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J Thorac Cardiovasc Surg 1994;107:374-0380
© 1994 Mosby, Inc.
Surgery for Congenital Heart Disease |
Glasgow, Scotland, and Cambridge, England
Glasgow, Scotland
Funded by grants from the Association for Children with Heart Disorders and the Greater Glasgow Health Board Research Support Group.
Read at the Seventy-third Annual Meeting of The American Association for Thoracic Surgery, Chicago, Ill., April 25-28, 1993.
Address for reprints: Ian M. Mitchell, FRCS, Department of Cardiac Surgery, Leeds General Infirmary, Great George Street, Leeds LS1 3EX, England.
Abstract
Failure to thrive is a common feature of children with congenital heart disease. Whether this is the result of poor nutrition or an abnormally high basal metabolic rate is unknown, yet the state of nutrition has a profound effect on the metabolic response to injury and strongly influences the outcome of surgical treatment. The aim of this study was therefore to measure the preoperative and postoperative energy requirements of children with congenital heart disease. Eighteen children (aged 4 to 33 months) were given two oral doses of doubly labeled water (H218O and2H2O), the first 1 week before operation and the second 6 hours after the end of cardiac surgery. By measuring the relative loss of each isotope from the body water pool, we were able to calculate the rate of carbon dioxide production and therefore total energy expenditure. In five patients, energy expenditure was clearly elevated, suggesting that a raised basal metabolic rate is an important factor in the observed failure to thrive in at least a proportion of such children. Postoperatively, energy expenditure fell to values below normal for healthy children (not having an operation), which suggests that the stress of surgery leads to smaller energy requirements than have previously been thought. (J THORAC CARDIOVASC SURG 1994;107:374-80)
Children with congenital heart disease are frequently undernourished. Although the term undernutrition and the criteria leading to such a diagnosis are poorly defined, there is no doubt that many biochemical and anthropometric markers of nutritional well-being are abnormal in this group of patients.
1-6 Why this should be so is uncertain, but there are three possible explanations: either energy intake is inadequate, the ingestion or absorption of nutrients must be impaired, or the metabolic demands of the child must be abnormally high.
Because evidence exists of an association between malnutrition and poor wound healing, 7-9 impaired immunity, 10-13 reduced muscle function, 14 and an increased risk of postoperative pneumonia, 15 the importance of any preexisting malnourishment becomes clear. Although the majority of children make a swift recovery and are able to recommence a normal diet on the first or second day, the growing trend for earlier and more complicated operations inevitably means that a proportion of patients will have a prolonged stay on the intensive care unit. These children are likely to be supported with a ventilator and may have a persistent ileus, both of which complicate a return to a normal diet. With poor reserves, the inability to reinstate adequate nutrition soon after the operation might be expected to carry more serious consequences for recovery in this particular population than in others undergoing cardiac operations.
Trauma produces a change in the metabolic rate, 16 yet the postoperative requirements of children undergoing cardiac operations remain unknown. It is just as important to provide sufficient nutrition, however, as it is to avoid excess nutrition and fluid overload. The aim of this study was therefore twofold: (1) to measure the energy expenditure of a cohort of children with congenital heart disease and to compare these results with the energy expenditure of age-matched normal healthy children; (2) to determine the energy requirements after cardiac surgery.
PATIENTS AND METHODS
Patients
Energy expenditure was measured in 18 children with congenital heart disease in the week before corrective or palliative cardiac operations and then in 17 of these children in the week immediately after the operation. The study was approved by the local hospital ethics committee, and informed consent was obtained from the parents. There were 11 boys and 7 girls (6 in the postoperative study), with ages ranging from 4 to 33 months. Three patients underwent operations not involving cardiopulmonary bypass. Patient details are summarized in Table I.
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17 and first applied to human beings by Schoeller and van Santen 18 in 1982. The technique depends on the oral administration of a bolus loading dose of water, labeled with two stable isotopes (2H2O and H218O), plus the following theoretical assumptions, which have been discussed in detail elsewhere 19:
In practice, water is predominantly removed from the body as urine. Because urine is simple to collect, the declining isotopic enrichment of the total body water pool can be monitored over a specific period of time by analyzing daily urine samples. As this decline follows an exponential pattern, a plot of the logarithm of the urinary enrichment versus time is linear. Because 18O is lost as expired carbon dioxide as well as water (e.g., urine, sweat), the regression line for 18O is steeper than that for deuterium. The difference in the elimination rate of the two isotopes is therefore equivalent to the rate of production of carbon dioxide, such that:
CO2 production rate = N(ko—kd)/2
where N is the total body water in moles and ko and kd are the elimination rate constants for 18O and 2H, respectively. This basic equation was then modified to take into account fractionation.
Provided that the respiratory quotient (RQ) and the rate of carbon dioxide production (VCO2) are known, the rate of oxygen consumption (VO2) can be calculated from this formula:
This formula can then be substituted in Wier's formula 20 to calculate the energy expenditure (EE):
EE = 3.941 VO2 + 1.106 VCO2 — 2.17 N
The energy expenditure calculated by this method is equivalent to the mean total number of kilocalories used by each child during the study period. Although this can be quoted in terms of body weight, because body weight varies according to the total body water content (which is influenced by many factors, particularly in this context by the degree of heart failure), a more accurate way of comparing the energy expenditure in different populations is by relating it to the fat free mass. 21 This latter was calculated from measurements of the 18O dilution space, assuming the level of hydration in lean tissue to be constant. Values for the percentage of water in lean tissue were taken from standard reference data. 22
Experimental details
Samples of home tap water were collected from each child participating in the study, together with samples of hospital tap water, commercially prepared milks, and, for the postoperative studies, samples of intravenous fluids and transfused whole blood. Isotope enrichments from these data and from pre-dose urine samples were measured and used to modify the calculations of energy expenditure described earlier.
Aliquots of two stable isotopes of water, 2H2O and H218O (Delta Isotopes, Crewe, Cheshire, England), were administered (orally) to each child in doses equivalent to 0.28 gm/kg body weight of 100% H218O and 0.1 gm/kg body weight of 99% 2H2O for children less than 1 year of age and 0.15 gm/kg body weight of 100% H218O and 0.05 gm/kg body weight of 99% 2H2O for children over 1 year of age (because the water turnover is lower in older children, less isotope is required). In the preoperative study, the doubly labeled water was given 1 week before the operation, and in the postoperative study it was administered nasogastrically 6 hours after return to the intensive care unit, once the child was in a hemodynamically stable condition. We assumed that each dose was fully absorbed, because even with an ileus there is a free exchange of water molecules across gastric mucosal cell membranes. Although a large volume of water may be aspirated from the stomach 1 hour after administration, previous studies have shown that this will contain only 1% of the labeled dose. 23 Nasogastric aspiration was nevertheless not permitted for 6 hours after administration of the 18O and 2H.
The doubly labeled water technique assumes that water loss is constant throughout the study; yet in the postoperative period this may not be so, particularly with the use of artificial ventilation and diuretics. Deviations from a constant water loss would however be reflected in a high error in both the 18O and 2H slopes. Such errors were not found. Therefore, although water loss may not be absolutely constant, the variations are sufficiently small to allow the technique to be used in the present context.
The child's weight was accurately recorded at the beginning and end of each study period, and urine samples were collected on the morning after administration of doubly labeled water and for 6 days thereafter. Deuterium and 18O were then analyzed by the MRC Dunn Nutrition Unit, Cambridge, by means of isotope-ratio mass spectrometry (Aqua-Sira model, VG Isogas, Cheshire).
In common with other studies, a mean respiratory quotient of 0.85 was assumed in the calculation of energy expenditure. 24-26 Although some variation in this would be expected during the course of a typical day, over a period of several days the mean value would change very little. 24 Even in the unlikely event that the true respiratory quotient was 0.7 or 1.0, the maximum error in the calculation of total energy expenditure would only be ±3%. 24
Energy expenditure was calculated as described earlier and was compared with normal values obtained from previous studies at the MRC Dunn Nutrition Unit, Cambridge [P.S.W. Davies, personal communication]. Normal values for energy expenditure are given in Fig. 1.
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The preoperative and postoperative energy expenditure of each child was calculated and compared with normal values in age-matched control subjects (Table II). Preoperatively, energy expenditure in children with congenital heart disease was not significantly different from normal (p > 0.05; Wilcoxon test). However, when assessed individually, energy expenditure was more than 20% above normal in 5 of 18 children, which suggests that an elevated basal metabolic rate is an important factor in the observed failure to thrive in at least a proportion of children with congenital heart disease.
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Six children had cyanotic congenital heart defects, but the presence or absence of cyanosis did not appear to affect energy expenditure.
In the week immediately after the operation, energy expenditure fell sharply to reach levels significantly below the preoperative values (p < 0.001; Wilcoxon test) and significantly below those in normal healthy (age-matched) children not undergoing operations (p < 0.001; Wilcoxon test).
These changes in energy expenditure were similar both in children undergoing thoracotomy and in children undergoing operations involving cardiopulmonary bypass. However, the differences between the preoperative energy expenditure in the study patients and the energy expenditure in normal healthy children were greater in the thoracotomy group, albeit not quite reaching statistical significance (p = 0.058; Mann-Whitney test). Although the energy expenditure in the three patients who had a thoracotomy decreased to subnormal levels after the operation, the values reached were generally not as low as those found in the patients who had undergone cardiopulmonary bypass. This difference was again not statistically significant (p > 0.05; Mann-Whitney test), but the sample size may be too small to allow significance to be readily demonstrated.
DISCUSSION
Children with congenital heart disease may be small for a variety of reasons (e.g., genetic defects, heredity). Even when a congenital cardiac defect is present, growth retardation may be only indirectly related, perhaps being due to chronic tissue hypoxia or an increased prevalence of respiratory disease (resulting from pulmonary congestion and a left-to-right shunt 1). Nevertheless, genuine growth failure has been associated with a variety of congenital cardiac defects, particularly those leading to congestive heart failure 4 and cyanosis. 2, 3, 27 In this study, energy expenditure did not appear to be correlated with the presence or absence of cyanosis, nor was there any correlation with the severity of the defect. This is in keeping with other observations (reported elsewhere 6) in which we found the severity of growth failure to be unrelated to the severity of the cardiac defect, but contrasts with the results of two studies from the 1960s, 2, 4 although in these the assessment of nutrition was based solely on the measurement of height and weight, which are important parameters, but only two of many that are relevant.
Discounting specific causes of failure to thrive and the possibility of an inadequate energy intake, the poor growth seen in children with congenital heart disease must result from either poor assimilation of food or increased demands. In this study, there was no overall statistically significant difference in energy expenditure between normal healthy children and those with congenital heart disease. Nevertheless, energy expenditure was elevated by 20% or more in 28% of children and, at least in these, hypermetabolism must account for the observed failure to thrive. This observation is in keeping with the hypermetabolism observed in adults with congestive heart failure and the one study that has investigated this problem in children. 28 Why it should occur is uncertain but may depend on an increase in catecholamine production and the abnormal demands of certain specific organs, for example, the muscles of respiration, the myocardium, and the hematopoietic system. In patients with congestive cardiac failure the increased respiration and the increased energy demands of the dilated heart both contribute to the associated increase in oxygen consumption. 29 Furthermore, in some malnourished infants there may be relative overgrowth of the brain; 30 because the brain has a high metabolic rate and because only minor changes are compatible with conscious life, this overgrowth may also account for some of the overall hypermetabolism.
The metabolic rate is altered after trauma, 16 and it is generally accepted that energy expenditure increases. The extent of the increase has variously been reported as minimal to as much as 25%, 31-37 partly as a result of discrepancies in the severity of the illness and the type of operation performed and partly as a result of the preexisting nutritional status of the patient, factors that are all known to influence energy expenditure. 38 Also, the methods used to measure energy expenditure and the difficulty in converting the measured resting energy expenditure (or sometimes the basal metabolic rate) to the true total energy expenditure adds to the apparent discrepancy. The doubly labeled water technique has the advantage that it provides an average total energy expenditure over a 1-week period and is not unduly influenced by bursts of activity and short-term fluctuations. The technique is also noninvasive and simple to perform, and it causes minimal upset to the patient.
Only two previous studies have used the doubly labeled water technique to measure energy expenditure in a surgical population. In the first of these, a postoperative increase of 18% was recorded in seven women undergoing laparotomy and bowel resection for Crohn's disease. 37 These patients, however, received total parenteral nutrition throughout the study period and were monitored for only a short length of time; a single dose of doubly labeled water was used for both the preoperative and postoperative studies. In addition, results are quoted as energy expenditure per patient per day, with no regard to either the patient's weight or, more important, to the fat free mass.
In the second study, energy expenditure was measured in 16 adults in the 10 days before and after coronary artery bypass grafting. 39 Depending on the degree of intraoperative cooling, energy expenditure (in relation to fat free mass) increased by between 3.3% and 5.8%. Because the activity level in the postoperative period was considerably reduced, this change probably does represent a genuine increase in the basal metabolic rate, although the increase may be partly explained by the withdrawal of ß-adrenergic blockers, which are known to reduce energy expenditure through antisympathetic actions. 40, 41
In contrast, we have demonstrated a significant postoperative reduction (of approximately 32%) in the energy expenditure of children with congenital heart disease, values falling below those expected in normal children not undergoing operation. This observation suggests that, at least in the short term, the nutritional requirements of children after cardiac operations are considerably less than have previously been thought; therefore the consequences of providing a suboptimal energy supply in the postoperative period may be less than might have been expected. This theory is in keeping with the observation that postoperative nitrogen losses are less in malnourished than in well-nourished patients, as a result of adaptation to a cachectic state and the development of nitrogen and protein-sparing metabolic cycles. 42 The preoperative undernutrition seen in children with congenital heart disease may therefore have a protective effect in terms of postoperative adaptation to a reduced food supply.
Irrespective of the exact nutritional requirements, however, an accurate fluid balance must be maintained in small children, particularly after cardiopulmonary bypass. It is therefore essential that both the volume and the calorie content of feeds are appropriate, particularly because of the evidence that an excessive calorie intake at this stage may actually be harmful (a high glucose and lipid intake, for example, can result in an increased carbon dioxide production, which may compromise respiratory function, especially in a ventilator-dependent patient). 34
Several possible explanations have been proposed for the apparent reduction in postoperative energy expenditure. In all children, the degree of activity is reduced after surgical procedures, with some patients requiring prolonged periods of ventilation and sedation, both known to reduce oxygen consumption and energy expenditure. 43, 44 The energy expenditure measured in this study was an average for a 7-day period. It was impossible, however, to determine whether this expenditure was higher or lower during the first few days and, although deviations in energy expenditure would affect the elimination slopes for 18O and 2H and result in high errors, such errors were not seen.
The brain is the major energy-consuming organ in the first year or two of life (accounting for 60% of the total energy requirement); sedation and increased periods of sleep could therefore contribute to the overall reduction in energy demand. In addition, with a high ambient temperature on the ward and the use of incubators or baby heaters on the intensive care unit, the child's need to generate heat (and the calorie cost of doing so) may be reduced. Despite the possibility that reduced activity levels may account for some of the apparent reduction in postoperative energy expenditure, the clinical value of this observation remains, because the children studied underwent recovery patterns that were typical of any group after surgical treatment for congenital heart disease.
The stress of major surgery may lead to a temporary period of growth stagnation so that energies may be concentrated on wound healing and recovery. Because growth is a net calorie-consuming process, a temporary halt may be seen as a reduction in total body energy expenditure.
The hormonal balance after operation may favor reduced energy expenditure; thyroid hormones, for example, are among the major determinants of the metabolic rate, but plasma concentrations are reduced for the first 5 to 7 days after cardiac surgery, favoring reduced substrate use. 45
Finally, although the preoperative energy expenditure may be high in some children, presumably related to the cardiac defect, it is still unclear which organ system or systems are actually responsible for the increased calorie consumption. It is possible that some systems that have been deprived of an adequate energy supply might take time to readjust to normality, with energy expenditure in the interim appearing to be reduced.
Appendix: DISCUSSION
Dr. Edward L. Bove(Ann Arbor, Mich.)
Could some of your results have been due to your patient selection? A number of your patients appear to have been particularly malnourished before the operation. Would you expect different results if some of these were not so malnourished, as were the children with longstanding left-to-right shunts?
Second, consistent with what you have found, our group has noted that the caloric requirements needed to maintain a positive nutritional and protein balance appear to be far less than have been previously published—in the range of 80 to 90 calories per kilogram. Do you have any data to either support or refute that?
Dr. Bradley S. Allen, (Chicago, Ill.)
You said you measured these metabolic changes every day during the first postoperative week, but I did not see a graph depicting what happened on each individual day. Did you measure higher metabolic rates immediately after the operation, when patients may have higher levels of circulating catecholamines, and were these changes decreased over the next several days? Conversely, was this lower metabolic rate increasing toward normal at the end of the week? Can you now discuss the trends over this entire 1-week period.
Mr. Mitchell
Thank you. Although I did not present the data, we studied these children as part of a larger series and we evaluated their nutritional well-being. We studied 30 parameters, both biochemical and anthropometric, and found that children with congenital heart disease are universally small and undernourished. This is not just a feature of the more complicated abnormalities but is found equally in the more straightforward cases, which I think is interesting.
We found no difference in our results in the presence of cyanosis, shunts, or any other variable.
In terms of individual points on the graph making a difference, by taking daily urine samples we obtained seven measurements. These can be plotted as the declining enrichment against time. However, plotting the logarithm of the enrichment against time removes much of the variability caused by individual data points.
Some of these patients received ventilatory support for the first few days, and one may think that ventilation would affect the carbon dioxide production. However, plotting the logarithm of the enrichment against time, as opposed to the raw data, eliminates spurious effects of individual data points.
Our purpose is not to look at one particular measurement of energy expenditure on any particular day. We were measuring an average of what has happened over the whole week. It is possible, of course, that if we had looked at this measurement during the third or fourth week, energy expenditure would have increased to normal.
The interesting point is that in the immediate postoperative period energy expenditure is very small. I think a lot of people do not think about feeding their patients for the first few days, and maybe this explains why they see no adverse effects. We have shown that there is not such a need to feed these patients early on, although logically one would think that because they are small and undernourished, they would not do very well if left unfed.
Footnotes
From the Department of Cardiac Surgery, Royal Hospital for Sick Children,a Yorkhill, Glasgow, Scotland, and the MRC Dunn Nutrition Unit,b Downhams Lane, Cambridge, England. 
References
This article has been cited by other articles:
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  I. L. Ackerman, C. A. Karn, S. C. Denne, G. J. Ensing, and C. A. Leitch Total But Not Resting Energy Expenditure Is Increased in Infants With Ventricular Septal Defects Pediatrics, November 1, 1998; 102(5): 1172 - 1177. [Abstract] [Full Text]
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 R. J. Gretebeck, D. A. Schoeller, R. A. Socki, J. Davis-Street, E. K. Gibson, L. O. Schulz, and H. W. Lane Adaptation of the doubly labeled water method for subjects consuming isotopically enriched water J Appl Physiol, February 1, 1997; 82(2): 563 - 570. [Abstract] [Full Text] [PDF]
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