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Ann Thorac Surg 2011;91:1460-1466. doi:10.1016/j.athoracsur.2011.01.020
© 2011 The Society of Thoracic Surgeons
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Original Articles: Pediatric Cardiac

Low Weight-for-Age Z-Score and Infection Risk After the Fontan Procedure

Jeffrey B. Anderson, MD, MPHa,*, Heidi J. Kalkwarf, PhDb, Jack E. Kehl, BSa, Pirooz Eghtesady, MD, PhDc, Bradley S. Marino, MD, MPPa,d

a Division of Cardiology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio
b Division of General and Community Pediatrics, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio
c Division of Cardiothoracic Surgery, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio
d Division of Critical Care Medicine, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio

Accepted for publication January 12, 2011.

* Address correspondence to Dr Anderson, Cincinnati Children's Hospital Medical Center, The Heart Institute, ML2003, Cincinnati, OH 45255 (Email: jeffrey.anderson{at}cchmc.org).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 References
 
Background: Poor growth is common in infants with a single ventricle. Lower weight-for-age z-score (WAZ) is associated with worse short-term outcome after bidirectional Glenn procedure. We sought to assess growth status at the time of the Fontan procedure and the effect of poor growth status on surgical outcomes.

Methods: This retrospective case series examined children who underwent Fontan at our institution between January 2003 and December 2008. Weight and height were obtained at the time of admission for Fontan. Data from preoperative echocardiogram and cardiac catheterization were abstracted to document cardiac function and hemodynamic measurements. Outcome variables included ventilator time, chest tube duration, postoperative infections (bacteremia, mediastinitis, urinary tract infection, gastroenteritis, or culture-positive pneumonia), and length of hospital stay.

Results: Fifty-five patients were included for analysis. The median age at Fontan was 46 months (range, 18 to 72); median WAZ was –1.0 (–3.8 to +2.0), and height for age z-score was –1.1 (–3.7 to +1.5). The WAZ was less than –2.0 in 19% of patients. Multivariable modeling revealed that patients with a WAZ less than –2.0 (p = 0.006) had a greater incidence of serious postoperative infections. The only factor predicting longer length of hospital stay was presence of a serious postoperative infection (p < 0.0001). Ventilator time was predicted only by length of cardiopulmonary bypass (p = 0.01). No factors were associated with longer chest tube duration.

Conclusions: Growth failure in children with a single ventricle persists through presentation for Fontan. A WAZ less than –2.0 at Fontan is associated with a higher rate of serious postoperative infections, which are associated with longer length of hospital stay.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 References
 
Infants with congenital heart disease are known to be at risk for failure to thrive, which occurs when the rate of growth is below expectations based on age- and sex-specific growth charts [1]. Specifically, failure to thrive is diagnosed when growth is below the fifth percentile, growth-for-age z-scores are below –2.0, or when growth has negatively crossed two major age-indexed percentiles [2, 3]. Growth failure in infants with congenital heart disease has been attributed to several different etiologies including inadequate caloric intake, increased energy expenditure, intestinal malabsorption, and decreased splanchnic blood flow [4, 5]. Failure to thrive is especially prevalent among children with a single ventricle [6]. These patients, who typically undergo a series of palliative surgical procedures [7-9], have difficulty achieving adequate nutritional and weight gain goals between the first and second surgical stages [6]. After the second surgical stage, there is some catch-up growth [10], although many children continue to exhibit somatic growth failure years after the Fontan procedure [11]. Despite some catch-up growth, as many as 15% of patients with a single ventricle enter the Fontan procedure with a weight-for-age z-score (WAZ) below –2.0 [11].

The etiology of poor growth and malnutrition is poorly understood in the single ventricle population. It is known that these infants have a lower than desired total caloric intake and that their growth improves with the introduction of high-caloric enteral feeds [6]. It has also been shown that infants with a single ventricle have oral-motor coordination problems and are slower to reach goal caloric intake [12]. Finally, energy expenditure is increased during the initial hours after first-stage palliation in infants with a single ventricle [13], but that has not been evaluated thereafter.

Poor nutrition in adults is associated with longer hospital stays and increased rate of readmission [14, 15]. Among pediatric patients admitted to the hospital with serious infections, poor nutrition has been linked to increased morbidities [16]. Few studies have looked at the relationship between nutritional status and surgical outcomes in children undergoing cardiac surgery. Leite and associates [17, 18] found increased rates of mortality and postsurgical infection in a group of patients with diverse types of congenital heart disease, with poor nutrition defined as low serum albumin level or low weight-for-age percentile. We have previously shown an association between lower WAZ and poor short-term surgical outcomes after the bidirectional Glenn (BDG) procedure [19]. There are no prior studies, to our knowledge, relating nutritional status and weight gain to perioperative morbidity in patients undergoing the Fontan procedure.

The purpose of this study was to identify specific anthropometric and cardiovascular variables that predict lower WAZ at Fontan, and poorer short-term surgical outcomes and perioperative morbidity in infants with a single ventricle after the Fontan procedure.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 References
 
Study Design
This study was a retrospective case series including all patients who underwent Fontan procedure at Cincinnati Children's Hospital Medical Center between January 2003 and December 2008. Our predetermined exclusion criteria included premature birth (<35 weeks gestational age), chromosomal abnormalities, and major congenital anomalies of the central nervous, gastrointestinal, or pulmonary systems. This study was approved by the Institutional Review Board at Cincinnati Children's Hospital Medical Center (2008-1639).

Data Collection
Study data were collected from hospital medical records and Heart Institute outpatient records, as well as cardiac catheterization, echocardiography, and cardiac surgical databases. Data collected included demographic information including sex, gestational age and race; anthropometric measurements and information regarding nutritional management; pre-Fontan medical and surgical management including length of neonatal and post-BDG hospitalizations, documentation of vocal cord paralysis after neonatal surgery and the need for readmission between BDG and Fontan; echocardiographic and hemodynamic data; and data from the Fontan operative and perioperative periods.

Anthropometric measurements and nutritional management
Anthropometric measures included absolute weight and WAZ at initial neonatal hospital admission and discharge and at admission for BDG, as well as weight, length, WAZ, and height-for-age z-score at the time of the Fontan procedure. The WAZ and height-for-age z-scores were calculated using the Centers for Disease Control Epi-Info program (Centers for Disease Control, Atlanta, GA). In addition to absolute WAZ, we identified patients who met criteria for failure to thrive at the time of their Fontan who had a WAZ below –2.0.

Pre-BDG medical and surgical management
Information regarding medical and surgical management before the Fontan procedure was recorded and included initial cardiac diagnosis, previous surgeries and hospital courses, history of necrotizing enterocolitis or vocal cord paralysis, and outpatient medications at the time of the Fontan procedure.

Echocardiographic and hemodynamic data
Findings from the most recent echocardiogram performed before the Fontan procedure were reviewed. Atrioventricular valve regurgitation and aortic or neoaortic regurgitation were considered significant if graded as moderate or greater. Significant residual defects including restrictive atrial communication (>2 mm Hg gradient) and aortic arch obstruction (>20 mm Hg peak corrected gradient) were noted. Depressed ventricular function was defined as a qualitative description of moderate or greater systolic dysfunction in a right or left single ventricle or a shortening fraction less than 28% in any left ventricle. Data from the most recent cardiac catheterization performed before the Fontan procedure were reviewed. Measurements recorded included mean pulmonary artery pressure, transpulmonary gradient, pulmonary vascular resistance, ventricular end-diastolic pressure, aortic arch systolic pressure gradient, systemic arterial and mixed venous oxygen saturation, and hemoglobin level.

Operative data
Operative variables recorded included intraoperative mortality, cardiopulmonary bypass time, aortic cross-clamp time, circulatory arrest time, and concomitant procedures performed in addition to the Fontan.

Perioperative data
Variables recorded from the postoperative course included postoperative mortality (<30 days of surgery); total ventilator time (time from operating room to final extubation); chest tube duration (time from operating room to final chest tube removal); documented significant postoperative infections including bacteremia, mediastinitis, culture-positive urinary tract infections, culture-positive gastroenteritis, and pneumonia, which was defined as culture-positive endotracheal tube aspirate with chest radiograph changes consistent with pneumonia; significant pleural effusions that required change in diuretic regimen or insertion of new chest tube; episodes of reintubation; total intensive care unit days; and total hospital days.

Statistical Analyses
The primary outcome variables assessed were WAZ at Fontan and total hospital length of stay. Secondary outcome variables included the need for Fontan takedown, ventilator time, chest tube duration, significant infections, significant pleural effusions, and episodes of reintubation after Fontan. The predictor variables for WAZ at Fontan were WAZ at the time of BDG discharge, longer neonatal and post-BDG hospitalizations, and the need for readmission to the hospital between BDG and Fontan.

The primary predictor variable for total hospital length of stay and secondary outcome variables was WAZ at Fontan. Potential covariates for all outcome variables included diagnosis of hypoplastic left heart syndrome or variants, preoperative significant atrioventricular valve regurgitation, and aortic or neoaortic regurgitation or aortic arch obstruction, restrictive atrial communication, depressed ventricular function, and elevated mean pulmonary artery pressure or pulmonary vascular resistance. Operative covariate predictor variables include the length of cardiopulmonary bypass and aortic cross-clamp time after Fontan.

Statistical analysis was performed using Stata 10.0 analysis software (Stata Corporation, College Station, TX). All continuous variables were described and tested for central tendency to determine the normality of the data distribution. Normally distributed continuous variables are expressed as mean plus or minus standard deviation. Nonnormally distributed data are expressed using the median value and range. Potential dichotomous predictor variables that did not occur in more than 10% of our study population were not statistically evaluated. Bivariate analyses of potential risk factors for adverse outcome were performed using the Wilcoxon rank sum test for continuous variables and Fisher's exact test for dichotomous variables. Candidate predictor variables for multivariable modeling had a p value of less than 0.1 on bivariate analyses. Multivariable analyses were performed using linear regression. A correlation table was utilized to assess for colinearity of variables. A p value of less than 0.05 was considered statistically significant.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 References
 
Study Population
A total of 55 patients underwent Fontan procedure at our institution during the study period; 3 patients had Fontan takedown in the immediate postoperative period. Patient characteristics are shown in Table 1.


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  		Table 1 Patient Characteristics
 
Anthropometric Measurements
At neonatal admission, infants in our study had a median weight of 3.2 kg (2.4 to 4.4 kg) and median WAZ of –0.2 (–1.9 to 3.2). At the time of the BDG, the median weight was 6 kg (3.6 to 8.4 kg), and the median WAZ had dropped to –1.2 (–3.3 to 0.6). By the time of the Fontan, their median weight was 14.3 kg (7.1 to 20.6 kg), and the median WAZ had slightly improved to –1.0 (–3.8 to 2). Progression of WAZ in this group of patients is shown in Figure 1 . At the time of Fontan, 19% of our patients had a WAZ below –2.0. None of the 3 patients who were excluded with Fontan takedown had a WAZ at the time of Fontan less than –2.0. Median z-score for height at the time of the Fontan was –1.0 (–3.7 to 1.5). Patients with hypoplastic left heart syndrome (n = 20) had a WAZ similar to that of the remainder of the cohort at neonatal admission (p = 0.6), at the BDG (p = 0.6), and at presentation for Fontan (p = 0.24). Characteristics of patients entering the Fontan with a WAZ less than –2.0 are seen in Table 2.


Figure 1
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  		Fig 1. Weight-for-age z-score progression over time (n = 55) (BDG = bidirectional Glenn.)

 

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  		Table 2 Patient Characteristics Based on Fontan Weight-for-Age Z-Score (WAZ)
 
Pre-Fontan Medical and Surgical Management
There were 52 patients who required neonatal hospitalization for a median hospital length of stay of 20 days (6 to 60). Three patients were discharged home after birth and later recognized to have congenital heart disease so did not have neonatal admissions. During the neonatal hospitalization, there were 2 patients who had necrotizing enterocolitis. It is policy at our institution to perform fibroscopic airway evaluation of all infants who have undergone the Norwood procedure before their discharge from the hospital because of risk of damage to the recurrent laryngeal nerve during aortic arch reconstruction, which may result in vocal cord paralysis or paresis and may affect feeding. After neonatal surgery, 12 patients had documented vocal cord paralysis. All 55 patients underwent BDG procedure, and had a median hospital length of stay after BDG of 6 days (4 to 56).

Information was available on feeding plans for 51 patients (93%) at neonatal discharge, 50 patients (91%) at BDG, and 53 patients (96%) at Fontan presentation. The number of patients exclusively fed orally steadily rose from 18 (29%) to 40 (71%) to 48 (87%), while the number of patients supported with either nasogastric or gastrostomy tube feedings fell from 40 (71%) to 18 (29%) to 9 (13%). There were 7 patients who had placement of gastrostomy tube: 2 during their neonatal hospitalization, 2 during the period before BDG, and 3 between BDG and Fontan. At the time of Fontan, there were 3 patients still requiring supplemental feeding utilizing their gastrostomy tube and 4 patients who were receiving overnight feeds through a nasogastric tube. Feeding plans were not standardized and were left to the discretion of individual cardiologists and pediatricians.

Echocardiographic and Hemodynamic Data
All patients had echocardiograms, and 54 of 55 patients underwent cardiac catheterization before surgery. Echocardiographic and hemodynamic findings are shown in Table 3.


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  		Table 3 Preoperative Echocardiographic and Hemodynamic Data
 
Operative Data
Of patients undergoing Fontan procedure in this series, 53 of 55 underwent placement of an extracardiac Fontan circuit, and 2 patients had a lateral tunnel Fontan performed. All patients had a Fontan fenestration created during the procedure. Ten patients had additional procedures performed at the time of the Fontan. Additional procedures performed included pulmonary artery reconstruction (n = 5), atrioventricular valve repair (n = 3), aortic arch reconstruction (n = 2), enlargement of the atrial communication (n = 2), Damus-Kaye-Stansel operation (n = 1), and supravalvar aortic stenosis repair (n = 1). The median cardiopulmonary bypass time was 113 minutes (38 to 207). Twelve patients required aortic cross-clamp for a median of 32 minutes (10 to 94), and 2 patients required circulatory arrest for a median of 29 minutes (28 to 31). There were no intraoperative deaths.

Outcome Data
There was no postoperative mortality after Fontan in this group of patients. Analysis of the primary postoperative outcome variable demonstrated a median hospital length of stay of 8 days (5 to 51), and the median intensive care unit length of stay was 4 days (1 to 15). Analysis of secondary outcome variables demonstrated a median ventilator time of 9.5 hours (0 to 233), and a median chest tube duration of 4.5 days (2 to 14). Three patients required replacement of chest tubes after removal. Nine patients (17%) had serious postoperative infection including pneumonia (n = 4), mediastinitis (n = 2), urinary tract infection (n = 1), bacteremia (n = 1), and gastroenteritis (n = 1). There were no patients with multiple infections.

Multivariable Modeling
Complete results of analyses are seen in Table 4. Multivariable modeling revealed that the only factor associated with a WAZ at the time of Fontan was a WAZ at time of BDG discharge (p < 0.0001). No echocardiographic or hemodynamic factors were associated with a WAZ at Fontan. There was no association between underlying cardiac diagnosis of hypoplastic left heart syndrome or variant and a WAZ at Fontan.


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  		Table 4 Univariate Analyses and Multivariable Modeling for Predictors of Worse Postoperative Outcome
 
Analyses of predictors of increased total hospital length of stay identified a trend toward association between entering the Fontan with a WAZ below –2.0 and a longer hospital stay, but the only factor significantly associated with increased hospital length of stay in multivariable modeling was the presence of a serious postoperative infection (p < 0.0001). Modeling of secondary outcome variables showed an association between entering the Fontan with a WAZ less than –2.0 (p = 0.006) with development of serious postoperative infections (odds ratio 8.7 [(1.5 to 48.6]). The only factor significantly associated with longer need for postoperative ventilation was longer cardiopulmonary bypass time (p = 0.01), and there were no factors associated with longer chest tube duration. There were no variables from pre-Fontan echocardiogram or cardiac catheterization that were associated with any outcome variable. While there were a number of patients who had additional procedures performed at the time of the Fontan (n = 10), this factor was not significantly associated with an outcome variable.


   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
References
 
The significant improvement in surgical mortality in children with a single ventricle has led to increased focus on morbidities related to their heart disease and surgical palliation. Growth failure is a common morbidity in this population and may be associated with both short- and long-term problems. Children in our study had poor weight gain throughout their neonatal admission and after neonatal discharge up to the time of BDG procedure. There was some catch-up growth seen after BDG, but children remained small for age in terms of both weight and height at presentation for the Fontan procedure. Patients presenting for Fontan with WAZ less than –2.0 were more likely to have a serious postoperative infection. Postoperative infections were associated with longer postoperative length of stay.

Poor growth has been noted in infants with a single ventricle [10], and specifically in infants with hypoplastic left heart syndrome [6, 12, 20]. Infants with a single ventricle who have grown poorly are at risk for worse short-term outcome after the BDG procedure [19]. Our study has assessed the association between poor growth and short-term outcomes after the Fontan procedure. While there was some catch-up growth noted between the BDG procedure in these children, they tended to still be small for age in both weight and height at the time of their Fontan. Several studies have shown an improvement in growth after BDG palliation, but there have been mixed reports regarding the level of catch-up growth that these children experience [11, 21]. Vogt and coworkers [10] observed that there was a significant increase in z-scores for weight in the pre-Fontan period, which leveled off after completion of the Fontan. However, z-scores for height remained below normal both before and after Fontan completion. Cohen and associates [11] reported that children with single ventricles were small in both height and weight at presentation for Fontan and remained significantly underweight and shorter than the general population and their siblings in follow-up at 4.4 years (range, 3 to 5.8) after surgery. Although etiologies have been proposed for growth disturbances in children with a single ventricle, the mechanisms of this problem remain poorly understood and require further investigation.

Undernutrition and poor growth have an adverse effect on short-term postoperative outcomes in this population. The children entering Fontan with a WAZ less than –2.0 trended toward a longer hospital stay (p = 0.06). The only factor that was significantly associated with longer hospital length of stay was the presence of a serious infection in the postoperative period. We hypothesize that with a larger sample size the association between WAZ and hospital length of stay would become more evident. There was a trend toward an association between WAZ at the time of Fontan and the development of serious postoperative infections. The importance of this relationship became more apparent when the children with failure to thrive were evaluated separately. There was significant association between entering the Fontan procedure with a low WAZ (below –2) and the development of postoperative infections, indicating a threshold effect. The children with the most growth failure were at most risk for development of serious infections.

The relationship between poor nutrition and development of serious infections is well established [22]. Inadequate dietary intake leads to impaired growth, lowered immunity, mucosal damage, and susceptibility to invasion by pathogens [22]. Adequate preoperative nutrition is especially important in the postoperative period as nutritional deficiencies are known to impede wound healing [23]. De Mello and colleagues [24] demonstrated that children with poor nutritional status, defined as a WAZ less than –2, admitted to the intensive care unit for medical and surgical problems were more likely to develop culture-positive bloodstream infections. Poor nutrition in children undergoing cardiac surgery for a diverse number of congenital heart defects has also been associated with increase in postoperative infections [17]. Infants with a single ventricle undergo multiple palliative procedures during the first several years of life. Each time they have a surgical procedure, their nutritional status plays a role in their recovery.

Although there are no data on specific nutritional interventions that will improve growth in this high-risk population, there may be simple interventions that could improve their nutrition and growth. The addition of a nutrition specialist to team of individuals caring for infants with other forms of congenital heart disease has been shown to improve growth in the first few months of life [25]. Close monitoring by parents of weight gain with home scales has also been shown to lead to improved growth in patients with complex congenital heart disease [26].

Children with a single ventricle experience growth failure at a high rate. This growth failure is persistent through their presentation for the Fontan procedure. As we continue to improve surgical techniques that will improve mortality in this high-risk population, we must also look for ways to improve their nutrition and growth. Not only will these improvements lead to better short-term surgical outcome, but also improvement in nutrition may improve neurodevelopmental outcome, which is known to be poor in these patients.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

  1. Argyle J. Approaches to detecting growth faltering in infancy and childhood Ann Hum Biol 2003;30:499-519.[Medline]
  2. Bauchner J. Failure to thriveIn: Behrman RE, Kleigman RM, Jensen HB, Stanton BF, editors. Nelson textbook of pediatrics. Philadelphia, PA: Saunders/Elsevier; 2007. pp. 184-187.
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