Immune Signature Against Plasmodium falciparum Antigens Predicts Clinical Immunity in Distinct Malaria Endemic Communities*
Identifieur interne : 000B46 ( Ncbi/Merge ); précédent : 000B45; suivant : 000B47Immune Signature Against Plasmodium falciparum Antigens Predicts Clinical Immunity in Distinct Malaria Endemic Communities*
Auteurs : Carla Proietti [Australie] ; Lutz Krause [Australie] ; Angela Trieu [Australie] ; Daniel Dodoo [Ghana] ; Ben Gyan [Ghana] ; Kwadwo A. Koram [Ghana] ; William O. Rogers ; Thomas L. Richie ; Peter D. Crompton [États-Unis] ; Philip L. Felgner [États-Unis] ; Denise L. Doolan [Australie]Source :
- Molecular & Cellular Proteomics : MCP [ 1535-9476 ] ; 2019.
Abstract
We have established a predictive modelling framework to systematically analyze IgG antibody responses against a large panel of
Url:
DOI: 10.1074/mcp.RA118.001256
PubMed: 31658979
PubMed Central: 6944240
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Richie</name><affiliation><nlm:aff id="aff5">Naval Medical Research Center, Silver Spring Maryland</nlm:aff><wicri:noCountry code="subfield">Silver Spring Maryland</wicri:noCountry></affiliation></author><author><name sortKey="Crompton, Peter D" sort="Crompton, Peter D" uniqKey="Crompton P" first="Peter D." last="Crompton">Peter D. Crompton</name><affiliation wicri:level="2"><nlm:aff id="aff6">Malaria Infection Biology and Immunity Section, Laboratory of Immunogenetics, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Maryland</region></placeName><wicri:cityArea>Malaria Infection Biology and Immunity Section, Laboratory of Immunogenetics, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville</wicri:cityArea></affiliation></author><author><name sortKey="Felgner, Philip L" sort="Felgner, Philip L" uniqKey="Felgner P" first="Philip L." last="Felgner">Philip L. Felgner</name><affiliation wicri:level="2"><nlm:aff id="aff7">Department of Medicine, Division of Infectious Diseases, University of California Irvine, Irvine, California</nlm:aff><country>États-Unis</country><placeName><region type="state">Californie</region></placeName><wicri:cityArea>Department of Medicine, Division of Infectious Diseases, University of California Irvine, Irvine</wicri:cityArea></affiliation></author><author><name sortKey="Doolan, Denise L" sort="Doolan, Denise L" uniqKey="Doolan D" first="Denise L." last="Doolan">Denise L. Doolan</name><affiliation wicri:level="1"><nlm:aff id="aff1">Centre for Molecular Therapeutics, Australian Institute of Tropical Health and Medicine, James Cook University, Cairns, QLD, Australia</nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Centre for Molecular Therapeutics, Australian Institute of Tropical Health and Medicine, James Cook University, Cairns, QLD</wicri:regionArea><wicri:noRegion>QLD</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="aff2">QIMR Berghofer Medical Research Institute, Brisbane, QLD, Australia</nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>QIMR Berghofer Medical Research Institute, Brisbane, QLD</wicri:regionArea><wicri:noRegion>QLD</wicri:noRegion></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">31658979</idno><idno type="pmc">6944240</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6944240</idno><idno 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sort="Proietti, Carla" uniqKey="Proietti C" first="Carla" last="Proietti">Carla Proietti</name><affiliation wicri:level="1"><nlm:aff id="aff1">Centre for Molecular Therapeutics, Australian Institute of Tropical Health and Medicine, James Cook University, Cairns, QLD, Australia</nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Centre for Molecular Therapeutics, Australian Institute of Tropical Health and Medicine, James Cook University, Cairns, QLD</wicri:regionArea><wicri:noRegion>QLD</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="aff2">QIMR Berghofer Medical Research Institute, Brisbane, QLD, Australia</nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>QIMR Berghofer Medical Research Institute, Brisbane, QLD</wicri:regionArea><wicri:noRegion>QLD</wicri:noRegion></affiliation></author><author><name sortKey="Krause, Lutz" sort="Krause, Lutz" uniqKey="Krause L" first="Lutz" last="Krause">Lutz Krause</name><affiliation wicri:level="1"><nlm:aff id="aff3">The University of Queensland Diamantina Institute, Brisbane, QLD, Australia</nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>The University of Queensland Diamantina Institute, Brisbane, QLD</wicri:regionArea><wicri:noRegion>QLD</wicri:noRegion></affiliation></author><author><name sortKey="Trieu, Angela" sort="Trieu, Angela" uniqKey="Trieu A" first="Angela" last="Trieu">Angela Trieu</name><affiliation wicri:level="1"><nlm:aff id="aff1">Centre for Molecular Therapeutics, Australian Institute of Tropical Health and Medicine, James Cook University, Cairns, QLD, Australia</nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Centre for Molecular Therapeutics, Australian Institute of Tropical Health and Medicine, James Cook University, Cairns, QLD</wicri:regionArea><wicri:noRegion>QLD</wicri:noRegion></affiliation></author><author><name sortKey="Dodoo, Daniel" sort="Dodoo, Daniel" uniqKey="Dodoo D" first="Daniel" last="Dodoo">Daniel Dodoo</name><affiliation wicri:level="4"><nlm:aff id="aff4">Noguchi Memorial Institute for Medical Research, University of Ghana, Ghana</nlm:aff><country xml:lang="fr">Ghana</country><wicri:regionArea>Noguchi Memorial Institute for Medical Research, University of Ghana</wicri:regionArea><placeName><settlement type="city">Accra</settlement><settlement type="town">Legon (Ghana)</settlement><region type="region">Région du Grand Accra</region></placeName><orgName type="university">Université du Ghana</orgName></affiliation></author><author><name sortKey="Gyan, Ben" sort="Gyan, Ben" uniqKey="Gyan B" first="Ben" last="Gyan">Ben Gyan</name><affiliation wicri:level="4"><nlm:aff id="aff4">Noguchi Memorial Institute for Medical Research, University of Ghana, Ghana</nlm:aff><country xml:lang="fr">Ghana</country><wicri:regionArea>Noguchi Memorial Institute for Medical Research, University of Ghana</wicri:regionArea><placeName><settlement type="city">Accra</settlement><settlement type="town">Legon (Ghana)</settlement><region type="region">Région du Grand Accra</region></placeName><orgName type="university">Université du Ghana</orgName></affiliation></author><author><name sortKey="Koram, Kwadwo A" sort="Koram, Kwadwo A" uniqKey="Koram K" first="Kwadwo A." last="Koram">Kwadwo A. Koram</name><affiliation wicri:level="4"><nlm:aff id="aff4">Noguchi Memorial Institute for Medical Research, University of Ghana, Ghana</nlm:aff><country xml:lang="fr">Ghana</country><wicri:regionArea>Noguchi Memorial Institute for Medical Research, University of Ghana</wicri:regionArea><placeName><settlement type="city">Accra</settlement><settlement type="town">Legon (Ghana)</settlement><region type="region">Région du Grand Accra</region></placeName><orgName type="university">Université du Ghana</orgName></affiliation></author><author><name sortKey="Rogers, William O" sort="Rogers, William O" uniqKey="Rogers W" first="William O." last="Rogers">William O. Rogers</name><affiliation><nlm:aff id="aff5">Naval Medical Research Center, Silver Spring Maryland</nlm:aff><wicri:noCountry code="subfield">Silver Spring Maryland</wicri:noCountry></affiliation></author><author><name sortKey="Richie, Thomas L" sort="Richie, Thomas L" uniqKey="Richie T" first="Thomas L." last="Richie">Thomas L. Richie</name><affiliation><nlm:aff id="aff5">Naval Medical Research Center, Silver Spring Maryland</nlm:aff><wicri:noCountry code="subfield">Silver Spring Maryland</wicri:noCountry></affiliation></author><author><name sortKey="Crompton, Peter D" sort="Crompton, Peter D" uniqKey="Crompton P" first="Peter D." last="Crompton">Peter D. Crompton</name><affiliation wicri:level="2"><nlm:aff id="aff6">Malaria Infection Biology and Immunity Section, Laboratory of Immunogenetics, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Maryland</region></placeName><wicri:cityArea>Malaria Infection Biology and Immunity Section, Laboratory of Immunogenetics, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville</wicri:cityArea></affiliation></author><author><name sortKey="Felgner, Philip L" sort="Felgner, Philip L" uniqKey="Felgner P" first="Philip L." last="Felgner">Philip L. Felgner</name><affiliation wicri:level="2"><nlm:aff id="aff7">Department of Medicine, Division of Infectious Diseases, University of California Irvine, Irvine, California</nlm:aff><country>États-Unis</country><placeName><region type="state">Californie</region></placeName><wicri:cityArea>Department of Medicine, Division of Infectious Diseases, University of California Irvine, Irvine</wicri:cityArea></affiliation></author><author><name sortKey="Doolan, Denise L" sort="Doolan, Denise L" uniqKey="Doolan D" first="Denise L." last="Doolan">Denise L. Doolan</name><affiliation wicri:level="1"><nlm:aff id="aff1">Centre for Molecular Therapeutics, Australian Institute of Tropical Health and Medicine, James Cook University, Cairns, QLD, Australia</nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Centre for Molecular Therapeutics, Australian Institute of Tropical Health and Medicine, James Cook University, Cairns, QLD</wicri:regionArea><wicri:noRegion>QLD</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="aff2">QIMR Berghofer Medical Research Institute, Brisbane, QLD, Australia</nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>QIMR Berghofer Medical Research Institute, Brisbane, QLD</wicri:regionArea><wicri:noRegion>QLD</wicri:noRegion></affiliation></author></analytic><series><title level="j">Molecular & Cellular Proteomics : MCP</title><idno type="ISSN">1535-9476</idno><idno type="eISSN">1535-9484</idno><imprint><date when="2019">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>We have established a predictive modelling framework to systematically analyze IgG antibody responses against a large panel of <italic>P. falciparum</italic>-specific antigens and identify a predictive signature of naturally acquired immunity to malaria. Our results show that an individual's immune status can be accurately predicted by measuring IgG antibody responses to a parsimonious set of 15 target antigens. The identified immune signature is highly versatile and capable of providing precise and accurate estimates of clinical protection from malaria in demographically distinct populations.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Cohen, S" uniqKey="Cohen S">S. Cohen</name></author><author><name sortKey="Mcgregor, I A" uniqKey="Mcgregor I">I. A. McGregor</name></author><author><name sortKey="Carrington, S" uniqKey="Carrington S">S. Carrington</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Osier, F H" uniqKey="Osier F">F. H. Osier</name></author><author><name sortKey="Fegan, G" uniqKey="Fegan G">G. Fegan</name></author><author><name sortKey="Polley, S D" uniqKey="Polley S">S. D. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Mol Cell Proteomics</journal-id><journal-id journal-id-type="iso-abbrev">Mol. Cell Proteomics</journal-id><journal-id journal-id-type="hwp">mcprot</journal-id><journal-id journal-id-type="pmc">mcprot</journal-id><journal-id journal-id-type="publisher-id">MCP</journal-id><journal-title-group><journal-title>Molecular & Cellular Proteomics : MCP</journal-title></journal-title-group><issn pub-type="ppub">1535-9476</issn><issn pub-type="epub">1535-9484</issn><publisher><publisher-name>The American Society for Biochemistry and Molecular Biology</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">31658979</article-id><article-id pub-id-type="pmc">6944240</article-id><article-id pub-id-type="publisher-id">RA118.001256</article-id><article-id pub-id-type="doi">10.1074/mcp.RA118.001256</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research</subject></subj-group></article-categories><title-group><article-title>Immune Signature Against <italic>Plasmodium falciparum</italic> Antigens Predicts Clinical Immunity in Distinct Malaria Endemic Communities<xref ref-type="fn" rid="FN1">*</xref><xref ref-type="fn" rid="FN2"><sup><inline-graphic xlink:href="sbox.jpg"></inline-graphic></sup></xref></article-title><alt-title alt-title-type="short">Immune Signature Predicts Clinical Immunity to Malaria</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Proietti</surname><given-names>Carla</given-names></name><xref ref-type="aff" rid="aff1">‡</xref><xref ref-type="aff" rid="aff2">§</xref><xref ref-type="author-notes" rid="FN3">‖‖</xref></contrib><contrib contrib-type="author"><name><surname>Krause</surname><given-names>Lutz</given-names></name><xref ref-type="aff" rid="aff3">¶</xref><xref ref-type="author-notes" rid="FN3">‖‖</xref></contrib><contrib contrib-type="author"><name><surname>Trieu</surname><given-names>Angela</given-names></name><xref ref-type="aff" rid="aff1">‡</xref><xref ref-type="author-notes" rid="FN3">‖‖</xref></contrib><contrib contrib-type="author"><name><surname>Dodoo</surname><given-names>Daniel</given-names></name><xref ref-type="aff" rid="aff4">‖</xref></contrib><contrib contrib-type="author"><name><surname>Gyan</surname><given-names>Ben</given-names></name><xref ref-type="aff" rid="aff4">‖</xref></contrib><contrib contrib-type="author"><name><surname>Koram</surname><given-names>Kwadwo A.</given-names></name><xref ref-type="aff" rid="aff4">‖</xref></contrib><contrib contrib-type="author"><name><surname>Rogers</surname><given-names>William O.</given-names></name><xref ref-type="aff" rid="aff5">**</xref></contrib><contrib contrib-type="author"><name><surname>Richie</surname><given-names>Thomas L.</given-names></name><xref ref-type="aff" rid="aff5">**</xref></contrib><contrib contrib-type="author"><name><surname>Crompton</surname><given-names>Peter D.</given-names></name><xref ref-type="aff" rid="aff6">‡‡</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0002-4117-8505</contrib-id><name><surname>Felgner</surname><given-names>Philip L.</given-names></name><xref ref-type="aff" rid="aff7">§§</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0001-7354-8817</contrib-id><name><surname>Doolan</surname><given-names>Denise L.</given-names></name><xref ref-type="aff" rid="aff1">‡</xref><xref ref-type="aff" rid="aff2">§</xref><xref ref-type="corresp" rid="cor1">¶¶</xref></contrib><aff id="aff1"><label>‡</label>Centre for Molecular Therapeutics, Australian Institute of Tropical Health and Medicine, James Cook University, Cairns, QLD, Australia</aff><aff id="aff2"><label>§</label>QIMR Berghofer Medical Research Institute, Brisbane, QLD, Australia</aff><aff id="aff3"><label>¶</label>The University of Queensland Diamantina Institute, Brisbane, QLD, Australia</aff><aff id="aff4"><label>‖</label>Noguchi Memorial Institute for Medical Research, University of Ghana, Ghana</aff><aff id="aff5"><label>**</label>Naval Medical Research Center, Silver Spring Maryland</aff><aff id="aff6"><label>‡‡</label>Malaria Infection Biology and Immunity Section, Laboratory of Immunogenetics, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland</aff><aff id="aff7"><label>§§</label>Department of Medicine, Division of Infectious Diseases, University of California Irvine, Irvine, California</aff></contrib-group><author-notes><corresp id="cor1">¶¶ To whom correspondence should be addressed:
<addr-line>Centre for Molecular Therapeutics, Australian Institute of Tropical Health and Medicine, James Cook University, Cairns, QLD, Australia.</addr-line> E-mail:
<email>denise.doolan@jcu.edu.au</email>.</corresp><fn fn-type="equal" id="FN3"><p>‖‖ These authors contributed equally to this work.</p></fn><fn fn-type="con"><p>Author contributions: C.P., A.T., D.D., B.G., K.A.K., and W.O.R. performed research; C.P., L.K., A.T., K.A.K., W.O.R., T.L.R., P.C., P.F., and D.L.D. analyzed data; C.P., L.K., A.T., D.D., B.G., K.A.K., W.O.R., T.L.R., P.C., P.F., and D.L.D. wrote the paper; K.A.K., W.O.R., P.L.F., and D.L.D. designed research.</p></fn></author-notes><pub-date pub-type="ppub"><month>1</month><year>2020</year></pub-date><pub-date pub-type="epub"><day>28</day><month>10</month><year>2019</year></pub-date><pub-date pub-type="pmc-release"><day>28</day><month>10</month><year>2019</year></pub-date><pmc-comment> PMC Release delay is 0 months and 0 days and was based on the
<volume>19</volume><issue>1</issue><fpage>101</fpage><lpage>113</lpage><history><date date-type="received"><day>3</day><month>12</month><year>2018</year></date><date date-type="rev-recd"><day>23</day><month>10</month><year>2019</year></date></history><permissions><copyright-statement>© 2020 Proietti et al.</copyright-statement><copyright-year>2020</copyright-year><copyright-holder>Proietti et al.</copyright-holder><license license-type="open-access"><license-p><italic>Author's Choice</italic>—Final version open access under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0">Creative Commons CC-BY license</ext-link>.</license-p></license></permissions><self-uri content-type="pdf" xlink:href="zjw001206059100.pdf"></self-uri><abstract abstract-type="precis"><p>We have established a predictive modelling framework to systematically analyze IgG antibody responses against a large panel of <italic>P. falciparum</italic>-specific antigens and identify a predictive signature of naturally acquired immunity to malaria. Our results show that an individual's immune status can be accurately predicted by measuring IgG antibody responses to a parsimonious set of 15 target antigens. The identified immune signature is highly versatile and capable of providing precise and accurate estimates of clinical protection from malaria in demographically distinct populations.</p></abstract><abstract abstract-type="graphical"><title>Graphical Abstract</title><p><fig id="F7" fig-type="featured" orientation="portrait" position="float"><graphic xlink:href="zjw0012060590007"></graphic></fig></p><p><bold>Highlights</bold></p><p><list list-type="bullet"><list-item><p>A predictive modelling framework has been established to analyze IgG antibody responses against a large panel of <italic>P. falciparum</italic>-specific antigens to identify a specific antigen signature of NAI.</p></list-item><list-item><p>An individual's immune status can be accurately predicted by measuring IgG responses against a small set of 15 defined parasite antigens.</p></list-item><list-item><p>Proteins identified in the 15-antigen signature represent potential candidates for next-generation malaria vaccines or biomarkers for monitoring the impact of malaria interventions.</p></list-item><list-item><p>The developed predictive framework can be adapted for developing novel surveillance and intervention tools for other infectious diseases.</p></list-item></list></p></abstract><abstract><p>A large body of evidence supports the role of antibodies directed against the <italic>Plasmodium spp.</italic> parasite in the development of naturally acquired immunity to malaria, however an antigen signature capable of predicting protective immunity against <italic>Plasmodium</italic> remains to be identified. Key challenges for the identification of a predictive immune signature include the high dimensionality of data produced by high-throughput technologies and the limitation of standard statistical tests in accounting for synergetic interactions between immune responses to multiple targets. In this study, using samples collected from young children in Ghana at multiple time points during a longitudinal study, we adapted a predictive modeling framework which combines feature selection and machine learning techniques to identify an antigen signature of clinical immunity to malaria. Our results show that an individual's immune status can be accurately predicted by measuring antibody responses to a small defined set of 15 target antigens. We further demonstrate that the identified immune signature is highly versatile and capable of providing precise and accurate estimates of clinical protection from malaria in an independent geographic community. Our findings pave the way for the development of a robust point-of-care test to identify individuals at high risk of disease and which could be applied to monitor the impact of vaccinations and other interventions. This approach could be also translated to biomarker discovery for other infectious diseases.</p></abstract><kwd-group><kwd>Biomarker: diagnostic</kwd><kwd>malaria</kwd><kwd>immunology</kwd><kwd>clinical data</kwd><kwd>modeling</kwd><kwd>antigen signature</kwd><kwd>feature selection</kwd><kwd>machine learning</kwd><kwd>Plasmodium falciparum</kwd><kwd>protein microarray</kwd></kwd-group><funding-group><award-group id="award1"><funding-source><institution-wrap><institution>Department of Health | National Health and Medical Research Council (NHMRC)
</institution><institution-id institution-id-type="open-funder-registry">10.13039/501100000925</institution-id></institution-wrap></funding-source><award-id>552423 1037304</award-id><principal-award-recipient><name><surname>Doolan</surname><given-names>Denise</given-names></name></principal-award-recipient></award-group></funding-group></article-meta></front></pmc><affiliations><list><country><li>Australie</li><li>Ghana</li><li>États-Unis</li></country><region><li>Californie</li><li>Maryland</li><li>Région du Grand Accra</li></region><settlement><li>Accra</li><li>Legon (Ghana)</li></settlement><orgName><li>Université du Ghana</li></orgName></list><tree><noCountry><name sortKey="Richie, Thomas L" sort="Richie, Thomas L" uniqKey="Richie T" first="Thomas L." last="Richie">Thomas L. Richie</name><name sortKey="Rogers, William O" sort="Rogers, William O" uniqKey="Rogers W" first="William O." last="Rogers">William O. Rogers</name></noCountry><country name="Australie"><noRegion><name sortKey="Proietti, Carla" sort="Proietti, Carla" uniqKey="Proietti C" first="Carla" last="Proietti">Carla Proietti</name></noRegion><name sortKey="Doolan, Denise L" sort="Doolan, Denise L" uniqKey="Doolan D" first="Denise L." last="Doolan">Denise L. Doolan</name><name sortKey="Doolan, Denise L" sort="Doolan, Denise L" uniqKey="Doolan D" first="Denise L." last="Doolan">Denise L. Doolan</name><name sortKey="Krause, Lutz" sort="Krause, Lutz" uniqKey="Krause L" first="Lutz" last="Krause">Lutz Krause</name><name sortKey="Proietti, Carla" sort="Proietti, Carla" uniqKey="Proietti C" first="Carla" last="Proietti">Carla Proietti</name><name sortKey="Trieu, Angela" sort="Trieu, Angela" uniqKey="Trieu A" first="Angela" last="Trieu">Angela Trieu</name></country><country name="Ghana"><region name="Région du Grand Accra"><name sortKey="Dodoo, Daniel" sort="Dodoo, Daniel" uniqKey="Dodoo D" first="Daniel" last="Dodoo">Daniel Dodoo</name></region><name sortKey="Gyan, Ben" sort="Gyan, Ben" uniqKey="Gyan B" first="Ben" last="Gyan">Ben Gyan</name><name sortKey="Koram, Kwadwo A" sort="Koram, Kwadwo A" uniqKey="Koram K" first="Kwadwo A." last="Koram">Kwadwo A. Koram</name></country><country name="États-Unis"><region name="Maryland"><name sortKey="Crompton, Peter D" sort="Crompton, Peter D" uniqKey="Crompton P" first="Peter D." last="Crompton">Peter D. Crompton</name></region><name sortKey="Felgner, Philip L" sort="Felgner, Philip L" uniqKey="Felgner P" first="Philip L." last="Felgner">Philip L. Felgner</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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