Rapid draft sequencing and real-time nanopore sequencing in a hospital outbreak of Salmonella
Identifieur interne : 000079 ( Main/Exploration ); précédent : 000078; suivant : 000080Rapid draft sequencing and real-time nanopore sequencing in a hospital outbreak of Salmonella
Auteurs : Joshua Quick ; Philip Ashton [Royaume-Uni] ; Szymon Calus ; Carole Chatt [Royaume-Uni] ; Savita Gossain [Royaume-Uni] ; Jeremy Hawker [Royaume-Uni] ; Satheesh Nair [Royaume-Uni] ; Keith Neal [Royaume-Uni] ; Kathy Nye [Royaume-Uni] ; Tansy Peters [Royaume-Uni] ; Elizabeth De Pinna [Royaume-Uni] ; Esther Robinson [Royaume-Uni] ; Keith Struthers [Royaume-Uni] ; Mark Webber ; Andrew Catto [Royaume-Uni] ; Timothy J. Dallman [Royaume-Uni] ; Peter Hawkey [Royaume-Uni] ; Nicholas J. LomanSource :
- Genome Biology [ 1474-7596 ] ; 2015.
Abstract
Foodborne outbreaks of
We demonstrate that rapid MiSeq sequencing can reduce the time to answer compared to the standard sequencing protocol with no impact on the results. We show, for the first time, that the MinION can acquire clinically relevant information in real time and within minutes of a DNA library being loaded. MinION sequencing permits confident assignment to species level within 20 min. Using a novel streaming phylogenetic placement method samples can be assigned to a serotype in 40 min and determined to be part of the outbreak in less than 2 h.
Both approaches yielded reliable and actionable clinical information on the
The online version of this article (doi:10.1186/s13059-015-0677-2) contains supplementary material, which is available to authorized users.
Url:
DOI: 10.1186/s13059-015-0677-2
PubMed: 26025440
PubMed Central: 4702336
Affiliations:
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type="city">Birmingham</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Midlands de l'Ouest</region></placeName></affiliation></author><author><name sortKey="Hawker, Jeremy" sort="Hawker, Jeremy" uniqKey="Hawker J" first="Jeremy" last="Hawker">Jeremy Hawker</name><affiliation wicri:level="3"><nlm:aff id="Aff4">Public Health England, Field Epidemiology Service (Birmingham Office), Birmingham, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Public Health England, Field Epidemiology Service (Birmingham Office), Birmingham</wicri:regionArea><placeName><settlement type="city">Birmingham</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Midlands de l'Ouest</region></placeName></affiliation></author><author><name sortKey="Nair, Satheesh" sort="Nair, Satheesh" uniqKey="Nair S" first="Satheesh" last="Nair">Satheesh Nair</name><affiliation wicri:level="3"><nlm:aff id="Aff3">Public Health England, Colindale, London, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Public Health England, Colindale, London</wicri:regionArea><placeName><settlement type="city">Londres</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Grand Londres</region></placeName></affiliation></author><author><name sortKey="Neal, Keith" sort="Neal, Keith" uniqKey="Neal K" first="Keith" last="Neal">Keith Neal</name><affiliation wicri:level="3"><nlm:aff id="Aff4">Public Health England, Field Epidemiology Service (Birmingham Office), Birmingham, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Public Health England, Field Epidemiology Service (Birmingham Office), Birmingham</wicri:regionArea><placeName><settlement type="city">Birmingham</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Midlands de l'Ouest</region></placeName></affiliation></author><author><name sortKey="Nye, Kathy" sort="Nye, Kathy" uniqKey="Nye K" first="Kathy" last="Nye">Kathy Nye</name><affiliation wicri:level="3"><nlm:aff id="Aff5">Public Health England Birmingham Public Health Laboratory, Heart of England NHS Trust, Birmingham, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Public Health England Birmingham Public Health Laboratory, Heart of England NHS Trust, Birmingham</wicri:regionArea><placeName><settlement type="city">Birmingham</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Midlands de l'Ouest</region></placeName></affiliation></author><author><name sortKey="Peters, Tansy" sort="Peters, Tansy" uniqKey="Peters T" first="Tansy" last="Peters">Tansy Peters</name><affiliation wicri:level="3"><nlm:aff id="Aff3">Public Health England, Colindale, London, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Public Health England, Colindale, London</wicri:regionArea><placeName><settlement type="city">Londres</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Grand Londres</region></placeName></affiliation></author><author><name sortKey="De Pinna, Elizabeth" sort="De Pinna, Elizabeth" uniqKey="De Pinna E" first="Elizabeth" last="De Pinna">Elizabeth De Pinna</name><affiliation wicri:level="3"><nlm:aff id="Aff3">Public Health England, Colindale, London, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Public Health England, Colindale, London</wicri:regionArea><placeName><settlement type="city">Londres</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Grand Londres</region></placeName></affiliation></author><author><name sortKey="Robinson, Esther" sort="Robinson, Esther" uniqKey="Robinson E" first="Esther" last="Robinson">Esther Robinson</name><affiliation wicri:level="1"><nlm:aff id="Aff6">Department of Microbiology, University of Warwick, Warwick, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Department of Microbiology, University of Warwick, Warwick</wicri:regionArea><wicri:noRegion>Warwick</wicri:noRegion></affiliation></author><author><name sortKey="Struthers, Keith" sort="Struthers, Keith" uniqKey="Struthers K" first="Keith" last="Struthers">Keith Struthers</name><affiliation wicri:level="3"><nlm:aff id="Aff5">Public Health England Birmingham Public Health Laboratory, Heart of England NHS Trust, Birmingham, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Public Health England Birmingham Public Health Laboratory, Heart of England NHS Trust, Birmingham</wicri:regionArea><placeName><settlement type="city">Birmingham</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Midlands de l'Ouest</region></placeName></affiliation></author><author><name sortKey="Webber, Mark" sort="Webber, Mark" uniqKey="Webber M" first="Mark" last="Webber">Mark Webber</name><affiliation><nlm:aff id="Aff2">NIHR Surgical Reconstruction and Microbiology Research Centre, University of Birmingham, Birmingham, B15 2TT UK</nlm:aff><wicri:noCountry code="subfield">B15 2TT UK</wicri:noCountry></affiliation></author><author><name sortKey="Catto, Andrew" sort="Catto, Andrew" uniqKey="Catto A" first="Andrew" last="Catto">Andrew Catto</name><affiliation wicri:level="3"><nlm:aff id="Aff7">Medical Directorate, Heart of England NHS Trust, Birmingham, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Medical Directorate, Heart of England NHS Trust, Birmingham</wicri:regionArea><placeName><settlement type="city">Birmingham</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Midlands de l'Ouest</region></placeName></affiliation></author><author><name sortKey="Dallman, Timothy J" sort="Dallman, Timothy J" uniqKey="Dallman T" first="Timothy J." last="Dallman">Timothy J. Dallman</name><affiliation wicri:level="3"><nlm:aff id="Aff3">Public Health England, Colindale, London, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Public Health England, Colindale, London</wicri:regionArea><placeName><settlement type="city">Londres</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Grand Londres</region></placeName></affiliation></author><author><name sortKey="Hawkey, Peter" sort="Hawkey, Peter" uniqKey="Hawkey P" first="Peter" last="Hawkey">Peter Hawkey</name><affiliation><nlm:aff id="Aff1">Institute of Microbiology and Infection, University of Birmingham, Birmingham, B15 2TT UK</nlm:aff><wicri:noCountry code="subfield">B15 2TT UK</wicri:noCountry></affiliation><affiliation wicri:level="3"><nlm:aff id="Aff5">Public Health England Birmingham Public Health Laboratory, Heart of England NHS Trust, Birmingham, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Public Health England Birmingham Public Health Laboratory, Heart of England NHS Trust, Birmingham</wicri:regionArea><placeName><settlement type="city">Birmingham</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Midlands de l'Ouest</region></placeName></affiliation></author><author><name sortKey="Loman, Nicholas J" sort="Loman, Nicholas J" uniqKey="Loman N" first="Nicholas J." last="Loman">Nicholas J. Loman</name><affiliation><nlm:aff id="Aff1">Institute of Microbiology and Infection, University of Birmingham, Birmingham, B15 2TT UK</nlm:aff><wicri:noCountry code="subfield">B15 2TT UK</wicri:noCountry></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">26025440</idno><idno type="pmc">4702336</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4702336</idno><idno type="RBID">PMC:4702336</idno><idno type="doi">10.1186/s13059-015-0677-2</idno><date when="2015">2015</date><idno type="wicri:Area/Pmc/Corpus">000180</idno><idno type="wicri:Area/Pmc/Curation">000180</idno><idno type="wicri:Area/Pmc/Checkpoint">000073</idno><idno type="wicri:Area/Ncbi/Merge">000641</idno><idno type="wicri:Area/Ncbi/Curation">000641</idno><idno type="wicri:Area/Ncbi/Checkpoint">000641</idno><idno type="wicri:doubleKey">1474-7596:2015:Quick J:rapid:draft:sequencing</idno><idno type="wicri:Area/Main/Merge">000079</idno><idno type="wicri:Area/Main/Curation">000079</idno><idno type="wicri:Area/Main/Exploration">000079</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Rapid draft sequencing and real-time nanopore sequencing in a hospital outbreak of <italic>Salmonella</italic></title><author><name sortKey="Quick, Joshua" sort="Quick, Joshua" uniqKey="Quick J" first="Joshua" last="Quick">Joshua Quick</name><affiliation><nlm:aff id="Aff1">Institute of Microbiology and Infection, University of Birmingham, Birmingham, B15 2TT UK</nlm:aff><wicri:noCountry code="subfield">B15 2TT UK</wicri:noCountry></affiliation><affiliation><nlm:aff id="Aff2">NIHR Surgical Reconstruction and Microbiology Research Centre, University of Birmingham, Birmingham, B15 2TT UK</nlm:aff><wicri:noCountry code="subfield">B15 2TT UK</wicri:noCountry></affiliation></author><author><name sortKey="Ashton, Philip" sort="Ashton, Philip" uniqKey="Ashton P" first="Philip" last="Ashton">Philip Ashton</name><affiliation wicri:level="3"><nlm:aff id="Aff3">Public Health England, Colindale, London, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Public Health England, Colindale, London</wicri:regionArea><placeName><settlement type="city">Londres</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Grand Londres</region></placeName></affiliation></author><author><name sortKey="Calus, Szymon" sort="Calus, Szymon" uniqKey="Calus S" first="Szymon" last="Calus">Szymon Calus</name><affiliation><nlm:aff id="Aff1">Institute of Microbiology and Infection, University of Birmingham, Birmingham, B15 2TT UK</nlm:aff><wicri:noCountry code="subfield">B15 2TT UK</wicri:noCountry></affiliation><affiliation><nlm:aff id="Aff2">NIHR Surgical Reconstruction and Microbiology Research Centre, University of Birmingham, Birmingham, B15 2TT UK</nlm:aff><wicri:noCountry code="subfield">B15 2TT UK</wicri:noCountry></affiliation></author><author><name sortKey="Chatt, Carole" sort="Chatt, Carole" uniqKey="Chatt C" first="Carole" last="Chatt">Carole Chatt</name><affiliation wicri:level="3"><nlm:aff id="Aff4">Public Health England, Field Epidemiology Service (Birmingham Office), Birmingham, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Public Health England, Field Epidemiology Service (Birmingham Office), Birmingham</wicri:regionArea><placeName><settlement type="city">Birmingham</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Midlands de l'Ouest</region></placeName></affiliation></author><author><name sortKey="Gossain, Savita" sort="Gossain, Savita" uniqKey="Gossain S" first="Savita" last="Gossain">Savita Gossain</name><affiliation wicri:level="3"><nlm:aff id="Aff5">Public Health England Birmingham Public Health Laboratory, Heart of England NHS Trust, Birmingham, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Public Health England Birmingham Public Health Laboratory, Heart of England NHS Trust, Birmingham</wicri:regionArea><placeName><settlement type="city">Birmingham</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Midlands de l'Ouest</region></placeName></affiliation></author><author><name sortKey="Hawker, Jeremy" sort="Hawker, Jeremy" uniqKey="Hawker J" first="Jeremy" last="Hawker">Jeremy Hawker</name><affiliation wicri:level="3"><nlm:aff id="Aff4">Public Health England, Field Epidemiology Service (Birmingham Office), Birmingham, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Public Health England, Field Epidemiology Service (Birmingham Office), Birmingham</wicri:regionArea><placeName><settlement type="city">Birmingham</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Midlands de l'Ouest</region></placeName></affiliation></author><author><name sortKey="Nair, Satheesh" sort="Nair, Satheesh" uniqKey="Nair S" first="Satheesh" last="Nair">Satheesh Nair</name><affiliation wicri:level="3"><nlm:aff id="Aff3">Public Health England, Colindale, London, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Public Health England, Colindale, London</wicri:regionArea><placeName><settlement type="city">Londres</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Grand Londres</region></placeName></affiliation></author><author><name sortKey="Neal, Keith" sort="Neal, Keith" uniqKey="Neal K" first="Keith" last="Neal">Keith Neal</name><affiliation wicri:level="3"><nlm:aff id="Aff4">Public Health England, Field Epidemiology Service (Birmingham Office), Birmingham, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Public Health England, Field Epidemiology Service (Birmingham Office), Birmingham</wicri:regionArea><placeName><settlement type="city">Birmingham</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Midlands de l'Ouest</region></placeName></affiliation></author><author><name sortKey="Nye, Kathy" sort="Nye, Kathy" uniqKey="Nye K" first="Kathy" last="Nye">Kathy Nye</name><affiliation wicri:level="3"><nlm:aff id="Aff5">Public Health England Birmingham Public Health Laboratory, Heart of England NHS Trust, Birmingham, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Public Health England Birmingham Public Health Laboratory, Heart of England NHS Trust, Birmingham</wicri:regionArea><placeName><settlement type="city">Birmingham</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Midlands de l'Ouest</region></placeName></affiliation></author><author><name sortKey="Peters, Tansy" sort="Peters, Tansy" uniqKey="Peters T" first="Tansy" last="Peters">Tansy Peters</name><affiliation wicri:level="3"><nlm:aff id="Aff3">Public Health England, Colindale, London, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Public Health England, Colindale, London</wicri:regionArea><placeName><settlement type="city">Londres</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Grand Londres</region></placeName></affiliation></author><author><name sortKey="De Pinna, Elizabeth" sort="De Pinna, Elizabeth" uniqKey="De Pinna E" first="Elizabeth" last="De Pinna">Elizabeth De Pinna</name><affiliation wicri:level="3"><nlm:aff id="Aff3">Public Health England, Colindale, London, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Public Health England, Colindale, London</wicri:regionArea><placeName><settlement type="city">Londres</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Grand Londres</region></placeName></affiliation></author><author><name sortKey="Robinson, Esther" sort="Robinson, Esther" uniqKey="Robinson E" first="Esther" last="Robinson">Esther Robinson</name><affiliation wicri:level="1"><nlm:aff id="Aff6">Department of Microbiology, University of Warwick, Warwick, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Department of Microbiology, University of Warwick, Warwick</wicri:regionArea><wicri:noRegion>Warwick</wicri:noRegion></affiliation></author><author><name sortKey="Struthers, Keith" sort="Struthers, Keith" uniqKey="Struthers K" first="Keith" last="Struthers">Keith Struthers</name><affiliation wicri:level="3"><nlm:aff id="Aff5">Public Health England Birmingham Public Health Laboratory, Heart of England NHS Trust, Birmingham, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Public Health England Birmingham Public Health Laboratory, Heart of England NHS Trust, Birmingham</wicri:regionArea><placeName><settlement type="city">Birmingham</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Midlands de l'Ouest</region></placeName></affiliation></author><author><name sortKey="Webber, Mark" sort="Webber, Mark" uniqKey="Webber M" first="Mark" last="Webber">Mark Webber</name><affiliation><nlm:aff id="Aff2">NIHR Surgical Reconstruction and Microbiology Research Centre, University of Birmingham, Birmingham, B15 2TT UK</nlm:aff><wicri:noCountry code="subfield">B15 2TT UK</wicri:noCountry></affiliation></author><author><name sortKey="Catto, Andrew" sort="Catto, Andrew" uniqKey="Catto A" first="Andrew" last="Catto">Andrew Catto</name><affiliation wicri:level="3"><nlm:aff id="Aff7">Medical Directorate, Heart of England NHS Trust, Birmingham, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Medical Directorate, Heart of England NHS Trust, Birmingham</wicri:regionArea><placeName><settlement type="city">Birmingham</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Midlands de l'Ouest</region></placeName></affiliation></author><author><name sortKey="Dallman, Timothy J" sort="Dallman, Timothy J" uniqKey="Dallman T" first="Timothy J." last="Dallman">Timothy J. Dallman</name><affiliation wicri:level="3"><nlm:aff id="Aff3">Public Health England, Colindale, London, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Public Health England, Colindale, London</wicri:regionArea><placeName><settlement type="city">Londres</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Grand Londres</region></placeName></affiliation></author><author><name sortKey="Hawkey, Peter" sort="Hawkey, Peter" uniqKey="Hawkey P" first="Peter" last="Hawkey">Peter Hawkey</name><affiliation><nlm:aff id="Aff1">Institute of Microbiology and Infection, University of Birmingham, Birmingham, B15 2TT UK</nlm:aff><wicri:noCountry code="subfield">B15 2TT UK</wicri:noCountry></affiliation><affiliation wicri:level="3"><nlm:aff id="Aff5">Public Health England Birmingham Public Health Laboratory, Heart of England NHS Trust, Birmingham, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Public Health England Birmingham Public Health Laboratory, Heart of England NHS Trust, Birmingham</wicri:regionArea><placeName><settlement type="city">Birmingham</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Midlands de l'Ouest</region></placeName></affiliation></author><author><name sortKey="Loman, Nicholas J" sort="Loman, Nicholas J" uniqKey="Loman N" first="Nicholas J." last="Loman">Nicholas J. Loman</name><affiliation><nlm:aff id="Aff1">Institute of Microbiology and Infection, University of Birmingham, Birmingham, B15 2TT UK</nlm:aff><wicri:noCountry code="subfield">B15 2TT UK</wicri:noCountry></affiliation></author></analytic><series><title level="j">Genome Biology</title><idno type="ISSN">1474-7596</idno><idno type="eISSN">1474-760X</idno><imprint><date when="2015">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec><title>Background</title><p>Foodborne outbreaks of <italic>Salmonella</italic> remain a pressing public health concern. We recently detected a large outbreak of <italic>Salmonella enterica</italic> serovar Enteritidis phage type 14b affecting more than 30 patients in our hospital. This outbreak was linked to community, national and European-wide cases. Hospital patients with <italic>Salmonella</italic> are at high risk, and require a rapid response. We initially investigated this outbreak by whole-genome sequencing using a novel rapid protocol on the Illumina MiSeq; we then integrated these data with whole-genome data from surveillance sequencing, thereby placing the outbreak in a national context. Additionally, we investigated the potential of a newly released sequencing technology, the MinION from Oxford Nanopore Technologies, in the management of a hospital outbreak of <italic>Salmonella</italic>.</p></sec><sec><title>Results</title><p>We demonstrate that rapid MiSeq sequencing can reduce the time to answer compared to the standard sequencing protocol with no impact on the results. We show, for the first time, that the MinION can acquire clinically relevant information in real time and within minutes of a DNA library being loaded. MinION sequencing permits confident assignment to species level within 20 min. Using a novel streaming phylogenetic placement method samples can be assigned to a serotype in 40 min and determined to be part of the outbreak in less than 2 h.</p></sec><sec><title>Conclusions</title><p>Both approaches yielded reliable and actionable clinical information on the <italic>Salmonella</italic> outbreak in less than half a day. The rapid availability of such information may facilitate more informed epidemiological investigations and influence infection control practices.</p></sec><sec><title>Electronic supplementary material</title><p>The online version of this article (doi:10.1186/s13059-015-0677-2) contains supplementary material, which is available to authorized users.</p></sec></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Scallan, E" uniqKey="Scallan E">E Scallan</name></author><author><name sortKey="Hoekstra, Rm" uniqKey="Hoekstra R">RM Hoekstra</name></author><author><name sortKey="Angulo, Fj" uniqKey="Angulo F">FJ Angulo</name></author><author><name sortKey="Tauxe, Rv" uniqKey="Tauxe R">RV Tauxe</name></author><author><name sortKey="Widdowson, M A" uniqKey="Widdowson M">M-A Widdowson</name></author><author><name sortKey="Roy, Sl" uniqKey="Roy S">SL Roy</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="O Rien, Sj" 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Loman</name><name sortKey="Quick, Joshua" sort="Quick, Joshua" uniqKey="Quick J" first="Joshua" last="Quick">Joshua Quick</name><name sortKey="Webber, Mark" sort="Webber, Mark" uniqKey="Webber M" first="Mark" last="Webber">Mark Webber</name></noCountry><country name="Royaume-Uni"><region name="Angleterre"><name sortKey="Ashton, Philip" sort="Ashton, Philip" uniqKey="Ashton P" first="Philip" last="Ashton">Philip Ashton</name></region><name sortKey="Catto, Andrew" sort="Catto, Andrew" uniqKey="Catto A" first="Andrew" last="Catto">Andrew Catto</name><name sortKey="Chatt, Carole" sort="Chatt, Carole" uniqKey="Chatt C" first="Carole" last="Chatt">Carole Chatt</name><name sortKey="Dallman, Timothy J" sort="Dallman, Timothy J" uniqKey="Dallman T" first="Timothy J." last="Dallman">Timothy J. Dallman</name><name sortKey="De Pinna, Elizabeth" sort="De Pinna, Elizabeth" uniqKey="De Pinna E" first="Elizabeth" last="De Pinna">Elizabeth De Pinna</name><name sortKey="Gossain, Savita" sort="Gossain, Savita" uniqKey="Gossain S" first="Savita" last="Gossain">Savita Gossain</name><name sortKey="Hawker, Jeremy" sort="Hawker, Jeremy" uniqKey="Hawker J" first="Jeremy" last="Hawker">Jeremy Hawker</name><name sortKey="Hawkey, Peter" sort="Hawkey, Peter" uniqKey="Hawkey P" first="Peter" last="Hawkey">Peter Hawkey</name><name sortKey="Nair, Satheesh" sort="Nair, Satheesh" uniqKey="Nair S" first="Satheesh" last="Nair">Satheesh Nair</name><name sortKey="Neal, Keith" sort="Neal, Keith" uniqKey="Neal K" first="Keith" last="Neal">Keith Neal</name><name sortKey="Nye, Kathy" sort="Nye, Kathy" uniqKey="Nye K" first="Kathy" last="Nye">Kathy Nye</name><name sortKey="Peters, Tansy" sort="Peters, Tansy" uniqKey="Peters T" first="Tansy" last="Peters">Tansy Peters</name><name sortKey="Robinson, Esther" sort="Robinson, Esther" uniqKey="Robinson E" first="Esther" last="Robinson">Esther Robinson</name><name sortKey="Struthers, Keith" sort="Struthers, Keith" uniqKey="Struthers K" first="Keith" last="Struthers">Keith Struthers</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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