Frequency of transmission, asymptomatic shedding, and airborne spread of Streptococcus pyogenes in schoolchildren exposed to scarlet fever: a prospective, longitudinal, multicohort, molecular epidemiological, contact-tracing study in England, UK.


Journal

The Lancet. Microbe
ISSN: 2666-5247
Titre abrégé: Lancet Microbe
Pays: England
ID NLM: 101769019

Informations de publication

Date de publication:
05 2022
Historique:
received: 09 07 2021
revised: 24 11 2021
accepted: 29 11 2021
entrez: 11 5 2022
pubmed: 12 5 2022
medline: 18 5 2022
Statut: ppublish

Résumé

Despite recommendations regarding prompt treatment of cases and enhanced hygiene measures, scarlet fever outbreaks increased in England between 2014 and 2018. We aimed to assess the effects of standard interventions on transmission of Streptococcus pyogenes to classroom contacts, households, and classroom environments to inform future guidance. We did a prospective, longitudinal, multicohort, molecular epidemiological, contact-tracing study in six settings across five schools in Greater London, UK. Schools and nurseries were eligible to participate if they had reported two cases of scarlet fever within 10 days of each other among children aged 2-8 years from the same class, with the most recent case arising in the preceding 48 h. We cultured throat swabs from children with scarlet fever, classroom contacts, and household contacts at four timepoints. We also cultured hand swabs and cough plates from all cases in years 1 and 2 of the study, and from classroom contacts in year 2. Surface swabs from toys and other fomites in classrooms were cultured in year 1, and settle plates from classrooms were collected in year 2. Any sample with S pyogenes detected was recorded as positive and underwent emm genotyping and genome sequencing to compare with the outbreak strain. Six classes, comprising 12 cases of scarlet fever, 17 household contacts, and 278 classroom contacts were recruited between March 1 and May 31, 2018 (year 1), and between March 1 and May 31, 2019 (year 2). Asymptomatic throat carriage of the outbreak strains increased from 11 (10%) of 115 swabbed children in week 1, to 34 (27%) of 126 in week 2, to 26 (24%) of 108 in week 3, and then five (14%) of 35 in week 4. Compared with carriage of outbreak S pyogenes strains, colonisation with non-outbreak and non-genotyped S pyogenes strains occurred in two (2%) of 115 swabbed children in week 1, five (4%) of 126 in week 2, six (6%) of 108 in week 3, and in none of the 35 children in week 4 (median carriage for entire study 2·8% [IQR 0·0-6·6]). Genome sequencing showed clonality of outbreak isolates within each of six classes, confirming that recent transmission accounted for high carriage. When transmissibility was tested, one (9%) of 11 asymptomatic carriers of emm4 and five (36%) of 14 asymptomatic carriers of emm3.93 had a positive cough plate. The outbreak strain was identified in only one (2%) of 60 surface swabs taken from three classrooms; however, in the two classrooms with settle plates placed in elevated locations, two (17%) of 12 and six (50%) of 12 settle plates yielded the outbreak strain. Transmission of S pyogenes in schools is intense and might occur before or despite reported treatment of cases, underlining a need for rapid case management. Despite guideline adherence, heavy shedding of S pyogenes by few classroom contacts might perpetuate outbreaks, and airborne transmission has a plausible role in its spread. These findings highlight the need for research to improve understanding and to assess effectiveness of interventions to reduce airborne transmission of S pyogenes. Action Medical Research, UK Research Innovation, and National Institute for Health Research.

Sections du résumé

BACKGROUND
Despite recommendations regarding prompt treatment of cases and enhanced hygiene measures, scarlet fever outbreaks increased in England between 2014 and 2018. We aimed to assess the effects of standard interventions on transmission of Streptococcus pyogenes to classroom contacts, households, and classroom environments to inform future guidance.
METHODS
We did a prospective, longitudinal, multicohort, molecular epidemiological, contact-tracing study in six settings across five schools in Greater London, UK. Schools and nurseries were eligible to participate if they had reported two cases of scarlet fever within 10 days of each other among children aged 2-8 years from the same class, with the most recent case arising in the preceding 48 h. We cultured throat swabs from children with scarlet fever, classroom contacts, and household contacts at four timepoints. We also cultured hand swabs and cough plates from all cases in years 1 and 2 of the study, and from classroom contacts in year 2. Surface swabs from toys and other fomites in classrooms were cultured in year 1, and settle plates from classrooms were collected in year 2. Any sample with S pyogenes detected was recorded as positive and underwent emm genotyping and genome sequencing to compare with the outbreak strain.
FINDINGS
Six classes, comprising 12 cases of scarlet fever, 17 household contacts, and 278 classroom contacts were recruited between March 1 and May 31, 2018 (year 1), and between March 1 and May 31, 2019 (year 2). Asymptomatic throat carriage of the outbreak strains increased from 11 (10%) of 115 swabbed children in week 1, to 34 (27%) of 126 in week 2, to 26 (24%) of 108 in week 3, and then five (14%) of 35 in week 4. Compared with carriage of outbreak S pyogenes strains, colonisation with non-outbreak and non-genotyped S pyogenes strains occurred in two (2%) of 115 swabbed children in week 1, five (4%) of 126 in week 2, six (6%) of 108 in week 3, and in none of the 35 children in week 4 (median carriage for entire study 2·8% [IQR 0·0-6·6]). Genome sequencing showed clonality of outbreak isolates within each of six classes, confirming that recent transmission accounted for high carriage. When transmissibility was tested, one (9%) of 11 asymptomatic carriers of emm4 and five (36%) of 14 asymptomatic carriers of emm3.93 had a positive cough plate. The outbreak strain was identified in only one (2%) of 60 surface swabs taken from three classrooms; however, in the two classrooms with settle plates placed in elevated locations, two (17%) of 12 and six (50%) of 12 settle plates yielded the outbreak strain.
INTERPRETATION
Transmission of S pyogenes in schools is intense and might occur before or despite reported treatment of cases, underlining a need for rapid case management. Despite guideline adherence, heavy shedding of S pyogenes by few classroom contacts might perpetuate outbreaks, and airborne transmission has a plausible role in its spread. These findings highlight the need for research to improve understanding and to assess effectiveness of interventions to reduce airborne transmission of S pyogenes.
FUNDING
Action Medical Research, UK Research Innovation, and National Institute for Health Research.

Identifiants

pubmed: 35544097
pii: S2666-5247(21)00332-3
doi: 10.1016/S2666-5247(21)00332-3
pmc: PMC9042792
pii:
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e366-e375

Subventions

Organisme : Medical Research Council
ID : MR/R015600/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/P022669/1
Pays : United Kingdom

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2022 The Author(s). Published by Elsevier Ltd. This is an Open Access article under the CC BY 4.0 license. Published by Elsevier Ltd.. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests We declare no competing interests.

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Auteurs

Rebecca Cordery (R)

London Health Protection Teams, Public Health England, London, UK.

Amrit K Purba (AK)

London Health Protection Teams, Public Health England, London, UK.

Lipi Begum (L)

London Health Protection Teams, Public Health England, London, UK.

Ewurabena Mills (E)

Department of Infectious Disease, Imperial College London, London, UK.

Mia Mosavie (M)

Department of Infectious Disease, Imperial College London, London, UK; NIHR Health Protection Research Unit in Healthcare Associated Infections and Antimicrobial Resistance, Imperial College London, London, UK.

Ana Vieira (A)

Department of Infectious Disease, Imperial College London, London, UK; NIHR Health Protection Research Unit in Healthcare Associated Infections and Antimicrobial Resistance, Imperial College London, London, UK; MRC Centre for Molecular Bacteriology and Infection, Imperial College London, London, UK.

Elita Jauneikaite (E)

NIHR Health Protection Research Unit in Healthcare Associated Infections and Antimicrobial Resistance, Imperial College London, London, UK; MRC Centre for Molecular Bacteriology and Infection, Imperial College London, London, UK; Department of Infectious Disease Epidemiology, School of Public Health, Imperial College London, London, UK.

Rhoda C Y Leung (RCY)

Department of Infectious Disease, Imperial College London, London, UK.

Matthew K Siggins (MK)

Department of Infectious Disease, Imperial College London, London, UK; MRC Centre for Molecular Bacteriology and Infection, Imperial College London, London, UK.

Derren Ready (D)

National Infection Service, Public Health England, London, UK; NIHR Health Protection Research Unit in Behavioural Science and Evaluation, University of Bristol, Bristol, UK.

Peter Hoffman (P)

National Infection Service, Public Health England, London, UK.

Theresa Lamagni (T)

National Infection Service, Public Health England, London, UK; NIHR Health Protection Research Unit in Healthcare Associated Infections and Antimicrobial Resistance, Imperial College London, London, UK.

Shiranee Sriskandan (S)

Department of Infectious Disease, Imperial College London, London, UK; NIHR Health Protection Research Unit in Healthcare Associated Infections and Antimicrobial Resistance, Imperial College London, London, UK; MRC Centre for Molecular Bacteriology and Infection, Imperial College London, London, UK. Electronic address: s.sriskandan@imperial.ac.uk.

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Classifications MeSH