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Rapid Emergence of a New Clone Impacts the Population at Risk and Increases the Incidence of Type emm89 Group A Streptococcus Invasive Disease.

ABSTRACT: BACKGROUND:Invasive group A Streptococcus (iGAS) disease caused by type emm89 strains has been increasing worldwide, driven by the emergence of an epidemic clonal variant (clade 3 emm89). The clinical characteristics of patients with emm89 iGAS disease, and in particular with clade 3 emm89 iGAS disease, are poorly described. METHODS:We used population-based iGAS surveillance data collected in metropolitan Toronto, Ontario, Canada during the period 2000-2014. We sequenced the genomes of 105 emm89 isolates representing all emm89 iGAS disease cases in the area during the period and 138 temporally matched emm89 iGAS isolates collected elsewhere in Ontario. RESULTS:Clades 1 and 2 and clade O, a newly discovered emm89 genetic variant, caused most cases of emm89 iGAS disease in metropolitan Toronto before 2008. After rapid emergence of new clade 3, previously circulating clades were purged from the population and the incidence of emm89 iGAS disease significantly increased from 0.14 per 100000 in 2000-2007 to 0.22 per 100000 in 2008-2014. Overall, emm89 organisms caused significantly more arthritis but less necrotizing fasciitis than strains of the more common type emm1. Other clinical presentations were soft tissue and severe respiratory tract infections. Clinical outcomes did not differ significantly between emm89 clades overall. However, clade 3 emm89 iGAS disease was more common in youth and middle-aged individuals. CONCLUSIONS:The rapid shift in emm89 iGAS strain genetics in metropolitan Toronto has resulted in a significant increase in the incidence of emm89 iGAS disease, with noticeably higher rates of clade 3 disease in younger patients.

SUBMITTER: Teatero S

PROVIDER: S-EPMC5407211 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Rapid Emergence of a New Clone Impacts the Population at Risk and Increases the Incidence of Type <i>emm89</i> Group A <i>Streptococcus</i> Invasive Disease.

Teatero Sarah S Coleman Brenda L BL Beres Stephen B SB Olsen Randall J RJ Kandel Christopher C Reynolds Olivia O Athey Taryn B T TBT Musser James M JM McGeer Allison A Fittipaldi Nahuel N

Open forum infectious diseases 20170304 2

<h4>Background</h4>Invasive group A <i>Streptococcus</i> (iGAS) disease caused by type <i>emm89</i> strains has been increasing worldwide, driven by the emergence of an epidemic clonal variant (clade 3 <i>emm89</i>). The clinical characteristics of patients with <i>emm89</i> iGAS disease, and in particular with clade 3 <i>emm89</i> iGAS disease, are poorly described.<h4>Methods</h4>We used population-based iGAS surveillance data collected in metropolitan Toronto, Ontario, Canada during the perio ...[more]

PMID: 28470020

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Project description:UnlabelledGroup A Streptococcus (GAS) genotype emm89 is increasingly recognized as a leading cause of disease worldwide, yet factors that underlie the success of this emm type are unknown. Surveillance identified a sustained nationwide increase in emm89 invasive GAS disease in the United Kingdom, prompting longitudinal investigation of this genotype. Whole-genome sequencing revealed a recent dramatic shift in the emm89 population with the emergence of a new clade that increased to dominance over previous emm89 variants. Temporal analysis indicated that the clade arose in the early 1990s but abruptly increased in prevalence in 2008, coinciding with an increased incidence of emm89 infections. Although standard variable typing regions (emm subtype, tee type, sof type, and multilocus sequence typing [MLST]) remained unchanged, uniquely the emergent clade had undergone six distinct regions of homologous recombination across the genome compared to the rest of the sequenced emm89 population. Two of these regions affected known virulence factors, the hyaluronic acid capsule and the toxins NADase and streptolysin O. Unexpectedly, and in contrast to the rest of the sequenced emm89 population, the emergent clade-associated strains were genetically acapsular, rendering them unable to produce the hyaluronic acid capsule. The emergent clade-associated strains had also acquired an NADase/streptolysin O locus nearly identical to that found in emm12 and modern emm1 strains but different from the rest of the sequenced emm89 population. The emergent clade-associated strains had enhanced expression of NADase and streptolysin O. The genome remodeling in the new clade variant and the resultant altered phenotype appear to have conferred a selective advantage over other emm89 variants and may explain the changes observed in emm89 GAS epidemiology.ImportanceSudden upsurges or epidemic waves are common features of group A streptococcal disease. Although the mechanisms behind such changes are largely unknown, they are often associated with an expansion of a single genotype within the population. Using whole-genome sequencing, we investigated a nationwide increase in invasive disease caused by the genotype emm89 in the United Kingdom. We identified a new clade variant that had recently emerged in the emm89 population after having undergone several core genomic recombination-related changes, two of which affected known virulence factors. An unusual finding of the new variant was the loss of the hyaluronic acid capsule, previously thought to be essential for causing invasive disease. A further genomic adaptation in the NADase/streptolysin O locus resulted in enhanced production of these toxins. Recombination-related genome remodeling is clearly an important mechanism in group A Streptococcus that can give rise to more successful and potentially more pathogenic variants.

Dataset Information

Rapid Emergence of a New Clone Impacts the Population at Risk and Increases the Incidence of Type emm89 Group A Streptococcus Invasive Disease.

Publications

Rapid Emergence of a New Clone Impacts the Population at Risk and Increases the Incidence of Type <i>emm89</i> Group A <i>Streptococcus</i> Invasive Disease.

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