2014 The pattern of Middle East respiratory syndrome coronavirus in Saudi Arabia_ a descriptive epidemiological analysis

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The pattern of Middle east respiratory
8 syndrome coronavirus in saudi arabia:
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v-
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N a descriptive epidemiological analysis
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3 of data from the saudi Ministry of health
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pre Ibrahim G alghamdi1,2 Purpose: This study describes the epidemiology of Middle East respiratory syndrome
e
v Issam I hussain1 coronavirus (MERS-CoV) in Saudi Arabia.
o
w.dnly. shaia s almalki2 Patients and methods: Epidemiological analysis was performed on data from all MERS-
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om https://wersonal use MMMoaonhhsaaommuemrd eM ds aaal lggehhl-aasmmheddeii4m3 y5 CTrehogeVio f ncre.a qTseuhsee nr aecvcyeo orradfg eceda msbeyos ntahtnhedl yS d ateeuamdthip sMe rwianatuiss rtcera yal cnoudfl ahHtueemdal itadhni tdby ea otdwfj ueinesftnee dcJut ebndye rm6e,go 2ino0tnh1s,3 st haenrxod, u aMggheao ygu r1to 4tuh, pe2, 0y a1ena4dr.
ded frFor p 1University of lincoln, Brayford wReass uallstos: cAal ctuoltaatle odf. 425 cases were recorded over the study period. The highest number of
a Pool, lincoln, UK; 2University of
nlo al-Baha, 3General Directorate of cases and deaths occurred between April and May 2014. Disease occurrence among men
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o health affairs, Ministry of health, (260 cases [62%]) was higher than in women (162 cases [38%]), and the case fatality rate
d
ne al-Baha, Kingdom of saudi arabia; was higher for men (52%) than for women (23%). In addition, those in the 45–59 years
ci 4King Fahad specialist hospital,
edi Dammam, Kingdom of saudi arabia; and 60 years age groups were most likely to be infected, and the case fatality rate for these
eral M 5hroesspeiatracl,h U annidte Dd elvienlcooplmnsehnirte, lincoln pine oRpilyea wdha s( 1h6ig9h cear sthesa;n 4 f3o rd oetahtehrs )g,r fooulplosw. Tehde b hyi gJheedsdta nhu (m1b5e6r coafs ceas;s e3s6 a dneda dtheas)th asn wd etrhee r eEpaosrteterdn
n hospitals national health service
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G Trust, lincoln, UK Region (24 cases; 22 deaths). The highest case fatality rate was in the Eastern Region (92%),
of
al followed by Medinah (36%) and Najran (33%). MERS-CoV infection actively causes disease
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ur in environments with low relative humidity (20%) and high temperature (15°C–35°C).
o
al J Conclusion: MERS-CoV is considered an epidemic in Saudi Arabia. The frequency of cases
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o and deaths is higher among men than women, and those above 45 years of age are most affected.
ati
n Low relative humidity and high temperature can enhance the spread of this disease in the entire
er
nt population. Further analytical studies are required to determine the source and mode of infection
I
in Saudi Arabia.
Keywords: Middle East respiratory syndrome, case fatality rate, descriptive epidemiology,
temperature, humidity
Introduction
Middle East respiratory syndrome coronavirus (MERS-CoV) is considered to be a
new viral epidemic, and the infection is associated with acute respiratory illness and
renal failure.1,2 In September 2012, this coronavirus was discovered and isolated from
an infected patient living in Saudi Arabia.1 The geographic distribution of cases has
correspondence: Ibrahim G alghamdi
been mainly confined to six countries in the Arabian Peninsula (Saudi Arabia, United
University of lincoln, school of life
sciences, Brayford Pool, lincoln, Arab Emirates, Qatar, Kuwait, Jordan, and Oman). However, in some countries in
ln6 7Ts, UK Europe and Africa, instances of the disease have been detected in imported cases from
Tel [phone]
email [email protected] endemic countries.3
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MERS-CoV has a very high mortality rate, and the primary objective of defining the burden of this disease
complications arising from infection can result in severe in Saudi Arabia. Currently, there are limited data in these
respiratory and renal failure.4 The mode of transmission reports, although each contains the number of cases diag-
and the source of MERS-CoV infection (ie, whether it is a nosed, the number of deaths confirmed, the sex of the patients,
zoonotic or human disease) is unclear.4 Recent research has and the region inhabited by the infected person.
shown that dromedaries may act as viral reservoirs, and anti- Data were analyzed using IBM SPSS for Windows, Version
8
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0 bodies against MERS-CoV have been found in dromedaries 20.0 (IBM Corp, Armonk, NY, USA). The frequency of cases of
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v-
o living in both the African and Arabian peninsulas.5,6 MERS-CoV infection and percentage of resulting deaths were
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14- Despite limited data on MERS-CoV in Saudi Arabia, we calculated and categorized by date of diagnosis, sex, age group,
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o have attempted to explore the epidemiological distribution and region. In addition, the case fatality rate (a measure of the
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2 of and describe the pattern of infection of this disease by severity of epidemic disease) was calculated and categorized by
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1 conducting a study of the reports of MERS-CoV published month, sex, age group, and region. The average relative humid-
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1 daily by the Saudi Ministry of Health.7 ity and temperature of the regions with the highest incidence
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y 2 of MERS-CoV in Saudi Arabia were calculated, to study the
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m/ Materials and methods geographical and temporal characteristics of this disease.
o
s.c An epidemiological study of all MERS-CoV cases recorded
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pre by the Saudi Ministry of Health between June 6, 2013 and Results
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ov May 14, 2014 was performed. As data are limited regarding A total of 425 MERS-CoV cases were recorded by the
w.dnly. MERS-CoV available from the Saudi Ministry of Health Saudi Ministry of Health between June 6, 2013 and May 14,
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om https://ersonal us wcoenbSfisiritnmec,e ewd Med icaaoygn nc2oe0sni1st3r, a,s teetxhd,e oa ngS ead ugisdreoia usMpe, i daninissdttr rirbyeug otiiofon nH. beya ldthat eh aosf 2fthr0oe1m 4ra . tJTeu hnwee e frureen qtoiulb esDnecreyvc eeodmf ibcnea rsJ eu2sn0 ea1 n3ad,n dda enSadet hpsstl eiwgmhabts e irinn c(c1roe7na sscieasstse einsnt;
ded frFor p published a daily report on MERS-CoV infections, with 11 deaths) (Figure 1A). In 2014, there was a low number of
a
o
nl
ow A 2013 B 2014
d
e 100 200
n
ci 90 180
edi 80 160
M 70 140
al cy 60 cy120
Gener quen 5400 quen10800
al of Fre 3200 Fre 6400
urn 10 20
Jo 0 0
al June July August SeptemberOctober NovemberDecember January February March April May
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o Month Month
ati Cases Deaths Cases Deaths
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er
Int C D Case fatality rate ×100
300 100
90
250
80
70
200
cy 60
n
e 150 % 50
u
q 40
Fre 100 30
20
50
10
0 0
Cases Deaths Male Female
Sex Sex
Male Female
Figure 1 Distribution off Mers-coV cases and deaths by date of diagnosis and sex in saudi arabia.
Notes: (A) The frequency of Mers-coV cases and deaths in saudi arabia, from June to December 2013. (B) The frequency of Mers-coV cases and deaths in saudi arabia,
from January to middle of May 2014. (C) The frequency of Mers-coV cases and deaths, adjusted by sex, in saudi arabia, from June 2013 to May 2014. (D) The case fatality
rate of Mers-coV disease, adjusted by sex, in saudi arabia.
Abbreviation: Mers-coV, Middle east respiratory syndrome coronavirus.
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cases and deaths in January, February, and March, but at the information about the temporal and environmental
beginning of April, there was a sharp increase, to 190 cases characteristics of this disease. Figure 3A shows that in
and 45 deaths (Figure 1B); the corresponding case fatality Riyadh, the average temperature ranged from 15°C–37°C
rate was 24% and 25% in April and May 2014, respectively in April and May 2014, the period with the highest rate of
(Table 1). cases and deaths. In contrast, the lowest average relative
Figure 1C shows the number of MERS-CoV cases and humidity values (between 8%–20%) occurred at this time
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0 deaths, categorized by sex. There were 260 cases (62%) (Figure 3A and B). Similarly, in Jeddah, the average tem-
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o among the male population and 162 cases (38%) among the perature ranged from 20°C–37°C in April and May 2014,
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14- female population. Furthermore, the number of deaths was and the average relative humidity was the lowest recoded for
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o higher among men (89 deaths [74%]) than among women the year, at 30%–35% (Figure 3C and D).
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2 (31 deaths [26%]), and the case fatality rate was higher among The average monthly temperature and relative humidity
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1 men (52%) than women (23%) (Figure 1D). were also calculated for the Eastern Region, to identify the
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1 The frequency of cases and deaths was further adjusted by environmental characteristics that contribute most to the
4.
y 2 age group. The defined age groups reported were 0–14, 15–29, spread of this disease among the population of Saudi Arabia.
b
m/ 30–44, 45–59, and 60 years. Those in the 60 years age group The average temperature in the Eastern Region ranged from
o
s.c were most frequently diagnosed with MERS-CoV infection, 17°C–37°C in April and May 2014, and the lowest average
s
pre followed by those aged 45–59 years (Figure 2A). In addition, relative humidity for the year (18%–30%) was recorded
e
ov the highest case fatality rate was recorded in the 45–59 years at this time (Figure 4A and B). Similarly, in Medinah, the
w.dnly. age group (55%), followed by those aged 60 years (45%). average temperature was between 17°C–38°C in April and
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ded frFor p by the region of Saudi Arabia, is presented in Figure 2C.
a The highest number of cases and deaths occurred in Riyadh Discussion
o
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w (169 cases; 43 deaths), followed by Jeddah (156 cases; MERS-CoV is a recent fatal epidemic that has drawn global
o
d
e 36 deaths) and the Eastern Region (24 cases; 22 deaths). attention. Our current study focuses on the epidemiological
n
dici However, the highest case fatality rate was recorded in the pattern of MERS-CoV infection in Saudi Arabia between
e
M Eastern Region (92%), followed by Medinah (36%) and June 6, 2013 and May 14, 2014. To the best of our knowledge,
al
er Najran (33%) (Table 3 and Figure 2D). this is the first study that describes the patterns and trends of
n
e
G The average monthly temperature and relative humidity MERS-CoV infection in Saudi Arabia.
of
al were calculated for the regions with the highest incidence Unfortunately, there are no data available for MERS-
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ur of MERS-CoV infection, and this provided significant CoV incidence between January and May 2013. Our results
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J
al
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o
ati
ern Table 1 case fatality rate in saudi arabia adjusted by date of diagnosis
nt
I Month Number of cases Number of deaths Case fatality rate ×100
Male Female Total Male Female Total Number of deaths/ %
total number of cases
June 2013 12 5 17 8 3 11 11/17 64
July 5 7 12 5 0 5 5/12 41
august 4 3 7 2 0 2 2/7 29
september 7 10 17 5 3 8 8/17 47
October 7 3 10 2 1 3 3/10 30
november 4 1 5 1 2 3 3/5 60
December 7 1 11 2 0 2 2/11 18
January 2014 2 0 2 2 0 2 2/2 100
February 4 1 5 2 0 2 2/5 40
March 13 2 15 3 0 3 3/15 20
april 131 59 190 35 10 45 45/190 24
May 64 70 134 22 12 34 34/134 25
Total 260 162 425 89 31 120 120/425 28
% 62% 38% 100% 74% 26% 100%
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A B Case fatality rate ×100
160 100
140 90
80
120
70
y
nc 100 60
ue 80 % 50
18 eq 60 40
20 Fr 30
ov- 40 20
N 20
4- 10
n 1 0 0
o 0–14 15–29 30–44 45–59 ≥60 0–14 15–29 30–44 45–59 ≥60
3
24 Cases Deaths Age group Age group
6.
0
1
0.
15 C D Case fatality rate ×100
4.
by 2 116800 19000
om/ cy 112400 8700
ess.c quen 10800 % 654000
vepr Fre 6400 3200
o 20 10
m https://www.dsonal use only. Easter0n Region RiyadhJeddah MakkahMediRnaehgioJonuf Taif Asir Najran NoTrtahbeurkn Region Eastern0 Region RiyadhJeddah MakkahMedinah ReJogufionTaif Asir NajranNorTtahberukn Region
oer
ded frFor p Cases Deaths
a Figure 2 Distribution off Mers-coV cases and deaths by age group and region in saudi arabia.
o
nl Notes: (A) The frequency of Mers-coV cases and deaths, adjusted by age group, in saudi arabia. (B) The case fatality rate of Mers-coV disease, adjusted by age group,
w
o in saudi arabia. (C) The frequency of Mers-coV cases and deaths, adjusted by region, in saudi arabia. (D) The case fatality rate of Mers-coV disease, adjusted by region,
d
e in saudi arabia.
cin Abbreviation: Mers-coV, Middle east respiratory syndrome coronavirus.
di
e
M
al
er indicate that the number of MERS-CoV cases and deaths between December and March.8 However, the highest rates of
n
Ge remained inconsistent from the beginning of June to the MERS-CoV cases and deaths were not observed in Winter,
al of end of December 2013 and that MERS-CoV incidence but in mid-Spring, between April and May.
n
ur peaked twice, in June and September 2013. MERS-CoV In this study, we observed a higher rate of MERS-CoV
o
al J incidence was very low in the months of January, Febru- incidence and deaths in men than in women. A recent study
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o ary, and March 2014; however, incidence was observed and suggests that there is also a higher incidence of influenza in
ati
ern then peaked at the end of April. Therefore, we expected that men than in women, which is due to a higher level of tes-
nt
I MERS-CoV incidence would continue to increase until the tosterone and a corresponding suppression of their immune
end of June 2014. Saudi Arabia is in the Northern hemisphere, response.9 Thus, a similar relationship may exist with MERS-
where the incidence of influenza is highest in winter, peaking CoV, and consequently, men with a lower level of testosterone
Table 2 case fatality rate in saudi arabia adjusted by age group
Age group, Number of cases Number of deaths Case fatality rate ×100
years
Male Female Total Male Female Total Number of deaths/ %
total number of cases
0–14 11 2 13 2 0 2 2/11 18
15–29 30 34 64 9 1 10 10/54 18.5
30–44 62 44 106 7 1 8 8/98 8
45–59 68 39 107 28 10 38 38/69 55
60 89 46 135 43 19 42 42/93 45
Total 260 165 425 89 31 120 120/305 39
Notes: case fatality rate for males: 89/171 ×100=52%; case fatality rate for females: 31/134 ×100=23%.
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Table 3 case fatality rate in saudi arabia adjusted by region
Region Number of cases Number of deaths Case fatality rate
Male Female Total Male Female Total Number of deaths/ %
total number of cases
eastern region 14 10 24 15 7 22 22/24 92
riyadh 91 78 169 32 11 43 43/169 25
8 Jeddah 105 51 156 27 9 36 36/156 23
1
20 Makkah 12 13 25 4 2 6 6/25 24
ov- Medinah 17 5 22 6 2 8 8/22 36
N
4- Jouf 1 1 2 0 0 0 2/2 0
1
n Taif 4 1 5 1 0 1 1/5 20
o
3 asir 5 2 7 1 0 1 1/7 14
4
6.2 najran 3 0 3 1 0 1 1/1 33
10 Tabuk 7 4 11 1 0 1 1/11 9
50. northern region 1 0 1 0 0 0 1/0 0
1
4. Total 260 162 425 89 31 120 120/425 28
2
y
b
m/
o
s.c may have improved immunity to viral infection.9 Another over 65 years of age and younger people with chronic diseases
s
e
pr possible explanation for a higher incidence of MERS-CoV are at a greater risk of complications resulting from influenza
e
ov among men is that men are likely to spend more time out- or viral infections than are healthy adults. This indicates that
w.dnly. doors and thus have a higher risk of exposure to a source of older and unhealthy younger people are more likely to become
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om https://ersonal us i4n5f–eO5c9tui oyr enfia.rnsd ainndg s i6n0d yiceaatres htahda tt hteh hoisgeh einst trhatee oagf Me gErRoSu-pCso oVf iannfdeO cintuefrde cswttiuiotdhny Mi sa EmlsRooS rer-e ClpiokoVerl,ty so wttohi anbtge ttfhoae taa rlw eigneia otkhn ei msoefm gRuroniyueap sdsy.h1s0 tehmad,
ded frFor p cases and related deaths. It has been documented that people the highest rate of MERS-CoV infections and deaths in
a
o
nl
w
o
e d A Average temperature in Riyadh B Average relative humidity in Riyadh
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ci
di 50 80
e
al M 4450 70
ner e35 60
Ge ad30 50
of gr25 %40
al nti20 30
urn Ce15 20
o 10
al J 5 10
n 0 0
o
ati Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
n
er Month Month
Int Low High Low High
C Average temperature in Jeddah D Average relative humidity in Jeddah
50 100
45 90
40 80
35 70
de30 60
ra25 % 50
entig2105 4300
C10 20
5 10
0 0
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
Month Month
Low High Low High
Figure 3 The impact of temperature and relative humidity on Mers-coV cases in different regions of saudi arabia.
Notes: (A) low and high average monthly temperature in riyadh. (B) low and high average monthly relative humidity in riyadh. (C) low and high average monthly
temperature in Jeddah. (D) low and high average monthly relative humidity in Jeddah.
Abbreviation: Mers-coV, Middle east respiratory syndrome coronavirus.
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A Average temperature in Eastern region B Average relative humidity in Eastern region
50 100
45 90
40 80
e 35 70
ad 30 60
gr 25 % 50
nti 20 40
18 Ce 15 30
20 10 20
v- 5 10
o
N 0 0
4- Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
1
n Month Month
o
3 Low High Low High
4
2
6.
0
1
0.
15 C Average temperature in Medinah D Average relative humidity in Medinah
4.
y 2 50 100
b 45 90
m/ 40 80
s.co de 3350 6700
vepres ntigra 2250 % 4500
o e 15 30
w.dnly. C 10 20
wo 5 10
om https://wersonal use 0 Jan LFoewb Mar HAigphr May JMunontJhul Aug Sep Oct Nov Dec 0 Jan LFoewb Mar HAigphr May JMunonJthul Aug Sep Oct Nov Dec
aded frFor p FNioguterse: 4(A T)h leo iwm paancdt hoifg hte amvepreargaetu mreo nanthdl yr etelamtivpee rhautumried iitny eoans tMerenr rs-ecgiooVn . c(aBse) sl oinw d aifnfedr ehnigth r eavgeiornags eo mf soanutdhil ya rrealbaitai.ve humidity in eastern region. (C) low and high average
nlo monthly temperature in Medinah. (D) low and high average monthly relative humidity in Medinah.
w Abbreviation: Mers-coV, Middle east respiratory syndrome coronavirus.
o
d
e
n
dici Saudi Arabia, followed by Jeddah and the Eastern Region. observed that higher relative humidity levels above 43% may
e
M However, despite the high number of cases and deaths in decrease the activity of influenza virus particles to 14%, while
al
er Riyadh and Jeddah, the case fatality rate was highest in the a relative humidity of 23% or less may increase the activity
n
e
G Eastern Region, and for this reason, MERS-CoV was first of influenza virus particles from 70%–77%.15 The source
of
al discovered here. In Jeddah and Mecca, there is concern about of infection should also be investigated and identified with
n
ur the increase of MERS-CoV cases because hundreds of thou- epidemiological surveillance, either passively or actively, in
o
J
al sands of people frequently travel to Saudi Arabia to perform order to control MERS-CoV in Saudi Arabia.
n
o
ati Umrah and Hajj. Although no Hajj-associated MERS-CoV
n
er cases have been reported, Umrah-associated cases have.11–13 Conclusion
nt
I Therefore, the World Health Organization suggests that Epidemiological analysis of the daily reports of MERS-CoV
governments should provide advice on the risk of infection incidence by the Saudi Ministry of Health, between June 6,
to pilgrims with major medical problems, such as chronic 2013 and May 14, 2014, revealed that the recent epidemic
diseases. In addition, general travel health information should of MERS-CoV has a high fatality rates and may spread
be provided, including advice on food safety practices, good from person to person. The rates of MERS-CoV cases and
personal hygiene, and avoiding unnecessary farm visits and deaths are higher in men than in women, and those in the age
contact with animals.14 groups of 45–59 and 60 years had the highest case fatality
We have observed that MERS-CoV incidence rates are rate. Furthermore, Riyadh, Jeddah, and the Eastern Region
higher in environments with low relative humidity (20%) had the highest number of cases and related deaths in Saudi
and high temperatures (20°C–35°C). Therefore, increasing Arabia. MERS-CoV is most active in environments with low
relative humidity to above 35% and maintaining tempera- relative humidity and high temperatures. However, further
tures ranging 5°C–15°C in hospitals and indoor places may epidemiological studies are required to determine the source
decrease the spread of this disease. However, it has been and the mode of MERS-CoV infection in Saudi Arabia.
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Disclosure 9. Furman D, Hejblum BP, Simon N, et al. Systems analysis of sex
differences reveals an immunosuppressive role for testosterone in
The authors report no conflicts of interest in this work.
the response to influenza vaccination. Proc Natl Acad Sci U S A.
2014;111(2):869–874.
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