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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Exposures among MERS Case-Patients, Saudi Arabia,
January–February 2016</title><author><name sortKey="Alhakeem, Raafat F" sort="Alhakeem, Raafat F" uniqKey="Alhakeem R" first="Raafat F." last="Alhakeem">Raafat F. Alhakeem</name></author><author><name sortKey="Midgley, Claire M" sort="Midgley, Claire M" uniqKey="Midgley C" first="Claire M." last="Midgley">Claire M. Midgley</name></author><author><name sortKey="Assiri, Abdullah M" sort="Assiri, Abdullah M" uniqKey="Assiri A" first="Abdullah M." last="Assiri">Abdullah M. Assiri</name></author><author><name sortKey="Alessa, Mohammed" sort="Alessa, Mohammed" uniqKey="Alessa M" first="Mohammed" last="Alessa">Mohammed Alessa</name></author><author><name sortKey="Al Hawaj, Hassan" sort="Al Hawaj, Hassan" uniqKey="Al Hawaj H" first="Hassan" last="Al Hawaj">Hassan Al Hawaj</name></author><author><name sortKey="Saeed, Abdulaziz Bin" sort="Saeed, Abdulaziz Bin" uniqKey="Saeed A" first="Abdulaziz Bin" last="Saeed">Abdulaziz Bin Saeed</name></author><author><name sortKey="Almasri, Malak M" sort="Almasri, Malak M" uniqKey="Almasri M" first="Malak M." last="Almasri">Malak M. Almasri</name></author><author><name sortKey="Lu, Xiaoyan" sort="Lu, Xiaoyan" uniqKey="Lu X" first="Xiaoyan" last="Lu">Xiaoyan Lu</name></author><author><name sortKey="Abedi, Glen R" sort="Abedi, Glen R" uniqKey="Abedi G" first="Glen R." last="Abedi">Glen R. Abedi</name></author><author><name sortKey="Abdalla, Osman" sort="Abdalla, Osman" uniqKey="Abdalla O" first="Osman" last="Abdalla">Osman Abdalla</name></author><author><name sortKey="Mohammed, Mutaz" sort="Mohammed, Mutaz" uniqKey="Mohammed M" first="Mutaz" last="Mohammed">Mutaz Mohammed</name></author><author><name sortKey="Algarni, Homoud S" sort="Algarni, Homoud S" uniqKey="Algarni H" first="Homoud S." last="Algarni">Homoud S. Algarni</name></author><author><name sortKey="Al Abdely, Hail M" sort="Al Abdely, Hail M" uniqKey="Al Abdely H" first="Hail M." last="Al-Abdely">Hail M. Al-Abdely</name></author><author><name sortKey="Alsharef, Ali Abraheem" sort="Alsharef, Ali Abraheem" uniqKey="Alsharef A" first="Ali Abraheem" last="Alsharef">Ali Abraheem Alsharef</name></author><author><name sortKey="Nooh, Randa" sort="Nooh, Randa" uniqKey="Nooh R" first="Randa" last="Nooh">Randa Nooh</name></author><author><name sortKey="Erdman, Dean D" sort="Erdman, Dean D" uniqKey="Erdman D" first="Dean D." last="Erdman">Dean D. Erdman</name></author><author><name sortKey="Gerber, Susan I" sort="Gerber, Susan I" uniqKey="Gerber S" first="Susan I." last="Gerber">Susan I. Gerber</name></author><author><name sortKey="Watson, John T" sort="Watson, John T" uniqKey="Watson J" first="John T." last="Watson">John T. Watson</name></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">27606432</idno><idno type="pmc">5088020</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5088020</idno><idno type="RBID">PMC:5088020</idno><idno type="doi">10.3201/eid2211.161042</idno><date when="2016">2016</date><idno type="wicri:Area/Pmc/Corpus">000867</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000867</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Exposures among MERS Case-Patients, Saudi Arabia,
January–February 2016</title><author><name sortKey="Alhakeem, Raafat F" sort="Alhakeem, Raafat F" uniqKey="Alhakeem R" first="Raafat F." last="Alhakeem">Raafat F. Alhakeem</name></author><author><name sortKey="Midgley, Claire M" sort="Midgley, Claire M" uniqKey="Midgley C" first="Claire M." last="Midgley">Claire M. Midgley</name></author><author><name sortKey="Assiri, Abdullah M" sort="Assiri, Abdullah M" uniqKey="Assiri A" first="Abdullah M." last="Assiri">Abdullah M. Assiri</name></author><author><name sortKey="Alessa, Mohammed" sort="Alessa, Mohammed" uniqKey="Alessa M" first="Mohammed" last="Alessa">Mohammed Alessa</name></author><author><name sortKey="Al Hawaj, Hassan" sort="Al Hawaj, Hassan" uniqKey="Al Hawaj H" first="Hassan" last="Al Hawaj">Hassan Al Hawaj</name></author><author><name sortKey="Saeed, Abdulaziz Bin" sort="Saeed, Abdulaziz Bin" uniqKey="Saeed A" first="Abdulaziz Bin" last="Saeed">Abdulaziz Bin Saeed</name></author><author><name sortKey="Almasri, Malak M" sort="Almasri, Malak M" uniqKey="Almasri M" first="Malak M." last="Almasri">Malak M. Almasri</name></author><author><name sortKey="Lu, Xiaoyan" sort="Lu, Xiaoyan" uniqKey="Lu X" first="Xiaoyan" last="Lu">Xiaoyan Lu</name></author><author><name sortKey="Abedi, Glen R" sort="Abedi, Glen R" uniqKey="Abedi G" first="Glen R." last="Abedi">Glen R. Abedi</name></author><author><name sortKey="Abdalla, Osman" sort="Abdalla, Osman" uniqKey="Abdalla O" first="Osman" last="Abdalla">Osman Abdalla</name></author><author><name sortKey="Mohammed, Mutaz" sort="Mohammed, Mutaz" uniqKey="Mohammed M" first="Mutaz" last="Mohammed">Mutaz Mohammed</name></author><author><name sortKey="Algarni, Homoud S" sort="Algarni, Homoud S" uniqKey="Algarni H" first="Homoud S." last="Algarni">Homoud S. Algarni</name></author><author><name sortKey="Al Abdely, Hail M" sort="Al Abdely, Hail M" uniqKey="Al Abdely H" first="Hail M." last="Al-Abdely">Hail M. Al-Abdely</name></author><author><name sortKey="Alsharef, Ali Abraheem" sort="Alsharef, Ali Abraheem" uniqKey="Alsharef A" first="Ali Abraheem" last="Alsharef">Ali Abraheem Alsharef</name></author><author><name sortKey="Nooh, Randa" sort="Nooh, Randa" uniqKey="Nooh R" first="Randa" last="Nooh">Randa Nooh</name></author><author><name sortKey="Erdman, Dean D" sort="Erdman, Dean D" uniqKey="Erdman D" first="Dean D." last="Erdman">Dean D. Erdman</name></author><author><name sortKey="Gerber, Susan I" sort="Gerber, Susan I" uniqKey="Gerber S" first="Susan I." last="Gerber">Susan I. Gerber</name></author><author><name sortKey="Watson, John T" sort="Watson, John T" uniqKey="Watson J" first="John T." last="Watson">John T. Watson</name></author></analytic><series><title level="j">Emerging Infectious Diseases</title><idno type="ISSN">1080-6040</idno><idno type="eISSN">1080-6059</idno><imprint><date when="2016">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><back><div1 type="bibliography"><listBibl><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct></listBibl></div1></back></TEI><pmc article-type="letter"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Emerg Infect Dis</journal-id><journal-id journal-id-type="iso-abbrev">Emerging Infect. Dis</journal-id><journal-id journal-id-type="publisher-id">EID</journal-id><journal-title-group><journal-title>Emerging Infectious Diseases</journal-title></journal-title-group><issn pub-type="ppub">1080-6040</issn><issn pub-type="epub">1080-6059</issn><publisher><publisher-name>Centers for Disease Control and Prevention</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">27606432</article-id><article-id pub-id-type="pmc">5088020</article-id><article-id pub-id-type="publisher-id">16-1042</article-id><article-id pub-id-type="doi">10.3201/eid2211.161042</article-id><article-categories><subj-group subj-group-type="heading"><subject>Letters to the Editor</subject></subj-group><subj-group subj-group-type="article-type"><subject>Letter</subject></subj-group><subj-group subj-group-type="TOC-title"><subject>Exposures among MERS Case-Patients, Saudi Arabia, January–February 2016</subject></subj-group></article-categories><title-group><article-title>Exposures among MERS Case-Patients, Saudi Arabia,
January–February 2016</article-title><alt-title alt-title-type="running-head">Exposures among MERS Case-Patients, Saudi
Arabia</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Alhakeem</surname><given-names>Raafat F.</given-names></name></contrib><contrib contrib-type="author" corresp="yes"><name><surname>Midgley</surname><given-names>Claire M.</given-names></name></contrib><contrib contrib-type="author"><name><surname>Assiri</surname><given-names>Abdullah M.</given-names></name></contrib><contrib contrib-type="author"><name><surname>Alessa</surname><given-names>Mohammed</given-names></name></contrib><contrib contrib-type="author"><name><surname>Al Hawaj</surname><given-names>Hassan</given-names></name></contrib><contrib contrib-type="author"><name><surname>Saeed</surname><given-names>Abdulaziz Bin</given-names></name></contrib><contrib contrib-type="author"><name><surname>Almasri</surname><given-names>Malak M.</given-names></name></contrib><contrib contrib-type="author"><name><surname>Lu</surname><given-names>Xiaoyan</given-names></name></contrib><contrib contrib-type="author"><name><surname>Abedi</surname><given-names>Glen R.</given-names></name></contrib><contrib contrib-type="author"><name><surname>Abdalla</surname><given-names>Osman</given-names></name></contrib><contrib contrib-type="author"><name><surname>Mohammed</surname><given-names>Mutaz</given-names></name></contrib><contrib contrib-type="author"><name><surname>Algarni</surname><given-names>Homoud S.</given-names></name></contrib><contrib contrib-type="author"><name><surname>Al-Abdely</surname><given-names>Hail M.</given-names></name></contrib><contrib contrib-type="author"><name><surname>Alsharef</surname><given-names>Ali Abraheem</given-names></name></contrib><contrib contrib-type="author"><name><surname>Nooh</surname><given-names>Randa</given-names></name></contrib><contrib contrib-type="author"><name><surname>Erdman</surname><given-names>Dean D.</given-names></name></contrib><contrib contrib-type="author"><name><surname>Gerber</surname><given-names>Susan I.</given-names></name></contrib><contrib contrib-type="author"><name><surname>Watson</surname><given-names>John T.</given-names></name></contrib><aff id="aff1">Ministry of Health, Riyadh, Saudi Arabia (R.F. Alhakeem, A.M. Assiri, M. Alessa, H. Al Hawaj, A. Bin Saeed, M.M. Almasri, O. Abdalla, M. Mohammed, H.S. Algarni, H.M. Al-Abdely, A.A. Alsharef, R. Nooh);</aff><aff id="aff2">US Centers for Disease Control and Prevention, Atlanta, Georgia, USA (C.M. Midgley, X. Lu, G.R. Abedi, D.D. Erdman. S.I. Gerber, J.T. Watson)</aff></contrib-group><author-notes><corresp id="cor1">Address for correspondence: Claire M. Midgley, Centers for
Disease Control and Prevention, 1600 Clifton Road NE, Atlanta, Georgia,
30329-4027, USA; email: <email xlink:href="ydk5@cdc.gov">ydk5@cdc.gov</email></corresp></author-notes><pub-date pub-type="ppub"><month>11</month><year>2016</year></pub-date><volume>22</volume><issue>11</issue><fpage>2020</fpage><lpage>2022</lpage><kwd-group kwd-group-type="author"><title>Keywords: </title><kwd>Middle East respiratory syndrome coronavirus</kwd><kwd>MERS</kwd><kwd>MERS-CoV</kwd><kwd>infections</kwd><kwd>disease outbreaks</kwd><kwd>infectious disease transmission</kwd><kwd>viruses</kwd><kwd>dromedary</kwd><kwd>camels</kwd><kwd>Saudi Arabia</kwd><kwd>respiratory infections</kwd></kwd-group></article-meta></front><body><p><bold>To the Editor:</bold> Risk factors for primary acquisition of Middle East
respiratory syndrome (MERS) coronavirus (CoV) include recent direct contact with
dromedary camels (<xref rid="R1" ref-type="bibr"><italic>1</italic></xref>), but
secondary transmission, associated with healthcare settings (<xref rid="R2" ref-type="bibr"><italic>2</italic></xref>–<xref rid="R4" ref-type="bibr"><italic>4</italic></xref>) or household contact (<xref rid="R5" ref-type="bibr"><italic>5</italic></xref>), accounts for most reported cases. Because persons
with MERS often do not report any of these risk factors, we investigated MERS cases in
Saudi Arabia during an apparent period of limited hospital transmission. Through
telephone interviews of case-patients and information from routine investigations, we
aimed to characterize exposures and to explore additional factors potentially important
in disease transmission. We also genetically sequenced MERS-CoV from respiratory
specimens to identify circulating strains.</p><p>For confirmed MERS cases (<xref rid="R6" ref-type="bibr"><italic>6</italic></xref>)
reported in Saudi Arabia during January–February 2016, we assessed exposures
during the 2 weeks before illness onset (exposure period), including direct (<xref rid="R1" ref-type="bibr"><italic>1</italic></xref>) and indirect camel contact;
indirect contact was defined as 1) having visited settings where camels were kept but
without having direct contact or 2) exposure to friends or household members who
themselves had direct camel exposure (<xref rid="R1" ref-type="bibr"><italic>1</italic></xref>). We assessed whether case-patients had worked at,
visited, or been admitted to a healthcare setting or had contact with a person known to
have MERS during the case-patient’s exposure period. We also asked about recent
travel and if any household members were healthcare personnel. For persons too ill to
participate or deceased, we interviewed relatives or close friends.</p><p>We classified as secondary any case identified through routine case-contact tracing and
testing. We considered persons whose cases were identified through routine testing of
occupational contacts of MERS-CoV–positive camels to have had direct camel
contact. For the remaining cases, we used interview responses to characterize
exposures.</p><p>All MERS cases reported during January–February 2016 were confirmed in Saudi
Arabia by testing of respiratory specimens with real-time reverse transcription PCR
assays targeting the MERS-CoV upstream envelope protein gene and the open reading frame
(ORF) 1a gene (<xref rid="R7" ref-type="bibr"><italic>7</italic></xref>,<xref rid="R8" ref-type="bibr"><italic>8</italic></xref>). Available specimens (or RNA
extracts) were shipped to the US Centers for Disease Control and Prevention (Atlanta,
GA, USA) for full genome sequencing. Methods for sequencing and phylogenetic analysis
have been described previously (<xref rid="R9" ref-type="bibr"><italic>9</italic></xref>).</p><p>During January–February 2016, a total of 27 MERS case-patients were reported by
public health officials from 6 of the 13 administrative regions of Saudi Arabia (<xref ref-type="local-data" rid="SD1">Technical Appendix 1</xref>). Case-patients were
evaluated at 20 different hospitals, 3 of which reported >1 case during the
investigation period. Among the 27 case-patients, 4 (15%) were identified through
routine contact tracing and testing as having secondary cases. Two case-patients (7%)
were identified as occupational contacts of MERS-CoV–positive camels. Of the
remaining 21 case-patients, 17 (81%) were interviewed during March 13–16, 2016;
three were unavailable for interview, and 1 provided incomplete data. Ten (59%) of the
17 interviews were completed by proxy.</p><p>Among the 17 case-patients interviewed, 5 (29%) reported direct camel contact (1 of these
also reported visiting a healthcare facility), and 4 (24%) reported indirect camel
contact (2 of these also reported visiting a healthcare facility) during the exposure
period (<xref ref-type="local-data" rid="SD1">Technical Appendix 1</xref>). Three
case-patients reported having close acquaintances who regularly interacted with camels
but reported they had not seen these acquaintances during the exposure period. One
case-patient was the spouse of a healthcare worker employed in a facility with a
reported MERS patient during the putative exposure period; the spouse was found to be
MERS-CoV–negative by real-time reverse transcription PCR of a respiratory
specimen. The 4 remaining cases could not be further characterized.</p><p>Viruses from 13 of the 27 case-patients were sequenced, and all belonged to the MERS-CoV
recombinant subclade NRC-2015 (<xref rid="R9" ref-type="bibr"><italic>9</italic></xref>), first detected in humans in January 2015; these 13
case-patients were from the Riyadh and Makkah regions (<xref ref-type="local-data" rid="SD1">Technical Appendix 1</xref>). Full genome sequences were obtained from the
specimens of 11 case-patients (<xref ref-type="local-data" rid="SD1">Technical Appendix
2</xref>. Continued and predominant circulation of NRC-2015 supports increased
epidemiologic fitness compared with other clades, as postulated previously (<xref rid="R9" ref-type="bibr"><italic>9</italic></xref>).</p><p>A novel nucleotide substitution was identified in the MERS-CoV sequence from 1
case-patient (<xref ref-type="local-data" rid="SD1">Technical Appendix 1</xref>) at
position 337 located in the stop codon of ORF8b (TAA [Stop] >CAA
[Gln] = Stop113Q), predicted to yield a 143aa protein versus the 112aa
wild-type. ORF8b is an internal ORF overlapped by the nucleocapsid protein gene (<xref rid="R10" ref-type="bibr"><italic>10</italic></xref>); the corresponding
substitution in the nucleocapsid protein gene predicts a conserved amino acid change
(V178A). The virologic and clinical significance of these findings is unknown.</p><p>Since the emergence of MERS-CoV in 2012, virus acquisition has been associated with
direct exposure to camels (<xref rid="R1" ref-type="bibr"><italic>1</italic></xref>) and
with person-to-person transmission in households and healthcare settings (<xref rid="R2" ref-type="bibr"><italic>2</italic></xref>–<xref rid="R5" ref-type="bibr"><italic>5</italic></xref>); other sources of infection are less clear.
Among the patients in our study whose cases were successfully characterized (23/27), 4
had contact with other known case-patients, and 7 reported direct camel contact. Among
the remaining 12 case-patients without these risk factors, 7 were identified as having
at least some exposure to persons with direct camel contact. Our findings suggest that
community and household exposure to persons with direct camel contact might play a role
in MERS-CoV acquisition. Further investigation is needed to determine any specific roles
of these interactions in MERS-CoV transmission.</p><supplementary-material content-type="local-data" id="SD1"><caption><title>Technical Appendix 1</title><p>Characteristics of 27 MERS cases-patients, Saudi Arabia,
January–February 2016</p></caption><media mimetype="application" mime-subtype="excel" xlink:href="16-1042-Techapp-s1.xlsx" xlink:type="simple" id="d36e304" position="anchor"></media></supplementary-material><supplementary-material content-type="local-data" id="SD2"><caption><title>Technical Appendix 2</title><p>Phylogeny of MERS-CoV genome sequences, Saudi Arabia, January–February
2016.</p></caption><media mimetype="application" mime-subtype="pdf" xlink:href="16-1042-Techapp-s2.pdf" xlink:type="simple" id="d36e311" position="anchor"></media></supplementary-material></body><back><fn-group><fn fn-type="citation"><p><italic>Suggested citation for this article</italic>: Alhakeem RF, Midgley CM,
Assiri AM, Alessa M, Al Hawaj H, Bin Saeed A, et al. Exposures among MERS
case-patients, Saudi Arabia, January–February 2016 [letter]. Emerg Infect
Dis. 2016 Nov [<italic>date cited</italic>]. <ext-link ext-link-type="uri" xlink:href="http://dx.doi.org/10.3201/eid2211.161042">http://dx.doi.org/10.3201/eid2211.161042</ext-link></p></fn></fn-group><ack><title>Acknowledgments</title><p>Thanks to Senthilkumar K. Sakthivel and Shifaq Kamili for specimen shipment and
processing.</p><p>This work was funded by the Saudi Arabia Ministry of Health and the US CDC as part of
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