Genomic Characterization of Skin and Soft Tissue Streptococcus pyogenes Isolates from a Low-Income and a High-Income Setting

Bah, Saikou Y.; Keeley, Alexander J; Armitage, Edwin P.; Khalid, Henna; Chaudhuri, Roy R.; Senghore, Elina; Manneh, Jarra; Tilley, Lisa; Marks, Michael; Darboe, Saffiatou; Sesay, Abdul Karim; Silva, Thushan I. de; Turner, Claire E.; Erhart, Annette; Smeesters, Pierre; Antonio, Martín; Jabang, Sona; Kampmann, Beate; Roca, Anna; Cox, Isatou Jagne; Tiencheu, Peggy-Estelle; Mackenzie, Grant

doi:10.1128/msphere.00469-22

Cited by 10 publications

(31 citation statements)

References 56 publications

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“…These isolates were confirmed to be the lineage of emm82 recently identified to have arisen through recombination and emm-switching of emm12 to emm82 [45,48]. (n=15) [28]; UK, 2009-18 (n=439) [31,38,39,42]; Denmark, 2018-23 (n=239) [14]; Portugal, 2022-23 (n=12) [16]; USA, 2015 (n=134) [45], 2016-17 (n=228) [46], and 2018-21 (n=2) [11];…”

Section: Emm12supporting

confidence: 56%

“…The presence of superantigen genes speA, speC, speG, speH, speI, speJ, speK, speL, speM, speK/M, speQ, speR, ssa , and smeZ and DNase genes sda1, sda2, sdn, spd1, spd3 , and spd4 were determined by BLAST (100% coverage, 80% identity) with representative gene sequences against assemblies, and a manual check where needed. For other genes ( covR/S , rocA , hasABC and the nga-ifs-slo locus with promoter region), sequences were extracted from the assembled genomes and compared to the reference genome, H293 (Genbank accession NZ_HG316453.1), as previously described [28]. Antimicrobial resistance (AMR) gene carriage was determined with ABRicate (https://github.com/tseemann/abricate) using the NCBI database [29].…”

Section: Methodsmentioning

confidence: 99%

“…Further comparison was made with previously published WGS data from Sheffield, consisting of 142 non-invasive skin and soft tissue isolates collected in 2019 [28], and national and international data from other published collections.…”

Section: Wgs Analysismentioning

confidence: 99%

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Molecular characterisation ofStreptococcus pyogenes(StrepA) non-invasive isolates during the 2022-23 UK upsurge

Hall,

Bah,

Khalid

et al. 2024

Preprint

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At the end of 2022 into early 2023 the UK Health Security Agency reported unusually high levels of scarlet fever and invasive disease caused by Streptococcus pyogenes (StrepA or group A Streptococcus). During this time, we collected and genome sequenced 341 non-invasive throat and skin S. pyogenes isolates identified during routine clinical diagnostic testing in Sheffield, a large UK city. We compared the data with that obtained from a similar collection of 165 isolates from 2016-17. Numbers of throat-associated isolates collected peaked in early December 2022, reflecting the national scarlet fever upsurge, while skin infections peaked later in December. The most common emm-types in 2022-23 were emm1 (28.7%), emm12 (24.9%), and emm22 (7.7%) in throat; and emm1 (22%), emm12 (10%), emm76 (18%), and emm49 (7%) in skin. Whilst all emm1 isolates were the M1UK lineage, comparison with 2016-17 revealed diverse lineages in other emm-types, including emm12, and emergent lineages within other types including a new acapsular emm75 lineage, demonstrating that the upsurge was not completely driven by a single genotype. Analysis of the capsule locus predicted only 51% of throat isolates would produce capsule compared to 78% of skin isolates. 90% of throat isolates were also predicted to have high NADase and Streptolysin O (SLO) expression, based on the promoter sequence, compared to only 56% of skin isolates. Our study has highlighted the value in analysis of non-invasive isolates to characterise tissue tropisms, as well as changing strain diversity and emerging genomic features which may have implications for spillover into invasive disease and future S. pyogenes upsurges.

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Section: Emm12supporting

confidence: 56%

Section: Methodsmentioning

confidence: 99%

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Molecular characterisation ofStreptococcus pyogenes(StrepA) non-invasive isolates during the 2022-23 UK upsurge

Hall,

Bah,

Khalid

et al. 2024

Preprint

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“…The lines connecting these two facets (geography and genomic lineage) indicate that although many lineages are globally dispersed, the Pacific and African geographical regions contain GAS lineages that are rarely observed in other locations. The contrasting population structure of GAS between diverse geographical settings is exemplified in preliminary findings from The Gambia 132 , Kenya 133 and remote Australia 17,134 where the circulating GAS lineages are largely evolutionarily distinct from those originating from high-income settings. One interpretation of these data is that the frequency of GAS lineages differs globally, in which there is maintenance of higher numbers of GAS genotypes from geographical regions where the disease burden is highest.…”

Section: Gas Epidemiology and Evolutionmentioning

confidence: 99%

Pathogenesis, epidemiology and control of Group A Streptococcus infection

et al. 2023

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Streptococcus pyogenes (Group A Streptococcus; GAS) is exquisitely adapted to the human host, resulting in asymptomatic infection, pharyngitis, pyoderma, scarlet fever or invasive diseases, with potential for triggering post-infection immune sequelae. GAS deploys a range of virulence determinants to allow colonization, dissemination within the host and transmission, disrupting both innate and adaptive immune responses to infection. Fluctuating global GAS epidemiology is characterized by the emergence of new GAS clones, often associated with the acquisition of new virulence or antimicrobial determinants that are better adapted to the infection niche or averting host immunity. The recent identification of clinical GAS isolates with reduced penicillin sensitivity and increasing macrolide resistance threatens both frontline and penicillin-adjunctive antibiotic treatment. The World Health Organization (WHO) has developed a GAS research and technology road Surface-bound virulence factors M protein. GAS is classified based on the sequence of the 5′ end of the gene encoding the M protein (emm). More than 220 emm genotypes have been identified 2 . The M protein is a dimeric coiled-coil fibrillar protein that extends from the bacterial cell wall 38 . It consists of a conserved Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author selfarchiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

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“…Wound swab cultures yielded S. aureus in 81% and S. pyogenes in 51% of cases. Scabies infechon (diagnosed clinically) was seen in 16% of children (95% CI [12][13][14][15][16][17][18][19][20] and was significantly associated with pyoderma [19]. Whole genome sequencing (WGS) of cultured samples demonstrated diverse emm-types [20].…”

Section: Introduc0onmentioning

confidence: 99%

Molecular methods enhance the detection of pyoderma-related Streptococcus pyogenes and emm-type distribution in children

Hall,

Armitage,

Senghore

et al. 2024

Preprint

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Background: Streptococcus pyogenes-related skin infections are increasingly implicated in the development of rheumatic heart disease (RHD) in lower-resourced settings, where they are often associated with scabies. The true prevalence of S. pyogenes-related pyoderma may be underestimated by bacterial culture. Methods: A multiplex qPCR for S. pyogenes, Staphylococcus aureus and Sarcoptes scabiei was applied to 250 pyoderma swabs from a cross-sectional study of children <5 years in The Gambia. Direct PCR-based emm-typing was used to supplement previous whole genome sequencing (WGS) of cultured isolates. Results: Pyoderma lesions with S. pyogenes increased from 51% (127/250) using culture to 80% (199/250) with qPCR. Compared to qPCR, the sensitivity of culture was 95.4% for S. pyogenes (95% CI 77.2-99.9) in samples with S. pyogenes alone (22/250, 9%), but 59.9% (95% CI 52.3-67.2) for samples with S. aureus co-infection (177/250, 71%). Direct PCR-based emm-typing was successful in 50% (46/92) of cases, identifying 27 emm-types, including six not identified by WGS (total 52 emm-types). Conclusions: Bacterial culture significantly underestimates the burden of S. pyogenes in pyoderma, particularly when co-infected with S. aureus. Molecular methods should be used to enhance the detection of S. pyogenes in surveillance studies and clinical trials of preventative measures in RHD-endemic settings.

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Genomic Characterization of Skin and Soft Tissue Streptococcus pyogenes Isolates from a Low-Income and a High-Income Setting

Cited by 10 publications

References 56 publications

Molecular characterisation ofStreptococcus pyogenes(StrepA) non-invasive isolates during the 2022-23 UK upsurge

Molecular characterisation ofStreptococcus pyogenes(StrepA) non-invasive isolates during the 2022-23 UK upsurge

Pathogenesis, epidemiology and control of Group A Streptococcus infection

Molecular methods enhance the detection of pyoderma-related Streptococcus pyogenes and emm-type distribution in children

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