. Phenotypic antimicrobial susceptibility testing was performed.
Results:
The proportion of severe cases increased from 7.4% (2021) to 19.9% (2024). Over the same interval, the P1-1/ST3 lineage rose from 41.9% to 84.0%, displacing previously co-circulating lineages. Core-genome analyses indicated reduced diversity and a compact ST3 cluster within the T1-3R subclade of the P1-type 1 lineage (EC1 clone), alongside a smaller P1-type 2/T2-2 (EC2/ST14) clade. Using a ≤11-SNP threshold, 74% of isolates fell within the largest connected component. Pan-genome comparisons suggested enrichment of replication/recombination/repair functions in T1-3R, whereas canonical adhesion factors and the CARDS toxin were conserved. All isolates carried the 23S rRNA A2063G substitution with phenotypic macrolide resistance, while in vitro susceptibility to tetracycline and levofloxacin was retained.
Discussion:
The 2023-2024 resurgence coincided with clonal replacement by P1-1/ST3 in a setting of fixed macrolide resistance and an increase in severe pediatric disease. Given the retrospective, culture-based design, this should be interpreted as a temporal association rather than evidence that ST3 intrinsically caused more severe disease. These findings support consideration of non-macrolide agents in similar high-resistance settings and motivate prospective genomic-clinical surveillance.
Insights
Mycoplasma pneumoniae resurgence in 2023 was linked to the P1-1/ST3 lineage, causing increased severe pediatric pneumonia. This highlights the need for alternative treatments due to macrolide resistance.
Area of Science:
- Infectious Diseases
- Genomics
- Microbiology
Background:
- Mycoplasma pneumoniae activity surged in 2023 after COVID-19 interventions, particularly in China, with high macrolide resistance.
- Pediatric M. pneumoniae pneumonia cases were studied retrospectively in Jinan, comparing pre-resurgence (2021) and resurgence (2023-2024) periods.
Purpose of the Study:
- To investigate the genetic lineage and antimicrobial resistance of M. pneumoniae during its resurgence.
- To assess the association between specific M. pneumoniae lineages and the severity of pediatric pneumonia.
Main Methods:
- Whole-genome sequencing of 227 M. pneumoniae isolates.
- Core-genome phylogenetics and SNP-threshold network analysis to determine lineage composition and relatedness.
- Phenotypic antimicrobial susceptibility testing and pan-genome functional profiling.
Main Results:
- The P1-1/ST3 lineage (EC1 clone) increased significantly, becoming dominant in 2023-2024.
- Severe pediatric pneumonia cases rose from 7.4% in 2021 to 19.9% in 2024.
- All isolates exhibited macrolide resistance due to the 23S rRNA A2063G substitution, but retained susceptibility to tetracycline and levofloxacin.
Conclusions:
- The M. pneumoniae resurgence was associated with clonal replacement by the P1-1/ST3 lineage.
- Increased severity of pediatric pneumonia may be linked to this dominant lineage, though further study is needed.
- Findings suggest non-macrolide antibiotics may be necessary in high-resistance settings, advocating for genomic-clinical surveillance.
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