AARRTTIICCLLEE OORRIIGGIINNAALL//OORRIIGGIINNAALL AARRTTIICCLLEE
INFLUENZA A (H1N1) 2009 PANDEMIA
THE EXPERIENCE OF A TERTIARY CARE CENTER IN BEIRUT
Rania NAOUFAL1, Jihad IRANI2, Isabelle DJAFFAR JUREIDINI1, Noha HAKIME1, Eid AZAR3
George JUVELEKIAN4, Mona HADDAD5, Claude AFIF3,5
Influenza A is a single-stranded RNA virus belonging to
the family Orthomyxoviridae. It is characterized by two
types of glycoprotein spikes that project from its surface:
hemaglutinin HA and neuraminidase NA [1-2]. Influenza
A viruses are subtyped according to those two glycopro-
teins. New strains of influenza are the result of mutations
in the HA and NA genes, which occur via two mechanisms
[3-4]. Antigenic drift occurs during replication of the influ-
enza virus, with errors in progeny genes leading to fre-
quent mutations. The second mechanism is the antigenic
Naoufal R, Irani J, Djaffar Jureidini I, Hakime N, Azar E,
Juvelekian G, Haddad M, Afif C. Influenza A (H1N1) 2009
pandemia : The experience of a tertiary care center in Beirut.
J Med Liban 2012 ; 60 (2) : 70-76.
Naoufal R, Irani J, Djaffar Jureidini I, Hakime N, Azar E,
Juvelekian G, Haddad M, Afif C. Influenza A (H1N1) : Expé-
rience d’un hôpital universitaire libanais durant la pandémie
de 2009. J Med Liban 2012 ; 60 (2) : 70-76.
ABSTRACT • INTRODUCTION : In March 2009, a new
influenza virus strain emerged, currently known as the
2009 pandemic H1N1 virus. The virus first appeared in
Mexico and rapidly spread globally to reach a pan-
demic level in June of the same year. We describe here
the experience of one major referral center in Beirut,
MATERIALS AND METHODS : The Laboratory Depart-
ment at St. George Hospital University Medical Center
received respiratory specimens from hospital wards,
the Emergency Department, in addition to a consider-
able proportion collected directly from “outpatients”
in the lab. We used the real time RT-PCR as our main
diagnostic test. We collected data about the patients
from the Laboratory Information System and from the
Hospital Medical Records Department.
RESULTS : From mid-August 2009 till the end of Jan-
uary 2010, a total of 1771 specimens were analyzed,
with 948 (53.5%) returning positive for influenza A
(H1N1) by RT-PCR. Only 79 patients with H1N1 in-
fection required hospitalization. Most of H1N1 con-
firmed patients were children and adolescents aged 5 to
17 years and young adults between 25 and 44 years.
The most common symptoms at presentation were:
fever, cough, shortness of breath, chills, rhinorrhea or
nasal congestion, as well as gastrointestinal symptoms.
Twenty-three patients required ICU care and eight pa-
tients died. The vast majority had an uncomplicated
course of illness and was managed in an outpatient
CONCLUSION : The percentage of positive tests dur-
ing the pandemia was significantly elevated, although
few patients experienced drastic clinical outcomes.
From the University of Balamand and Saint George Hospital University Medical Center, Beirut, Lebanon.
Departments of • Laboratory Medicine1 • Medicine: Division of Family Medicine2, Division of Infectious Diseases3, Division of
Pulmonary Medicine4 • Infection Control5.
Correspondence to: Claude Afif, MD. University of Balamand, St George Hospital University Medical Center. PO Box 166378.
e-mail: email@example.com Tel.: +961 1 566 781 Fax: +961 1 566 780
RÉSUMÉ • INTRODUCTION : En mars 2009, une nouvelle
souche de virus influenza a émergé, couramment connue
sous le nom de grippe pandémique du virus H1N1 2009.
Apparu au Mexique, le virus s’est propagé rapidement
dans le monde pour atteindre un niveau pandémique en
juin de la même année. Nous décrivons ici l’expérience
d’un centre hospitalier universitaire à Beyrouth (Liban).
MATÉRIELS ET MÉTHODES : Le laboratoire de l’hôpi-
tal St. Georges, centre médical universitaire, a collecté
les échantillons respiratoires provenant des différents
services de l’hôpital, des urgences en plus d’une pro-
portion considérable prélevés en consultations externes.
Nous avons utilisé la PCR en temps réel (RT-PCR)
comme test de diagnostic principal. Les données des
patients ont été recueillies à partir du système informa-
tique du laboratoire et du département des archives
RÉSULTATS : De la mi-août 2009 jusqu’à fin janvier
2010, un total de 1771 échantillons a été analysé, avec
948 (53,5%) tests positifs pour la grippe A (H1N1) par
RT-PCR. Seulement 79 patients infectés par le virus
H1N1 ont dû être hospitalisés. La plupart des patients
atteints de grippe A H1N1/09 étaient des enfants et des
adolescents âgés de 5 à 17 ans, et de jeunes adultes entre
25 et 44 ans. Les symptômes les plus fréquents à l’ad-
mission étaient : fièvre, toux, essoufflement, frissons,
rhinorrhée ou congestion nasale, ainsi que des symp-
tômes gastro-intestinaux. Vingt-trois patients ont néces-
sité des soins intensifs et huit patients sont décédés.
Dans la grande majorité des cas la maladie a suivi un
cours normal, sans complications, et a été gérée en
CONCLUSION : Le pourcentage de tests positifs au cours
de la pandémie était significativement élevé, bien que peu
de patients aient présenté un tableau clinique sévère avec
R. NAOUFAL et al. – Influenza A (H1N1) 2009 pandemia in Lebanon Lebanese Medical Journal 2012 • Volume 60 (2) 71
shift, which happens when a cell is co-infected with two or
more different influenza A subtypes, enabling exchange
of full RNA segments. The 2009 pandemic H1N1 virus is
a triple reassortant influenza virus containing genes from
avian, human, and swine influenza viruses. Since swine
cells have receptors for both avian and human influenza
strains, co-infected swine cells served as mixing vessels
and allowed antigenic shift resulting in the emergence of a
new influenza subtype [5-7].
In March 2009, an increased number of influenza-like
illnesses were reported in Mexico. In April 2009, a novel
influenza A virus (H1N1) was identified, later on desig-
nated as the 2009 pandemic virus. On June 11, the World
Health Organization (WHO) declared the 2009 H1N1
influenza a phase 6 pandemic [8-9] characterized by com-
munity level outbreaks in at least two continents.
The first cases of H1N1 in Lebanon were reported dur-
ing the month of June. The Ministry of Public Health
(MOPH) activated surveillance systems and kept track of
all reported cases. Several actions were undertaken by the
MOPH: holding awareness campaigns, providing medical
care in all health care systems; offering free testing in a
governmental hospital in Beirut, and distribution of anti-
viral treatment. Saint George Hospital was one of the two
major centers where diagnosis of H1N1/09 was available.
Real time polymerase chain reaction was used (RT-PCR).
Epidemiological data about the pandemic 2009 influenza
A virus in Lebanon is scarce, and no study have been pub-
lished so far about the outbreak in Lebanon.
The objective of this study is to describe the experience
of one major center in Lebanon with the H1N1/09 influen-
za A virus. It represents the first medical report about
H1N1 pandemia in Lebanon. This will help drawing con-
clusions and learning lessons for better preparedness dur-
ing future pandemics.
MATERIALS AND METHODS
As of the third of August 2009, the Laboratory Depart-
ment at Saint George Hospital University Medical Center
(SGHUMC) started analyzing respiratory specimens for
H1N1 influenza. Before that date, the Governmental Hos-
pital of Beirut was the sole institution performing such
analysis. We included in our review all analyzed speci-
mens collected between that date and January 2010,
The specimens consisted of nasal and/or throat swabs,
sputum, bronchoalveolar lavage fluids, and endotracheal
tubes. The majority of specimens were collected from out-
patients presenting to the Laboratory Department, the rest
were sent from patients visiting the Emergency Depart-
ment, and from hospitalized patients. We screened all the
patients for H1N1 positivity, but only those who were
hospitalized were retained for further analysis retrospec-
tively. Specimens were submitted to the Molecular Sec-
tion of the Laboratory Department and were directly pro-
cessed after collection during the working hours or stored
at –80 ºC until processing. The results were reported with-
in 12-24 hours. The technique of choice was nucleic acid
analysis; we didn’t use the Rapid Antigen Test (RAT) as it
wasn’t recommended due to high rates of false negative
[10-13]. Viral nucleic acid was extracted using the High
Pure Viral Nucleic Acid Kit (Roche Diagnostics). For
each specimen, the screening for influenza A virus and
influenza A pandemic H1N1 subtype was conducted in
parallel by real time polymerase chain reaction (RT-PCR).
A one-step RT-PCR using the Real-Time Ready RNA
Virus Master and the Real-Time Ready Influenza A/H1N1
detection set (Roche Diagnostics) was performed on the
Light Cycler 2.0 Instrument according to the recommen-
dations of the manufacturer. The detection of influenza A
viruses was done through Influenza A Matrix Protein 2
gene M2, whereas that of the influenza pandemic H1N1
2009 strain relied on a specific H1N1 gene only present in
this new strain.
Specimens that were positive with both assays were
reported as positive for the influenza pandemic H1N1
2009 strain, and those which were negative with both
assays as negative. A positivity with the H1N1 assay with
a negative result with the Influenza A assay shou