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Ann Thorac Surg 2005;80:678-684
© 2005 The Society of Thoracic Surgeons

Original article: Cardiovascular

"Early" Delayed Sternal Closure Following Pediatric Cardiac Surgery

Shelley Riphagen, FCP a , * , Marilyn McDougall, FCP a , Shane M. Tibby, MRCP a , Nelson Alphonso, FRCS b , David Anderson, FRCS b , Conal Austin, FRCS b , Andrew Durward, FCP a , Ian A. Murdoch, FRCP a

a Department of Pediatric Intensive Care, Guy’s Hospital, London, United Kingdom
b Department of Cardiothoracic Surgery, Guy’s Hospital, London, United Kingdom

Accepted for publication February 9, 2005.

* Address reprint requests to Dr Riphagen, Pediatric Intensive Care Unit, Guy’s Hospital, Saint Thomas Street, London SE1 9RT, United Kingdom (Email: shelley.riphagen{at}gstt.sthames.nhs.uk).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 References
 
BACKGROUND: Delayed sternal closure is commonly used following pediatric cardiopulmonary bypass surgery for many reasons including support of the failing myocardium. We hypothesized that, as a result of improvements in perioperative care, sternal closure could be achieved at an earlier postoperative time than the 3 to 5 days typically reported in the literature.

METHODS: Retrospective chart review of all bypass surgery (n = 585) performed in a single center over a 3-year period (2000–2002).

RESULTS: We identified 66 children (11.3%), median age 5 days old, who underwent delayed sternal closure. In 60 of these patients, sternal closure was achieved at a median (interquartile) postoperative time of 21 hours (18 to 40 hours). The most common indication was inadequate hemostasis, although early sternal closure was also achieved in the subgroup with poor myocardial function as the primary indication at a median of 36 hours (21 to 44 hours). There was no noticeable hemodynamic, respiratory or metabolic compromise following sternal closure, although patients with poor myocardial function tended to have a lower mean blood pressure than those with inadequate hemostasis (ANOVA, p = 0.02). The overall mortality was 19.7% (13 of 66), with a median duration of ventilation and intensive care stay among survivors of 3.8 days (2.4 to 6.3 days) and 4.8 days (3.7 to 7.9 days), respectively.

CONCLUSIONS: Delayed sternal closure is possible at an earlier stage than previously reported.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 References
 
Delayed sternal closure (DSC) is a well-established technique for optimizing myocardial support following complex pediatric cardiac surgery [1]. This procedure was first described in adults in 1975, with subsequent reports appearing in the early 1980s [2, 3]. The potential for benefit from DSC is greater in children, because of a larger cardiac size relative to the thoracic cavity. The utility of DSC in children has become evident over the last two decades, with the shift from palliative to earlier corrective surgery, resulting in longer cardiopulmonary bypass times on younger patients [4].

Indications in children are similar to those described in adults, including myocardial edema, depressed myocardial function, inadequate intraoperative hemostasis, dysrhythmias, and access for external cardiac support systems [5]. In many pediatric institutions it is routine to leave the sternum open prophylactically following long operations or specific procedures [6, 7]. Delayed sternal closure may improve cardiac and pulmonary function in the immediate postoperative period by reducing intrathoracic pressure with consequent effects on ventricular filling, cardiac output, and resultant pulmonary blood flow mechanics [8]. However, it may expose children to the risks associated with an increased duration of ventilation and prolonged intensive care stay, particularly nosocomial infection [9].

The optimal time to sternal closure remains unclear. Generally the sternum is left open for at least 3 days, with closure occurring any time from 2 to 14 days postoperatively [7, 10, 11]. Although attempted sternal closure should only occur after resolution of the primary indication (hemorrhage, edema, etc), several authors have suggested achievement of negative fluid balance to be desirable also [5, 11, 12]. Our institution has an aggressive approach to DSC, aiming for closure within 24 hours. This does not mandate achieving a negative fluid balance, but rather avoiding excessive fluid overload. The rationale for this approach is twofold. First, the majority of indications for DSC resolve within 24 hours [13, 14]. Second, achieving a negative fluid balance in the face of DSC is often difficult due to lack of patient mobilization.

Here we report our experience with "early" DSC. Our aims were threefold: to confirm the impression that DSC typically occurs within 24 hours of surgery; to record any adverse haemodynamic and metabolic consequences at the time of DSC; and to document the perioperative mortality and morbidity in this patient population.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 References
 
We reviewed retrospectively the records of all children (newborn to 16 years old) undergoing cardiac surgery over the 3-year period from January 2000 to December 2002. A total of 751 procedures were performed on 640 children (585 operations on cardiopulmonary bypass), median (interquartile) age 6.4 months old (0.5 to 32 months old), with a crude mortality of 5.2%.

We identified cases of DSC from the pediatric intensive care database, corroborated by reviewing the operative records of two surgeons (DA, CA). Case notes and charts were reviewed, and demographic and physiological data collected. Surgical complexity was graded using the risk adjustment in congenital heart surgery method (RACHS-1) [15].

The following details concerning DSC were recorded: indication, mode of occurrence (left open from theater versus emergency sternotomy), time of opening (if in the intensive care unit), and time to successful closure. Cumulative fluid balance was documented up until the time of successful DSC. Cardiopulmonary and metabolic instability over the 6-hour period following sternal closure were recorded. Inotropic support was quantified via a validated score that accounts for the potency of differing agents [13, 16]. The potencies were assigned such that dopamine, dobutamine, and enoximone were assigned a score of 1 per µg/kg/min administered, and adrenaline was allotted a score 100 µg/kg/minute. Thus a patient receiving dopamine at 5 µg/kg/min concurrently with adrenaline at 0.1 µg/kg/min is calculated to have an inotrope score of 15 ([5 x 1] + [100 x 0.1]).

Pediatric intensive care unit mortality, length of ventilation, and duration of stay were recorded along with the incidence of wound infection, wound dehiscence, and bloodstream infection.

Intraoperative Management
Anesthetic induction consisted of intravenous fentanyl or ketamine, and maintained using inhaled isoflurane (0.5%) and intermittent fentanyl. All patients received dexamethasone (0.25 mg/kg), at induction of anesthesia.

The extracorporeal system was nonheparin bonded, and the volume and composition of the pump prime varied between 400 and 700 mL and included: packed red cells (to maintain hematocrit 20%–25% on bypass), 8.4% sodium bicarbonate at 20 mL/L for clear primes, and 1 mL/bag of packed red cells; heparin 250 µg/kg body weight; and either Hartmann’s solution in equal volumes with Haes-Steril 6% (only with clear primes) or Haes-Steril alone (with blood primes) as the remainder of the priming volume. Cardiopulmonary bypass was initiated at a cardiac index of 2.6 L/min/m2 and maintained at this flow rate regardless of the degree of induced hypothermia. Flow was nonpulsatile and an alpha-stat blood gas strategy was utilized. All patients received slow continuous ultrafiltration while on bypass. Patients were weaned from bypass after rewarming to a rectal temperature of 37°C. Cardioplegia technique differed between surgeons: one surgeon (CA) used single-dose, cold blood cardioplegia; the other surgeon (DA) used single-dose (10–15 mL/kg) cold crystalloid.

Postoperative Management and Timing of Sternal Closure
Patients in whom a low cardiac output state was likely to occur received a loading dose of enoximone prior to termination of bypass [17]. Enoximone and dopamine were used as first line inotropic agents when indicated; further afterload reduction, if required, was achieved using sodium nitroprusside. Maintenance fluid was restricted to 50 mL/kg/day for patients less than 10 kg, 25 mL/kg/day for those 10 to 40 kg, and 40 mL/hr for those above 40 kg. Isotonic fluids were used (0.9% saline in either 5% or 10% dextrose), and enteral feeding started as soon as possible. Nonblood product volume replacement consisted of Hartman’s solution to avoid the development of hyperchloremic acidosis [18]; colloids were not routinely given. The significance of a metabolic acidosis (base deficit greater than 5 mEq/L) was interpreted in conjunction with hemodynamic trends, echocardiographic findings, serial blood lactate measurements, and the ratio of plasma chloride to sodium. We have previously reported that a hyperchloremic acidosis can be diagnosed by the presence of a chloride:sodium ratio greater than 0.79 [19]. Thus, volume replacement was not initiated in the face of a hyperchloremic acidosis alone. Patients were mechanically ventilated aiming for tidal volumes of 10 mL/kg. Sedation consisted of morphine infusion, intermittent lorazepam (as required), and oral clonidine was occasionally used. Neuromuscular blockade was not routine. Loop diuretics were usually commenced on the first postoperative day.

Prior to sternal closure, the wound was covered with a gauze swab and an "op-site" adhesive dressing; sternal stenting was not utilized. Routine perioperative antibiotics (cefuroxime) were continued, and vancomycin and gentamicin were given as a single dose during attempted closure. Sternal closure was attempted in the intensive care unit, generally within 24 postoperative hours. When DSC was initiated because of poor myocardial function or myocardial edema, closure was preceded by a short trial period whereby the sternal edges were approximated. If the left atrial pressure increased rapidly by greater than 5 to 6 mm Hg, closure was abandoned. Sternal closure was achieved using absorbable monofilament PDS and absorbable Vicryl for the subcutaneous and subcuticular layers in a manner identical to intraoperative closure. Antiseptic irrigation (such as iodine solution) was not routine.

Statistical Analysis
Demographic data are presented as median (interquartile range) and compared using the Mann-Whitney test. Temporal data are reported as mean (standard deviation) with analysis by two-way repeated measures analysis of variance (ANOVA). The p values are reported for group, time, and group-time interactions. Proportions were compared using Fisher’s exact test. Analysis was performed using SPSS 12.0 (SPSS Inc, Chicago, IL).


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 References
 
We identified 66 children who underwent DSC of 585 receiving cardiopulmonary bypass (11.3%). Children requiring DSC were significantly younger and smaller than the remainder of the cardiopulmonary bypass group. The median (interquartile) age and weight of these children was 5 days (3 to 12.5 days) and 3.0 kg (2.9 to 3.4 kg), respectively, compared with 10.9 months (2.5 to 49 months) and 8.8 kg (3.7 to 15.5 kg) for non-DSC patients (both p < 0.001).

Anatomical diagnoses for the DSC group are shown in Table 1. The most common procedure, occurring in 42% (28/66), was the Norwood 1 operation for hypoplastic left heart syndrome. Interestingly, the Norwood 1 operation per se was not an absolute indication for DSC, as only 37% patients (28 of 76 patients) undergoing this procedure underwent DSC during the study period. Despite the surgical complexity (median RACHS-1 score of 5.5 [3 to 6]), the DSC group demonstrated modest extracorporeal support times: median cardiopulmonary bypass time 84 minutes (55 to 113), aortic cross-clamp 54 minutes (43 to 69), and deep hypothermic cardiac arrest 38 minutes (3 to 53).


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  		Table 1. Anatomical Diagnoses of Patients Requiring Delayed Sternal Closure
 
Forty-eight children returned from theater with an open chest, whereas the remaining 18 underwent emergency sternotomy on the intensive care unit. The indications for initiation of DSC in theater were inadequate hemostasis (n = 33), poor myocardial function (n = 10), inadequate hemostasis and poor myocardial function (n = 4), and re-do operation (n = 1). Emergency sternotomy in the intensive care unit occurred at a median postoperative time of 4 hours (1 to 18) for the following indications: cardiac tamponade secondary to hemoserous/serous effusion (n = 12), tamponade secondary to surgical bleeding (n = 4), and poor myocardial function (n = 2).

Sternal closure was achieved in 60 patients at a median postoperative time of 21 hours (18 to 40 hours). The time to successful closure was associated with the indication for DSC, tending to occur earlier in patients with inadequate hemostasis than those with poor myocardial function: 21 hours (17 to 26) versus 36 hours (21 to 44) (p = 0.08). Six children never underwent sternal closure and died at a median time of 11 hours postoperatively (10 to 38 hours). The indications for delayed sternal closure in this group were uncontrolled hemostasis in theater (n = 3) and poor cardiac function (n = 3).

It is conceivable that the hemodynamic, respiratory, and metabolic profiles at the time of sternal closure may differ according to the indication for DSC. For this reason we subdivided patients into two groups: one in whom DSC was initiated because of inadequate hemostasis (drain losses are shown in Fig 1) and the second group encompassed all other patients (of which poor myocardial function was the most common reason). Table 2 illustrates that patients with poor myocardial function tended to have lower overall blood pressures (group effect, p = 0.02), however this did not change after sternal closure (time effect, p = 0.2; group-time interaction, p = 0.91). Furthermore, blood pressure was not maintained at the expense of an increased inotrope requirement (p values 0.64–0.91). There were no significant changes associated with sternal closure for any of the other measured variables (Table 2). Thirty-six patients had left atrial lines placed intraoperatively; the mean (standard deviation) left atrial pressure for these patients was 9.0 mm Hg (3.2) at the time of DSC. The left atrial line was removed at the time of DSC in 19 patients, for the remaining 17 the mean (standard deviation) change in left atrial pressure at 1-hour post-DSC was 0.4 mm Hg (1.4). Cumulative fluid balance at the time of DSC was slightly positive, at +42 mL (0 to +114).



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  		Fig 1. Early postoperative mediastinal drain losses for patients in whom delayed sternal closure was initiated for inadequate hemostasis. Bars are mean and error bars are standard error of the mean.

 

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  		Table 2. Hemodynamic, Respiratory and Metabolic Trends Following Sternal Closure
 
The intensive care unit mortality for the DSC group was 13 of 66 (19.7%). As discussed earlier, 6 deaths occurred without attempting sternal closure, whereas the remaining 7 deaths occurred at a median time of 288 hours (69 to 396 hours) post-DSC. The indications for DSC among patients who died were: hemostasis (n = 6), poor function (n = 6), and cardiac tamponade (n = 1). Thus patients who died had a higher proportion of poor myocardial function as the primary indication for DSC compared to those who survived: 6 of 13 versus 7 of 53, p = 0.015; odds ratio 5.63 (1.46 to 21.73). Causes of death for the 7 patients who underwent sternal closure included: sepsis (n = 3), necrotizing enterocolitis (n = 2), myocardial failure (n = 1), and intracranial hemorrhage (n = 1). The incidence and timing of DSC and outcome for all patients is summarized in Figure 2.



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  		Fig 2. Incidence, timing, and outcome of patients undergoing delayed sternal closure. (DSC = delayed sternal closure; IQR = interquartile range; RACHS = risk adjustment in congenital heart surgery method.)

 
The median duration of ventilation was 3.8 days (2.4 to 6.3). The median length of stay in the intensive care unit after sternal closure was 4.0 days (2.9 to 7.0), producing an overall time in the intensive care unit of 4.8 days (3.7 to 7.9 days). Two children had minor wound dehiscence, which subsequently healed by secondary intention, however there were no documented episodes of sternal instability or mediastinitis requiring surgical re-exploration. There were 5 cases of superficial wound infection with positive wound swabs (4 staphylococcal, 1 pseudomonal) that required antibiotic treatment. One neonate developed methicillin-resistant Staphylococcus aureus sepsis and died 12 days after sternal closure.

Other associated morbidity relating to the underlying cardiac conditions included 2 cases of necrotizing enterocolitis, one of whom underwent successful cardiac surgery and sternal closure but died 67 hours later. One other child had postoperative seizures associated with extensive intraventricular and intracranial hemorrhage; intensive care was withdrawn for this reason, 48 hours after successful sternal closure.


   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
References
 
The value of DSC is well recognized following pediatric cardiopulmonary bypass surgery, although the optimal time to attempt sternal closure remains unclear. The primary findings from this retrospective study are that DSC can be achieved at an earlier stage than previously reported (0.9 days versus 3 to 5 days), without significant hemodynamic, respiratory or metabolic compromise, while demonstrating a mortality and morbidity comparable to that reported in the literature (Table 3). Possible reasons for these findings are discussed below.


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  		Table 3. Comparison Between Studies Published Within the Last Decade
 
Our patient population is similar to that previously reported with regard to age (median age 5 days old), surgical complexity (median RACHS-1 score 5.5) and incidence of DSC, however there are significant differences in terms of cardiopulmonary bypass times and the indications for DSC. This may be related to the differing time periods examined; our study spanned 2000 to 2003, while all prior reports document the practice of DSC during the late 1980s to mid-1990s (Table 3). There have been many advances in surgical and cardiopulmonary bypass techniques and perioperative care since this time that may have influenced our results.

The cardioprotective and antiinflammatory effects of many of the therapies utilized during our study are well established, including administration of steroids before bypass [22, 23], modified ultrafiltration while on bypass [24, 25], and early postoperative use of phosphodiesterase inhibitors [26]. The modest cardiopulmonary bypass times (median 84 minutes) in the current study were also likely to reduce the inflammatory response after bypass [27, 28]. We postulate that these factors helped to both decrease the incidence and attenuate the severity of the low cardiac output syndrome in the postoperative period, thereby facilitating early sternal closure.

The majority of studies cite a negative fluid balance as a prerequisite for achieving DSC [5, 11, 12]. Our philosophy is rather one of avoiding excessive edema formation, which is undoubtedly helped by the perioperative factors highlighted above. Additional postoperative factors that may be important include avoidance of prolonged neuromuscular blockade [29], isotonic fluid restriction, and judicious volume replacement aided by a focused approach to the causes of a metabolic acidosis [19, 30].

A possible criticism of this study is that our DSC population contained a high proportion of patients in whom the primary indication was hemostasis, as sternal closure should be achieved early in this subgroup. We do not know why we have such a high incidence of inadequate hemostasis; this is the focus of an ongoing study at our institution. However, 75% of patients for whom DSC was initiated for poor myocardial function underwent successful sternal closure within 48 hours (median time 36 hours), which is well below the typical mean time of 3 to 5 days reported previously (Table 3). These patients did not appear to suffer any adverse hemodynamic, respiratory or metabolic consequences following sternal closure, although we acknowledge that central venous oxygen saturations were not measured. Furthermore, the timing of closure did not appear to influence either the cause or timing of death among the 7 patients who died following sternal closure. Case note review revealed that only 1 death was due to primary myocardial failure occurring 24 hours after closure, well below the median time to death of 288 hours for this subgroup.

It is also apparent from Table 3 that no patients received extracorporeal membrane oxygenation during the study period. Although this therapy is offered on an ad hoc basis for cardiac surgical patients only, we maintain strict criteria for instituting this therapy (including adequate surgical repair of the primary lesion and reversibility of associated underlying conditions); also our center does not perform cardiac transplantation. This has resulted historically in approximately 2 to 4 patients requiring extracorporeal membrane oxygenation each year, which surprisingly did not occur during the study period. We feel that this represents a statistical "blip", as a few cases requiring extracorporeal membrane oxygenation have been identified since this time.

There are several limitations to this study. Although we could not demonstrate hemodynamic instability following sternal closure, we cannot rule out a degree of hemodynamic compromise, as mixed venous oxygen monitoring was not routine at this time, cardiac output was not measured, and left atrial pressure monitoring lines were removed in the majority of patients. Also, the retrospective nature of the study may have resulted in under-reporting of complications such a wound infections. Also, it is important to note that this study does not address the issue of when to attempt sternal closure in individual patients, as all of the variables that may have contributed to the clinical decision-making are not apparent from a retrospective review.

Nonetheless, we believe that our center is typical of many performing cardiac surgery. We postulate, as a result of advances in perioperative management, that DSC can now be achieved at an earlier time than previously reported.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

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