2019 Burden of Middle East respiratory syndrome coronavirus infection in Saudi Arabia

2019·0.44 MB·English

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ContentslistsavailableatScienceDirect
Journal of Infection and Public Health

journal homepage: http://www.elsevier.com/locate/jiph
Burden of Middle East respiratory syndrome coronavirus infection in

Saudi Arabia

RajaaM.Al-Raddadia,∗,OmaimaI.Shabounib,ZeyadM.Alraddadic,

AbdulmohsenH.Alzalabanid,AhmadM.Al-Asmarib,c,AdelIbrahimb,

AbdullatifAlmarashib,TariqA.Madanie

aDepartmentofCommunityMedicine,CollegeofMedicine,KingAbdulazizUniversity,Jeddah,SaudiArabia
bMinistryofH ea lth,Jeddah, SaudiArab ia
cKingFais al Speciali stHospi taland ResearchCenter,Riyadh,SaudiArabia
dDepa rtmen tofFamil yandCom mu nityMed icine,Fa cultyof Medic ine,TaibahUniversity,Madinah,SaudiArabia
eDepartment of Medicin e,F aultyofMed icine,King Abdula ziz University ,Jedda h,SaudiAra bia

a r t i c l e i n f o a b s t r a c t

Articlehistory: MERS-coronavirusinfectioniscurrentlyresponsibleforconsiderablemorbidityandmortalityinSaudi
Receiv ed20June2019 Arabia.Understand ingitsbu rd en,asane merginginfe ctio usdisease,is vitalforde visin gappropr iat econ-
RAeccceepivteedd i1n1 rNevoivsee md fboerrm2 02179 August 2019 trol stra tegies. In this s tu dy, the b ur de n of MERS -CoV was estimate d over 31 months p eriod from June
6,2012toJanuary5,2015.Thetotalnumberofpatientswas835;528(63.2%)patientsweremale,771
(9 2.3%) pa tientswe re ≥25y ears ofag e,and21 0 (25.1%)p atien tswe reh ealthcar eworker s.Ato talof 751
Keywords: (89.9%) patients requi redh ospita liz atio n.Th em ediandu rationb etwee nonsetof illnessan d hospi tal iza-
MERS-Coronavirus
tionwas2days(interquartilerange,0–5).Themedianlengthofhospitalstaywas14days(IQR,6–27).
SaudiArabia
Theoverallcasefatalityratewas43.1%.Basicreproductivenumberwas0.9.BeingSaudi,non-healthcare
BCHauesraedlt efhantcaalriteyw raotrekers winofer ckteiorsn, acna du saegde a≥s6u5b yset aanrst iwa lehree aslitghnibfiu cradnetnly i nasSsaoucdiaitAedra wb iiath. highe r mo rtal ity. In conclu sion, MERS-CoV
©20 19TheA u thor(s).Pub lished byElse vie rLtdo nbehalfofKingSaudBinAbdulazizUniversityfor

HealthSciences.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense(http://creativecommons.

org/licenses/by-nc-nd/4.0/).
Introduction piratoryillnessoftenevolvesintoshortnessofbreathandsevere

respiratory illness. Disease severity varies widely from asymp-

In2012,anovelviralinfectioncausingsevereacuterespiratory tomaticcasestofataloutcomes.Itisbelievedthatmostinfected

illness in humans was identified in Saudi Arabia. The virus, now personsdonotshowsymptomsasindicatedbyaseroprevalence

knownasMiddleEastrespiratorysyndromecoronavirus(MERS- surveythatestimatedthenumberofseropositivepeopleinSaudi

CoV),wassubsequentlyreportedfrom27othercountriesininthe Arabiatobenearly45,000persons[3].Thecasefatalityrateamong

Middle East, North Africa, Asia, Europe and the United States of clinicalcaseshasbeenestimatedtobe40%[4].Althoughthehigh

America[1].ThelargestoutbreakswerereportedfromSaudiAra- case fatality of the disease and the frequent occurrence of out-

bia,UnitedArabEmirates,andtheRepublicofKorea.AsofJuly2019, breaks provoked calls to develop a vaccine [5], several obstacles

WHOreportedatotalof2458laboratory-confirmedcasesworld- wereencounteredincludinglackofananimalmodelandthehigh

wideincludingatleast848deathssinceApril2012[1].Amongall costofvaccinedevelopment[6].

casesreportedworldwide,2067(84%)caseswerereportedfrom MERS-CoV causes considerable morbidity and mortality with

SaudiArabia[1,2]. a substantial healthcare cost. Understanding the burden of this

Patients with MERS-CoV infection usually present with acute emerginginfectiousdiseaseisvitalfordevisingcontrolstrategies.

respiratorysignsandsymptomsincludingfever,cough,headache, Previousstudiesdescribedtheepidemiologyofhospitaloutbreaks

myalgia, and sometimes nausea, vomiting, or diarrhea. The res- [7,8],communityoutbreaks[9],aswellasregionalortime-specific

cases [10–13]. The objective of this study was to estimate the

burdenofMERS-CoVovera31months-periodfollowingitsfirst

identification in 2012 including the nation-wide MERS-CoV epi-
∗Correspondingauthorat:FacultyofMedicine,KingAbdulazizUniversity,POBox
demicthatoccurredinSaudiArabiain2014uptoJanuary2015.
80215,Jeddah21589,SaudiArabia.

E-mailaddress:[email protected](R.M.Al-Raddadi).

https://doi.org/10.1016/j.jiph.2019.11.016
1876-0341/©2019TheAuthor(s).PublishedbyElsevierLtdonbehalfofKingSaudBinAbdulazizUniversityforHealthSciences.Thisisanopenaccessarticleunderthe

CCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).

Pleasecitethisarticleinpressas:Al-RaddadiRM,etal.BurdenofMiddleEastrespiratorysyndromecoronavirusinfectioninSaudi

Arabia.JInfectPublicHealth(2019),https://doi.org/10.1016/j.jiph.2019.11.016
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Table1 Table3

Demographiccharacteristicsoflaboratory-confirmedMERS-CoVcases–June1st, Numberofcasesandcasefatalityrateoflaboratory-confirmedMERS-CoVcasesby

2012–January5th,2015(n=835). year.

Characteristics No.(%) Year Numberofcases Deaths Casefatalityrate

Age 2012 5 3 60

<15 28(3.3) 2013 160 84 51.5

15–<25 36(4.3) 2014 670 274 36.9

25–<55 434(52.0)

55–<65 142(17.0)
≥65 195 (23.4)
Multiplelogisticregressionsanalysiswasperformedtoadjust
Sex
Male 528(63.2) forconfoundingfactorsandidentifythefactorsassociatedwithcase
Fema le 307(36.8) fata lity.Allvaria blewit hpv alue<0. 1in thebiv ariateanal ysisw ere

Nationality includedintheregressionmodel.Thiswaspresentedasoddsratio
Saudi 545(65.3)
(OR)withconfidenceinterval(CI).Thelevelofsignificancewasset
Non Saudi 290 (34.7) atp≤ 0.05 .
Region
Jeddah 240(28.7)

Riyadh 250(29.9)
Results
Others 345(41.4)

Job
Healthcareworkers 210(25.1) The total number of reported cases during the study period

Non-healthcareworkers 625(74.9) was835cases.Table1showsthedemographiccharacteristicsof

alllaboratory-confirmedMERS-CoVcases.Malesweremorecom-

monlyaffectedthanfemales(63.2%versus36.8%).Thevastmajority
Methods ofpati entswer ebet ween25 -54ye ars(52 %)or≥ 65 year s(23.4%)

ofage.HCWscomprised25.1%ofthecases.HealthCareworkers
This study analyzed the data of all MERS-CoV cases that con- we re y ounger than the other p at ient s (mea n age 38.9± 11.6 vs
firmed by Real time PCR by Ministry of Health’s surveillance 52.7± 20.3yea rs,re spec tively, pvalue< 0.001) .Sau disc om pris ed
programfromJune6,2012toJanuary5,2015.
63.2%ofthecases.AlthoughMERS-CoVcaseswerereportedfrom
ThissurveillancewasnationwideunderthesupervisionofMin-
virtuallyallregionsofthecountry,abouttwothirdsofthecases
istryofHealthtoensurethatthecasedefinitionwasfollowedas
werereportedfromRiyadh(29.9%)andJeddah(28.7%).
pernationalMERS-CoVguidelines.
Afterthefirst2casesofMERS-CoVinfectionreportedin2012,
Ethical approval was obtained from the Institutional review
the number of reported cases ranged between 1-27 cases per
boardofJeddahHealthdirectorate(IRBapprovalnumberA00223).
month. This rate continued till March 2014 when 53 cases were
Basic information for the confirmed cases that was collected
reportedinthatmonthfollowedbyamoredramaticincreasein
includedage,sex,occupation,dateofonset,hospitalization,dura-
thenumberofcasesinthefollowingmonth(April2014)whenthe
tion of hospital stay for hospitalized patients, and mortality.
numberofcasesreachedupto317casesinonemonth.Emergency
Durationbetweenonsetofillnessandadmissiontohospital,case
investigationsandcontrolmeasurescoordinatedbytheMinistryof
fatalityrate,secondaryattackrate,andbasicreproductionnumber
Healthledtoasharpdeclineinthenumberofreportedcasesto150
werecalculated.
casesinMay2014andfurtherdownto29casesinJune2014.Since
Descriptiveepidemiologywasperformedondemographicdata,
then,thenumberofreportedcasesreturnedbacktoitsprevious
andanalyticepidemiologywasperformedtoassessanydifference
rate(Fig.1).Thebasicreproductivenumberwas0.9.
incasefatalityrateamonghealthcareworkersandothers.Statis-
Hospitalization associated with the MERS-CoV was estimated
ticalanalyseswereperformedusingSPSSversion21.0(SPSSInc.,
tobe2per100,000population.Themediandurationbetweenthe
Chicago,IL).Categoricalvariableswerepresentedasfrequencyand
onsetofclinicalsymptomsandpresentationtohospitalswas2days
percentages.Agewaspresentedasmeanandstandarddeviation
withaninterquartilerange(IQR)of0–5days.HCWspresentedto
(SD). Length of stay in hospital and duration between onset of ill- hosp ital s earlier than non− HCW s ( 2 ve rsus 3 days, respective ly,
ness and admission were presented as median and interquartile
p=0.001).Themedianlengthofhospitalstaywas14days(Table2).
range (IQR). Th e length ofs tayamo ngnon − HCWsw assi gnifi can tlym oreth an
The basic reproduction number or ratio (R0), defined as the that among H CWs (15ver sus12days, resp ectively,p=0 .023) .
expectednumberofsecondarycasesproducedbyatypicalinfected
Table3showsthecasefatalityratebyyearfrom2012to2014.
individual early in an epidemic in an otherwise uninfected and
Theoverallcasefatalityratewas43.2%.Thehighestcasefatalityrate
completelysusceptiblepopulation[14],wascalculatedusingthe
wasobservedinthefirst2years(60%for2012and51.5%for2013)
followingformula:
whichdecreasedto36.9%in2014whenmorecaseswerereported

R =(infection/contact)×(contact/time)×(time/infection). duringtheoutbreakin2014.Table4showsthecasefatalityrateby
0
agegroupsandage-specificmortalityrateper100,000population.

=(835/19)×(19/7)×(7/835) = 0.9. Table 5 shows the results of the multivariable logistic regression
analysisforpatients’characteristicsassociatedwithmortality.

Table2
Length ofstayanddurationbetweenonsetofsymptomandadmissionamonghealthcareworkers(HCWs)andnon-healthcareworkers(Non−HCWs).

Allcases(n=574) HCWs(n=178) Non-HCWs(n=396)
Characteristics p-Value**
Median IQR* Median IQR* Median IQR*

Lengthofstay 14 6–27 12 6–21 15 6–31 0.023

Durationbetweenonsetofsymptomandadmission 2 0–5 2 0–5 3 1–6 0.001

* Inter-quartilerange.
** Man–Whitney test.

Pleasecitethisarticleinpressas:Al-RaddadiRM,etal.BurdenofMiddleEastrespiratorysyndromecoronavirusinfectioninSaudi

Arabia.JInfectPublicHealth(2019),https://doi.org/10.1016/j.jiph.2019.11.016
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R.M.Al-Raddadietal./JournalofInfectionandPublicHealthxxx(2019)xxx–xxx 3

Fig.1. EpidemiccurveofMERS-CoVcasesbymonthandoutcomebasedondateofonsetforsymptomaticanddateofdiagnosisforasymptomaticpatientsinSaudiArabia

fromJune1st,2012–January5th,2015(total:835cases).

Table4

Casefatalityratebyagegroupsandagespecificmortalityrateper100,000populationofpatientswithlaboratory-confirmedMERS-CoVinfectionfromJune1st,2012to

January5th,2015(n:835cases).

Age(years) Numberofpatients Deaths Casefatalityrate Age-specificmortalityrate/100,000population

<15 28 7 25.0 0.33

15–<25 36 8 22.2 0.64

25–<55 434 116 26.7 3.3

55–<65 142 76 53.5 10.8
≥65 195 15 4 79.0 21.1

All 835 361 43.2 1.24

Table5

FactorsassociatedwithmortalityamongMERS-CoVcases.

Characteristic Totalnumberofcases Numberofdeaths(%) OddsRatio(95%CI) pValue

Age
<15 28 7(25) Reference

15–<25 36 8(22.5) 2.7(0.6–12) 0.2

25–<55 434 116(26.7) 4(1.1–14.1) 0.03

55–<65 142 76(53.5) 10.3(2.8–37.9) <0.001
≥65 195 15 4(79) 35.6 (9.6–132.3 ) <0.001

Sex
Female 307 107(34.9) Reference

Male 528 253(47.9) 1.4(0.9–2) 0.1

Nationality
Non-Saudi 290 70(24.1) Reference

Saudi 545 290(53.2) 1.6(1–2.6) 0.07

Region
Jeddah 240 101(42.1) Reference

Riyadh 250 108(43.2) 0.7(0.4–1.2) 0.2

Others 345 151(43.8) 0.8(0.5–1.3) 0.4

Job
Healthcareworkers 210 18(8.6) Reference

Non-healthcareworkers 625 342(54.7) 5.4(2.9–10.1) <0.001

Eachfactorisadjustedforallotherfactorsinthetable.

Discussion JeddahandRiyadhwerethehardest-hitcitiesandSaudicitizens

comprisedtwothirdsofthecases.Healthcareworkerscomprised

TheemergenceofMRES-CoVisabigchallengefortheSaudiAra- quarterofthereportedcases.Thisledtoacuteshortageofstaffin

bianhealthcaresystem.SincetheMiddleEastisacenterfortourism healthcarefacilitiesparticularlyinJeddahandRiyadhasaresult

andbusinessactivities,travelingtothisregionprovidesopportuni- ofsickleavesandfearfromgoingtotheworkplace(Personalcom-

tiestoacquireandspreadMERS-CoVbeyonditsboundaries.Saudi munication,MinistryofHealth).

Arabia,asadestinationofmillionsofpilgrimsfortheHajjseason Recent studies showed that the primary source of MERS-CoV

everyyearandforOmrayear-round,isparticularlyunderanenor- infectiontohumansisdromedarycamels[17,18].Humansprimar-

mouschallengetoprotectnotonlyitsowncitizensandresidents ily acquire the virus from camels either directly through direct

butalsotheentireworld’spopulationasawholefromthisemerging contactwithinfectedcamels’respiratorysecretionsorindirectly

infectiousdisease. throughcontactwithpeoplewhohavehadcontactwithinfected

Emergencyinvestigationsandevidence-basedcontrolmeasures camels’respiratorysecretions[18].Theseprimaryinfectionsmay

fortheMERS-CoVepidemicthatoccurredinAprilandMay2014in in sequence lead to secondary human-to-human transmission

SaudiArabiaseemstohaveledtoasharpdeclineofcasesdownto throughclosecontactwithinfectedhuman-respiratorysecretions

thebaselinelevel[15,16]. usuallyinthehealthcare[11,12,16,19–22]or,lesscommonly,the

Pleasecitethisarticleinpressas:Al-RaddadiRM,etal.BurdenofMiddleEastrespiratorysyndromecoronavirusinfectioninSaudi

Arabia.JInfectPublicHealth(2019),https://doi.org/10.1016/j.jiph.2019.11.016
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householdsettings[23–26].Community-basedtransmissionout- were admitted to the ICU or not. Therefore, we were unable to

side the household settings is rare [12,27]. Factors that cause identifytheburdenofMERSCoVontheICUadmissions.

amplification of MERS-CoV infection in the healthcare settings Inconclusion,MERS-CoVinfectioncausedasubstantialhealth

includesuboptimaladherencetostandardinfectioncontrolprac- burdeninSaudiArabiaduetohighmorbidity,mortality,andhospi-

ticeandrespiratoryetiquette,failuretoperformtriagetosegregate talizationrate,longhospitalstay,andshortageofstaff.Enhancing

patients with acute respiratory illness particularly in the Emer- MERS-CoVdata-sharingandanalysisforbetterunderstandingof

gencyDepartmentsandDialysisunits,overcrowdingofpatients, theepidemiologyofthisnovelviruswouldhelpindevisingeffec-

anddelayeddiagnosisbecauseofatypicalpresentationoftenmim- tivepreventivestrategiestoreducetheburdenofthisviralinfection

ickingheartfailureoracutedengue[16,19–22,28]. onthehealthsystem.

The basic reproduction number or ratio (R ) is used to mea-
0

surethetransmissionpotentialofadisease.Itisthoughtofasthe Funding

numberofsecondaryinfectionsproducedbyatypicalcaseofan

infectioninapopulationthatistotallysusceptible.WhenR0is<1, Nofundingsources.

theinfectionwilldieoutinthelongrun,whereas,ifR is>1,the
0

infectionwillbeabletospreadinapopulation.Generally,thelarger Competinginterests

thevalueofR ,theharderitistocontroltheepidemic.Thebasic
0

reproductive number in our study was 0.9 which indicated that Nonedeclared.

eachcasewouldonaverageleadtolessthanoneadditionalcase

andthattransmissionofthisinfectionwilleventuallystopifthere References

wasnoexternalre-infection.ThecontinuallyreportedMERS-CoV

caseswithoccasionalclustersobservedinSaudiArabiadespitethe [1] World Health Organization. Middle East respiratory syndrome coronavi-
low R 0is lik ely due to repeated external re- introd uction of the vi rus reumse r(gM eEnRciSe-sC/om Ve)r;s -2c0o1v/9e n(/A.cc essed 2 4 Au gust 2019) http://ww w.who.int/
fromcamels.
Th eincreaseofcommunity-acquiredcasesofMERS-CoVinfec- [2] 2M0i1n9is)thrytt opfs :H//ewawlthw. .Cmoomhm.goavn.ds aa/nend/ CcoCnCt/rPoalg ceesn/dteerf;a u2l0t.1a9s p(xA.ccessed 24 August
tionno tedinthe p eriodbetweenMarch -May in SaudiArabi amay [3] Müller MA,MeyerB,CormanVM,Al-MasriM,TurkestaniA,RitzD,etal.Pres-
enceo fMi ddleEa st respirat ory syndrome c oronavirus an tibo die s in Saudi
lciokrerleysplionnkde dtot oa seexapsoosnuarle fatcotocra imn eclosm[2m9u].niTthyi-sbapsoesds itbrlaenssmeaissosinoanl 2A0ra1b5 i;a1:5 :a5 5n9a–ti6o4 n,whtidtp e:, //cdrxo.sdso-is.eocr tgi/o1n0a.1l,0 s1e6r/oS l1o4g7ic3a-l3 0s9tu9d( 1y5. )L7a0n0c9e0t -3I n.fe ct Dis
increa seofh um anMERS-C oV casesc orres pond stothee ndofthe [4] MajumderMS,Ri versC,LofgrenE,FismanD.EstimationofMERS-coronavirus
reproducti ven umber an dcasef at alityrat ef orthesprin g 2014SaudiArabia
calving season (December–February) for camels in Saudi Arabia Outbreak:ins ightsfro mp ublic lyavaila bled ata .PL oSCurr 2014 ;6,htt p://dx.
[30,31]. It also corresponds to the weaning season when camels doi.org/10 .1371/cu rrents .outbrea ks.98d2f8 f3382 d84f3 9073 6cd5f5fe 133c.

areweanedofmilkat12–16monthsofage.Arecentprospective [5] ZhangN,JiangS,DuL.Currentadvancementsandpotentialstrategiesinthe
develo pm ento f MER S -CoVvac cines.ExpertR evV accines2 014;13:76 1– 74,
study showed that MERS-CoV detection by RT-PCR in dromedary http://dx.doi. org /10.1586/14 760584.2 014.912 134 .
camelswasmorecommonintheperiodbetweenNovemberand [6] PapaneriAB,JohnsonRF,WadaJ,BollingerL,JahrlingPB,KuhnJH.Middle
January ,cor respon dingtot he cam els’cal vingseaso n[32].Sev eral Eastresp irato rysyndr ome :obsta cl esandpro sp ectsfor vacc inede velo pment.
studies a lso showed th at MER S-CoV R NA she dding i s mor e com- E2x0p1e5 r.1t 0R3e6v0 3V3a.c cines 2015 ;14:949–6 2, h ttp://dx.d oi.o rg/10.15 86/14760584.
moninjuvenilethaninadultcamels[31–34].Therefore,juvenile [7] AssiriA,McGeerA,PerlTM,PriceCS,AlRabeeahAA,CummingsDAT,etal.
came ls younger than 2 years ofagea relikely tobeanim portant Hospi tal outbreak o fmid dle eastr espi rat orysyndr ome coronaviru s.N Eng lJ
source of new M ERS-C o V infe ctio ns i n ca mels a nd hu ma ns leading [8] MAle-Adb 2d0a1l l3a;t36M9M:4,0P7 a–y1 n6e, hDttCp,: A//ldqxa. sdroaiw.oirgS/,1R0h.1a 05B6,/TNoEhJmMeo aR1A3,0A6b7e4d2i.G R, eta l.
tMoa hricghhaenr dinMciadyen[3ce1 ,o3f3 h,3u4m].an infection during the period between Hviorusps:itaal-ases sroolcoiagti ec,d eopuidt bermeai okl oogf icM,iadndd le c Eliansitc arle sdpeirsactroipr tyi osny. ndCrlionm Ien fceoc rtonD ais-
The ove rallC FRwas43.2%.Thehighestratewasamongcases 2014; 59 :1225–33, http://dx.doi.org /10.1 093/cid /ciu359.
1≥56–52 y5e yaresa r(s79(2 %2) .2o%f )agoef , awghe.ileT htehree lwowasesat n raetxep wonaes n atmialoningc rceaaseses [9] mAMlue-Bmnaiittsyihn c ,ZaKAsien, Cgcodlutotsmeten ro Msf oS, faW uMdaitidsAdorlnea b SEiJaa, sK:tae rldelaesmpsci rrPai,pt Zotiurvyme slgyaen And,o rAmolmhicaesk tceuoedrmoyn. RIanFvt,i erJutI nsa flie.n cC tHoDmaifs-r
in CFR after age 55. Pa tient s ≥65 years of age had the highest 2014;23: 63–8,http :/ /dx.do i.org/10 .1 016/j.ijid.20 14.03.13 72.
[10] AlghamdiIG,H ussainII,AlmalkiSS,AlghamdiMS,AlghamdiMM,El-Sheemy
risk of mortality with OR of 35.6 (95% CI = 9.6–132.3). Males had MA.Thep atte rnofMid dl eEastre spir atorysynd rom ecoronavi rusin SaudiAra-
1.4 times higher case fatality compared to females but this was bia: ade scriptiv ee pidemi olog icalanalysis ofdatafr omtheSaud iM inist ryof
not statis tically signifi cant. A higher ris k o f morta lity was also Hea lth .IntJGenM ed2014;7:417– 23,http: //d x.doi .org/1 0.2 147/IJG M.S6706 1.
[11] Drosten C, M uth D,Co rmanVM,Huss ainR,AlMasriM,HajOmarW,etal.An
CnIo=ti1ce.0d– a2m.6o).nNg oSnau−dHi CcWasehs acdomsipganriefidc aton tnlyonh-Sigahuedrism (OoRrt =a l1it.6y; r9a5t%e soybnsedrrvoamt ieo ncoalr,o lnaab voir rautsoriny-Jbea dsdeadh staunddyR oify aodu htb,rk eiankgsd oo fm Mo ifddSaleu dEaisAt r raebs ipai, r2a0t o1r4y.
co m pared to HCWs (OR =5.4 95% CI=2.9 –10.1). Multiple l ogis- ClinInfect Dis2015;60 :36 9–77,h ttp:/ /dx.doi. org/10.10 93 /cid/ci u812.
taincd re≥g6re5ssy ieoan r sshoofwaeg de twh eart ebes iignngi fiS acaund ti l, ynoasns-ohceiaalt tehdcawreit hwo hrikgehresr, [12] 2MO0be1od4 h2 oM0 I1KE5R, T; S3o-7Cm2o c:V8z y4ok6u –Stb5Mr4e,, Aahklt- tAipns: m/J/edad xrdi. daAhoMi .—o, Br aga /nl1ijn0akr.1 At0oA5 ,6h A/eNla-EMltJhMu gcoatair 1He4 ,f 0Aa8cloi6lri3at6iien.si. M NS E, entg al lJ.
CFR .Unli kethe re lated SARS coronavirus ,theMERS- CoVi sasso- [13] Saad M,OmraniAS,Baig K,BahloulA,ElzeinF,MatinMA,etal.Clinicalaspects
ciate d with a re latively highe r CFR (>30%) and noticeable ag e and annadvi ro uust cinofmecetsi oo nf: 7a 0s ipnagt liee- nctesn wteirthe xMp eidridelnec Eea isnt Sraeus pdiiraAt roarb yi as. yInndtrJoImn fee cctoDrois-
sraetxi odiafmfeorenngcecos nafimrmonegd ccoansfiesrmofedM cRaEsSe-sC [o1V2]i.s Trheep omrtaelde ttoo bfeem2a:l1e, [14] 2Fr0a1s4e;r29 C:,30D1o–n6n, ehlt ltyp :/C/Adx,.dCoaiu.ocrhge/m 10e.z101S,6/Hj.iajin da.2g 0e14W.0P9 ,.0V0a3n. Ker kh ove M D,
with highest rates of m orbid ity and morta lit y occurri ng am ong Holling sw orthTD,et al.P andemicpot ent ialofast raino finflu enzaA(H1 N1):
opbatsieer nvtesd ≥a5m0 oy negarHs Co Wf a sgien [c1o2m]. Tphaer i ssiognn wifiictahnntolyn l−o HwCeWr msoisrltiak leitlyy rdautee [15] e1Ma1ar7dl6ya 0nfi6in2Td.Ain.Cgass. eScdiee finnc iet i2o 0n0a9n;d32m4a:n1 5ag5e7m–6e1n,t h otftp pa: /t/iednxt.ds owi.io thrgM/1E0R.1S1c2o 6r o/sncaievnircues.
toearlier present ation( 2v s3days,res pecti vely),young er age(3 8.9 inSaud iAr abia. LancetIn fect Dis2014;14: 91 1–3,htt p://dx .doi.o rg/10.1016/
S1 473-3 099(14) 70918-1 .
vs52.7years,respectively),andlowerriskofhavingcomorbidities.
[16] HastingsDL,TokarsJI,AbdelAzizIZAM,AlkhaldiKZ,BensadekAT,Alraddadi
We acknowledge two limitations to our study including that BM,etal. Out breako fm iddle east respira torysynd rom eattertia ryc arehospi-
person swhodevelop mild symptoms w illlik elylea dtoanun der- tal,J ed da h,SaudiA ra bia,201 4.Em ergInfect Dis2016;2 2: 794–801 ,htt p://dx.
doi .org/10.3 201/e id2205. 15179 7.
estimation of the diseases burden and an overestimation of the
[17] AzharEI,El-KafrawySA,FarrajSA,HassanAM,Al-SaeedMS,HashemAM,etal.
severity.Thesurveillancedatadidnotindicatewhetherpatients Eviden ce forcamel-t o-h umant ran smissio nof MERScor onav irus.NE nglJ M ed
2014;370 :24 99–505,http://dx .doi.org/10.10 5 6/NEJM oa1401505.

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[18] AlraddadiBM,WatsonJT,AlmarashiA,AbediGR,TurkistaniA,SadranM,etal. [27] World Health Organization. Middle East respiratory syndrome coronavi-
Riskfactor sfor primar yM iddleEast re spirato rys yndromec or onaviru sil lne ss rus (M ERS-CoV ): summary o f curren t situ ation, litera ture updat e and risk
inhu mans,S au diArabia ,2014.E mer gInfectDis 2016;22:4 9–55,http:// dx.doi. asse ssment–asof 5February 20 15;2019 (Accessed 15April20 16)http ://w ww.
or g/10.3201 /eid2 201.151 340. who.int/csr/dis ea se /coronav irusin fectio ns/mers-5 -fe bruar y-201 5.pdf?ua=1.
[19] ChoiJY.AnoutbreakofMiddleEastrespiratorysyndromecoronavirusinfection [28] Madani TA, Althaqafi AO, Alrad dadi BM. Infection prevention and control
inSo uth Ko rea,2015 .Y onseiM edJ2 015;56:117 4–6,http: //dx.doi.org/ 10.3349/ guidelin esf orpatient swi thMiddle East respirator ysyndrome coro navirus
ym j.201 5.56.5.1 174. (MERS-CoV )in fection.S audi MedJ20 14;3 5:897–913.
[20] KiM.2015MERSoutbreakinKorea:hospital-to-hospitaltransmission.Epi- [29] SprengerM, Coulombi erD. Midd le Eastrespiratorysyndromecoronavirus-
de mio lHea lth201 5;37:e201 50 33,htt p://dx.doi.org/10.417 8/epih/e20150 33. twoyears in totheepidem ic .EuroS urve illBullEurS urLesMal Transm=Eu r
[21] LeeSS, Wong NS.Probabletransm issionchainsofMiddleEastrespiratory Com munD isB ull2 014;19:20 783.
syn drom ecor onav irusand themultipleg enerat ion sofsec onda ryinfection [30] Almutairi SE, Bou jenaneI,MusaadA,Awad-AcharariF.Non-geneticfactors
inSouthK orea.IntJIn fectD is2 015;38:6 5–7,http://d x.d oi.org/10.1 016/j.ijid. influencin gre productive tr aitsandc alv ingweightinSa ud icamels.Tro pAnim
20 15.07. 014. HealthProd 2010;42:108 7–92, http ://dx.do i.org/10 .1 007/s1 1250-0 10-95 29-y.
[22] KhanA,FarooquiA,GuanY,KelvinDJ.LessonstolearnfromMERS-CoVoutbreak [31] Hemid aMG ,ChuDKW,PoonLL M,RAPMPerera,AlhammadiMA,NgH-Y,etal.
inSou th Korea.J In fectD ev Ctries 20 15;9:543 – 6. MERSco rona viru sind romed ary camel herd,Sa udiArabia. Eme rg Infec tD is
[23] M emish ZA,Zu m laAI, Al-H akeem RF,Al-RabeeahAA,StephensGM.Family 2014; 20:1231–4,h ttp ://dx.doi.or g/10.32 01/eid 2007. 140571 .
clustero fM iddleE ast respiratory synd romecoron avir usinfectio ns.N EnglJ [32] KhalafallaAI,LuX ,Al-MubarakAIA,DalabAHS,Al-BusadahKAS,ErdmanDD.
Med20 13 ;368:24 87–9 4,http://dx .doi.org/10 .1056/NEJMo a1303729. MERS-CoV in upp er respiratoryt ract andlun gsof dromedaryc ame ls,SaudiA ra-
[24] Abro ugF,SlimA,Ouane s-BesbesL,HadjKacemM-A,DachraouiF,OuanesI, bia,2013-2 01 4.Em ergInfectD is20 15;2 1:115 3– 8,http://d x.doi.org /10.3 201/
etal.Fam i lyclu ste rofMiddleEastr es pirato rysynd rome coronaviru si nfection s, eid2 107.150070 .
Tu nis ia,201 3.Eme rg InfectD is2 014;20:152 7–30,http ://dx.doi.org /10.3201/ [33] AlagailiAN,BrieseT,MishraN,KapoorV,SameroffSC,BurbeloPD,etal.Middle
eid2009 .14037 8. Eastres pira torysy nd romec oro navirus in fectionin dro medary cam e lsi nSaudi
[25] OmraniAS,MatinMA,HaddadQ,Al-NakhliD,MemishZA,AlbarrakAM.A Arab ia.MBio20 14;5:e0088 4–14,http:/ /dx.doi.o rg/ 10.1128/mB io.0088 4- 14.
family c lust er of M idd le East r esp iratory sy nd rome co rona virus infe ctio ns [34] Werner y U, Corman VM, Wong EYM, Tsang AKL, Muth D, Lau SKP, et al.
related toalik ely unreco gnize dasymptom aticormi ldcase.IntJ InfectDis Acutemi dd leEastre spira torysy ndrom ecor onavi rusinf ect ioni nlive sto ck
2013;17 :e 66 8–72, http://dx.doi.o rg/10.1016/j.iji d.2 013.0 7.001 . Drome daries, Duba i,2014.Eme rgInfectD is2015;21:1 019–22,h ttp ://dx.doi.
[26] DrostenC,Meyer B,MüllerMA,CormanVM,Al-MasriM,HossainR,etal. org/10.3201/e id2106 .15003 8.
Transmi ssi on of M E RS-coro navir us in h ouseh old cont acts . N Eng l J M ed
2014;371:828 –3 5,http://dx.doi.org/1 0.1 056/NEJMo a1405858 .

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