Prospective surveillance of healthcare associated infections in a Cambodian pediatric hospital
Hearn et al. Antimicrobial Resistance and Infection Control
Prospective surveillance of healthcare associated infections in a Cambodian pediatric hospital
Pasco Hearn 0
Thyl Miliya 0
Nicholas P. J. Day
Claudia Turner 0
Paul Turner 0
0 Cambodia-Oxford Medical Research Unit, Microbiology Department, Angkor Hospital for Children , PO Box 50, Siem Reap , Cambodia
Background: Healthcare associated infections (HAI) are the most common preventable adverse events following admission to healthcare facilities. Data from low-income countries are scarce. We sought to prospectively define HAI incidence at Angkor Hospital for Children (AHC), a Cambodian pediatric referral hospital. Methods: Prospective HAI surveillance was introduced for medical admissions to AHC. Cases were identified on daily ward rounds and confirmed using locally adapted Centers for Disease Control and Prevention (CDC) definitions. During the surveillance period, established infection prevention and control (IPC) activities continued, including hand hygiene surveillance. In addition, antimicrobial stewardship practices such as the creation of an antimicrobial guideline smartphone app were introduced. Results: Between 1st January and 31st December 2015 there were 3,263 medical admissions and 102 HAI cases. The incidence of HAI was 4.6/1,000 patient-days (95% confidence interval 3.8-5.6) and rates were highest amongst neonates. Median length of stay was significantly longer in HAI cases: 25 days versus 5 days for non-HAI cases (p < 0.0001). All-cause in-hospital mortality increased from 2.0 to 16.1% with HAI (p < 0.0001). Respiratory infections were the most common HAI (54/102; 52.9%). Amongst culture positive infections, Gram-negative organisms predominated (13/16; 81.3%). Resistance to third generation cephalosporins was common, supporting the use of more expensive carbapenem drugs empirically in HAI cases. The total cost of treatment for all 102 HCAI cases combined, based on additional inpatient days, was estimated to be $299,608. Conclusions: Prospective HAI surveillance can form part of routine practice in low-income healthcare settings. HAI incidence at AHC was relatively low, but human and financial costs remained high due to increased carbapenem use, prolonged admissions and higher mortality rates.
Healthcare associated infection; Prospective HAI surveillance; Pediatric HAI; Cambodia
The most common, preventable adverse event following
admission to a healthcare facility is a healthcare
associated infection (HAI). Such infections are now a major
cause of morbidity and mortality worldwide [1, 2].
Admissions are often prolonged by HAI, whilst their
association with increasingly resistant bacteria requires
that more expensive antimicrobials are often employed.
As such, HAI represent an ever growing human and
financial cost in both high and low-income settings, but
estimating the scale of the issue is problematic.
The World Health Organization (WHO) report on the
global burden of HAI in 2011 stated that “there is an
urgent need to establish reliable systems for HAI
surveillance and to gather data on the actual burden on a
regular basis” . Pooled information from high-income
countries suggested an overall HAI prevalence of 7.6 per
100 admissions and an incidence of 17.0 per 1,000
patient-days . Few middle and low-income countries
carry out HAI surveillance, but pooled data from such
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studies show a significantly higher prevalence of 15.5 per
100 admissions and incidence of 47 · 9 per 1,000
intensive care unit (ICU)-days . It is estimated that 4.5
million HAI episodes occur each year in Europe, costing
around €7 billion . Estimating costs in low-income
settings is very challenging due to the variety of settings,
standards of medical care and lack of data. Nevertheless,
an extended length of stay (LOS) of 5–29.5 days per
HAI and an excess mortality of 18–29.5%  are likely
to represent significant burdens for these countries.
Limited resources are available to carry out
prospective studies on HAI . Much of the available data come
from adult populations within high-income countries.
Accurate comparisons between healthcare systems have
been facilitated by the introduction of clear case
definitions [7–9], but these are centered on adult infections.
The risks of HAI are different for children, as are their
clinical presentations . Children have immature
immune systems, increased susceptibility to viral
infections and frequently present without fever, making the
diagnosis of HAI more challenging . Such factors
highlight the need for more consistent approaches to
HAI surveillance, particularly in pediatric populations.
Reductions in HAI rates of 20 to 30% have been
seen with the introduction of effective infection
prevention and control (IPC) programs, alongside
HAI surveillance [12–14]. Other interventions known
to reduce HAI rates include written guidelines;
organization of IPC at a hospital level; education and
training, especially when accompanied by audit and
feedback; and surgical instrument sterilization
procedures [15–17]. Lack of resources, however, requires
prioritization of the most cost-effective methods. Poor
hand hygiene is widely accepted as the most
important risk factor for HAI [2, 18, 19]. The International
Nosocomial Infection Control Consortium (INICC)
has repeatedly shown, in resource-poor settings, a
comprehensive and multifaceted approach can improve
hand hygiene compliance by up to 48% [20–23]. Focusing
on antimicrobial stewardship in addition to hand
hygiene has also been shown to improve HAI rates in
low-income settings .
In Cambodia, a low-income Southeast Asian country,
there are very limited data on the burden of HAI.
Stoesser et al. reported previously the effects of
introducing an IPC program to Angkor Hospital for Children
(AHC). Hand hygiene surveillance and a
ventilatorassociated pneumonia (VAP) care bundle were
introduced in 2010 and the impact measured by regular HAI
point prevalence survey (PPS). During the study period,
hand hygiene compliance doubled to 51.6%. A
significant reduction in HAI prevalence was also noted, from a
median of 15.8% in the first half of the year to 11.1% in
the second .
However, the lack of prospective, incidence-based
surveillance means that the true burden of pediatric HAI in
low-income countries is not well understood.
Recognized approaches to HAI reduction are also more
challenging where resources are limited. The aim of this
surveillance program was to prospectively define the
incidence of HAI in medical admissions to AHC during a
period of ongoing IPC activity and increased
antimicrobial stewardship. Once established into routine care,
ongoing prospective surveillance will allow the assessment
of future IPC interventions to occur in real time.
AHC is located in Siem Reap, the capital town of Siem
Reap province, northwest Cambodia. According to the
2008 national census, the province had a total
population of 896,443, including 322,857 children aged
<15 years . AHC is a non-governmental organization
and one of two pediatric hospitals located in the
province. This 89 bedded hospital provides secondary and
tertiary level care to children aged <16 years with no
geographic restriction. There are approximately 160,000
patient presentations and over 4,000 admissions per
year. In addition to medical and surgical wards, there is
an ICU, neonatal intensive care unit (NICU) and special
care baby unit (SCBU).
The microbiology department at AHC provides
microscopy, culture and antimicrobial sensitivity results to
clinicians on a range of samples, along with treatment
advice where required. The laboratory follows guidance
from the Clinical & Laboratory Standards Institute
(CLSI) for antimicrobial susceptibility testing and
participates in internal and external quality assurance
programs (Pacific Paramedical Training Centre). The
clinical microbiologists, having trained as physicians
prior to specializing in infection, regularly discuss and
review patients and their treatment on the wards.
IPC and antimicrobial stewardship activities
IPC activities started at AHC in 2010 and include
regular hand hygiene surveillance, monthly multidisciplinary
IPC meetings, quarterly PPS and an annual staff training
course. Compliance with the first moment of the WHO
guidelines on hand hygiene is monitored and rates fed
back to ward representatives at monthly meetings.
Education focusses on improving hand hygiene,
maintaining a clean clinical environment and minimizing the
duration of exposure to major HAI risk factors, such as
urinary catheters, central venous catheters and ventilation.
The IPC program uses the WHO-supported Cambodian
national IPC guideline as a reference point .
Infection and antimicrobial stewardship ward rounds
started on a weekly basis on medical wards and twice
weekly on ICU. These were attended by medical
students, junior and senior doctors and focused on
infection cases within each ward.
Pre-existing hospital antimicrobial guidelines were
updated and converted into a free smartphone app
(“MicroGuide” ), also available on ward computers.
The app included local and national guidelines where
available and appropriate international guidelines where
they were not. In addition to diagnostic and treatment
algorithms, the app contained HAI definitions and
details about our surveillance. A survey of doctors at AHC
was conducted one month after release of the app to
assess its ease of use and utility in daily practice. Use of
the app was also monitored throughout by its producers.
Four continued medical education (CME) sessions for
all clinical staff were used to introduce the “MicroGuide”
app, to discuss increasing antimicrobial resistance, the
benefits of antimicrobial stewardship and the purpose of
monitoring HAI rates.
Quarterly PPS continued, with an additional
appropriateness measure, based on the assessment of a clinical
microbiologist. A prescription was deemed inappropriate
if the choice of antimicrobial deviated from the
guidelines for the documented diagnosis; if the dose was not
as per guidelines and according to the patient’s weight; if
the duration was longer than the guidelines suggested,
without clearly documented reason.
Prospective HAI surveillance
Daily ward rounds started on medical, ICU, NICU and
SCBU. Discussion with the attending team enabled HAI
case-finding five days per week, with weekend cases
identified each Monday.
HAI were considered possible in patients admitted for
at least 48 h, or if presenting with likely infection
following discharge from AHC within the preceding 48 h. Cases
were confirmed and categorized by syndrome using locally
adapted CDC definitions (see Additional file 1). “Possible
HAI” cases were those given a clinical diagnosis of HAI
and treatment to reflect this, but who did not satisfy the
criteria for any HAI syndromes.
Case report forms recorded patient demographics,
reasons for admission, risk factors for HAI, symptoms,
signs and key investigation results. The medical team
was offered management advice, but investigations and
final decisions were made at the discretion of the
clinicians. Treatment, admission duration and outcome data
were recorded and reported at the end of each calendar
month to heads of department within the hospital.
Data management and analysis
Following case identification, patient data were
anonymized and entered into a password protected database
(Access 2013, Microsoft, Redmond, WA). Data were
analyzed using the R statistical package, version 3.2.0
. HAI incidence was determined as the number of
cases per 1,000 patient-days. For comparison within the
literature the ‘attack rate’ was also calculated as the
number of HAI cases per 100 admissions. Poisson
confidence intervals were calculated for incidence rates.
Denominator information was extracted from the
hospital electronic database which documents all admission
and discharge dates for all in-patients. Each case was
matched by age and admission ward with two controls
and comparisons between groups were made using the
Wilcoxon Rank Sum test for continuous variables and
the Chi-squared test for proportions. Two-sided
p-values of < 0.05 were considered an indication of
The impact of HAI on LOS was estimated by comparing
each HAI case with two non-HAI controls, matched by
both age-group and admission-ward, as a correlate for
severity at presentation. Costings from a complete
topdown economic analysis of AHC in 2011 were
inflationadjusted to reflect current prices . This produced a
cost per patient-day of $130 on the medical ward/SCBU
and $184.50 on ICU/NICU. These figures were then
combined with the additional LOS data to estimate
overall HAI costs. As a separate calculation, the cost of
antimicrobial usage in HAI cases was calculated using
pharmacy pricing records for each drug prescribed,
assuming single drug vials were used per dose.
There were 4,300 admissions to AHC during 2015.
Surgical admissions, where surveillance was not active,
were removed from analysis, along with those admitted
for <48 h. A total of 3,263 (76%) medical admissions
were followed until discharge, representing 21,995
patient-days. The most frequent reasons for admission
were pneumonia, gastroenteritis and dengue, followed
by acute bronchiolitis and asthma.
One hundred two HAI episodes were identified from
93 separate admissions, resulting in an annual HAI
incidence of 4.6 per 1,000 patient-days (95% confidence
interval (CI) 3.8–5.6) and an attack rate of 3.1 per 100
admissions (95% CI 2.5–3.8). Incidence varied by age
group, with the majority of infections affecting those
under one year of age (Fig. 1). Over the course of the
surveillance period there was a downward trend in HAI
incidence. This was not, however, found to be
statistically significant (Fig. 2).
The median age of those with an HAI was lower than
those without (0.7 vs. 1.8 years, p < 0.0001; Table 1) and
the HAI syndromes diagnosed varied by age group
(Fig. 3). Overall, the most common HAI were respiratory
Fig. 2 HAI incidence by month during 2015 (dashed line showing linear trend)
Table 1 Demographic details for all Non-HAI and HAI admissions
to Angkor Hospital for Children, 1st January – 31st December 2015
Age, years (range)
Gender, % male
(male (n): female (n))
mortality rate, % (n)
n number of patients
infections: 52.9% (54/102) of cases. These were
categorized as hospital acquired pneumonia (29), ventilator
associated pneumonia (13), lower respiratory tract
infection (8), and upper respiratory tract infection (4).
Necrotizing enterocolitis (NEC) was the most common
to affect the neonatal age group. Microbiology results
revealed 16 HAI cases (15.7%) were associated with
significant bacterial isolates from any site, 14 of which were
blood cultures. Gram negative organisms numbered 13/
16 (81.3%) and overall, third generation cephalosporins
were ineffective against 12/16 (75%) clinical isolates
(Table 2). Results lead to a change in empirical
treatment in 5/16 (31.3%) cases. Third generation
cephalosporins made up 18.7% of antimicrobial use in HAI
cases, whilst carbapenems accounted for 67.1%.
HAI were associated with increased mortality.
NonHAI patients had an all-cause in-hospital mortality rate
of 2.0% compared to 16.1% for HAI cases (p < 0.0001).
These infections were deemed to have directly
contributed to the deaths of 11 patients, giving an attributable
mortality of 11.8%.
Overall, the median LOS for HAI cases was
significantly longer than for non-HAI controls: 25 days
(interquartile range (IQR) 12–37) compared with 5 days (IQR
3–9; p < 0.0001; Table 3). The total cost of treatment for
all 102 HAI cases combined was estimated to be
$299,608 (Table 3). The direct cost of antimicrobials for
the same group combined was $28,472, of which
$27,668 (97.2%) was due to carbapenem use.
During the 12-month surveillance period, average
hand hygiene compliance rates at AHC were 81%. The
“MicroGuide” app was viewed a total of 4,615 times and
a survey of AHC doctors suggested that 96% had used
the app during their clinical practice, whilst over half
found the app met their needs ‘very’ or ‘extremely well’.
Fig. 3 HAI syndrome by age group. BSI Blood stream infection, IV intravenous, m months of age, n number of patients, NEC necrotizing
enterocolitis, UTI urinary tract infection, yr years of age
Table 2 Significant bacterial isolates from specimens submitted during work up for suspected HAI
Escherichia coli Pseudomonas
Staphylococcus aureus (MRSA)
3GC third generation cephalosporin, B/C blood culture, BSI blood stream infection, ETT endotracheal tube secretions, Gastro gastroenteritis, HAP hospital-acquired
pneumonia, Imi/mero carbapenem (imipenem or meropenem), Int-R intrinsically resistant, MRSA methicillin resistant Staphylococcus aureus, NEC necrotizing
enterocolitis, R resistant, Rx treatment, S sensitive, SSTI skin and soft tissue infection, UTI urinary tract infection, VAP ventilator-associated pneumonia,
aThis coliform could not be identified to a satisfactory level using the biochemistry short set or bioMerieux API kits available at AHC
PPS data determined that antimicrobial prescriptions
were appropriate in 75.4% of all infection cases assessed.
This surveillance demonstrates that accurate HAI
incidence data can be produced as part of routine
microbiology input in a low-income setting. Few prospective
studies have attempted to longitudinally monitor HAI
rates in such settings, especially within the pediatric
population. These results highlight how simple,
affordable measures, such as can be provided by an IPC nurse
and an infection doctor, working with ward staff well
educated on IPC issues, can result in an HAI incidence
of 4.6 per 1,000 patient-days. This is significantly
lower than would have been expected from the
literature [4, 31] and the trend is downward during the
course of the year, although not statistically significant.
Nevertheless, HAI cases are avoidable and represent
significant costs in terms of broad spectrum antimicrobial
use, additional LOS and increased mortality rates.
Murni et al. showed that in resource-limited pediatric
settings, a multifaceted intervention including a hand
hygiene campaign and the introduction of antimicrobial
stewardship can have significant effects on HAI rates
and mortality . At AHC the IPC program was
established in 2011, with antimicrobial stewardship activities
following more recently. Since that time, the HAI attack
rate has decreased from 13.8  to the current 3.1 per
100 admissions. The two rates were produced using
quite different methodologies and populations, but are
nevertheless informative. Ongoing prospective
surveillance will bring consistency and allow the impact of
future IPC activities to be assessed more accurately.
The introduction of freely available, locally relevant
guidelines is a key component of IPC and antimicrobial
stewardship [17, 32, 33]. The direct effects of the AHC
“MicroGuide” app could not be measured, but it has
been widely adopted and utilized by ward clinicians.
Antimicrobial prescribing was found to be appropriate
in over 75% of cases. The rate of carbapenem use for
HAI was high at 67.1%, representing 97.2% of the overall
antimicrobial costs, but this is supported by local
susceptibility patterns and guidelines . As resistance
patterns change and different antimicrobial
combinations become available, this practice will continue to be
the focus of antimicrobial stewardship efforts, to ensure
appropriate use of precious antimicrobials.
According to the literature, around 80% of all HAI are
related to medical devices or surgical interventions .
However, at AHC urinary and central venous catheters
were present in only 9.8 and 2.0% of HAI cases
respectively. Limiting the duration of exposure to such medical
devices forms part of IPC training at AHC and may have
helped maintain the low HAI rates. Future HAI
surveillance would benefit further from the collection of data
regarding ‘device-days’, to allow comparisons between
healthcare settings internationally. These should include
ventilator-days, central venous catheter-days and urinary
catheter-days and their lack is a limitation of this
surveillance, but requires records to be kept for patients
throughout the hospital, rather than just the HAI cases
Having a dedicated infection team, permanently based
on the wards, would likely produce more accurate HAI
incidence rates, but may not be possible in many
resource-limited settings due to staffing constraints.
Major strengths of this work are that it employed a
practicable approach, confirmed each HAI case according to
strict definitions and involved clinicians in the
identification of cases and the collection of clinical data. However,
collaboration with the surgical team was limited and
accurate data collection was therefore not possible. This is
likely to have produced an incomplete picture of the
overall HAI incidence. Since surgical site infections are
known to be a common cause of HAI [2, 3, 35], working
alongside surgical teams must remain a priority
wherever possible and the focus of future efforts.
In the context of this surveillance period, it was not
possible to link patterns of HAI rates to possible
seasonal variations in pathogen prevalence. Limited
diagnostics at AHC meant the role of viruses could not be
investigated. Viruses are known to contribute to
pediatric HAI cases in a way that they do not in adults
. It is possible that testing for viruses would have
reduced the number of “possible HAI” diagnoses, whilst
continuation of the program may yet uncover seasonal
patterns, explaining some of the undulation within the
Rates of NEC were found to be high and, after
respiratory HAI, represented the second most commonly
diagnosed syndrome. The pathogenesis of NEC is
incompletely understood, but likely to be multifactorial
and limited data exist regarding approaches to reducing
its rates . Resistant organisms are quick to colonize
areas such as the neonatal unit  and difficult to treat
once implicated in infections. It remains to be seen
whether efforts to improve IPC practices will reduce the
chances of colonization with multiply-resistant
organisms rather than reduce the number of NEC cases, but
this is a question for future research.
Another limitation of this work is the possibility that
the incremental human and economic costs of HAI have
been overestimated, since confounding or competing
risks of adverse outcome and HAI were not accounted
for in the analysis. Furthermore, the incremental cost of
longer admissions was calculated using the average cost
per inpatient day, which does not account for the
unequal distribution of costs over the course of an
admission. The methods do, however, give a useful estimate of
the overall costs of treatment using available data in a
setting where more sophisticated models for calculating
costs throughout an admission are lacking.
This report demonstrates that prospective HAI
surveillance is possible as part of routine practice in a
low-income, pediatric setting. It describes how, in the context
of simple IPC and antimicrobial stewardship activities, a
relatively low rate of HAI can be maintained. However,
despite this low incidence, the overall impact of HAI
remains high. The increased mortality rate, cost
implications of additional carbapenem use and extra LOS in
hospital are all compelling reasons to pursue cost
effective and sustainable approaches to HAI reduction.
Ongoing, prospective surveillance will allow the
effectiveness of these approaches to be closely monitored
and will inform ways in which further reductions to HAI
rates can best be achieved.
Additional file 1: HAI_case_definitions. (DOCX 23 kb)
AHC: Angkor Hospital for Children; CDC: Centers for disease control and
prevention; CI: Confidence interval; CLSI: Clinical & Laboratory Standards
Institute; CME: Continued medical education; HAI: Healthcare associated
infection; ICU: Intensive care unit; INICC: International nosocomial infection
control consortium; IPC: Infection prevention and control; IPD: In-patient
department (medical wards); IQR: Interquartile range; LOS: Length of stay;
NEC: Necrotizing enterocolitis; NICU: Neonatal intensive care unit; PPS: Point
prevalence survey; SCBU: Special care baby unit; VAP: Ventilator associated
pneumonia; WHO: World Health Organization
Thanks to Dr Nicholas Grundmann, MD, MBA, who performed the costing
study at Angkor Hospital for Children in 2011. Thanks also to the doctors
and staff of Angkor Hospital for Children for their ongoing input into the
monitoring and treatment of healthcare associated infections.
The Cambodia Oxford Medical Research Unit is funded by the Wellcome
Trust as part of the Wellcome Trust-Mahidol University-Oxford Tropical
Medicine Research Programme.
Availability of data and materials
The dataset generated during the surveillance period are not publicly available
but are available from the corresponding author on reasonable request.
PH, TM and PT were responsible for all data collection and analysis. All authors
contributed to and approved the final manuscript.
The authors declare that they have no competing interests.
Consent for publication
Ethics approval and consent to participate
Surveillance activities were approved by the AHC Institutional Review Board.
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