Transmission of a 2009 H1N1 Pandemic Influenza Virus Occurs before Fever Is Detected, in the Ferret Model
Identifieur interne : 000D49 ( Pmc/Curation ); précédent : 000D48; suivant : 000D50Transmission of a 2009 H1N1 Pandemic Influenza Virus Occurs before Fever Is Detected, in the Ferret Model
Auteurs : Kim L. Roberts ; Holly Shelton ; Peter Stilwell ; Wendy S. BarclaySource :
- PLoS ONE [ 1932-6203 ] ; 2012.
Abstract
During the early phase of the 2009 influenza pandemic, attempts were made to contain the spread of the virus. Success of reactive control measures may be compromised if the proportion of transmission that occurs before overt clinical symptoms develop is high. In this study we investigated the timing of transmission of an early prototypic strain of pandemic H1N1 2009 influenza virus in the ferret model. Ferrets are the only animal model in which this can be assessed because they display typical influenza-like clinical signs including fever and sneezing after infection. We assessed transmission from infected animals to sentinels that were placed either in direct contact or in adjacent cages, the latter reflecting the respiratory droplet (RD) transmission route. We found that pre-symptomatic influenza transmission occurred via both contact and respiratory droplet exposure before the earliest clinical sign, fever, developed. Three of 3 animals exposed in direct contact between day 1 and 2 after infection of the donor animals became infected, and 2/3 of the animals exposed at this time period by the RD route acquired the infection, with the third animal becoming seropositive indicating either a low level infection or significant exposure. Moreover, this efficient transmission did not temporally correlate with respiratory symptoms, such as coughs and sneezes, but rather with the peak viral titre in the nose. Indeed respiratory droplet transmission did not occur late in infection, even though this was when sneezing and coughing were most apparent. None of the 3 animals exposed at this time by the RD route became infected and these animals remained seronegative at the end of the experiment. These data have important implications for pandemic planning strategies and suggest that successful containment is highly unlikely for a human-adapted influenza virus that transmits efficiently within a population.
Url:
DOI: 10.1371/journal.pone.0043303
PubMed: 22952661
PubMed Central: 3430703
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<front><div type="abstract" xml:lang="en"><p>During the early phase of the 2009 influenza pandemic, attempts were made to contain the spread of the virus. Success of reactive control measures may be compromised if the proportion of transmission that occurs before overt clinical symptoms develop is high. In this study we investigated the timing of transmission of an early prototypic strain of pandemic H1N1 2009 influenza virus in the ferret model. Ferrets are the only animal model in which this can be assessed because they display typical influenza-like clinical signs including fever and sneezing after infection. We assessed transmission from infected animals to sentinels that were placed either in direct contact or in adjacent cages, the latter reflecting the respiratory droplet (RD) transmission route. We found that pre-symptomatic influenza transmission occurred via both contact and respiratory droplet exposure before the earliest clinical sign, fever, developed. Three of 3 animals exposed in direct contact between day 1 and 2 after infection of the donor animals became infected, and 2/3 of the animals exposed at this time period by the RD route acquired the infection, with the third animal becoming seropositive indicating either a low level infection or significant exposure. Moreover, this efficient transmission did not temporally correlate with respiratory symptoms, such as coughs and sneezes, but rather with the peak viral titre in the nose. Indeed respiratory droplet transmission did not occur late in infection, even though this was when sneezing and coughing were most apparent. None of the 3 animals exposed at this time by the RD route became infected and these animals remained seronegative at the end of the experiment. These data have important implications for pandemic planning strategies and suggest that successful containment is highly unlikely for a human-adapted influenza virus that transmits efficiently within a population.</p>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id>
<journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id>
<journal-id journal-id-type="publisher-id">plos</journal-id>
<journal-id journal-id-type="pmc">plosone</journal-id>
<journal-title-group><journal-title>PLoS ONE</journal-title>
</journal-title-group>
<issn pub-type="epub">1932-6203</issn>
<publisher><publisher-name>Public Library of Science</publisher-name>
<publisher-loc>San Francisco, USA</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">22952661</article-id>
<article-id pub-id-type="pmc">3430703</article-id>
<article-id pub-id-type="publisher-id">PONE-D-12-12377</article-id>
<article-id pub-id-type="doi">10.1371/journal.pone.0043303</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
<subj-group subj-group-type="Discipline-v2"><subject>Biology</subject>
<subj-group><subject>Microbiology</subject>
<subj-group><subject>Virology</subject>
<subj-group><subject>Viral Transmission and Infection</subject>
</subj-group>
</subj-group>
</subj-group>
<subj-group><subject>Model Organisms</subject>
<subj-group><subject>Animal Models</subject>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v2"><subject>Medicine</subject>
<subj-group><subject>Infectious Diseases</subject>
<subj-group><subject>Viral Diseases</subject>
<subj-group><subject>Influenza</subject>
</subj-group>
</subj-group>
<subj-group><subject>Infectious Disease Control</subject>
<subject>Infectious Disease Modeling</subject>
</subj-group>
</subj-group>
<subj-group><subject>Pulmonology</subject>
<subj-group><subject>Respiratory Infections</subject>
</subj-group>
</subj-group>
</subj-group>
</article-categories>
<title-group><article-title>Transmission of a 2009 H1N1 Pandemic Influenza Virus Occurs before Fever Is Detected, in the Ferret Model</article-title>
<alt-title alt-title-type="running-head">Influenza Transmission before Symptoms</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Roberts</surname>
<given-names>Kim L.</given-names>
</name>
<xref ref-type="author-notes" rid="fn1"><sup>¤a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Shelton</surname>
<given-names>Holly</given-names>
</name>
<xref ref-type="author-notes" rid="fn2"><sup>¤b</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Stilwell</surname>
<given-names>Peter</given-names>
</name>
</contrib>
<contrib contrib-type="author"><name><surname>Barclay</surname>
<given-names>Wendy S.</given-names>
</name>
<xref ref-type="aff" rid="aff1"></xref>
<xref ref-type="corresp" rid="cor1"><sup>*</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff1"><addr-line>Section of Virology, Department of Infectious Disease, Faculty of Medicine, Imperial College London, London, United Kingdom</addr-line>
</aff>
<contrib-group><contrib contrib-type="editor"><name><surname>Cowling</surname>
<given-names>Benjamin J.</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1"><addr-line>University of Hong Kong, Hong Kong</addr-line>
</aff>
<author-notes><corresp id="cor1">* E-mail: <email>w.barclay@imperial.ac.uk</email>
</corresp>
<fn fn-type="COI-statement"><p><bold>Competing Interests: </bold>
The authors have declared that no competing interests exist.</p>
</fn>
<fn fn-type="con"><p>Conceived and designed the experiments: KLR HS WSB. Performed the experiments: KLR HS PS. Analyzed the data: KLR HS WSB. Contributed reagents/materials/analysis tools: KLR HS. Wrote the paper: KLR HS WSB.</p>
</fn>
<fn id="fn1" fn-type="current-aff"><label>¤a</label>
<p>Current address: Department of Microbiology, Moyne Institute of Preventive Medicine, Trinity College, Dublin, Ireland</p>
</fn>
<fn id="fn2" fn-type="current-aff"><label>¤b</label>
<p>Current address: Institute for Animal Health, Compton Laboratory, Newbury, United Kingdom</p>
</fn>
</author-notes>
<pub-date pub-type="collection"><year>2012</year>
</pub-date>
<pub-date pub-type="epub"><day>29</day>
<month>8</month>
<year>2012</year>
</pub-date>
<volume>7</volume>
<issue>8</issue>
<elocation-id>e43303</elocation-id>
<history><date date-type="received"><day>2</day>
<month>5</month>
<year>2012</year>
</date>
<date date-type="accepted"><day>19</day>
<month>7</month>
<year>2012</year>
</date>
</history>
<permissions><copyright-statement>© 2012 Roberts et al</copyright-statement>
<copyright-year>2012</copyright-year>
<copyright-holder>Roberts et al</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.</license-p>
</license>
</permissions>
<abstract><p>During the early phase of the 2009 influenza pandemic, attempts were made to contain the spread of the virus. Success of reactive control measures may be compromised if the proportion of transmission that occurs before overt clinical symptoms develop is high. In this study we investigated the timing of transmission of an early prototypic strain of pandemic H1N1 2009 influenza virus in the ferret model. Ferrets are the only animal model in which this can be assessed because they display typical influenza-like clinical signs including fever and sneezing after infection. We assessed transmission from infected animals to sentinels that were placed either in direct contact or in adjacent cages, the latter reflecting the respiratory droplet (RD) transmission route. We found that pre-symptomatic influenza transmission occurred via both contact and respiratory droplet exposure before the earliest clinical sign, fever, developed. Three of 3 animals exposed in direct contact between day 1 and 2 after infection of the donor animals became infected, and 2/3 of the animals exposed at this time period by the RD route acquired the infection, with the third animal becoming seropositive indicating either a low level infection or significant exposure. Moreover, this efficient transmission did not temporally correlate with respiratory symptoms, such as coughs and sneezes, but rather with the peak viral titre in the nose. Indeed respiratory droplet transmission did not occur late in infection, even though this was when sneezing and coughing were most apparent. None of the 3 animals exposed at this time by the RD route became infected and these animals remained seronegative at the end of the experiment. These data have important implications for pandemic planning strategies and suggest that successful containment is highly unlikely for a human-adapted influenza virus that transmits efficiently within a population.</p>
</abstract>
<funding-group><funding-statement>This work was funded by a Medical Research Council project grant G06000504 to WB and by a National Institute for Health Research (NIHR) Imperial Biomedical Research Centre award P26591 to WB and KR. The views expressed are those of the author(s) and not necessarily those of the NHS, the NIHR or the Department of Health. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement>
</funding-group>
<counts><page-count count="8"></page-count>
</counts>
</article-meta>
</front>
</pmc>
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