Sustained Emergence of Influenza A H1N1 and epidemiologic aspects of H1N1 in Saudi Arabia
Rana Almaghrabi*, Amal Yosof Aidaroos, Moudi Alsoghier, Abdulrahman Nasser Alodyani, Fayza Amer Alnahdi, Wedyan Hussein
Hasawi, Nourah Alkhazi , Sameera Mohamed Aljohani, Abdulrhman Mohamed Alnemri.
Background: In April 2009, an emergent strain of influenza A virus has been discovered and known as H1N1. Since the descriptive
epidemiology report for the first reported 100 cases of this virus in Saudi Arabia in 2010, there are paucity of similar reports.
Objectives: This study aimed to describe some epidemiologic aspects of this emergent disease among all lobaratory confirmed cases
in Riyadh, Saudi Arabia from Feb., 2014 to Dec., 2015.
Methods: A total of 107 influenza A H1N1 laboratory confirmed cases reported at Prince Sultan Miltary Medical City in Riyadh, Saudi
Arabia were investigated based on their personal characteristics (age, sex, nationality, clinical presentation and associated medical
condition), case fatality, and time distribution. The data was obtained form the medical files of the studied cases during the period from
Feb., 2014 to Dec., 2015. The data of the cases were analysed by appropriate statistical methods.
Results: H1N1 infection was more among male Saudi subjects as most of the reported cases were male (60.8%). The reported cases
were more among those aged ≥ 60 years (28%) and those aged from 30-< 45 years (26.2%). Of the reported 107, 21 cases (19.6%) were
reported in March 2015. The overall case fatility rate was 10.3% and it was high among cases less than 15 years (21.4%) and those aged
age ≥ 60 years (20.0). The risk factors associated with increased case fatality were cases admitted to ICU (OR= 4.2; 95% CI= 1.14-15.3),
those aged ≥ 60 years (OR=3.6; 95% CI= 1.10-12.8), and associated co-morbidities (OR= 3.3; 95% CI= 1.02-12.90). Male sex, however,
was associated with a low risk of mortality (OR= 0.75; 95% CI= 0.23-15.3).
Conclusions: Influeza A H1N1 infection in Saudi Arabia is still a threat with a reported high fataility rate of 10.3%. Because not much data are available regarding this disease in recent years, it has become a growing concern to enhance the Saudi surveillence system for
this virus, especially during Hajj and Umrah seasons. National researches on large scale are also needed for a better understanding of
epidemiology of this infection.
Epidemiology, Fatality, H1N1, Influenza A, Saudi Arabia.
In April 2009, a new strain of Influenza virus A H1N1, commonly
referred to as “swine flu,” began to spread in several countries
around the world. The recent H1N1 virus strain has been found
to be closely related to the swine flu virus, but with a genetic
composition that is quite different from the earlier known isolates
(1,2). In late April, the WHO declared a “public health emergency
of international concern” under the rules of the WHO's new
International Health Regulations when the first few cases of the
pandemic influenza A (H1N1) virus were reported in the United
States (3,4). As of late June, the WHO reported that pandemic
influenza A (H1N1) had been confirmed in almost 60,000 people
in more than 100 countries, and 263 deaths were confirmed to have
been caused by the disease. On June 11, 2009, the WHO raised the
pandemic alert level to phase 6 (indicating a global pandemic).
By December 2009, more than 208 countries and territories had
reported swine flu cases (5).
Symptoms of the 2009 “swine flu” pandemic influenza A (H1N1)
virus in humans are similar to those of seasonal influenza and of
influenza-like illness in general. They include fever, cough, sore throat, body aches, headache, chills, and fatigue. However, the
2009 outbreak has shown an increased percentage of patients reporting diarrhea and vomiting (6).
According to the Saudi Ministry of Health, the number of laboratoryconfirmed
cases in Saudi Arabia as of December 30, 2009 was
15850, with 124 deaths. Since the descriptive epidemiology report
for the first reported 100 cases of this virus in Saudi Arabia in 2010
(7). there were very limited studies relating to Influenza A H1N1
and its epidemiology in the Saudi situation, this study aimed to
describe some epidemiologic aspects of Influenza A H1N1 among
the reported cases at the Prince Sultan Medical City, Riyadh, Saudi
Arabia during the period from February 2014 to December 2015.
This study analyzed data for 107 influenza A H1N1 laboratory
confirmed cases collected by Prince Sultan Miltary Medical
City in Riyad city, Saudi Arabia from the February 1st, 2014 to
December 31, 2015. Information such as age, sex, nationality,
date of onset, clinical presentation, associated medical condition,
patients’ admission to ICU, duration of stay in ICU, and outcome were collected.
Descriptive epidemiology was performed on collected data to
describe the characteristics of the studied cases, to depict the
epidemic curve (number of cases vs. time of diagnosis) and to
assess the case fatality rate among the studied cases by their age
group. Age specific mortality rate was also estimated according to
2010 Saudi Census (8).
The statistical analysis was performed using statical analysis system
(SAS) software package (9). Categorical variables were presented
as frequencies and percentages while continuous variables were
presented as mean and standard deviation. The mean length of
stay in ICU was compared between cases with associated medical
condition and those without associated medical condition. The
level of statistical significance was set at P ≤ 0.05.
A univariate logistic regression analysis was also done to examine
factors that are associated with mortality where odds Ratio (OR)
and its 95% confidence interval (CI) were used.
The total reported cases during the study period were 107 cases.
In context to nationality, 105 cases were Saudi districts while only
two individuals were non-native. Most reported cases were male
(60.8%), aged ≥ 60 years years (28%), and those aged from 30 to
45 years (26.2%). The majority of cases were diagnosed in winter
and spring seasons; where 58% diagnosed in spring and 21.5% in
summer season. Fever and flu symptoms were the main clinical
presention in 100 cases (93.5%); while faver and gastrointinal
manifestations (vomiting and diarrhoea) were observed in only
7 patients (6.5%). Nearly half of the cases were associated
with medical problems where 16.8% were diabetic, 14% were
hypertensive with or without IHD, 3.7% with renal problems,
7.5% with asthma, 19% with HCV, and there were three pregnant
Table 1: Characteristics of Laboratory-Confirmed H1N1 cases,
Riyadh, saudi Arabia from Jan., 2014 to Dec., 2015 (n=107)
Figure.1 Epidemic Curve to demonstrate cases of H1N1 by month
(based on date of onset), Riyadh, KSA from Feb., 2014-Dec., 2015
(Total: 107 cases)
Figure 1 showed that H1N1 spread among 21 patients in March
2015, recorded as highest prevalence throughout. However, the
figure reduced to 3 patients a month later. The high-low fluctuations
have been witnessed since March 2014 untill June 2014,
and since Feberuary 2015 until August 2015, which demonstrate a
declining trend in the summer season.
Of the studied 107 cases, 21 cases were admitted to ICU. Of those admitted cases, more than half (n= 12) were associated with medical
problems, but with statistical significant difference between them and those cases without associated medical problems. The mean length
of stay was 10 ± 3.5 days and it showed significant differences between those with associated medical problems and cases without associated
medical problems (Table 2).
Table3: Cumulative number of cases and case fatality rate of Laboratory-Confirmed H1N1 cases by years, Riyadh, Saudi Arabia
Table 3 showed the cumulative number of cases and their fatality rates during the study years. The year 2014 and 2015 reported 107
cases of H1N1, and 11 (10.3%) deaths. The year 2015, however, recorded the higher cumulative number of cases with reported 59 cases,
but with the lower death rate (8.5%).
Table 4: Case Fatality Rate and Age specific Mortality Rate of Laboratory-confirmed cases of H1N1, Riyadh, Saudi Arabia from
Feb., 2014– Dec., 2015 (n= 107 cases)
Table 4 presented the case fatility rate by age distribution. The overall case fatilty rate among the studied 107 cases was 10.3%. The
highest case fatility rate was among cases less than 15 years (21.4%) and those aged age ≥ 60 years (20.0). The case fatality was the
lowest among those aged from 15 to less than 45 years and it was 0% among those from 45 to less than 60 years.
Table 5: Factors associated with mortality among the studied H1N1 cases, Riyadh, Saudi Arabia (n= 107)
Table 5 display the results of the univariate logistic regression analysis for the association of case fatility with the studied cases'characteristics.
Age ≥ 60 years was associated a significant high risk of mortality with an odds ratio 3.6 (95% CI= 1.10-12.8). A significant
high risk of mortality was also dected among cases with associated medical problems (OR= 3.3; 95% CI= 1.02-12.90) and among those
cases admitted to ICU (OR= 4.2; 95% CI= 1.14-15.3). Male sex, however, was associated with a low risk of fatailty with 25% reduction
in the risk was detected (OR= 0.75; 95% CI= 0.23-15.3).
Since its emergence in April 2009, influenza A H1N1 is still
threat worldwide. The present study aimed to shed light about
some epidemiologic characteristics of H1N1 in Riyadh, Saudi
Arabi using the data available from the reported 107 confirmed
cases during the period from February 2014 to December 2015.
The highest incidence of H1N1 in this study was reported among
young and older age groups and it was more among male subjects.
Similar characteristics were reported in several previous repportd.
In 2009, Influenza A H1N1 predominantly affected young subjects
in Mineapolis (10), and New Zealand (11). In a Tiwan study, the
highest percentage was among 11-15-year-olds (12). According to
a study done in Queensland, a large number of cases were reported
in the 10-19 years age group (28%), followed by the 20-29 years
age group (26%) (13).
The characteristics of H1N1 cases reported in the first Saudi report
in 2010 (7), however, showed that the highest percentage of cases
was in the age group of 20 to 30 years followed by the age group
of 1 to 10 years, and females were presented more than half of the
studied 100 cases.
Almost all the studied patients were presented by fever and flu
symptoms such as running nose, cough, sneezing, sore throat. In
China, fever was the main presenting symptom of H1N1 infection,
together with cough (40%) and sore throat (35%) (14). Fever was
also reported to be the most common symptom, followed by cough
(54%), sore throat (32%), rhinitis (17%) and difficulty in breathing
(7%) in a study of the first 100 cases of Influenza A H1N1 in Saudi
Arabia report (7). In a study conducted at Chile, fever was the
most common presentation (83%), followed by cough (72%),
odynopahgia (54%), myalgia (48%) and dehydration (4%) (15) A
study done in Japan described fever (87%) as the most common
symptom, followed by cough (86.3%) and sore throat (65%) (16).
The present report has revealed that vominting and dirrhoea
were the main presenting symptoms with fever in 7 patients
(6.5%). Up to 50% of all patients present with gastrointestinal
symptoms including diarrhea and vomiting. The spectrum of clinical presentation varies from asymptomatic cases to primary
viral pneumonia resulting in respiratory failure, acute respiratory
distress, multi-organ failure, and death (17).
The incidence of H1N1 infection was fluctuating all over the
year. However, steep rise in the epidemic curve was noticed
reaching its peak on March 2014 followed steep descend in the
following months. The same curve characteristics has occurred in
2015, where the peak of curve reached on March with the highest
reported cases of 21 cases. The observed high peak on March on
the two consuctive studied years may indicate that the disease has
intense in late winter and erly spring. Consistent with this study
peak, the CDC has announced the first cases of H1N1 March-april
2009 in two children-Southern California (1).
The study findings revealed 19.6% of cases admitted to ICU.
The mean length of ICU stay was 10 ± 3.5 days and it was
significantly higher among cases with comorbidities (14 ± 3.1days
vs. 7 ±3.7 days among cases with co-morbidities). Using data
from existing surveillance systems, public health laboratories,
and local hospitals, Doshi etal. (18) have estimated numbers of
pH1N1-associated illnesses, emergency department (ED) visits,
hospitalizations, intensive care unit (ICU) admissions, and deaths
occurring in metropolitan Atlanta during the period August
16, 2009-September 26, 2009. The authors estimated 132,140
pediatric and 132,110 adult symptomatic cases of pH1N1 in
metropolitan Atlanta during the investigation time frame. Among
children, these cases were associated with 4,560 ED visits, 190
hospitalizations, 51 ICU admissions, and 4 deaths. Among adults,
they were associated with 1,130 ED visits, 590 hospitalizations,
140 ICU admissions, and 63 deaths. The rate of hospitalization
could actually be as high as 10% in some cities. Most, but not
all, of the hospitalized patients have underlying conditions such
as cardiovascular disease, respiratory disease including asthma,
autoimmune disorders, obesity, diabetes, or cancer. Although
the prevalence of H1N1 was greatest among children and young
adults, older patients and those with co-morbidities are more likely
to experience worse clinical outcome that needs ICU admission
(11). Also, pregnant women, especially in their second and third
trimester, are also at a high risk for more severe disease (19). In
our study, there were 2 pregnant women, one of them diagnosed
in 1st and the other in 2nd trimester. Both cases were hospitalized
and discharged after one week without any complications for hers
or their fetuses.
The case fatality in this study was 10.3% where 21 out of 107 cases
were died. The highest fatality rate was among these cases less
than 15 years (21.4%) and those aged ≥ 60 years (20%), whilest
the lowest case fatility rate was among cases in the age groups
from 15 to less than 60 yaers. These findings clearly reflects high
prevalence, morbidity and mortality of influenza A H1N1 among
the younger and older population. A systematic review reported a
very substantial heterogeneity in published estimates of case fatality
risk for H1N1pdm09, ranging from <1 % to > 10%, with the higher
estimates were based on laboratory confirmed cases (20). In this
report all the studied 107 cases were laboratory confirmed cases.
Recently, a meta analysis study included 179 studies published
in MEDLINE (PubMed) between April 1, 2009, and January 9,
2014. The study estimated the crude fatality rate to range from
0% to 52%, with higher estimates was from tertiary-care referral
hospitals in countries with a lower gross domestic product, but
in wealthy countries the estimate was 1%-3% in all settings. The
study found the point estimates to increase substantially with age
and with lower gross domestic product (21).
Unlike other similar studies, this report has used univariate logistic
regression analyses to investage the possible risk factors associated
with mortality among the studies cases. Old age (≥ 60 years),
associated medical problems (co-morbidities) and ICU admission
were the significant risk factors affecting mortality of the studied
cases in this report. The estimated odds ratio was 3.6, 3,3 and 4.2,
respectively. Male sex, however, was a protective factor, although
The limitation of this report was that the analysis included data
was from only one city and that the analysed laboratory-confirmed
cases represented a small subset of cases of H1N1 influenza
during the study period as only laboratory-confirmed cases were
analyzed. The report did not include subjects with symptoms who
did not undergo laboratory testing.
In conclusion, the study findings demonstrated those people at high
risk to get H1N1 infection, and the time when the risk of infection
is the highest. The report has also revealed that the infection is
still a threat in Saudia Arabia with a reported high fataility rate.
Because there not much data are available, it is recommended to
build up surveillance system for H1N1 all over the year, especially
during Hajj and Umrah seasons. Annual conduction of such
studies not only help in better understanding of the epidemiologic
characteristics of this emergent disease, but it also help in
monitoring the effectiveness of Ministry of Health and community
mitigation efforts. Finally, because Saudi Arabia annually hosts the
largest international gathering of the Hajj n a small geographical
area. This always puts the kingdom in the threat of of spread of the
disease. Establishment of surveillance system, particularly during
Hajj season appeared essential to face any epidemic wave of this
Conflict of Interest
The author declares that there is no conflict of interest.
- Centers for Disease Control and Prevention (CDC) Swine
influenza A (H1N1) infection in two children-Southern California,
March-April 2009. MMWR Morb Mortal Wkly Rep.2009;58:400-402. [PubMed]
- Dawood FS, Jain S, Finelli L, Shaw MW, Lindstrom S, Garten
RJ, Gubareva LV, Xu X, Bridges CB, Uyeki TM. Novel SwineOrigin
Influenza A (H1N1) Virus Investigation Team. Emergence
of a Novel Swine-Origin Influenza A (H1N1) Virus in Humans. N
Engl J Med.2009;360:2605-2615. [PubMed]
- Centers for Disease Control “Outbreak of Swine-Origin
Influenza A (H1N1) Virus Infection-Mexico, March--April 2009”
Centers for Disease Control. Available from:http://www.cdc.gov/
mmwr/preview/mmwrhtml/mm58d0430a2.htm. [accessed on
2017 Apr 3] [PubMed]
- Kahn LH. “Stirring up “swine flu” hysteria” Bulletin of the
Atomic Scientists. Available from:http://thebulletin.org/webedition/columnists/laura-h-kahn/stirring-swine-flu-hysteria.
[accessed on 2017 Apr 3]
- WHO. Influenza A (H1N1): Special Highlights. World Health Organization. Available from:http://www.who.int/en/. [accessed
on 2017 Apr 3]
- CDC “Swine Flu and You” CDC. 2009-04-26. Available
from:http://www.cdc.gov/swineflu/swineflu_you.htm. [accessed on 2017 Apr 3]
- AlMazroa MA, Memish ZA, AlWadey AM. Pandemic influenza A (H1N1) in Saudi Arabia: description of the first one hundred cases. Annals of Saudi Medicine. 2010;30(1):11-14.
- Statistical Yearbook: Central Department Of Statistics &
Information. Statistical Yearbook 47; 2011. Retrieved 3 April
- SAS Institute Inc. Proprietary Software Release 8.2. , Cary, NC,
SAS Institute Inc, 1999.
- Delaney JW, Fowler RA. 2009 Influenza A (H1N1): A Clinical
review. Hosp Pract (Minneap) 2010;38:74-81. [PubMed]
- Dee S, Jayathissa S. Clinical and epidemiological characteristics
of the hospitalized Patients due to Pandemic H1N1 2009 Viral
infection: Experience at Hutt Hospital, New Zealand. N Z Med J.
- Appuchamy RD, Beard FH, Phung HN, Selvey CE, Birell
FA, Culleton TH. The changing phases of pandemic (H1N1)
2009 in Queensland: An overview of Public Health Action and
Epidemiology. Med J Aust. 2010;192:94-97. [PubMed]
- Lan YC, Su MC, Chen CH, Huang SH, Chen WL, Tien N,
Lin CW. Epidemiology of pandemic influenza A/H1N1 virus
during 2009-2010 in Taiwan. Virus Res. 2013 Oct;177(1):46-54.
- Li YQ, Qian Q, Fung LQ, Yang H, Wei MT, Gao Y, et al.
Epidemiological characteristics of 420 influenza A (H1N1) cases
confirmed in the early stage of the epidemic in Mainland China.
Zhonghua Liu Xing Bing Xue Za Zhi. 2009;30:1102-1105.
- Torres JP, Ryan M, Herve B, Espionza R, Acuna G, Manalich
J, et al. Impact of the novel influenza A (H1N1) during the 2009
autumn winter season in a large hospital setting in Santiago, Chile.
Clin Infect Dis. 2010;50:860-868. [PubMed]
- Chibana N. Clinical Review of 1017 influenza A cases between
30 and 35 weeks in 2009. Kansenshogaku Zasshi. 2010;84:153-
- World Health Organization “Acute respiratory update”.
en/index5. [accessed on 2017 Apr 3]
- Doshi SS, Stauffer KE, Fiebelkorn AP, Lafond KE, Davidson
HA, Apostolou A, Taylor TH Jr, Smith W, Karcz AN, Watson
JR, Openo KP, Brooks JG, Zheteyeva Y, Schrag SJ, Fry AM.The
burden and severity of illness due to 2009 pandemic influenza A
(H1N1) in a large US city during the late summer and early fall of
2009. Am J Epidemiol. 2012 15;176(6):519-526. [PubMed]
- Peiris JS, Poon LL, Guan Y. Emergence of a novel swineorigin
influenza A virus (S-OIV) H1N1 virus in humans. J Clin
Virol. 2009;45:169-173. [PubMed]
- Wong JY, Kelly H, Ip DKM, Wu JT, Leung GM, Cowling
BJ. Case fatality risk of influenza A(H1N1pdm09): a systematic
review. Epidemiology (Cambridge, Mass). 2013;24(6):10.1097/
- Wong JY, Kelly H, Cheung C-MM, et al. Hospitalization
Fatality Risk of Influenza A(H1N1)pdm09: A Systematic
Review and Meta-Analysis. American Journal of Epidemiology.