Risk factors for early secondary infections after cardiopulmonary bypass in children with congenital heart disease: a single-center analysis of 265 cases
Introduction
Congenital heart disease (CHD) is the most common type of birth defect in Western countries, affecting approximately 10 per 1,000 newborns (1). In China, CHD is the leading birth defect across numerous provinces and regions, with reported detection rates ranging from 2.9 to 16.0 per 1,000 live births (2). Direct cardiac surgery with cardiopulmonary bypass (CPB) is a pivotal therapeutic modality for the majority of CHDs and represents the sole treatment option for complex CHDs. Annually, approximately 25,000 children in China require open-heart surgical intervention for CHD under CPB (3). During open-heart surgery with CPB, children are susceptible to a cytokine storm due to factors including hypothermia, aortic clamping, surgical trauma, and myocardial and pulmonary ischemia/reperfusion, which collectively impair immune function (4). In addition, invasive postoperative treatments such as mechanical ventilation, central venous catheterization, pericardial and thoracic drainage, and urinary catheterization heighten the risk of secondary infections in the early postoperative phases. The reported incidence of secondary infections following surgical intervention for CHD in children ranges from 15% to 38.9%, with pulmonary infections, surgical site infections, and bloodstream infections being the most prevalent types (5,6). Postoperative secondary infections are associated with increased treatment costs and mortality rates in pediatric patients (7,8). Thus, mitigating the risk of early secondary infections in children after CHD surgery with CPB is a critical clinical task. Our present study was designed to inform the clinical efforts in this area. We present this article in accordance with the STROBE reporting checklist (available at https://tp.amegroups.com/article/view/10.21037/tp-2024-575/rc).
Methods
Participants
Pediatric patients diagnosed with CHD and treated with open-heart surgery under CPB at the First Affiliated Hospital of Guangxi Medical University between July 2020 and June 2023 were enrolled and divided into infected and non-infected groups according to the infection status within seven days after surgery.
The inclusion criteria were as follows: (I) aged >28 days but younger than 18 years; (II) children diagnosed with CHD and received open-heart correction surgery utilizing CPB; and (III) without evidence of active infection within one week preceding the surgical procedure. The exclusion criteria were as follows: (I) children who died within 24 hours following surgery; (II) preoperative presence of hepatic and renal insufficiency, or with a prior history of thyroid disorders, autoimmune diseases, or malignancies; and (III) with incomplete medical records. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). This study was approved by the Medical Ethics Committee of the First Affiliated Hospital of Guangxi Medical University (No. 2023-E630-01). Individual consent for this retrospective analysis was waived.
Variables
The following variables were collected: gender, age, body weight, preoperative hospital stay (days), total hospital stay (days), preoperative New York Heart Association (NYHA) functional status, preoperative and postoperative serum albumin levels, degree of preoperative pulmonary arterial hypertension (PAH) (9), preoperative and postoperative left ventricular ejection fraction (LVEF), preoperative and postoperative comorbidities and anemia status, CHD type, American Society of Anesthesiologists (ASA) physical status, Risk Adjustment for Congenital Heart Surgery (RACHS) score, operative time, duration of CPB, aortic cross-clamping (ACC) time, duration of postoperative mechanical ventilation, length of postoperative intensive care unit (ICU) stay, total duration of postoperative drainage tube placement, duration of postoperative indwelling urinary catheter use, incidence of postoperative arrhythmias and low cardiac output syndrome (LCOS).
Definitions
Infection was defined as the presence of symptoms, signs or imaging findings of infection and evidence of microbiological infection, and positive culture of blood or other specimens, according to the diagnostic criteria of nosocomial infection issued by the Ministry of Health of China (10).
Preoperative medication and extracorporeal circulation
All pediatric patients received prophylactic antibiotics before surgery to reduce the risk of infection. The preferred antibiotics were cefovecin or cefazolin, with clindamycin used as an alternative for those allergic to cephalosporins. A single intravenous dose was administered 30 minutes prior to the procedure. During surgery, hypothermic CPB was utilized, with the priming solution mainly composed of colloids, and red blood cell suspension was added minimally to avoid excessive hemodilution. Myocardial protection was provided by antegrade delivery at the aortic root, using either St. Thomas’ Hospital cardioplegia solution or histidine-tryptophan-ketoglutarate (HTK) solution.
Statistical analyses
All data processing was conducted using the software SPSS 26.0 (IBM Corp., Armonk, NY, USA). The normality of all continuous variables was assessed using the Shapiro-Wilk test, among which the normally distributed continuous variables were described using mean ± standard deviation (SD), and their univariate analyses were based on Student’s t-test. For continuous variables that did not conform to a normal distribution, median and interquartile range (IQR) were used for description, with the Wilcoxon rank-sum test applied for univariate analyses. Categorical variables were characterized by frequency (percentage), denoted as n (%), for which the Chi-squared test was utilized for univariate analyses. Variables with a P value of less than 0.1 in the univariate analyses were included as independent variables in the multivariate model, and multivariate binary logistic regression analysis was employed to identify independent risk factors for early secondary infections following CPB for CHD in pediatric patients.
Results
General information
The study cohort comprised a total of 265 cases, with 118 cases (44.5%) in the infected group and 147 (55.5%) in the non-infected group. The distribution of CHD types is presented in Table 1. There were 137 males (51.7%) and 128 females (48.3%), with a median age of 56 months (IQR, 33.5–95.5 months). Of the total cases, 29.8% (n=79) were infants, 35.1% (n=93) were preschoolers, 24.5% (n=65) were school-aged, and 10.6% (n=28) were adolescents (Table 2). The median body weight was 16.0 kg (IQR, 11.6–22.0 kg). Six patients (2.3%) abandoned treatment or died postoperatively, all of whom were members of the infected group.
Table 1
| Congenital heart disease types | N (%) |
|---|---|
| Ventricular septal defect | 117 (44.2) |
| Atrial septal defect | 76 (28.7) |
| Tetralogy of Fallot | 10 (3.8) |
| Complete or partial endocardial cushion defect | 10 (3.8) |
| Coronary artery anomalies | 9 (3.4) |
| Aortic valve malformation with or without stenosis | 8 (3.0) |
| Right ventricular outflow tract or pulmonary valve stenosis | 6 (2.3) |
| Severe mitral or tricuspid valve regurgitation | 5 (1.9) |
| Cor triatriatum | 4 (1.5) |
| Others (including total anomalous venous drainage, aortic arch dissection, Ebstein’s anomaly, double-outlet right ventricle, etc.) | 20 (7.5) |
Table 2
| Age groups | N (%) |
|---|---|
| Infants | 79 (29.8) |
| Preschoolers | 93 (35.1) |
| School-aged children | 65 (24.5) |
| Adolescents | 28 (10.6) |
Types and pathogen spectrum of early secondary infections after CPB
In the infected group (n=118), the median time to symptom onset of secondary infections was 17.0 hours (IQR, 12.0–21.5 hours). The infection types included lung infection alone (n=88, 74.6%), pulmonary infection complicated by sepsis (n=26, 22.0%), sepsis alone (n=3, 2.5%), and pulmonary infection co-occurring with urinary tract infection (n=1, 0.8%). A total of 22 pathogenic strains were isolated from the respiratory secretions of 20 children in the infected group, with two distinct pathogenic strains detected in three children. Among the 22 isolated strains, Gram-negative bacteria predominated (n=14, 63.6%), followed by fungi (n=7, 31.8%) and Gram-positive bacteria (n=1, 4.5%) (Figure 1). Stool cultures were positive for Candida albicans in two children.
Univariate analysis of risk factors for early secondary infections after CPB
Children in the infected group were younger and had a lower body weight. They also had a longer preoperative hospital stay, higher proportions of no shunt and right-to-left shunt, higher NYHA class, more severe preoperative pulmonary hypertension, higher proportion of children with underlying diseases, and higher ASA class, along with significantly longer duration of ACC, CPB, surgical procedure, postoperative mechanical ventilation, postoperative ICU stay, postoperative drainage tube placement, and postoperative urethral catheterization. Furthermore, the incidence rates of postoperative arrhythmias and LCOS were also significantly higher in the infected group (all P<0.05) (Tables 3-6).
Table 3
| Item | Total (n=265) | Infected group (n=118) | Non-infected group (n=147) | Z/χ2 | P value |
|---|---|---|---|---|---|
| Gender | 0.244 | 0.62 | |||
| Male | 137 (51.7) | 63 (53.4) | 74 (50.3) | ||
| Female | 128 (48.3) | 55 (46.6) | 73 (49.7) | ||
| Age (months) | 56 (33.5–95.5) | 40.5 (24.0–77.8) | 66.0 (43.0–110.0) | −4.253 | <0.001 |
| Body weight (kg) | 16.0 (11.6–22.0) | 13.0 (9.7–19.0) | 17.7 (13.5–25.0) | −4.609 | <0.001 |
All the continuous data are non-normally distributed and are presented using median (interquartile range); categorical variables are described using number (percentage).
Table 4
| Item | Total (n=265) | Infected group (n=118) | Non-infected group (n=147) | Z/χ2 | P value |
|---|---|---|---|---|---|
| Length of hospital stay prior to surgery (days) | 6.0 (4.0–8.0) | 7.0 (5.0–9.0) | 6.0 (4.0–7.0) | −3.391 | <0.001 |
| Type of congenital heart disease | 24.453 | <0.001 | |||
| No shunt | 29 (10.9) | 19 (16.1) | 10 (6.8) | ||
| Left-to-right shunt | 220 (83.0) | 84 (71.2) | 136 (92.5) | ||
| Right-to-left shunt | 16 (6.0) | 15 (12.7) | 1 (0.7) | ||
| Preoperative cardiac function (NYHA class) | −5.036 | <0.001 | |||
| I | 181 (68.3) | 63 (53.4) | 118 (80.3) | ||
| II | 54 (20.4) | 30 (25.4) | 24 (16.3) | ||
| III | 29 (10.9) | 24 (20.3) | 5 (3.4) | ||
| IV | 1 (0.4) | 1 (0.8) | 0 | ||
| Preoperative left ventricular ejection fraction (%) | 70.0 (66.6–73.0) | 69.0 (65.0–73.0) | 70.0 (67.0–73.0) | −1.389 | 0.16 |
| Preoperative pulmonary hypertension | 41.265 | <0.001 | |||
| None | 137 (51.7) | 37 (31.4) | 100 (68.0) | ||
| Mild | 25 (9.4) | 21 (17.8) | 4 (2.7) | ||
| Moderate | 60 (22.6) | 33 (28.0) | 27 (18.4) | ||
| Severe | 43 (16.2) | 27 (22.9) | 16 (10.9) | ||
| Preoperative underlying disease | 10.086 | 0.001 | |||
| Yes | 69 (26.0) | 42 (35.6) | 27 (18.4) | ||
| None | 196 (74.0) | 76 (64.4) | 120 (81.6) | ||
| Preoperative anemia | 0.417 | 0.52 | |||
| Yes | 45 (17.0) | 22 (18.6) | 23 (15.6) | ||
| None | 220 (83.0) | 96 (81.4) | 124 (84.4) | ||
| Preoperative albumin (g/L) | 41.80 (39.4–44.5) | 41.75 (39.0–44.5) | 41.80 (39.6–44.5) | −0.443 | 0.66 |
All continuous data are non-normally distributed and are presented using median (interquartile range); categorical variables are described using number (percentage). NYHA, New York Heart Association.
Table 5
| Item | Total (n=265) | Infected group (n=118) | Non-infected group (n=147) | Z/χ2 | P value |
|---|---|---|---|---|---|
| Anesthesia status (ASA class) | 18.457 | <0.001 | |||
| 1–2 | 122 (46.0) | 37 (31.4) | 85 (57.8) | ||
| 3–6 | 143 (54.0) | 81 (68.6) | 62 (42.2) | ||
| Risk-adjusted Classification for Congenital Heart Surgery score | 0.574 | 0.45 | |||
| 1–2 | 29 (10.9) | 11 (9.3) | 18 (12.2) | ||
| 3–6 | 236 (89.1) | 107 (90.7) | 129 (87.8) | ||
| Duration of ACC (min) | 62.0 (0.0–93.0) | 81.5 (51.8–117.3) | 46.0 (0.0–9.0) | −6.134 | <0.001 |
| Duration of CPB (min) | 100.0 (72.0–130.5) | 113.0 (91.5–157.8) | 87.0 (60.0–115.0) | −5.963 | <0.001 |
| Operative time (min) | 270.0 (230.0–323.0) | 297.0 (258.5–346.3) | 260.0 (211.0–296.0) | −5.097 | <0.001 |
Continuous data are non-normally distributed and are presented using median (interquartile range); categorical variables are described using number (percentage). ACC, aortic cross-clamping; CPB, cardiopulmonary bypass; ASA, American Society of Anesthesiologists.
Table 6
| Item | Total (n=265) | Infected group (n=118) | Non-infected group (n=147) | Z/χ2 | P value |
|---|---|---|---|---|---|
| Length of postoperative mechanical ventilation (hours) | 12.8 (7.9–37.0) | 43.8 (15.2–134.5) | 9.0 (6.1–12.8) | −10.728 | <0.001 |
| Length of postoperative intensive care unit stay (hours) | 21.0 (15.0–86.0) | 100.3 (35.3–188.1) | 17.0 (13.0–21.0) | −10.359 | <0.001 |
| Total duration of postoperative drain indwelling (hours) | 62.0 (53.5–100.3) | 96.25 (61.0–157.9) | 58.00 (44.5–63.0) | −8.470 | <0.001 |
| Postoperative duration of indwelling catheter (hours) | 31.0 (17.8–69.8) | 69.75 (37.9–144.9) | 20.0 (14.50–28.5) | −10.758 | <0.001 |
| Postoperative left ventricular ejection fraction (%) | 67.0 (63.0–71.0) | 67.0 (62.0–72.0) | 67.0 (63.0–71.0) | −0.048 | 0.96 |
| Serum albumin concentration (g/L) on the first postoperative day | 42.2 (39.4–45.5) | 41.70 (39.5–44.5) | 42.80 (39.3–45.9) | −1.351 | 0.18 |
| Postoperative arrhythmias | 5.808 | 0.02 | |||
| Yes | 13 (4.9) | 10 (8.5) | 3 (2.0) | ||
| None | 252 (95.1) | 108 (91.5) | 144 (98.0) | ||
| Postoperative LCOS | 35.913 | <0.001 | |||
| Yes | 26 (9.8) | 26 (22.0) | 0 | ||
| None | 239 (90.2) | 92 (78.0) | 147 (100.0) |
Continuous data are non-normally distributed and are presented using median (interquartile range); categorical variables are described using number (percentage). LCOS, low cardiac output syndrome.
Results of multivariate analysis
Variables that were statistically significant in the univariate analyses were incorporated into the multivariate logistic regression model. The results indicated that age, preoperative NYHA class, preoperative pulmonary hypertension, ASA class, operative time, and duration of ACC were independent risk factors for early secondary infections following CHD surgery with CPB in pediatric patients (Table 7).
Table 7
| Item | B | SE | Wald | OR (95% CI) | P value |
|---|---|---|---|---|---|
| Age | −0.022 | 0.004 | 25.107 | 0.979 (0.970–0.987) | <0.001 |
| Preoperative cardiac function (NYHA class) | 0.628 | 0.278 | 5.119 | 1.874 (1.088–3.229) | 0.02 |
| Preoperative pulmonary hypertension | |||||
| None | 44.586 | <0.001 | |||
| Mild | 2.920 | 0.522 | 31.313 | 18.541 (6.667–51.559) | <0.001 |
| Moderate | 2.260 | 0.452 | 24.979 | 9.582 (3.950–23.245) | <0.001 |
| Severe | 3.493 | 0.859 | 16.529 | 32.887 (6.105–177.157) | <0.001 |
| Anesthesia status (ASA class) | |||||
| ≤2 | 10.297 | <0.001 | |||
| ≥3 | 0.773 | 0.349 | 4.908 | 2.166 (1.093–4.290) | 0.03 |
| Operative time | 0.007 | 0.003 | 6.106 | 1.007 (1.001–1.012) | 0.01 |
| Duration of ACC | 0.017 | 0.005 | 14.095 | 1.017 (1.008–1.026) | <0.001 |
SE, standard error; OR, odds ratio; CI, confidence interval; NYHA, New York Heart Association; ASA, American Society of Anesthesiologists; ACC, aortic cross-clamping.
Discussion
The survival rate for infants with CHD has increased over the past three decades, from 67.4% to the current rate of 82.5%. However, in 2017, approximately 180,000 children died from CHD and its related complications (11). It was found that the mortality rate among children with postoperative secondary infections was three-fold higher than that in those without infection, and postoperative secondary infection was identified as the primary independent risk factor for mortality within 1 week following a CHD surgery (8). Hence, minimizing postoperative secondary infections has become a key clinical priority.
Recent research has demonstrated that the incidence of postoperative secondary infections in CHD children is comparable in China and internationally, ranging from 15% to 38.9% in Europe and North America (5,6) and 11.1% to 37.5% in China (12,13). Our study indicated that age at the time of surgery was an independent risk factor for secondary infection in the early postoperative phase, which may be explained by the fact that younger children have relatively lower body weights, a diminished capacity to withstand physiological stress, and underdeveloped immune function and organs. Furthermore, previous research demonstrated that a younger age at the time of surgery, as well as prolonged postoperative dependence on mechanical ventilation and an extended length of ICU stay, was associated with an extended recovery time (14). Nevertheless, the optimal age for surgical intervention warrants further investigations. A multitude of factors, including the CHD type, cardiopulmonary function, growth and development status, and nutrition, need to be considered before developing an individualized treatment protocol (15). Although the NYHA classification system is limited by its high subjectivity and low reproducibility, its benefits—such as non-invasiveness, simplicity, and high speed—have led to its widespread application in numerous guidelines and studies (16,17). In our study, higher NYHA class was associated with higher risk of secondary infection following open-heart surgical procedures with CPB for CHD. Those with higher NYHA functional classes require a greater diversity and higher doses of vasoactive medications to support cardiac function and increased ventilator settings to maintain adequate oxygenation, which lead to an extended period of mechanical ventilation and an increased duration of ICU stay (18). Our study revealed that the severity of preoperative PAH in CHD children was an independent risk factor for the development of secondary infections after CPB. Furthermore, children with severe PAH exhibited the greatest risk of postoperative secondary infections, consistent with previous study (19). One possible explanation is that PAH increases to varying degrees after CPB (20), leading to an increase in pulmonary vascular hydrostatic pressures. In addition, CPB-induced lung injury and inflammatory cytokine storm increase the risk of postoperative infection and the duration of mechanical ventilation (21). The severity of preoperative PAH has been closely associated with the risk of postoperative arrhythmias and LCOS (22), consistent with our findings. To mitigate the risk of postoperative secondary infections in children with CHD-PAH, adequate preoperative assessment of the pulmonary vascular status is crucial for determining the optimal surgical timing and developing appropriate surgical protocols; additionally, the rational use of pharmacotherapy to lower pulmonary artery pressure is essential (23). Our study revealed that an ASA class of ≥3 constituted an independent risk factor for secondary infections in pediatric patients following surgical procedures. Vo et al. (24) found that the incidence of postoperative complications was significantly higher in children with a preoperative ASA class 3, which was also an independent risk factor for unplanned hospital readmission within 30 days following surgery. Tao et al. (25) discovered a robust association between ASA class and the incidence of perioperative respiratory adverse events in pediatric patients under general anesthesia, confirming that an elevated ASA class was positively associated with an increased risk of respiratory complications. These patients typically exhibit a diminished preoperative physical status, a reduced capacity to withstand physiological stress, inadequate compensatory mechanisms, and a lower tolerance for anesthesia. Consequently, these patients are at a heightened risk for secondary infections after CPB. The duration of ACC was significantly longer in children with secondary infections following surgery for CHD compared to the non-infected cohort (26). Consequently, an extended duration of surgery and ACC is associated with an increased risk of postoperative infections. In our current study, multivariate logistic regression analysis revealed that both the operative time and the duration of ACC were independent risk factors for postoperative secondary infections, aligning with the previously mentioned findings.
In summary, selecting the optimal timing for surgical intervention, maintaining normal preoperative organ function, and proactively managing pulmonary hypertension preoperatively are key strategies that can decrease the risk of early postoperative secondary infections in children undergoing CHD surgery with CPB. Furthermore, reducing the duration of surgery and ACC is also a valuable consideration. Nevertheless, our study had limitations, including a small sample size, limited indicators, and potential biases due to its single-center, retrospective design. To improve reliability, we plan to expand the sample size through collaboration with other centers.
Conclusions
In our study, younger surgical age, higher preoperative NYHA class, severe preoperative pulmonary hypertension, ASA grade ≥3, prolonged ACC and operative time are independent risk factors for the development of early secondary infections in CHD children after CPB.
Acknowledgments
Funding: This work was supported by
Footnote
Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://tp.amegroups.com/article/view/10.21037/tp-2024-575/rc
Data Sharing Statement: Available at https://tp.amegroups.com/article/view/10.21037/tp-2024-575/dss
Peer Review File: Available at https://tp.amegroups.com/article/view/10.21037/tp-2024-575/prf
Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://tp.amegroups.com/article/view/10.21037/tp-2024-575/coif). The authors have no conflicts of interest to declare.
Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). This study was approved by the Medical Ethics Committee of the First Affiliated Hospital of Guangxi Medical University (approval No. 2023-E630-01). Individual consent for this retrospective analysis was waived.
Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.
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