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http://dx.doi.org/10.2147/IDR.S51283

Middle east respiratory syndrome coronavirus: epidemiology and disease control measures

Jaffar A Al-Tawfiq1,2

Ziad A Memish3,4

1Johns Hopkins Aramco Healthcare, Dhahran, Saudi Arabia; 2Indiana University School of Medicine, Indianapolis, IN, USA; 3Ministry of Health, 4Alfaisal University, Riyadh, Saudi Arabia

Correspondence: Ziad A Memish Ministry of Health, College of Medicine, Alfaisal University, PO Box 54146, Riyadh, 11514, Saudi Arabia Tel +966 505 483 515 email [email protected]

Abstract: The emergence of Middle East respiratory syndrome coronavirus (MERS-CoV) infection in 2012 resulted in an increased concern of the spread of the infection globally.

MERS-CoV infection had previously caused multiple health-care-associated outbreaks and

resulted in transmission of the virus within families. Community onset MERS-CoV cases con-

tinue to occur. Dromedary camels are currently the most likely animal to be linked to human

MERS-CoV cases. Serologic tests showed significant infection in adult camels compared to

juvenile camels. The control of MERS-CoV infection relies on prompt identification of cases

within health care facilities, with institutions applying appropriate infection control measures.

In addition, determining the exact route of transmission from camels to humans would further

add to the control measures of MERS-CoV infection.

Keywords: MERS, Middle East respiratory syndrome coronavirus, epidemiology, control measures, transmission, Saudi Arabia

Introduction Middle East respiratory syndrome coronavirus (MERS-CoV) was initially identi-

fied from a 60-year-old Saudi man who was admitted to a private hospital in Jeddah

(Figure 1) on June 13, 2012, with history of fever, cough, expectoration, and shortness

of breath.1 He subsequently died 11 days later from progressive respiratory failure.1

A sputum sample tested negative for common respiratory viruses (influenza A and B

viruses, parainfluenza virus types 1 to 3, respiratory syncytial virus, and adenovirus).

Inoculation of sputum in LLC-MK2 and Vero cells resulted in viral cytopathic changes.1

The virus was later identified as a new coronavirus and called Human Coronavirus Eras-

mus Medical Center (HCoV-EMC).1 A subsequent patient from Qatar, a 49- year-old

man, was diagnosed in September 2012 with the novel coronavirus (MERS-CoV) and

he was transported to the United Kingdom for intensive care.2 The isolated viruses

from the Saudi and the Qatari cases were 99.5% identical.2 Subsequently, the virus

was designated as MERS-CoV instead of HCoV-EMC according to the Coronavirus

Study Group.3 Retrospective analysis of stored samples from an outbreak in Zarqa,

Jordan of a cluster of hospital cases of severe respiratory illness dating back to April

2012 confirmed MERS-CoV as the cause of the outbreak.4 Since the initial description

and as of July 14, 2014, a total of 834 laboratory-confirmed cases of infection with

MERS-CoV including 288 (34.5%) deaths were reported to the World Health Orga-

nization (WHO).5 In this review, we highlight the epidemiology and disease control

measures of MERS-CoV. We reviewed the available literature from the beginning of

June 2012 to June 2014 utilizing PubMed and Google Scholar.

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Epidemiology The knowledge about the epidemiology of MERS-CoV

was expanded after exploring the large hospital outbreak

in Al-Hasa, Saudi Arabia.6 The initial occurrence of

MERS-CoV was thought to have particular predominance

for male patients and those with comorbid diseases.6–8

The male-to-female ratio was between 2.8:1 to 3.3:1.6,7

This male predominance might have been related to the

nature of the outbreak. Initial cases were reported among

elderly patients with a median age of 56 years. A sum-

mary of demographics of major MERS-CoV studies

is shown in Table 1.6,7,9–12 During the second quarter

of 2014 (April–May) there was an unusual increase in

the number of reported cases from Saudi Arabia. From

April 11 to June 9, 2014, a total of 515 cases of MERS-

CoV were reported to WHO.11 A total of 113 cases were

reported on June 2, 2014 retrospectively to WHO. These

cases are summarized in Table 1. Of the initial cases,

there were eleven cases of childhood MERS-CoV and all

but two of the cases were asymptomatic.13

Change of MERS-CoV case demography over time Early in the course of MERS-CoV, the initial cases were more

common in males than females and later the male-to-female

ratio was less pronounced. The initial predominance of male

cases may be due to the characteristics of the outbreak in Al-

Hasa (Figure 1).6 As more cases were identified, this predomi-

nance was lost and a more balanced sex distribution started to

reflect the true distribution of the cases. In an initial analysis of

the first 179 cases, there were some differences between primary

(sporadic and index cases) and secondary cases.14 Primary cases

were more likely to be male (80% versus 58%), and to be older

(median age: 58 years versus 48 years). Health care workers

constituted 35% of secondary cases versus 3% of the primary

cases.14 When comparing the Al-Hasa outbreak in 2013 with

the most recent cases in April–May 2014, the Al-Hasa cases

were older in age (56 years versus 46 years), there were more

male cases (male-to-female ratio 2.8:1 versus 1.4:1), there were

more severe cases (100% versus 44.5%), and there was a higher

mortality rate (65% versus 28.3%) (Table 1).6,7,9–12

Seasonality pattern of MERS-CoV The occurrence of the majority of cases seems to follow

a seasonal distribution: April 2012 (Zarqa public health

hospital, Jordan),4 April–May 2013 (Al-Hasa outbreak),6

and April–May 2014 (Jeddah and United Arab Emirates

outbreak).14 The occurrence of the cases in the spring raises

the possibility of seasonal cycles of MERS-CoV, as was sug-

gested.15 This notion is further substantiated by the fact that

camels give birth in March (spring) and that MERS-CoV is

more common in adult camels (2 years old) than young

camels (Table 2).6,7,9–12,16–19 The difference in the positivity rate

was not statistically significant in three studies.16–19

Asymptomatic cases The initial cases of MERS-CoV were detected among patients

admitted with severe community-acquired pneumonia and the

Table 1 A summary of demographics of major MeRS-Cov studies

Number of cases

Median age (range) years

Male-to- female ratio

Percentage asymptomatic

Percentage severe cases

Case fatality rate (%)

Reference

23 56 (24–94) 2.8:1 0 100 65 6 47 NA 3.3:1 0 100 60 7 133 NA 1.5:1 13.5 86.5 45 9 161 50 (14–94) 1.8:1 11.1 63.4 – 10 402 46 (0.75–94) 1.4:1 28.6 44.5 28.3 11 113 41 (0.25–89) 1.3:1 28.9 NA 30 12

Abbreviations: MeRS-Cov, Middle east respiratory syndrome coronavirus; NA, not available.

Figure 1 A map of the Kingdom of Saudi Arabia showing the main cities described in this paper: Riyadh (the capital); Al-Hasa (2013 outbreak); Jeddah (2014 outbreak); Hafr Al-Batin (community cluster); and the holy Cities (Makkah and Madinah).

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MeRS-Cov epidemiology and disease control measures

majority of them required intensive care unit admission.6,7

Subsequently, individuals with mild or no symptoms were

reported. Contact investigation of cases of MERS-CoV resulted

in the identification of asymptomatic cases (Table 1).6,7,9–12 The

rate of positivity of contacts by polymerase chain reaction was

0%–15.4%.4,20–23 The largest screening came from Saudi Arabia

and the rate of positivity among health care workers and family

contacts was 1.12% and 3.6%, respectively.20

Transmission Understanding the epidemiology and transmission of

MERS-CoV requires the classif ications of cases into:

sporadic (community-onset), intra-familial transmission,

and health-care-related transmission. The WHO MERS-CoV

Research Group defined sporadic and index cases as meeting

one of the following criteria: no history of contact with other

MERS-CoV cases, occurring in an area with no previous

cases within the last 2 months, or the first or index case in

a cluster.10

Sporadic: animal to human transmission Of all the cases reported to WHO, only 25% of the cases are

considered as primary cases.24 The acquisition of MERS-CoV

in these sporadic cases could be from animal contact. The

data suggest that camels are the likely source of MERS-CoV.

Previous studies showed a high rate of positive serology

in dromedary camels in multiple countries including: the

Kingdom of Saudi Arabia (KSA), Oman, Canary Islands,

Egypt, Qatar, the United Arab Emirates, Jordan, and African

countries.17,18,25–33 A summary of the number of tested camels

and the percentage rates are shown in Figure 2.

A stronger evidence of the connection comes from the

detection of MERS-CoV by polymerase chain reaction from

camels from Jeddah, KSA,34,35 and in Qatar.25 The presence

of a few genomic variants of MERS-CoV in dromedary

camels suggests the transmission of MERS-CoV from

camels to humans.36 The route of transmission of MERS-

CoV from camels to humans remains to be identif ied.

Table 2 A summary of the serology results of juvenile and adult (2 years old) camels in different studies

Juvenile Adult P-value Country Reference

Total tested Percent positive Total tested Percent positive

65 72 245 95 0.0001 Saudi Arabia 16 8 13 97 14 1.0 Spain 17 31 93 157 97 0.325 ethiopia 18 46 30 158 54 0.007 Tunisia 18 104 55 98 95 0.0001 Saudi Arabia 19 21 76 23 91 0.237 Saudi Arabia 19 56 72 26 92 0.04 Saudi Arabia 19

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Figure 2 A graph showing the total number of tested camels and the percentage positive. Note: x-axis shows the country of testing (reference number). Abbreviation: UAe, United Arab emirates.

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Al-Tawfiq and Memish

Camels’ milk may play a role as MERS-CoV was detected

in 41.7% of 12 tested camel milk samples which were col-

lected according to the custom of the people in the region.37

Whether there was a contamination during the process of

milk collection or not is not known. There was variation in

the number of cases that reported camel contact, with the

highest proportion of contact coming from Oman and the

United Arab Emirates.38 Since not all cases have contact with

camels, another source may exist.

People working with camels such as farm workers,

slaughterhouse workers, and veterinarians may be at higher

risk of MERS-CoV infection than other people.39 Goats,

cows, sheep, water buffalo, and birds were negative for

antibodies to MERS-CoV.16,31,39 Thus, so far no other animal

link has been identified apart from camels and bats.40,41

Community outbreaks (intra-familial) Community outbreaks of MERS-CoV have been limited

to intra-familial transmission. In an initial report of a fam-

ily cluster, 28 individuals lived in an extended household

and four of them tested positive for MERS-CoV, including

the index case.42 The secondary attack rate in this cluster

was 11%.43 In a second family cluster, two brothers tested

positive for MERS-CoV from eight contacts of an index

case42 with an attack rate of 13%.43,44

In a third community cluster occurring in an extended

family in Hafr Al-Batin (Figure 1), an index case was closely

associated with five additional MERS-CoV cases and one

of the secondary contacts was associated with another four

cases.45 The secondary attack rate was 19.4%.45 However,

the calculated rate of secondary transmissions among fam-

ily contacts was 3.03% in a large screening of 462 family

members.19 Intra-familial transmission of MERS-CoV is

thought to be secondary to person-to-person transmission and

is limited to close contacts.43 The presence of another source

of infection among family contacts could not be excluded

as phylogenetic analysis of the Hafr Al-Batin cluster showed

that two of the infected contacts could not have been directly

infected from the index patient.45 Being a member of the

same family may result in exposure to the same unknown

source of infection.

Health-care-associated transmission It is known that a large proportion of MERS-CoV cases

occurred in the health care setting. The first identified hospital

outbreak was in Zarqa, Jordan.4 This outbreak was identified

retrospectively after the identification of the first MERS-CoV

case in Jeddah, Saudi Arabia. The Zarqa outbreak involved

eleven patients and eight of them were health care workers.4

MERS-CoV was retrospectively confirmed in two patients.4

Further analysis showed that nine (7.2%) of 124 contacts in

this outbreak were positive by serology.46

The Al-Hasa outbreak in 2013 provided valuable infor-

mation about MERS-CoV transmission in the health care

setting.6 The outbreak initially started in a hemodialysis unit

in a private hospital in Al-Hasa and subsequently involved

an additional three hospitals.6 The transmission was thought

to be person-to-person in 21 of 23 cases and occurred in the

hemodialysis unit, the intensive care unit, and/or the in-patient

units.6 The transmission was secondary to droplet as well as

direct or indirect contact. Further phylogenetic analysis of

this outbreak showed that only eight of the 13 epidemiologic

transmissions were related, suggesting multiple introduc-

tions of MERS-CoV in that outbreak.47 The most recent

health care transmission occurred in Jeddah, Saudi Arabia in

April–May 2014. There was no change in the virus transmis-

sion or mutation.48 Near full genome sequence analyses of

three viruses from the early phase of the Jeddah outbreak were

highly similar but not identical, with no genome insertions

or deletions.48 Most of the human-to-human infections were

in the health care setting and 25% of all cases were health

care workers.49 In April 2014, another health-care-associated

cluster was reported from Al-Ain, United Arab Emirates

and resulted in infection of 16 health care workers of the

23 total cases.50 The recent increase in the number of cases

of MERS-CoV in April–May 2014 showed that 75% of the

cases were secondary cases and that most of these cases were

health care workers who acquired the infection in the health

care setting.24 In the most recent outbreak in Saudi Arabia,

of the 402 cases reported in June 2014, at least 25% were

health care workers.11 One study showed that health care

workers who contracted MERS-CoV were involved in aerosol

generating procedures such as intubation, airway suctioning,

and sputum induction.49–51

Travel related With the emergence of MERS, there was a great concern for

the possible transmission of MERS-CoV during travel and

during the annual Pilgrimage. A number of sporadic cases

were reported in different countries where these cases origi-

nated in that area. Travel-associated infection was reported in

Greece, Jordan, Malaysia, and the Philippines;24 the United

Kingdom, France, Tunisia, Italy, Egypt, the United States, and

the Netherlands.52–57 Only limited human-to-human transmis-

sion of travel-related cases was reported in France and the

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MeRS-Cov epidemiology and disease control measures

United Kingdom.21,22 The annual Hajj in 2012 and 2013 was

not associated with any MERS-CoV cases.58–61

MERS-CoV disease control measures Understanding the route of transmission of MERS-CoV and

the pattern of transmission of the disease is important for

control and prevention. Currently, as mentioned above, the

pattern of the disease transmission will dictate the methods

for prevention. Sporadic cases are thought to be secondary to

animal exposure, mostly related to camels. The WHO advises

people at risk of acquiring MERS-CoV to avoid contact with

camels, to practice good hand hygiene, and to avoid drinking

raw milk or eating contaminated food unless it is properly

washed, peeled, or cooked.24

Since most of the cases occur in the health care setting,

it is prudent that all health care workers practice appropriate

infection control measures when taking care of patients with

suspected or confirmed MERS-CoV. Specifically, health

care workers should apply standard precautions consistently

with all patients.24 The application of droplet precautions are

needed when providing care to patients with symptoms of

acute respiratory infection.5 The addition of contact precau-

tions and eye protection is required when caring for suspected

or confirmed MERS-CoV infection.5 During aerosol generat-

ing procedures, airborne infection isolation precautions should

be applied.5 The United States Centers for Disease Control

and Prevention continues to recommend the use of airborne

infection isolation precautions with all patients.62,63

As far as travel is concerned, WHO does not restrict travel

to countries in the Middle East with cases of MERS-CoV.24

For the Hajj and Umrah, the Saudi Ministry of Health recom-

mended that people at increased risk of MERS-CoV infection

and its complications should postpone their Hajj. These people

include: certain age groups (,12 years, and $65 years), indi-

viduals with chronic diseases (heart disease, kidney disease,

respiratory disease, and diabetes), and those with immune

deficiency, malignancy, terminal illnesses, or pregnancy.64

Conclusion The epidemiology and the transmission pattern of MERS-CoV

to date indicate that the majority of cases occur in the health

care setting. Strengthening the infection control measures in

the health care setting is of great importance. Since about 25%

of cases are community based, there is a real need to further

prevent the animal-to-human transmission of MERS-CoV.

It is also important to further delineate the transmission routes

and the presence of any other animal or intermediate hosts.

Disclosure The authors report no conflicts of interest in this work.

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