Evolution of strain diversity and virulence factor repertoire in pediatric Staphylococcus aureus isolates.

<h4>Background</h4>Invasive Staphylococcus aureus infections cause high morbidity and mortality in children and adults. With rising antimicrobial resistance, optimal prevention strategies and novel therapeutics are needed. As an effective vaccine remains elusive, characterization of inva...

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Main Authors: Margaret Free, Nicole Soper, James C Slaughter, Andries Feder, Colleen Bianco, Ahmed M Moustafa, Paul Planet, C Buddy Creech, Isaac Thomsen
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2025-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0326353
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author Margaret Free
Nicole Soper
James C Slaughter
Andries Feder
Colleen Bianco
Ahmed M Moustafa
Paul Planet
C Buddy Creech
Isaac Thomsen
author_facet Margaret Free
Nicole Soper
James C Slaughter
Andries Feder
Colleen Bianco
Ahmed M Moustafa
Paul Planet
C Buddy Creech
Isaac Thomsen
author_sort Margaret Free
collection DOAJ
description <h4>Background</h4>Invasive Staphylococcus aureus infections cause high morbidity and mortality in children and adults. With rising antimicrobial resistance, optimal prevention strategies and novel therapeutics are needed. As an effective vaccine remains elusive, characterization of invasive isolates over time is required to identify determinants of invasive infection.<h4>Methods</h4>S. aureus isolates recovered from children with invasive infection and those with colonization were obtained. Isolates were examined by whole genome sequencing to evaluate gene repertoire, sequence type, clonal complex, and phylogenetic characterization, and isolate characteristics were correlated to clinical data.<h4>Results</h4>118 children with invasive S. aureus infections were enrolled; 56% of infections were caused by methicillin-susceptible S. aureus (MSSA). Methicillin-resistance (MRSA) was associated with increased inflammation, though clinical outcomes of MRSA vs MSSA did not differ. Colonization isolates exhibited higher sequence type diversity than invasive isolates. Nine distinct clonal complexes (CC) were identified among all isolates; CC8 and CC5 were associated with higher clinical severity scores. Accessory gene regulator locus type 1, Panton-Valentine Leukocidin, and arginine catabolic mobile element declined over time. Staphylokinase and leukocidin ED were associated with invasive infection, while enterotoxin B was more frequent in colonizing isolates.<h4>Conclusions</h4>We observed a significant expansion in sequence type diversity among invasive clinical isolates over 12 years with the emergence of newly invasive clones in recent years. The presence of staphylokinase and LukED were associated with invasive infection over time. These findings provide insights into the pathogenesis of invasive S. aureus and may provide putative targets for immunologic approaches to prevention.
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spelling doaj-art-774fa94393ba41d98ce141afb7fb64a52025-08-20T03:23:30ZengPublic Library of Science (PLoS)PLoS ONE1932-62032025-01-01207e032635310.1371/journal.pone.0326353Evolution of strain diversity and virulence factor repertoire in pediatric Staphylococcus aureus isolates.Margaret FreeNicole SoperJames C SlaughterAndries FederColleen BiancoAhmed M MoustafaPaul PlanetC Buddy CreechIsaac Thomsen<h4>Background</h4>Invasive Staphylococcus aureus infections cause high morbidity and mortality in children and adults. With rising antimicrobial resistance, optimal prevention strategies and novel therapeutics are needed. As an effective vaccine remains elusive, characterization of invasive isolates over time is required to identify determinants of invasive infection.<h4>Methods</h4>S. aureus isolates recovered from children with invasive infection and those with colonization were obtained. Isolates were examined by whole genome sequencing to evaluate gene repertoire, sequence type, clonal complex, and phylogenetic characterization, and isolate characteristics were correlated to clinical data.<h4>Results</h4>118 children with invasive S. aureus infections were enrolled; 56% of infections were caused by methicillin-susceptible S. aureus (MSSA). Methicillin-resistance (MRSA) was associated with increased inflammation, though clinical outcomes of MRSA vs MSSA did not differ. Colonization isolates exhibited higher sequence type diversity than invasive isolates. Nine distinct clonal complexes (CC) were identified among all isolates; CC8 and CC5 were associated with higher clinical severity scores. Accessory gene regulator locus type 1, Panton-Valentine Leukocidin, and arginine catabolic mobile element declined over time. Staphylokinase and leukocidin ED were associated with invasive infection, while enterotoxin B was more frequent in colonizing isolates.<h4>Conclusions</h4>We observed a significant expansion in sequence type diversity among invasive clinical isolates over 12 years with the emergence of newly invasive clones in recent years. The presence of staphylokinase and LukED were associated with invasive infection over time. These findings provide insights into the pathogenesis of invasive S. aureus and may provide putative targets for immunologic approaches to prevention.https://doi.org/10.1371/journal.pone.0326353
spellingShingle Margaret Free
Nicole Soper
James C Slaughter
Andries Feder
Colleen Bianco
Ahmed M Moustafa
Paul Planet
C Buddy Creech
Isaac Thomsen
Evolution of strain diversity and virulence factor repertoire in pediatric Staphylococcus aureus isolates.
PLoS ONE
title Evolution of strain diversity and virulence factor repertoire in pediatric Staphylococcus aureus isolates.
title_full Evolution of strain diversity and virulence factor repertoire in pediatric Staphylococcus aureus isolates.
title_fullStr Evolution of strain diversity and virulence factor repertoire in pediatric Staphylococcus aureus isolates.
title_full_unstemmed Evolution of strain diversity and virulence factor repertoire in pediatric Staphylococcus aureus isolates.
title_short Evolution of strain diversity and virulence factor repertoire in pediatric Staphylococcus aureus isolates.
title_sort evolution of strain diversity and virulence factor repertoire in pediatric staphylococcus aureus isolates
url https://doi.org/10.1371/journal.pone.0326353
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