A prospective survey of Streptococcus pyogenes infections in French Brittany from 2009 to 2017: Comprehensive dynamic of new emergent emm genotypes
Streptococcus pyogenes or group A Streptococcus (GAS) causes diseases ranging from uncomplicated pharyngitis to life-threatening infections. It has complex epidemiology driven by the diversity, the temporal and geographical fluctuations of the circulating strains. Despite the global burden of GAS di...
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| description | Streptococcus pyogenes or group A Streptococcus (GAS) causes diseases ranging from uncomplicated pharyngitis to life-threatening infections. It has complex epidemiology driven by the diversity, the temporal and geographical fluctuations of the circulating strains. Despite the global burden of GAS diseases, there is currently no available vaccination strategy against GAS infections. This study, based on a longitudinal population survey, aimed to understand the dynamic of GAS emm types and to give leads to better recognition of underlying mechanisms for the emergence of successful clones. From 2009 to 2017, we conducted a systematic culture-based diagnosis of GAS infections in a French Brittany population with a prospective recovery of clinical data. The epidemiological analysis was performed using emm typing combined with the structural and functional cluster-typing system for all the recovered strains. Risk factors for the invasiveness, identified by univariate analysis, were computed in a multiple logistic regression analysis, and the only independent risk factor remaining in the model was the age (OR for the entire range [CI95%] = 6.35 [3.63, 11.10]; p |
| doi_str_mv | 10.1371/journal.pone.0244063 |
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It has complex epidemiology driven by the diversity, the temporal and geographical fluctuations of the circulating strains. Despite the global burden of GAS diseases, there is currently no available vaccination strategy against GAS infections. This study, based on a longitudinal population survey, aimed to understand the dynamic of GAS emm types and to give leads to better recognition of underlying mechanisms for the emergence of successful clones. From 2009 to 2017, we conducted a systematic culture-based diagnosis of GAS infections in a French Brittany population with a prospective recovery of clinical data. The epidemiological analysis was performed using emm typing combined with the structural and functional cluster-typing system for all the recovered strains. Risk factors for the invasiveness, identified by univariate analysis, were computed in a multiple logistic regression analysis, and the only independent risk factor remaining in the model was the age (OR for the entire range [CI95%] = 6.35 [3.63, 11.10]; p<0.0001). Among the 61 different emm types identified, the most prevalent were emm28 (16%), emm89 (15%), emm1 (14%), and emm4 (8%), which accounted for more than 50% of circulating strains. During the study period, five genotypes identified as emm44, 66, 75, 83, 87 emerged successively and belonged to clusters D4, E2, E3, and E6 that were different from those gathering "Prevalent" emm types (clusters A-C3 to 5, E1 and E4). We previously reported significant genetic modifications for emm44, 66, 83 and 75 types resulting possibly from a short adaptive evolution. Herein we additionally observed that the emergence of a new genotype could occur in a susceptible population having specific risk factors or probably lacking a naturally-acquired cluster-specific immune cross-protection. Among emergent emm types, emm75 and emm87 tend to become prevalent with a stable annual incidence and the risk of a clonal expansion have to be considered.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0244063</identifier><identifier>PMID: 33332468</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adolescent ; Adult ; Aged ; Aged, 80 and over ; Biology and Life Sciences ; Child ; Child, Preschool ; Clusters ; Cross-protection ; Data recovery ; Disease control ; Distribution ; Epidemiology ; Female ; France - epidemiology ; Genetic aspects ; Genetic variation ; Genotype ; Genotypes ; Health aspects ; Health risks ; Hospitals ; Humans ; Identification and classification ; Immunology ; Infant ; Infant, Newborn ; Infections ; Invasiveness ; Life Sciences ; Male ; Medicine and Health Sciences ; Middle Aged ; Pharyngitis ; Polls & surveys ; Population ; Prospective Studies ; Proteins ; Regions ; Regression analysis ; Risk analysis ; Risk factors ; Statistics ; Strains (organisms) ; Streptococcal infections ; Streptococcal Infections - epidemiology ; Streptococcal Infections - genetics ; Streptococcal Infections - metabolism ; Streptococcus infections ; Streptococcus pyogenes ; Streptococcus pyogenes - genetics ; Streptococcus pyogenes - isolation & purification ; Streptococcus pyogenes - metabolism ; Structure-function relationships ; Vaccination</subject><ispartof>PloS one, 2020-12, Vol.15 (12), p.e0244063-e0244063</ispartof><rights>COPYRIGHT 2020 Public Library of Science</rights><rights>2020 Boukthir et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>2020 Boukthir et al 2020 Boukthir et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c792t-9624dcdeb408728900b73e74c12c4753aeb8d48b59b3440bcf63665cebcb0d83</citedby><cites>FETCH-LOGICAL-c792t-9624dcdeb408728900b73e74c12c4753aeb8d48b59b3440bcf63665cebcb0d83</cites><orcidid>0000-0002-4734-1713</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7746304/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7746304/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2095,2914,23846,27903,27904,53769,53771,79346,79347</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33332468$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-03102045$$DView record in HAL$$Hfree_for_read</backlink></links><search><contributor>Melo-Cristino, Jose</contributor><creatorcontrib>Boukthir, Sarrah</creatorcontrib><creatorcontrib>Moullec, Séverine</creatorcontrib><creatorcontrib>Cariou, Marie-Estelle</creatorcontrib><creatorcontrib>Meygret, Alexandra</creatorcontrib><creatorcontrib>Morcet, Jeff</creatorcontrib><creatorcontrib>Faili, Ahmad</creatorcontrib><creatorcontrib>Kayal, Samer</creatorcontrib><title>A prospective survey of Streptococcus pyogenes infections in French Brittany from 2009 to 2017: Comprehensive dynamic of new emergent emm genotypes</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Streptococcus pyogenes or group A Streptococcus (GAS) causes diseases ranging from uncomplicated pharyngitis to life-threatening infections. It has complex epidemiology driven by the diversity, the temporal and geographical fluctuations of the circulating strains. Despite the global burden of GAS diseases, there is currently no available vaccination strategy against GAS infections. This study, based on a longitudinal population survey, aimed to understand the dynamic of GAS emm types and to give leads to better recognition of underlying mechanisms for the emergence of successful clones. From 2009 to 2017, we conducted a systematic culture-based diagnosis of GAS infections in a French Brittany population with a prospective recovery of clinical data. The epidemiological analysis was performed using emm typing combined with the structural and functional cluster-typing system for all the recovered strains. Risk factors for the invasiveness, identified by univariate analysis, were computed in a multiple logistic regression analysis, and the only independent risk factor remaining in the model was the age (OR for the entire range [CI95%] = 6.35 [3.63, 11.10]; p<0.0001). Among the 61 different emm types identified, the most prevalent were emm28 (16%), emm89 (15%), emm1 (14%), and emm4 (8%), which accounted for more than 50% of circulating strains. During the study period, five genotypes identified as emm44, 66, 75, 83, 87 emerged successively and belonged to clusters D4, E2, E3, and E6 that were different from those gathering "Prevalent" emm types (clusters A-C3 to 5, E1 and E4). We previously reported significant genetic modifications for emm44, 66, 83 and 75 types resulting possibly from a short adaptive evolution. Herein we additionally observed that the emergence of a new genotype could occur in a susceptible population having specific risk factors or probably lacking a naturally-acquired cluster-specific immune cross-protection. Among emergent emm types, emm75 and emm87 tend to become prevalent with a stable annual incidence and the risk of a clonal expansion have to be considered.</description><subject>Adolescent</subject><subject>Adult</subject><subject>Aged</subject><subject>Aged, 80 and over</subject><subject>Biology and Life Sciences</subject><subject>Child</subject><subject>Child, Preschool</subject><subject>Clusters</subject><subject>Cross-protection</subject><subject>Data recovery</subject><subject>Disease control</subject><subject>Distribution</subject><subject>Epidemiology</subject><subject>Female</subject><subject>France - epidemiology</subject><subject>Genetic aspects</subject><subject>Genetic variation</subject><subject>Genotype</subject><subject>Genotypes</subject><subject>Health aspects</subject><subject>Health risks</subject><subject>Hospitals</subject><subject>Humans</subject><subject>Identification and classification</subject><subject>Immunology</subject><subject>Infant</subject><subject>Infant, Newborn</subject><subject>Infections</subject><subject>Invasiveness</subject><subject>Life Sciences</subject><subject>Male</subject><subject>Medicine and Health Sciences</subject><subject>Middle Aged</subject><subject>Pharyngitis</subject><subject>Polls & surveys</subject><subject>Population</subject><subject>Prospective Studies</subject><subject>Proteins</subject><subject>Regions</subject><subject>Regression analysis</subject><subject>Risk analysis</subject><subject>Risk factors</subject><subject>Statistics</subject><subject>Strains (organisms)</subject><subject>Streptococcal infections</subject><subject>Streptococcal Infections - epidemiology</subject><subject>Streptococcal Infections - genetics</subject><subject>Streptococcal Infections - metabolism</subject><subject>Streptococcus infections</subject><subject>Streptococcus pyogenes</subject><subject>Streptococcus pyogenes - genetics</subject><subject>Streptococcus pyogenes - isolation & purification</subject><subject>Streptococcus pyogenes - metabolism</subject><subject>Structure-function relationships</subject><subject>Vaccination</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNk1Fv0zAQxyMEYmPwDRBYQkLsocWxXTvhAalUjFWqNIlNvFqOc2kzJXFmO4V8Dr4wTttNzbQHkgefLr_7X-58F0VvYzyNqYg_35rONqqatqaBKSaMYU6fRadxSsmEE0yfH9kn0SvnbjGe0YTzl9EJDQ9hPDmN_s5Ra41rQftyC8h1dgs9MgW69hZab7TRunOo7c0aGnCobIoBNc1gogsLjd6gb7b0XjU9KqypEcE4Rd6EMxZf0MLUrYUNNG7Qz_tG1aUeEjTwG0ENNuj6YNQoGMb3LbjX0YtCVQ7eHM6z6Obi-83icrK6-rFczFcTLVLiJyknLNc5ZAwngiQpxpmgIJiOiWZiRhVkSc6SbJZmNHQn0wWnnM80ZDrDeULPovd72bYyTh7a6SRhAqdYcIEDsdwTuVG3srVlrWwvjSrlzmHsWirrS12BLGhOcxLuReeUZSxTUHBgnCQFUSmwLGh9PWTrshpyHaq2qhqJjr805UauzVYKwTjFLAic7wU2j8Iu5ys5-DCNMcFsto0D--mQzJq7DpyXdek0VJVqwHS7GmM2S1MydOHDI_TpThyotQrFhiEw4R_1ICrnnIWxIiIetKZPUOHNIVx6mNOiDP5RwPkoIDAe_vi16pyTy-uf_89e_RqzH4_YDajKb5yput3gjkG2B3VYAmeheOhsjOWwZvfdkMOaycOahbB3x5f5EHS_V_QfqHEi7w</recordid><startdate>20201217</startdate><enddate>20201217</enddate><creator>Boukthir, Sarrah</creator><creator>Moullec, Séverine</creator><creator>Cariou, Marie-Estelle</creator><creator>Meygret, Alexandra</creator><creator>Morcet, Jeff</creator><creator>Faili, Ahmad</creator><creator>Kayal, Samer</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>1XC</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-4734-1713</orcidid></search><sort><creationdate>20201217</creationdate><title>A prospective survey of Streptococcus pyogenes infections in French Brittany from 2009 to 2017: Comprehensive dynamic of new emergent emm genotypes</title><author>Boukthir, Sarrah ; Moullec, Séverine ; Cariou, Marie-Estelle ; Meygret, Alexandra ; Morcet, Jeff ; Faili, Ahmad ; Kayal, Samer</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c792t-9624dcdeb408728900b73e74c12c4753aeb8d48b59b3440bcf63665cebcb0d83</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Adolescent</topic><topic>Adult</topic><topic>Aged</topic><topic>Aged, 80 and over</topic><topic>Biology and Life Sciences</topic><topic>Child</topic><topic>Child, Preschool</topic><topic>Clusters</topic><topic>Cross-protection</topic><topic>Data recovery</topic><topic>Disease control</topic><topic>Distribution</topic><topic>Epidemiology</topic><topic>Female</topic><topic>France - epidemiology</topic><topic>Genetic aspects</topic><topic>Genetic variation</topic><topic>Genotype</topic><topic>Genotypes</topic><topic>Health aspects</topic><topic>Health risks</topic><topic>Hospitals</topic><topic>Humans</topic><topic>Identification and classification</topic><topic>Immunology</topic><topic>Infant</topic><topic>Infant, Newborn</topic><topic>Infections</topic><topic>Invasiveness</topic><topic>Life Sciences</topic><topic>Male</topic><topic>Medicine and Health Sciences</topic><topic>Middle Aged</topic><topic>Pharyngitis</topic><topic>Polls & surveys</topic><topic>Population</topic><topic>Prospective Studies</topic><topic>Proteins</topic><topic>Regions</topic><topic>Regression analysis</topic><topic>Risk analysis</topic><topic>Risk factors</topic><topic>Statistics</topic><topic>Strains (organisms)</topic><topic>Streptococcal infections</topic><topic>Streptococcal Infections - epidemiology</topic><topic>Streptococcal Infections - genetics</topic><topic>Streptococcal Infections - 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Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Boukthir, Sarrah</au><au>Moullec, Séverine</au><au>Cariou, Marie-Estelle</au><au>Meygret, Alexandra</au><au>Morcet, Jeff</au><au>Faili, Ahmad</au><au>Kayal, Samer</au><au>Melo-Cristino, Jose</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A prospective survey of Streptococcus pyogenes infections in French Brittany from 2009 to 2017: Comprehensive dynamic of new emergent emm genotypes</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2020-12-17</date><risdate>2020</risdate><volume>15</volume><issue>12</issue><spage>e0244063</spage><epage>e0244063</epage><pages>e0244063-e0244063</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Streptococcus pyogenes or group A Streptococcus (GAS) causes diseases ranging from uncomplicated pharyngitis to life-threatening infections. It has complex epidemiology driven by the diversity, the temporal and geographical fluctuations of the circulating strains. Despite the global burden of GAS diseases, there is currently no available vaccination strategy against GAS infections. This study, based on a longitudinal population survey, aimed to understand the dynamic of GAS emm types and to give leads to better recognition of underlying mechanisms for the emergence of successful clones. From 2009 to 2017, we conducted a systematic culture-based diagnosis of GAS infections in a French Brittany population with a prospective recovery of clinical data. The epidemiological analysis was performed using emm typing combined with the structural and functional cluster-typing system for all the recovered strains. Risk factors for the invasiveness, identified by univariate analysis, were computed in a multiple logistic regression analysis, and the only independent risk factor remaining in the model was the age (OR for the entire range [CI95%] = 6.35 [3.63, 11.10]; p<0.0001). Among the 61 different emm types identified, the most prevalent were emm28 (16%), emm89 (15%), emm1 (14%), and emm4 (8%), which accounted for more than 50% of circulating strains. During the study period, five genotypes identified as emm44, 66, 75, 83, 87 emerged successively and belonged to clusters D4, E2, E3, and E6 that were different from those gathering "Prevalent" emm types (clusters A-C3 to 5, E1 and E4). We previously reported significant genetic modifications for emm44, 66, 83 and 75 types resulting possibly from a short adaptive evolution. Herein we additionally observed that the emergence of a new genotype could occur in a susceptible population having specific risk factors or probably lacking a naturally-acquired cluster-specific immune cross-protection. Among emergent emm types, emm75 and emm87 tend to become prevalent with a stable annual incidence and the risk of a clonal expansion have to be considered.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>33332468</pmid><doi>10.1371/journal.pone.0244063</doi><tpages>e0244063</tpages><orcidid>https://orcid.org/0000-0002-4734-1713</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2020-12, Vol.15 (12), p.e0244063-e0244063 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_2470907670 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Public Library of Science (PLoS); PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Adolescent Adult Aged Aged, 80 and over Biology and Life Sciences Child Child, Preschool Clusters Cross-protection Data recovery Disease control Distribution Epidemiology Female France - epidemiology Genetic aspects Genetic variation Genotype Genotypes Health aspects Health risks Hospitals Humans Identification and classification Immunology Infant Infant, Newborn Infections Invasiveness Life Sciences Male Medicine and Health Sciences Middle Aged Pharyngitis Polls & surveys Population Prospective Studies Proteins Regions Regression analysis Risk analysis Risk factors Statistics Strains (organisms) Streptococcal infections Streptococcal Infections - epidemiology Streptococcal Infections - genetics Streptococcal Infections - metabolism Streptococcus infections Streptococcus pyogenes Streptococcus pyogenes - genetics Streptococcus pyogenes - isolation & purification Streptococcus pyogenes - metabolism Structure-function relationships Vaccination |
| title | A prospective survey of Streptococcus pyogenes infections in French Brittany from 2009 to 2017: Comprehensive dynamic of new emergent emm genotypes |
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