RESEARCHTable 2. Middle East respiratory syndrome coronavirus among dromedary camels, by sample group and camel age, Al-Ahsa Province,Saudi Arabia, 2013–2014*Nasal swab samples, live camels Lung tissue samples, camel carcasses Total samplesAge, yNo. tested No. (%) positive No. tested No. (%) positive No. tested No. (%) positiveYoung, 4 60 13 (21.7) 63 33 (52.4) 123 46 (37.4)Total samples 96 28 (29.2) 91 56 (61.5) 187 84 (44.9)*Tested by reverse transcription PCR.of specimen collection, or even between geographicallyproximate dromedary camel herds where rates of MERS-CoV detection can vary dramatically (9).Of note, detection of MERS-CoV RNA by RT-PCRdoes not necessarily indicate active virus replication. When3 dromedary camels were experimentally inoculated, infectiousMERS-CoV was detected in the upper respiratorytract for only 7 days, but RNA could be detected by RT-PCR for up to 35 days after inoculation (23). We were unableto perform virus isolation studies because of lack ofsuitable biosafety infrastructure.We also found that a high proportion of lung tissuesfrom slaughtered dromedary camels at the Al Omran abattoirwere MERS-CoV positive by RT-PCR. In their experimentalinoculation study, Adney et al. (23) observedhistologic lesions in the epithelium of the upper and lower(trachea, bronchi, and bronchioles) respiratory tract and recoveredviable virus from these tissues and from 1 of 4 lunglobes of an animal euthanized 5 days after inoculation; viablevirus was not recovered from tissues of 2 other animalsat 28 and 42 days after inoculation. Although that limitedstudy found infection extending to the lung of 1 animal, theauthors found that the upper respiratory tract was the predominantsite of virus replication and offered that findingas an explanation for the lack of observed systemic illnessamong naturally infected dromedary camels. An alternativehypothesis posits that, in the natural setting, subclinicalMERS-CoV infection of the lower respiratory tract alsooccurs, possibly enhanced by crowding and stress enduredduring transport and corralling before slaughter. Althoughwe did not collect matching premortem nasal swab samplesfrom slaughtered animals to determine how many were alsopositive for MERS-CoV in the upper respiratory tract, ourfindings raise the possibility that testing upper respiratorytract samples alone may underestimate the true numberof actively infected animals. In humans, MERS-CoV wasdetected in the lower respiratory tract of infected patientsfor ≈1 month while oronasal swab samples were negative(24). Likewise, MERS-CoV detection has been found tobe enhanced from lower respiratory tract specimens, andtherefore these specimens are recommended by the WorldHealth Organization for diagnosis of MERS-CoV infection(2,24,25). Although great care was taken to avoid contaminationwith ambient MERS-CoV present in the abattoir, thepossibility that sample contamination occurred cannot beentirely ruled out. Further studies that include immunohistologicexamination and virus isolation from the lower respiratorytract of naturally infected dromedary camels willbe needed to substantiate these findings.Our detection of MERS-CoV RNA in 2 camel calveswith purulent nasal discharge was consistent with those ofHemida et al. (16), who also observed mild clinical signscharacterized by nasal discharge in some naturally infectedyoung dromedary camels, and of Adney et al. (23), whodocumented appearance of purulent nasal discharge in the3 experimentally infected adult dromedary camels. We alsodetected MERS-CoV RNA in a higher proportion of specimensfrom younger than from older adult dromedary camels,consistent with findings of previous studies that MERS-CoVinfection is more common among young camels (5,16).Our study also investigated temporal variation inMERS-CoV infection in dromedary camels. Althoughdata interpretation was complicated by discontinuity in themonths sampled and sampling from only 1 animal groupin some months, a temporal pattern in MERS-CoV prevalencewas apparent. For both animal groups, peak detectionoccurred during November 2013–January 2014, followedby a steady decline, reaching the lowest point in May 2014.Although we observed no clear temporal differences in thegeographic origins or ages of dromedary camels brought toslaughter, which might bias these results, our data are neverthelesslimited and should not be used to imply a generalpattern of MERS-CoV circulation in dromedary camels inSaudi Arabia. Nevertheless, these findings would not beunexpected. Increased circulation of MERS-CoV amongdromedary camels during the cool season is consistent withthe prevailing cooler ambient temperatures, which havebeen shown to enhance coronavirus survivability outsidethe host (26,27), and the cool season is the period of peakcirculation of other respiratory viral pathogens of humansin Saudi Arabia (28–30). This period also corresponds withthe peak calving season for dromedary camels in SaudiArabia (16); higher rates of MERS-CoV infections amonga greater proportion of young animals with higher virusloads may increase opportunities for virus spread (5,16).Whereas the link between dromedary camels andMERS-CoV infection of humans is well established(15,31), the overall contribution of zoonotic infections tocommunity-acquired MERS-CoV remains unclear. Serologicstudies of animal handlers in Saudi Arabia who work1156 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 21, No. 7, July 2015
MERS-CoV in Respiratory Tract of Camelsin close proximity to dromedary camels have shown limitedevidence of MERS-CoV infection (32–34). Alghamdi etal. (35), who examined patterns of MERS-CoV infectionsamong humans in Saudi Arabia between June 2013 andMay 2014, did not find a concomitant temporal increasein human infections that corresponded with our findings indromedary camels. Those authors observed a slight, temporaryincrease in cases among humans in June and September2013 and few cases from October through February,after which cases and deaths sharply increased beginningin April 2014. The authors concluded that lower relativehumidity and higher temperatures during these monthsmight have contributed to the dramatic surge in reportedcases. However, more recent data from the World HealthOrganization (36) show a sharp decline in MERS-CoVcases among humans in May 2014; low numbers of caseswere reported from June through August 2014, when meantemperature was highest and relative humidity was lowestin Saudi Arabia (34). Moreover, a recent increase in numbersof MERS-CoV cases in humans from September 2014through February 2015 corresponds more closely with thetemporal pattern we found in dromedary camels the precedingyear. Further studies conducted over multiple yearsare needed to better understand the ecology of MERS-CoV,which might help inform intervention strategies to reducezoonotic infections.AcknowledgmentsWe thank Isam Al Jalii and Khalid Borsais for assistance withsample collection and Marzooq M. Al Eknah for financial support.Dr. Khalafalla is professor of veterinary virology at King FaisalUniversity, Al-Ahsa, Saudi Arabia. His research focus is on viraldiseases of dromedary camels.Figure 2. Midpoint-rooted phylogenetic tree of Middle Eastrespiratory syndrome coronavirus spike gene open reading framesequences of this virus obtained from camels and select humans(sequences available from GenBank). The estimated neighborjoiningtree was constructed from nucleotide alignments by usingMEGA <strong>version</strong> 6.06 (http://www.megasoftware.net). Sequencenames are derived from GenBank accession number | virus strainname | month-year of collection. Numbers in parentheses denotenumber of additional available identical spike gene sequencesobtained from same identified region of the representativestrains. Bootstrap support values (1,000 replicates) >70% areplotted at the indicated internal branch nodes. Scale bars indicatenumber of nucleotide substitutions per site. Sequences obtainedfrom camels are designated by an icon; sequences obtainedfrom camels in Al-Ahsa Province, Saudi Arabia, 2013–2014, aredesignated by an asterisk (*).References1. Zaki AM, van Boheemen S, Bestebroer TM, Osterhaus AD,Fouchier RA. Isolation of a novel coronavirus from a man withpneumonia in Saudi Arabia. N Engl J Med. 2012;367:1814–20.http://dx.doi.org/10.1056/NEJMoa12117212. Drosten C, Seilmaier M, Corman VM, Hartmann W, Scheible G,Sack S, et al. Clinical features and virological analysis of a case ofMiddle East respiratory syndrome coronavirus infection. LancetInfect Dis. 2013;13:745–51. http://dx.doi.org/10.1016/S1473-3099(13)70154-33. Memish ZA, Mishra N, Olival KJ, Fagbo SF, Kapoor V,Epstein JH, et al. Middle East respiratory syndrome coronavirus inbats, Saudi Arabia. Emerg Infect Dis. 2013;19:1819–23.http://dx.doi.org/10.3201/eid1911.1311724. Albarrak AM, Stephens GM, Hewson R, Memish ZA.Recovery from severe novel coronavirus infection. Saudi Med J.2012;33:1265–9.5. Alagaili AN, Briese T, Mishra N, Kapoor V, Sameroff SC, de Wit E,et al. Middle East respiratory syndrome coronavirus infection indromedary camels in Saudi Arabia. MBiol. 2014; e00884–14.6. Hemida MG, Perera RA, Wang P, Alhammadi MA, Siu LY, Li M,et al. Middle East respiratory syndrome (MERS) coronavirusEmerging Infectious Diseases • www.cdc.gov/eid • Vol. 21, No. 7, July 2015 1157
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