The spectrum of respiratory pathogens among returning Hajj pilgrims: myths and reality
Identifieur interne : 000D58 ( Pmc/Corpus ); précédent : 000D57; suivant : 000D59The spectrum of respiratory pathogens among returning Hajj pilgrims: myths and reality
Auteurs : Phillipe Gautret ; Samir Benkouiten ; Jaffar A. Al-Tawfiq ; Ziad A. MemishSource :
- International Journal of Infectious Diseases [ 1201-9712 ] ; 2016.
Abstract
Surveillance systems detect and investigate any possible cases of Middle East respiratory syndrome coronavirus (MERS-CoV) among travellers. Only a few sporadic travel-associated MERS-CoV cases have been reported in Hajj pilgrims. Respiratory infections were due to influenza viruses, rhinoviruses, and non-MERS coronaviruses.
Url:
DOI: 10.1016/j.ijid.2016.01.013
PubMed: 26845442
PubMed Central: 7110688
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PMC:7110688Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">The spectrum of respiratory pathogens among returning Hajj pilgrims: myths and reality</title><author><name sortKey="Gautret, Phillipe" sort="Gautret, Phillipe" uniqKey="Gautret P" first="Phillipe" last="Gautret">Phillipe Gautret</name><affiliation><nlm:aff id="aff0005">Aix Marseille Université, URMITE, UM63, CNRS 7278, IRD 198, Inserm 1095, 13005 Marseille, France</nlm:aff></affiliation></author><author><name sortKey="Benkouiten, Samir" sort="Benkouiten, Samir" uniqKey="Benkouiten S" first="Samir" last="Benkouiten">Samir Benkouiten</name><affiliation><nlm:aff id="aff0010">Institut Hospitalo-Universitaire Méditerranée Infection, Marseille, France</nlm:aff></affiliation></author><author><name sortKey="Al Tawfiq, Jaffar A" sort="Al Tawfiq, Jaffar A" uniqKey="Al Tawfiq J" first="Jaffar A." last="Al-Tawfiq">Jaffar A. Al-Tawfiq</name><affiliation><nlm:aff id="aff0015">Johns Hopkins Aramco Healthcare, Dhahran, Kingdom of Saudi Arabia</nlm:aff></affiliation><affiliation><nlm:aff id="aff0020">Indiana University School of Medicine, Indianapolis, USA</nlm:aff></affiliation></author><author><name sortKey="Memish, Ziad A" sort="Memish, Ziad A" uniqKey="Memish Z" first="Ziad A." last="Memish">Ziad A. Memish</name><affiliation><nlm:aff id="aff0025">Ministry of Health, Riyadh, College of Medicine, Al Faisal University, Kingdom of Saudi Arabia</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">26845442</idno><idno type="pmc">7110688</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7110688</idno><idno type="RBID">PMC:7110688</idno><idno type="doi">10.1016/j.ijid.2016.01.013</idno><date when="2016">2016</date><idno type="wicri:Area/Pmc/Corpus">000D58</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000D58</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">The spectrum of respiratory pathogens among returning Hajj pilgrims: myths and reality</title><author><name sortKey="Gautret, Phillipe" sort="Gautret, Phillipe" uniqKey="Gautret P" first="Phillipe" last="Gautret">Phillipe Gautret</name><affiliation><nlm:aff id="aff0005">Aix Marseille Université, URMITE, UM63, CNRS 7278, IRD 198, Inserm 1095, 13005 Marseille, France</nlm:aff></affiliation></author><author><name sortKey="Benkouiten, Samir" sort="Benkouiten, Samir" uniqKey="Benkouiten S" first="Samir" last="Benkouiten">Samir Benkouiten</name><affiliation><nlm:aff id="aff0010">Institut Hospitalo-Universitaire Méditerranée Infection, Marseille, France</nlm:aff></affiliation></author><author><name sortKey="Al Tawfiq, Jaffar A" sort="Al Tawfiq, Jaffar A" uniqKey="Al Tawfiq J" first="Jaffar A." last="Al-Tawfiq">Jaffar A. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Int J Infect Dis</journal-id><journal-id journal-id-type="iso-abbrev">Int. J. Infect. Dis</journal-id><journal-title-group><journal-title>International Journal of Infectious Diseases</journal-title></journal-title-group><issn pub-type="ppub">1201-9712</issn><issn pub-type="epub">1878-3511</issn><publisher><publisher-name>The Authors. Published by Elsevier Ltd on behalf of International Society for Infectious Diseases.</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">26845442</article-id><article-id pub-id-type="pmc">7110688</article-id><article-id pub-id-type="publisher-id">S1201-9712(16)00014-X</article-id><article-id pub-id-type="doi">10.1016/j.ijid.2016.01.013</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title>The spectrum of respiratory pathogens among returning Hajj pilgrims: myths and reality</article-title></title-group><contrib-group><contrib contrib-type="author" id="aut0005"><name><surname>Gautret</surname><given-names>Phillipe</given-names></name><email>philippe.gautret@club-internet.fr</email><xref rid="aff0005" ref-type="aff">a</xref><xref rid="cor0005" ref-type="corresp">⁎</xref></contrib><contrib contrib-type="author" id="aut0010"><name><surname>Benkouiten</surname><given-names>Samir</given-names></name><xref rid="aff0010" ref-type="aff">b</xref></contrib><contrib contrib-type="author" id="aut0015"><name><surname>Al-Tawfiq</surname><given-names>Jaffar A.</given-names></name><xref rid="aff0015" ref-type="aff">c</xref><xref rid="aff0020" ref-type="aff">d</xref></contrib><contrib contrib-type="author" id="aut0020"><name><surname>Memish</surname><given-names>Ziad A.</given-names></name><xref rid="aff0025" ref-type="aff">e</xref></contrib></contrib-group><aff id="aff0005"><label>a</label>Aix Marseille Université, URMITE, UM63, CNRS 7278, IRD 198, Inserm 1095, 13005 Marseille, France</aff><aff id="aff0010"><label>b</label>Institut Hospitalo-Universitaire Méditerranée Infection, Marseille, France</aff><aff id="aff0015"><label>c</label>Johns Hopkins Aramco Healthcare, Dhahran, Kingdom of Saudi Arabia</aff><aff id="aff0020"><label>d</label>Indiana University School of Medicine, Indianapolis, USA</aff><aff id="aff0025"><label>e</label>Ministry of Health, Riyadh, College of Medicine, Al Faisal University, Kingdom of Saudi Arabia</aff><author-notes><corresp id="cor0005"><label>⁎</label>Corresponding author. Tel.: +33 (0)491 96 35 35/36; fax: +33 (0)491 96 89 38. <email>philippe.gautret@club-internet.fr</email></corresp></author-notes><pub-date pub-type="pmc-release"><day>1</day><month>2</month><year>2016</year></pub-date><pmc-comment> PMC Release delay is 0 months and 0 days and was based on .</pmc-comment>
<pub-date pub-type="ppub"><month>6</month><year>2016</year></pub-date><pub-date pub-type="epub"><day>1</day><month>2</month><year>2016</year></pub-date><volume>47</volume><fpage>83</fpage><lpage>85</lpage><history><date date-type="received"><day>29</day><month>11</month><year>2015</year></date><date date-type="rev-recd"><day>23</day><month>1</month><year>2016</year></date><date date-type="accepted"><day>25</day><month>1</month><year>2016</year></date></history><permissions><copyright-statement>© 2016 The Authors</copyright-statement><copyright-year>2016</copyright-year><license><license-p>Since January 2020 Elsevier has created a COVID-19 resource centre with free information in English and Mandarin on the novel coronavirus COVID-19. The COVID-19 resource centre is hosted on Elsevier Connect, the company's public news and information website. Elsevier hereby grants permission to make all its COVID-19-related research that is available on the COVID-19 resource centre - including this research content - immediately available in PubMed Central and other publicly funded repositories, such as the WHO COVID database with rights for unrestricted research re-use and analyses in any form or by any means with acknowledgement of the original source. These permissions are granted for free by Elsevier for as long as the COVID-19 resource centre remains active.</license-p></license></permissions><abstract abstract-type="author-highlights" id="abs0005"><title>Highlights</title><p><list list-type="simple" id="lis0005"><list-item id="lsti0005"><label>•</label><p id="par0005">Surveillance systems detect and investigate any possible cases of Middle East respiratory syndrome coronavirus (MERS-CoV) among travellers.</p></list-item><list-item id="lsti0010"><label>•</label><p id="par0010">Only a few sporadic travel-associated MERS-CoV cases have been reported in Hajj pilgrims.</p></list-item><list-item id="lsti0015"><label>•</label><p id="par0015">Respiratory infections were due to influenza viruses, rhinoviruses, and non-MERS coronaviruses.</p></list-item></list></p></abstract><abstract id="abs0010"><title>Summary</title><p>Enhanced surveillance systems have been implemented recently in many countries in order to rapidly detect and investigate any possible cases of Middle East respiratory syndrome coronavirus (MERS-CoV) infection among travellers returning from the Middle East, including notably Hajj pilgrims. According to the available surveillance data, only a few sporadic travel-associated MERS-CoV cases have been reported outside the Arabian Peninsula so far, mainly in Europe, North Africa, and Asia. These have resulted in no cases, or limited numbers of secondary cases except in Korea. The vast majority of viral respiratory infections in pilgrims returning home have been due to seasonal influenza viruses, rhinoviruses, and other known coronaviruses distinct from the MERS coronavirus. Influenza vaccination should be a priority for all Hajj pilgrims, as recommended by experts.</p></abstract><kwd-group id="kwd0005"><title>Keywords</title><kwd>Surveillance</kwd><kwd>Hajj</kwd><kwd>Umrah</kwd><kwd>Coronavirus</kwd><kwd>Influenza</kwd><kwd>Rhinovirus</kwd></kwd-group></article-meta><notes><p id="misc0005"><bold>Corresponding Editor:</bold> Eskild Petersen, Aarhus, Denmark.</p></notes></front><body><p id="par0020">The emergence of severe acute respiratory syndrome coronavirus (SARS-CoV) in 2003 in China,<xref rid="bib0150" ref-type="bibr"><sup>1</sup></xref> the H1N1 influenza pandemic in 2009,<xref rid="bib0155" ref-type="bibr"><sup>2</sup></xref> and the emergence of Middle East respiratory syndrome coronavirus (MERS-CoV) in the Kingdom of Saudi Arabia (KSA) in 2012<xref rid="bib0160" ref-type="bibr"><sup>3</sup></xref> has aroused widespread fear and concern for their potential threat to global health security.<xref rid="bib0165" ref-type="bibr">4</xref>, <xref rid="bib0170" ref-type="bibr">5</xref> Elaborate surveillance and infection control measures were put in place during the 2009 Hajj. In the event, it was found that there were more cases of seasonal influenza reported than of H1N1.<xref rid="bib0175" ref-type="bibr"><sup>6</sup></xref></p><p id="par0025">One thousand six hundred and twenty-four laboratory-confirmed cases of MERS-CoV, including 586 related deaths, had been reported to the World Health Organization as of January 23, 2016 (<ext-link ext-link-type="uri" xlink:href="http://www.who.int/emergencies/mers-cov/en/" id="intr0005">http://www.who.int/emergencies/mers-cov/en/</ext-link>). Millions of Muslims, from over 180 countries worldwide, make the annual pilgrimage to Mecca, Saudi Arabia. Due to the overcrowded conditions, there is the potential for increased person-to-person spread of infectious diseases and a favourable transmission of respiratory tract infections.<xref rid="bib0175" ref-type="bibr"><sup>6</sup></xref> The occurrence of such events spreads fear of a massive outbreak among pilgrims that could spread to their countries of origin.<xref rid="bib0180" ref-type="bibr"><sup>7</sup></xref></p><p id="par0030">This situation has prompted health authorities to establish enhanced surveillance systems in many countries in order to rapidly detect and investigate any possible cases of MERS-CoV infection among travellers returning from the Middle East. Fortunately, only a few sporadic travel-associated MERS-CoV cases have been reported outside the Arabian Peninsula, mainly in Europe, North Africa, and Asia.<xref rid="bib0185" ref-type="bibr">8</xref>, <xref rid="bib0190" ref-type="bibr">9</xref> These have resulted in no cases, or some secondary cases, with the notable exception of the Republic of Korea. In the Republic of Korea, 185 cases were epidemiologically linked to a single index case who had visited several countries in the Middle East.<xref rid="bib0195" ref-type="bibr"><sup>10</sup></xref></p><p id="par0035">A large-scale surveillance study has provided interesting insights into the epidemiology of respiratory tract infections in travellers returning from the Middle East, including Hajj and Umrah pilgrims. During September 2012 to October 2013, 77 travellers from the Middle East who met the possible case definition for MERS were tested in England and two of them tested positive for MERS-CoV.<xref rid="bib0200" ref-type="bibr"><sup>11</sup></xref> Also, 22 had positive results for alternative respiratory pathogens, including 10 (13%) cases of influenza A or B and four (5%) cases of rhinovirus.<xref rid="bib0190" ref-type="bibr"><sup>9</sup></xref> UK surveillance data focusing on the period of return of Hajj pilgrims during the years 2013–2015 (September–October) evidenced influenza infection in 46% and rhinovirus in 30% of 50 patients suspected of MERS (<ext-link ext-link-type="uri" xlink:href="https://www.gov.uk/government/publications/health-protection-report-volume-9-2015/hpr-volume-9-issue-36-news-9-october" id="intr0010">https://www.gov.uk/government/publications/health-protection-report-volume-9-2015/hpr-volume-9-issue-36-news-9-october</ext-link>). Of the first 14 patients returning from the Middle East who were hospitalized for respiratory symptoms and screened for MERS-CoV in Marseille, France in October 2013, nine (64%) were infected with influenza and all samples tested negative for MERS-CoV.<xref rid="bib0205" ref-type="bibr"><sup>12</sup></xref> In another small survey conducted in 2014 in Austria and investigating seven Hajj pilgrims suspected of MERS, none had MERS-CoV, five had influenza, and two were infected by rhinovirus.<xref rid="bib0210" ref-type="bibr"><sup>13</sup></xref> A survey conducted among 177 travellers from the Middle East suspected of MERS on returning to Ontario, Canada in 2012–2014, showed that none tested positive for MERS-CoV, 41 (23%) were positive for influenza, and 35 (20%) for rhinovirus.<xref rid="bib0215" ref-type="bibr"><sup>14</sup></xref> Finally, in a survey conducted in 2013–2014 in California, USA among 52 patients suspected of MERS, none was positive for MERS, 17 (33%) were positive for influenza, and seven (13%) for rhinovirus.<xref rid="bib0220" ref-type="bibr"><sup>15</sup></xref> Other pathogens were isolated in smaller proportions, including parainfluenza viruses, human metapneumovirus, respiratory syncytial virus, enterovirus, adenovirus, non-MERS coronaviruses, <italic>Chlamydia pneumoniae</italic>, and <italic>Legionella spp</italic>.<xref rid="bib0200" ref-type="bibr">11</xref>, <xref rid="bib0205" ref-type="bibr">12</xref>, <xref rid="bib0210" ref-type="bibr">13</xref>, <xref rid="bib0215" ref-type="bibr">14</xref>, <xref rid="bib0220" ref-type="bibr">15</xref></p><p id="par0040">Besides surveillance implemented in returned travellers suspected of MERS, several teams in Egypt, Iran, Saudi Arabia, France, and Ghana have conducted systematic PCR-based screening surveys among cohorts of returning Hajj pilgrims independently of their clinical status. MERS-CoV carriage was investigated in four studies and was not detected.<xref rid="bib0205" ref-type="bibr">12</xref>, <xref rid="bib0225" ref-type="bibr">16</xref>, <xref rid="bib0230" ref-type="bibr">17</xref>, <xref rid="bib0235" ref-type="bibr">18</xref> Influenza carriage was investigated in six studies and its mean prevalence was 3% (range 1–8%);<xref rid="bib0235" ref-type="bibr">18</xref>, <xref rid="bib0240" ref-type="bibr">19</xref>, <xref rid="bib0245" ref-type="bibr">20</xref>, <xref rid="bib0250" ref-type="bibr">21</xref>, <xref rid="bib0255" ref-type="bibr">22</xref>, <xref rid="bib0260" ref-type="bibr">23</xref> rhinovirus carriage was investigated in four studies and its mean prevalence was 13% (range 8–17%).<xref rid="bib0235" ref-type="bibr">18</xref>, <xref rid="bib0250" ref-type="bibr">21</xref>, <xref rid="bib0255" ref-type="bibr">22</xref>, <xref rid="bib0260" ref-type="bibr">23</xref> Carriage of non-MERS coronavirus was investigated in two studies and the prevalence was found to be 1% and 21%, respectively.<xref rid="bib0250" ref-type="bibr">21</xref>, <xref rid="bib0260" ref-type="bibr">23</xref> Finally, the carriage of <italic>Streptococcus pneumoniae</italic> was investigated in two studies, which reported prevalences of 20% (nasal carriage) and 62% (throat carriage).<xref rid="bib0255" ref-type="bibr">22</xref>, <xref rid="bib0260" ref-type="bibr">23</xref> Other viruses were isolated in smaller proportions, including parainfluenza viruses, human metapneumovirus, respiratory syncytial virus, enterovirus, and adenovirus.<xref rid="bib0235" ref-type="bibr">18</xref>, <xref rid="bib0250" ref-type="bibr">21</xref>, <xref rid="bib0255" ref-type="bibr">22</xref>, <xref rid="bib0260" ref-type="bibr">23</xref> Finally, two PCR-based studies were conducted among returning Iranian pilgrims suffering from upper respiratory tract infections and reported a prevalence of influenza of 10% and 12%, respectively.<xref rid="bib0265" ref-type="bibr">24</xref>, <xref rid="bib0270" ref-type="bibr">25</xref></p><p id="par0045">Taken together, these results strongly suggest that Mecca may act as a global hub for respiratory pathogens through the Muslim pilgrimage and contribute to their globalization.<xref rid="bib0275" ref-type="bibr"><sup>26</sup></xref></p><p id="par0050">Obviously, the vast majority of viral respiratory infections in Hajj and Umrah pilgrims returning home are due to seasonal influenza viruses, rhinoviruses, and other know coronaviruses distinct from the MERS coronavirus. Bacteria like <italic>S. pneumoniae</italic> may also play a role, as well as <italic>Haemophilus influenzae</italic> and <italic>Klebsiella pneumoniae</italic>, for which a high rate of acquisition following participation in the Hajj has been observed in pilgrims before leaving Saudi Arabia.<xref rid="bib0275" ref-type="bibr"><sup>26</sup></xref> Tuberculosis has also been reported among patients admitted to hospital during the Hajj;<xref rid="bib0175" ref-type="bibr"><sup>6</sup></xref> however, given the incubation time of the disease, it is challenging to identify such cases.</p><p id="par0055">Clinicians should be aware that influenza is the most commonly identified pathogen in returning pilgrims with an acute respiratory tract infection. However, a microbial cause is not identified in a significant proportion of patients with a respiratory infection, which makes the overall incidence of influenza very low. Empirical antiviral treatment for influenza on admission when indicated may be considered pending the results of laboratory investigations, although oseltamivir resistance among influenza strains has been reported. Influenza vaccination should be a priority for all Hajj pilgrims, as recommended by experts.<xref rid="bib0280" ref-type="bibr">27</xref>, <xref rid="bib0285" ref-type="bibr">28</xref> However, since Hajj dates are now moving to the summer season, the lack of availability of the influenza vaccine in many countries during this period will hamper this strategy. Public health measures introduced by Saudi Arabia in 2015, banning the sacrifice of camels for Hajj and discouraging visits by pilgrims to camel barns during Hajj pilgrimage activities, are sensible precautionary measures that should be considered as part of pre-travel advice in the home countries of pilgrims.</p><p id="par0060">Despite the paucity of actual cases of MERS in travellers returning from the Middle East and the virtual absence of Hajj-associated cases in this context, continuous surveillance should be implemented to ensure the timely detection of possible imported cases of MERS and their immediate isolation in order to avoid secondary cases. The recent experience in South Korea, with a single chain of transmission associated with healthcare facilities resulting in many cases, is a reminder that enhanced surveillance at ports of entry is critical. The few pilgrimage-associated cases of MERS in travellers reported so far were in Umrah pilgrims.<xref rid="bib0180" ref-type="bibr"><sup>7</sup></xref> An estimated eight million pilgrims perform the Umrah yearly.<xref rid="bib0290" ref-type="bibr"><sup>29</sup></xref> The number of Umrah pilgrims is particularly high during the month of Ramadan, and that period could be considered the second mass gathering in Saudi Arabia, although of a lesser size compared to the Hajj. Studies on respiratory tract infections during Ramadan are scarce; thus continued surveillance of respiratory infections and of the spectrum of associated pathogens among pilgrims returning from the Umrah during Ramadan and from the subsequent Hajj is of critical importance.</p><p id="par0065"><italic>Conflict of interest:</italic> No conflict of interest to declare.</p></body><back><ref-list id="bibl0005"><title>References</title><ref id="bib0150"><label>1</label><element-citation publication-type="journal" id="sbref0150"><person-group person-group-type="author"><name><surname>Lee</surname><given-names>N.</given-names></name><name><surname>Hui</surname><given-names>D.</given-names></name><name><surname>Wu</surname><given-names>A.</given-names></name><name><surname>Chan</surname><given-names>P.</given-names></name><name><surname>Cameron</surname><given-names>P.</given-names></name><name><surname>Joynt</surname><given-names>G.M.</given-names></name></person-group><article-title>A major 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