Population structure, antibiotic resistance and molecular characteristics of Streptococcus pneumoniae causing invasive disease in Hubei, China.

Abstract

Introduction. This research sought to examine the epidemiological features, antibiotic resistance profiles and molecular characteristics of Streptococcus pneumoniae infections among hospitalized patients in Hubei, China, thus providing epidemiological evidence to inform the effective prevention and management of pneumococcal infections.Hypothesis/Gap Statement. Current research predominantly focuses on large urban centres, leaving a substantial knowledge gap regarding pneumococcal infections and resistance patterns in smaller city-level hospitals, such as those in Hubei Province.Aim. This study aimed to investigate the epidemiological features, antibiotic resistance profiles and molecular characteristics of invasive S. pneumoniae isolates from hospitalized patients in Tianmen City, Hubei, China.Methodology. S. pneumoniae strains were isolated from hospitalized patients at the First People's Hospital of Tianmen, Hubei, China, between September 2021 and September 2022. Epidemiological characteristics, serological typing and antimicrobial susceptibility of the isolates were analysed. Whole-genome sequencing was performed on the strains to identify resistance genes and virulence genes.Results. A total of 194 S. pneumoniae isolates were analysed, with 90% (174/194) from community-acquired pneumonia cases. Respiratory samples accounted for 96% of isolates, and children under 5 years old comprised 78% of cases. Seasonal variation was observed, with infections peaking in winter and spring. Antibiotic resistance analysis revealed notable age-related differences: penicillin resistance was 12.37% overall but absent in elderly patients. Ceftriaxone showed no resistance, whereas cefotaxime and meropenem exhibited higher resistance in children than in the elderly. Multilocus sequence typing identified 56 sequence types (STs), with ST271 (24.2%) being the most prevalent. Serotyping revealed 24 serotypes, with 19F (27.8%, 54/194) as the dominant type. Phylogenetic analysis showed two major clades, with strong correlations between serotype and ST distribution. Resistance genes ermB and tetM were highly prevalent (99.0% and 97.9%, respectively). Comparative genomic analysis demonstrated significantly higher resistance rates in ST271 strains than in non-ST271 strains, particularly for cefotaxime (76.60% vs. 4.76%) and meropenem (53.19% vs. 14.29%). ST271 strains predominantly expressed serotype 19F, accounting for 87% (47/54) of all serotype 19F isolates, carrying distinct resistance and virulence genes, highlighting its clinical significance.Conclusion. This study highlights a significant burden of invasive S. pneumoniae infections, predominantly affecting children under five, with notable peaks during winter and spring. ST271, predominantly associated with serotype 19F, exhibited significantly higher antibiotic resistance rates compared with other strains, indicating the necessity of tailored antibiotic strategies and robust local antibiotic stewardship programmes. The widespread presence of resistance and virulence genes underscores the evolutionary adaptability of S. pneumoniae, emphasizing the importance of continuous genetic surveillance. The current pneumococcal vaccination (13-valent pneumococcal conjugate vaccine) coverage of the predominant serotype provides a favourable outlook for disease control.