Characterization of <i>Streptococcus pyogenes</i> Strains from Tonsillopharyngitis and Scarlet Fever Resurgence, 2023—FIRST Detection of M1<sub>UK</sub> in Bulgaria

Recently a resurgence of <i>Streptococcus pyogenes infections</i> has arisen, with concerns around the highly virulent M1<sub>UK</sub> lineage. Our aim was to characterize <i>S. pyogenes</i>, the immune responses it causes, and to determine the presence of the M1&...

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Main Authors: Emma Keuleyan, Theodor Todorov, Deyan Donchev, Ani Kevorkyan, Radoslava Vazharova, Alexander Kukov, Georgi Todorov, Boriana Georgieva, Iskra Altankova, Yordanka Uzunova
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Language:English
Published: MDPI AG 2025-01-01
Series:Microorganisms
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Online Access:https://www.mdpi.com/2076-2607/13/1/179
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author Emma Keuleyan
Theodor Todorov
Deyan Donchev
Ani Kevorkyan
Radoslava Vazharova
Alexander Kukov
Georgi Todorov
Boriana Georgieva
Iskra Altankova
Yordanka Uzunova
author_facet Emma Keuleyan
Theodor Todorov
Deyan Donchev
Ani Kevorkyan
Radoslava Vazharova
Alexander Kukov
Georgi Todorov
Boriana Georgieva
Iskra Altankova
Yordanka Uzunova
author_sort Emma Keuleyan
collection DOAJ
description Recently a resurgence of <i>Streptococcus pyogenes infections</i> has arisen, with concerns around the highly virulent M1<sub>UK</sub> lineage. Our aim was to characterize <i>S. pyogenes</i>, the immune responses it causes, and to determine the presence of the M1<sub>UK</sub> lineage in Sofia, Bulgaria. In our study, the infections were confirmed by culture testing or rapid antigen test. Identification was performed by MALDI-TOF and was followed up by antibiotic susceptibility testing (EUCAST). Virulence factors were identified using multiplex PCR and whole genome sequencing (WGS). Immune responses were measured through detection of serum complement levels, lymphocyte subsets, and cytokine profiling. Out of 82 children, 38 had scarlet fever and the rest had streptococcal pharyngitis. Strains were susceptible to penicillin (β-lactams), macrolides, clindamycin, tetracyclines, co-trimoxazole, fluoroquinolones, and linezolid. Superantigen profiles were identified: SpeA + SpeJ (45%), SpeC, and SpeI + SpeH (27.5% each). A novel Multilocus sequence typing (MLST) haplotype in the <i>mut</i>S gene (d90b) was found in four strains. The M1<sub>UK</sub> lineage was detected for the first time in Bulgaria. We observed an increase in complement fractions C3 and C4 and a decrease in T lymphocytes. A significant increase in the levels of IFN-γ, IL-6, and IL-10 with corresponding reduction in IL-17A were revealed. In conclusion, the studied <i>S. pyogenes</i> strains were characterized by their susceptibility to antibiotics and the predominance of SpeA superantigen; for the first time in Bulgaria the presence of M1<sub>UK</sub> and a novel SNP variation in the <i>mut</i>S gene (d90b) were found. A mixed pattern of pro- and anti-inflammatory immune responses in patients was observed.
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spelling doaj-art-19c5b82428ae4a98b544afb02422eb232025-01-24T13:42:56ZengMDPI AGMicroorganisms2076-26072025-01-0113117910.3390/microorganisms13010179Characterization of <i>Streptococcus pyogenes</i> Strains from Tonsillopharyngitis and Scarlet Fever Resurgence, 2023—FIRST Detection of M1<sub>UK</sub> in BulgariaEmma Keuleyan0Theodor Todorov1Deyan Donchev2Ani Kevorkyan3Radoslava Vazharova4Alexander Kukov5Georgi Todorov6Boriana Georgieva7Iskra Altankova8Yordanka Uzunova9Clinical Microbiology and Virology Laboratory, University Hospital “Lozenetz”, 1407 Sofia, BulgariaLaboratory of Medical Genetics and Molecular Biology, University Hospital “Lozenetz”, 1407 Sofia, BulgariaNational Reference Laboratory for Control and Monitoring of Antimicrobial Resistance, National Center for Infectious and Parasitic Diseases, 1504 Sofia, BulgariaDepartment of Epidemiology and Disaster Medicine, Faculty of Public Health, Medical University—Plovdiv, 4002 Plovdiv, BulgariaLaboratory of Medical Genetics and Molecular Biology, University Hospital “Lozenetz”, 1407 Sofia, BulgariaLaboratory of Clinical Immunology, University Hospital “Lozenetz”, 1407 Sofia, BulgariaClinical Microbiology and Virology Laboratory, University Hospital “Lozenetz”, 1407 Sofia, BulgariaClinic of Pediatrics, University Hospital “Lozenetz”, 1407 Sofia, BulgariaMedical Faculty, Sofia University “St. Kliment Ohridski”, 1407 Sofia, BulgariaMedical Faculty, Sofia University “St. Kliment Ohridski”, 1407 Sofia, BulgariaRecently a resurgence of <i>Streptococcus pyogenes infections</i> has arisen, with concerns around the highly virulent M1<sub>UK</sub> lineage. Our aim was to characterize <i>S. pyogenes</i>, the immune responses it causes, and to determine the presence of the M1<sub>UK</sub> lineage in Sofia, Bulgaria. In our study, the infections were confirmed by culture testing or rapid antigen test. Identification was performed by MALDI-TOF and was followed up by antibiotic susceptibility testing (EUCAST). Virulence factors were identified using multiplex PCR and whole genome sequencing (WGS). Immune responses were measured through detection of serum complement levels, lymphocyte subsets, and cytokine profiling. Out of 82 children, 38 had scarlet fever and the rest had streptococcal pharyngitis. Strains were susceptible to penicillin (β-lactams), macrolides, clindamycin, tetracyclines, co-trimoxazole, fluoroquinolones, and linezolid. Superantigen profiles were identified: SpeA + SpeJ (45%), SpeC, and SpeI + SpeH (27.5% each). A novel Multilocus sequence typing (MLST) haplotype in the <i>mut</i>S gene (d90b) was found in four strains. The M1<sub>UK</sub> lineage was detected for the first time in Bulgaria. We observed an increase in complement fractions C3 and C4 and a decrease in T lymphocytes. A significant increase in the levels of IFN-γ, IL-6, and IL-10 with corresponding reduction in IL-17A were revealed. In conclusion, the studied <i>S. pyogenes</i> strains were characterized by their susceptibility to antibiotics and the predominance of SpeA superantigen; for the first time in Bulgaria the presence of M1<sub>UK</sub> and a novel SNP variation in the <i>mut</i>S gene (d90b) were found. A mixed pattern of pro- and anti-inflammatory immune responses in patients was observed.https://www.mdpi.com/2076-2607/13/1/179<i>Streptococcus pyogenes</i>virulence factorsantibiotic susceptibilityM1<sub>UK</sub>tonsillopharyngitisscarlet fever
spellingShingle Emma Keuleyan
Theodor Todorov
Deyan Donchev
Ani Kevorkyan
Radoslava Vazharova
Alexander Kukov
Georgi Todorov
Boriana Georgieva
Iskra Altankova
Yordanka Uzunova
Characterization of <i>Streptococcus pyogenes</i> Strains from Tonsillopharyngitis and Scarlet Fever Resurgence, 2023—FIRST Detection of M1<sub>UK</sub> in Bulgaria
Microorganisms
<i>Streptococcus pyogenes</i>
virulence factors
antibiotic susceptibility
M1<sub>UK</sub>
tonsillopharyngitis
scarlet fever
title Characterization of <i>Streptococcus pyogenes</i> Strains from Tonsillopharyngitis and Scarlet Fever Resurgence, 2023—FIRST Detection of M1<sub>UK</sub> in Bulgaria
title_full Characterization of <i>Streptococcus pyogenes</i> Strains from Tonsillopharyngitis and Scarlet Fever Resurgence, 2023—FIRST Detection of M1<sub>UK</sub> in Bulgaria
title_fullStr Characterization of <i>Streptococcus pyogenes</i> Strains from Tonsillopharyngitis and Scarlet Fever Resurgence, 2023—FIRST Detection of M1<sub>UK</sub> in Bulgaria
title_full_unstemmed Characterization of <i>Streptococcus pyogenes</i> Strains from Tonsillopharyngitis and Scarlet Fever Resurgence, 2023—FIRST Detection of M1<sub>UK</sub> in Bulgaria
title_short Characterization of <i>Streptococcus pyogenes</i> Strains from Tonsillopharyngitis and Scarlet Fever Resurgence, 2023—FIRST Detection of M1<sub>UK</sub> in Bulgaria
title_sort characterization of i streptococcus pyogenes i strains from tonsillopharyngitis and scarlet fever resurgence 2023 first detection of m1 sub uk sub in bulgaria
topic <i>Streptococcus pyogenes</i>
virulence factors
antibiotic susceptibility
M1<sub>UK</sub>
tonsillopharyngitis
scarlet fever
url https://www.mdpi.com/2076-2607/13/1/179
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