Major infections following pediatric cardiac surgery pre- and post-CLABSI bundle implementation

Introduction

Congenital cardiac surgery (CCS) has become more common in developing countries and outcomes have improved. Children with CCS are at high risk for healthcare–associated infections (HAIs), leading to considerable morbidity and mortality, increased use of antibiotics, and longer hospital stays. Surgical site infection (SSI), bloodstream infection (BSI), and ventilator-associated pneumonia (VAP) are common after cardiac surgery (Alten et al., 2018; Axelrod et al., 2015; Barker et al., 2010; Sen et al., 2017). The incidence of major infections in pediatric CCS has been reported to be between 15% and 30% (Barker et al., 2010; Sen et al., 2017; Levy et al., 2003; Vijarnsorn et al., 2012; Chang et al., 2020). Risk factors for postoperative infections following CCS include younger age at surgery and complexity of the procedure (Alten et al., 2018; Axelrod et al., 2015; Barker et al., 2010; Sen et al., 2017; Levy et al., 2003). In-hospital mortality, prolonged duration of mechanical ventilation, and long stays in the intensive care unit (ICU) have been well-documented (Sen et al., 2017; Vijarnsorn et al., 2012; Agarwal et al., 2014). To improve safety and quality for children undergoing congenital heart surgery in developing countries, the International Quality Improvement Collaborative (IQIC) developed and piloted a safe surgical checklist, team-based practice, and a focus on hand hygiene (Sen et al., 2017; Jenkins et al., 2014; Balachandran et al., 2015). The primary aim was to reduce mortality associated with CCS, but also resulted in a considerable reduction in bacterial sepsis and SSI. For example, a study by Balachandran et al. reported a significant reduction in bacterial sepsis from 15.1% in 2010 to 9.6% in 2012 after launching the IQIC program (Balachandran et al., 2015).

Our pediatric cardiac service has seen an increase in surgical demand and complexity. In 2005, the mortality following CCS in our center was 6.1%. We identified high complexity, bypass time >85 min, and cross clamp time >60 min as the main risk factors for mortality (Vijarnsorn et al., 2011). At the time, 13.5% of our patients experienced major infections such as BSI, SSI, VAP, or urinary tract infection (Vijarnsorn et al., 2012). In 2013, we implemented a safe surgical checklist and a hand hygiene program as described in the IQIC campaign. In 2016, we introduced a VAP prevention package consisting of strategies for weaning, hygienic hand washing, aspiration precaution, prevention of contamination, and chest physiotherapy; together known as the WHAP-C bundle (Smulders, Van Gestel & Bos, 2013; Chang & Schibler, 2016). Use of checklists, regular audits and reassessments are common practices to ensure adherence to the bundles.

In our center between 2018 and early 2019, central-line associated bloodstream infections (CLABSI) and VAP with antibiotic resistant bacteria such as carbapenem-resistant enterobacteriacae (CRE) were identified following CCS in pediatric cardiac care units (PCCU). These infections required extensive contact precautions and prolonged antibiotic treatments (Guh, Limbago & Kallen, 2014). There is growing evidence that the addition of a maintenance bundle to a central-line insertion bundle can reduce the incidence of CLABSI in critically ill patients of all ages (Smulders, Van Gestel & Bos, 2013; Ista et al., 2016; Hussain et al., 2017; Costello et al., 2008). Beginning in April 2019, our institutional infection control committee and the PCCU team started a modified pediatric CLABSI bundle for all children undergoing CCS. The principal components of the CLABSI bundle (Ista et al., 2016; Hussain et al., 2017) are illustrated in Fig. 1. We modified additional practices to prevent CRE from the report by Guh, Limbago & Kallen (2014) (Fig. 2) and used 80% alcohol spray to disinfect the three-way extension tube that connects to the central line (Oishi et al., 2004). The modified CLABSI bundle was implemented using a team-based approach. Following one month of training the prevention package to all medical staff and nurses in the unit, infection control personnel provided detailed education to physicians and nurses, daily goal sheets were established for timely removal of the central venous line, and real-time feedback on the CLABSI data was used to monitor the program. Processes and procedures were often observed directly by unit and infection control personnel, and team discussions were held regularly to identify obstacles and track progress (Chang et al., 2020; Smulders, Van Gestel & Bos, 2013; Hussain et al., 2017; Costello et al., 2008). Physicians and nurses were encouraged to assist each other to be aware of and adhere to the maintenance bundles.

Therefore, we aimed to measure the effect of the CLABSI bundle on the incidence of major infections such as BSI, SSI, and VAP after pediatric CCS. We hypothesized that implementation of the CLABSI bundle would reduce BSI, VAP and SSI. We also explored risk factors for the occurrence of major infections in children undergoing CCS at Siriraj Hospital between 1 April 2018 and 31 March 2020.

Materials and Methods

This retrospective study was approved by the Siriraj Institutional Review Board, Faculty of Medicine, Siriraj Hospital, Mahidol University (Study number 258/2563(IRB4), COA Si 275/2020). Informed consent from patients was waived and multiple steps were taken to ensure the protection of patient confidentiality. All research methods were performed according to Good Clinical Practice (GCP) guidelines and regulations.

Data were reviewed from children <18 years old who underwent CCS at Siriraj hospital during a one-year period pre-CLABSI bundle (1 April 2018–31 March 2019), and one year post-CLABSI bundle implementation (1 April 2019–31 March 2020). Preterm infants (gestational age <37 weeks), patients with underlying disease such as autoimmune disease or cancer, and patients with extracardiac surgery in the same operation such as tracheoplasty, gastrostomy were excluded from the study. Demographic data, including age, gender, weight, height, diagnosis of congenital heart disease, genetic syndromes, preoperative history of major infection within three months prior to operation, preoperative ventilator use, central line usage, presence of clinical heart failure/pulmonary hypertension, previous cardiovascular surgery and intraoperative data, including type of operation and complexity of the surgical procedure using the Aristotle Basic Complexity score (ABC score), operative time, cardiopulmonary bypass time (CPB time), aortic cross clamp time (AoX time), delayed sternal closure, and extracorporeal membrane oxygenator (ECMO) were collected.

Postoperative outcomes included in-hospital mortality, duration of ventilator use, hospital length of stay (LOS) and major infections; BSI, SSI and VAP. BSI was defined as any two clinical signs of sepsis (fever or hypothermia, tachycardia, hypotension, tachypnea, leukocytosis or leucopenia) with a positive blood culture (Chang et al., 2020; Haughey, White & Seckeler, 2019). SSI was defined as an infection related to an incisional procedure that included superficial incisional SSI, deep incisional SSI or mediastinitis (Chang et al., 2020; Hodge et al., 2019). VAP was defined as a pneumonia in patients on a mechanical ventilator for >2 days with evidence of new pulmonary infiltration, signs of systemic infection or detection of causative agents (Chang & Schibler, 2016). The outcomes were compared between pre- and post-CLABSI bundle implementation.

Results

Patient characteristics

Five hundred and forty-eight pediatric patients were included in the analysis (Fig. 3). The demographic, clinical, and operative management of the patients are shown in Table 1. The patients had a median age of 1.9 years (0.01–17.5 years). Two hundred and ninety-three patients (53%) were male, and 96 patients (12.6%) had a genetic syndrome. The median Aristotle Basic Complexity score was 7.1 (range 3–14.5). Four hundred and ninety-two patients (89%) underwent open-heart surgery.

The overall in-hospital mortality of pediatric CCS was 5.5% (n = 30) (Table 2). Major infections (BSI, SSI and VAP) were reported in 126 patients (23%) (Fig. 4). Twenty-two patients had two major infections in their postoperative course. Among the 286 patients in the pre-CLABSI bundle period, 24 patients (8.4%) had BSI, while eight of the 262 patients (3.1%) in the post-CLABSI bundle period had BSI (p = 0.01). The pathogens causing BSI included Methicillin-Resistant Coagulase-Negative Staphylococci (n = 11), Klebsiella pneumonia e (n = 6), Acinetobacter baumannii (n = 6), Stenotrophomonas maltophilia (n = 4), Candida parapsilosis (n = 2), Staphylococcus haemolyticus (n = 1), Alpha-hemolyticus streptococci (n = 1), and Escherichia coli (n = 1). SSI occurred in 1.7% and 1.9% of patients in the pre- and post-bundle implementation period, respectively (p = 0.727). There was a reduction in the incidence of VAP after the implementation of the CLABSI bundle (21% to 17.6%), however; the incidence of VAP did not decrease significantly (p = 0.331).

Consequences and risks of major infection

In children with major postoperative infection, hospital LOS and ventilator use were significantly higher (median LOS 17.5 days vs 7 days; p < 0.001; median ventilator use 5 days vs 1 day; p < 0.001). Mortality was 11.1% in patients with major infection compared to 3.8% in those without infection (p = 0.002). The proportion of patients with/without major infections are shown with risk variables in Table S1. The adjusted OR for major postoperative infections in the pre-CLABSI bundle period was 1.83 (95% CI [1.13–2.96]; p = 0.01). Independent risk factors for major postoperative infections were age at surgery less than 6 months (adjusted OR 1.871; 95% CI [1.02–3.43]; p = 0.04), ventilator usage >2 days (adjusted OR 3.94; 95% CI [2.22–6.99]; p < 0.001) and central line usage >4 days (adjusted OR 2.20; 95% CI [1.02–4.93]; p = 0.04) (Table 3). The risk factors for mortality are presented in Table S2. Factors that independently increased the mortality risks were single ventricle (adjusted OR 6.66; 95% CI [1.76–25.02]; p-value=0.005), emergent or urgent procedure (adjusted OR 5.35; 95% CI [1.24–22.98]; p-value=0.02), and operative time >240 min (adjusted OR 3.79; 95% CI [1.19–12.01]; p-value = 0.02).

Discussion

Using a pre- and post-intervention design, we measured significant reductions in BSI from 8.4% to 3.1% (p = 0.01). The incidence of VAP did not decrease significantly (21% to 17.6%; p = 0.33), and the SSI rate remained unchanged at less than 2%. A team-based approach, continuous education, real-time feedback, and direct observation monitoring were key to successful implementation. Independent risk factors for major postoperative infections were age at surgery less than six months, postoperative ventilator usage >2 days, central line usage >4 days, and pre-CLABSI bundle implementation period.

We observed that hospital LOS and ventilator use in children with major postoperative infection were much higher (p < 0.001), underscoring the importance of preventing these infections in this vulnerable population. Following an outbreak of antibiotic- resistant bacterial infection in our PCCU, we modified the standard CLABSI bundle for children and neonates, with specific changes based on unit-based consensus and consultation with infection control experts (Smulders, Van Gestel & Bos, 2013; Ista et al., 2016; Hussain et al., 2017). An alcohol spray of 80% was used to disinfect three-way ports and extension tubes that connect to the central line as soon as the patient was transferred to the PCCU bed and, to prevent CRE, pre- and postoperative baths were administered to children older than 2 months using 4% chlorhexidine scrub diluted 1:1 in sterile water (Guh, Limbago & Kallen, 2014; Oishi et al., 2004). No skin reaction was reported after preoperative and postoperative baths in the study. It is underlined that standard central venous catheter cares including catheter flushing, dressing, blood withdrawal, heparin flushing to thrombosis prevention were also emphasized and performed with aseptic technique as neonate or pediatric protocol along with modified CLABSI bundle implementation. Maintenance and sustained application of the prevention bundle using team-based monitoring and performing constructive compliance audits is an ongoing process.

Conclusion

Following the implementation of the CLABSI prevention bundle in our pediatric CCS unit, the incidence of BSI was reduced significantly. The incidence of VAP tended to decrease, while the SSI was unchanged. Sustained application of the prevention bundle using team-based monitoring, empowering nurses to prevent infections, and performing constructive compliance audits is an ongoing challenge.

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