Prevalence of the M1UK sublineage among emm1 Streptococcus pyogenes invasive strains isolated in the Czech Republic from December 2022 to May 2023

Česká verze

Authors: R. Veselá ¹ ; S. Vohrnová ^1,2 ; J. Kozáková ¹
Authors place of work: Státní zdravotní ústav, Centrum epidemiologie a mikrobiologie, Národní referenční laboratoř pro streptokokové nákazy ¹; 3. lékařská fakulta Univerzity Karlovy, Praha ²
Published in the journal: Epidemiol. Mikrobiol. Imunol. 73, 2024, č. 2, s. 76-83
Category: Původní práce
doi: https://doi.org/10.61568/emi/11-6306/20240424/137080

Summary

Aims: Since December 2022, an increase in invasive disease caused by Streptococcus pyogenes has been observed in the Czech Republic, with a shift in the clinical presentation and age of patients. Unlike in previous years, invasive disease is more common in children and adolescents under 18 years of age and in previously healthy middle-aged adults. An increase has been noticed in the number of S. pyogenes isolates from primarily sterile sites such as haemoculture, cerebrospinal fluid, pleural effusion fluid, joint fluid, and postmortem specimens. Routine emm gene typing revealed emm1 to be the predominant emm type of S. pyogenes. Between January 2023 and July 2023, 46% of all S. pyogenes isolates from invasive cases were assigned to the emm1 type. The globally spread M1UK sublineage is characterized by differences in the expression of seven genes, including the streptococcal pyrogenic toxin A (speA) gene, compared to historical emm1 iGAS strains. The aim of this study is to determine whether the more toxigenic M1UK sublineage is associated with the increase in invasive disease in the Czech Republic.

Methods: Whole genome sequencing of 41 S. pyogenes isolates from patients with invasive disease recovered in the Czech Republic in 2018 and 2019 and from December 2022 to May 2023 was performed using the MiSeq instrument (Illumina). Bioinformatics analysis was performed using freely available online tools the Bacterial and Viral Bioinformatics Resource Center.

Results: Based on whole genome sequencing data of 41 emm1 isolates of S. pyogenes from patients with invasive infectious disease recovered in 2018 and 2019 and from December 2022 to May 2023, the M1UK sublineage was found to be predominant from December 2022 to May 2023.

Conclusion: The reason for the spread of the M1UK sublineage in the Czech Republic late in 2022 and in the first half of 2023 is not entirely clear, but it may be related to reduced immunity due to limited GAS transmission during lockdowns, especially in children. Another factor that may have contributed to the high incidence of invasive infectious diseases is the seasonal circulation of respiratory viruses.

Keywords:

Phylogenetic analysis – whole genome sequencing – Streptococcus pyogenes – GAS – superantigen – outbreak iGAS

Zdroje

Thompson KM, Sterkel AK, McBride JA, et al. The Shock of Strep: Rapid Deaths Due to Group a Streptococcus. Acad Forensic Pathol. 2018;8(1):136–149. doi: 10.23907/2018.010.
Turner CE, Abbott J, Lamagni T, et al. Emergence of a New Highly Successful Acapsular Group A Streptococcus Clade of Genotype emm89 in the United Kingdom. mBio. 2015;6(4):e00622. doi: 10.1128/mBio.00622–15.

Imohl M, Fitzner Ch, Perniciaro S, et al. Epidemiology and distribution of 10 superantigens among invasive Streptococcus pyogenes disease in Germany from 2009 to 2014. Plos One. 2017;12(7):e0180757. doi: 10.1371/journal.pone.0180757.
Lintges M, Arlt S, Uciechowski P, et al. A new closed-tube multiplex real-time PCR to detect eleven superantigens of Streptococcus pyogenes identifies a strain without superantigen activity. Int J Med Microbiol., 2007;297(6):471–478. doi: 10.1016/j. ijmm.2007.03.015.
Nelson DC, Garbe J, Collin M. Cysteine proteinase SpeB from Streptococcus pyogenes – a potent modifier of immunologically important host and bacterial proteins. Biol Chem., 2011;392(12):1077–1088. doi: 10.1515/BC.2011.208.
Lynskey NN, Jauneikaite E, Li HK, et al. Emergence of dominant toxigenic M1T1 Streptococcus pyogenes clone during increased scarlet fever activity in England: a population-based molecular epidemiological study. Lancet Infect Dis. 2019;19(11):1209– 1218. doi: 10.1016/S1473-3099(19)30446-3.
Li HK, Zhi X, Vieira A, et al. Characterization of emergent toxigenic M1UK Streptococcus pyogenes and associated sublineages. Microb Genom., 2023;9(4):mgen000994. doi: 10.1099/mgen.0.000994.
Imöhl M, van der Linden M, Reinert RR, et al. Invasive group A streptococcal disease and association with varicella in Germany, 1996–2009. FEMS Immunol Med Microbiol., 2011;62(1):101–109. doi: 10.1111/j.1574-695X.2011.00788.x.
Rümke LW, de Gier B, Vestjens SMT, et al. Dominance of M1UK clade among Dutch M1 Streptococcus pyogenes. Lancet Infectious Diseases, 2020;20(5):539–540. doi: 10.1016/S14733099(20)30278-4.
Demczuk W, Martin I, Domingo FR, et al. Identification of Streptococcus pyogenes M1UK clone in Canada. Lancet Infectious Diseases, 2019;19(12):1284–1285. doi: 10.1016/S14733099(19)30622-X.
Vohrnová S, Veselá R, Kozáková J, et al. Zvýšený výskyt invazivních onemocnění vyvolaných Streptococcus pyogenes od prosince 2022 do srpna 2023 – výsledky emm typizace, MLST, testování citlivosti na antibiotika a celogenomové sekvenace. Zprávy CEM (SZÚ Praha). 2023;31(10):377–382.
Wick RR, Judd LM, Gorrie CL, et al. Unicycler: resolving bacteria genome assemblies from short and long sequencing reads. PloS Computational Biology. 2017;13(6):e1005595. doi: 10.1371/ journal.pcbi.1005595.
Olson RD, Assaf R, Brettin T, et al. Introducing the Bacterial and Viral Bioinformatics Resource Center (BV-BRC): a resource combining PATRIC, IRD and ViPR. Nucleic Acids Res. 2023;51(D1):D678–D689. doi: 10.1093/nar/gkac1003.
Jolley KA, Maiden MCJ. BIGSdb: Scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics, 2010;11(1). doi: 10.1186/1471-2105-11-595.
Sumby P, Porcella SF, Madrigal AG, et al. Evolutionary origin and emergence of a highly successful clone of serotype M1 group a Streptococcus involved multiple horizontal gene transfer events. J Infect Dis., 2005;192(5):771–782. doi: 10.1086/432514.
Li H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM, 2013 arXiv:1303.3997
Li H. Toward better understanding of artifacts in variant calling from high-coverage samples. Bioinformatics, 2014;30(20):2843– 2851. doi: 10.1093/bioinformatics/btu356.
Davis JJ, Gerdes S, Olsen GJ, et al. PATtyFams: Protein Families for the Microbial Genomes in the PATRIC Database. Front Microbiol., 2016;7:118. doi: 10.3389/fmicb.2016.00118.
Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 2014;30(9):1312–1313. doi: 10.1093/bioinformatics/btu033.
Li Y, Nanduri SA, Van Beneden CA, et al. M1UK lineage in invasive group A streptococcus isolates from the USA. Lancet Infect Dis., 2020;20(5):538–539. doi: 10.1016/S1473-3099(20)30279-6.
Veselá R, Vohrnová S, Kozáková J. Detekce superantigenů u izolátů Streptococcus pyogenes na základě dat celogenomové sekvenace. Epidemiol Mikrobiol Imunol, 2023; 72(3):191–194.
Cohen R, Ashman M, Taha MK, et al. Pediatric Infectious Disease Group (GPIP) position paper on the immune debt of the COVID-19 pandemic in childhood, how can we fill the immunity gap? Infect Dis Now., 2021;51(5):418–423. doi: 10.1016/j.idnow.2021.05.004.
Johannesen TB, Munkstrup C, Edslev SM, et al. Increase in invasive group A streptococcal infections and emergence of novel, rapidly expanding sub-lineage of the virulent Streptococcus pyogenes M1 clone, Denmark, 2023. Euro Surveill., 2023;28(26):2300291. doi: 10.2807/1560-7917.
Štefan M. Invazivní infekce způsobené Streptococcus pyogenes s protrahovaným průběhem a rekurencí. Olomouc: Kongres Klinické Mikrobiologie, Infekčních nemocí a Epidemiologie, 6. října 2023.
Heinige P, Prchlík M, Zaoral M, et al. Upozornění pracovní skupiny sekce intenzivní medicíny při České pediatrické společnosti na opakovaný výskyt velmi závažných invazivních infekcí pyogenními streptokoky v ČR. Čes-slov Pediat., 2023;78(5):281–282.
de Gier B, Vlaminckx BJM, Woudt SHSb, et al. Associations between common respiratory viruses and invasive group A streptococcal infection: A time-series analysis. Influenza Other Respir Viruses. 2019;13(5):453–458. doi: 10.1111/irv.12658.
Research and analysis. Group A streptococcal infections: report on seasonal aktivity in England, 2022 to 2023 [online]. Dostupné na www: https://www.gov.uk/government/publications/ group-a-streptococcal-infections-activity-during-the-2022-to2023-season/group-a-streptococcal-infections-second-updateon-seasonal-activity-in-england-2022-to-2023.
Blechová Z. Nárůst streptokokových infekcí u dětí včetně závažných manifestací [online]. 2023-05-20. Dostupné na www: https://infektologie.cz/zprava23-15.htm.
WHO. Mitigating Shortages of Antibiotics [online]. Dostupné na www: https://www.who.int/groups/mitigating-shortages-of- antibiotics.
Kreikemeyer B, Beckert S, Braun-Kiewnick A, et al. Group A streptococcal RofA-type global regulators exhibit a strainspecific genomic presence and regulation pattern. Microbiology (Reading), 2002;148(Pt 5):1501–1511. doi: 10.1099/00221287148-5-1501.
Beckert S, Kreikemeyer B, Podbielski A. Group A streptococcal rofA gene is involved in the control of several virulence genes and eukaryotic cell attachment and internalization. Infect Immun., 2001;69(1):534–537. doi: 10.1128/IAI.69.1.534537.2001.
Johannesen TB, Munkstrup C, Edslev SM, et al. Increase in invasive group A streptococcal infections and emergence of novel, rapidly expanding sub-lineage of the virulent Streptococcus pyogenes M1 clone, Denmark, 2023. Euro Surveill, 2023;28(26):2300291. doi: 10.2807/1560-7917. ES.2023.28.26.2300291.