Using Neisseria meningitidis genomic diversity to inform outbreak strain identification
Meningococcal disease is a life-threatening illness caused by the human-restricted bacterium Neisseria meningitidis . Outbreaks in the USA involve at least two cases in an organization or community caused by the same serogroup within three months. Genome comparisons, including phylogenetic analysis...
Saved in:
| Published in | PLoS pathogens Vol. 17; no. 5; p. e1009586 |
|---|---|
| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
18.05.2021
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
Cover
Loading…
| Abstract | Meningococcal disease is a life-threatening illness caused by the human-restricted bacterium
Neisseria meningitidis
. Outbreaks in the USA involve at least two cases in an organization or community caused by the same serogroup within three months. Genome comparisons, including phylogenetic analysis and quantification of genome distances can provide confirmatory evidence of pathogen transmission during an outbreak. Interpreting genome distances depends on understanding their distribution both among isolates from outbreaks and among those not from outbreaks. Here, we identify outbreak strains based on phylogenetic relationships among 141
N
.
meningitidis
isolates collected from 28 outbreaks in the USA during 2010–2017 and 1516 non-outbreak isolates collected through contemporaneous meningococcal surveillance. We show that genome distance thresholds based on the maximum SNPs and allele distances among isolates in the phylogenetically defined outbreak strains are sufficient to separate most pairs of non-outbreak isolates into separate strains. Non-outbreak isolate pairs that could not be distinguished from each other based on genetic distances were concentrated in the clonal complexes CC11, CC103, and CC32. Within each of these clonal complexes, phylodynamic analysis identified a group of isolates with extremely low diversity, collected over several years and multiple states. Clusters of isolates with low genetic diversity could indicate increased pathogen transmission, potentially resulting in local outbreaks or nationwide clonal expansions. |
|---|---|
| AbstractList | Meningococcal disease is a life-threatening illness caused by the human-restricted bacterium
Neisseria meningitidis
. Outbreaks in the USA involve at least two cases in an organization or community caused by the same serogroup within three months. Genome comparisons, including phylogenetic analysis and quantification of genome distances can provide confirmatory evidence of pathogen transmission during an outbreak. Interpreting genome distances depends on understanding their distribution both among isolates from outbreaks and among those not from outbreaks. Here, we identify outbreak strains based on phylogenetic relationships among 141
N
.
meningitidis
isolates collected from 28 outbreaks in the USA during 2010–2017 and 1516 non-outbreak isolates collected through contemporaneous meningococcal surveillance. We show that genome distance thresholds based on the maximum SNPs and allele distances among isolates in the phylogenetically defined outbreak strains are sufficient to separate most pairs of non-outbreak isolates into separate strains. Non-outbreak isolate pairs that could not be distinguished from each other based on genetic distances were concentrated in the clonal complexes CC11, CC103, and CC32. Within each of these clonal complexes, phylodynamic analysis identified a group of isolates with extremely low diversity, collected over several years and multiple states. Clusters of isolates with low genetic diversity could indicate increased pathogen transmission, potentially resulting in local outbreaks or nationwide clonal expansions. Meningococcal disease is a life-threatening illness caused by the human-restricted bacterium Neisseria meningitidis. Outbreaks in the USA involve at least two cases in an organization or community caused by the same serogroup within three months. Genome comparisons, including phylogenetic analysis and quantification of genome distances can provide confirmatory evidence of pathogen transmission during an outbreak. Interpreting genome distances depends on understanding their distribution both among isolates from outbreaks and among those not from outbreaks. Here, we identify outbreak strains based on phylogenetic relationships among 141 N. meningitidis isolates collected from 28 outbreaks in the USA during 2010-2017 and 1516 non-outbreak isolates collected through contemporaneous meningococcal surveillance. We show that genome distance thresholds based on the maximum SNPs and allele distances among isolates in the phylogenetically defined outbreak strains are sufficient to separate most pairs of non-outbreak isolates into separate strains. Non-outbreak isolate pairs that could not be distinguished from each other based on genetic distances were concentrated in the clonal complexes CC11, CC103, and CC32. Within each of these clonal complexes, phylodynamic analysis identified a group of isolates with extremely low diversity, collected over several years and multiple states. Clusters of isolates with low genetic diversity could indicate increased pathogen transmission, potentially resulting in local outbreaks or nationwide clonal expansions. Meningococcal disease is a life-threatening illness caused by the human-restricted bacterium Neisseria meningitidis. Outbreaks in the USA involve at least two cases in an organization or community caused by the same serogroup within three months. Genome comparisons, including phylogenetic analysis and quantification of genome distances can provide confirmatory evidence of pathogen transmission during an outbreak. Interpreting genome distances depends on understanding their distribution both among isolates from outbreaks and among those not from outbreaks. Here, we identify outbreak strains based on phylogenetic relationships among 141 N. meningitidis isolates collected from 28 outbreaks in the USA during 2010-2017 and 1516 non-outbreak isolates collected through contemporaneous meningococcal surveillance. We show that genome distance thresholds based on the maximum SNPs and allele distances among isolates in the phylogenetically defined outbreak strains are sufficient to separate most pairs of non-outbreak isolates into separate strains. Non-outbreak isolate pairs that could not be distinguished from each other based on genetic distances were concentrated in the clonal complexes CC11, CC103, and CC32. Within each of these clonal complexes, phylodynamic analysis identified a group of isolates with extremely low diversity, collected over several years and multiple states. Clusters of isolates with low genetic diversity could indicate increased pathogen transmission, potentially resulting in local outbreaks or nationwide clonal expansions.Meningococcal disease is a life-threatening illness caused by the human-restricted bacterium Neisseria meningitidis. Outbreaks in the USA involve at least two cases in an organization or community caused by the same serogroup within three months. Genome comparisons, including phylogenetic analysis and quantification of genome distances can provide confirmatory evidence of pathogen transmission during an outbreak. Interpreting genome distances depends on understanding their distribution both among isolates from outbreaks and among those not from outbreaks. Here, we identify outbreak strains based on phylogenetic relationships among 141 N. meningitidis isolates collected from 28 outbreaks in the USA during 2010-2017 and 1516 non-outbreak isolates collected through contemporaneous meningococcal surveillance. We show that genome distance thresholds based on the maximum SNPs and allele distances among isolates in the phylogenetically defined outbreak strains are sufficient to separate most pairs of non-outbreak isolates into separate strains. Non-outbreak isolate pairs that could not be distinguished from each other based on genetic distances were concentrated in the clonal complexes CC11, CC103, and CC32. Within each of these clonal complexes, phylodynamic analysis identified a group of isolates with extremely low diversity, collected over several years and multiple states. Clusters of isolates with low genetic diversity could indicate increased pathogen transmission, potentially resulting in local outbreaks or nationwide clonal expansions. Meningococcal disease is a life-threatening illness caused by the human-restricted bacterium Neisseria meningitidis . Outbreaks in the USA involve at least two cases in an organization or community caused by the same serogroup within three months. Genome comparisons, including phylogenetic analysis and quantification of genome distances can provide confirmatory evidence of pathogen transmission during an outbreak. Interpreting genome distances depends on understanding their distribution both among isolates from outbreaks and among those not from outbreaks. Here, we identify outbreak strains based on phylogenetic relationships among 141 N . meningitidis isolates collected from 28 outbreaks in the USA during 2010–2017 and 1516 non-outbreak isolates collected through contemporaneous meningococcal surveillance. We show that genome distance thresholds based on the maximum SNPs and allele distances among isolates in the phylogenetically defined outbreak strains are sufficient to separate most pairs of non-outbreak isolates into separate strains. Non-outbreak isolate pairs that could not be distinguished from each other based on genetic distances were concentrated in the clonal complexes CC11, CC103, and CC32. Within each of these clonal complexes, phylodynamic analysis identified a group of isolates with extremely low diversity, collected over several years and multiple states. Clusters of isolates with low genetic diversity could indicate increased pathogen transmission, potentially resulting in local outbreaks or nationwide clonal expansions. Meningococcal disease is a life-threatening illness caused by the bacterium Neisseria meningitidis . Meningococcal disease outbreaks occur when the same serogroup of N . meningitidis causes multiple cases of disease over a short time period in a population such as a community, college, or prison. As with many other pathogens, genome sequencing can reveal genetic relationships among N . meningitidis based on genomic changes that accumulated as the bacteria were transmitted from person to person. Here, we review 28 outbreaks that occurred over eight years in the United States and identify outbreak strains based on how the N . meningitidis isolated from these outbreaks relate to each other and to N . meningitidis isolated from hundreds of other cases from across the country. We show that pairs of isolates from the same outbreak strain have much higher genome similarity than is typical for pairs of isolates that are not from outbreaks; therefore, genome similarity can help delimit outbreak strains during future outbreak investigations. We also identify groups of N . meningitidis that had similar genomes despite being collected over several years and in multiple states; illustrating how changes in meningococcal disease epidemiology could be affected by the spread of these bacteria. Introduction Meningococcal disease outbreaks in the United States are public health emergencies due to their high case fatality rate [1–3]. CDC guidelines provide flexible thresholds for outbreak declarations, based on detecting multiple primary cases of the same meningococcal serogroup during a 3-month period; outbreaks in organizations may be declared after 2–3 cases, while outbreaks in geographically defined communities require an increased disease incidence [4]. Here we identify genome distance values that indicate outbreaks by evaluating the genomic diversity of meningococcal isolates from US outbreaks relative to the diversity of non-outbreak invasive isolates collected from surveillance programs within the United States and isolates from the UK and Ireland with sequences included in an international genome collection. The phylogenetic distance among any two isolates in a genomic cluster ranges from the minimum possible value of 2×10−8 up to 1.56×10−3 subs/site (S1 Fig), and has a strong monotonic association with cgMLST allele distances (Spearman’s rank correlation rs = 0.96, range of 0 to 1240 alleles) and SNP distances, both when excluding small SNP clusters (rs = 0.94, 0–9067 SNPs, k-mer size k = 25) and when excluding large SNP clusters (rs = 0.97, 0–866 SNPs, k = 251) (S2 Fig). Introduction Meningococcal disease outbreaks in the United States are public health emergencies due to their high case fatality rate [1–3]. CDC guidelines provide flexible thresholds for outbreak declarations, based on detecting multiple primary cases of the same meningococcal serogroup during a 3-month period; outbreaks in organizations may be declared after 2–3 cases, while outbreaks in geographically defined communities require an increased disease incidence [4]. Here we identify genome distance values that indicate outbreaks by evaluating the genomic diversity of meningococcal isolates from US outbreaks relative to the diversity of non-outbreak invasive isolates collected from surveillance programs within the United States and isolates from the UK and Ireland with sequences included in an international genome collection. The phylogenetic distance among any two isolates in a genomic cluster ranges from the minimum possible value of 2×10−8 up to 1.56×10−3 subs/site (S1 Fig), and has a strong monotonic association with cgMLST allele distances (Spearman’s rank correlation rs = 0.96, range of 0 to 1240 alleles) and SNP distances, both when excluding small SNP clusters (rs = 0.94, 0–9067 SNPs, k-mer size k = 25) and when excluding large SNP clusters (rs = 0.97, 0–866 SNPs, k = 251) (S2 Fig). |
| Audience | Academic |
| Author | Chen, Alex McNamara, Lucy A. Retchless, Adam C. Wang, Xin Mustapha, Mustapha M. Harrison, Lee H. Chang, How-Yi Blain, Amy E. |
| AuthorAffiliation | University of Oxford, UNITED KINGDOM 2 Microbial Genomic Epidemiology Laboratory, Center for Genomic Epidemiology, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America 1 Division of Bacterial Diseases, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America |
| AuthorAffiliation_xml | – name: University of Oxford, UNITED KINGDOM – name: 1 Division of Bacterial Diseases, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America – name: 2 Microbial Genomic Epidemiology Laboratory, Center for Genomic Epidemiology, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America |
| Author_xml | – sequence: 1 givenname: Adam C. orcidid: 0000-0001-7185-591X surname: Retchless fullname: Retchless, Adam C. – sequence: 2 givenname: Alex orcidid: 0000-0002-3563-2556 surname: Chen fullname: Chen, Alex – sequence: 3 givenname: How-Yi orcidid: 0000-0001-9097-7445 surname: Chang fullname: Chang, How-Yi – sequence: 4 givenname: Amy E. surname: Blain fullname: Blain, Amy E. – sequence: 5 givenname: Lucy A. orcidid: 0000-0001-8240-7493 surname: McNamara fullname: McNamara, Lucy A. – sequence: 6 givenname: Mustapha M. surname: Mustapha fullname: Mustapha, Mustapha M. – sequence: 7 givenname: Lee H. surname: Harrison fullname: Harrison, Lee H. – sequence: 8 givenname: Xin orcidid: 0000-0002-7157-0022 surname: Wang fullname: Wang, Xin |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34003852$$D View this record in MEDLINE/PubMed |
| BookMark | eNqVkl2L1DAUhousuB_6D0QL3ujFjEmTpuleCMvix8Cygrp4GdKTtGZskzFJF_ffm-50ZGdZBOlFyslz3uQ9eY-zA-uszrLnGC0xqfDbtRu9lf1ys5FxiRGqS84eZUe4LMmiIhU9uPN_mB2HsEaIYoLZk-yQUIQIL4uj7PtVMLbLL7UJQXsj80HbVDDRKBPyTls3GMiVudY-mHiTR5cb2zo_5G6MjdfyZx6il8bmRmkbTWtARuPs0-xxK_ugn83rSXb14f2380-Li88fV-dnFwtgDMcF05ixpq4YAa4KBRSU0hQoqhsOLWokbqAtC5XsgaSsKeu2lCBrTmsglBfkJHu51d30Loh5JkEUJcU8uWcTsdoSysm12HgzSH8jnDTituB8J6SPBnotuKwoR0gpXCiqJeO4Ag5NDWWLaUEgab2bTxubQStIjr3s90T3d6z5ITp3LZJSxUqUBF7PAt79GnWIYjABdN9Lq9043bvgNa4KghP66h76sLuZ6mQyMD1NOhcmUXHGGKlLjDBN1PIBKn1Kp-dNuWpNqu81vNlrSEzUv2MnxxDE6uuX_2Av99kXdwf4d3K7QCbgdAuAdyF43Qow8TZRU8p6gZGY0r-bhZjSL-b0p2Z6r3mn_8-2P6VZCsc |
| CitedBy_id | crossref_primary_10_1016_j_ijid_2023_04_005 crossref_primary_10_2807_1560_7917_ES_2022_27_9_2100224 crossref_primary_10_3201_eid3101_240940 crossref_primary_10_1093_gbe_evab287 crossref_primary_10_1016_j_jadohealth_2024_01_016 crossref_primary_10_1038_s41467_023_43528_0 crossref_primary_10_1093_ofid_ofae249 |
| Cites_doi | 10.1177/2051013614526592 10.3201/eid2210.160468 10.1093/nar/gku1196 10.1016/S2666-5247(20)30149-X 10.1038/s41564-020-0738-5 10.1128/JCM.39.1.75-85.2001 10.3201/eid2503.181574 10.1128/AEM.00362-16 10.1093/sysbio/syaa009 10.1111/1755-0998.12630 10.3389/fmicb.2018.01482 10.3201/eid2109.141333 10.1016/j.jinf.2018.06.008 10.1093/bioinformatics/btp163 10.1093/cid/cix993 10.1093/bioinformatics/btz305 10.1111/j.1574-6976.2006.00057.x 10.1016/j.jinf.2019.09.001 10.1093/bioinformatics/btv271 10.1038/nmicrobiol.2016.185 10.1038/s41598-018-33622-5 10.3389/fgene.2020.579411 10.1128/JCM.00080-17 10.1038/s41579-019-0282-6 10.1007/s40471-018-0170-z 10.1093/cid/ciy548 10.1371/journal.pone.0202615 10.3389/fmicb.2019.02897 10.1101/gr.241455.118 10.1093/infdis/jiaa002 10.1038/s41592-019-0686-2 10.12688/wellcomeopenres.14826.1 |
| ContentType | Journal Article |
| Copyright | COPYRIGHT 2021 Public Library of Science This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication: https://creativecommons.org/publicdomain/zero/1.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. |
| Copyright_xml | – notice: COPYRIGHT 2021 Public Library of Science – notice: This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication: https://creativecommons.org/publicdomain/zero/1.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. |
| DBID | AAYXX CITATION NPM ISN ISR 3V. 7QL 7U9 7X7 7XB 88E 8FE 8FH 8FI 8FJ 8FK ABUWG AEUYN AFKRA AZQEC BBNVY BENPR BHPHI C1K CCPQU COVID DWQXO FYUFA GHDGH GNUQQ H94 HCIFZ K9. LK8 M0S M1P M7P PHGZM PHGZT PIMPY PJZUB PKEHL PPXIY PQEST PQGLB PQQKQ PQUKI PRINS 7X8 5PM DOA |
| DOI | 10.1371/journal.ppat.1009586 |
| DatabaseName | CrossRef PubMed Gale In Context: Canada Gale In Context: Science ProQuest Central (Corporate) Bacteriology Abstracts (Microbiology B) Virology and AIDS Abstracts Health & Medical Collection ProQuest Central (purchase pre-March 2016) Medical Database (Alumni Edition) ProQuest SciTech Collection ProQuest Natural Science Collection ProQuest Hospital Collection Hospital Premium Collection (Alumni Edition) ProQuest Central (Alumni) (purchase pre-March 2016) ProQuest Central (Alumni) ProQuest One Sustainability ProQuest Central UK/Ireland ProQuest Central Essentials Biological Science Database ProQuest Central Natural Science Collection Environmental Sciences and Pollution Management ProQuest One Community College Coronavirus Research Database ProQuest Central Korea Health Research Premium Collection Health Research Premium Collection (Alumni) ProQuest Central Student AIDS and Cancer Research Abstracts SciTech Premium Collection ProQuest Health & Medical Complete (Alumni) Biological Sciences ProQuest Health & Medical Collection Proquest Medical Database Biological Science Database ProQuest Central Premium ProQuest One Academic (New) Publicly Available Content Database ProQuest Health & Medical Research Collection ProQuest One Academic Middle East (New) ProQuest One Health & Nursing ProQuest One Academic Eastern Edition (DO NOT USE) ProQuest One Applied & Life Sciences ProQuest One Academic ProQuest One Academic UKI Edition ProQuest Central China MEDLINE - Academic PubMed Central (Full Participant titles) DOAJ Directory of Open Access Journals |
| DatabaseTitle | CrossRef PubMed Publicly Available Content Database ProQuest Central Student ProQuest One Academic Middle East (New) ProQuest Central Essentials ProQuest Health & Medical Complete (Alumni) ProQuest Central (Alumni Edition) SciTech Premium Collection ProQuest One Community College ProQuest One Health & Nursing ProQuest Natural Science Collection ProQuest Central China Environmental Sciences and Pollution Management ProQuest Central ProQuest One Applied & Life Sciences ProQuest One Sustainability ProQuest Health & Medical Research Collection Health Research Premium Collection Health and Medicine Complete (Alumni Edition) Natural Science Collection ProQuest Central Korea Bacteriology Abstracts (Microbiology B) Health & Medical Research Collection Biological Science Collection AIDS and Cancer Research Abstracts ProQuest Central (New) ProQuest Medical Library (Alumni) Virology and AIDS Abstracts ProQuest Biological Science Collection ProQuest One Academic Eastern Edition Coronavirus Research Database ProQuest Hospital Collection Health Research Premium Collection (Alumni) Biological Science Database ProQuest SciTech Collection ProQuest Hospital Collection (Alumni) ProQuest Health & Medical Complete ProQuest Medical Library ProQuest One Academic UKI Edition ProQuest One Academic ProQuest One Academic (New) ProQuest Central (Alumni) MEDLINE - Academic |
| DatabaseTitleList | CrossRef PubMed MEDLINE - Academic Publicly Available Content Database |
| Database_xml | – sequence: 1 dbid: DOA name: DOAJ Directory of Open Access Journals url: https://www.doaj.org/ sourceTypes: Open Website – sequence: 2 dbid: NPM name: PubMed url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed sourceTypes: Index Database – sequence: 3 dbid: BENPR name: ProQuest Central url: https://www.proquest.com/central sourceTypes: Aggregation Database |
| DeliveryMethod | fulltext_linktorsrc |
| Discipline | Biology Public Health |
| DocumentTitleAlternate | Genomic diversity of Neisseria meningitidis outbreak strains |
| EISSN | 1553-7374 |
| ExternalDocumentID | 2541855362 oai_doaj_org_article_8a74800dd12d4ea6817c8cb9c5f1423c PMC8177650 A663951014 34003852 10_1371_journal_ppat_1009586 |
| Genre | Journal Article |
| GeographicLocations | United States Oregon California United Kingdom--UK United States--US Ireland |
| GeographicLocations_xml | – name: United States – name: California – name: Oregon – name: Ireland – name: United Kingdom--UK – name: United States--US |
| GroupedDBID | --- 123 29O 2WC 53G 5VS 7X7 88E 8FE 8FH 8FI 8FJ AAFWJ AAUCC AAWOE AAYXX ABDBF ABUWG ACGFO ACIHN ACPRK ACUHS ADBBV AEAQA AENEX AEUYN AFKRA AFPKN AFRAH AHMBA ALMA_UNASSIGNED_HOLDINGS AOIJS B0M BAWUL BBNVY BCNDV BENPR BHPHI BPHCQ BVXVI BWKFM CCPQU CITATION CS3 DIK DU5 E3Z EAP EAS EBD EMK EMOBN ESX F5P FPL FYUFA GROUPED_DOAJ GX1 HCIFZ HMCUK HYE IAO IHR INH INR ISN ISR ITC KQ8 LK8 M1P M48 M7P MM. O5R O5S OK1 OVT P2P PGMZT PHGZM PHGZT PIMPY PQQKQ PROAC PSQYO PV9 QF4 QN7 RNS RPM RZL SV3 TR2 TUS UKHRP WOW ~8M 3V. M~E NPM PMFND 7QL 7U9 7XB 8FK AZQEC C1K COVID DWQXO GNUQQ H94 K9. PJZUB PKEHL PPXIY PQEST PQGLB PQUKI PRINS 7X8 5PM PUEGO - AAPBV ABPTK ADACO BBAFP |
| ID | FETCH-LOGICAL-c661t-6e166b9763c8d2dc4cdde4c409b8cf0ba1bcf52d009ca46b59f5aca9849c34823 |
| IEDL.DBID | M48 |
| ISSN | 1553-7374 1553-7366 |
| IngestDate | Fri Nov 26 17:13:16 EST 2021 Wed Aug 27 01:25:40 EDT 2025 Thu Aug 21 14:05:32 EDT 2025 Mon Jul 21 09:39:33 EDT 2025 Fri Jul 25 10:41:12 EDT 2025 Tue Jun 17 21:36:18 EDT 2025 Tue Jun 10 20:30:32 EDT 2025 Fri Jun 27 04:16:13 EDT 2025 Fri Jun 27 03:32:38 EDT 2025 Wed Feb 19 02:28:55 EST 2025 Thu Apr 24 22:53:20 EDT 2025 Tue Jul 01 01:13:52 EDT 2025 |
| IsDoiOpenAccess | true |
| IsOpenAccess | true |
| IsPeerReviewed | true |
| IsScholarly | true |
| Issue | 5 |
| Language | English |
| License | This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. Creative Commons CC0 public domain |
| LinkModel | DirectLink |
| MergedId | FETCHMERGED-LOGICAL-c661t-6e166b9763c8d2dc4cdde4c409b8cf0ba1bcf52d009ca46b59f5aca9849c34823 |
| Notes | new_version ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Current address: Division of Preparedness And Emerging Infections, National Center For Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America Current address: Division of Viral Diseases, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America L.H.H. has served as a consultant for GSK, Sanofi Pasteur, Pfizer, and Merck in the area of epidemiology and vaccine prevention of bacterial diseases. The other authors have declared that no competing interests exist. |
| ORCID | 0000-0002-7157-0022 0000-0001-8240-7493 0000-0002-3563-2556 0000-0001-9097-7445 0000-0001-7185-591X |
| OpenAccessLink | https://doaj.org/article/8a74800dd12d4ea6817c8cb9c5f1423c |
| PMID | 34003852 |
| PQID | 2541855362 |
| PQPubID | 1436335 |
| ParticipantIDs | plos_journals_2541855362 doaj_primary_oai_doaj_org_article_8a74800dd12d4ea6817c8cb9c5f1423c pubmedcentral_primary_oai_pubmedcentral_nih_gov_8177650 proquest_miscellaneous_2528917231 proquest_journals_2541855362 gale_infotracmisc_A663951014 gale_infotracacademiconefile_A663951014 gale_incontextgauss_ISR_A663951014 gale_incontextgauss_ISN_A663951014 pubmed_primary_34003852 crossref_citationtrail_10_1371_journal_ppat_1009586 crossref_primary_10_1371_journal_ppat_1009586 |
| ProviderPackageCode | CITATION AAYXX |
| PublicationCentury | 2000 |
| PublicationDate | 20210518 |
| PublicationDateYYYYMMDD | 2021-05-18 |
| PublicationDate_xml | – month: 5 year: 2021 text: 20210518 day: 18 |
| PublicationDecade | 2020 |
| PublicationPlace | United States |
| PublicationPlace_xml | – name: United States – name: San Francisco – name: San Francisco, CA USA |
| PublicationTitle | PLoS pathogens |
| PublicationTitleAlternate | PLoS Pathog |
| PublicationYear | 2021 |
| Publisher | Public Library of Science Public Library of Science (PLoS) |
| Publisher_xml | – name: Public Library of Science – name: Public Library of Science (PLoS) |
| References | SA Mbaeyi (ppat.1009586.ref002) 2018; 68 P Stefanelli (ppat.1009586.ref011) 2019; 25 AM Kozlov (ppat.1009586.ref038) 2019; 35 NJ Croucher (ppat.1009586.ref037) 2015; 43 ppat.1009586.ref004 SE Oliver (ppat.1009586.ref019) 2018; 5 T Popovic (ppat.1009586.ref009) 2001; 39 MM Mustapha (ppat.1009586.ref017) 2020 F Coll (ppat.1009586.ref028) 2020; 1 CB Kretz (ppat.1009586.ref036) 2016; 22 SN Gardner (ppat.1009586.ref041) 2015; 31 PJ Cock (ppat.1009586.ref042) 2009; 25 C Trotter (ppat.1009586.ref003) 2016 J Lawler (ppat.1009586.ref012) 2019; 24 DA Caugant (ppat.1009586.ref029) 2020; 18 A Moura (ppat.1009586.ref014) 2016; 2 CJ Villabona-Arenas (ppat.1009586.ref021) 2020; 5 KA Jolley (ppat.1009586.ref005) 2007; 31 A Jamet (ppat.1009586.ref025) 2020 J Lucidarme (ppat.1009586.ref026) 2016; 21 CC Potts (ppat.1009586.ref033) 2018; 77 MD Karcher (ppat.1009586.ref040) 2017; 17 JR MacNeil (ppat.1009586.ref001) 2018; 66 A Saltykova (ppat.1009586.ref007) 2019; 10 EM Volz (ppat.1009586.ref039) 2014; 11 AW Pightling (ppat.1009586.ref013) 2018; 9 ppat.1009586.ref032 G Langley (ppat.1009586.ref030) 2015; 21 BH Raphael (ppat.1009586.ref015) 2016; 82 AJ Cody (ppat.1009586.ref023) 2017; 55 A Lo Presti (ppat.1009586.ref027) 2019 JA Lees (ppat.1009586.ref018) 2019; 29 KA Jolley (ppat.1009586.ref034) 2018; 3 EM Volz (ppat.1009586.ref016) 2020; 69 JC Holmes (ppat.1009586.ref008); 11 T Seemann (ppat.1009586.ref035) 2015 E Chacon-Cruz (ppat.1009586.ref022) 2014; 2 P Virtanen (ppat.1009586.ref043) 2020; 17 OB Harrison (ppat.1009586.ref024) 2020; 222 I Ezeoke (ppat.1009586.ref010) 2018; 13 HM Soeters (ppat.1009586.ref020) 2019; 25 MJ Whaley (ppat.1009586.ref006) 2018; 8 HY Chang (ppat.1009586.ref031) 2019; 79 |
| References_xml | – year: 2015 ident: ppat.1009586.ref035 publication-title: Snippy: Rapid haploid variant calling and core SNP phylogeny – volume: 2 start-page: 71 issue: 3 year: 2014 ident: ppat.1009586.ref022 article-title: An outbreak of serogroup C (ST-11) meningococcal disease in Tijuana, Mexico. publication-title: Therapeutic advances in vaccines doi: 10.1177/2051013614526592 – volume: 22 start-page: 1762 issue: 10 year: 2016 ident: ppat.1009586.ref036 article-title: Whole-Genome Characterization of Epidemic Neisseria meningitidis Serogroup C and Resurgence of Serogroup W, Niger, 2015 publication-title: Emerging infectious diseases doi: 10.3201/eid2210.160468 – volume: 43 start-page: e15 issue: 3 year: 2015 ident: ppat.1009586.ref037 article-title: Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins publication-title: Nucleic acids research doi: 10.1093/nar/gku1196 – volume: 1 start-page: e328 issue: 8 year: 2020 ident: ppat.1009586.ref028 article-title: Definition of a genetic relatedness cutoff to exclude recent transmission of meticillin-resistant Staphylococcus aureus: a genomic epidemiology analysis publication-title: The Lancet Microbe. doi: 10.1016/S2666-5247(20)30149-X – volume: 5 start-page: 876 issue: 7 year: 2020 ident: ppat.1009586.ref021 article-title: Phylogenetic interpretation during outbreaks requires caution publication-title: Nature microbiology doi: 10.1038/s41564-020-0738-5 – volume: 39 start-page: 75 issue: 1 year: 2001 ident: ppat.1009586.ref009 article-title: Evaluation of pulsed-field gel electrophoresis in epidemiological investigations of meningococcal disease outbreaks caused by Neisseria meningitidis serogroup C publication-title: J Clin Microbiol doi: 10.1128/JCM.39.1.75-85.2001 – ident: ppat.1009586.ref004 – volume: 25 start-page: 434 issue: 3 year: 2019 ident: ppat.1009586.ref020 article-title: University-Based Outbreaks of Meningococcal Disease Caused by Serogroup B, United States, 2013–2018 publication-title: Emerging infectious diseases doi: 10.3201/eid2503.181574 – volume: 82 start-page: 3582 issue: 12 year: 2016 ident: ppat.1009586.ref015 article-title: Genomic Resolution of Outbreak-Associated Legionella pneumophila Serogroup 1 Isolates from New York State publication-title: Applied and environmental microbiology doi: 10.1128/AEM.00362-16 – year: 2020 ident: ppat.1009586.ref025 article-title: High resolution typing of Staphylococcus epidermidis based on cgMLST to investigate the hospital spread of multidrug resistant clones publication-title: J Clin Microbiol – volume: 69 start-page: 884 issue: 5 year: 2020 ident: ppat.1009586.ref016 article-title: Identification of hidden population structure in time-scaled phylogenies publication-title: Systematic biology doi: 10.1093/sysbio/syaa009 – volume: 17 start-page: 96 issue: 1 year: 2017 ident: ppat.1009586.ref040 article-title: phylodyn: an R package for phylodynamic simulation and inference publication-title: Molecular ecology resources doi: 10.1111/1755-0998.12630 – volume: 9 start-page: 1482 year: 2018 ident: ppat.1009586.ref013 article-title: Interpreting Whole-Genome Sequence Analyses of Foodborne Bacteria for Regulatory Applications and Outbreak Investigations. publication-title: Frontiers in microbiology doi: 10.3389/fmicb.2018.01482 – volume: 21 start-page: 1520 issue: 9 year: 2015 ident: ppat.1009586.ref030 article-title: Twenty Years of Active Bacterial Core Surveillance publication-title: Emerging infectious diseases doi: 10.3201/eid2109.141333 – volume: 77 start-page: 427 issue: 5 year: 2018 ident: ppat.1009586.ref033 article-title: Population structure of invasive Neisseria meningitidis in the United States, 2011–15. publication-title: The Journal of infection doi: 10.1016/j.jinf.2018.06.008 – volume: 25 start-page: 1422 issue: 11 year: 2009 ident: ppat.1009586.ref042 article-title: Biopython: freely available Python tools for computational molecular biology and bioinformatics publication-title: Bioinformatics (Oxford, England). doi: 10.1093/bioinformatics/btp163 – volume: 66 start-page: 1276 issue: 8 year: 2018 ident: ppat.1009586.ref001 article-title: Current Epidemiology and Trends in Meningococcal Disease-United States, 1996–2015 publication-title: Clin Infect Dis doi: 10.1093/cid/cix993 – volume: 35 start-page: 4453 issue: 21 year: 2019 ident: ppat.1009586.ref038 article-title: RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference publication-title: Bioinformatics (Oxford, England). doi: 10.1093/bioinformatics/btz305 – volume: 31 start-page: 89 issue: 1 year: 2007 ident: ppat.1009586.ref005 article-title: Molecular typing of meningococci: recommendations for target choice and nomenclature publication-title: FEMS microbiology reviews doi: 10.1111/j.1574-6976.2006.00057.x – volume: 79 start-page: 426 issue: 5 year: 2019 ident: ppat.1009586.ref031 article-title: Distribution of Neisseria meningitidis serogroup b (NmB) vaccine antigens in meningococcal disease causing isolates in the United States during 2009–2014, prior to NmB vaccine licensure publication-title: The Journal of infection doi: 10.1016/j.jinf.2019.09.001 – volume: 31 start-page: 2877 issue: 17 year: 2015 ident: ppat.1009586.ref041 article-title: kSNP3.0: SNP detection and phylogenetic analysis of genomes without genome alignment or reference genome publication-title: Bioinformatics (Oxford, England). doi: 10.1093/bioinformatics/btv271 – volume: 21 issue: 45 year: 2016 ident: ppat.1009586.ref026 article-title: An international invasive meningococcal disease outbreak due to a novel and rapidly expanding serogroup W strain, Scotland and Sweden, July to August 2015. publication-title: Euro surveillance: bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin – volume: 2 start-page: 16185 year: 2016 ident: ppat.1009586.ref014 article-title: Whole genome-based population biology and epidemiological surveillance of Listeria monocytogenes publication-title: Nature microbiology doi: 10.1038/nmicrobiol.2016.185 – ident: ppat.1009586.ref032 – start-page: 1 volume-title: Handbook of Meningococcal Disease Management year: 2016 ident: ppat.1009586.ref003 – volume: 8 start-page: 15803 issue: 1 year: 2018 ident: ppat.1009586.ref006 article-title: Whole genome sequencing for investigations of meningococcal outbreaks in the United States: a retrospective analysis. publication-title: Scientific reports doi: 10.1038/s41598-018-33622-5 – volume: 11 start-page: 579411 ident: ppat.1009586.ref008 article-title: Rapid Transmission of a Hyper-Virulent Meningococcal Clone Due to High Effective Contact Numbers and Super Spreaders. publication-title: Front Genet. 2020 doi: 10.3389/fgene.2020.579411 – volume: 25 start-page: 111.e1 issue: 1 year: 2019 ident: ppat.1009586.ref011 article-title: An outbreak of severe invasive meningococcal disease due to a capsular switched Neisseria meningitidis hypervirulent strain B:cc11. Clinical microbiology and infection: the official publication of the publication-title: European Society of Clinical Microbiology and Infectious Diseases – volume: 55 start-page: 2086 issue: 7 year: 2017 ident: ppat.1009586.ref023 article-title: Core Genome Multilocus Sequence Typing Scheme for Stable, Comparative Analyses of Campylobacter jejuni and C. coli Human Disease Isolates publication-title: J Clin Microbiol doi: 10.1128/JCM.00080-17 – volume: 18 start-page: 84 issue: 2 year: 2020 ident: ppat.1009586.ref029 article-title: Neisseria meningitidis: using genomics to understand diversity, evolution and pathogenesis publication-title: Nature Reviews Microbiology doi: 10.1038/s41579-019-0282-6 – volume: 24 issue: 23 year: 2019 ident: ppat.1009586.ref012 article-title: Suspected cluster of Neisseria meningitidis W invasive disease in an elderly care home: do new laboratory methods aid public health action? United Kingdom, 2015 publication-title: Euro surveillance: bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin – volume: 5 start-page: 321 issue: 4 year: 2018 ident: ppat.1009586.ref019 article-title: Review of Global Epidemiology and Response to Meningococcal Disease Outbreaks among Men Who Have Sex with Men, 2001–2018 publication-title: ACurrent Epidemiology Reports doi: 10.1007/s40471-018-0170-z – volume: 68 start-page: 580 issue: 4 year: 2018 ident: ppat.1009586.ref002 article-title: Epidemiology of meningococcal disease outbreaks in the United States, 2009–2013 publication-title: Clin Infect Dis doi: 10.1093/cid/ciy548 – volume: 13 start-page: e0202615 issue: 11 year: 2018 ident: ppat.1009586.ref010 article-title: Tracking a serial killer: Integrating phylogenetic relationships, epidemiology, and geography for two invasive meningococcal disease outbreaks. publication-title: PLoS One doi: 10.1371/journal.pone.0202615 – volume: 11 start-page: 20140945 issue: 101 year: 2014 ident: ppat.1009586.ref039 article-title: Sampling through time and phylodynamic inference with coalescent and birth-death models publication-title: Journal of the Royal Society – volume: 10 start-page: 2897 year: 2019 ident: ppat.1009586.ref007 article-title: Detailed Evaluation of Data Analysis Tools for Subtyping of Bacterial Isolates Based on Whole Genome Sequencing: Neisseria meningitidis as a Proof of Concept. publication-title: Frontiers in microbiology doi: 10.3389/fmicb.2019.02897 – volume: 29 start-page: 304 issue: 2 year: 2019 ident: ppat.1009586.ref018 article-title: Fast and flexible bacterial genomic epidemiology with PopPUNK publication-title: Genome Res doi: 10.1101/gr.241455.118 – volume: 222 start-page: 1816 issue: 11 year: 2020 ident: ppat.1009586.ref024 article-title: Neisseria gonorrhoeae Population Genomics: Use of the Gonococcal Core Genome to Improve Surveillance of Antimicrobial Resistance publication-title: The Journal of infectious diseases doi: 10.1093/infdis/jiaa002 – start-page: 58 year: 2019 ident: ppat.1009586.ref027 article-title: Reconstruction of Dispersal Patterns of Hypervirulent Meningococcal Strains of Serogroup C:cc11 by Phylogenomic Time Trees publication-title: J Clin Microbiol – volume: 17 start-page: 261 issue: 3 year: 2020 ident: ppat.1009586.ref043 article-title: SciPy 1.0: fundamental algorithms for scientific computing in Python. publication-title: Nat Methods. doi: 10.1038/s41592-019-0686-2 – year: 2020 ident: ppat.1009586.ref017 article-title: Neisseria meningitidis During Carriage and Invasive Disease in High School Students in Georgia and Maryland, 2006–2007 publication-title: The Journal of infectious diseases – volume: 3 start-page: 124 year: 2018 ident: ppat.1009586.ref034 article-title: Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications publication-title: Wellcome open research doi: 10.12688/wellcomeopenres.14826.1 |
| SSID | ssj0041316 |
| Score | 2.3858407 |
| Snippet | Meningococcal disease is a life-threatening illness caused by the human-restricted bacterium
Neisseria meningitidis
. Outbreaks in the USA involve at least two... Meningococcal disease is a life-threatening illness caused by the human-restricted bacterium Neisseria meningitidis. Outbreaks in the USA involve at least two... Introduction Meningococcal disease outbreaks in the United States are public health emergencies due to their high case fatality rate [1–3]. CDC guidelines... Introduction Meningococcal disease outbreaks in the United States are public health emergencies due to their high case fatality rate [1–3]. CDC guidelines... |
| SourceID | plos doaj pubmedcentral proquest gale pubmed crossref |
| SourceType | Open Website Open Access Repository Aggregation Database Index Database Enrichment Source |
| StartPage | e1009586 |
| SubjectTerms | Alleles Biology and Life Sciences Causes of Clusters Computer and Information Sciences Epidemics Genetic aspects Genomes Genomics Genotype Health aspects Identification and classification Medicine and Health Sciences Meningococcal disease Neisseria meningitidis Outbreaks Phylogenetics Phylogeny Population Public health United States |
| SummonAdditionalLinks | – databaseName: DOAJ Directory of Open Access Journals dbid: DOA link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV1Lb9QwELbQSkhcEO8uFGQQEqfQdezE8bEgqoLEHoCK3iLHD4jaJiuSPfDvmbGd1QYV9cI1HkfxzGT8jTz-hpDXHLs-al1l3FcqE9bkmXZKZp4VUjVcK-vxovDndXl6Jj6dF-d7rb6wJizSA0fFHVVaCgA11rLcCqfLiklTmUaZwjOAAgajL-x5UzIVYzBE5tD0FJviZJKXZbo0xyU7SjZ6u9lopI8GiIH3qPc2pcDdv4vQi81lP1wHP_-uotzblk7ukbsJT9LjuI775JbrHpDbscPk74fkeygJoGsXjt1bTa9cbFHU2nagSNB61Rpqp-IMOvY0UqnSfjtCtqwv6BC6SNDWprqiYMpH5Ozkw7f3p1nqpZAZ2IHHrHSsLBvAHtxUNrdGGIhrwkB211TGrxrNGuOL3II-jBZlUyhfaKNVJZRB_hv-mCy6vnMHhCrpucuVWHHlRa6t9rnjlsH7V74otFoSPimzNoloHL_0sg6nZxISjqibGk1QJxMsSbabtYlEGzfIv0M77WSRJjs8AOepk_PUNznPkrxCK9dIhNFhpc0PvR2G-uPXdX0MUAzRJxP_FPoyE3qThHwPizU63W4AlSHB1kzycCYJv7OZDR-gx01rHmrI4AFTFQA0YObkhdcPv9wN40uxeq5z_RZlIK0GpMrZkjyJTrvTGxfhcBhmy5k7zxQ7H-nan4GHHLQpAeA__R-WeEbu5FgthLy41SFZjL-27jnAvbF5Ef7sP6OOU3s priority: 102 providerName: Directory of Open Access Journals – databaseName: Health & Medical Collection dbid: 7X7 link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwhV1Lb9QwELZgERISQlAeXSjIICROoZvYieMTKoiqILEHoGJvkeNHG9Emocke-PfMOE5oUIFrPI6SGXv8jT3-hpCXDKs-KpVHzOUy4kYnkbJSRC5OhSyZksbhReFP6-zomH_cpJuw4daFtMrRJ3pHbRqNe-T7EMjA0pKCv33T_oiwahSeroYSGtfJDaQuw5QusZkCLvDPvvQplsaJBMuycHWOiXg_WOp12yokkQaggbepLy1NnsF_8tOL9qzprgKhf-ZSXlqcDu-SOwFV0oNhGNwj12y9Q24OdSZ_7pDbw-YcHe4c3SfffKIAXVt_GF8pem6HwkWVqTqKtK3nIG3GlA3aN3QgWKXNtocYWn2nna8tQSsTso28gR-Q48P3X98dRaHCQqRhXe6jzMZZVgIiYTo3idFcg7fjGmK-MtduVaq41C5NDOhHK56VqXSp0krmXGpkxWEPyaJuartLqBSO2UTyFZOOJ8ool1hmYnj_yqWpkkvCRuUWOtCP45eeFf5MTUAYMuiqQJMUwSRLEk292oF-4z_yb9FukyySZ_sHzcVJEeZikSvBAScbEyeGW5XlsdC5LqVOXQzoUi_JC7R6gfQYNebfnKht1xUfvqyLAwBoiElj_lehzzOhV0HINfCzWoU7D6AypN2aSe7NJGGS61nzLo7A8Z-74vd0gJ7jqLy6-fnUjC_FnLraNluUgWAb8CuLl-TRMIgnvTHuj4yht5gN75li5y11derZyUGbAmD_439_1hNyK8HsIOTBzffIor_Y2qcA7_rymZ_DvwCO5U_f priority: 102 providerName: ProQuest |
| Title | Using Neisseria meningitidis genomic diversity to inform outbreak strain identification |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/34003852 https://www.proquest.com/docview/2541855362 https://www.proquest.com/docview/2528917231 https://pubmed.ncbi.nlm.nih.gov/PMC8177650 https://doaj.org/article/8a74800dd12d4ea6817c8cb9c5f1423c http://dx.doi.org/10.1371/journal.ppat.1009586 |
| Volume | 17 |
| hasFullText | 1 |
| inHoldings | 1 |
| isFullTextHit | |
| isPrint | |
| link | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwhV3db9MwELe2TqC9IL4XGJVBSDxlqmMnjh8Q2tCmgbQKDSr6Fjn-GBFdUppWYv89Z-dDBLXiNT5byfnO_l18_h1Cb6mr-ihlGlKbipBpFYXSCB5aEnORUym0dReFr6bJ5Yx9nsfzPdTVbG0VWG8N7Vw9qdlqcfL7190HcPj3vmoDJ12nk-VSOkJoAA1pso8OYG_izlWvWH-uACs2SdoLdLt6HqL7lPkDs2iwV3lK_37hHi0XVb0Nlf6bXPnXbnXxED1oYSY-beziEdoz5WN0ryk8efcEffeZAnhq_Gl8IfGtaSoXFbqoseNtvS0U1l3OBl5XuGFYxdVmDUG0_IlrX1wCF7pNN_Iz_BTNLs6_fbwM2xILoYKNeR0mhiRJDpCEqlRHWjEFyx1TEPTlqbKTXJJc2TjSoBolWZLHwsZSSZEyoRwtDn2GRmVVmiOEBbfURIJNqLAsklrayFBNYPyJjWMpAkQ7ZWaq5R93b7rI_KEahzik0U3mZiNrZyNAYd9r2fBv_Ef-zM1TL-vYs_2DanWTtc6YpZIzAMpak0gzI5OUcJWqXKjYEoCXKkBv3Cxnjh-jdAk4N3JT19mnr9PsFBCaA6WE7RS6Hgi9a4VsBR-rZHvpAVTmeLcGkscDSfByNWg-chbXfXOdQWAPUCsG_AE9Oyvc3vy6b3aDuqS60lQbJwPRNgBYSgL0vDHaXm-dCwSID8x5oNhhS1n88PTkoE0OuP_FzjFfosPIZQY5Dtz0GI3Wq415BdBunY_RPp_zMTo4O59-uR77HyRj78F_ACpeUh4 |
| linkProvider | Scholars Portal |
| linkToHtml | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwtV1Lb9QwELbKVggkhKA8ulDAIBCn0E3sPHxAqIVWW9quUGnV3ozjR1nRJkuzK9Q_xW9kJnGWBhU49RqPrWQ8nkc88w0hLxl2fVQqC5jLRMCNjgJlRRq4ME5FzpQwDguFd0fJ8IB_PIqPFsjPthYG0ypbnVgralNq_Ee-CoEMmJYY9O27yfcAu0bh7WrbQqMRi217_gNCturt1gfY31dRtLmx_34Y-K4CgQZbNA0SGyZJDlaY6cxERnMNJ5xriHPyTLtBrsJcuzgy4HxoxZM8Fi5WWomMC41IMAzWvUYWOYNQpkcW1zdGn_Za3Q8WoW62is14gpQliS_WY2m46mXjzWSiELYaXBus375gDOueAXPL0JuclNVlbu-f2ZsXzOHmHXLb-7F0rRG8u2TBFkvketPZ8nyJ3Gp-B9KmyukeOaxTE-jI1tf_Y0VPbdMqaWzGFUWg2FOgNm2SCJ2WtIF0peVsClG7-karupsFHRuf31SL1H1ycCXcf0B6RVnYZUJF6piNBB8w4XikjHKRZSaE9QcujpXoE9YyV2oPeI5veiLrW7wUAp-GVxK3RPot6ZNgPmvSAH78h34d921Oi3Dd9YPy7Fj60y8zlXLwzI0JI8OtSrIw1ZnOhY5dCP6s7pMXuOsSATkKzPg5VrOqklufR3INXEL0gkP-V6K9DtFrT-RK-FitfJUFsAyBvjqUKx1KUCu6M7yMEth-cyV_H0CY2Url5cPP58O4KGbxFbacIQ2E9-Axs7BPHjZCPOcb4_UlNcxOO-LdYWx3pBh_rfHQgZspBBqP_v1az8iN4f7ujtzZGm0_JjcjzE1CFN5shfSmZzP7BJzLaf7Un2hKvly1EvkFWtmPbg |
| linkToPdf | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwtV3db9MwELdGEQgJIRgfKwwwCMRTaBM7cfyA0GBUK4MKAdP6Fhx_jIqtKUsrtH-Nv44754MFDXjaa3y2kvP5PuK73xHyhGHXR6XSgLlUBtzoKFBWisCFsZA5U9I4LBR-P0l29vjbaTxdIz-bWhhMq2x0olfUptD4j3wAgQyYlhj07cDVaREftkcvF98D7CCFN61NO41KRHbtyQ8I38oX423Y66dRNHrz-fVOUHcYCDTYpWWQ2DBJcrDITKcmMpprOO1cQ8yTp9oNcxXm2sWRAUdEK57ksXSx0kqmXGpEhWGw7gVyUbA4xDMmpm2wB7bBt13FtjyBYElSl-0xEQ5qKXm-WCgEsAYnByu5T5lF3z2gtRG9xWFRnuUA_5nHecowjq6Ta7VHS7cqEbxB1ux8nVyqelyerJOr1Y9BWtU73ST7PkmBTqxPBJgpemSrpkkzMyspQsYeAbVp0kXosqAVuCstVkuI39U3Wvq-FnRm6kwnL1y3yN658P426c2Lud0gVArHbCT5kEnHI2WUiywzIaw_dHGsZJ-whrmZrqHP8U0PM3-fJyAEqniV4ZZk9Zb0SdDOWlTQH_-hf4X71tIicLd_UBwfZLUeyFIlOPjoxoSR4VYlaSh0qnOpYxeCZ6v75DHueobQHHMU8gO1Ksts_GmSbYFziP5wyP9K9LFD9KwmcgV8rFZ1vQWwDCG_OpSbHUpQMLozvIES2Hxzmf0-ijCzkcqzhx-1w7go5vPNbbFCGgj0wXdmYZ_cqYS45Rvj_roaZouOeHcY2x2Zz756ZHTgpoCQ4-6_X-shuQyqI3s3nuzeI1ciTFJCON50k_SWxyt7H7zMZf7AH2dKvpy3_vgFRlqSPg |
| openUrl | ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Using+Neisseria+meningitidis+genomic+diversity+to+inform+outbreak+strain+identification&rft.jtitle=PLoS+pathogens&rft.au=Retchless%2C+Adam+C&rft.au=Chen%2C+Alex&rft.au=Chang%2C+How-Yi&rft.au=Blain%2C+Amy+E&rft.date=2021-05-18&rft.eissn=1553-7374&rft.volume=17&rft.issue=5&rft.spage=e1009586&rft_id=info:doi/10.1371%2Fjournal.ppat.1009586&rft_id=info%3Apmid%2F34003852&rft.externalDocID=34003852 |
| thumbnail_l | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1553-7374&client=summon |
| thumbnail_m | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1553-7374&client=summon |
| thumbnail_s | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1553-7374&client=summon |