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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Reply to Pawar et al</title><author><name sortKey="Todd, Stacy" sort="Todd, Stacy" uniqKey="Todd S" first="Stacy" last="Todd">Stacy Todd</name><affiliation><nlm:aff id="jiu034_af1"><institution>Oxford University Clinical Research Unit, Wellcome Trust Major Overseas Programme</institution>,<addr-line>Ho Chi Minh City</addr-line>,<country>Vietnam</country></nlm:aff></affiliation><affiliation><nlm:aff id="jiu034_af2"><institution>Liverpool School of Tropical Medicine</institution>,<addr-line>Liverpool</addr-line></nlm:aff></affiliation></author><author><name sortKey="De Bruin, Erwin" sort="De Bruin, Erwin" uniqKey="De Bruin E" first="Erwin" last="De Bruin">Erwin De Bruin</name><affiliation><nlm:aff id="jiu034_af4"><institution>National Institute for Public Health and the Environment</institution>,<addr-line>Bilthoven</addr-line></nlm:aff></affiliation></author><author><name sortKey="Nhat, Nguyen Thi Duy" sort="Nhat, Nguyen Thi Duy" uniqKey="Nhat N" first="Nguyen Thi Duy" last="Nhat">Nguyen Thi Duy Nhat</name><affiliation><nlm:aff id="jiu034_af1"><institution>Oxford University Clinical Research Unit, Wellcome Trust Major Overseas Programme</institution>,<addr-line>Ho Chi Minh City</addr-line>,<country>Vietnam</country></nlm:aff></affiliation></author><author><name sortKey="Koopmans, Marion" sort="Koopmans, Marion" uniqKey="Koopmans M" first="Marion" last="Koopmans">Marion Koopmans</name><affiliation><nlm:aff id="jiu034_af4"><institution>National Institute for Public Health and the Environment</institution>,<addr-line>Bilthoven</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="jiu034_af5"><addr-line>Department of Virology</addr-line>,<institution>Erasmus Medical Center</institution>,<addr-line>Rotterdam</addr-line>,<country>the Netherlands</country></nlm:aff></affiliation></author><author><name sortKey="Boni, Maciej F" sort="Boni, Maciej F" uniqKey="Boni M" first="Maciej F." last="Boni">Maciej F. Boni</name><affiliation><nlm:aff id="jiu034_af1"><institution>Oxford University Clinical Research Unit, Wellcome Trust Major Overseas Programme</institution>,<addr-line>Ho Chi Minh City</addr-line>,<country>Vietnam</country></nlm:aff></affiliation><affiliation><nlm:aff id="jiu034_af3"><addr-line>Centre for Tropical Medicine, Nuffield Department of Clinical Medicine</addr-line>,<institution>University of Oxford</institution>,<addr-line>Oxford</addr-line>,<country>United Kingdom</country></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">24453262</idno><idno type="pmc">4054897</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4054897</idno><idno type="RBID">PMC:4054897</idno><idno type="doi">10.1093/infdis/jiu034</idno><date when="2014">2014</date><idno type="wicri:Area/Pmc/Corpus">000506</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000506</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Reply to Pawar et al</title><author><name sortKey="Todd, Stacy" sort="Todd, Stacy" uniqKey="Todd S" first="Stacy" last="Todd">Stacy Todd</name><affiliation><nlm:aff id="jiu034_af1"><institution>Oxford University Clinical Research Unit, Wellcome Trust Major Overseas Programme</institution>,<addr-line>Ho Chi Minh City</addr-line>,<country>Vietnam</country></nlm:aff></affiliation><affiliation><nlm:aff id="jiu034_af2"><institution>Liverpool School of Tropical Medicine</institution>,<addr-line>Liverpool</addr-line></nlm:aff></affiliation></author><author><name sortKey="De Bruin, Erwin" sort="De Bruin, Erwin" uniqKey="De Bruin E" first="Erwin" last="De Bruin">Erwin De Bruin</name><affiliation><nlm:aff id="jiu034_af4"><institution>National Institute for Public Health and the Environment</institution>,<addr-line>Bilthoven</addr-line></nlm:aff></affiliation></author><author><name sortKey="Nhat, Nguyen Thi Duy" sort="Nhat, Nguyen Thi Duy" uniqKey="Nhat N" first="Nguyen Thi Duy" last="Nhat">Nguyen Thi Duy Nhat</name><affiliation><nlm:aff id="jiu034_af1"><institution>Oxford University Clinical Research Unit, Wellcome Trust Major Overseas Programme</institution>,<addr-line>Ho Chi Minh City</addr-line>,<country>Vietnam</country></nlm:aff></affiliation></author><author><name sortKey="Koopmans, Marion" sort="Koopmans, Marion" uniqKey="Koopmans M" first="Marion" last="Koopmans">Marion Koopmans</name><affiliation><nlm:aff id="jiu034_af4"><institution>National Institute for Public Health and the Environment</institution>,<addr-line>Bilthoven</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="jiu034_af5"><addr-line>Department of Virology</addr-line>,<institution>Erasmus Medical Center</institution>,<addr-line>Rotterdam</addr-line>,<country>the Netherlands</country></nlm:aff></affiliation></author><author><name sortKey="Boni, Maciej F" sort="Boni, Maciej F" uniqKey="Boni M" first="Maciej F." last="Boni">Maciej F. Boni</name><affiliation><nlm:aff id="jiu034_af1"><institution>Oxford University Clinical Research Unit, Wellcome Trust Major Overseas Programme</institution>,<addr-line>Ho Chi Minh City</addr-line>,<country>Vietnam</country></nlm:aff></affiliation><affiliation><nlm:aff id="jiu034_af3"><addr-line>Centre for Tropical Medicine, Nuffield Department of Clinical Medicine</addr-line>,<institution>University of Oxford</institution>,<addr-line>Oxford</addr-line>,<country>United Kingdom</country></nlm:aff></affiliation></author></analytic><series><title level="j">The Journal of Infectious Diseases</title><idno type="ISSN">0022-1899</idno><idno type="eISSN">1537-6613</idno><imprint><date when="2014">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Pawar, Sd" uniqKey="Pawar S">SD Pawar</name></author><author><name sortKey="Tandale, Bv" uniqKey="Tandale B">BV Tandale</name></author><author><name sortKey="Raut, Cg" uniqKey="Raut C">CG Raut</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Pawar, Sd" uniqKey="Pawar S">SD Pawar</name></author><author><name sortKey="Tandale, Bv" uniqKey="Tandale B">BV Tandale</name></author><author><name sortKey="Gurav, Yk" uniqKey="Gurav Y">YK Gurav</name></author><author><name sortKey="Parkhi, Ss" uniqKey="Parkhi S">SS Parkhi</name></author><author><name sortKey="Kode, Ss" uniqKey="Kode S">SS Kode</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Boni, Mf" uniqKey="Boni M">MF Boni</name></author><author><name sortKey="Chau, Nvv" uniqKey="Chau N">NVV Chau</name></author><author><name sortKey="Dong, N" uniqKey="Dong N">N Dong</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Blair, Pj" uniqKey="Blair P">PJ Blair</name></author><author><name sortKey="Putnam, Sd" uniqKey="Putnam S">SD Putnam</name></author><author><name sortKey="Krueger, Ws" uniqKey="Krueger W">WS Krueger</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Uyeki, Tm" uniqKey="Uyeki T">TM Uyeki</name></author><author><name sortKey="Nguyen, Dc" uniqKey="Nguyen D">DC Nguyen</name></author><author><name sortKey="Rowe, T" uniqKey="Rowe T">T Rowe</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Wang, M" uniqKey="Wang M">M Wang</name></author><author><name sortKey="Fu, Cx" uniqKey="Fu C">CX Fu</name></author><author><name sortKey="Zheng, Bj" uniqKey="Zheng B">BJ Zheng</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kayali, G" uniqKey="Kayali G">G Kayali</name></author><author><name sortKey="Ortiz, Ej" uniqKey="Ortiz E">EJ Ortiz</name></author><author><name sortKey="Chorazy, Ml" uniqKey="Chorazy M">ML Chorazy</name></author><author><name sortKey="Gray, Gc" uniqKey="Gray G">GC Gray</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Gray, Gc" uniqKey="Gray G">GC Gray</name></author><author><name sortKey="Mccarthy, T" uniqKey="Mccarthy T">T McCarthy</name></author><author><name sortKey="Capuano, Aw" uniqKey="Capuano A">AW Capuano</name></author><author><name sortKey="Setterquist, Sf" uniqKey="Setterquist S">SF Setterquist</name></author><author><name sortKey="Alavanja, Mc" uniqKey="Alavanja M">MC Alavanja</name></author><author><name sortKey="Lynch, Cf" uniqKey="Lynch C">CF Lynch</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Stephenson, I" uniqKey="Stephenson I">I Stephenson</name></author><author><name sortKey="Nicholson, Kg" uniqKey="Nicholson K">KG Nicholson</name></author><author><name sortKey="Gluck, R" uniqKey="Gluck R">R Glück</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Karron, Ra" uniqKey="Karron R">RA Karron</name></author><author><name sortKey="Callahan, K" uniqKey="Callahan K">K Callahan</name></author><author><name sortKey="Luke, C" uniqKey="Luke C">C Luke</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Atmar, Rl" uniqKey="Atmar R">RL Atmar</name></author><author><name sortKey="Keitel, Wa" uniqKey="Keitel W">WA Keitel</name></author><author><name sortKey="Quarles, Jm" uniqKey="Quarles J">JM Quarles</name></author></analytic></biblStruct></listBibl></div1></back></TEI><pmc article-type="letter"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">J Infect Dis</journal-id><journal-id journal-id-type="iso-abbrev">J. Infect. Dis</journal-id><journal-id journal-id-type="publisher-id">jid</journal-id><journal-id journal-id-type="hwp">jinfdis</journal-id><journal-title-group><journal-title>The Journal of Infectious Diseases</journal-title></journal-title-group><issn pub-type="ppub">0022-1899</issn><issn pub-type="epub">1537-6613</issn><publisher><publisher-name>Oxford University Press</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">24453262</article-id><article-id pub-id-type="pmc">4054897</article-id><article-id pub-id-type="doi">10.1093/infdis/jiu034</article-id><article-id pub-id-type="publisher-id">jiu034</article-id><article-categories><subj-group subj-group-type="heading"><subject>Correspondence</subject></subj-group></article-categories><title-group><article-title>Reply to Pawar et al</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Todd</surname><given-names>Stacy</given-names></name><xref ref-type="aff" rid="jiu034_af1">1</xref><xref ref-type="aff" rid="jiu034_af2">2</xref></contrib><contrib contrib-type="author"><name><surname>De Bruin</surname><given-names>Erwin</given-names></name><xref ref-type="aff" rid="jiu034_af4">4</xref></contrib><contrib contrib-type="author"><name><surname>Nhat</surname><given-names>Nguyen Thi Duy</given-names></name><xref ref-type="aff" rid="jiu034_af1">1</xref></contrib><contrib contrib-type="author"><name><surname>Koopmans</surname><given-names>Marion</given-names></name><xref ref-type="aff" rid="jiu034_af4">4</xref><xref ref-type="aff" rid="jiu034_af5">5</xref></contrib><contrib contrib-type="author"><name><surname>Boni</surname><given-names>Maciej F.</given-names></name><xref ref-type="aff" rid="jiu034_af1">1</xref><xref ref-type="aff" rid="jiu034_af3">3</xref></contrib><aff id="jiu034_af1"><label>1</label><institution>Oxford University Clinical Research Unit, Wellcome Trust Major Overseas Programme</institution>,<addr-line>Ho Chi Minh City</addr-line>,<country>Vietnam</country></aff><aff id="jiu034_af2"><label>2</label><institution>Liverpool School of Tropical Medicine</institution>,<addr-line>Liverpool</addr-line></aff><aff id="jiu034_af3"><label>3</label><addr-line>Centre for Tropical Medicine, Nuffield Department of Clinical Medicine</addr-line>,<institution>University of Oxford</institution>,<addr-line>Oxford</addr-line>,<country>United Kingdom</country></aff><aff id="jiu034_af4"><label>4</label><institution>National Institute for Public Health and the Environment</institution>,<addr-line>Bilthoven</addr-line></aff><aff id="jiu034_af5"><label>5</label><addr-line>Department of Virology</addr-line>,<institution>Erasmus Medical Center</institution>,<addr-line>Rotterdam</addr-line>,<country>the Netherlands</country></aff></contrib-group><author-notes><corresp>Correspondence: Stacy Todd, MBChB, Oxford University Clinical Research Unit, Hospital for Tropical Diseases, 764 Vo Van Kiet St, District 5, Ho Chi Minh City, Vietnam (<email>stodd@oucru.org</email>).</corresp></author-notes><pub-date pub-type="ppub"><day>01</day><month>7</month><year>2014</year></pub-date><pub-date pub-type="epub"><day>22</day><month>1</month><year>2014</year></pub-date><pub-date pub-type="pmc-release"><day>22</day><month>1</month><year>2014</year></pub-date><pmc-comment> PMC Release delay is 0 months and 0 days and was based on the
<volume>210</volume><issue>1</issue><fpage>161</fpage><lpage>163</lpage><history><date date-type="received"><day>15</day><month>11</month><year>2013</year></date><date date-type="accepted"><day>18</day><month>11</month><year>2013</year></date></history><permissions><copyright-statement>© The Author 2013. Published by Oxford University Press on behalf of the Infectious Diseases Society of America.</copyright-statement><copyright-year>2013</copyright-year><license license-type="creative-commons" xlink:href="http://creativecommons.org/licenses/by/3.0/"><license-p>This is an Open Access article distributed under the terms of the Creative Commons Attribution License (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/3.0/">http://creativecommons.org/licenses/by/3.0/</ext-link>), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.</license-p></license></permissions><self-uri content-type="pdf" xlink:type="simple" xlink:href="jiu034.pdf"></self-uri><related-article id="d35e187" related-article-type="letter" ext-link-type="doi" xlink:href="10.1093/infdis/jiu033"></related-article></article-meta></front><body><p><sc>To</sc><sc>the</sc><sc>Editor</sc>—In this issue of the <italic>Journal</italic> and in a recent study, Pawar et al reported results of serologic tests performed on a high-risk group of 446 poultry workers and 162 individuals from the general population in Maharashtra and Jamshedpur states, India [<xref rid="JIU034C1" ref-type="bibr">1</xref>, <xref rid="JIU034C2" ref-type="bibr">2</xref>]. None of the 608 samples tested positive for antibodies to influenza A virus subtypes H5N1 or H7N1 by hemagglutination-inhibition (HI) or microneutralization (MN) assays. None of the 162 individuals from the general population tested positive for H9N2 antibodies by HI or MN assay. A total of 4.7% and 10% of high-risk individuals in Pune and Jamshedpur, respectively, tested positive by the HI assay for influenza A(H9N2); 3.8% and 4.7%, respectively, had positive results of the MN assay. The authors suggest that this higher rate of seropositivity could be related to the circulation of influenza A(H9N2) in Jamshedpur in poultry, with resultant zoonotic spread to humans, and reference our publication showing presence of antibodies to avian influenza virus antigens in Vietnam.</p><p>As noted by the authors, H9 titers were highest among all antibodies to avian influenza virus strains in our general population sample [<xref rid="JIU034C3" ref-type="bibr">3</xref>]. Other publications looking at high-risk individuals in South East Asia have demonstrated a higher seropositivity rate for influenza A(H9) strains, compared with influenza A(H5) and/or A(H7) strains [<xref rid="JIU034C4" ref-type="bibr">4</xref>–<xref rid="JIU034C6" ref-type="bibr">6</xref>], but this is not a consistent finding globally, even in high-risk groups [<xref rid="JIU034C7" ref-type="bibr">7</xref>, <xref rid="JIU034C8" ref-type="bibr">8</xref>]. Vaccine studies conducted in locations thought to have a low risk of avian influenza exposure (ie, the United Kingdom and United States) found that up to a third of participants were seropositive for H9 [<xref rid="JIU034C9" ref-type="bibr">9</xref>–<xref rid="JIU034C11" ref-type="bibr">11</xref>]. Of those positive for H9 antibodies (>1:40 by the HI assay), a greater proportion were born before 1968, and it was postulated that this was related to cross-reactivity from influenza A virus subtype H2N2, which was circulating in humans from 1957 to 1968. Within our data set, there was a significantly higher seropositivity (and, accordingly, mean titer) for all avian strains in individuals born before 1968 (multivariate analysis of variance [MANOVA]: F = 4.7, <italic>P</italic> < .0005, Pillai 0.1256), with the H9 titer being the highest. However, when we investigate other birth year cutoffs (±20 years), we find the same trend, suggesting that this effect is more related to an increase in age rather than to a specific exposure event.</p><p>In the Vietnam sample set (n = 1424; slightly reduced due to quality checks from our original sample set), antibody titers to avian influenza A virus antigens increased with age. The optimal fitted regression curve among nonlinear models was a fifth-order polynomial (ANOVA: <italic>P</italic> < .001), but this curve provided no additional qualitative explanations of the data than the second best fit model, a simple quadratic regression (Figure <xref ref-type="fig" rid="JIU034F1">1</xref>). Titers to H9 antigen increase more rapidly with age than titers to H7 or H5. One hypothesis is that this difference is caused by varying levels of exposure to avian influenza viruses. A second hypothesis is that this is caused by differences in cross-reactivity between human influenza antibodies and each of the subtypes H9, H7, and H5. Our analysis provides more support for the second hypothesis (<ext-link ext-link-type="uri" xlink:href="http://jid.oxfordjournals.org/lookup/suppl/doi:10.1093/infdis/jiu034/-/DC1">supplementary figures 1 and 2</ext-link> in the article by Boni et al [<xref rid="JIU034C3" ref-type="bibr">3</xref>]).<fig id="JIU034F1" position="float"><label>Figure 1.</label><caption><p>Scatterplot of avian strain titer against age with polynomial regressions lines. The black line denotes the second-order polynomial, and the red line denotes the fifth-order polynomial.</p></caption><graphic xlink:href="jiu03401"></graphic></fig></p><p>As noted in our article, the microarray assay used in this analysis is more sensitive than traditional HI and MN tests when comparing titers for the homologous antigens. A problem in doing studies to evaluate zoonotic exposure is that the exact antigenic composition of the infecting virus may be unknown. Therefore, HI/MN tests may yield false-negative results, a problem that is less evident with the microarray, which measures antibodies to the head of hemagglutinin and is, therefore, more broadly reactive within subtype. The differences we see in response between H9 and H5 avian strains (and to a lesser extent between H7 and H5 strains) are robust even when a much higher titer cutoff is used (up to 1:320, using microarray). With a cutoff titer of 1:20, 76% of individuals aged ≥50 years test positive for H9 antibodies (compared with 33% aged <50 years; χ<sup>2</sup> = 89.9; <italic>P</italic> < .001). With a more conservative (and probably more appropriate) titer cutoff of 1:80, this percentage is 41% (18% among those aged <50 years; χ<sup>2</sup> = 40.6; <italic>P</italic> < .001), suggesting that age distribution needs to be carefully taken into account when designing seroepidemiologic studies of avian influenza virus in humans. This result is robust for site effects in Vietnam, strengthening the hypothesis that this phenomenon is not related to poultry exposure.</p><p>Understanding the best way to interpret avian influenza virus serologic data, including cross-reactions generated by nonavian strains, is crucial for measuring incidence in both high-risk groups and the general population. The results generated by Pawar et al contribute to this understanding, but their study, as with all studies showing H9 positivity, should be interpreted with caution, as these H9-positive signals are possibly cross-reactions.</p><sec sec-type="supplementary-material" id="jiu034_s2"><title>Supplementary Data</title><p><ext-link ext-link-type="uri" xlink:href="http://jid.oxfordjournals.org/lookup/suppl/doi:10.1093/infdis/jiu034/-/DC1">Supplementary materials</ext-link> are available at <italic>The Journal of Infectious Diseases</italic> online (<uri xlink:type="simple" xlink:href="http://jid.oxfordjournals.org/">http://jid.oxfordjournals.org/</uri>). Supplementary materials consist of data provided by the author that are published to benefit the reader. The posted materials are not copyedited. The contents of all supplementary data are the sole responsibility of the authors. Questions or messages regarding errors should be addressed to the author.</p></sec></body><back><ack><title>Notes</title><p><bold><italic>Financial</italic></bold><bold><italic>support</italic></bold>. This work was supported by <funding-source id="cs1" rid="cn1">the Wellcome Trust</funding-source> (<award-id id="cn1" rid="cs1">098511/Z/12/Z</award-id>, <award-id id="cn2" rid="cs2">089276/B/09/7, 097465/B/11/Z, 084368/Z/07/Z</award-id>), <funding-source id="cs2" rid="cn2">the British Medical Association</funding-source> (<award-id id="cn3" rid="cs3">HC Roscoe 2011</award-id>), and <funding-source id="cs3" rid="cn3">the Dutch Ministry of Economic Affairs, Agriculture, and Innovation, Castellum Project</funding-source>.</p><p><bold><italic>Potential conflicts of interest.</italic></bold> All authors: No reported conflicts.</p><p>All authors have submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. 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