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Asian Cardiovasc Thorac Ann 2002;10:329-333
© 2002 Asia Publishing EXchange Pte Ltd

ORIGINAL CONTRIBUTION

Infection Risk Factors in Pediatric Cardiac Surgery

Wojciech Mrowczynski, MD, Michal Wojtalik, MD, Danuta Zawadzka, MSc1, Girish Sharma, MD, Jacek Henschke, MD, Rafal Bartkowski, MD, Malgorzata Pawelec-Wojtalik, MD, Andrzej Wodzinski, MD, Przemyslaw Westerski, MD

Department of Paediatric Cardiac Surgery
1 Clinical Analysis Department
2 Department of Paediatric Radiology Karol Marcinkowski University of Medical Sciences Poznan, Poland
For reprint information contact: Wojciech Mrowczynski, MD Tel: 48 61 849 1277 Fax: 48 61 847 5228 email: schant{at}main.amu.edu.pl Department of Paediatric Cardiac Surgery, Karol Marcinkowski University of Medical Sciences, ul. Szpitalna 27/33, Poznan 60-572, Poland.

   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Cardiac operations were preformed in 499 children from January 1998 through December 1999. Their median age was 263 days. A positive culture from blood, bronchoalveolar lavage, wound, or central catheter was obtained in 110 patients (22%). Age, sex, presence of pulmonary hypertension, body surface area, ratio of body surface area to oxygenator surface area, whether heart surgery was open or closed, and the duration of the operation, cardiopulmonary bypass, intubation, and intensive care were analyzed. Patients who developed infections were significantly younger, with smaller body surface areas and disparity with the oxygenator surface area, longer operative and bypass times, extended intubation, and prolonged intensive care. There was a significant correlation between infection and pulmonary hypertension. Sex and type of operation were not predictors of infection.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Children with congenital heart defects who undergo urgent surgery in the neonatal period or during infancy may endure prolonged intensive care unit (ICU) stay because of hemodynamic derangements. Such patients are at risk of nosocomial infections due to the invasiveness of cardiopulmonary bypass (CPB) and blood pressure monitoring, prolonged mechanical ventilation, and potential contamination from microbial flora in the ICU. The cost of treating a patient in the ICU for infection is considerable, especially when drug-resistant strains are encountered.1,2 The problem of postoperative infection is intensified by the lack of a standard protocol for antibiotic prophylaxis in pediatric cardiac surgery. Increased mortality and morbidity due to postoperative infection mars the results of cardiac surgery, delays patient rehabilitation, and reduces quality of life.3–5 Hence, identification of risk factors for infection in such patients would be of great benefit. The aim of this study was to evaluate perioperative variables in relation to infection risk in children undergoing surgery for congenital heart defects.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
The records of all children treated in our department during the 2 years from January 1998 through December 1999 were reviewed. Patients who were operated upon and transferred to other departments on the day of surgery and those who died within 24 hours postoperatively were excluded from the study. The study population comprised 499 patients: 264 girls and 235 boys. Their median age at surgery was 263 days. The age profile is illustrated in Figure 1Go. The spectrum of congenital heart defects is shown in Figure 2Go. Cardiac operations were performed under CPB in 373 patients (75%); 126 (25%) were closed heart procedures without CPB. Piperacillin was used for perioperative antibiotic prophylaxis in all cases during 1998, and cefazolin or cefuroxime was used in 1999. The first dose of antibiotic was administered in the operating room 30 to 60 min before surgery. In most cases, antibiotics were continued until chest tube removal. Patients were observed from surgery to discharge or death. Samples were taken for culture postoperatively when there were clinical indications of infection.



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  		Figure 1. Age profile in 499 patients.

 


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  		Figure 2. Congenital heart defects in 499 patients. AI = aortic insufficiency, AS = aortic stenosis, ASD = atrial septal defect, CoA = coarctation of the aorta, CAVC = common atrioventricular canal, DORV = double-outlet right ventricle, HAA = hypoplastic aortic arch, HLHS = hypoplastic left heart syndrome, PDA = patent ductus arteriosus, TGA = transposition of the great arteries, ToF = tetralogy of Fallot, UVH = univentricular heart, VSD = ventricular septal defect.

 
Microbiological culture was carried out according to current standard methods. Samples were cultured on Bactec media for aerobic, anaerobic and fungal cultures, and incubated at 35ºC in a Bactec 9120 device (Becton-Dickinson, Franklin Lakes, NJ, USA). Identification and antibiotic sensitivity evaluation with minimum inhibitory concentration values were performed on the Becton-Dickinson Sceptor system. The first positive culture of blood, bronchoalveolar lavage fluid, wound or central catheter samples postoperatively was the event of interest in Cox analysis, and a grouping variable for univariate analyses. Repeat cultures in the same patient were not included in the analyses. Only microbiological assays showing frequently occurring strains (Candida, Escherichia coli, Pseudomonas, Klebsiella pneumoniae, Staphylococcus aureus, Staphylococcus epidermidis) were considered; cultures indicating rare strains or evident contamination were excluded. The number of positive cultures was expressed as the nosocomially infected patient ratio (NIPR) which is the percentage of patients with nosocomial infection among all surgical patients.6

Independent variables for analysis included age, sex, pulmonary hypertension, body surface area (BSA), BSA to oxygenator surface area ratio (patient variables), and open/closed heart surgery, duration of operation, CPB time, intubation time, ICU stay (perioperative variables). For data analysis, the patients were divided into 4 age groups: neonates up to 30 days old, infants from 31 days to 1 year old, younger children (between 1 and 4 years), and older children (4 years and older). A numerical variable without a normal distribution was expressed as the median and range. The Mann-Whitney U test was applied to compare variables without a normal distribution. The chi-squared test was used for comparison of nominal variables. Univariate analysis was employed to compare variables in children with and without infection (according to grouping variable, positive culture). The dynamics of postoperative infection in patients treated under CPB was analyzed by the Cox proportional hazard model. Predictive variables were evaluated as well as the probability of freedom from a positive culture. The operation was the analysis starting point. Positive culture (complete observation), discharge, or death (incomplete observations) were the endpoints of the observation. Only time-independent variables significantly influencing the occurrence of a positive culture (evaluated in univariate analyses) were entered into the model. Variables for the Cox model were selected by backward stepwise elimination of independent variables to obtain the best model. The influence of predictive variables on the infection risk was expressed in terms of the odds ratio and 95% confidence interval. In all tests, a p-value less than 0.05 was considered statistically significant.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
There was at least one positive culture in 110 patients (NIPR, 22%). The number of positive cultures in each age group is shown in Figure 3Go. The distribution of positive cultures according to the type of congenital heart defect is illustrated in Figure 4Go. The highest percentage of patients with positive cultures was observed in the group with simple and complex transposition of the great arteries and Taussig-Bing double-outlet right ventricle. The results of univariate analyses of patient and perioperative variables are shown in Tables 1 and 2GoGo. The probability of freedom from a positive culture was estimated by entering the following variables in the Cox model: pulmonary hypertension, CPB time, and BSA to oxygenator surface area ratio. They were expressed in odds ratios, as presented in Table 3Go. Probability functions for means of predictive variables and for values expressing risk factors are shown in Figures 5 and 6GoGo.



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  		Figure 3. Positive microbiological cultures (shaded) according to age group.

 


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  		Figure 4. Positive microbiological cultures (shaded) according to congenital heart defect. AI = aortic insufficiency, AS = aortic stenosis, ASD = atrial septal defect, CoA = coarctation of the aorta, CAVC = common atrioventricular canal, DORV = double-outlet right ventricle, HLHS = hypoplastic left heart syndrome, PDA = patent ductus arteriosus, TGA = transposition of the great arteries, ToF = tetralogy of Fallot, UVH = univentricular heart, VSD = ventricular septal defect.

 

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  		Table 1. Univariate Analyses of Patient Variables
 

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  		Table 2. Univariate Analyses of Perioperative Variables
 

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  		Table 3. Predictive Variables of Cox Regression Model
 


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  		Figure 5. Probability function for mean values.

 


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  		Figure 6. Probability functions with 3 and no risk factors, according to the Cox regression model.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Microbiological culture is essential in the treatment of postoperative infections, usually confirming the clinical diagnosis and enabling appropriate therapy, in spite of the potential drawbacks of false negative results or false positives due to contamination.7 This test enabled quick and easy detection of postoperative infection after pediatric cardiac surgery, and it could be of great value when establishing new antibiotic prophylaxis protocols. The overall NIPR of 22% in this study was higher than results reported by Dagan and colleagues8 (15.8%) and Wessel and colleagues9 (17.8%, decreasing to 3.6% in 1983). Orita and colleagues10 found NIPR values of 17.4% for infants and 4.9% for children 1–15 years old. In our study, the NIPR also decreased in older patients, although still higher than other reports. Differences in operative and postoperative protocols, antibiotic prophylaxis, and ICU microbial flora may explain the discrepancies, as well as age and clinical status at operation.11–14 More than half of our patients were neonates and infants (frequently undergoing urgent surgery) compared to 27% to 35% in other studies.9 Pulmonary hypertension was diagnosed in 58 children and this was a predisposing factor for infection revealed in univariate and multivariate analyses. Higher NIPR values may be partly attributable to false positive cultures inconsistent with clinical findings, e.g., due to catheters and tracheal tubes colonized by the bacteria producing glycocalix.15,16

The number of patients with a positive culture varied with the type of heart defect and ranged from 0% for those with a patent ductus arteriosus, to 48.1% in cases of transposition of the great arteries or double-outlet right ventricle (undergoing an arterial switch procedure). Those with a patent ductus arteriosus were older children in whom surgical intervention was necessitated by difficulty with coil occlusion. After the arterial switch procedure, patients had prolonged invasive pressure monitoring and mechanical ventilation, resulting in longer ICU stay. The last 2 variables had a significant impact on infection risk as revealed in univariate analysis. Prolonged ICU stay is known to increase the risk of bacterial colonization and further infection.7 Patients with infections were also hospitalized significantly longer, as observed by others.1,7,17 It is important to minimize ICU stay by early removal of catheters and chest tubes.

Neonates and small infants are especially prone to the side effects of CPB because of low body weight and less BSA in relation to the oxygenator surface area. Small BSA and a lower ratio of BSA to oxygenator surface area were identified as infection risk factors in this study. This disproportion as well as long CPB time (complex heart defects) can cause massive depletion of complement factors that play a role in the anti-infective response, especially against gram-negative bacteria.19,18 Furthermore, this group of patients has low immunoglobulin levels because of immaturity of the immune system.20 The type of surgery per se (with or without CPB) did not significantly influence the incidence of infection; in both closed and open heart surgery, longer operative and CPB times predisposed to a positive culture, according to univariate analysis, although multivariate analysis showed CPB to be a rather weak risk factor. Whether CPB prolongation augments the effect of low BSA remains to be clarified. Pulmonary hypertension influenced postoperative infection according to univariate and multivariate analyses, which can be explained by the young age in this group and potential predisposition due to defects causing left-to-right shunting. Patients with pulmonary hypertension required longer intubation and ICU stay, adding to the risk factors.

This study was a preliminary evaluation of the frequency of nosocomial infection in a cardiac surgical ICU. A future prospective study with systematic bacteriological monitoring and clinical data evaluation would make further analysis more accurate. However, it could be concluded that postoperative infections affected mainly younger patients with low BSA and pulmonary hypertension, who tended to have longer ICU and intubation times.

Presented at the 15th Biennial Congress of the Association of Thoracic and Cardiovascular Surgeons of Asia, December 6–9, 2001, Mumbai, India.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

    Li LY, Wang SQ. Economic effects of nosocomial infections in cardiac surgery. J Hosp Infect 1990;16:339–41.[Medline]

    French GL, Shannon KP, Simmons N. Hospital outbreak of Klebsiella pneumoniae resistant to broad-spectrum cephalosporins and beta-lactam-beta-lactamase inhibitor combinations by hyperproduction of SHY-5 beta-lactamase. J Clin Microbiol 1996;34:358–63.[Abstract/Free Full Text]

    Walsh TJ, Hutchins GM. Postoperative Candida infections of the heart in children: clinicopathologic study of a continuing problem of diagnosis and therapy. J Pediatr Surg 1980;15:325–31.[Medline]

    Yau YC, de Nanassy J, Summerbell RC, Matlow AG, Richardson SE. Fungal sternal wound infection due to Curvularia lunate in a neonate with congenital heart disease: case report and review. Clin Infect Dis 1994;19:735–40.[Medline]

    Horan TC, Culver DH, Gaynes RP, Jarvis WR, Edwards JR, Reid CR. Nosocomial infections in surgical patients in the United States, January 1986-June 1992. National Nosocomial Infections Surveillance (NNIS) System. Infect Control Hosp Epidemiol 1993;14:73–80.[Medline]

    Pollock E, Ford-Jones EL, Corey M. Use of the pediatric risk of mortality score to predict nosocomial infection in a pediatric intensive care unit. Crit Care Med 1991;19:160–4.[Medline]

    Damen J, Van der Tweel I. Positive tip cultures and related risk factors associated with intravascular catheterization in pediatric cardiac patients. Crit Care Med 1988;16:221–8.[Medline]

    Dagan O, Cox PN, Ford-Jones L, Ponsonby J, Bohn DJ. Nosocomial infection following cardiovascular surgery: comparison of two periods, 1987 vs. 1992. Crit Care Med 1999;27:104–8.[Medline]

    Wessel A, Simon C, Regensburger D. Bacterial and fungal infections after cardiac surgery in children. Eur J Pediatr 1987;146:31–3.[Medline]

    Orita H, Shimanuki T, Fukasawa M. A clinical study of postoperative infections following open-heart surgery: occurrence and microbiological findings in 782 cases. Surg Today 1992;22:207–12.[Medline]

    Faden H. Prophylactic antibiotics in pediatric cardiovascular surgery. Current practices. Ann Thorac Surg 1981;31:211–3.[Abstract]

    Lee KR, Ring JC, Leggiadro RJ. Prophylactic antibiotic use in pediatric cardiovascular surgery: a survey of current practice. Pediatr Infect Dis 1995;14:267–9.

    Mehta G, Khanna SK, Trehan H, Gupta V. Postoperative infection in cardiac surgery: the influence of a change in prophylactic antibiotic regimen. J Hosp Infect 1990;15:353–62.[Medline]

    Wellens F, Pirlet M, Larbuisson R, De Meireleire F, De Somer P. Prophylaxis in cardiac surgery. A controlled randomized comparison between cefazolin and cefuroxime. Eur J Cardio-thorac Surg 1995;9:325–9.[Abstract]

    Nickel JC, Ruseska I, Wright JB, Costerton JW. Tobramycin resistance of Pseudomonas aeruginosa cells growing as biofilm on urinary catheter material. Antimicrob Agents Chemother 1985;27:619–24.[Abstract/Free Full Text]

    Waldvogel FA, Vaudaux PE, Pittel D, Lew PD. Perioperative antibiotic prophylaxis of wound and foreign body infections: microbial factors affecting efficacy. Rev Infect Dis 1991;10(Suppl 10):S782–9.

    Kollef MH, Sharpless L, Vlasnik J, Pasque C, Murphy D, Fraser VJ. The impact of nosocomial infections on patient outcomes following cardiac surgery. Chest 1997;112:666–75.[Abstract/Free Full Text]

    Tarnok A, Hambsch J, Emmrich F. Complement activation, cytokines and adhesion molecules in children undergoing cardiac surgery with or without cardiopulmonary bypass. Pediatr Cardiol 1999;20:113–25.[Medline]

    Wan S, LeClerc JL, Vincent JL. Inflammatory response to cardiopulmonary bypass: mechanisms involved and possible therapeutic strategies. Chest 1997;112:676–92.[Abstract/Free Full Text]

    Ballow M, Cates KL, Rowe JC, Goetz C, Desbonnet C. Development of the immune system in very low birth weight (less than 1,500g) premature infants: concentration of plasma immunoglobulins and pattern of infection. Pediatr Res 1988;112:278–83.




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