MAJOR ARTICLE

Prevalence of MERS-CoV Nasal Carriage and

Compliance With the Saudi Health
Recommendations Among Pilgrims Attending
the 2013 Hajj
Ziad A. Memish,1,2 Abdullah Assiri,1 Malak Almasri,1 Rafat F. Alhakeem,1 Abdulhafeez Turkestani,3
Abdullah A. Al Rabeeah,1 Jaffar A. Al-Tawq,4,5 Abdullah Alzahrani,1 Essam Azhar,6 Hatem Q. Makhdoom,7
Waleed H. Hajomar,8 Ali M. Al-Shangiti,9 and Saber Yezli1
1
Global Centre for Mass Gatherings Medicine (GCMGM), Ministry of Health, 2College of Medicine, Alfaisal University, Riyadh, 3Makkah Regional Health
Affairs, Ministry of Health, Jeddah, 4Saudi Aramco Medical Services Organization, Dhahran, Kingdom of Saudi Arabia; 5Indiana University School of

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Medicine, Indianapolis; 6Special Infectious Diseases Unit, King Abdualziz University, King Fahad Medical Research Center, Jeddah, 7Jeddah Regional
Laboratory and Blood Bank, Ministry of Health, 8Riyadh Regional Laboratory and Blood Bank, Ministry of Health, and 9General Directorate of Laboratory
Services, Ministry of Health, Riyadh, Kingdom of Saudi Arabia

Background. Annually, Saudi Arabia is the host of the Hajj mass gathering. We aimed to determine the Middle
East respiratory syndrome coronavirus (MERS-CoV) nasal carriage rate among pilgrims performing the 2013 Hajj
and to describe the compliance with the Saudi Ministry of Health vaccine recommendations.
Method. Nasopharyngeal samples were collected from 5235 adult pilgrims from 22 countries and screened for
MERS-CoV using reverse transcriptasepolymerase chain reaction. Information regarding the participants age, gen-
der, country of origin, medical conditions, and vaccination history were obtained.
Results. The mean age of the screened population was 51.8 years (range, 1893 years) with a male/female ratio of
1.17:1. MERS-CoV was not detected in any of the samples tested (3210 pre-Hajj and 2025 post-Hajj screening). Ac-
cording to the vaccination documents, all participants had received meningococcal vaccination and the majority of
those from at-risk countries were vaccinated against yellow fever and polio. Only 22% of the pilgrims (17.5% of those
65 years and 36.3% of diabetics) had u vaccination, and 4.4% had pneumococcal vaccination.
Conclusion. There was no evidence of MERS-CoV nasal carriage among Hajj pilgrims. While rates of compul-
sory vaccinations uptake were high, uptake of pneumococcal and u seasonal vaccinations were low, including
among the high-risk population.
Keywords. Hajj pilgrimage; MERS-CoV; nasal carriage; screening; vaccination.

The Middle East respiratory syndrome coronavirus MERS-CoV was identied in a patient with acute pneu-
(MERS-CoV) is a newly emerged respiratory virus with monia and renal failure in Jeddah, Kingdom of Saudi Ara-
initial high fatality rate among identied cases [1]. bia (KSA) in June 2012 [2]. As of 27 January 2014, the
MERS-CoVis an enveloped, single-stranded, positive- World Health Organization (WHO) has been notied of
sense RNA virus in lineage C of the genus Betacoronavirus 180 laboratory-conrmed MERS-CoV cases from 9 coun-
within the subfamily Coronavirinae [2, 3]. The rst case of tries (France, Germany, Italy, Jordan, KSA, Qatar, Tunisia,
United Arab Emirates [UAE], and the United Kingdom
[UK] [1], all with a direct or indirect link with the Middle
Received 11 February 2014; accepted 3 March 2014; electronically published 11
March 2014.
East. Of these cases, 77 patients (42.7%) have died [4].
Correspondence: Ziad A. Memish, MD, FRCPC, FACP, Deputy Minister Public While the majority of cases now reported have likely
Health, Ministry of Health, PO Box 54146, Riyadh, Central Province, 11514, Kingdom acquired infection through human-to-human transmis-
of Saudi Arabia ([email protected]).
The Journal of Infectious Diseases 2014;210:106772
sion, the primary sporadic cases in clusters are more
The Author 2014. Published by Oxford University Press on behalf of the Infectious likely to have been acquired through contact with non-
Diseases Society of America. All rights reserved. For Permissions, please e-mail:
human sources of the virus [1]. Transmission could be
[email protected].
DOI: 10.1093/infdis/jiu150 through respiratory droplets, or direct or indirect

MERS-CoV Carriage Among Hajj Pilgrims JID 2014:210 (1 October) 1067

contact [5]. Hospital outbreaks [57] and family clusters were calculated based on the number of pilgrims attending the
described [8]. Travel-associated cases were observed in Europe, 2012 Hajj season with 95% condence level and 2% error mar-
notably in UK, France, Germany, and Italy, with secondary gin. The countries of the study population were preselected to
cases in close contacts of index cases without a travel history [1]. cover a wide range of pilgrims from different continents. The
Seventy-six percent of patients with MERS-CoV infection selection reected the Hajj pilgrims population, and included
had at least 1 underlying medical condition, and fatal cases countries with MERS-CoV cases, countries with close geo-
were more likely to have an underlying condition (86.8% graphic proximity to KSA, and countries with frequent and sig-
among fatal cases vs 42.4% among recovered or asymptomatic nicant population movement from and to KSA. These
cases; P < .001) [1]. In a study of 47 conrmed patients from countries included those with the highest annual number of
KSA identied between September 2012 and June 2013, almost Hajj pilgrims. The individuals chosen for the trail from the se-
all (45/47) cases had at least 1 underlying condition, including lected ights were recruited on a voluntary and random basis
diabetes (68%), hypertension (34%), chronic cardiac disease (by selecting every 4th pilgrim from the queue at the airport
(28%), and chronic renal disease (49%) [9]. processing area upon arrival or before boarding returning
The role of asymptomatic carriers in virus transmission and ights) regardless of their age, gender, or medical conditions
the prevalence among the general population is unknown. (excluding children). A standardized data collection form was
Asymptomatic carriage of MERS-CoV has been described [1], used to obtain information regarding the participants age, gen-
including among family contacts [10]. In a study of 7 healthcare der, country of origin, and medical conditions. Vaccination his-
workers with MERS-CoV infection, 2 of them were asymptom- tory was determined from the participants vaccination

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atic and 5 had mild upper-respiratory-tract symptoms [11]. documents.
Asymptomatic carriers of the virus could be a source of trans-
mission and infection, especially among the high-risk popula- Screaming and Processing of the Samples
tion. Hence, the potential of global spread of MERS-CoV is Nasopharyngeal samples were collected from all participants by
great if asymptomatic pilgrims were to be identied. trained physicians. Collection, handling, and storage of the
KSA annually hosts more than 2 million Muslim pilgrims from samples were done as per the CDCs guidelines for patients
around 184 countries during the Hajj pilgrimage, making it one of under investigation for MERS-CoV [18]. A single nasopharyn-
the largest and most culturally and geographically diverse mass geal swab was obtained from each pilgrim using a swab with
gatherings in the world [12]. The presence of elderly pilgrims synthetic ber with a plastic shaft (Remel). The samples were
from across the globe and being in close contact to perform phys- then immediately placed in viral transport medium, transported
ically exhausting religious rites increases their susceptibility to in- on ice to the lab, and stored at 70C. The screening process
fections and creates conditions with a potential transmission of was conducted at the Hajj terminal of King Abdulaziz Interna-
respiratory pathogens [13, 14]. Given the predicted population tional Airport at 2 time periods: a pre-Hajj screening (which in-
movement out of Saudi Arabia, the potential for worldwide cluded 3210 pilgrims and was conducted in the period between
spread of MERS-CoV is a continued concern [15]. To reduce 29th of September and 9th of October 2013 as the pilgrims were
the risk of infectious diseases transmission during the Hajj, the arriving to KSA for the Hajj), and a post-Hajj screening (which
Saudi Ministry of Health (MoH) issues health conditions and rec- involved another 2025 pilgrims and was conducted at the end of
ommendations for travelers to KSA for the Hajj pilgrimage, in- the Hajj between the 14th and 26th of October 2013 as pilgrims
cluding vaccinations requirement [16]. Recommendations were returning to their respective countries).
specic to the emergence of MERS-CoV have been issued and
at-risk individuals coming for Hajj in 2013 were advised to post- Detection of MERS-CoV in Samples
pone the performance of the Hajj for their own safety [17]. MERS-CoV was detected in the samples using reverse transcrip-
In order to evaluate the compliance with the Hajj recommen- tasepolymerase chain reaction (RT-PCR) targeting the region
dations and to evaluate the possibility of acquiring MERS-CoV upstream of the E gene (upE) and the open reading frame 1a
during the 2013 Hajj, we undertook this cross-sectional study to (nsp6 protein) as described previously [19, 20]. Briey, nucleic
screen 2 pilgrims cohorts (beginning of Hajj cohort and end of acid was puried from a 200 L volume of sample using Magna
Hajj cohort) for MERS-CoV, and we sought to describe the Pure LC nucleic acid extraction kit (Roche). Each sample was
compliance with the Saudi MoH health recommendations. independently tested with the 2 RT-PCR assays in a 25 L reac-
tion containing 5 L RNA, 12.5 L of 2X buffer (SuperScript
METHODS III one-Step RT-PCR with Platinum Taq [Invitrogen]),
0.4 L MgCl2 (50 mM), 1 L forward primer (10 M), 1 L re-
Study Population verse primer (10 M), 1 L probe (5 M), 3.1 L RNAse-free
The screening was conducted on 5235 adult (>18 years of age) H2O2, and 1 L SSIII/Platinum Taq enzyme mix (1 U). The
pilgrims performing the 2013 Hajj. The sample size was RT-PCR reactions were performed in a real-time LightCycler

1068 JID 2014:210 (1 October) Memish et al

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Figure 1. Percentage contribution from each country and geographical spread of the 5235 screened pilgrims.

480 machine (Roche) under the following cycling prole: (2.1%). India was the most represented country with 17.1%
1 cycle of 55C for 20 minutes followed by 1 cycle of 94C for of the screened population, followed by Indonesia (12.9%),
3 minutes, then 45 cycles of 94C for 15 seconds, 45 cycles of Pakistan (11.9%), and Turkey (10.7%). Pilgrims from Yemen,
58C for 30, seconds and a single cycle of 40C for 30 seconds. Afghanistan, China, Ethiopia, Sudan, Djibouti, and Canada
A sample was conrmed MERS-CoV positive if both RT-PCR were represented in the post-Hajj screening only. Bangladesh,
assays were positive as per current recommendations [20]. Turkey, India, Indonesia, Malaysia, Pakistan, Egypt, and Nigeria
were represented in both pre- and post-Hajj screenings. The
Ethics screened population included 410 pilgrims from 3 out of
The study was approved by the King Fahad Medical City Insti- the 9 countries with MERS-CoV cases notied to the WHO
tutional Review Board. All participants were recruited on a vol- (Jordan, Tunisia, and UK).
untary basis and gave verbal consent before being included in According to the vaccination documents, all participants re-
the study. ceived meningococcal vaccination; 93% were vaccinated with
the recommended quadrivalent vaccine (serogroups A, C,
RESULTS W-135, and Y). A minority of pilgrims (6.8%), all from Nigeria,
were immunized against cerebrospinal meningitis (CSM,
Samples were obtained from 5235 pilgrims (3210 pre-Hajj, 2025 meningococcal serogroup A) without further details on the
post-Hajj) representing 22 countries (Figure 1) from Asia, Af- type of vaccine used. Ten pilgrims, 9 of whom were from the
rica, Australia, North America, and Europe. The characteristics United States, were vaccinated with the meningococcal conju-
of the screened population are summarized in Table 1. The gate vaccines MCV4. Only 22% of the pilgrims screened had
mean age was 51.8 years (range, 1893 years) with a male/ u vaccination, including 17.5% of those 65 years of age
female ratio of 1.17:1. Approximately 15% of the population and 36.3% of the diabetics. The overall vaccination rate for yel-
screened was 65 years of age or more. Most participants were low fever was 8.8% (among all pilgrims), but 100% for pilgrims
from Asia (78%), followed by Africa (18.7%), then Europe from countries that are required to have such vaccination

MERS-CoV Carriage Among Hajj Pilgrims JID 2014:210 (1 October) 1069

Table 1. Characteristics of the Screened Population Only 4.4% of all pilgrims, 1.5% of those 65 years old and
27.3% of those with diabetes, had pneumococcal vaccination.
Number (Number/Total Number) % No information on the type of pneumococcal or polio vaccines
Pilgrims screened could be obtained from the pilgrims vaccination documents.
Pre-Hajj 3210 3210/5235 61.3 Data on underlining health conditions was available for only
Post-Hajj 2025 2025/5235 38.7 3% of the screened population. Nevertheless, 13.1% had hyper-
Total screened 5235 5235/5235 100 tension and 6.8% were diabetic.
Gender MERS-CoV was not detected in any of the 5235 (3210 pre-
Males 2831 2831/5235 54 Hajj, 2025 post-Hajj) nasopharyngeal samples tested.
Females 2404 2404/5235 46
Age (mean = 51.8)
<18 0 0/5213 0
DISCUSSION
1864 4413 4413/5213 84.6
65 800 800/5213 15.4
We screened 5235 pilgrims attending the 2013 Hajj season for
Continent nasal carriage of the emerging respiratory virus, MERS-CoV.
Asia 4080 4096/5235 78 These included pilgrims from 3 out of the 9 countries with
Africa 979 980/5235 18.7 MERS-CoV cases notied to the WHO (Jordan, Tunisia, and
Australia 46 48/5235 0.9 UK) in addition to a number of countries with close geographic
North America 19 21/5235 0.3 proximity to KSA (Bahrain, Yemen, Kuwait, and Egypt) and

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Europe 111 112/5235 2.1 with frequent and signicant population movement to and
Vaccination history out of KSA (Bangladesh, Pakistan, India, Malaysia, and Indone-
Preflu vaccination 1149 1157/5235 22 sia). The screened population was over-represented by Asian
65 y of age 140 140/800 17.5
countries (78%), and 60% of the pilgrims were 50 years of
Diabetes 4 4/11 36.3
age, which is representative of the general Hajj pilgrims popu-
Prepneumococcal 232 237/5235 4.4
vaccination lation. No samples were positive for the presence of the MERS-
65 y of age 12 12/800 1.5 CoV virus by the 2 RT-PCR assays.
Diabetes 3 3/11 27.3 These results show that among the population screened, there
Preyellow fever 465 466/5235 8.8 was a lack of MERS-CoV nasal carriage. Moreover, the lack of
vaccination
nasal carriage of the virus among the post-Hajj cohort suggests
Nigeria 357 357/357 100
that there were no events of MERS-CoV acquisition in the cohort
Sudan 30 30/30 100
once the pilgrims have been in KSA, performed the Hajj, and
Ethiopia 78 78/78 100
Other countries 0 0 0
were in close contact with other pilgrims and the local popula-
Prepolio vaccination 2228 2228/5235 42.5 tion. These results are in accordance with a previous cohort sur-
Nigeria 358 358/358 100 vey conducted during the 2012 Hajj, which showed lack of nasal
Pakistan 615 615/623 98.7 carriage of MERS-CoV among French pilgrims returning from
India 893 893/894 99.9 Hajj [21]. A cohort of 154 French Hajj pilgrims were systemati-
Afghanistan 121 121/121 100 cally sampled with nasal swabs prior to returning to France, and
Other countries 599 599/599 100 screened for MERS-CoV using the same RT-PCR assay used in
Premeningococcal 5229 5229/5229 100 our study. Despite a high rate of respiratory symptoms (83.4%),
vaccination
including 41.0% inuenza-like illness, no case of MERS-CoV
ACYW135 4861 4861/5229 93
CSM 354 354/5229 6.8
nasal carriage was detected [21]. Although our cohort represents
MCV4 10 10/5229 0.2 a small proportion of the overall Hajj pilgrims population (>1.9
Underlying health conditions million in 2013), the results showed a lack of nasal carriage of
Diabetes 11 11/161 6.8 MERS-CoV among pilgrims. In addition, the results showed
Hypertension 21 21/160 13.1 the lack of transmission of the virus among pilgrims.
Abbreviations: ACYW135, quadrivalent vaccine against meningitis; CSM,
Given the predicted population movement out of Saudi Ara-
cerebrospinal meningitis; MCV4, meningococcal conjugate vaccine 4. bia, the potential for worldwide spread of MERS-CoV exists ac-
cording to Khan and colleagues [15]. By contrast, Breban and
colleagues [22] calculated that the risk of MERS-CoV to have
pandemic potential does not exceed 5%, but they did not take
(Nigeria, Sudan, and Ethiopia). Approximately 43% of all pil- into account the effect of the Hajj mass gathering in their
grims and 99.5% of those from at-risk countries (Pakistan, scenario. Memish et al [23] showed that circulation of the
India, Nigeria, or Afghanistan) received polio vaccination. MERS-CoV in Saudi Arabia is much lower than it was feared,

1070 JID 2014:210 (1 October) Memish et al

announced, or predicted, and that no signicant rise in detec- In accordance with the International Health Regulations
tion rates could be observed along 1 year. In addition, mass 2005 [26], yellow fever vaccination is mandatory for all travelers
gatherings in KSA during the pilgrimages of 2012 and 2013 arriving from countries or areas at risk of yellow fever. Travelers
were associated neither with an increased number of cases, should show evidence of vaccination at least 10 days and at most
nor with reported clusters of cases [24], suggesting poor or 10 years before arrival to KSA. Three countries at risk of yellow
moderate interhuman transmission. Our results support the lat- fever transmission (as dened by the International Travel and
ter and that MERS-CoV in its current form may not have the Health 2012 [27]) were represented in our cohort population:
pandemic potential as those of other respiratory viruses, includ- Nigeria, Sudan, and Ethiopia. Although the overall yellow
ing that of severe acute respiratory syndrome coronavirus [22]. fever vaccination rate was low (8.8%), all (465/465) pilgrims
Due to the MERS-CoV situation, the Saudi MoH recommend- from these 3 high-risk countries were vaccinated against yellow
ed that elderly people (>65 years), people with chronic diseases fever [16].
(eg, heart disease, kidney disease, respiratory disease, and diabe- According to the Saudi MoH health regulations, proof of
tes), and pilgrims with immune deciency (congenital and ac- polio vaccination at least 6 weeks prior to departure to KSA is
quired), malignant disease, and terminal illnesses, as well as mandatory for all travelers arriving from polio-endemic coun-
pregnant women and children (<12 years), postpone the perfor- tries and reestablished transmission countries, namely, Afghan-
mance of the 2013 Hajj for their own safety. This advice was also istan, Chad, Nigeria, and Pakistan, as well as from recently
endorsed by the US CDC for pilgrims traveling to Saudi Arabia endemic countries at high risk of reimportation of poliovirus
for the 2013 Hajj. In our study, 15.3% of the population was 65 (ie, India) [16]. The overall polio vaccination rate was 42.5%,

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years old, and although data on underling health conditions were but 99.5% of all pilgrims from high-risk countries (Afghanistan,
available for a minority of the cohort and only related to diabetes Pakistan, India, and Nigeria) were vaccinated against polio, ac-
and hypertension, 18.7% had at least 1 of these 2 conditions. Both cording to their vaccination documents.
are disorders for which the Saudi MoH recommended potential Vaccination with the quadrivalent ACYW135 vaccine against
participants postpone doing the Hajj in 2013. Although our re- meningitis is required for all pilgrims coming to KSA regardless
sults cannot be extrapolated to all Hajj pilgrims, they suggest that of their country of origin. Travelers should show evidence of
despite the MoH recommendations, a proportion of the pilgrims vaccination no more than 3 years and no less than 10 days be-
were unaware or did ignore this advice. This is not without pre- fore arrival to KSA. In addition, pilgrims from the African men-
cedent; a study of a cohort of 167 French pilgrims participating in ingitis belt are automatically administered ciprooxacin tablets
the 2012 Hajj season found that 39% were over 65 years of age (500 mg) chemoprophylaxis at port of entry to KSA to lower the
and 59% had at least 1 risk factor mentioned in the MERS- rate of carriers [16]. All pilgrims screened were vaccinated
CoV MoH recommendations [21]. In 2013, in preparation of against meningitis according to their documents, 93% of
the Hajj, a similar study (360 French cohort) reported that whom were vaccinated with the recommended quadrivalent
30.8% were over 65 years of age, and nearly half had at least 1 vaccine for serogroups A, C, W-135, and Y.
disorders for which the Saudi MoH recommended potential par- Pneumococci are estimated to cause 1.6 million deaths annu-
ticipants postpone doing the Hajj [25]. In the latter study, nearly ally [28]. Pneumococcal vaccines are widely available, and vac-
65% of the respondents were aware of the ongoing MERS epi- cination is recommended for all adults aged 65 years and for
demic in the KSA and 35.3% were aware of the Saudi MoH rec- adults at high risk who are aged 1964 years and are immuno-
ommendations for at-risk pilgrims to postpone performing the compromised [29]. Of note, a considerable percentage of Hajj
Hajj in 2013. Among 179 at-risk individuals, none decided to pilgrims have preexisting illnesses or are elderly, both important
cancel their participation in the Hajj, even after advice during risk factors for pneumococcal infection [29, 30]. Nevertheless,
pretravel consultation [25]. the rate of pneumococcal vaccination among our cohort was
In addition to the MERS-CoV recommendations, the Saudi low, including among those 65 years of age.
MoH has a set of other health conditions for travelers to KSA Our study has some limitations. Although the cohort
for Hajj [16]. Seasonal inuenza vaccination is recommended screened was large, it only represented a relatively small per-
for international pilgrims before arrival into KSA, particularly centage of the total number of pilgrims attending the 2013
those at increased risk of severe inuenza diseases, including Hajj; hence, the results cannot be extrapolated to all the pil-
pregnant women, children <5 years of age, the elderly, and in- grims population. The use of upper-respiratory-tract swabs in-
dividuals with underlying health conditions (such as HIV/ stead of lower-respiratory specimens may have inuenced the
AIDS, asthma, diabetes, and chronic heart or lung diseases) results. The MERS-CoV load in upper-respiratory-tract speci-
[16]. The rate of seasonal inuenza vaccination was low in mens is generally lower than in the lower-respiratory specimens,
our study, including among the high-risk population. Only though data are limited. The data on vaccination are based on
22% of the screened population (17.5% of those 65 years documentations provided by the pilgrims, and without a possi-
and 36.3% of those with diabetes) was vaccinated. bility of verifying the authenticity of these documents, the rate

MERS-CoV Carriage Among Hajj Pilgrims JID 2014:210 (1 October) 1071

of vaccination in our study may be an overestimation. In addi- infections related to a likely unrecognized asymptomatic or mild case.
Int J Infect Dis 2013; 17:e66872.
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All authors have submitted the ICMJE Form for Disclosure of Potential 20. Corman VM, Muller MA, Costabel U, et al. Assays for laboratory con-
Conicts of Interest. Conicts that the editors consider relevant to the con- rmation of novel human coronavirus (hCoV-EMC) infections. Euro
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