Outbreak of Chikungunya on Reunion Island: Early Clinical and Laboratory Features in 157 Adult Patients
Identifieur interne : 001925 ( Istex/Corpus ); précédent : 001924; suivant : 001926Outbreak of Chikungunya on Reunion Island: Early Clinical and Laboratory Features in 157 Adult Patients
Auteurs : Gianandrea Borgherini ; Patrice Poubeau ; Frederik Staikowsky ; Manuella Lory ; Nathalie Le Moullec ; Jean Philippe Becquart ; Catherine Wengling ; Alain Michault ; Fabrice PaganinSource :
- Clinical Infectious Diseases [ 1058-4838 ] ; 2007.
Abstract
Background. Chikungunya is a reemerging disease. In 2005–2006, a severe outbreak occurred on Reunion Island in the southwestern part of the Indian Ocean. Other islands in this area were affected during the same period. Methods. Adult patients with acute chikungunya (defined as onset of fever and/or polyarthralgia in the 5 days preceding consultation) and laboratory-confirmed chikungunya who were referred to Groupe Hospitalier Sud Reunion during the period from March 2005 through April 2006 were included in this retrospective study. Their clinical and laboratory features are reported. Results. Laboratory-confirmed acute chikungunya was documented in 157 patients. The mean age of patients was 57.9 years, and the ratio of male to female patients was 1.24 : 1. Sixty percent of patients had at least 1 comorbidity. Ninety-seven patients (61.8%) were hospitalized, and 60 (38.2%) were treated as outpatients. Five fatalities were reported. One hundred fifty-one patients (96.1%) experienced polyarthralgia, and 129 (89%) experienced fever. Gastrointestinal symptoms were reported by 74 patients (47.1%), and skin rash was reported by 63 (40.1%). Hemorrhagic signs were rare. Lymphopenia and hypocalcemia were the prominent laboratory findings. Severe thrombocytopenia was rarely observed. Conclusions. Chikungunya virus can be responsible for explosive outbreaks of disease. Polyarthralgia and fever are the 2 main clinical features. In this era of travel and globalization, chikungunya should be considered in the differential diagnosis of febrile polyarthralgia with an abrupt onset.
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DOI: 10.1086/517537
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ISTEX:CFB04B855E574C0F7D30CA6B0CA8E43236FEA356Le document en format XML
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France</mods:affiliation></affiliation><affiliation><mods:affiliation>E-mail: gianu.borg@wanadoo.fr</mods:affiliation></affiliation><affiliation><mods:affiliation>Reprints or correspondence: Dr. Gianandrea Borgherini, Service de Pneumologie et Maladies Infectieuses, Groupe Hospitalier Sud Reunion, BP 350, 97448 Saint Pierre, La Réunion, France (gianu.borg@wanadoo.fr).</mods:affiliation></affiliation></author><author><name sortKey="Poubeau, Patrice" sort="Poubeau, Patrice" uniqKey="Poubeau P" first="Patrice" last="Poubeau">Patrice Poubeau</name><affiliation><mods:affiliation>Services de Pneumologie et Maladies Infectieuses, La Réunion, France</mods:affiliation></affiliation></author><author><name sortKey="Staikowsky, Frederik" sort="Staikowsky, Frederik" uniqKey="Staikowsky F" first="Frederik" last="Staikowsky">Frederik Staikowsky</name><affiliation><mods:affiliation>Urgences, La Réunion, France</mods:affiliation></affiliation></author><author><name sortKey="Lory, Manuella" sort="Lory, Manuella" uniqKey="Lory M" first="Manuella" last="Lory">Manuella Lory</name><affiliation><mods:affiliation>Services de Pneumologie et Maladies Infectieuses, La Réunion, France</mods:affiliation></affiliation></author><author><name sortKey="Moullec, Nathalie Le" sort="Moullec, Nathalie Le" uniqKey="Moullec N" first="Nathalie Le" last="Moullec">Nathalie Le Moullec</name><affiliation><mods:affiliation>Endocrinologie, La Réunion, France</mods:affiliation></affiliation></author><author><name sortKey="Becquart, Jean Philippe" sort="Becquart, Jean Philippe" uniqKey="Becquart J" first="Jean Philippe" last="Becquart">Jean Philippe Becquart</name><affiliation><mods:affiliation>Gastro-enterologie, La Réunion, France</mods:affiliation></affiliation></author><author><name sortKey="Wengling, Catherine" sort="Wengling, Catherine" uniqKey="Wengling C" first="Catherine" last="Wengling">Catherine Wengling</name><affiliation><mods:affiliation>Medecine Interne, La Réunion, France</mods:affiliation></affiliation></author><author><name sortKey="Michault, Alain" sort="Michault, Alain" uniqKey="Michault A" first="Alain" last="Michault">Alain Michault</name><affiliation><mods:affiliation>Laboratoire de Virologie, Groupe Hospitalier Sud Reunion, Saint Pierre, La Réunion, France</mods:affiliation></affiliation></author><author><name sortKey="Paganin, Fabrice" sort="Paganin, Fabrice" uniqKey="Paganin F" first="Fabrice" last="Paganin">Fabrice Paganin</name><affiliation><mods:affiliation>Services de Pneumologie et Maladies Infectieuses, La Réunion, France</mods:affiliation></affiliation></author></analytic><monogr></monogr><series><title level="j" type="main">Clinical Infectious Diseases</title><title level="j" type="abbrev">Clinical Infectious Diseases</title><idno type="ISSN">1058-4838</idno><idno type="eISSN">1537-6591</idno><imprint><publisher>The University of Chicago Press</publisher><date type="published">2007</date><biblScope unit="vol">44</biblScope><biblScope unit="issue">11</biblScope><biblScope unit="page" from="1401">1401</biblScope><biblScope unit="page" to="1407">1407</biblScope></imprint><idno type="ISSN">1058-4838</idno></series></biblStruct></sourceDesc><seriesStmt><idno type="ISSN">1058-4838</idno></seriesStmt></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract">Background. Chikungunya is a reemerging disease. In 2005–2006, a severe outbreak occurred on Reunion Island in the southwestern part of the Indian Ocean. Other islands in this area were affected during the same period. Methods. Adult patients with acute chikungunya (defined as onset of fever and/or polyarthralgia in the 5 days preceding consultation) and laboratory-confirmed chikungunya who were referred to Groupe Hospitalier Sud Reunion during the period from March 2005 through April 2006 were included in this retrospective study. Their clinical and laboratory features are reported. Results. Laboratory-confirmed acute chikungunya was documented in 157 patients. The mean age of patients was 57.9 years, and the ratio of male to female patients was 1.24 : 1. Sixty percent of patients had at least 1 comorbidity. Ninety-seven patients (61.8%) were hospitalized, and 60 (38.2%) were treated as outpatients. Five fatalities were reported. One hundred fifty-one patients (96.1%) experienced polyarthralgia, and 129 (89%) experienced fever. Gastrointestinal symptoms were reported by 74 patients (47.1%), and skin rash was reported by 63 (40.1%). Hemorrhagic signs were rare. Lymphopenia and hypocalcemia were the prominent laboratory findings. Severe thrombocytopenia was rarely observed. Conclusions. Chikungunya virus can be responsible for explosive outbreaks of disease. Polyarthralgia and fever are the 2 main clinical features. In this era of travel and globalization, chikungunya should be considered in the differential diagnosis of febrile polyarthralgia with an abrupt onset.</div></front></TEI><istex><corpusName>oup</corpusName><author><json:item><name>Gianandrea Borgherini</name><affiliations><json:string>Services de Pneumologie et Maladies Infectieuses, La Réunion, France</json:string><json:string>E-mail: gianu.borg@wanadoo.fr</json:string><json:string>Reprints or correspondence: Dr. Gianandrea Borgherini, Service de Pneumologie et Maladies Infectieuses, Groupe Hospitalier Sud Reunion, BP 350, 97448 Saint Pierre, La Réunion, France (gianu.borg@wanadoo.fr).</json:string></affiliations></json:item><json:item><name>Patrice Poubeau</name><affiliations><json:string>Services de Pneumologie et Maladies Infectieuses, La Réunion, France</json:string></affiliations></json:item><json:item><name>Frederik Staikowsky</name><affiliations><json:string>Urgences, La Réunion, France</json:string></affiliations></json:item><json:item><name>Manuella Lory</name><affiliations><json:string>Services de Pneumologie et Maladies Infectieuses, La Réunion, France</json:string></affiliations></json:item><json:item><name>Nathalie Le Moullec</name><affiliations><json:string>Endocrinologie, La Réunion, France</json:string></affiliations></json:item><json:item><name>Jean Philippe Becquart</name><affiliations><json:string>Gastro-enterologie, La Réunion, France</json:string></affiliations></json:item><json:item><name>Catherine Wengling</name><affiliations><json:string>Medecine Interne, La Réunion, France</json:string></affiliations></json:item><json:item><name>Alain Michault</name><affiliations><json:string>Laboratoire de Virologie, Groupe Hospitalier Sud Reunion, Saint Pierre, La Réunion, France</json:string></affiliations></json:item><json:item><name>Fabrice Paganin</name><affiliations><json:string>Services de Pneumologie et Maladies Infectieuses, La Réunion, France</json:string></affiliations></json:item></author><arkIstex>ark:/67375/HXZ-822ZKS17-6</arkIstex><language><json:string>unknown</json:string></language><originalGenre><json:string>research-article</json:string></originalGenre><abstract>Background. Chikungunya is a reemerging disease. In 2005–2006, a severe outbreak occurred on Reunion Island in the southwestern part of the Indian Ocean. Other islands in this area were affected during the same period. Methods. Adult patients with acute chikungunya (defined as onset of fever and/or polyarthralgia in the 5 days preceding consultation) and laboratory-confirmed chikungunya who were referred to Groupe Hospitalier Sud Reunion during the period from March 2005 through April 2006 were included in this retrospective study. Their clinical and laboratory features are reported. Results. Laboratory-confirmed acute chikungunya was documented in 157 patients. The mean age of patients was 57.9 years, and the ratio of male to female patients was 1.24 : 1. Sixty percent of patients had at least 1 comorbidity. Ninety-seven patients (61.8%) were hospitalized, and 60 (38.2%) were treated as outpatients. Five fatalities were reported. One hundred fifty-one patients (96.1%) experienced polyarthralgia, and 129 (89%) experienced fever. Gastrointestinal symptoms were reported by 74 patients (47.1%), and skin rash was reported by 63 (40.1%). Hemorrhagic signs were rare. Lymphopenia and hypocalcemia were the prominent laboratory findings. Severe thrombocytopenia was rarely observed. Conclusions. Chikungunya virus can be responsible for explosive outbreaks of disease. Polyarthralgia and fever are the 2 main clinical features. 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Data</json:string><json:string>Nathalie Le Moullec</json:string><json:string>Jean Philippe</json:string><json:string>Nonhospitalized</json:string><json:string>Patrice Poubeau</json:string><json:string>Manuella Lory</json:string><json:string>Sud</json:string><json:string>Alain Michault</json:string><json:string>La Reunion</json:string></persName><placeName><json:string>Madras City</json:string><json:string>Madagascar</json:string><json:string>United States</json:string><json:string>Tanganyika</json:string><json:string>Taiwan</json:string><json:string>Mombasa</json:string><json:string>Kenya</json:string><json:string>India</json:string><json:string>Europe</json:string><json:string>France</json:string><json:string>Lyon</json:string></placeName><ref_url></ref_url><ref_bibl><json:string>De Ranitz et al. [24]</json:string><json:string>March 2006</json:string><json:string>December 2005</json:string><json:string>[29]</json:string><json:string>[5, 23]</json:string><json:string>[28]</json:string><json:string>March 2005</json:string><json:string>[1]</json:string><json:string>[10]</json:string><json:string>[27]</json:string><json:string>November 2004</json:string><json:string>Thiruvengadam et al. [23]</json:string><json:string>[31]</json:string><json:string>Thiruvengadam et al.</json:string><json:string>[7,23]</json:string><json:string>[30]</json:string><json:string>Hochedez et al. [17]</json:string><json:string>[7]</json:string><json:string>[25]</json:string><json:string>[9]</json:string><json:string>August 2004</json:string><json:string>[13]</json:string><json:string>Borgherini et al.</json:string><json:string>[19]</json:string></ref_bibl><bibl></bibl></unitex></namedEntities><ark><json:string>ark:/67375/HXZ-822ZKS17-6</json:string></ark><categories><wos><json:string>1 - science</json:string><json:string>2 - microbiology</json:string><json:string>2 - infectious diseases</json:string><json:string>2 - immunology</json:string></wos><scienceMetrix><json:string>1 - health sciences</json:string><json:string>2 - biomedical research</json:string><json:string>3 - microbiology</json:string></scienceMetrix><scopus><json:string>1 - Health Sciences</json:string><json:string>2 - Medicine</json:string><json:string>3 - Infectious Diseases</json:string><json:string>1 - Health Sciences</json:string><json:string>2 - Medicine</json:string><json:string>3 - Microbiology 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type="first">Alain</forename></persName><affiliation><orgName type="institution">Laboratoire de Virologie, Groupe Hospitalier Sud Reunion, Saint Pierre</orgName><address><addrLine>La Réunion, France</addrLine></address></affiliation></author><author xml:id="author-0008"><persName><surname>Paganin</surname><forename type="first">Fabrice</forename></persName><affiliation><orgName type="institution">Services de Pneumologie et Maladies Infectieuses</orgName><address><addrLine>La Réunion, France</addrLine></address></affiliation></author><idno type="istex">CFB04B855E574C0F7D30CA6B0CA8E43236FEA356</idno><idno type="ark">ark:/67375/HXZ-822ZKS17-6</idno><idno type="DOI">10.1086/517537</idno></analytic><monogr><title level="j" type="main">Clinical Infectious Diseases</title><title level="j" type="abbrev">Clinical Infectious Diseases</title><idno type="hwp">cid</idno><idno type="publisher-id">cid</idno><idno type="pISSN">1058-4838</idno><idno type="eISSN">1537-6591</idno><imprint><publisher>The 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<ref target="http://www.tei-c.org/">We use TEI</ref></desc></application></appInfo></encodingDesc><profileDesc><abstract><p><hi rend="bold"><hi rend="italic">Background</hi></hi>. Chikungunya is a reemerging disease. In 2005–2006, a severe outbreak occurred on Reunion Island in the southwestern part of the Indian Ocean. Other islands in this area were affected during the same period.</p><p><hi rend="bold"><hi rend="italic">Methods</hi></hi>. Adult patients with acute chikungunya (defined as onset of fever and/or polyarthralgia in the 5 days preceding consultation) and laboratory-confirmed chikungunya who were referred to Groupe Hospitalier Sud Reunion during the period from March 2005 through April 2006 were included in this retrospective study. Their clinical and laboratory features are reported.</p><p><hi rend="bold"><hi rend="italic">Results</hi></hi>. Laboratory-confirmed acute chikungunya was documented in 157 patients. The mean age of patients was 57.9 years, and the ratio of male to female patients was 1.24 : 1. Sixty percent of patients had at least 1 comorbidity. Ninety-seven patients (61.8%) were hospitalized, and 60 (38.2%) were treated as outpatients. Five fatalities were reported. One hundred fifty-one patients (96.1%) experienced polyarthralgia, and 129 (89%) experienced fever. Gastrointestinal symptoms were reported by 74 patients (47.1%), and skin rash was reported by 63 (40.1%). Hemorrhagic signs were rare. Lymphopenia and hypocalcemia were the prominent laboratory findings. Severe thrombocytopenia was rarely observed.</p><p><hi rend="bold"><hi rend="italic">Conclusions</hi></hi>. Chikungunya virus can be responsible for explosive outbreaks of disease. Polyarthralgia and fever are the 2 main clinical features. In this era of travel and globalization, chikungunya should be considered in the differential diagnosis of febrile polyarthralgia with an abrupt onset.</p></abstract><textClass ana="subject"><keywords scheme="heading"><term>Articles and Commentaries</term></keywords></textClass><langUsage><language ident="EN"></language></langUsage></profileDesc><revisionDesc><change when="2020-04-06" who="#istex" xml:id="pub2tei">formatting</change></revisionDesc></teiHeader></istex:fulltextTEI><json:item><extension>txt</extension><original>false</original><mimetype>text/plain</mimetype><uri>https://api.istex.fr/ark:/67375/HXZ-822ZKS17-6/fulltext.txt</uri></json:item></fulltext><metadata><istex:metadataXml wicri:clean="corpus oup, element #text not found" wicri:toSee="no header"><istex:xmlDeclaration>version="1.0"</istex:xmlDeclaration><istex:docType PUBLIC="-//NLM//DTD Journal Publishing DTD v2.3 20070202//EN" URI="journalpublishing.dtd" name="istex:docType"></istex:docType><istex:document><article article-type="research-article">
<front>
<journal-meta>
<journal-id journal-id-type="hwp">cid</journal-id>
<journal-id journal-id-type="publisher-id">cid</journal-id>
<journal-title>Clinical Infectious Diseases</journal-title>
<abbrev-journal-title>Clinical Infectious Diseases</abbrev-journal-title>
<issn pub-type="ppub">1058-4838</issn>
<issn pub-type="epub">1537-6591</issn>
<publisher>
<publisher-name>The University of Chicago Press</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="doi">10.1086/517537</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Articles and Commentaries</subject>
<subj-group subj-group-type="heading">
<subject>Major Articles</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Outbreak of Chikungunya on Reunion Island: Early Clinical and Laboratory Features in 157 Adult Patients</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Borgherini</surname>
<given-names>Gianandrea</given-names>
</name>
<xref rid="aff1" ref-type="aff">1</xref>
<xref rid="cor1" ref-type="corresp"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Poubeau</surname>
<given-names>Patrice</given-names>
</name>
<xref rid="aff1" ref-type="aff">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Staikowsky</surname>
<given-names>Frederik</given-names>
</name>
<xref rid="aff2" ref-type="aff">2</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Lory</surname>
<given-names>Manuella</given-names>
</name>
<xref rid="aff1" ref-type="aff">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Moullec</surname>
<given-names>Nathalie Le</given-names>
</name>
<xref rid="aff3" ref-type="aff">3</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Becquart</surname>
<given-names>Jean Philippe</given-names>
</name>
<xref rid="aff4" ref-type="aff">4</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Wengling</surname>
<given-names>Catherine</given-names>
</name>
<xref rid="aff5" ref-type="aff">5</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Michault</surname>
<given-names>Alain</given-names>
</name>
<xref rid="aff6" ref-type="aff">6</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Paganin</surname>
<given-names>Fabrice</given-names>
</name>
<xref rid="aff1" ref-type="aff">1</xref>
</contrib>
<aff id="aff1"><label>1</label><institution>Services de Pneumologie et Maladies Infectieuses</institution>, <addr-line>La Réunion, France</addr-line></aff>
<aff id="aff2"><label>2</label><institution>Urgences</institution>, <addr-line>La Réunion, France</addr-line></aff>
<aff id="aff3"><label>3</label><institution>Endocrinologie</institution>, <addr-line>La Réunion, France</addr-line></aff>
<aff id="aff4"><label>4</label><institution>Gastro-enterologie</institution>, <addr-line>La Réunion, France</addr-line></aff>
<aff id="aff5"><label>5</label><institution>Medecine Interne</institution>, <addr-line>La Réunion, France</addr-line></aff>
<aff id="aff6"><label>6</label><institution>Laboratoire de Virologie, Groupe Hospitalier Sud Reunion, Saint Pierre</institution>, <addr-line>La Réunion, France</addr-line></aff>
</contrib-group>
<author-notes>
<corresp id="cor1">Reprints or correspondence: Dr. Gianandrea Borgherini, Service de Pneumologie et Maladies Infectieuses, Groupe Hospitalier Sud Reunion, BP 350, 97448 Saint Pierre, La Réunion, France (<email>gianu.borg@wanadoo.fr</email>).</corresp>
</author-notes>
<pub-date pub-type="ppub">
<day>1</day>
<month>6</month>
<year>2007</year>
</pub-date>
<volume>44</volume>
<issue>11</issue>
<fpage>1401</fpage>
<lpage>1407</lpage>
<history>
<date date-type="received">
<day>16</day>
<month>12</month>
<year>2006</year>
</date>
<date date-type="accepted">
<day>15</day>
<month>2</month>
<year>2007</year>
</date>
</history>
<copyright-statement>© 2007 by the Infectious Diseases Society of America</copyright-statement>
<copyright-year>2007</copyright-year>
<abstract>
<p><bold><italic>Background</italic></bold>. Chikungunya is a reemerging disease. In 2005–2006, a severe outbreak occurred on Reunion Island in the southwestern part of the Indian Ocean. Other islands in this area were affected during the same period.</p>
<p><bold><italic>Methods</italic></bold>. Adult patients with acute chikungunya (defined as onset of fever and/or polyarthralgia in the 5 days preceding consultation) and laboratory-confirmed chikungunya who were referred to Groupe Hospitalier Sud Reunion during the period from March 2005 through April 2006 were included in this retrospective study. Their clinical and laboratory features are reported.</p>
<p><bold><italic>Results</italic></bold>. Laboratory-confirmed acute chikungunya was documented in 157 patients. The mean age of patients was 57.9 years, and the ratio of male to female patients was 1.24 : 1. Sixty percent of patients had at least 1 comorbidity. Ninety-seven patients (61.8%) were hospitalized, and 60 (38.2%) were treated as outpatients. Five fatalities were reported. One hundred fifty-one patients (96.1%) experienced polyarthralgia, and 129 (89%) experienced fever. Gastrointestinal symptoms were reported by 74 patients (47.1%), and skin rash was reported by 63 (40.1%). Hemorrhagic signs were rare. Lymphopenia and hypocalcemia were the prominent laboratory findings. Severe thrombocytopenia was rarely observed.</p>
<p><bold><italic>Conclusions</italic></bold>. Chikungunya virus can be responsible for explosive outbreaks of disease. Polyarthralgia and fever are the 2 main clinical features. In this era of travel and globalization, chikungunya should be considered in the differential diagnosis of febrile polyarthralgia with an abrupt onset.</p>
</abstract>
</article-meta>
</front>
<body>
<p>Chikungunya is a mosquitoborne disease caused by an alphavirus of the Togaviridae family. Chikungunya virus was first isolated from both humans and mosquitoes in 1953 during an epidemic of febrile polyarthralgia in Tanganyika [<xref rid="ref1" ref-type="bibr">1</xref>]. Since then, chikungunya virus has caused numerous epidemics in Africa, India, and southeast Asia that have involved hundreds of thousands of people [<xref rid="ref2" ref-type="bibr">2</xref>,<xref rid="ref8" ref-type="bibr">8</xref>]. The virus is transmitted by mosquitoes of the genus <italic>Aedes</italic>– (mainly <italic>Aedes aegypti</italic> and <italic>Aedes albopictus</italic>). Chikungunya is characterized by an abrupt clinical onset involving fever and polyarthralgia, sometimes followed by a maculopapular rash. The articular symptoms, often debilitating, usually resolve within days to a few weeks, but in some cases, they may last for months or even years [<xref rid="ref9" ref-type="bibr">9</xref>]. Sporadic cases of neurological and cardiac complications have been reported [<xref rid="ref10" ref-type="bibr">10</xref>–<xref rid="ref12" ref-type="bibr">12</xref>].</p>
<p>In August 2004, an outbreak of an acute febrile illness was reported in Lamu, Kenya [<xref rid="ref13" ref-type="bibr">13</xref>]. Most patients complained of severe joint pain. The attack rate was >50%. Chikungunya virus was later identified as the causative agent of this outbreak of illness. In the following months, other confirmed outbreaks of chikungunya were reported in Mombasa, Kenya (in November 2004), and in Grand Comores, an island in the Indian Ocean (from January to April 2005) [<xref rid="ref14" ref-type="bibr">14</xref>].</p>
<p>In March 2005, the first cases of chikungunya occurred on Reunion Island (a French overseas territory in the Indian Ocean), where this virus had never been detected before. The disease incidence was not relevant until the beginning of the hot and rainy season, in December 2005, when an explosive outbreak of illness began. It is estimated that 266,000 people (from a population of 770,000) were affected by chikungunya in the subsequent months. The disease incidence started to decrease in March 2006 [<xref rid="ref15" ref-type="bibr">15</xref>]. <italic>A. albopictus</italic> has been identified as the likely vector in the Reunion Island outbreak. Meanwhile, on other islands of the Indian Ocean (Madagascar, Seychelles, Mayotte, and Mauritius), cases of chikungunya were being reported [<xref rid="ref16" ref-type="bibr">16</xref>], and imported cases of chikungunya in several European countries (mostly France) occurred in travelers returning from Indian Ocean islands [<xref rid="ref17" ref-type="bibr">17</xref>]. Since February 2006, an epidemic of chikungunya has affected 8 states in India, with an estimated number of 1.25 million cases [<xref rid="ref18" ref-type="bibr">18</xref>]. In this study, we report the clinical features of and the laboratory findings for a series of 157 acutely ill adults with laboratory-confirmed chikungunya from the Reunion Island outbreak.</p>
<sec sec-type="materials|methods" id="sec1">
<title>Materials and Methods</title>
<p>Reunion Island is located in the southwestern part of the Indian Ocean, east of Madagascar. On Reunion Island, the medical system and accessibility to medical care are no different from that in France. The Groupe Hospitalier Sud Reunion is a tertiary nonteaching institution with a referral population of ∼350,000 people. The following 6 units participated in our study: Pulmonary and Infectious Diseases, Emergency Department, Endocrinology, Gastroenterology, Internal Medicine, and Neurology. As a first step, we investigated the records for patients with an RT-PCR and/or an IgM serologic test result positive for chikungunya virus (every ward kept a register of chikungunya cases) and who were referred to one of the units taking part in the study during the period from March 2005 through April 2006. After referral, patients were either treated as outpatients or hospitalized.</p>
<p>Our study included patients aged ≥16 years who presented with acute chikungunya. An acute case of chikungunya was defined as any case with a presentation of fever and/or polyarthralgia that occurred in the 5 days preceding the referral to our institution, with laboratory-confirmed diagnosis of chikungunya by RT-PCR, seroconversion on paired serum specimens, or positive IgM serologic test results. Patients with a positive IgM serologic test result (with a negative RT-PCR result or no RT-PCR data) in the 3 days after the onset of symptoms were considered to not have been affected by acute chikungunya and, therefore, were excluded from the study.</p>
<p>For this retrospective study, we reviewed the medical chart records for the enrolled patients to collect the following information: demographic characteristics, comorbidity data, clinical history, and physical examination and routine laboratory test findings (i.e., complete blood cell count, electrolyte level, kidney and liver function test results, creatinine kinase level, and C-reactive protein level) at admission. For hospitalized patients, laboratory tests were repeated during the hospital stay. Demographic data and laboratory findings for hospitalized patients were compared with those for nonhospitalized patients.</p>
<p>Chikungunya virus—specific IgM antibody was detected by IgM-capture ELISA [<xref rid="ref19" ref-type="bibr">19</xref>] using a chikungunya virus antigen produced by the Centre National de Référence des Arbovirus (Lyon, France). One-step TaqMan real-time quantitative RT-PCR was performed using the Light Cycler 2.0 system (Roche Diagnostics). Chikungunya virus RNA was extracted from 200 µL of plasma using the MagNa Pure system (Roche Diagnostics). The primers that we used were located in the glycoprotein E1 conserved region [<xref rid="ref20" ref-type="bibr">20</xref>].</p>
<p>Results are expressed as mean ± SD and as percentages. The Mann-Whitney <italic>U</italic> test was used to calculate differences in laboratory findings and continuous variables between hospitalized and nonhospitalized patients with chikungunya. Univariate analysis was conducted using the χ<sup>2</sup> test, with use of Fisher's exact test, as needed, for comparison of categorical variables between hospitalized and nonhospitalized patients. Adjusted ORs and 95% CIs were calculated. <italic>P</italic> values of <.05 were considered to be statistically significant.</p>
</sec>
<sec sec-type="results" id="sec2">
<title>Results</title>
<p>Among the 264 patients who presented with a RT-PCR and/or an IgM serologic test result positive for chikungunya virus, 157 had cases that fulfilled the case definition for acute chikungunya. Of the 107 patients who were not included, 92 were referred to the institution >5 days after the onset of symptoms, 10 had a positive IgM assay result in the 3 days after the onset of symptoms (with negative RT-PCR results or without having undergone RT-PCR testing), and 5 had incomplete clinical and laboratory data.</p>
<p>The demographic and clinical data for the enrolled patients are presented in <xref ref-type="fig" rid="tab1">table 1</xref>. The mean age of the patients was 57.9 years, and the ratio of male to female patients was 1.24 : 1. Forty-six patients (29.2%) had no underlying illness, and 29 patients (18.5%) had >2 underlying illnesses, the most common of which were blood hypertension and diabetes. The majority of patients (147 [93.6%]) were referred to our institution during the period from December 2005 through April 2006, which corresponded to the outbreak's peak.</p>
<p>Ninety-seven patients (61.8%) were hospitalized, and 60 patients (38.2%) were treated as outpatients. The mean length of hospital stay was 9.2 ± 7.3 days (range, 0–46 days). Older age and later referral were significantly more common among hospitalized patients, and the prevalences of diabetes and ischemic heart disease were also higher among hospitalized patients.</p>
<p>The diagnosis of chikungunya was confirmed by a positive RT-PCR result for 78 patients (49.7%), by a positive IgM antibody test result for 69 patients (43.9%), and by seroconversion noted in paired serum specimens in 10 patients (6.4%). <xref ref-type="fig" rid="tab2">Table 2</xref> shows the salient clinical features of the patients.</p>
<p>A total of 151 patients (96%) were experiencing arthralgia and 129 (89%) had fever on the day of referral. (Data about fever were available for 145 patients.) It is worth noting that, among the 17 patients who did not have a fever on that day (possibly because they had received treatment with antipyretics), 10 reported that they had experienced fever on the previous days. With this finding considered, we may consider that fever was present in 95.9% of patients. Fever was usually severe (mean temperature, 38.9°C) and had an abrupt onset.</p>
<p>Joint pain always involved >1 articulation. Oligoarthralgia or polyarthralgia was symmetrical in 73% of patients. Joint pain was mainly distal, and lower limbs were more frequently involved. Joint swelling was reported by 50 patients (31.8%).</p>
<p>Maculopapular skin rash was observed in 63 patients (40.1%). The rash was itchy in one-half of patients and rarely affected the face. Bullous skin lesions were noted in 3 patients. Seventy-four patients (47.1%) complained of gastrointestinal symptoms. Among other, less common signs and symptoms, lymphadenopathy (mostly cervical) was reported in 14 patients (8.9%), 4 patients (2.5%) had aphthous buccal ulcerations, and 14 patients (8.9%) presented with a dry cough.</p>
<p>Signs of neurologic involvement were reported in 19 cases (12%). Twelve patients (7.6%) presented in an acute confusional state. Two cases of convulsions were observed in patients who had a past medical history of epilepsy and a history of heavy alcohol consumption.</p>
<p>Hemorrhagic manifestations were present in 10 patients (6.4%). An alternative cause of the hemorrhagic manifestations was found for 3 of these 10 patients (1 case of hematemesis and 1 case of macroscopic hematuria were secondary to a complication of oral anticoagulant treatment, and 1 case of hemoptysis was due to a pulmonary embolism).</p>
<p>All patients with hemorrhagic signs had a platelet count of >100 × 10<sup>3</sup> platelets/mm<sup>3</sup>. Five patients (3 men and 2 women) died. The mean age of these patients was 79.4 years (range, 70–88 years), and the causes of death were as follows: respiratory failure in a patient with myasthenia, cardiac failure in a patient with ischemic cardiopathy, septic shock due to community-acquired <italic>Escherichia coli</italic> infection, respiratory failure secondary to a pleural effusion of unknown origin in a patient with gastric cancer, and myocardial infarct in a diabetic patient with brain stroke sequelae.</p>
<p>The laboratory findings for patients at hospital admission are shown in tables <xref ref-type="fig" rid="tab3">3</xref> and <xref ref-type="fig" rid="tab4">4</xref>. Lymphopenia (lymphocyte count, <1000 cells/mm<sup>3</sup>) was the most common abnormality; it was observed in 124 patients (79%) and was severe (i.e., the lymphocyte count was <500 cells/mm<sup>3</sup>) in 61 patients (38.9%). Moderate thrombocytopenia (thrombocyte count, <150 × 10<sup>3</sup> cells/mm<sup>3</sup>) was noted in 69 patients (43.9%). Hypocalcemia (blood calcium level, <2.25 mmol/L) was present in 86 patients (54.8%). Liver enzyme levels were 2-fold greater than normal values for <10% of patients. A marked increase in the creatinine kinase level occurred in 10% of patients. Creatinine and aspartate transaminase levels were significantly higher in hospitalized patients than in nonhospitalized patients. Impairment of renal function had to be assessed with consideration of the enrolled population: of 11 patients who presented with a creatinine level >200 µmol/L, 7 had previously experienced chronic renal failure.</p>
<p>For some of the hospitalized patients, additional laboratory tests were performed between days 3 and 5 of hospitalization. During days 3–5, thrombocytopenia was reported in 35 (51.5%) of 68 tested patients, and platelet counts were <100 × 10<sup>3</sup>/mm<sup>3</sup> in 17 patients (25%). Severe lymphopenia became less common (10% of patients), although the number of patients who had hypocalcemia increased (75% of patients).</p>
</sec>
<sec sec-type="discussion" id="sec3">
<title>Discussion</title>
<p>The first clinical description of chikungunya was given by Robinson [<xref rid="ref1" ref-type="bibr">1</xref>] during the Tanganyika epidemic in 1952–1953. In most of the additional clinical studies of chikungunya [<xref rid="ref3" ref-type="bibr">3</xref>–<xref rid="ref8" ref-type="bibr">8</xref>, <xref rid="ref21" ref-type="bibr">21</xref>, <xref rid="ref22" ref-type="bibr">22</xref>], the majority of reported cases did not have a laboratory-confirmed diagnosis, and some of these studies were performed in countries where dengue, a disease with signs and symptoms that can be similar to those of chikungunya, was frequently reported.</p>
<p>To our knowledge, the only clinical study that included a considerable number of patients (86 patients) with laboratory-confirmed diagnoses of chikungunya is the study by Thiruvengadam et al. [<xref rid="ref23" ref-type="bibr">23</xref>] about the Madras City outbreak, and this study dates back to 1965. Our study aims to fill this striking gap in clinical and laboratory reports about chikungunya, and to our knowledge, we describe the largest series of patients with laboratory-confirmed acute chikungunya to date.</p>
<p>The majority of the patients observed in this study were aged >45 years and presented with at least 1 comorbidity. As expected, hospitalized patients were significantly older and had more comorbidities than did patients who did not require hospitalization. The complication of an underlying illness often required a longer hospital stay. All 5 deaths that were reported in this study occurred among older patients with underlying illnesses. Chikungunya probably played an indirect role in these fatalities, but additional studies of its pathogenicity are clearly needed.</p>
<p>As previously reported, fever and polyarthralgia are the 2 chief clinical features of chikungunya. In our study, these features were present in almost all patients. Arthritis with effusion is rare in patients with chikungunya [<xref rid="ref9" ref-type="bibr">9</xref>], and it was absent in our study. The only articular sign noted in this study was soft-tissue swelling, which was present in 30% of patients.</p>
<p>We did not evaluate the intensity of arthralgia in this article. However, it is interesting to note that many patients described this pain as the worst they had ever experienced; the same observation was made by patients in the 1964 study by De Ranitz et al. [<xref rid="ref24" ref-type="bibr">24</xref>] during the Madras city epidemic. The description made by Robinson [<xref rid="ref1" ref-type="bibr">1</xref>] in 1955 ("the pain was frightening in its severity, completely immobilizing many patients"; p. 29) applied to some of the patients in our study.</p>
<p>In our judgement, polyarthralgia is particularly important in the differential diagnosis with dengue—a problem that clinicians encounter when they work in countries where both conditions are present. During the 2002 outbreak of dengue in Taiwan [<xref rid="ref25" ref-type="bibr">25</xref>], polyarthralgia was not reported in 644 confirmed cases in a population that was similar (with regard to age [mean age, 47 years] and the presence of comorbidities) to the one investigated in our study.</p>
<p>The frequency of skin rash, which was reported in 40% of patients, was probably underestimated. Thiruvengadam et al. [<xref rid="ref23" ref-type="bibr">23</xref>] noticed that exanthema appeared after the third day after onset of illness in 75% of patients, and in our study, most patients were examined within 2 days after the onset of the illness. In the previous reports, the occurrence of skin manifestations was extremely variable, ranging from 14% of patients in the study by Thiruvengadam et al. [<xref rid="ref23" ref-type="bibr">23</xref>] to 86% in a small South African study [<xref rid="ref20" ref-type="bibr">20</xref>]. As was recently reported in a group of travelers by Hochedez et al. [<xref rid="ref17" ref-type="bibr">17</xref>], we observed that skin rash rarely affected the patient's face. An associated itching has also been reported elsewhere [<xref rid="ref7" ref-type="bibr">7</xref>], but it did not occur with the frequency (53.9% of patients) reported in our study. Bullous lesions, which occurred in 3 patients in our study, had never been associated with chikungunya before the Reunion Island outbreak; several cases, mostly among children, were reported in the Reunion Island outbreak [<xref rid="ref26" ref-type="bibr">26</xref>].</p>
<p>Gastrointestinal symptoms were a quite common complaint among the patients in our study. Such complaints have already been described by other authors [<xref rid="ref5" ref-type="bibr">5</xref>, <xref rid="ref23" ref-type="bibr">23</xref>], but they have never occurred as frequently as they did in our study, in which one-half of patients were affected. It is interesting to note that a similar prevalence (abdominal pain, 42% of patients; diarrhea, 35% of patients) was reported in patients with dengue fever during the 2002 outbreak in Taiwan [<xref rid="ref25" ref-type="bibr">25</xref>].</p>
<p>Neurologic involvement in chikungunya has already been sporadically reported [<xref rid="ref10" ref-type="bibr">10</xref>]. During the Reunion Island outbreak, several cases of chikungunya encephalopathy were virologically proven [<xref rid="ref27" ref-type="bibr">27</xref>]. Patients with chikungunya encephalopathy were referred later in the course of disease (∼2 weeks after the onset of symptoms) and were thus not included in our study. The rate of acute confusion among the patients in our study (almost 10% of patients; mean age, 73.5 years) is probably associated with very severe fever among the elderly patients.</p>
<p>With the exception of the Calcutta epidemic in 1963 [<xref rid="ref28" ref-type="bibr">28</xref>], when the frequency of hemorrhagic manifestations was probably overestimated because of cocirculation of dengue virus, hemorrhagic signs are rarely reported in chikungunya. Our study confirms this observation. Very little is known about hematologic and biochemical findings in chikungunya; the few published reports involve small series of patients or patients without confirmed cases [<xref rid="ref7" ref-type="bibr">7</xref>,<xref rid="ref23" ref-type="bibr">23</xref>].</p>
<p>In this study, the hallmark laboratory findings at admission were lymphopenia, which was present in 124 patients (79%) and was severe (lymphocyte count, <500 cells/mm<sup>3</sup>) in 61 (39%), and hypocalcemia, which was observed in more than one-half of patients. If lymphopenia is commonly associated with viral infection, the origin of hypocalcemia is less clear. It may be of interest to note that this abnormality has been reported in patients with severe acute respiratory syndrome, too [<xref rid="ref29" ref-type="bibr">29</xref>]. Thrombocytopenia—a typical finding with dengue—was not prominent (38% of patients); it was moderate in most of the affected patients at the time of admission, but it was observed in one-half of patients later in the course of the disease.</p>
<p>Aspartate aminotransferase and serum creatinine levels were usually more elevated in hospitalized patients than in nonhospitalized patients. Because most patients received antipyretic and analgesic drugs (acetaminophen and/or nonsteroid anti-inflammatory drugs) before hospital admission, it is possible that these results are also related to drug toxicity in this vulnerable population.</p>
<p>This study has the usual limitations of a retrospective study. Symptoms and laboratory data may not have been recorded comprehensively, and this may have affected the results. The patients included in our report represent a very small sample of the population that was affected by chikungunya (∼266,000 people) during the Reunion Island outbreak. The majority of people consulted a general practitioner and were not referred to the hospital, so patients with milder forms of the disease are not represented in our study. Among the patients who were hospitalized, only a minority had laboratory-confirmed infection; for want of laboratory facilities, in most of cases, the diagnosis was presumed on the basis of clinical presentation, especially during the peak of the outbreak. Therefore, we may wonder whether the enrolled patients are representative of the general affected population. It is important to remember that, on Reunion Island, although the life expectancy at birth (75.5 years) is similar to that of industrialized countries, the age distribution is quite different with the majority of the population (65%) aged <40 years. Considering these data and the mean age of the included patients, we could conclude that there is a major selection bias, because most of the observed cases occurred in persons aged >40 years.</p>
<p>According to the estimates reported by the general practitioners on Reunion Island at the beginning of May 2006 [<xref rid="ref30" ref-type="bibr">30</xref>], 55% of adult patients with suspected chikungunya were women, and 57% were aged >45 years. These data seem to confirm that chikungunya, for reasons that are not clear and that deserve further research, more frequently affects middle-aged and elderly people. Comparing these data with the results of our study, in which male patients slightly predominated (55%) and in which 73% of patients were aged >45 years, the differences do not look major.</p>
<p><italic>A. albopictus</italic>, one of the competent vectors of chikungunya virus, can now be found in many temperate areas of the Eastern and Western Hemispheres, including Europe and the United States [<xref rid="ref31" ref-type="bibr">31</xref>]. Therefore, there is some risk that chikungunya virus could be introduced into previously unexposed areas, where it is not currently endemic, by travelers with viremia, thereby leading to local transmission of the virus. A prompt diagnosis of chikungunya is, therefore, paramount in countries where a competent vector is present, especially if the population has not been previously in contact with the virus. Early recognition of local transmission, followed by rapid, aggressive vector control and other public health measures, may prevent explosive outbreaks. We think that the data presented in this study represent a useful tool for the early diagnosis of this reemerging disease, which is often mistaken for diseases due to other arboviruses.</p>
</sec>
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<back>
<ack>
<title>Acknowledgments</title>
<p>We thank Drs. Patrice Tournebize, Marion Lagrange, and Alain Clabe for their assistance in data retrieval, as well as Dr. Liliane Cotte from the Centre d'Investigation Clinique for her assistance in reviewing the manuscript.</p>
<p><bold><italic>Potential conflicts of interest</italic></bold>. All authors: no conflicts.</p>
</ack>
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<sec sec-type="display-objects">
<title>Figures and Tables</title>
<fig position="float" id="tab1">
<label>Table 1</label>
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<p>Demographic and clinical data for hospitalized and nonhospitalized patients with acute chikungunya, with univariate analysis.</p>
</caption>
<graphic mimetype="image" xlink:href="44-11-1401-tbl001.tif"></graphic>
</fig>
<fig position="float" id="tab2">
<label>Table 2</label>
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<p>Clinical features of 157 patients with acute chikungunya.</p>
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<graphic mimetype="image" xlink:href="44-11-1401-tbl002.tif"></graphic>
</fig>
<fig position="float" id="tab3">
<label>Table 3</label>
<caption>
<p>Laboratory findings for patients with acute chikungunya on the day of referral.</p>
</caption>
<graphic mimetype="image" xlink:href="44-11-1401-tbl003.tif"></graphic>
</fig>
<fig position="float" id="tab4">
<label>Table 4</label>
<caption>
<p>Abnormal laboratory findings in patients with acute chikungunya on the day of referral.</p>
</caption>
<graphic mimetype="image" xlink:href="44-11-1401-tbl004.tif"></graphic>
</fig>
</sec>
</back>
</article></istex:document></istex:metadataXml><mods version="3.6"><titleInfo><title>Outbreak of Chikungunya on Reunion Island: Early Clinical and Laboratory Features in 157 Adult Patients</title></titleInfo><titleInfo type="alternative" contentType="CDATA"><title>Outbreak of Chikungunya on Reunion Island: Early Clinical and Laboratory Features in 157 Adult Patients</title></titleInfo><name type="personal" displayLabel="corresp"><namePart type="given">Gianandrea</namePart><namePart type="family">Borgherini</namePart><affiliation>Services de Pneumologie et Maladies Infectieuses, La Réunion, France</affiliation><affiliation>E-mail: gianu.borg@wanadoo.fr</affiliation><affiliation>Reprints or correspondence: Dr. Gianandrea Borgherini, Service de Pneumologie et Maladies Infectieuses, Groupe Hospitalier Sud Reunion, BP 350, 97448 Saint Pierre, La Réunion, France (gianu.borg@wanadoo.fr).</affiliation><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">Patrice</namePart><namePart type="family">Poubeau</namePart><affiliation>Services de Pneumologie et Maladies Infectieuses, La Réunion, France</affiliation><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">Frederik</namePart><namePart type="family">Staikowsky</namePart><affiliation>Urgences, La Réunion, France</affiliation><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">Manuella</namePart><namePart type="family">Lory</namePart><affiliation>Services de Pneumologie et Maladies Infectieuses, La Réunion, France</affiliation><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">Nathalie Le</namePart><namePart type="family">Moullec</namePart><affiliation>Endocrinologie, La Réunion, France</affiliation><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">Jean Philippe</namePart><namePart type="family">Becquart</namePart><affiliation>Gastro-enterologie, La Réunion, France</affiliation><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">Catherine</namePart><namePart type="family">Wengling</namePart><affiliation>Medecine Interne, La Réunion, France</affiliation><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">Alain</namePart><namePart type="family">Michault</namePart><affiliation>Laboratoire de Virologie, Groupe Hospitalier Sud Reunion, Saint Pierre, La Réunion, France</affiliation><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">Fabrice</namePart><namePart type="family">Paganin</namePart><affiliation>Services de Pneumologie et Maladies Infectieuses, La Réunion, France</affiliation><role><roleTerm type="text">author</roleTerm></role></name><typeOfResource>text</typeOfResource><genre type="research-article" displayLabel="research-article" authority="ISTEX" authorityURI="https://content-type.data.istex.fr" valueURI="https://content-type.data.istex.fr/ark:/67375/XTP-1JC4F85T-7">research-article</genre><originInfo><publisher>The University of Chicago Press</publisher><dateIssued encoding="w3cdtf">2007-06-01</dateIssued><dateCreated encoding="w3cdtf">2007-02-15</dateCreated><copyrightDate encoding="w3cdtf">2007</copyrightDate></originInfo><abstract>Background. Chikungunya is a reemerging disease. In 2005–2006, a severe outbreak occurred on Reunion Island in the southwestern part of the Indian Ocean. Other islands in this area were affected during the same period. Methods. Adult patients with acute chikungunya (defined as onset of fever and/or polyarthralgia in the 5 days preceding consultation) and laboratory-confirmed chikungunya who were referred to Groupe Hospitalier Sud Reunion during the period from March 2005 through April 2006 were included in this retrospective study. Their clinical and laboratory features are reported. Results. Laboratory-confirmed acute chikungunya was documented in 157 patients. The mean age of patients was 57.9 years, and the ratio of male to female patients was 1.24 : 1. Sixty percent of patients had at least 1 comorbidity. Ninety-seven patients (61.8%) were hospitalized, and 60 (38.2%) were treated as outpatients. Five fatalities were reported. One hundred fifty-one patients (96.1%) experienced polyarthralgia, and 129 (89%) experienced fever. Gastrointestinal symptoms were reported by 74 patients (47.1%), and skin rash was reported by 63 (40.1%). Hemorrhagic signs were rare. Lymphopenia and hypocalcemia were the prominent laboratory findings. Severe thrombocytopenia was rarely observed. Conclusions. Chikungunya virus can be responsible for explosive outbreaks of disease. Polyarthralgia and fever are the 2 main clinical features. 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