Frequency of transmission, asymptomatic shedding, and airborne spread of Streptococcus pyogenes among schoolchildren exposed to scarlet fever: a longitudinal multi-cohort molecular epidemiology contact tracing study

Background Despite recommendations regarding prompt treatment of cases and enhanced hygiene measures, scarlet fever outbreaks increased in England between 2014-2018. We aimed to assess the impact of standard interventions on transmission of Streptococcus pyogenes to classroom contacts, households, and classroom environments. Methods We undertook a prospective, contact tracing study in schools with 2 consecutive scarlet fever cases that were reported to local Health Protection teams in London between March 1 st and May 31st in 2018 and 2019. We cultured throat swabs from cases, household contacts, and classroom contacts at four time points. We also cultured hand swabs and cough plates from all cases, and from classroom contacts in 2019. Surface swabs from toys and other fomites in classrooms were cultured in 2018, and settle plates from classrooms were collected in 2019. 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 scarlet fever cases, 17 household contacts, and 278 classroom contacts were recruited from March 1 st to May 31st in 2018 and the same period in 2019. Prevalence of the outbreak S. pyogenes strain in throat swabs from asymptomatic classroom contacts was high, increasing from 9.6% (11/115) in week 1, to 26.9% (34/126) in week 2, to 24.1% (26/108) in week 3, then 14.3% (5/35) in week 4. Colonisation with non-outbreak and non-genotyped S. pyogenes strains was 1.7% (2/115); 3.9% (5/126); 5.6% (6/108); and 0/35 in the same weeks. Genome sequencing showed clonality of isolates within each of six classes, confirming recent transmission accounted for high carriage. When transmissibility was tested, children who were asymptomatic carriers of emm 4 and emm 3.93 had positive cough plates on 1/14 (7.1%) and 7/21 (33.3%) occasions respectively. Only 1/60 surface swabs taken in 3 classrooms yielded the outbreak S. pyogenes strain. In contrast, 2/12 and 6/12 settle plates placed in elevated locations yielded the outbreak S. pyogenes strain in the two classrooms tested. Interpretation S. pyogenes transmission in schools is intense and may occur prior to, or inspite of reported treatment of cases, underlining a need for rapid case management. Despite guideline adherence, heavy shedding of S. pyogenes by small numbers of classroom contacts may perpetuate outbreaks, and airborne transmission has a plausible role in spread. The findings highlight the need for research to improve understanding and assess effectiveness of interventions to reduce S. pyogenes airborne transmission.