|Year : 2017 | Volume
| Issue : 3 | Page : 100-107
Bacterial healthcare-associated infection rates among children admitted to Pediatric Intensive Care Unit of a Tertiary Care Hospital, Egypt
Azza A Moustafa1, May M Raouf2, Mona S El-Dawy1
1 Department of Pediatrics, Faculty of Medicine, Alexandria University, Alexandria, Egypt
2 Department of Medical Microbiology and Immunology, Faculty of Medicine, Alexandria University, Alexandria, Egypt
|Date of Submission||06-Nov-2017|
|Date of Acceptance||08-Jan-2018|
|Date of Web Publication||20-Apr-2018|
Azza A Moustafa
Department of Pediatrics, Faculty of Medicine, Alexandria University, Alexandria
Source of Support: None, Conflict of Interest: None
Background Healthcare-associated infections (HAIs) are life-threatening complications especially in pediatric ICU (PICU).
Objective This study aimed to calculate the incidence of HAIs and device-associated infections (DAIs), as well as HAIs and DAI incidence density rate in a Alexandria University Children Hospital PICU, Egypt.
Patients and methods A prospective cohort study was carried out over a period of 1 year. Personal, clinical, and laboratory data were recorded. HAIs were identified according to Centers for Disease Control and Prevention and National Healthcare Safety Network CDC/National Health Surveillance Network case definitions. Standard microbiological techniques were adopted.
Results A total of 195 patients (of 282 admissions) who stayed more than 48 h in PICU were included. Overall, 16 patients developed bacterial HAIs, with a total of 25 episodes. HAIs incidence rate was 12.8/100 PICU admissions and incidence density was 15.6/1000 PICU days. All HAIs detected were DAI. Ventilator-associated pneumonia accounted for 72%, followed by central line (CL)-associated bloodstream infections at 24% and catheter-associated urinary tract infections at 4%.The rates of the DAI per 1000 device days were as follows: ventilator-associated pneumonia 12.4/1000 ventilator days, CL-associated bloodstream infections 4.2/1000 CL days, and catheter-associated urinary tract infections 0.69/1000 urinary catheter days. Gram negative bacteria were the most common isolated pathogens (n=18/25, 72%). All isolates were multidrug-resistant organisms.
Conclusion and recommendations HAIs and DAI incidence rates in the current study were close to those of developed countries and lower than those of developing countries. Presence of an invasive device has a high risk for acquiring HAIs, resulting in higher mortality. The key to prevent HAIs is continuous education of infection prevention and control practices including an adoption of a surveillance program.
Keywords: catheter-associated urinary tract infection, central line-associated bloodstream infection, device-associated infections, healthcare-associated infections, pediatric intensive care unit, ventilator-associated pneumonia
|How to cite this article:|
Moustafa AA, Raouf MM, El-Dawy MS. Bacterial healthcare-associated infection rates among children admitted to Pediatric Intensive Care Unit of a Tertiary Care Hospital, Egypt. Alex J Pediatr 2017;30:100-7
|How to cite this URL:|
Moustafa AA, Raouf MM, El-Dawy MS. Bacterial healthcare-associated infection rates among children admitted to Pediatric Intensive Care Unit of a Tertiary Care Hospital, Egypt. Alex J Pediatr [serial online] 2017 [cited 2019 Jan 23];30:100-7. Available from: http://www.ajp.eg.net/text.asp?2017/30/3/100/230762
| Introduction|| |
Healthcare-associated infections (HAIs) are infections that occur on or after the third calendar day of hospital admission . They are an important cause of morbidity and mortality worldwide.
Although 5–10% of hospitalized cases have HAIs in developed countries, this ratio exceeds over 25%, in developing countries . Even though ICUs have less than 10% of the beds in hospitals, more than 20% of HAIs occur in ICUs . The incidence of HAIs in pediatric ICUs (PICUs) varies between developed and developing countries (6.1 and 23.5%, respectively), whereas the incidence density rate of HAIs varies between 14.1 and 27.2/1000 patient-days, respectively .
HAIs remain an important cause of increased morbidity, mortality, length of stay (LOS), and healthcare costs ,. Among the factors that make the children more susceptible to HAIs in PICUs are their immune-compromised condition, broad-spectrum antibiotic usage, and medical manipulations that disrupt the natural defenses of the host including the use of invasive devices [e.g. intravascular devices, intubation, nasogastric tubes, and urinary catheters (UC)] .
In developed countries, infection prevention and control programs (IPC) have been implemented as an essential element in healthcare institutes mainly focusing on device-associated infection (DAI) surveillance . In many countries of limited resources, a sustainable surveillance IPC is being developed ,.
| Aim|| |
This prospective study aimed to calculate incidence of HAI and DAI in Alexandria University Children Hospital PICU, Egypt, as a part of continuous monitoring of IPC measures in this PICU.
| Patients and methods|| |
Study design and setting
The Alexandria University Children’s Hospital at Al-Shatby is a 200-bed tertiary healthcare teaching hospital with one nine-bed PICU. The PICU receives children aged 1 month to 14 years. It has an average daily occupancy of 85%, and the nurse to patient ratio is 1 : 1.
A prospective cohort study was conducted over 1 year, starting from 1 September 2014 through 31 August 2015. We included all patients admitted to the PICU during the study period and stayed for 48 h or more. They were monitored during their stay and until 48 h after discharge.
Demography, admission diagnosis, Pediatric Index of Mortality (PIM2) score, referral place, daily clinical and laboratory data, risk factors for HAIs acquisition, and outcomes of HAIs including LOS and mortality data were collected.
Microbiologic methods and healthcare-associated infections definitions
The study was conducted using Centers for Disease Control and Prevention and National Health Surveillance Network case definitions.
Catheter-associated urinary tract infection (CAUTI): It is a UTI where an indwelling UC was in place for more than 2 calendar days and an indwelling UC was in place on the date of event or the day before. Central line-associated bloodstream infection (CLABSI): It is a laboratory-confirmed bloodstream infection where central line (CL) or umbilical catheter was in place for more than 2 calendar days and the line was also in place on the date of event or the day before. Ventilator-associated pneumonia (VAP): it is a case of pneumonia where the patient is on mechanical ventilation (MV) for more than 2 calendar days, and the ventilator was in place on the date of event or the day before. It is identified by using a combination of imaging, clinical, and laboratory criteria .
Bacteriologic cultures from different sites were collected on admission from blood, urine, sputum, bronchoalveolar lavage, and cerebrospinal fluid if needed. On suspicion, cultures were taken per suspected site(s) of infection.
An episode was considered a second one if it occurred with another type of infection or with the same type of infection occurring more than 14 days after the start of the initial episode. Infection with a different organism within 14 days timeframe was included in the same episode.
Standard microbiology methods were used for identification and antimicrobial susceptibility testing of bacterial isolates from all samples ,. Cultures and susceptibility tests were performed in the Microbiology Central Laboratories, Faculty of Medicine, Alexandria, Egypt.
Data were collected and entered into the computer using statistical package for the social sciences (SPSS) program for statistical analysis (version 21) (IPM, Armonk, NY, USA) . Data were entered as numerical or categorical, as appropriate. Kolmogorov–Smirnov test of normality revealed significance in the distribution of some variables, so the nonparametric statistics was adopted . Data were described using median and interquartile range. Categorical variables were described using frequency and percentage. Comparisons were carried out between two studied independent non-normally distributed subgroups using Mann–Whitney U-test . χ2-Test was used to test association between qualitative variables. An α level was set to 5% with a significance level of 95%, and a β error was accepted up to 20% with a power of study of 80%.
This study was approved by Medical Research Ethics Committee at Faculty of Medicine, Alexandria University, Egypt, and an informed consent was obtained from children’s guardians.
| Results|| |
During the study period, 282 children were admitted to our PICU. A total of 195 stayed for more than 48 h for a total of 1603 PICU-days. Overall, 25 HAI episodes in 16 children, fulfilling the inclusion criteria, were identified and included in the analysis. Of the 16 children, three (18.8%) had more than a month stay in PICU owing to congenital lung anomalies and had two or more episodes.
Personal and clinical criteria of pediatric ICU patients with respect to healthcare-associated infections acquisition (n=195)
Personal and clinical criteria of the patients without and those with bacterial HAIs are summarized in [Table 1]. The results showed that patients with HAIs had statistically significant longer median LOS [19.50 (13.50–33.00) vs. 5 (3.00–9.00) days, P=0.000] and had higher mean pediatric logistic organ dysfunction (PELOD) score [16.50 (12.00–26.00) vs. 10.00 (1.00–14.40), P=0.000]. On comparing device usage as a risk factor of acquisition of HAIs among the two groups, patients with HAIs had significantly more MV days (93.75 vs. 43.58%, P=0.000). Regarding the fate, patients with HAIs had statistically significant higher mortality rate (62.5 vs. 19.55%, P=0.000) compared with the group without HAIs.
|Table 1 Personal and clinical characteristics of studied pediatric ICU patients with respect to healthcare-associated infections (n=195)|
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Criteria that were significantly associated with HAIs in univariate analysis (LOS, PELOD, and MV) were included in multivariate analysis using logistic regression model ([Table 2]). The overall model was significant (model χ2=57.2, P=0.000); significant predictors of HAIs were LOS [odds ratio (OR): 1.298; 95% confidence interval (CI): 1.146–1.470] and MV (OR: 11.52; 95% CI: 1.205–110.051). According to the results, patients with MV were 11 times more likely to have HAIs compared with patients with no MV. Although in univariate analysis PELOD was significantly associated with HAIs, this association was no longer significant after adjustment for other covariates in multivariate analysis.
|Table 2 Predictors of healthcare-associated infections in the studied pediatric ICU patients group (n=195)|
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Types of healthcare-associated infections and recovered bacterial isolates
The incidence of HAIs was 12.8/100 PICU admissions and 15.6/1000 PICU-days. All HAIs detected were DAI. VAP was the most frequent nosocomial infection episode (18 episodes, 72%), followed by CLABSI (six episodes, 24%) whereas CAUTIs were the least common (one episode, 4%). Device utilization ratio was 0.9 for MV, CL, and UC.
The DAI incidence density rates were VAP 12.4/1000 ventilator days, CLABSIs 4.2/1000 CL days, and CAUTIs 0.69/1000 UC days ([Table 3]).
During the study period, 25 microorganisms were isolated. Of these 25 microorganisms, 18 (72%) isolates were Gram-negative bacteria (GNB) and seven (28%) isolates were Gram-positive bacteria. The most frequently isolated pathogens were Klebsiella spp. (14 isolates, 56%), followed by Acinetobacter spp. and Staphylococci spp. (three isolates, 12% each). Diphtheroids spp., Streptococcus viridans group, and Stenotrophomonas spp. accounted for 8, 8, and 4%, respectively. Klebsiella spp. caused 44.4% of VAP, 83% of CLABSI, and 100% of CAUTI.
Antimicrobial susceptibility showed that all the isolates were multidrug resistant. All Klebsiella spp. isolates were extended-spectrum β-lactamase producers. Two isolates of Staphylococcus aureus were methicillin resistant and one isolate of coagulase-negative staphylococcus was also methicillin resistant. Acinetobacter spp. isolates were sensitive only to quinolones. The Stenotrophomonas spp. isolate was sensitive only to ceftazidime, levofloxacin, and trimethoprim/sulphamethoxazole ([Table 4]).
|Table 4 Distribution of isolated bacteria according to site of infection and their antimicrobial susceptibility|
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Personal and clinical criteria of pediatric ICU patients with respect to fate
Of 195 patients admitted to our PICU during the study period, 45 (23.08%) patients died. On comparing personal and clinical criteria among deceased versus discharged group, the results showed statistically significant higher PIM2 score value, higher mean PELOD score, and higher incidence of HAIs among the deceased group (P=0.000, 0.000 and 0.000, respectively) ([Table 5]).
|Table 5 Personal and clinical criteria among studied pediatric ICU patients with respect to fate (n=195)|
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Criteria that were significantly associated with mortality in univariate analysis were included in multivariate analysis using logistic regression model. The overall model was significant (model χ2=57.592, P=0.000); significant predictors of mortality were PIM2 score (OR: 1.022; 95% CI: 1.007–1.039) and mean PELOD score (OR: 1.130; 95% CI: 1.077–1.189) ([Table 6]).
|Table 6 Mortality predictors among studied pediatric ICU patients (n=195)|
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HAIs incidence was no longer significant predictor of mortality after adjustment for other covariates in multivariate analysis.
| Discussion|| |
The current study was a 1-year prospective study of HAIs in a PICU. Comparing the results with the study by El-Nawawy et al.  conducted for 1 year, HAI rates decreased significantly (HAIs incidence: 12.8/100 PICU admissions vs. 29.6/100, P=0.000 and incidence density: 15.6/1000 PICU days vs. 40/1000, P=0.000).
In fact, HAIs incidence in the present study was lower than rates in developing countries (15.1–22.1%)  and close to the rates of developed countries (9.2–11.9%) .
As reported in most studies, LOS at PICU was longer for patients with HAIs versus those without HAIs ,. It is important to keep in mind that other factors interact with length of hospital stay, such as the patient’s underlying clinical condition and associated comorbidities. Some authors also consider prolonged LOS as a risk factor for HAIs, as longer hospitalization leads to colonization of patients by pathogenic microorganisms and longer duration of invasive procedures which favors the development of HAIs .
In the present study, children with HAIs had higher mean PELOD scores during their stay in the PICU than children without HAIs [16.50 (12.00–26.00) vs. 10.00 (1.00–14.40), P=0.000]. Mansour et al.  reported the same finding (25±10.4 vs. 15.7±9.3).
Presence of an invasive device has a high risk for acquiring HAIs. The current results demonstrated significant increase in HAIs in patients with MV. This is comparable to many studies in the USA and China ICUs ,.
The current results of device utilization ratio (DUR) were almost the same for MV, CL, and UC (0.9%). Our DUR is higher than that recorded in 2012 National Health Surveillance Network report .
VAP was the most frequently reported episode in this study. These data are in agreement with other studies and are very close to International Nosocomial Infection Control Consortium (INICC) study of DAI in 703 ICUs in 50 countries (12.2/1000) and other studies ,,. However, many studies reported bloodstream infections as the leading cause of HAIs in the PICU ,.
The CLABSIs rate was lower than the rates reported from other studies (24 vs. 47% and 48.6%) ,, whereas it lies in the same range of most studies from developed countries (22–30%) ,.
The CAUTI rate (4%) is considered among the lowest CAUTI reported rates, which vary across the world (3.4 and 15.8%) ,.
Of the isolated pathogens, 72% were GNB and 28% were Gram-positive bacteria. This distribution agrees with previous studies, conducted in both adults and children, showing that in ICUs most HAIs are due to GNB, with Enterobacteriaceae accounting for 25–30% of all isolates ,.
Klebsiella spp. was the most frequently isolated organism in VAP in the present study. This is consistent with other studies ,. However, many studies reported Pseudomonas spp. as the most common microorganism associated with VAP .
The National Nosocomial Infection Surveillance System survey (NNISS) of PICU patients identified coagulase-negative Staphylococcus spp. as the predominant organism associated with CLABSI, accounting for 37.8% of reported cases . GNB accounted for 19 and 21% of CLABSIs reported to CDC and the Surveillance and Control of Pathogens of Epidemiological Importance database, respectively . In the present study, we found a predominance of GNB causing CLABSI which is consistent with other studies from developing countries ,. This raises the possibility that GNB continue to dominate in developing countries.
In agreement with the literature available on PICU, the mortality rate in the current study was higher for the patients with HAIs than those free of HAIs . Higher mortality rate for patients with HAIs could be attributed to the severity of underlying pathology as our unit is a referral tertiary PICU. However, it is difficult to know HAIs-attributable mortality.
Comparing discharged children with the deceased ones, the present study showed that the PIM2 score was significantly higher among the deceased children, which is an expected finding as PIM2 score is documented to be a useful risk assessment tool for prediction of mortality among pediatric patients, being the most accurate among several models, and having the best fit in different diagnostic and risk groups .
In the present study, the mean PELOD score during PICU stay was significantly higher among the deceased children than the discharged. Ibrahiem et al.  reported the same finding in their study who reported a median PELOD score of 11.5 in the deceased children compared with one in survivors.
Surveillance done by INICC in developing countries is focused on outcome surveillance by monitoring DAIs ,,,, and process of surveillance, which assesses IPC strategies . INICC provides continuous education, free training, and free online surveillance tools to promote IC in limited-resource countries . Although DAI rates in ICU patients in the INICC study of 50 countries are still higher than CDC-NSHN ICUs rates representing the developed world, significant reduction is observed .
| Conclusion|| |
DAIs are important healthcare complications that result in increased morbidity and mortality. The current study concluded the following:
- MV and UC were significantly associated with HAIs.
- Patients with HAIs had significantly longer LOS and higher mortality.
- DAI incidence rates were close to those of developed countries and lower than those of developing countries.
HAIs prevention through continuous education of infection control and prevention practices including hand hygiene, restricted and early withdrawal of invasive devices, and restricted usage of antibiotics is a top priority worldwide. Adoption of a surveillance program in low-resource countries is mandatory.
Authors are appreciative of all Alexandria University Children’s Hospital PICU staff and the patients and their guardians, who agreed to participate, readily cooperated with the research team, and agreed to undergo the necessary investigations.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
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[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]