Advances in Infectious Diseases, 2013, 3, 300-305
Published Online December 2013 (
Open Access AID
Healthcare Associated Infection in the Neonatal Intensive
Care Unit of King Abdl Aziz Specialist Hospital, Taif, KSA
A. K. Al-Zahrani1, E. M. Eed2, A. A. Alsulaimani3, S. H. Abbadi4*
1Department Pediatrics, College of Medicine Taif University, Neonatal Intensive Care Unit King Abdulaziz Specialist Hospital, Taif,
KSA; 2Department of Medical Microbiology and Immunology, Faculty of Medicine Menoufia University, Egypt and College of Ap-
plied Medical Sciences Taif University, Taif, KSA; 3Associate Prof. Medical College, Consultant Pediatrician & Neonatologist, Taif
University, Taif, KSA; 4Department of Medical Microbiology and Immunology, Faculty of Medicine Suez Canal University, Egypt
and College of Medicine, Taif University, KSA.
Email: *
Received October 13th, 2013; revised November 13th, 2013; accepted November 20th, 2013
Copyright © 2013 A. K. Al-Zahrani et al. This is an open access article distributed under the Creative Commons Attribution License,
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Healthcare-associated infection is a common problem of newborn in neonatal intensive care units. It results in high
mortality rate and serious complications. The Aim: to assess the incidence, etiology and the mortality of healthcare-
associated infections of patients in neonatal intensive care unit at King Abdl Aziz Specialist Hospital (KAASH), Taif,
Kingdom of Saudi Arabia. Material and Methods: This is a retrospective study including 8033 neonates admitted to
neonatal intensive care unit during period between April, 2006 and December, 2012. The health-care associated infec-
tion rate, mortality rate, causative organism and risk factors were studied. Results: The prevalence of health-care asso-
ciated infection was found to be 6.03%; the mortality rate was 27.1%. The highest prevalence was among children with
the birth weight below 1000 g. The most frequent causative pathogen was klebseilla spp, followed by other gram nega-
tive bacilli. Conclusion: The rate of healthcare-associated infections in neonatal intensive care unit at KAASH was
relatively high. In addition, the mortality rate was observed to be high (27.1%) owing to the high virulence of the causa-
tive organisms.
Keywords: Healthcare-Associated Infection; Newborn; Neonatal Intensive Care Unit
1. Introduction
Health-care associated infections (HAIs) continue to be a
major public health problem throughout the world, espe-
cially in the neonatal intensive care unit (NICU). Neo-
nates in the NICU are a very vulnerable group due to de-
fective immunity and the increasing number of technol-
ogy dependant infants [1,2]. Deficiencies of both innate
and adaptive immunity contribute to the impaired neona-
tal host defense [3]. A domination of naive immune cells,
functional impairments and lower leukocyte subset num-
bers contribute further to an increased susceptibility [4,5].
The mode of infection transmission is mainly through the
care-giver staff specially if the proper antiseptic meas-
ures are not considered [4]. Infection control for prevent-
ing nosocomial infections may play an important role in
reducing medical costs, period of hospital stay, and mor-
tality in hospitalized patients [6].
Sepsis in the newborn is classified into early-onset
form (EONS), within the first 72 hours of life, and late-
onset form (LONS), which takes place afterwards (3).
HAI in the NICU takes many forms, and the most frequent
forms are the blood stream infection (septicemia) (28%),
ventilator associated pneumonia (21%). Meningitis, gas-
tro-enteritis, skin and eye infections are also common
infections [7]. Many risk factors of HAI in the NICU are
involved. The most important is excessive invasive pro-
cedures such as peripheral cannulation, central venous
catheter placement, tracheal incubation and ventilation
[6]. Furthermore, the duration of hospital stay, plays an
important role; that is, the longer the stay, the higher the
incidence of HAI [7]. Premature infants, with a birth
weight less than 1000 g (ELBW: extremely low birth
weight infants), are particularly predisposed to sepsis, as
there is an inverse correlation between gestational age,
birth weight, and sepsis [8,9]. Furthermore, the age of the
neonate has a role in the incidence of HAI. Previous stu-
*Corresponding author.
Healthcare Associated Infection in the Neonatal Intensive Care Unit of
King Abdl Aziz Specialist Hospital, Taif, KSA
dies have shown that the peak incidence of infection oc-
curred between the age of 10th and 20th day [2].
Many organisms are involved in neonatal HAI, and the
commonest are E. coli (36.6%), Staphylococcusaureus
(29.5%), Pseudomonas spp (22.4%), Klebsiella spp
(7.6%) and Proteus spp (3.8%). St pneumoniae, entero-
cocci and Serratia are also involved [10,11]. In spite of
the high prevalence and severity of neonatal HAI, the ho-
spital represents a well established reservoir for resistant
organisms that makes the problem difficult to control,
and neonatal HAI is still a preventable problem, as risk
factors can potentially be employed to develop local
strategy for prevention [12]. This could be achieved
through strict antiseptic measures for environment, staff,
equipment, and minimizing invasive procedures [13].
These perfect control measures require proper epidemi-
ological studies and tracing of infection [14]. The princi-
pal method of diagnosing sepsis is the isolation of causa-
tive organisms from blood cultures and antimicrobial sus-
ceptibility testing [15,16]. Results are usually available
between 48 - 72 hours after specimen collection and
therefore, initial antimicrobial treatment has been usually
empirical with the aim that the most likely pathogens
would be susceptible to the chosen drugs [15]. Therefore,
this study was conducted in order to investigate the epi-
demiological characteristics of HAI in the aspects of in-
fection rate, common pathogens and risk factors in our
NICU in order to guide empirical therapy and improve bet-
ter preventive measures.
2. Subjects and Methods
2.1. Clinical Setting and Patients Population
This is a retrospective, hospital-based study. It was car-
ried out in the neonatal intensive care unit (NICU) at
King Abdul Aziz Specialist Hospital (KAASH), Taif,
Kingdom of Saudi Arabia during the period April 2006 -
December, 2012. KAASH is a 500-bed tertiary-level hos-
pital. The NICU is a level III nursery with 60 bed ca-
pacity, dealing with all cases delivered in the hospital that
ranges between 12,000 to 14,000 deliveries each year.
Data were collected from the medical records in stan-
dardized collection sheets and included demographic
data, birth weight, gestational age, gender, outcome, and
delivery data (mode of delivery, maturity). The preva-
lence of sepsis was calculated by dividing the number of
newborns with sepsis by the total number of newborns
admitted to the NICU.
2.2. Case Definition
Health care associated sepsis, defined as a positive blood
culture taken after 48 hours of admission to NICU with
presence of clinical signs that are suggestive of neonatal
septicemia [12].
2.3. Culture and Susceptibility
Each neonate showing manifestation of sepsis was sub-
jected to sampling for blood culture, cerebrospinal fluid
(CSF) culture, or other samples according the clinical
presentation. Blood culture was done for all neonates
who were suspected to have sepsis. All blood samples
were collected from the peripheral vein under strict asep-
tic precautions, before starting antibiotic therapy. Blood
culture samples were incubated in the BacT/ALERT 3D
(bioMerieux, France), sub-cultures were done on blood
agar, chocolate agar, Mannitol salt agar and Mac Con-
key’s agar plates (Oxoid) and incubated at 37˚C for 24 -
48 hours. The bacterial isolates were identified by stan-
dard laboratory techniques, using standard culture media
and biochemical reactions according to the Clinical La-
boratory Standard Institute (CLSI) criteria. Thereafter,
antibiotic susceptibility testing was performed on Muller
Hinton agar (Oxoid) by Kirby-Bauer disk diffusion me-
thod and interpreted according to CLSI criteria [17]. Data
were analyzed using SPSS software (Version 10.0; SPSS
Inc., Chicago).
3. Results
Tab le 1 shows that during the study period (April, 2006-
December, 2012) the total number of the patients admit-
ted to the neonatal intensive care unit were 8033 neo-
nates. The total HAI rate in our ICU was 6.03%. Being
highest in year 2006 followed by year 2007. While was
lowest in year 2008. There were a total 484 health care
associated infections, of them 258 infant were males and
226 were females.
The studied newborn were categorized acceding to the
birth weight into four groups group I (less than 1000 g),
group II (1000 - 1500 g), group III (1501 - 2500 g) and
group IV (more than 2500 g).
The results showed different HAI rate among four
birth weight groups. The highest rate (29.54%) was
found in patients with weight below 1000 g, and was
26.65% in group II, 28.7% in group III while, the HAI
rate among the fourth group was only 14% (Table 2).
Also, the studied newborn were categorized acceding
to the gestational age in weeks into four groups group I
(less than 28 w), group II (28 - 31 w + 6 days), group III
(32 - 36 w + 6 days) and group IV (equal or more than 37
w) (Table 2). During the study period, the most com-
mon recovered organism was klebseilla spp (128 isolates)
followed by Enterobacter spp species, E. coli and Acine-
tobacterspp (79, 78 and 72 isolates respectively. Whereas
gram positive cocci as CoNS, Staphylococcus aureus and
Enterococcus were less frequent (31, 9, and 7 isolates re-
spectively) (Table 3).
Open Access AID
Healthcare Associated Infection in the Neonatal Intensive Care Unit of
King Abdl Aziz Specialist Hospital, Taif, KSA
Table 1. Healthcare-associated infection (HAI) among those
admitted to the neonatal intensive care unit at King Abdu-
laziz Specialist Hospital, Taif, Kigdom of Saudi Arabia du-
ring the period April 2006 - December 2012.
Years No. of Admissions in NICU No. HAI HAI Rate
2006 1006 155 15.4%
2007 959 79 8.2%
2008 970 11 1.14%
2009 1259 81 6.4%
2010 1254 73 5.8%
2011 1301 48 3.7%
2012 1284 37 2.9%
Total 8033 484
Table 2. Characteristics of the 484 patients with health care
associated infections among those admitted to the neonatal
intensive care unit at King Abdulaziz Specialist Hospital,
Taif, Kingdom of Saudi Arabia during the period April
2006 - December 2012.
Number of
Male 258 53.3%
Female 226 46.7%
G I (<1000) 148 29.54%
G II (1000 - 1500) 129 27.9%
G III (1501 - 2500) 139 28.5%
G IV (>2500) 68 14.%
G I (<28) 151 16.7%
G II (28 - 31 + 6) 123 26.7%
G III (32- 36 + 6) 129 25.4%
G IV (37) 81 31.2%
Alive 353 72.9%
status Died 131 27.1%
Total 484
The most common organism associated with compli-
cation was klebseilla spp (128 total complication) where-
as death was the most frequent complication where 131
case of death were reported. Resistance to amoxicillin
was the highest as it was observed in 90% of Klebsiella
and 81% of E. coli, whilst other Gram negative bacilli
showed complete resistance to this drug. Klebsiella and E.
coli also exhibited increased resistance to gentamycin
(60% and 57% respectively), as well as to Cipro-floxacin
Table 3. Distribution of causative pathogens HAI according
to the year of the study among pateints admitted to the ne-
onatal intensive care unit at King Abdulaziz Specialist Hos-
pital, Taif, Kigdom of Saudi Arabia during the period April
2006 - December 2012.
No. of Isolates (%)
2006 2007 2008 2009 2010 2011 2012Total
Escherichia coli2214 3 11 15 5 8 78
species 2523 0 11 9 5 6 79
Klebsiella species288 1 21 31 28 11128
species 36213 3 4 0 5 72
aeruginosa 5 4 2 9 1 3 3 27
aureus 1 2 1 2 1 1 1 9
CoNS 140 1 9 6 1 0 31
Enterococcus 4 0 0 2 0 1 0 7
Serratiamarcescens5 5 0 6 5 1 2 24
Group B
Streptococcus 5 0 0 2 0 0 0 7
Candida albican s102 0 5 1 3 1 22
Total 15579 11 81 73 48 37484
(45%, 43% respectively). More than 50% of E. coli
(40/78) and 46% of Klebsiella species (59/128) were
resistant to one or more third generation Cephalosporins.
Other Gram negative bacilli (mostly Enterobacter species)
also recorded high-level resistance to third-generation ce-
phalosporins (75%). Approximately one-third of Klebsi-
ella species (42/128) and E. coli (26/78 were ESBL pro-
ducers (Table 4).
4. Discussion
Health care associated infections in the NICU constitute
a major health problem and may be associated with sub-
stantial morbidity and mortality. Those infections in neo-
nates are life-threatening emergencies. Identification of
the common bacteria causing such infections and their
susceptibility patterns will provide necessary information
for timely intervention [18]. In the present study, the col-
lective HAI rate in our NICU over years 2006-2012 was
6.03%. The highest rate was observed in 2006 (15.4%)
while the lowest rate in 2008 (1.14%). The sudden drop
in the infection rate in 2008 may be due to the strict in-
fection control precaution taken after the exaggerated
high rate in the previous years (more than 15% in 2006)
Open Access AID
Healthcare Associated Infection in the Neonatal Intensive Care Unit of
King Abdl Aziz Specialist Hospital, Taif, KSA
Table 4. Distribution of causative pathogens of HAI accord-
ing to complications of sepsis among patients admitted to
the neonatal intensive care unit at King Abdulaziz Special-
ist Hospital, Taif, Kingdom of Saudi Arabia during the pe-
riod April 2006 - December 2012.
Pathogen Ventilation NEC DIC DeathTotal
Escherichia coli 32 5 20 20 78
species 23 8 15 18 79
Klebsiella species 46 7 18 37 128
species 29 2 22 20 72
Pseudomonas aeru-
ginosa 6 2 7 10 27
aureus 5 1 1 5 9
CONS 10 5 6 3 31
Enterococcus 5 4 4 2 7
Serratiamarcescens 6 4 5 9 24
Group B
Streptococcus 1 1 1 1 7
Candida albican s 7 5 4 6 22
Total 170 44 103 131 484
but generally the infection rate had declined in our NICU
(Ta bl e 2 ). The results of the present study are in agree-
ment with previous study reported by Iwona et al., (2012)
over the 6-year period, from 2005 to 2010, in which 2610
neonates were hospitalized in NICU and HAI was 7.32%
[19]. Furthermore, a retrospective study done in the neo-
natal intensive care unit of the Mexican institute in the
period between 2004 and 2007, HAI was found 4.3%
(514 out of 11,790 newborns) [20]. However, on the oth-
er hand, a similar study conducted in Nigeria estimated
HAI rate in university of Port Harcourt Teaching Hos-
pital was 34.2%, [21,22]. Also in Korea, Jeong et al., [23]
reported a HAI rate in NICU of 30.3% [24]. This vari-
ability in HAI rate depends besides infection control mea-
sure on many determinant factors such as the gestational
age, birth weight distribution of the infants surveyed for
the report, and on the specific environment and care prac-
tices, [23].
In the present study, HAI rate differs among four birth
weight groups. The highest rate (29.54%) was found in
patients with weight below 1000 g. However it was sur-
prising that the HAI rate was the higher in group III
(1501 - 2500 g) than in group II (100 - 1500 g) which
was found to be 28.7% and 26.65% respectively, while,
the HAI rate among the fourth group was only 14%. With
regards to the effect of gestational age on HAI in the
present study was in line with that of birth weight (the
highest in newborn less than 28 weeks), this may be re-
lated to fact that low birth weight and premature labor
mostly occur in combination. The majority of investiga-
tors have indicated that the risk of developing HAI in-
creased with lower birth weight. Stoll et al., [3] reported
infection rates of 50% for infants weighting below 750 g,
33% for those between 751 and 1000 g, 21% for those
between 1001 and 1250 g and 10% for those between
1251 and 1500 g [3]. During the study period, the most
common pathogen incriminated for health care-associ-
ated infection was klebseilla spp (128 isolates) followed
by Enterobacter spp species, E coli and Acinetobacter
spp (79, 78 and 72 isolates respectively), which means
that Gram negative bacilli were the major causative pa-
thogen in our NICU. The same findings were reported by
Yilmaz et al., [25] where Klebsiella spp. And E. coli, to-
gether, were responsible for 67% of HAI occurred in
NICU [25]. Many investigators concur with our study in
reporting that Gram-negative rods as the most common
etiological factors [26]. Whereas, Gaynes et al., [27] and
Stoll et al., [3], differ as they found that co-agulase-nega-
tive staphylococci were the most common pathogen, pre-
senting in 51% and 55% of cases, respectively [3,27].
The similar observation had Yelda et al., [20], they found
that Gram-positive cocci account for 55.4% of HAI, and
the most common organisms were Staphylococci [20].
Most of these isolates showed multiple antibiotics re-
sistance. Results showed that approximately one-third of
Klebsiella species (42/128) and E. coli (26/78) were
ESBL producers .These results are in agreement with Di-
nesh et al., (2011) who described a widespread problem
of ESBL-producing multidrug-resistant strains of Kleb-
siella and E. coli in hospital [28]. Also Amita et al.,
(2003) reported that more than 78% of Gram-negative
isolates were positive in the screening test for ESBL pro-
duction in blood borne neonatal infections [29].
The mortality rate was relatively high in the present
study (27%); since all fatality cases were associated with
Gram-negative pathogens. Gram-negative HAI often pre-
sents with a more rapid clinical deterioration and is com-
monly associated with shock and coagulation problems.
According to Makhoul et al., [30] mortality after Gram-
negative sepsis (26.2%) and Candida sepsis (27.6%) is
similar and significantly higher than with Gram-positive
sepsis (8.7%) [30]. Although other authors show that mor-
tality caused by Gram positive pathogens is lower, about
2.83% to 6.98% [31]. However, organisms like co-agu-
lase-negative Staphylococci may be underestimated be-
cause many cultures that grow Gram-positive bacteria re-
present skin contaminants rather than true blood stream
Open Access AID
Healthcare Associated Infection in the Neonatal Intensive Care Unit of
King Abdl Aziz Specialist Hospital, Taif, KSA
5. Conclusion
The overall HAI rate in our NICU over years 2006 -
2012 was relatively high although declining in the recent
years due to application of strict infection control meas-
ures, and the most prevalent organism was klebseilla spp,
followed by other gram negative bacilli which commonly
associated with shock and coagulation problems. There-
fore, these organisms are blamed for relatively high mor-
tality rate.
6. Acknowledgements
I would like to express my sincere thanks and apprecia-
tion to the microbiology laboratory members in King Ab-
del Aziz Specialized Hospital (KAASH) for their support
to complete of this research.
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