Original Article

Healthcare-associated Infections at a Tertiary Level Pediatric Intensive Care Unit From Turkey


  • Gülhadiye Avcu
  • Başak Yıldız Atıkan

Received Date: 17.04.2020 Accepted Date: 11.10.2020 J Pediatr Res 2021;8(3):246-250


Healthcare-associated infections are important conditions, as they may increase morbidity and mortality, prolong hospital stay and increase costs. A higher incidence of healthcare-associated infections has been reported in developing countries, but data on its epidemiology in pediatric patients are limited. The aim of this study was to determine the rate and distribution of health care-associated infections and antimicrobial susceptibility patterns in a pediatric intensive care unit.

Materials and Methods:

Demographic and clinical details, microbiological findings, antibiotic susceptibility results and the outcomes of all hospitalized pediatric intensive care unit patients were collected for one year (September 2017 to September 2018).


The health care-associated infections rate was 5.6 per 100 admissions and the incidence density was 7.2 per 1,000 patient-days. Bloodstream infections (50%) were the most common type and Klebsiella species (40.9%) was the most common cause of health careassociated infections. All of the Klebsiella spp. were resistant strains producing extended-spectrum beta-lactamases (77.7%) and the remaining were resistant to carbapenem. Acinetobacter species and colistin resistance was not detected in any isolates.


This study demonstrated a low prevalence of health care-associated infections but a high rate of antibiotic resistance in Klebsiella species in a pediatric intensive care unit. In addition to improved surveillance, consultation with infectious disease specialists will allow the development of interventions to reduce healthcare-associated infections, in order to regulate both empirical treatment and ongoing management, and also to provide appropriate targeted therapy.

Keywords: Healthcare-associated infections, antimicrobial resistance, children


Healthcare-associated infections (HAI) continue to be an important source of morbidity and mortality worldwide, but especially in developing countries such as our country (1). They cause a major public health problem with prolonged hospitalization, broad spectrum antibiotic requirement, increased resistance patterns and consequent additional healthcare costs. Although intensive care units (ICUs) account for fewer than 10 percent of the total beds in most hospitals, the incidence of HAI is higher in ICUs than any other hospital units. More than 20 percent of all nosocomial infections are acquired in ICU (2,3). Patients hospitalized in an ICU are more prone to HAI due to their severe clinical conditions and the consequent invasive procedures (4).

Although the rate of HAI in pediatric intensive care units (PICUs) in developed countries is lower than in adult ICUs, this situation is different in developing countries (1). Also, the rate of HAI is higher in PICUs than in other children’s units. In a multicenter study conducted in Europe, the incidence of HAI in general pediatric units was reported to be 1% while it was 23.6%. in PICU (5). In a study from our country, the HAI rate was reported to be 22.24% in a PICU (1).

Infections and sepsis are the leading cause of death in non-cardiac ICUs. The most important nosocomial infections in ICUs are bloodstream infections (BSIs), ventilator-associated pneumonia (VAP), and urinary tract infections (UTIs).

In this study, we aimed to determine the incidence of HAIs, the distributions of the pathogens and the antimicrobial susceptibility in a PICU, in a city hospital in Turkey.

Materials and Methods

Balıkesir City Hospital is a non-tertiary state hospital which was opened with the aim of providing health service to a wide region. The hospital started admitting patients in 2017. The pediatric ICU, which is the only one in the area, consists of nine tertiary level beds. Each nurse has to care for two patients. Two pediatric infectious diseases specialists work and participate in the active surveillance of HAI with the infection control team.

In this study, the data of the patients, aged 1 month to 18 years and hospitalized between September 2017 and September 2018 in the PICU, were collected retrospectively. The information of the patients (age, gender, disease, period of hospital stay, ventilator or device use, antibiotic treatment, clinical and laboratory findings) and their culture results were investigated. The definition of HAI was made according to the “Centers for Disease Control and Prevention” criteria (6), a nd HAI was defined as an infection occurring 48 hours after hospitalization or 10 days after discharge. The rate of HAI was calculated according to the following formula; the number of HAIs/the number of all hospitalized patients x100.

The incidence density was calculated according to the formula; the number of HAIs/total patient-days x 1,000 in a given period.
This research was made with the approval decision of Balıkesir University Clinical Research Ethics Committee dated 05.12.2018 and numbered 2018/199.

Statistical Analysis

The study was registered with IBM SPSS 20.0 for Windows. In statistical analysis; for the analysis of numerical data, arithmetic mean ± standard deviation with minimum and maximum values were used while in categorical data, the number (n) and percentage (%) are given.


During the one-year study period, 398 patients were hospitalized in the tertiary level PICU and HAI developed in 22 of these patients. Only two of them died because of underlying chronic diseases, namely severe hydrocephalus and cerebral palsy. The mean age of the patients was 81.9 months (range: 3-190 months). Half of the patients who developed HAI (n=11, 50%) were female. When the patients were evaluated according to their primary diagnosis, neurological disorders were the largest group (81.8%) with 18 patients (11 cerebral palsy, 3 epilepsy, 2 hydrocephalus, 2 spinal muscular atrophy). Two (9%) had genetic syndrome with tracheostomy, 1 (4.5%) patient had acute diarrhea-dehydration and 1 (4.5%) patient had glioma (Table I).

The HAI rate was 5.6 per 100 admissions and the incidence density was 7.2 per 1,000 patient-days. The most frequently detected HAI types were BSI (50%), VAP (40.9%) and UTI (9.1%), respectively. Klebsiella species (40.9%) was the most common cause of HAI, followed by Candida species (18.1%), Pseudomonas aeruginosa (13.6%), Serratia marcescens (9.1%), Enterobacter cloacae (9.1%), Stenotrophomonas maltophilia (4.5%) and coagulase-negative Staphylococcus (methicillin-resistant) (4.5%) (Table II). Four of the BSIs were central line-associated BSI (CLABSI); It was detected in patients who had been hospitalized for more than 30 days and diagnosed with cerebral palsy. The microorganisms were determined to be Candida spp. in three cases, while in one case it was Stenotrophomonas maltophilia. All of the isolated Klebsiella species were resistant strains; 77.7% of them produced Extended spectrum betalactamases (ESBLs) and the remaining were resistant to carbapenem. Carbapenem susceptibility was detected in 66.6% of Pseudomonas aeruginosa and 100% of Serratia marcescens and Enterobacter spp. (Table III). Colistin resistance was not detected among the microorganisms produced in cultures. The only coagulase-negative Staphylococcus was methicillin-resistant.


HAIs in PICUs are an important problem resulting in prolonged hospital stay, increased medical costs, and increased morbidity and mortality (7). Most of the HAIs occurring in ICUs are associated with the use of invasive devices such as central line or mechanical ventilators (8). In developing countries, it has been reported that the incidence of HAI is higher than in developed countries due to the high number of patients, limited staffing and poor compliance with infection control measures (9-10). In developed countries, HAI rates are lower among children than among adults. In the United States, 5-10% of hospitalized adult patients are reported to have HAIs, while the rate is 1.5% to 4% for ten-year-olds and 7% -9% for infants younger than 1 year old (5). In our country, it was reported that the rates of HAIs in pediatric and adult patients varied between 1.3% and 16% in 2009 (10).

HAIs from PICU are reported to range 6% to 13.7% according to one study (11). Some previous studies have shown that the prevalence of PICU-acquired HAIs ranged from 9.1% to 42.5% (11-13). In our study, the HAI rate was lower than most of the similar reports with a rate of 5.6 per 100 admissions.

The incidence of the HAI type may differ according to the characteristics of the department, hospital and region. In the United States, the most common HAI types were reported to be BSI (28%), pneumonia (21%) and UTI (15%) in PICUs (14). In our study, the most common HAI type was BSI (50%), VAP (40.9%) and UTI (9.1%). Similarly, from our country, Atici et al. (1) reported that the most commonly observed HAIs were BSI (37.5%), pneumonia (21.4%), and UTI (20.5%) while Kepenekli et al. (15) reported that the most common HAIs were pneumonia (55%), BSI (27%) and UTI (7%), respectively. In another study with HAI ratios between 1.4% and 2.4%, the most commonly observed infections were UTI, surgical site and BSIs, and the most frequently isolated pathogens were E. coli, Klebsiella pneumoniae, Enterococcus spp. and Staphylococcus aureus (16).

In previous years, gram-positive factors were the most common causes of hospital infections. Today, Pseudomonas, Klebsiella and Acinetobacter species are among the leading factors in both adult and pediatric patients, in addition to coagulase-negative Staphylococcus strains (17,18). Pseudomonas aeruginosa is reported to be the most common agent of infections in PICUs in Europe (5). In our study, consistent with the literature, gram-negative agents were the most common agents in HAIs. Klebsiella spp. were the most often isolated microorganisms in all types of HAIs including BSI and VAP. Acinetobacter species, which are a common and important agent of HAIs in the world, were not detected in our study but interestingly, Candida species were the second most common, especially in BSIs. This was due to long-term hospitalized patients with cerebral palsy and respiratory failure, who had central venous catheter and a history of treatment with broad spectrum antibiotics.

The resistance characteristics of microbiological agents responsible for hospital infections also vary over the years (19). There has been a rapid rise in the rate of resistance among bacterial pathogens in ICUs. The widespread use of antibiotics is associated with the development of resistance to antimicrobial agents. An international, multicenter study reported that the 78% of Klebsiella pneumoniae isolates produce ESBLs (17). In a study from our country, 50% of Klebsiella spp. and E. coli isolates were reported to be ESBL positive (1). The resistance rates found in our study were consistent with the literature; 77.7% of Klebsiella spp. produced ESBLs and 22.3% were resistant to carbapenem. In some previous studies, it was reported that the susceptibility rate to carbapenem ranged from 48% to 71% (20,21). It was reported to be 63% among Pseudomonas aeruginosa isolates in a national study (1). In our study, carbapenem susceptibility was detected in 66.6% of Pseudomonas aeruginosa and colistin resistance was not detected in any isolate.

The low number of patients and the retrospective nature are the most important limitations of our study.


In conclusion; we report a low rate of HAIs in our study but most were resistant bacteria. The low rate may be due to the unit being newly opened and the good condition of the hospital as well as the daily intensive care visits provided by pediatric infectious diseases specialists. Active surveillance is required for effective infection control, and pediatric infectious disease consultation leads to appropriate antibiotic use, reduced HAI rates, and finally improved PICU patient outcomes.


Ethics Committee Approval: This research was made with the approval decision of Balıkesir University Faculty of Medicine Clinical Research Ethics Committee dated 05.12.2018 and numbered 2018/199.

Informed Consent: Retrospective study.

Peer-review: Externally peer-reviewed.

Authorship Contributions

Concept: G.A., Design: G.A., Data Collection or Processing: G.A., B.Y.A., Analysis or Interpretation: G.A., Literature Search: G.A., B.Y.A., Writing: G.A.

Conflict of Interest: No conflict of interest was declared by the authors.

Financial Disclosure: The authors declared that this study received no financial support.


  1. Atici S, Soysal A, Kepenekli Kadayifci E, et al. Healthcare-associated infections in a newly opened pediatric intensive care unit in Turkey: results of four-year surveillance. J Infect Dev Ctries 2016; 10:254-9.
  2. Fridkin SK, Welbel SF, Weinstein RA. Magnitude and prevention of nosocomial infections in the intensive care unit. Infect Dis Clin North Am 1997; 11:479-96.
  3. Vincent JL, Rello J, Marshall J, et al. EPIC II Group of Investigators. International study of the prevalence and outcomes of infection in intensive care units. JAMA 2009; 302:2323-9.
  4. McGrath EJ, Asmar BI. Nosocomial infections and multidrug-resistant bacterial organisms in the pediatric intensive care unit. Indian J Pediatr 2011; 78:176-84.
  5. Raymond J, Aujard Y. Nosocomial infections in pediatric patients: a European, multicenter prospective study. European Study Group. Infect Control Hosp Epidemiol 2000; 21:260-3.
  6. Horan TC, Andrus M, Dudeck MA. CDC/NHSN surveillance definition of health care-associated infection and criteria for specific types of infections in the acute care setting. Am J Infect Control 2008; 36:309-32.
  7. Sodhi J, Satpathy S, Sharma DK, et al. Healthcare associated infections in Paediatric Intensive Care Unit of a tertiary care hospital in India: Hospital stay & extra costs. Indian J Med Res 2016; 143:502-6.
  8. Lakshmi KS, Jayashree M, Singhi S, Ray P. Study of nosocomial primary bloodstream infections in a pediatric intensive care unit. J Trop Pediatr 2007; 53:87-92.
  9. El-Nawawy AA, Abd El-Fattah MM, Metwally HA, Barakat SS, Hassan IA. One year study of bacterial and fungal nosocomial infections among patients in pediatric intensive care unit (PICU) in Alexandria. J Trop Pediatr 2006; 52:185-191.
  10. Hacımustafaoğlu M, Çelebi S, Tuncer E, Ozkaya G, Cakır D, Bozdemir S. Nosocomial infection incidence in pediatric clinic and pediatric intensive care unit. J Pediatr Inf 2009; 3:112-7.
  11. Saptharishi LG, Jayashree M, Singhi S. Development and validation of the “Pediatric Risk of Nosocomial Sepsis (PRiNS)” score for health care-associated infections in a medical pediatric intensive care unit of a developing economy--a prospective observational cohort study. J Crit Care 2016; 32:152-8.
  12. Grohskopf LA, Sinkowitz-Cochran RL, Garrett DO, et al. A national point-prevalence survey of pediatric intensive care unit-acquired infections in the United States. J Pediatr 2002; 140:432-8.
  13. Richards MJ, Edwards JR, Culver DH, et al. Nosocomial infections in pediatric intensive care units in the United States. Pediatrics 1999; 103:39.
  14. Gravel D, Matlow A, Ofner-Agostini M, et al. A point prevalence survey of health care-associated infections in pediatric populations in major Canadian acute care hospitals. Am J Infect Control 2007; 35:157-62.
  15. Kepenekli E, Soysal A, Yalindag-Ozturk N, et al. Healthcare-associated infections in a newly opened pediatric intensive care unit in Turkey: results of four-year surveillance. J Infect Dev Ctries 2016; 10:254-9.
  16. Erdinc FS, Yetkin MA, Hatipoglu CA, et al. Five-year surveillance of nosocomial infections in Ankara training and research hospital. J Hosp Infect 2006;64: 391-6.
  17. Paterson DL, Ko WC, Von Gottberg A, et al. International prospective study of Klebsiella pneumoniaebacteremia: Implications of extended spectrum b-lactamase production in nosocomial infections. Ann Int Med 2004; 140:26-32.
  18. Rutledge-Taylor K, Matlow A, Gravel D, et al. Canadian Nosocomial Infection Surveillance Program. A point prevalence survey of health care-associated infections in Canadian pediatric pnpatients. Am J Infect Control 2012; 40:491-6.
  19. Gould IM. Antibiotic resistance: the perfect storm. Int J Antimicrob Agents 2009; 34:2-5.
  20. Esen S, Leblebicioğlu H. Prevalence of nosocomial infections at intensive care units in Turkey: a multicenter 1-day point prevalence study. Scand J Infect Dis 2004; 36:144-8.
  21. Aksaray S, Dokuzoğuz B, Güvener E, et al. Surveillance of antimicrobial resistance among Gram-negative isolates from intensive care units in eight hospitals in Turkey. J Antimicrob Chemother 2000; 45:695-9.