Delayed Sternal Closure Following Complex Cardiac Surgery in Neonates

Abstract

Background

Delayed sternal closure (DSC) is a well-established management strategy following complex congenital cardiac surgery that is used to mitigate postoperative hemodynamic and respiratory instability. It is mostly used in neonates requiring prolonged cardiopulmonary bypass (CPB), long aortic cross-clamp times, or deep hypothermic circulatory arrest who are predisposed to myocardial edema or bleeding. Our study evaluates morbidity and mortality after DSC in neonates including superficial and deep sternal wound infections, along with requirement for surgical debridement.

Methods

Retrospective review of neonates who underwent DSC after cardiac surgery at a single center from 2015 to 2021.

Results

A total of 187 neonates were identified. Mean age and weight were 12.8 ± 6.8 days and 3.3 ± 0.5 kg, respectively. Mean days of open chest were 3.8 ± 5.8 days. Two neonates (1.07%) required sternal wound debridement, while 19 cases (10.2%) had superficial wound infections. Mean intensive care unit (ICU) and hospital stay were 12.8 ± 16.6 and 25.9 ± 36.9 days, respectively; 30-day mortality occurred in nine of 187 cases (4.8%). Univariate analysis indicated that DSC days (P = .01), extracorporeal membrane oxygenation (ECMO) (P = .000), aortic cross clamp time (P = .007), and CPB time (P = .006) were associated with 30-day mortality, while in multivariable analysis, only ECMO was significant (P = .002). Risk Adjustment for Congenital Heart Surgery (RACHS-1) score was the only independent risk factor for sternal wound infection in univariate analysis (P = .019) and multivariable analysis (P = .05).

Conclusion

Delayed sternal closure is a safe therapeutic option following complex neonatal cardiac surgery, where cardiac compression by sternal approximation is not tolerated due to myocardial edema, hemodynamic instability, or coagulopathy. Higher RACHS-1 score was associated with a greater incidence of sternal wound infections.

Keywords

delayed sternal closure congenital cardiac surgery sternal wound infection neonatal cardiac surgery

Introduction

Delayed sternal closure (DSC) is a widely recognized mangement strategy aimed at mitigating postoperative hemodynamic and respiratory instability in pediatric patients following complex cardiac surgery.¹ Approximately 10% of pediatric cardiac patients leave the operating room with an open chest, with subsequent sternal closure performed after an average duration of three days.^2–4

DSC is most frequently indicated in complex cases involving prolonged cardiopulmonary bypass and aortic cross-clamp time, which can potentially lead to intraoperative bleeding and myocardial edema.⁵ In such circumstances, sternal closure can trigger hemodynamic instability with a reduction in cardiac output and diastolic filling.⁵ DSC can improve morbidity and mortality for patients following complex pediatric cardiac operations, by preventing the onset of hemodynamic instability.

However, DSC may predispose patients to sternal wound infections (SWI) and mediastinitis.^6–9 Sternal wound infections can be categorized into two types: superficial SWIs, managed conservatively with antibiotics, and deep SWIs which require surgical debridement. Albeit rare, severe complications such as sepsis, can be life-threatening.⁶ Moreover, mortality rates in this critically ill patient subgroup vary considerably, ranging from 8% to as high as 34%.^1–6

Considering the pros and cons of DSC, a lack of consensus exists within the literature concerning the indication for or timing of sternal closure in these patients. Moreover, different clinical series report variable morbidity and mortality rates associated with this procedure. A prevalence of 3.5% to 18.0% for SWIs following delayed sternal closure has been documented in the literature.^2–4,6–15 This retrospective review aims to evaluate the morbidity and mortality following delayed sternal closure in the neonatal population, focusing on the occurrence of superficial and deep SWIs and the requirement of surgical debridement.

Materials and Methods

Study Design and Patient Population

This study has been approved by Liverpool John Moores University Ethical committee (UREC reference number: 25/NAP/001). A retrospective data collection was performed for neonates who underwent DSC following congenital cardiac surgery via sternotomy from 2015 to 2021, at Alder Hey Children's Hospital, Liverpool, United Kingdom. Patients who were over 28 days of age and patients with incomplete data were excluded.

Variables including indication of DSC, time to sternal closure, mean pediatric intensive care unit, hospital stay duration, superficial and deep wound infections, 30-day mortality, sepsis and surgical risk according to the Risk Adjustment for Congenital Heart Surgery (RACHS-1) score, need for extracorporeal membrane oxygenation (ECMO) were extracted from our database. Data related to the incidence of SWI, surgical intervention, and 30-day mortality were double-checked by another author.

Endpoints

The primary endpoints of this study were the superficial and deep SWI and mediastinitis rates with the need for sternal wound debridement rate. Superficial SWIs were defined as inflammatory changes confirmed with wound swabs. Deep SWIs were confirmed if the muscular layers were affected. Mediastinitis is defined as a positive pathogen identified by culture swabs affecting the mediastinum and the sternum. Secondary endpoints involved evaluating associated morbidity such as sepsis, intensive cares unit (ICU) stay, hospital stay duration, and 30-day mortality rates.

Indication for Delayed Sternal Closure

The decision to delay sternal closure is determined preoperatively for operations such as the arterial switch operation (ASO) for transposition of the great arteries (TGA) and the Norwood procedure for hypoplastic left heart syndrome. In other instances, it is decided intraoperatively in case of myocardial edema and myocardial distention from a variety of clinical conditions such as low cardiac output, arrhythmias, and respiratory failure needing high ventilation pressures. Coagulopathy with the need to leave the chest packed with swabs is a further indication or in patients with postoperative circulatory support through central ECMO. Also, we adopt the DSC policy in the case of pulmonary artery banding (PAB) for single ventricle circulation and in certain case of septal defects (multiple ventricular septal defects [VSDs], apical VSD, or complete atrioventricular septal defect [AVSD] not amenable to closure in conjunction with hypoplastic aortic arch [HAA] repair under circulatory arrest). In such cases we have experienced that the PAB will often require further adjustments in the first few days after surgery. We use intravenous (IV) cefuroximecephalosporin) during the duration of an open chest, and we continue it for two doses after chest closure. In case of cephalosporin or penicillin allergy, we use IV teicoplanin plus IV gentamicin as an alternative to cefuroxime and we continue using them for two doses after chest closure.

Surgical Techniques

Our approach to open chest treatment encompasses various techniques depending on the surgeon's preference. In patients who were placed on ECMO, we utilize a silastic membrane that is sutured to the skin with continuous 5/0 polypropylene sutures, then we further cover it with two layers of antimicrobial drape (Ioban 3 M).

In non-ECMO patients we utilize different techniques based on the individual surgeon's preference which can be:

Silastic membrane that is sutured to the skin with continuous 5/0 polypropylene sutures and covered with two layers of antimicrobial drape (Ioban 3 M).

Direct skin closure using subcuticular monocryl sutures, leaving the sternal edges open, then covering the wound with sterile dressing.

Sterile dressings over a small-sized swab left in the chest.

Antimicrobial drape (Ioban 3 M) alone over the open chest with one small swab left inside the chest.

A few cases required the use of a sternal bridge to keep the sternal edges apart with a piece of chest tube drain sutured to the sternal edges to prevent compression of the heart or a right ventricle to pulmonary artery (RV-PA) conduit. Then, a silastic membrane is sutured to the skin edges covered by a sterile dressing.

Upon chest closure, any dressing is removed in a sterile fashion. To expose the sternum we remove retained swabs, use a mediastinal cavity washout with warm saline solution, followed by standard median sternotomy closure in layers using 2/0 PDS for the sternum, 3/0 vicryl for the muscle and subcutaneous layers, and 5/0 monocryl for subcuticular skin closure. We do all our chest closures in the ICU including those who need weaning from ECMO and decannulation. We do not use routinely use Gore-Tex membrane to cover the heart. However, in cases where the heart or great vessels need to be covered, suturing an ePTFE 0.1 mm membrane (Gore-Tex) to the pericardial edges with polypropylene 5/0 interrupted sutures is done at the time of chest closure in the ICU.

Regarding the Patients who had Surgical Wound Infections

Out of the two cases that required wound revision and debridement in the operating room, the first patient exhibited sternal dehiscence on examination and had positive mediastinal wound swab cultures. The second patient developed signs of a deep SWI, characterized by a high C-reactive protein, pyrexia, positive blood cultures and chest swab cultures, as well as purulent material on swabs covering the midline sternotomy incision with sternal dehiscence.

However, in cases of superficial wound infection, we managed this conservatively with antibiotics based on the culture and sensitivity results and regular dressings. If the baby needed frequent dressing change because of superficial discharge, we tend to use PICO negative pressure wound dressing and we change it every 5 to 7 days.

Statistical Analysis

Categorical data were reported as frequencies and proportions. Mean and standard deviation were used to express quantitative data. Univariate and multivariable regression analyses were conducted to identify risk factors for SWI and 30-day mortality. The level of significance was considered at P value < .05. Statistical analyses were conducted with SPSS Version 27.0 (SBSS Inc).

Results

Demographic Data

Over a 6-year period, 1896 patients were identified and screened of which 187 neonates were included in our patient cohort. Mean age and weight at operation were 12.8 ± 6.8 days and 3.3 ± 0.5 kg, respectively. Mean aortic cross clamp time and CPB time were 102.8 ± 52.5 and 183 ± 81 min, respectively. Mean RACHS-1 Score was 4 ± 1.05. The arterial switch operation, with or without VSD repair was performed in 70/187 (37.4%) patients, HAA repair in 49/187 (26.2%), and the Norwood operation in 30/187 (16.0%). These operations comprised the most frequent procedures performed in the DSC cohort as depicted in Figure 1.

Mean days of open chest were 3.8 ± 5.8 days. Only 2/187 patients (1.07%) needed sternal wound debridement in the operating room for deep SWI, while 19/187 cases (10.2%) had superficial wound infections managed conservatively with antibiotics. Mean days of wound infection were 10.76 ± 6.65 days, and the two patients who needed wound revision and debridement were at the seventh and 17th day after chest closure.

Mean ICU and hospital stay were 12.8 ± 16.6 and 25.9 ± 36.9 days, respectively. Preoperative ECMO was required in 1/187 neonate (0.5%). Intraoperative ECMO was required in 6/187 cases (3.2%), while 21/187 patients (11.2%) needed postoperative ECMO; 52/187 cases (27.8%) required further chest explorations; 30-day hospital mortality occurred in nine of 187 cases (4.8%); 24/187 neonates (12.8%) developed sepsis within 30 days of primary operation. Demographic data have been summarized in Table 1.

Table 1.

Demographic Data.

Variables	All cases (n = 187)
Age at operation in days (mean, SD)	12.86 ± 6.45
Female gender (N, %)	59 (31.6%)
RACHS-1 score (mean, SD)	4 ± 1.05
Weight at surgery in kg (mean, SD)	3.33 ± 0.48
ICU stay in days (mean, SD)	12.75 ± 16.57
Hospital stay in days (mean, SD)	25.93 ± 36.88
Time to DSC in days (mean, SD)	3.81 ± 5.80
Preoperative ECMO (N, %)	1 (0.5%)
Operative ECMO (N, %)	6 (3.2%)
Postoperative ECMO (N, %)	21 (11.2%)
Cardiopulmonary bypass time in minutes (mean, SD)	183.1 ± 80.94
Aortic cross clamp time in minutes (mean, SD)	102.75 ± 52.50
30-day mortality (N, %)	9 (4.8%)
Sepsis (N, %)	24 (12.8%)
Chest explorations (N, %)	52 (27.8%)

Abbreviations: DSC, delayed sternal closure; ECMO, extracorporeal membrane oxygenation; ICU, intensive care unit; RACHS-1, Risk Adjustment for Congenital Heart Surgery.

Regression Analysis

Univariate regression analysis showed that the RACHS-1 score (P = .019, 95% CI −0.047 to 0.178) was found to be significantly associated with SWI as described in Table 2. Furthermore, DSC days (P = .011, 95% CI −0.19 to −0.003), ECMO (P = .000, 95% CI 0.251-0.465), aortic cross clamp time (P = .007, 95% CI 0.000-0.003), and CPB time (P = .006, 95% CI −0.002 to 0.000) were found to be significantly associated with 30-day mortality, in the univariate regression analysis, which has been depicted in Table 3.

Table 2.

Univariate Logistic Regression Analysis for Dependent Variable, Sternal Wound Infections.^a

Variables	P value	95% CI
Age at operation (days)	.139	−0.006 to 0.007
Sex	.168	−0.156 to 0.027
Weight at operation	.462	−0.129 to 0.059
ICU days	.987	−0.003 to 0.003
DSC days	.074	−0.025 to 0.001
ECMO	.299	−0.248 to 0.077
RACHS-1 (surgical risk score)	. 019	0.009 to 0.101
Aortic cross clamp time	.388	−0.003 to 0.001
CPB time	.07	0.000 to 0.003
Number of chest explorations	.251	−0.047 to 0.178

Abbreviations: CI, confidence interval; CPB, cardiopulmonary bypass; DSC, delayed sternal closure; ECMO, extracorporeal membrane oxygenation; ICU, intensive care unit; RACHS-1, Risk Adjustment for Congenital Heart Surgery.

Bold values show statistical significance (P < .05).

Table 3.

Univariate Logistic Regression Analysis for Dependent Variable, 30-Day Mortality Rate.^a

Variables	P value	95% CI
Age at operation (days)	.583	−0.005 to 0.003
Sex	.833	−0.067 to 0.054
Operative weight	.845	−0.068 to 0.056
ICU days	.207	−0.003 to 0.001
DSC days	. 011	−0.019 to −0.003
ECMO	.000	0.251 to 0.465
RACHS-1 (surgical risk score)	.665	−0.037 to 0.024
Aortic cross clamp time	.007	0.000 to 0.003
CPB time	.006	−0.002 to 0.000
Number of chest explorations	.215	−0.027 to 0.121

Bold values show statistical significance (P < .05).

On multivariate analysis, the RACHS-1 score was found to be the one significant independent risk factor for SWI, P = .05, 95% CI 0.995-4.012, as described in Table 4. In addition, ECMO was found to be the sole significant risk factor for 30-day mortality, (P = .002, 95% CI 0.000-0.122). Multivariate analysis for 30-day mortality is shown in Table 5.

Table 4.

Multivariable Logistic Regression Analysis for Risk Factors of Sternal Wound Infections Among Neonates Undergoing DSC Post Cardiac Surgery.^a

Variables	P value	95% CI
Age at operation (days)	.722	0.925 to 1.120
Sex	.237	0.607 to 7.533
Weight at operation	.49	0.158 to 2.417
ICU days	.82	0.964 to 1.048
DSC days	.211	0.768 to 1.060
ECMO	.232	0.450 to 26.953
RACHS-1 (surgical risk score)	. 05	0.995 to 4.012
Aortic cross clamp time	.536	0.972 to 1.015
CPB time	.165	0.995 to 1.030
Number of chest explorations	.347	0.526 to 6.210

Bold values show statistical significance (P < .05).

Table 5.

Multivariable Logistic Regression Analysis for Risk Factors of 30-Day Mortality Among Neonates Undergoing DSC Post Cardiac Surgery.^a

Variables	P value	95% CI
Age at operation (days)	.359	0.666 to 1.159
Sex	.336	0.180 to 150.776
Operative weight	.629	0.023 to 9.672
ICU days	.116	0.680 to 1.043
DSC days	.824	0.648 to 1.412
ECMO	. 002	0.000 to 0.122
RACHS-1 (surgical risk score)	.126	0.029 to 1.550
Aortic cross clamp time	.159	0.987 to 1.086
CPB time	.604	0.966 to 1.020
Number of chest explorations	.915	0.068 to 20.174

Bold values show statistical significance (P < .05).

Discussion

Median sternotomy with delayed sternal closure has become standard practice in a select subgroup of patients to optimize postoperative recovery. This strategy proves particularly advantageous in the case of hemodynamic or respiratory instability, myocardial edema, and dilation, when coagulopathy and bleeding require packing of the chest or the necessity for central ECMO support. For some subgroups of patients, the decision to leave the chest open is made preoperatively, as in the case of ASO for TGA, or following the Norwood procedure for HLHS. In other cases, when it is likely that additional procedures need to be performed, like tightening a PAB, the DSC stategy is adopted. Adopting a DSC policy is not without risks; for instance, patients with prolonged CPB time, low cardiac output, or coagulopathy needing transfusion are recognized to be at higher risk for SWI.¹ Furthermore, SWIs have been associated with longer postoperative stays, as well as increasing the cost of stay due to the requirement for prolonged ventilation.⁶

A significant challenge in comparing our findings with the existing literature lies in the lack of standardization in defining infection subtypes. Variability in the criteria used to classify superficial and deep wound infections across studies introduces potential inconsistencies and may account for some of the observed differences in reported incidence rates.^6–16

There exists a variance in the reported incidence rates of SWI in patients with DSC. Some retrospective series have found superficial SWI rates as high as 6.7%-9.7% and deep SWIs as high as 3.9%-10.5%, respectively^1,6,16 while others have reported no significant association between DSC and an increase in surgical site infections. Von Stumm et al described a 7.3% superficial SWI rate in 358 pediatric patients but no deep SWIs requiring surgical debridement.¹ Furthermore, Yang et al reported a 9.7% surgical site infection rate in neonates post DSC, of which there were 28 cases of mediastinitis.¹⁶ Our retrospective study demonstrates similar superficial SWI rates, 10.2%, while our deep SWI rate is considerably lower at 1.07%.

Tabbutt and Özker et al reported a 19% mortality rate following pediatric DSC.^6,17 Hurtado-Sierra et al reported mortality as 22.4% with patients RACHS-1 score ≥3 posing a higher risk of mortality.³ Our study shows a considerably lower 30-day mortality rate of 4.8%. A 30-day mortality rate may be attributed to nosocomial infections; 12.8% of our neonates developed sepsis within 30 days of admission, significantly lower than Elassal et al, who reported 54.1% in a pediatric cohort.¹⁸ Infection rates are reported to be higher in patients with prolonged ICU stay.¹⁸ Our study depicts an association between prolonged ICU stay and the risk of SWIs on univariate analysis. Our ICU and hospital stay of 12.8 days (SD 16.6) and 25.9 days (SD 36.9), respectively, are higher than other neonatal cohorts; Yang et al report an ICU and hospital length of stay in their SWI patients as 11.64 days (SD 2.6) and 22.26 days (SD 4.3), respectively.¹⁶

On univariate analysis, cardiopulmonary bypass time, prolonged DSC time, and aortic cross clamp time were significantly associated with 30-day mortality. Cardiac surgery–related morbidity has been primarily attributed to the use of cardiopulmonary bypass. This can be explained by the fact that extracorporeal circulation can induce a systemic inflammatory response, trauma, ischemia and reperfusion injury, endothelial dysfunction, and activation of the coagulation cascade.^19–22 Prolonged cross-clamp time has also been shown to be an independent predictor of 30-day mortality in the literature, similar to our findings.²³ Furthermore, an aortic cross-clamp time of more than 60 min is associated with a 91.2% higher probability of SWI. Our study, on the other hand, did not find such an association.¹⁶

Our retrospective study found one significant association between a higher RACHS-1 score and risk of SWIs on multivariable analysis. The majority of our DSC cohort had undergone arterial switch operations and HAA repairs with high RACHS-1 scores of 4, similar to several other series.^6,23,24 This may be explained as more complex operations with higher RACHS-1 scores are more likely to lead to myocardial edema, coagulopathy, and hemodynamic instability, increasing the risk of infection.

Application of ECMO was a significant risk factor for 30-day mortality in our multivariable analysis, similar to previous reports.²⁵ Gupta et al in a cohort of 998 pediatric patients described a 48.1% survival rate to hospital discharge with ECMO, with a mortality rate increasing by 12% every day after seven days of venoarterial ECMO use.²⁵

Timing of sternal closure is still a matter of controversy. Riphagen et al recommend DSC within 24 h to lower rates of nosocomial infections and ventilator-associated complications.²⁴ However, premature closure of the sternum can lead to repeated DSCs leading to more deleterious effects than a prolonged period of DSC.⁷ Our study reports a DSC time of 3.8 (SD 5.8) days, comparable to the existing literature average of three days.^17,18 Furthermore, our study reports no association between DSC time and risk of SWI. This is contradictory to previous retrospective studies which reported a higher incidence of infection with longer periods of open chest.^2,26 This demonstrates the importance of avoiding premature closure of the sternum as premature closure may lead to further attempts at reopening the chest.^7,18

Limitations

It is important to note that although several retrospective studies have been referenced, their outcomes cannot be generalized or used as a basis for comparison due to the significant variance in reported mortality and morbidity. Limitations of our study include it being retrospective and a single center. Moreover, different surgical delayed sternal closure protocols exist within our surgeons’ group.

Conclusion

Delayed sternal closure represents an efficacious surgical approach for the management of complex cardiac surgery in the pediatric population. Reassuringly, our findings reveal minimal incidence of SWI associated with delayed sternal closure in these high-risk cases. High RACHS-1 score was the only independent risk factor for SWI in univariate analysis (P = .019) and multivariable analysis (P = .05). Delayed sternal closure facilitates PAB adjustment in high-risk complex cases. Moreover, DSC allows quick access to initiate postoperative lifesaving ECMO in this critical group of patients.

Footnotes

Abbreviations

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

ORCID iDs

Amr Ashry

Hesham Hassan Ahmed

Robyn Lotto

Ram Dhannapuneni

Attilio A. Lotto

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