A systematic review of emerging respiratory viruses at the Hajj and possible coinfection with Streptococcus pneumoniae
Identifieur interne : 001414 ( Pmc/Corpus ); précédent : 001413; suivant : 001415A systematic review of emerging respiratory viruses at the Hajj and possible coinfection with Streptococcus pneumoniae
Auteurs : Jaffar A. Al-Tawfiq ; Samir Benkouiten ; Ziad A. MemishSource :
- Travel Medicine and Infectious Disease [ 1477-8939 ] ; 2018.
Abstract
The annual Hajj to the Kingdom of Saudi Arabia attracts millions of pilgrims from around the world. International health community's attention goes towards this mass gathering and the possibility of the development of any respiratory tract infections due to the high risk of acquisition of respiratory viruses.
We searched MEDLINE/PubMed and Scopus databases for relevant papers describing the prevalence of respiratory viruses among Hajj pilgrims.
The retrieved articles were summarized based on the methodology of testing for these viruses. A total of 31 studies were included in the quantitative/qualitative analyses. The main methods used for the diagnosis of most common respiratory viruses were polymerase chain reaction (PCR), culture and enzyme-linked immunosorbent assay (ELISA). Influenza, rhinovirus and parainfluenza were the most common viruses detected among pilgrims. Coronaviruses other than MERS-CoV were also detected among pilgrims. The acquisition of MERS-CoV remains very limited and systematic screening of pilgrims showed no infections.
Well conducted multinational follow-up studies using the same methodology of testing are necessary for accurate surveillance of respiratory viral infections among Hajj pilgrims. Post-Hajj cohort studies would further evaluate the impact of the Hajj on the acquisition of respiratory viruses.
Url:
DOI: 10.1016/j.tmaid.2018.04.007
PubMed: 29673810
PubMed Central: 7110954
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PMC:7110954Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">A systematic review of emerging respiratory viruses at the Hajj and possible coinfection with <italic>Streptococcus pneumoniae</italic></title><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="aff1">Specialty Internal Medicine Unit, Johns Hopkins Aramco Healthcare, Dhahran, Saudi Arabia</nlm:aff></affiliation><affiliation><nlm:aff id="aff2">Indiana University School of Medicine, Indianapolis, IN 46202, USA</nlm:aff></affiliation><affiliation><nlm:aff id="aff3">Johns Hopkins University School of Medicine, Baltimore, MD, USA</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="aff4">Aix Marseille Université, URMITE, UM63, CNRS 7278, IRD 198, Inserm 1095, 13005 Marseille, France</nlm:aff></affiliation><affiliation><nlm:aff id="aff5">Institut Hospitalo-Universitaire Méditerranée Infection, Marseille, France</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="aff6">Department of Medicine and Research, Prince Mohammed Bin Abdulaziz Hospital, Ministry of Health, College of Medicine, Alfaisal University, Riyadh, Saudi Arabia</nlm:aff></affiliation><affiliation><nlm:aff id="aff7">Rollins School of Public Health, Emory University, Atlanta, GA, United States</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">29673810</idno><idno type="pmc">7110954</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7110954</idno><idno type="RBID">PMC:7110954</idno><idno type="doi">10.1016/j.tmaid.2018.04.007</idno><date when="2018">2018</date><idno type="wicri:Area/Pmc/Corpus">001414</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">001414</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">A systematic review of emerging respiratory viruses at the Hajj and possible coinfection with <italic>Streptococcus pneumoniae</italic></title><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="aff1">Specialty Internal Medicine Unit, Johns Hopkins Aramco Healthcare, Dhahran, Saudi Arabia</nlm:aff></affiliation><affiliation><nlm:aff id="aff2">Indiana University School of Medicine, Indianapolis, IN 46202, USA</nlm:aff></affiliation><affiliation><nlm:aff id="aff3">Johns Hopkins University School of Medicine, Baltimore, MD, USA</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="aff4">Aix Marseille Université, URMITE, UM63, CNRS 7278, IRD 198, Inserm 1095, 13005 Marseille, France</nlm:aff></affiliation><affiliation><nlm:aff id="aff5">Institut Hospitalo-Universitaire Méditerranée Infection, Marseille, France</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="aff6">Department of Medicine and Research, Prince Mohammed Bin Abdulaziz Hospital, Ministry of Health, College of Medicine, Alfaisal University, Riyadh, Saudi Arabia</nlm:aff></affiliation><affiliation><nlm:aff id="aff7">Rollins School of Public Health, Emory University, Atlanta, GA, United States</nlm:aff></affiliation></author></analytic><series><title level="j">Travel Medicine and Infectious Disease</title><idno type="ISSN">1477-8939</idno><idno type="eISSN">1873-0442</idno><imprint><date when="2018">2018</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec><title>Background</title><p>The annual Hajj to the Kingdom of Saudi Arabia attracts millions of pilgrims from around the world. International health community's attention goes towards this mass gathering and the possibility of the development of any respiratory tract infections due to the high risk of acquisition of respiratory viruses.</p></sec><sec><title>Method</title><p>We searched MEDLINE/PubMed and Scopus databases for relevant papers describing the prevalence of respiratory viruses among Hajj pilgrims.</p></sec><sec><title>Results</title><p>The retrieved articles were summarized based on the methodology of testing for these viruses. A total of 31 studies were included in the quantitative/qualitative analyses. The main methods used for the diagnosis of most common respiratory viruses were polymerase chain reaction (PCR), culture and enzyme-linked immunosorbent assay (ELISA). Influenza, rhinovirus and parainfluenza were the most common viruses detected among pilgrims. Coronaviruses other than MERS-CoV were also detected among pilgrims. The acquisition of MERS-CoV remains very limited and systematic screening of pilgrims showed no infections.</p></sec><sec><title>Conclusions</title><p>Well conducted multinational follow-up studies using the same methodology of testing are necessary for accurate surveillance of respiratory viral infections among Hajj pilgrims. Post-Hajj cohort studies would further evaluate the impact of the Hajj on the acquisition of respiratory viruses.</p></sec></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Memish, Z A" uniqKey="Memish Z">Z.A. Memish</name></author><author><name sortKey="Zumla, A" uniqKey="Zumla A">A. Zumla</name></author><author><name sortKey="Alhakeem, R F" uniqKey="Alhakeem R">R.F. Alhakeem</name></author><author><name sortKey="Assiri, A" uniqKey="Assiri A">A. Assiri</name></author><author><name sortKey="Turkestani, A" uniqKey="Turkestani A">A. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Travel Med Infect Dis</journal-id><journal-id journal-id-type="iso-abbrev">Travel Med Infect Dis</journal-id><journal-title-group><journal-title>Travel Medicine and Infectious Disease</journal-title></journal-title-group><issn pub-type="ppub">1477-8939</issn><issn pub-type="epub">1873-0442</issn><publisher><publisher-name>Elsevier Ltd.</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">29673810</article-id><article-id pub-id-type="pmc">7110954</article-id><article-id pub-id-type="publisher-id">S1477-8939(18)30060-7</article-id><article-id pub-id-type="doi">10.1016/j.tmaid.2018.04.007</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title>A systematic review of emerging respiratory viruses at the Hajj and possible coinfection with <italic>Streptococcus pneumoniae</italic></article-title></title-group><contrib-group><contrib contrib-type="author" id="au1"><name><surname>Al-Tawfiq</surname><given-names>Jaffar A.</given-names></name><xref rid="aff1" ref-type="aff">a</xref><xref rid="aff2" ref-type="aff">b</xref><xref rid="aff3" ref-type="aff">c</xref></contrib><contrib contrib-type="author" id="au2"><name><surname>Benkouiten</surname><given-names>Samir</given-names></name><xref rid="aff4" ref-type="aff">d</xref><xref rid="aff5" ref-type="aff">e</xref></contrib><contrib contrib-type="author" id="au3"><name><surname>Memish</surname><given-names>Ziad A.</given-names></name><email>zmemish@yahoo.com</email><xref rid="aff6" ref-type="aff">f</xref><xref rid="aff7" ref-type="aff">g</xref><xref rid="cor1" ref-type="corresp">∗</xref></contrib></contrib-group><aff id="aff1"><label>a</label>Specialty Internal Medicine Unit, Johns Hopkins Aramco Healthcare, Dhahran, Saudi Arabia</aff><aff id="aff2"><label>b</label>Indiana University School of Medicine, Indianapolis, IN 46202, USA</aff><aff id="aff3"><label>c</label>Johns Hopkins University School of Medicine, Baltimore, MD, USA</aff><aff id="aff4"><label>d</label>Aix Marseille Université, URMITE, UM63, CNRS 7278, IRD 198, Inserm 1095, 13005 Marseille, France</aff><aff id="aff5"><label>e</label>Institut Hospitalo-Universitaire Méditerranée Infection, Marseille, France</aff><aff id="aff6"><label>f</label>Department of Medicine and Research, Prince Mohammed Bin Abdulaziz Hospital, Ministry of Health, College of Medicine, Alfaisal University, Riyadh, Saudi Arabia</aff><aff id="aff7"><label>g</label>Rollins School of Public Health, Emory University, Atlanta, GA, United States</aff><author-notes><corresp id="cor1"><label>∗</label>Corresponding author. Ministry of Health, P.O. Box 54146, Riyadh 11514, Saudi Arabia. <email>zmemish@yahoo.com</email></corresp></author-notes><pub-date pub-type="pmc-release"><day>16</day><month>4</month><year>2018</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" iso-8601-date="2018-06-01"><season>May-June</season><year>2018</year></pub-date><pub-date pub-type="epub"><day>16</day><month>4</month><year>2018</year></pub-date><volume>23</volume><fpage>6</fpage><lpage>13</lpage><history><date date-type="received"><day>28</day><month>2</month><year>2018</year></date><date date-type="rev-recd"><day>10</day><month>4</month><year>2018</year></date><date date-type="accepted"><day>11</day><month>4</month><year>2018</year></date></history><permissions><copyright-statement>© 2018 Elsevier Ltd. All rights reserved.</copyright-statement><copyright-year>2018</copyright-year><copyright-holder>Elsevier Ltd</copyright-holder><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 id="abs0010"><sec><title>Background</title><p>The annual Hajj to the Kingdom of Saudi Arabia attracts millions of pilgrims from around the world. International health community's attention goes towards this mass gathering and the possibility of the development of any respiratory tract infections due to the high risk of acquisition of respiratory viruses.</p></sec><sec><title>Method</title><p>We searched MEDLINE/PubMed and Scopus databases for relevant papers describing the prevalence of respiratory viruses among Hajj pilgrims.</p></sec><sec><title>Results</title><p>The retrieved articles were summarized based on the methodology of testing for these viruses. A total of 31 studies were included in the quantitative/qualitative analyses. The main methods used for the diagnosis of most common respiratory viruses were polymerase chain reaction (PCR), culture and enzyme-linked immunosorbent assay (ELISA). Influenza, rhinovirus and parainfluenza were the most common viruses detected among pilgrims. Coronaviruses other than MERS-CoV were also detected among pilgrims. The acquisition of MERS-CoV remains very limited and systematic screening of pilgrims showed no infections.</p></sec><sec><title>Conclusions</title><p>Well conducted multinational follow-up studies using the same methodology of testing are necessary for accurate surveillance of respiratory viral infections among Hajj pilgrims. Post-Hajj cohort studies would further evaluate the impact of the Hajj on the acquisition of respiratory viruses.</p></sec></abstract><kwd-group id="kwrds0010"><title>Keywords</title><kwd>Respiratory viruses</kwd><kwd>Streptococcus pneumonia</kwd><kwd>Hajj</kwd><kwd>Mass gatherings</kwd><kwd>Saudi Arabia</kwd></kwd-group></article-meta></front><body><sec id="sec1"><label>1</label><title>Introduction</title><p id="p0010">Religious events and festivals are types of mass gathering that draw large numbers of pilgrims from a large geographical region and people around the globe [<xref rid="bib1" ref-type="bibr">1</xref>,<xref rid="bib2" ref-type="bibr">2</xref>]. The annual Hajj pilgrimage to Makkah in the Kingdom of Saudi Arabia (KSA) attracts more than 2 million pilgrims from 184 countries around the world [<xref rid="bib1" ref-type="bibr">1</xref>]. The climatic conditions and the inevitable overcrowding of pilgrims in Makkah and surrounding holy sites during the Hajj rituals create a situation that may promote the occurrence and spread of communicable diseases and possibly the spread of multi-drug resistance (MDR) bacteria [<xref rid="bib1" ref-type="bibr">1</xref>,<xref rid="bib3" ref-type="bibr">[3]</xref>, <xref rid="bib4" ref-type="bibr">[4]</xref>, <xref rid="bib5" ref-type="bibr">[5]</xref>, <xref rid="bib6" ref-type="bibr">[6]</xref>, <xref rid="bib7" ref-type="bibr">[7]</xref>, <xref rid="bib8" ref-type="bibr">[8]</xref>, <xref rid="bib9" ref-type="bibr">[9]</xref>]. Thus, the spread of respiratory illnesses during the Hajj is a major public health concerns with the potential of dissemination of these infectious diseases beyond the Hajj itself [<xref rid="bib10" ref-type="bibr">[10]</xref>, <xref rid="bib11" ref-type="bibr">[11]</xref>, <xref rid="bib12" ref-type="bibr">[12]</xref>]. Risk factors for such an event to occur include close proximity between pilgrims, crowded accommodation, and congregation [<xref rid="bib1" ref-type="bibr">1</xref>,<xref rid="bib6" ref-type="bibr">6</xref>]. Studies had shown that respiratory tract infections occur commonly among the majority of pilgrims [<xref rid="bib10" ref-type="bibr">10</xref>,<xref rid="bib13" ref-type="bibr">13</xref>]. Also, it is estimated that more than 90% of pilgrims develop what is known as the “Hajj cough” during their stay in KSA [<xref rid="bib14" ref-type="bibr">[14]</xref>, <xref rid="bib15" ref-type="bibr">[15]</xref>, <xref rid="bib16" ref-type="bibr">[16]</xref>]. Many studies showed that a variety of upper and lower respiratory tract infections due to viral and bacterial infections can cause infections among pilgrims [<xref rid="bib3" ref-type="bibr">[3]</xref>, <xref rid="bib4" ref-type="bibr">[4]</xref>, <xref rid="bib5" ref-type="bibr">[5]</xref>,<xref rid="bib10" ref-type="bibr">10</xref>,<xref rid="bib17" ref-type="bibr">[17]</xref>, <xref rid="bib18" ref-type="bibr">[18]</xref>, <xref rid="bib19" ref-type="bibr">[19]</xref>, <xref rid="bib20" ref-type="bibr">[20]</xref>, <xref rid="bib21" ref-type="bibr">[21]</xref>]. A range of respiratory viruses were recovered from pilgrims, with influenza and rhinovirus the most common [<xref rid="bib10" ref-type="bibr">10</xref>]. In this review, we summarize the available data about emerging respiratory viruses, including Middle East Respiratory Syndrome Coronavirus (MERS-CoV), Severe Acute Respiratory Syndrome (SARS), and other respiratory viruses such as influenza. We also discuss here the possible role of <italic>Streptococcus pneumoniae</italic> coinfection.</p></sec><sec id="sec2"><label>2</label><title>Search strategy</title><p id="p0015">We searched MEDLINE and Scopus databases for articles published in English using the following search strategy:</p><p id="p0020">#1: “hadj” OR “hajj” OR “pilgrimage”;</p><p id="p0025">#2: “respiratory”;</p><p id="p0030">#3: “viral” OR “virus” OR “viruses” OR “pathogens” OR “infection” OR “infections”;</p><p id="p0035">#4: “influenza”;</p><p id="p0040">#5: “Middle East Respiratory Syndrome Coronavirus” OR “MERS-CoV”;</p><p id="p0045">#6: “Severe Acute Respiratory Syndrome” OR “SARS”;</p><p id="p0050">#7: “Pandemic H1N1”;</p><p id="p0055">#8: #1 AND #2 AND #3 AND #4 AND #5 AND #6 AND #7.</p><p id="p0060">We also hand searched the Saudi Epidemiology Bulletin (available at: <ext-link ext-link-type="uri" xlink:href="http://www.fetp.edu.sa/Bulletin.html" id="intref0010">http://www.fetp.edu.sa/Bulletin.html</ext-link>) for additional articles for inclusion.</p><p id="p0065">The search results were surveyed for methodological articles, and their titles and abstracts were then scanned. Additional studies were identified through bibliographies of original articles or relevant reviews. The search was done according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines [<xref rid="bib22" ref-type="bibr">22</xref>]. One author (JAT) performed the searches, screened titles/abstracts for eligibility, selected relevant papers and reviewed each of the selected manuscripts in full. All authors were in agreement regarding the choice of papers.</p></sec><sec id="sec3"><label>3</label><title>Results</title><sec id="sec3.1"><label>3.1</label><title>Included studies</title><p id="p0070">The search strategy initially yielded 365 records of which 71 were duplicates. Twenty additional papers were identified through hand searching. Of the 104 full text articles reviewed, 31 studies were included in the final analysis. The results of the search strategy are shown in <xref rid="fig1" ref-type="fig">Fig. 1</xref>according to the PRISMA methodology [<xref rid="bib22" ref-type="bibr">22</xref>].<fig id="fig1"><label>Fig. 1</label><caption><p>Flow diagram of the search strategy.</p></caption><alt-text id="alttext0010">Fig. 1</alt-text><graphic xlink:href="gr1_lrg"></graphic></fig></p></sec><sec id="sec3.2"><label>3.2</label><title>Types of included studies</title><p id="p0075">The included studies were classified based on the methods used to detect respiratory viruses. Methods include polymerase chain reaction (PCR) [<xref rid="bib15" ref-type="bibr">15</xref>,<xref rid="bib23" ref-type="bibr">[23]</xref>, <xref rid="bib24" ref-type="bibr">[24]</xref>, <xref rid="bib25" ref-type="bibr">[25]</xref>, <xref rid="bib26" ref-type="bibr">[26]</xref>, <xref rid="bib27" ref-type="bibr">[27]</xref>, <xref rid="bib28" ref-type="bibr">[28]</xref>, <xref rid="bib29" ref-type="bibr">[29]</xref>, <xref rid="bib30" ref-type="bibr">[30]</xref>, <xref rid="bib31" ref-type="bibr">[31]</xref>, <xref rid="bib32" ref-type="bibr">[32]</xref>, <xref rid="bib33" ref-type="bibr">[33]</xref>, <xref rid="bib34" ref-type="bibr">[34]</xref>, <xref rid="bib35" ref-type="bibr">[35]</xref>, <xref rid="bib36" ref-type="bibr">[36]</xref>, <xref rid="bib37" ref-type="bibr">[37]</xref>, <xref rid="bib38" ref-type="bibr">[38]</xref>, <xref rid="bib39" ref-type="bibr">[39]</xref>, <xref rid="bib40" ref-type="bibr">[40]</xref>, <xref rid="bib41" ref-type="bibr">[41]</xref>, <xref rid="bib42" ref-type="bibr">[42]</xref>] (<xref rid="tbl1" ref-type="table">Table 1</xref>), cell culture [<xref rid="bib26" ref-type="bibr">26</xref>,<xref rid="bib27" ref-type="bibr">27</xref>,<xref rid="bib43" ref-type="bibr">[43]</xref>, <xref rid="bib44" ref-type="bibr">[44]</xref>, <xref rid="bib45" ref-type="bibr">[45]</xref>] (<xref rid="tbl2" ref-type="table">Table 2</xref>), direct immunofluorescence staining [<xref rid="bib46" ref-type="bibr">46</xref>], and enzyme-linked immunosorbent assay (ELISA) [<xref rid="bib47" ref-type="bibr">[47]</xref>, <xref rid="bib48" ref-type="bibr">[48]</xref>, <xref rid="bib49" ref-type="bibr">[49]</xref>] (<xref rid="tbl3" ref-type="table">Table 3</xref>).<table-wrap position="float" id="tbl1"><label>Table 1</label><caption><p>A Summary of Studies addressing the Prevalence of Respiratory Viruses among Pilgrims using PCR Methods, data presented as percentage of the total number of included pilgrims in each study.</p></caption><alt-text id="alttext0025">Table 1</alt-text><table frame="hsides" rules="groups"><thead><tr><th>Reference</th><th>[<xref rid="bib23" ref-type="bibr">23</xref>]</th><th>[<xref rid="bib24" ref-type="bibr">24</xref>]</th><th>[<xref rid="bib25" ref-type="bibr">25</xref>]</th><th>[<xref rid="bib26" ref-type="bibr">26</xref>]</th><th>[<xref rid="bib27" ref-type="bibr">27</xref>]</th><th>[<xref rid="bib28" ref-type="bibr">28</xref>]</th><th>[<xref rid="bib29" ref-type="bibr">29</xref>]</th><th>[<xref rid="bib30" ref-type="bibr">30</xref>]</th><th>[<xref rid="bib31" ref-type="bibr">31</xref>]</th><th>[<xref rid="bib32" ref-type="bibr">32</xref>]</th><th>[<xref rid="bib33" ref-type="bibr">33</xref>]</th><th>[<xref rid="bib34" ref-type="bibr">34</xref>]</th><th>[<xref rid="bib35" ref-type="bibr">35</xref>]</th><th>[<xref rid="bib36" ref-type="bibr">36</xref>]</th><th>[<xref rid="bib37" ref-type="bibr">37</xref>]</th><th>[<xref rid="bib38" ref-type="bibr">38</xref>]</th><th>[<xref rid="bib38" ref-type="bibr">38</xref>]</th><th>[<xref rid="bib15" ref-type="bibr">15</xref>]</th><th>[<xref rid="bib39" ref-type="bibr">39</xref>]</th><th>[<xref rid="bib39" ref-type="bibr">39</xref>]</th><th>[<xref rid="bib40" ref-type="bibr">40</xref>]</th><th>[<xref rid="bib41" ref-type="bibr">41</xref>]</th><th>[<xref rid="bib42" ref-type="bibr">42</xref>]</th><th>[<xref rid="bib54" ref-type="bibr">54</xref>]</th></tr></thead><tbody><tr><td align="left">Number of Included Pilgrims</td><td align="left">202</td><td align="left">555</td><td align="left">110</td><td align="left">255</td><td align="left">275</td><td align="left">80</td><td align="left">112</td><td align="left">38</td><td align="left">7</td><td align="left">551</td><td align="left">305</td><td align="left">2699</td><td align="left">484</td><td align="left">1600</td><td align="left">839</td><td align="left">169</td><td align="left">129</td><td align="left">129</td><td align="left">692</td><td align="left">470</td><td align="left">3840</td><td align="left">847</td><td align="left">300</td><td align="left">125</td></tr><tr><td align="left">Influenza A-H1N1</td><td align="left">0.5</td><td></td><td></td><td></td><td align="left">1.8</td><td></td><td align="left">0.9</td><td></td><td align="left">0</td><td align="left">0</td><td align="left">1.6</td><td align="left">0.1</td><td align="left">3.5</td><td align="left">0.5</td><td></td><td align="left">0</td><td align="left">0.8</td><td align="left">0.7</td><td align="left">1.6</td><td align="left">3</td><td align="left">6.7</td><td></td><td align="left">3</td><td></td></tr><tr><td align="left">Influenza A-H3N2</td><td align="left">9.9</td><td></td><td></td><td></td><td align="left">2.9</td><td></td><td align="left">3.6</td><td></td><td align="left">28.6</td><td align="left">1</td><td></td><td></td><td align="left">5.6</td><td></td><td></td><td align="left">0</td><td align="left">6.2</td><td align="left">6.2</td><td align="left">2</td><td align="left">1.7</td><td align="left">2.6</td><td></td><td align="left">4.3</td><td></td></tr><tr><td align="left">Influenza A (all)</td><td align="left">10.4</td><td align="left">8.2</td><td align="left">8.1</td><td></td><td align="left">4.7</td><td align="left">6.3</td><td align="left">4.5</td><td align="left">15.8</td><td align="left">28.6</td><td align="left">1</td><td align="left">2.6</td><td align="left">0.3</td><td align="left">9.1</td><td align="left">7.5</td><td align="left">1.3</td><td></td><td></td><td align="left">6.9</td><td align="left">3.6</td><td align="left">4.7</td><td align="left">9.3</td><td align="left">7.2</td><td align="left">7.3</td><td align="left">3</td></tr><tr><td align="left">Influenza B</td><td align="left">3.5</td><td align="left">2.3</td><td align="left">2.3</td><td></td><td align="left">7.3</td><td></td><td></td><td></td><td></td><td></td><td></td><td align="left">0.1</td><td align="left">5.4</td><td></td><td></td><td align="left">1.3</td><td align="left">0.8</td><td align="left">0.7</td><td align="left">0</td><td align="left">0.2</td><td align="left">3.5</td><td align="left">3.3</td><td align="left">3.6</td><td align="left">2</td></tr><tr><td align="left">Influenza overall</td><td align="left">13.9</td><td align="left">10.5</td><td align="left">10.4</td><td></td><td align="left">12</td><td align="left">6.3</td><td align="left">4.5</td><td align="left">15.8</td><td align="left">28.6</td><td align="left">1</td><td></td><td align="left">0.5</td><td align="left">14.5</td><td align="left">8</td><td></td><td align="left">1.3</td><td align="left">7.8</td><td align="left">7.6</td><td align="left">3.6</td><td align="left">9.6</td><td align="left">13</td><td align="left">10.5</td><td align="left">10.9</td><td align="left">5</td></tr><tr><td align="left">RSV</td><td align="left">4.5</td><td></td><td align="left">0.4</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td align="left">0.2</td><td></td><td></td><td align="left">5.1</td><td></td><td align="left">0.8</td><td></td><td align="left">0.7</td><td align="left">0.2</td><td></td><td></td><td></td><td align="left">1</td></tr><tr><td align="left">Parainfluenza 1</td><td></td><td></td><td align="left">0</td><td></td><td></td><td align="left">0</td><td align="left">0.9</td><td align="left">0</td><td></td><td></td><td></td><td align="left">0</td><td></td><td></td><td></td><td></td><td></td><td></td><td align="left">0</td><td align="left">0</td><td></td><td></td><td></td><td align="left">1</td></tr><tr><td align="left">Parainfluenza 2</td><td></td><td></td><td align="left">0</td><td></td><td></td><td align="left">0</td><td align="left">0</td><td align="left">0</td><td></td><td></td><td></td><td align="left">0</td><td></td><td></td><td></td><td></td><td></td><td></td><td align="left">0.3</td><td align="left">0.4</td><td></td><td></td><td></td><td align="left">0</td></tr><tr><td align="left">Parainfluenza 3</td><td></td><td></td><td align="left">0.4</td><td></td><td></td><td align="left">1.3</td><td align="left">1.8</td><td align="left">0</td><td></td><td></td><td></td><td align="left">0</td><td></td><td></td><td></td><td></td><td></td><td></td><td align="left">0.1</td><td align="left">0.2</td><td></td><td></td><td></td><td align="left">2</td></tr><tr><td align="left">Parainfluenza overall</td><td></td><td></td><td align="left">0.4</td><td></td><td></td><td align="left">1.3</td><td align="left">2.7</td><td align="left">2.6</td><td></td><td></td><td></td><td align="left">0</td><td></td><td></td><td></td><td></td><td align="left">0.8</td><td></td><td align="left">0.5</td><td align="left">0.6</td><td></td><td></td><td></td><td align="left">0</td></tr><tr><td align="left">Rhinovirus</td><td></td><td></td><td align="left">9.2</td><td align="left">5.9</td><td></td><td align="left">48.8</td><td align="left">26.8</td><td align="left">39.5</td><td align="left">26.6</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td align="left">14.7</td><td></td><td align="left">34.4</td><td align="left">30.9</td><td></td><td></td><td></td><td></td></tr><tr><td align="left">Entero-rhino virus</td><td></td><td></td><td></td><td align="left">2</td><td></td><td align="left">0</td><td></td><td align="left">0</td><td></td><td></td><td></td><td align="left">12.9</td><td></td><td></td><td align="left">16.8</td><td></td><td align="left">2.3</td><td></td><td></td><td></td><td></td><td></td><td></td><td align="left">47</td></tr><tr><td align="left">CoV-229E</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td align="left">7.8</td><td></td><td></td><td></td><td align="left">0.2</td><td></td><td></td><td></td><td></td><td align="left">12.4</td><td></td><td align="left">14.6</td><td align="left">10.2</td><td></td><td></td><td></td><td align="left">6</td></tr><tr><td align="left">CoV-NL63</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td align="left">0</td><td></td><td></td><td></td><td align="left">0.1</td><td></td><td></td><td></td><td></td><td align="left">0.8</td><td></td><td align="left">2</td><td align="left">0.2</td><td></td><td></td><td></td><td align="left">3</td></tr><tr><td align="left">CoV-HKU1</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td align="left">0</td><td></td><td></td><td></td><td align="left">0.1</td><td></td><td></td><td></td><td></td><td align="left">3.9</td><td></td><td align="left">1.3</td><td align="left">1.5</td><td></td><td></td><td></td><td align="left">0</td></tr><tr><td align="left">CoV-OC43</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td align="left">2.6</td><td></td><td></td><td></td><td align="left">0.5</td><td></td><td></td><td></td><td></td><td align="left">3.9</td><td></td><td align="left">1.6</td><td align="left">1.9</td><td></td><td></td><td></td><td align="left">3</td></tr><tr><td align="left">CoV overall</td><td></td><td></td><td></td><td></td><td></td><td></td><td align="left">2.7</td><td align="left">10.4</td><td></td><td></td><td></td><td align="left">0.9</td><td></td><td></td><td></td><td></td><td align="left">21</td><td></td><td align="left">19.5</td><td align="left">13.8</td><td></td><td></td><td></td><td align="left">12</td></tr><tr><td align="left">Metapneumovirus</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td align="left">0</td><td></td><td></td><td></td><td align="left">0.1</td><td></td><td></td><td></td><td></td><td align="left">0.8</td><td></td><td align="left">0.1</td><td align="left">0.6</td><td></td><td></td><td></td><td></td></tr></tbody></table></table-wrap><table-wrap position="float" id="tbl2"><label>Table 2</label><caption><p>A Summary of Studies addressing the Prevalence of Respiratory Viruses among Pilgrims using Cell Culture, data presented as percentage of the total number of included pilgrims in each study.</p></caption><alt-text id="alttext0030">Table 2</alt-text><table frame="hsides" rules="groups"><thead><tr><th>Reference</th><th>[<xref rid="bib43" ref-type="bibr">43</xref>]</th><th>[<xref rid="bib44" ref-type="bibr">44</xref>]</th><th>[<xref rid="bib49" ref-type="bibr">49</xref>]</th><th>[<xref rid="bib26" ref-type="bibr">26</xref>]</th><th>[<xref rid="bib27" ref-type="bibr">27</xref>]</th></tr></thead><tbody><tr><td align="left">Study Design</td><td align="left">Cross-sectional study (Saudi Arabia)</td><td align="left">Cross-sectional study (Saudi Arabia)</td><td align="left">Cross-sectional study (Saudi Arabia)</td><td align="left">Cross-sectional airport study (Iran)</td><td align="left">Cross-sectional airport study (Iran)</td></tr><tr><td align="left">Number of Included Pilgrims</td><td align="left">761</td><td align="left">500</td><td align="left">105</td><td align="left">225</td><td align="left">275</td></tr><tr><td align="left">Influenza A</td><td align="left">4.5</td><td align="left">0.6</td><td align="left">1.9</td><td align="left">5.1</td><td></td></tr><tr><td align="left">H1N1</td><td></td><td></td><td></td><td></td><td align="left">1.1</td></tr><tr><td align="left">Influenza B</td><td align="left">2</td><td align="left">5.4</td><td align="left">11.4</td><td align="left">5.1</td><td></td></tr><tr><td align="left">Influenza overall</td><td align="left">6.5</td><td align="left">6</td><td align="left">13.3</td><td align="left">5.1</td><td align="left">1.1</td></tr><tr><td align="left">Parainfluenza 1</td><td align="left">2</td><td></td><td></td><td></td><td></td></tr><tr><td align="left">Parainfluenza 2</td><td align="left">1.7</td><td></td><td></td><td></td><td></td></tr><tr><td align="left">Parainfluenza 3</td><td align="left">2.2</td><td></td><td></td><td></td><td></td></tr><tr><td align="left">Parainfluenza overall</td><td align="left">5.9</td><td align="left">0.8</td><td align="left">0</td><td></td><td></td></tr><tr><td align="left">Adenovirus</td><td align="left">4.7</td><td align="left">0</td><td align="left">36.2</td><td></td><td></td></tr><tr><td align="left">Respiratory syncytial virus</td><td align="left">2.4</td><td align="left">1.4</td><td align="left">1.9</td><td></td><td></td></tr><tr><td align="left">Herpes virus</td><td align="left">2.6</td><td></td><td></td><td></td><td></td></tr></tbody></table></table-wrap><table-wrap position="float" id="tbl3"><label>Table 3</label><caption><p>A Summary of Studies addressing the Prevalence of Respiratory Viruses among Pilgrims using Direct Immunofluorescence Staining or ELISA, data presented as percentage of the total number of included pilgrims in each study.</p></caption><alt-text id="alttext0035">Table 3</alt-text><table frame="hsides" rules="groups"><thead><tr><th>Reference</th><th>[<xref rid="bib46" ref-type="bibr">46</xref>]</th><th>[<xref rid="bib47" ref-type="bibr">47</xref>]</th><th>[<xref rid="bib48" ref-type="bibr">48</xref>]</th><th>[<xref rid="bib49" ref-type="bibr">49</xref>]</th></tr></thead><tbody><tr><td align="left">Methodology</td><td align="left">Direct immunofluorescence staining</td><td align="left">ELISA</td><td align="left">ELISA</td><td align="left">ELISA</td></tr><tr><td align="left">Year</td><td align="left">1994</td><td align="left">2000</td><td align="left">2004</td><td align="left">2004–5</td></tr><tr><td align="left">Number of Included Pilgrims</td><td align="left">64</td><td align="left">305</td><td align="left">360</td><td align="left">105</td></tr><tr><td align="left">Influenza A</td><td align="left">3.1</td><td align="left">5.9</td><td></td><td></td></tr><tr><td align="left">H1N1</td><td></td><td></td><td></td><td align="left">6.9</td></tr><tr><td align="left">H3N2</td><td></td><td></td><td></td><td align="left">6.1</td></tr><tr><td align="left">Influenza B</td><td align="left">1.6</td><td align="left">11.5</td><td></td><td align="left">20.8</td></tr><tr><td align="left">Influenza overall</td><td align="left">4.7</td><td align="left">17.4</td><td align="left">12.8</td><td></td></tr><tr><td align="left">Parainfluenza 1</td><td align="left">0</td><td></td><td></td><td></td></tr><tr><td align="left">Parainfluenza 2</td><td align="left">1.6</td><td></td><td></td><td></td></tr><tr><td align="left">Parainfluenza 3</td><td align="left">0</td><td></td><td></td><td></td></tr><tr><td align="left">Parainfluenza overall</td><td align="left">1.6</td><td></td><td></td><td></td></tr></tbody></table></table-wrap></p></sec><sec id="sec3.3"><label>3.3</label><title>Study designs</title><p id="p0080">The included studies were cross-sectional studies, case-control studies, and prospective cohort studies. These studies had different designs and methodology, and varied widely in terms of the number of included pilgrims. We included studies addressing the prevalence of viral respiratory infections. Many of these studies reported the prevalence of clinical respiratory tract infections among pilgrims, including upper respiratory tract infection (URTI), acute respiratory infection (ARI) or influenza-like illness (ILI) [<xref rid="bib16" ref-type="bibr">16</xref>,<xref rid="bib28" ref-type="bibr">28</xref>,<xref rid="bib38" ref-type="bibr">38</xref>,<xref rid="bib40" ref-type="bibr">40</xref>,<xref rid="bib50" ref-type="bibr">[50]</xref>, <xref rid="bib51" ref-type="bibr">[51]</xref>, <xref rid="bib52" ref-type="bibr">[52]</xref>, <xref rid="bib53" ref-type="bibr">[53]</xref>]. We included in the analysis studies addressing microbiology and laboratory diagnosis of viral respiratory infections based on culture, ELISA or PCR methods.</p></sec><sec id="sec3.4"><label>3.4</label><title>Studies based on polymerase chain reaction methods</title><p id="p0085">Included studies that used PCR methods for the detection of the respiratory viruses are summarized in <xref rid="tbl1" ref-type="table">Table 1</xref> [<xref rid="bib15" ref-type="bibr">15</xref>,<xref rid="bib23" ref-type="bibr">[23]</xref>, <xref rid="bib24" ref-type="bibr">[24]</xref>, <xref rid="bib25" ref-type="bibr">[25]</xref>, <xref rid="bib26" ref-type="bibr">[26]</xref>, <xref rid="bib27" ref-type="bibr">[27]</xref>, <xref rid="bib28" ref-type="bibr">[28]</xref>, <xref rid="bib29" ref-type="bibr">[29]</xref>, <xref rid="bib30" ref-type="bibr">[30]</xref>, <xref rid="bib31" ref-type="bibr">[31]</xref>, <xref rid="bib32" ref-type="bibr">[32]</xref>, <xref rid="bib33" ref-type="bibr">[33]</xref>, <xref rid="bib34" ref-type="bibr">[34]</xref>, <xref rid="bib35" ref-type="bibr">[35]</xref>, <xref rid="bib36" ref-type="bibr">[36]</xref>, <xref rid="bib37" ref-type="bibr">[37]</xref>, <xref rid="bib38" ref-type="bibr">[38]</xref>, <xref rid="bib39" ref-type="bibr">[39]</xref>, <xref rid="bib40" ref-type="bibr">[40]</xref>, <xref rid="bib41" ref-type="bibr">[41]</xref>, <xref rid="bib42" ref-type="bibr">[42]</xref>, <xref rid="bib54" ref-type="bibr">[54]</xref>,<xref rid="bib54" ref-type="bibr">54</xref>]. The overall analysis of these studies shows the most common viruses detected among pilgrims (<xref rid="fig2" ref-type="fig">Fig. 2</xref>), including influenza (A and B) virus (7.1%), influenza A (5.1%), rhinovirus (5.1%), and influenza B (1.9%). These studies did not screen for the same surveyed viruses and there was a large variation in the screened viruses (see <xref rid="fig2" ref-type="fig">Fig. 2</xref>).<fig id="fig2"><label>Fig. 2</label><caption><p>A summary of studies among pilgrims showing the most common respiratory viruses using PCR based techniques.</p></caption><alt-text id="alttext0015">Fig. 2</alt-text><graphic xlink:href="gr2_lrg"></graphic></fig></p></sec><sec id="sec3.5"><label>3.5</label><title>Studies based on culture methods</title><p id="p0090">A number of studies have detected respiratory viruses among pilgrims using culture methods (<xref rid="tbl2" ref-type="table">Table 2</xref>). These studies included a total of 1866 pilgrims, and the most common viruses detected among them are shown in
<xref rid="fig3" ref-type="fig">Fig. 3</xref>.<fig id="fig3"><label>Fig. 3</label><caption><p>A Summary of Studies among Pilgrims Showing the Most Common Respiratory Viruses Using Culture based Methods.</p></caption><alt-text id="alttext0020">Fig. 3</alt-text><graphic xlink:href="gr3_lrg"></graphic></fig></p></sec><sec id="sec3.6"><label>3.6</label><title>Other studies using alternative methods for the detection of respiratory viruses</title><p id="p0095">Other studies, using alternative methods for the detection of respiratory viruses, have detected respiratory viruses (primarily influenza viruses) among pilgrims. ELISA was used in three studies [<xref rid="bib47" ref-type="bibr">[47]</xref>, <xref rid="bib48" ref-type="bibr">[48]</xref>, <xref rid="bib49" ref-type="bibr">[49]</xref>] and direct immunofluorescence staining was used in one study [<xref rid="bib46" ref-type="bibr">46</xref>]. A summary of the findings of these studies are presented in <xref rid="tbl3" ref-type="table">Table 3</xref>.</p></sec><sec id="sec3.7"><label>3.7</label><title>2009 pandemic influenza A (H1N1) and the Hajj</title><p id="p0100">It was feared that the 2009 pandemic influenza A (H1N1) would result in a significant impact on the Hajj [<xref rid="bib55" ref-type="bibr">55</xref>,<xref rid="bib56" ref-type="bibr">56</xref>], especially that 200,000 pilgrims in 2008 were from resource-limited countries [<xref rid="bib56" ref-type="bibr">56</xref>]. In total, six studies investigated the prevalence of H1N1 virus among pilgrims [<xref rid="bib27" ref-type="bibr">27</xref>,<xref rid="bib32" ref-type="bibr">[32]</xref>, <xref rid="bib33" ref-type="bibr">[33]</xref>, <xref rid="bib34" ref-type="bibr">[34]</xref>, <xref rid="bib36" ref-type="bibr">[36]</xref>,<xref rid="bib36" ref-type="bibr">36</xref>] and one study was conducted among healthcare workers at the pilgrimage sites [<xref rid="bib57" ref-type="bibr">57</xref>] (<xref rid="tbl4" ref-type="table">Table 4</xref>). During the 2009 Hajj season, the prevalence of H1N1 virus among 275 symptomatic Iranian pilgrims was 1.8% [<xref rid="bib27" ref-type="bibr">27</xref>]. However, none of the 184 screened healthcare workers was infected [<xref rid="bib57" ref-type="bibr">57</xref>]. A large cross sectional study of 2699 departing pilgrims showed that 0.1% of them were positive for H1N1 virus [<xref rid="bib34" ref-type="bibr">34</xref>]. Two other studies have also founded prevalence of 1.6% [<xref rid="bib33" ref-type="bibr">33</xref>] and 1.8% [<xref rid="bib27" ref-type="bibr">27</xref>], but none of the 551 Egyptian pilgrims survived in another study were positive for H1N1 virus [<xref rid="bib32" ref-type="bibr">32</xref>].<table-wrap position="float" id="tbl4"><label>Table 4</label><caption><p>A Summary of Studies addressing the Prevalence of Pandemic H1N1 Influenza among Pilgrims.</p></caption><alt-text id="alttext0040">Table 4</alt-text><table frame="hsides" rules="groups"><thead><tr><th>Reference</th><th>Study Design</th><th>Population</th><th>Number Tested</th><th>n (%) Positive</th></tr></thead><tbody><tr><td align="left">[<xref rid="bib27" ref-type="bibr">27</xref>]</td><td align="left">cross sectional</td><td align="left">Returning Iranian pilgrims</td><td align="left">275</td><td align="left">5 (1.8)</td></tr><tr><td align="left">[<xref rid="bib32" ref-type="bibr">32</xref>]</td><td align="left">cross sectional</td><td align="left">Returning Egyptian pilgrims</td><td align="left">551</td><td align="left">0 (0)</td></tr><tr><td align="left">[<xref rid="bib33" ref-type="bibr">33</xref>]</td><td align="left">cross sectional</td><td align="left">Returning Iranian pilgrims</td><td align="left">305</td><td align="left">5 (1.6)</td></tr><tr><td align="left">[<xref rid="bib34" ref-type="bibr">34</xref>]</td><td align="left">cross sectional</td><td align="left">Departing pilgrims</td><td align="left">2699</td><td align="left">2 (0.1)</td></tr><tr><td align="left">[<xref rid="bib36" ref-type="bibr">36</xref>]</td><td align="left">cross sectional</td><td align="left">Pilgrims</td><td align="left">1600</td><td align="left">9 (0.5)</td></tr><tr><td align="left">[<xref rid="bib57" ref-type="bibr">57</xref>]</td><td align="left">cross sectional</td><td align="left">Healthcare workers</td><td align="left">184</td><td align="left">0 (0)</td></tr></tbody></table></table-wrap></p></sec><sec id="sec3.8"><label>3.8</label><title>Threat of emerging coronaviruses</title><p id="p0105">In the last decade, two coronaviruses emerged, the SARS-CoV in 2003 and the MERS-CoV in 2012. Coronavirus infections were detected in 0.6–0.8% of tested population in regard to the Hajj seasons [<xref rid="bib3" ref-type="bibr">3</xref>]. There were no cases of SARS linked to the Hajj [<xref rid="bib58" ref-type="bibr">58</xref>].</p><sec id="sec3.8.1"><label>3.8.1</label><title>Systematic screening for MERS-CoV among attendees of the annual Hajj</title><p id="p0110">Despite the 2012 Hajj season started few weeks after the first case of MERS-CoV infection was reported, there were no reported cases among pilgrims in 2012 [<xref rid="bib5" ref-type="bibr">5</xref>,<xref rid="bib25" ref-type="bibr">25</xref>,<xref rid="bib32" ref-type="bibr">32</xref>]. Systematic screening of pilgrims for MERS-CoV was done in multiple studies among >10,000 pilgrims [<xref rid="bib5" ref-type="bibr">5</xref>,<xref rid="bib14" ref-type="bibr">14</xref>,<xref rid="bib29" ref-type="bibr">29</xref>,<xref rid="bib31" ref-type="bibr">31</xref>,<xref rid="bib35" ref-type="bibr">35</xref>,<xref rid="bib37" ref-type="bibr">[37]</xref>, <xref rid="bib38" ref-type="bibr">[38]</xref>, <xref rid="bib39" ref-type="bibr">[39]</xref>, <xref rid="bib41" ref-type="bibr">[41]</xref>, <xref rid="bib42" ref-type="bibr">[42]</xref>, <xref rid="bib54" ref-type="bibr">[54]</xref>, <xref rid="bib59" ref-type="bibr">[59]</xref>, <xref rid="bib60" ref-type="bibr">[60]</xref>, <xref rid="bib61" ref-type="bibr">[61]</xref>, <xref rid="bib62" ref-type="bibr">[62]</xref>, <xref rid="bib63" ref-type="bibr">[63]</xref>,<xref rid="bib41" ref-type="bibr">41</xref>,<xref rid="bib42" ref-type="bibr">42</xref>,<xref rid="bib54" ref-type="bibr">54</xref>,<xref rid="bib59" ref-type="bibr">[59]</xref>, <xref rid="bib60" ref-type="bibr">[60]</xref>, <xref rid="bib61" ref-type="bibr">[61]</xref>, <xref rid="bib62" ref-type="bibr">[62]</xref>, <xref rid="bib63" ref-type="bibr">[63]</xref>] (<xref rid="tbl5" ref-type="table">Table 5</xref>).<table-wrap position="float" id="tbl5"><label>Table 5</label><caption><p>Systematic screening of MERS-CoV among pilgrims.</p></caption><alt-text id="alttext0045">Table 5</alt-text><table frame="hsides" rules="groups"><thead><tr><th>Reference</th><th>Year of the study</th><th>Study population</th><th>Method</th><th>Number Screened</th><th>N (%) positive</th></tr></thead><tbody><tr><td align="left">[<xref rid="bib5" ref-type="bibr">5</xref>]</td><td align="left">2012</td><td align="left">Symptomatic French</td><td align="left">Nasopharyngeal swab</td><td align="left">300</td><td align="left">0</td></tr><tr><td align="left">[<xref rid="bib14" ref-type="bibr">14</xref>]</td><td align="left">2012</td><td align="left">French cohort</td><td align="left">Nasopharyngeal swab</td><td align="left">154</td><td align="left">0</td></tr><tr><td align="left">[<xref rid="bib15" ref-type="bibr">15</xref>]</td><td align="left">2013</td><td align="left">Departing Pilgrims</td><td align="left">Nasal swabs</td><td align="left">129</td><td align="left">0</td></tr><tr><td align="left">[<xref rid="bib29" ref-type="bibr">29</xref>]</td><td align="left">2013</td><td align="left">Pilgrims from Saudi Arabia, Australia and Qatar</td><td align="left">Nasal swabs</td><td align="left">1038</td><td align="left">0</td></tr><tr><td align="left">[<xref rid="bib30" ref-type="bibr">30</xref>]</td><td align="left">2013</td><td align="left">Admitted Pilgrims with Pneumonia</td><td align="left">Sputum</td><td align="left">38</td><td align="left">0</td></tr><tr><td align="left">[<xref rid="bib31" ref-type="bibr">31</xref>]</td><td align="left">2014</td><td align="left">Symptomatic pilgrims returning to Austria</td><td align="left">Sputum, throat swab, or bronchoalveolar lavage</td><td align="left">7</td><td align="left">0</td></tr><tr><td align="left">[<xref rid="bib35" ref-type="bibr">35</xref>]</td><td align="left">2012–2015</td><td align="left">Egyptian</td><td align="left">Nasopharyngeal and oropharyngeal swabs</td><td align="left">484</td><td align="left">0</td></tr><tr><td align="left">[<xref rid="bib37" ref-type="bibr">37</xref>]</td><td align="left">2013</td><td align="left">Adult African Hajj pilgrims returning to Ghana, West Africa</td><td align="left">Nasopharyngeal swab</td><td align="left">839</td><td align="left">0</td></tr><tr><td align="left">[<xref rid="bib39" ref-type="bibr">39</xref>]</td><td align="left">2013</td><td align="left">Departing Pilgrims, paired and non-paired cohort</td><td align="left">Nasal swabs</td><td align="left">692 (paired cohort),<break></break>514 (non-paired arriving cohorts);<break></break>and 470 (non-paired departing cohort)</td><td align="left">0</td></tr><tr><td align="left">[<xref rid="bib38" ref-type="bibr">38</xref>] [<xref rid="bib15" ref-type="bibr">15</xref>]</td><td align="left">2013</td><td align="left">French pilgrims</td><td align="left">Nasal and throat swab</td><td align="left">129</td><td align="left">0</td></tr><tr><td align="left">[<xref rid="bib60" ref-type="bibr">60</xref>]</td><td align="left">2013</td><td align="left">Multiple nationalities</td><td align="left">Nasopharyngeal swab</td><td align="left">3210 pre-Hajj</td><td align="left">0</td></tr><tr><td align="left">[<xref rid="bib60" ref-type="bibr">60</xref>]</td><td align="left">2013</td><td align="left">Multiple nationalities</td><td align="left">Nasopharyngeal swab</td><td align="left">2025 post-Hajj</td><td align="left">0</td></tr><tr><td align="left">[<xref rid="bib61" ref-type="bibr">61</xref>]</td><td align="left">2013–2015</td><td align="left">Symptomatic British Pilgrims</td><td align="left">Upper and lower respiratory tract</td><td align="left">202</td><td align="left">0</td></tr><tr><td align="left">[<xref rid="bib63" ref-type="bibr">63</xref>]</td><td align="left">2013–15</td><td align="left">Ill French travelers</td><td align="left">Not indicated</td><td align="left">33</td><td align="left">0</td></tr><tr><td align="left">[<xref rid="bib41" ref-type="bibr">41</xref>]</td><td align="left">2013–2015</td><td align="left">Chinese</td><td align="left">Lower respiratory tract sputum, washes, and upper respiratory tract oropharyngeal swab</td><td align="left">847</td><td align="left">0</td></tr><tr><td align="left">[<xref rid="bib54" ref-type="bibr">54</xref>]</td><td align="left">2015</td><td align="left">Jordanian</td><td align="left">Nasopharyngeal and oropharyngeal</td><td align="left">125</td><td align="left">0</td></tr><tr><td align="left">[<xref rid="bib42" ref-type="bibr">42</xref>]</td><td align="left">2014–2015</td><td align="left">Kashmir, north India</td><td align="left">nasopharyngeal and throat swabs</td><td align="left">300</td><td align="left">0</td></tr></tbody></table></table-wrap></p></sec></sec><sec id="sec3.9"><label>3.9</label><title>Coinfection of respiratory viruses and <italic>S. pneumoniae</italic></title><p id="p0115">In a recent study conducted among 129 French pilgrims in 2013, about 39% of those who tested positive for <italic>S. pneumoniae</italic> after the Hajj pilgrimage were co-infected with at least one virus [<xref rid="bib38" ref-type="bibr">38</xref>]. However, there is no information on whether the pilgrims were carrying <italic>S. pneumoniae</italic> or were ill secondary to this organism.</p></sec></sec><sec id="sec4"><label>4</label><title>Discussion</title><p id="p0120">The most common viruses were rhinovirus, influenza A and coronavirus 229E. In addition, the acquisition of MERS-CoV remains very limited and systematic screening of pilgrims showed no infections. MERS-CoV is absent in all Hajj pilgrims tested so far. Different methods were used for the diagnosis of respiratory pathogens and included: PCR, culture methods and ELISA. The ease and rapidity of PCR method make this method an attractive method for further use in subsequent studies to detect respiratory viruses. Interestingly, it appears that some viruses are more prone to transmission during Hajj (influenza and Rhinoviruses). The difference in the transmission could be related to a predominant aerial transmission for Influenza and Rhinoviruses whereas other (less prevalent) could rely on direct contact (hands carry-over). Camels were not allowed in the Hajj areas due to the risk of MERS-CoV transmission and this strategy may further decrease the risk of MERS-CoV transmission. Different respiratory viruses might be acquired during the Hajj and these viruses might be introduced into pilgrims' home countries upon their return, thus contributing to the potential for international spread of these viruses.</p><p id="p0125">Preventing influenza transmission during Hajj is an important target for public health. Influenza vaccination should be a priority for all Hajj pilgrims [<xref rid="bib64" ref-type="bibr">64</xref>]. Vaccination is not so easy due to regulation on seasonal vaccine availability [<xref rid="bib65" ref-type="bibr">65</xref>]. In addition, non-pharmacological preventive measures are needed for the prevention of respiratory infections during the Hajj: maintaining good infection control practice among healthcare workers, the use of face masks or respirators, and hand hygiene [<xref rid="bib66" ref-type="bibr">66</xref>,<xref rid="bib67" ref-type="bibr">67</xref>]. The majority of viral respiratory infections acquired during pilgrimage are due to influenza viruses, and rhinoviruses [<xref rid="bib64" ref-type="bibr">64</xref>]. The diagnosis of seasonal influenza during the hajj was a major focus of most studies addressing the prevalence of respiratory viruses among pilgrims [<xref rid="bib23" ref-type="bibr">23</xref>,<xref rid="bib25" ref-type="bibr">25</xref>,<xref rid="bib32" ref-type="bibr">[32]</xref>, <xref rid="bib33" ref-type="bibr">[33]</xref>, <xref rid="bib34" ref-type="bibr">[34]</xref>, <xref rid="bib36" ref-type="bibr">[36]</xref>, <xref rid="bib39" ref-type="bibr">[39]</xref>, <xref rid="bib40" ref-type="bibr">[40]</xref>, <xref rid="bib43" ref-type="bibr">[43]</xref>, <xref rid="bib56" ref-type="bibr">[56]</xref>, <xref rid="bib68" ref-type="bibr">[68]</xref>, <xref rid="bib69" ref-type="bibr">[69]</xref>, <xref rid="bib70" ref-type="bibr">[70]</xref>, <xref rid="bib71" ref-type="bibr">[71]</xref>, <xref rid="bib72" ref-type="bibr">[72]</xref>, <xref rid="bib73" ref-type="bibr">[73]</xref>, <xref rid="bib74" ref-type="bibr">[74]</xref>, <xref rid="bib75" ref-type="bibr">[75]</xref>, <xref rid="bib76" ref-type="bibr">[76]</xref>, <xref rid="bib77" ref-type="bibr">[77]</xref>, <xref rid="bib78" ref-type="bibr">[78]</xref>, <xref rid="bib79" ref-type="bibr">[79]</xref>, <xref rid="bib80" ref-type="bibr">[80]</xref>,<xref rid="bib36" ref-type="bibr">36</xref>,<xref rid="bib39" ref-type="bibr">39</xref>,<xref rid="bib40" ref-type="bibr">40</xref>,<xref rid="bib43" ref-type="bibr">43</xref>,<xref rid="bib56" ref-type="bibr">56</xref>,<xref rid="bib68" ref-type="bibr">[68]</xref>, <xref rid="bib69" ref-type="bibr">[69]</xref>, <xref rid="bib70" ref-type="bibr">[70]</xref>, <xref rid="bib71" ref-type="bibr">[71]</xref>, <xref rid="bib72" ref-type="bibr">[72]</xref>, <xref rid="bib73" ref-type="bibr">[73]</xref>, <xref rid="bib74" ref-type="bibr">[74]</xref>, <xref rid="bib75" ref-type="bibr">[75]</xref>, <xref rid="bib76" ref-type="bibr">[76]</xref>, <xref rid="bib77" ref-type="bibr">[77]</xref>, <xref rid="bib78" ref-type="bibr">[78]</xref>, <xref rid="bib79" ref-type="bibr">[79]</xref>, <xref rid="bib80" ref-type="bibr">[80]</xref>]. In these studies, different methods were used to detect respiratory viruses, with PCR being the most common used method. There are multiple contributing factors for the transmission and acquisition of respiratory viruses during the Hajj and include the crowdedness, close proximity, and indoor or outdoor venue [<xref rid="bib80" ref-type="bibr">80</xref>].</p><p id="p0130">Consistent with few studies worldwide, entero-rhinovirus was the most common virus isolated among pilgrims. However, this result is related to a single study of 2699 departing pilgrims that showed a 13% acquisition rate [<xref rid="bib34" ref-type="bibr">34</xref>]. It was shown that entero-rhinovirus the primary cause of common colds [<xref rid="bib81" ref-type="bibr">81</xref>,<xref rid="bib82" ref-type="bibr">82</xref>].</p><p id="p0135">With the emergence of the pandemic 2009 H1N1, there was a fear of the significant impact on the Hajj [<xref rid="bib55" ref-type="bibr">55</xref>,<xref rid="bib56" ref-type="bibr">56</xref>]. However, different studies showed very low rate of acquisition of this virus during the 2009 Hajj. Also, the emergence of SARS-CoV and MERS-CoV was of major concerns for mass gatherings such as the Hajj [<xref rid="bib2" ref-type="bibr">2</xref>,<xref rid="bib5" ref-type="bibr">5</xref>]. However, to date neither SARS-CoV nor MERS-CoV was found to be transmitted among pilgrims. Systematic screening for MERS-COV among returning or departing pilgrims showed no positive cases [<xref rid="bib5" ref-type="bibr">5</xref>,<xref rid="bib14" ref-type="bibr">14</xref>,<xref rid="bib15" ref-type="bibr">15</xref>,<xref rid="bib29" ref-type="bibr">[29]</xref>, <xref rid="bib30" ref-type="bibr">[30]</xref>, <xref rid="bib31" ref-type="bibr">[31]</xref>, <xref rid="bib35" ref-type="bibr">[35]</xref>, <xref rid="bib37" ref-type="bibr">[37]</xref>, <xref rid="bib38" ref-type="bibr">[38]</xref>, <xref rid="bib39" ref-type="bibr">[39]</xref>, <xref rid="bib60" ref-type="bibr">[60]</xref>, <xref rid="bib61" ref-type="bibr">[61]</xref>, <xref rid="bib63" ref-type="bibr">[63]</xref>,<xref rid="bib35" ref-type="bibr">35</xref>,<xref rid="bib37" ref-type="bibr">[37]</xref>, <xref rid="bib38" ref-type="bibr">[38]</xref>, <xref rid="bib39" ref-type="bibr">[39]</xref>, <xref rid="bib60" ref-type="bibr">[60]</xref>, <xref rid="bib61" ref-type="bibr">[61]</xref>, <xref rid="bib63" ref-type="bibr">[63]</xref>,<xref rid="bib60" ref-type="bibr">60</xref>,<xref rid="bib61" ref-type="bibr">61</xref>,<xref rid="bib63" ref-type="bibr">63</xref>]. However, four cases were linked to Umrah (also known as the lesser pilgrimage) [<xref rid="bib69" ref-type="bibr">69</xref>,<xref rid="bib83" ref-type="bibr">[83]</xref>, <xref rid="bib84" ref-type="bibr">[84]</xref>, <xref rid="bib85" ref-type="bibr">[85]</xref>, <xref rid="bib86" ref-type="bibr">[86]</xref>]. It was estimated that the risk MERS-CoV transmission among pilgrims could be 1–7 cases per Hajj season and 3–10 per Umrah per year [<xref rid="bib87" ref-type="bibr">87</xref>].</p><p id="p0140">Various studies showed different acquisition rates of respiratory viruses, but only one study showed coinfection with <italic>S. pneumoniae.</italic> Recent studies showed a significant acquisition of <italic>S. pneumoniae</italic> and <italic>Hemophilus influenzae</italic> by returning pilgrims [<xref rid="bib3" ref-type="bibr">3</xref>,<xref rid="bib10" ref-type="bibr">10</xref>,<xref rid="bib12" ref-type="bibr">12</xref>,<xref rid="bib66" ref-type="bibr">66</xref>,<xref rid="bib88" ref-type="bibr">88</xref>].</p><p id="p0145">Viral respiratory tract infections, mainly rhinovirus, influenza A and coronavirus 229E, are of major concern during the Hajj. Despite extensive systematic screening, MERS-CoV had not been isolated from pilgrims. Continued surveillance for MERS-CoV is needed to ensure timely detection of any possible imported MERS cases [<xref rid="bib8" ref-type="bibr">8</xref>,<xref rid="bib9" ref-type="bibr">9</xref>,<xref rid="bib64" ref-type="bibr">64</xref>]. Differential transmission of different viruses may play a role in the observed frequencies. Understanding these factors facilitate the development of preventive measures. Further paired prospective studies using a systematic evaluation of pilgrims for these viruses are needed in order to estimate the total burden of viral respiratory diseases during the Hajj. International collaboration would foster evidence-based practices and guidelines for implementation during mass gathering events [<xref rid="bib10" ref-type="bibr">10</xref>].</p></sec><sec id="sec5"><title>Funding</title><p id="p0150">None.</p></sec><sec id="sec6"><title>Conflicts of interest</title><p id="p0155">The authors have no conflicts of interest to declare.</p></sec></body><back><ref-list id="cebib0010"><title>References</title><ref id="bib1"><label>1</label><element-citation publication-type="journal" id="sref1"><person-group person-group-type="author"><name><surname>Memish</surname><given-names>Z.A.</given-names></name><name><surname>Zumla</surname><given-names>A.</given-names></name><name><surname>Alhakeem</surname><given-names>R.F.</given-names></name><name><surname>Assiri</surname><given-names>A.</given-names></name><name><surname>Turkestani</surname><given-names>A.</given-names></name><name><surname>Al 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