Increase in invasive group A streptococcal infections in Milan, Italy: a genomic and clinical characterization
Group A Streptococcus (GAS) causes multiple clinical manifestations, including invasive (iGAS) or even life-threatening (severe-iGAS) infections. After the drop in cases during COVID-19 pandemic, in 2022 a sharp increase of GAS was reported globally. GAS strains collected in 09/2022-03/2023 in two u...
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| Veröffentlicht in: | Frontiers in microbiology Jg. 14; S. 1287522 |
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| Abstract | Group A Streptococcus (GAS) causes multiple clinical manifestations, including invasive (iGAS) or even life-threatening (severe-iGAS) infections. After the drop in cases during COVID-19 pandemic, in 2022 a sharp increase of GAS was reported globally.
GAS strains collected in 09/2022-03/2023 in two university hospitals in Milan, Italy were retrospectively analyzed. Clinical/epidemiological data were combined with whole-genome sequencing to: (i) define resistome/virulome, (ii) identify putative transmission chains, (iii) explore associations between
types and clinical severity.
Twenty-eight isolates were available, 19/28 (67.9%) from adults and 9/28 (32.1%) from pediatric population. The criteria for iGAS were met by 19/28 cases (67.9%), of which 11/19 (39.3%) met the further criteria for severe-iGAS. Pediatric cases were mainly non-invasive infections (8/9, 88.9%), adult cases were iGAS and severe-iGAS in 18/19 (94.7%) and 10/19 (52.6%), respectively. Thirteen
-types were detected, the most prevalent being
1 and
12 (6/28 strains each, 21.4%). Single nucleotide polymorphism (SNP) analysis of
1.0 and
12.0 strains revealed pairwise SNP distance always >10, inconsistent with unique transmission chains.
12.0-type, found to almost exclusively carry virulence factors
H and
I, was mainly detected in children and in no-iGAS infections (55.6 vs. 5.3%,
= 0.007 and 66.7 vs. 0.0%,
< 0.001, respectively), while
1.0-type was mainly detected in severe-iGAS (0.0 vs. 45.5%,
= 0.045).
This study showed that multiple
-types contributed to a 2022/2023 GAS infection increase in two hospitals in Milan, with no evidence of direct transmission chains. Specific
-types could be associated with disease severity or invasiveness. Overall, these results support the integration of classical epidemiological studies with genomic investigation to appropriately manage severe infections and improve surveillance. |
|---|---|
| AbstractList | Group A Streptococcus (GAS) causes multiple clinical manifestations, including invasive (iGAS) or even life-threatening (severe-iGAS) infections. After the drop in cases during COVID-19 pandemic, in 2022 a sharp increase of GAS was reported globally.BackgroundGroup A Streptococcus (GAS) causes multiple clinical manifestations, including invasive (iGAS) or even life-threatening (severe-iGAS) infections. After the drop in cases during COVID-19 pandemic, in 2022 a sharp increase of GAS was reported globally.GAS strains collected in 09/2022-03/2023 in two university hospitals in Milan, Italy were retrospectively analyzed. Clinical/epidemiological data were combined with whole-genome sequencing to: (i) define resistome/virulome, (ii) identify putative transmission chains, (iii) explore associations between emm-types and clinical severity.MethodsGAS strains collected in 09/2022-03/2023 in two university hospitals in Milan, Italy were retrospectively analyzed. Clinical/epidemiological data were combined with whole-genome sequencing to: (i) define resistome/virulome, (ii) identify putative transmission chains, (iii) explore associations between emm-types and clinical severity.Twenty-eight isolates were available, 19/28 (67.9%) from adults and 9/28 (32.1%) from pediatric population. The criteria for iGAS were met by 19/28 cases (67.9%), of which 11/19 (39.3%) met the further criteria for severe-iGAS. Pediatric cases were mainly non-invasive infections (8/9, 88.9%), adult cases were iGAS and severe-iGAS in 18/19 (94.7%) and 10/19 (52.6%), respectively. Thirteen emm-types were detected, the most prevalent being emm1 and emm12 (6/28 strains each, 21.4%). Single nucleotide polymorphism (SNP) analysis of emm1.0 and emm12.0 strains revealed pairwise SNP distance always >10, inconsistent with unique transmission chains. Emm12.0-type, found to almost exclusively carry virulence factors speH and speI, was mainly detected in children and in no-iGAS infections (55.6 vs. 5.3%, p = 0.007 and 66.7 vs. 0.0%, p < 0.001, respectively), while emm1.0-type was mainly detected in severe-iGAS (0.0 vs. 45.5%, p = 0.045).ResultsTwenty-eight isolates were available, 19/28 (67.9%) from adults and 9/28 (32.1%) from pediatric population. The criteria for iGAS were met by 19/28 cases (67.9%), of which 11/19 (39.3%) met the further criteria for severe-iGAS. Pediatric cases were mainly non-invasive infections (8/9, 88.9%), adult cases were iGAS and severe-iGAS in 18/19 (94.7%) and 10/19 (52.6%), respectively. Thirteen emm-types were detected, the most prevalent being emm1 and emm12 (6/28 strains each, 21.4%). Single nucleotide polymorphism (SNP) analysis of emm1.0 and emm12.0 strains revealed pairwise SNP distance always >10, inconsistent with unique transmission chains. Emm12.0-type, found to almost exclusively carry virulence factors speH and speI, was mainly detected in children and in no-iGAS infections (55.6 vs. 5.3%, p = 0.007 and 66.7 vs. 0.0%, p < 0.001, respectively), while emm1.0-type was mainly detected in severe-iGAS (0.0 vs. 45.5%, p = 0.045).This study showed that multiple emm-types contributed to a 2022/2023 GAS infection increase in two hospitals in Milan, with no evidence of direct transmission chains. Specific emm-types could be associated with disease severity or invasiveness. Overall, these results support the integration of classical epidemiological studies with genomic investigation to appropriately manage severe infections and improve surveillance.ConclusionsThis study showed that multiple emm-types contributed to a 2022/2023 GAS infection increase in two hospitals in Milan, with no evidence of direct transmission chains. Specific emm-types could be associated with disease severity or invasiveness. Overall, these results support the integration of classical epidemiological studies with genomic investigation to appropriately manage severe infections and improve surveillance. Group A Streptococcus (GAS) causes multiple clinical manifestations, including invasive (iGAS) or even life-threatening (severe-iGAS) infections. After the drop in cases during COVID-19 pandemic, in 2022 a sharp increase of GAS was reported globally. GAS strains collected in 09/2022-03/2023 in two university hospitals in Milan, Italy were retrospectively analyzed. Clinical/epidemiological data were combined with whole-genome sequencing to: (i) define resistome/virulome, (ii) identify putative transmission chains, (iii) explore associations between types and clinical severity. Twenty-eight isolates were available, 19/28 (67.9%) from adults and 9/28 (32.1%) from pediatric population. The criteria for iGAS were met by 19/28 cases (67.9%), of which 11/19 (39.3%) met the further criteria for severe-iGAS. Pediatric cases were mainly non-invasive infections (8/9, 88.9%), adult cases were iGAS and severe-iGAS in 18/19 (94.7%) and 10/19 (52.6%), respectively. Thirteen -types were detected, the most prevalent being 1 and 12 (6/28 strains each, 21.4%). Single nucleotide polymorphism (SNP) analysis of 1.0 and 12.0 strains revealed pairwise SNP distance always >10, inconsistent with unique transmission chains. 12.0-type, found to almost exclusively carry virulence factors H and I, was mainly detected in children and in no-iGAS infections (55.6 vs. 5.3%, = 0.007 and 66.7 vs. 0.0%, < 0.001, respectively), while 1.0-type was mainly detected in severe-iGAS (0.0 vs. 45.5%, = 0.045). This study showed that multiple -types contributed to a 2022/2023 GAS infection increase in two hospitals in Milan, with no evidence of direct transmission chains. Specific -types could be associated with disease severity or invasiveness. Overall, these results support the integration of classical epidemiological studies with genomic investigation to appropriately manage severe infections and improve surveillance. BackgroundGroup A Streptococcus (GAS) causes multiple clinical manifestations, including invasive (iGAS) or even life-threatening (severe-iGAS) infections. After the drop in cases during COVID-19 pandemic, in 2022 a sharp increase of GAS was reported globally.MethodsGAS strains collected in 09/2022–03/2023 in two university hospitals in Milan, Italy were retrospectively analyzed. Clinical/epidemiological data were combined with whole-genome sequencing to: (i) define resistome/virulome, (ii) identify putative transmission chains, (iii) explore associations between emm-types and clinical severity.ResultsTwenty-eight isolates were available, 19/28 (67.9%) from adults and 9/28 (32.1%) from pediatric population. The criteria for iGAS were met by 19/28 cases (67.9%), of which 11/19 (39.3%) met the further criteria for severe-iGAS. Pediatric cases were mainly non-invasive infections (8/9, 88.9%), adult cases were iGAS and severe-iGAS in 18/19 (94.7%) and 10/19 (52.6%), respectively. Thirteen emm-types were detected, the most prevalent being emm1 and emm12 (6/28 strains each, 21.4%). Single nucleotide polymorphism (SNP) analysis of emm1.0 and emm12.0 strains revealed pairwise SNP distance always >10, inconsistent with unique transmission chains. Emm12.0-type, found to almost exclusively carry virulence factors speH and speI, was mainly detected in children and in no-iGAS infections (55.6 vs. 5.3%, p = 0.007 and 66.7 vs. 0.0%, p < 0.001, respectively), while emm1.0-type was mainly detected in severe-iGAS (0.0 vs. 45.5%, p = 0.045).ConclusionsThis study showed that multiple emm-types contributed to a 2022/2023 GAS infection increase in two hospitals in Milan, with no evidence of direct transmission chains. Specific emm-types could be associated with disease severity or invasiveness. Overall, these results support the integration of classical epidemiological studies with genomic investigation to appropriately manage severe infections and improve surveillance. |
| Author | Bussini, Linda Teri, Antonio Carella, Francesco Muscatello, Antonio Bartoletti, Michele Carloni, Sara Bandera, Alessandra Lombardi, Andrea Cariani, Lisa Comelli, Agnese Alteri, Claudia Fox, Valeria Mangioni, Davide Saltini, Paola Cento, Valeria Matinato, Caterina Terranova, Leonardo |
| AuthorAffiliation | 1 Infectious Diseases Unit, Foundation Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) Ca' Granda Ospedale Maggiore Policlinico , Milan , Italy 8 Microbiology and Virology, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) Humanitas Research Hospital , Milan , Italy 6 Microbiology Laboratory, Clinical Pathology, Foundation Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) Ca' Granda Ospedale Maggiore Policlinico , Milan , Italy 2 Department of Pathophysiology and Transplantation, University of Milano , Milan , Italy 9 Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) Humanitas Research Hospital , Rozzano , Italy 4 Infectious Disease Unit, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) Humanitas Research Hospital , Milan , Italy 3 Department of Oncology and Hemato-Oncology, University of Milan , Milan , Italy 5 Department of Biomedical Sciences, Humanitas University , Milan , Italy 7 Respiratory Unit and Adult Cystic Fibrosis Center, Depart |
| AuthorAffiliation_xml | – name: 4 Infectious Disease Unit, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) Humanitas Research Hospital , Milan , Italy – name: 1 Infectious Diseases Unit, Foundation Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) Ca' Granda Ospedale Maggiore Policlinico , Milan , Italy – name: 7 Respiratory Unit and Adult Cystic Fibrosis Center, Department of Internal Medicine, Foundation Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) Cà Granda Ospedale Maggiore Policlinico , Milan , Italy – name: 8 Microbiology and Virology, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) Humanitas Research Hospital , Milan , Italy – name: 6 Microbiology Laboratory, Clinical Pathology, Foundation Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) Ca' Granda Ospedale Maggiore Policlinico , Milan , Italy – name: 9 Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) Humanitas Research Hospital , Rozzano , Italy – name: 3 Department of Oncology and Hemato-Oncology, University of Milan , Milan , Italy – name: 2 Department of Pathophysiology and Transplantation, University of Milano , Milan , Italy – name: 5 Department of Biomedical Sciences, Humanitas University , Milan , Italy |
| Author_xml | – sequence: 1 givenname: Davide surname: Mangioni fullname: Mangioni, Davide – sequence: 2 givenname: Valeria surname: Fox fullname: Fox, Valeria – sequence: 3 givenname: Paola surname: Saltini fullname: Saltini, Paola – sequence: 4 givenname: Andrea surname: Lombardi fullname: Lombardi, Andrea – sequence: 5 givenname: Linda surname: Bussini fullname: Bussini, Linda – sequence: 6 givenname: Francesco surname: Carella fullname: Carella, Francesco – sequence: 7 givenname: Lisa surname: Cariani fullname: Cariani, Lisa – sequence: 8 givenname: Agnese surname: Comelli fullname: Comelli, Agnese – sequence: 9 givenname: Caterina surname: Matinato fullname: Matinato, Caterina – sequence: 10 givenname: Antonio surname: Muscatello fullname: Muscatello, Antonio – sequence: 11 givenname: Antonio surname: Teri fullname: Teri, Antonio – sequence: 12 givenname: Leonardo surname: Terranova fullname: Terranova, Leonardo – sequence: 13 givenname: Valeria surname: Cento fullname: Cento, Valeria – sequence: 14 givenname: Sara surname: Carloni fullname: Carloni, Sara – sequence: 15 givenname: Michele surname: Bartoletti fullname: Bartoletti, Michele – sequence: 16 givenname: Claudia surname: Alteri fullname: Alteri, Claudia – sequence: 17 givenname: Alessandra surname: Bandera fullname: Bandera, Alessandra |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/38274761$$D View this record in MEDLINE/PubMed |
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| Copyright | Copyright © 2024 Mangioni, Fox, Saltini, Lombardi, Bussini, Carella, Cariani, Comelli, Matinato, Muscatello, Teri, Terranova, Cento, Carloni, Bartoletti, Alteri and Bandera. Copyright © 2024 Mangioni, Fox, Saltini, Lombardi, Bussini, Carella, Cariani, Comelli, Matinato, Muscatello, Teri, Terranova, Cento, Carloni, Bartoletti, Alteri and Bandera. 2024 Mangioni, Fox, Saltini, Lombardi, Bussini, Carella, Cariani, Comelli, Matinato, Muscatello, Teri, Terranova, Cento, Carloni, Bartoletti, Alteri and Bandera |
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| Keywords | GAS Streptococcus pyogenes WGS virulence factors necrotizing fasciitis genomic surveillance |
| Language | English |
| License | Copyright © 2024 Mangioni, Fox, Saltini, Lombardi, Bussini, Carella, Cariani, Comelli, Matinato, Muscatello, Teri, Terranova, Cento, Carloni, Bartoletti, Alteri and Bandera. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Edited by: Thomas Proft, The University of Auckland, New Zealand Mark Davies, The University of Melbourne, Australia Stephen B. Beres, Houston Methodist Research Institute, United States These authors have contributed equally to this work and share first authorship Reviewed by: Luke Blagdon Snell, King's College London, United Kingdom |
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| Title | Increase in invasive group A streptococcal infections in Milan, Italy: a genomic and clinical characterization |
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