Energy expenditure, nutrition status, and body composition in children with cystic fibrosis

APPLIED NUTRITIONAL INVESTIGATION

Energy Expenditure, Nutrition Status, and Body Composition in Children With Cystic Fibrosis Vero´nica B. Marı´n, MD, Sylvia Velandia, MSc, Bessie Hunter, MD, Vivien Gattas, Oscar Fielbaum, MD, Oscar Herrera, MD, and Erik Dı´az, MSc, PhD From the Institute of Nutrition and Food Technology, University of Chile, Santiago, Chile; and the Gastroenterology Unit and Bronchopulmonary Unit, Calvo Mackenna Hospital, Ministry of Health, Santiago, Chile OBJECTIVE: Undernutrition is a frequent complication in patients with cystic fibrosis (CF). Elevated energy requirements have been found to be 4% to 33% higher than in controls in some studies. Whether or not this is caused by a primary defect or energy metabolism is still a matter of controversy. To this end, we assessed energy expenditure, nutrition status, and body composition of clinically stable CF outpatients. METHODS: Fifteen clinically stable CF patients, ages 2 to 15 y, were paired with 15 healthy control children. Measurements consisted of anthropometry and body composition. Plasma tocopherol, retinol, and hair zinc content were measured. Resting energy expenditure was determined by indirect calorimetry. Physical activity and dietary intake were recorded by recall methods. RESULTS: Two children were nutritionally at risk according to the weight/height index, eight were normal, three were overweight, and two were obese. Body composition was similar in both groups. Zinc, tocopherol, and retinol levels were low in three, two, and three patients, respectively. Resting energy expenditures were 4.7 MJ/d (1127 ⫾ 220 kcal/d) in CF children and 4.63 MJ/d (1108 ⫾ 191 kcal/d) in control children (P ⫽ not significant). Physical activity level was sedentary in 86.6% of CF patients; the rest had a light physical activity pattern. Energy intake represented 141% of the estimated daily energy expenditure. CONCLUSIONS: Non– oxygen-dependent CF children, without acute respiratory infection, had resting energy expenditures comparable to those of matched controls. Total energy expenditure was similar to or slightly lower than that in healthy children. Dietary recommendations for CF patients need to be reassessed. Nutrition 2004;20:181–186. ©Elsevier Inc. 2004 KEY WORDS: cystic fibrosis, energy expenditure, body composition

INTRODUCTION Undernutrition and growth retardation are usually found in patients with cystic fibrosis (CF),1–3 resulting from the effect of several factors such as insufficient energy intake, malabsorption, increased energy expenditure, or some combination of these. Body composition studies in CF children as assessed by anthropometry and more robust methods such as deuterated water and total-body electrical conductivity have usually indicated a depletion of lean body mass and body fat plus a slower accretion rate of the two tissues throughout school age.4 –7 Accurate and reliable methods to estimate body composition are necessary, particularly when diagnosis of nutrition status is so relevant, as with this disease.8 Body composition measurements are very valuable for surveillance during medical and nutrition treatments of patients.5,9 In addition, it is necessary to assess the individual energy requirements because these values are compromised to different degrees depending on existing hypermetabolism, infection, and/or malabsorption. To determine individual energy requirements and nutrient allowances, it is necessary to estimate resting energy expenditure (REE) and physical activity. According to the literature, REE in CF patients has been reported to increase from 4% to 33% in relation to healthy controls or predicted values.10 Whether or not

Correspondence to: Erik Dı´az, MSc, PhD, Institute of Nutrition and Food Technology, University of Chile, Macul 5540, Santiago, Chile. E-mail: [email protected] Nutrition 20:181–186, 2004 ©Elsevier Inc., 2004. Printed in the United States. All rights reserved.

there is a primary defect in energy metabolism or whether the disease is associated solely to the clinical condition is a matter of controversy. The basis for an energy-leaking defect remains unclear, although some evidence has suggested that a primary defect may exist.9 –16 For instance, oxygen consumption studies performed with cultured fibroblasts from CF patients have indicated that the mitochondrial electron transport system is unusually active, suggesting the existence of an increased energy dissipation process.11 Others have proposed that the basic CF defect may be characterized by impaired hydrolysis of adenosine triphosphate (ATP), because the primary mutation is located in a nucleotidebinding domain in the CF gene product.12 It has been further suggested that variability in energy expenditure levels may be related to genotype, with the speculation that the effect of an abnormal ATP binding domain in the ⌬F508 allele of CF transmembrane conductance regulator may prevent the proper binding of ATP required for oxidative phosphorylation, thus providing a cellular basis for a higher metabolism by blocking movement of a high-energy phosphate bond within the cell.13 In a Chilean sample, the ⌬F508 mutation has been found in 45% of CF patients.14 Bronstein et al.15 observed that the primary CF defect does not increase energy requirements in presymptomatic CF infants. Similarly, Bines et al.16 found no significant differences in energy expenditure between newly diagnosed CF children and healthy children. No relation between energy expenditure and ⌬F508 mutation was found.16 Buchdahl et al.17 found, in a group of CF children, that the raised REE is mostly related to the degree of pulmonary dysfunction but not to nutrition status. Fried et al.18 observed a slight REE increase (4% to 5% above expected) in a 0899-9007/04/$30.00 doi:10.1016/j.nut.2003.10.010

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Nutrition Volume 20, Number 2, 2004 Arm circumference and skinfold thickness (bicipital, tricipital, subscapular, and suprailiac) were measured with a Harpenden caliper with 1-mm precision by the same observer (S.V.) according to standard techniques.24,25 Values were compared with Frisancho’s reference.26 Skinfold thicknesses were summed to describe the amount of body fat deposited in every individual. Percentage of body fat and fat-free mass (FFM) were estimated by the equations of Slaughter et al.27 Biochemical Measurements

FIG. 1. RMR in matched control and CF children (pair no. 15, female control subject and male CF subject). CF, cystic fibrosis; RMR, resting metabolic rate.

group of well-nourished CF patients as compared with normal children. It was increased, however, by 25% in those with more advanced lung disease. The likely causes of the higher REE, among others, have been attributed to respiratory inflammation, repeated infections and increased respiratory muscle activity,19 the use of drugs such as salbutamol, and/or the basal genetic defect.1,20 –22 Considering these findings and the lack of information in our country, we studied REE in a group of CF children who were not dependent on oxygen and had no acute infection after ambulatory treatment. These subjects were chosen so that we could estimate energy requirements more appropriately and restore their nutrition status whenever they were clinically stable. The present study design aimed to eliminate some of the limitations in other studies in CF children such as the presence of acute infection, severe chronic lung disease (O2 dependent), and the use of bronchodilators before the measurement, because our children were free from these conditions at the time they were measured.

MATERIALS AND METHODS Fifteen non– oxygen-dependent CF patients (nine boys and six girls) younger than 15 y were studied. All were ambulatory and treated at the respiratory, gastroenterology, and nutrition units in the Calvo Mackenna Hospital, Santiago, Chile. Fifteen healthy children matched by age, sex (except case no. 15, shown in Figure 1, because of difficulties in obtaining the corresponding control of the same age and sex), socioeconomic status, and nutrition status constituted the control group. Most CF children needed enzyme treatment (80%), with an average dose of 3213 IU/kg of body weight (range, 698 –9391 IU/kg) and 3425 IU/100 kcal (range, 709 –9538 IU). Anthropometry Weight was measured with the minimum clothing on a mechanical scale (Seca) with 0.01-kg precision and 20-kg capacity in those younger than 2 y. Older children were weighed on a mechanical scale (Seca) with 0.1-kg precision and 150-kg capacity. Recumbent length was measured in subjects younger than 2 y. Standing height in older children was measured with 1 mm of precision in both cases. Nutrition status was classified according to the National Center for Health Statistics (NCHS) standards based on the Z score index.23 Nutrition status was calculated with Epi-Info 6.0.

The following were performed as suggested by standard methods28,29: plasma measurements of albumin (g/dL; bromocresol blue), phosphate (mg/dL; phospho-molybdate complex by calorimetry at 340 ␮V), calcium (cresolphthalein complexometric method), alkaline phosphatase (4-nitrophenil phosphate), glutamic-pyruvic (GPT) and oxaloacetic transaminases (GOT) (IFCC method), percentage of prothrombin activity (Quick time), plasma carotene (␮g/dL; saponification and acid extraction), vitamins A and E in plasma (high-performance liquid chromatography), and hemoglobin (cyanmethemoglobin). Hair zinc measurements were performed by atomic absorption mass spectrometry. Dietary Intake Assessment Twenty-four– hour recall and food-frequency questionnaire were used in one occasion to estimate the intake of energy, macronutrients, and micronutrients. Usual portions were obtained from previous studies plus food weighing during the interview when necessary. The Chilean food database in Excel was used for the calculation. Information was obtained by the same observer (S.V.). Food intake adequacy was calculated in comparison with 1996 International Dietary Energy Consultative Group (IDECG) energy and protein requirements.30 Other nutrients were compared with U.S.31 recommended dietary allowances (RDAs). Specific micronutrient recommendations were obtained from the literature.32–34 There were eight CF children supplemented with vitamin ADEK, which contains vitamins A, D, and E and zinc. Mean intakes of these vitamins were 8658 ⫾ 3.6 UI/d for vitamin A, 243.1 ⫾ 126 mg/d for vitamin E, and 28.5 ⫾ 24.7 mg/d for zinc. Four children had additional vitamin E supplementation, with an average of 400 mg/d. Only one CF child received an additional 3 mg/d of vitamin A supplementation. Four children had zinc sulfate supplements (46 ⫾ 10.5 mg/d). Although this supplementation was recommended according to clinical criteria, no signs of deficiency were observed in these children. It is worth noting that these plasma nutrients are not routinely assessed in CF patients. Resting Metabolic Rate (REE) Open-circuit indirect calorimetry was used to measure oxygen consumption and CO2 production (model 2900, Sensor Medics Corp., Yorba Linda, CA, USA). The oxygen Zirconia analyzer and infrared CO2 analyzer were calibrated once a day by using calibration gases. Energy expenditure was calculated with classic equations.35 Children were measured after an overnight fast of 11 to 12 h and were free from cough, fever, or evident respiratory infection. Bronchial secretion was microbiologically assayed to discard acute infection. On the examination day, no medication or bronchodilators were allowed. Children were asked to refrain from intense physical activity the day before the test. On arrival, subjects rested comfortably on a clinical bed for 30 min. Patients were then connected to the equipment through a facemask. Data were collected continuously for at least 20 to 30 min. Physical Activity Daily physical activity was assessed in the CF group by questionnaire during weekdays and weekends. Each activity was assigned

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TABLE I. CHARACTERISTICS AND NUTRITION STATUS OF CF CHILDREN AND CONTROL CHILDREN Characteristics Age (y) Female/male Weight (kg) Height (cm) Weight-for-height (Z score) Height-for-age (Z score) Triceps (mm) Arm circumference (mm) ⌺ Skinfolds

CF (n ⫽ 15)*

Control (n ⫽ 15)*

P

8.2 ⫾ 3.8 (3.0–14.4) 6/9 26.8 ⫾ 11.3 (14.8–51.6) 122.2 ⫾ 17.9 (97.0–151.5) 0.4 ⫾ 1.2 ⫺0.7 ⫾ 1.1 10.1 ⫾ 5.3 193.5 ⫾ 36.2 31.7 ⫾ 19.5

7.9 ⫾ 3.2 (3.0–13.6) 5/10 26.0 ⫾ 10.6 (16.0–48.4) 121.9 ⫾ 16.0 (98.0–47.5) 0.2 ⫾ 1.2 ⫺0.64 ⫾ 0.9 9.0 ⫾ 4.0 192.7 ⫾ 34.6 30.3 ⫾ 16.5

NS NS NS NS NS NS NS NS

* Values are mean ⫾ standard deviation (range). CF, cystic fibrosis; NS, not significant

an energy cost and classified according to physical activity levels based on the IDECG report.30 This approach was used in CF children only as a rough estimate of energy expenditure to describe the physical activity pattern in these children. The amount of energy spent per day was calculated from the REE plus the calculated energy equivalents of physical activity calculated as above, and the thermic effect of food (7% to 10%) was calculated from the average proportions of macronutrients in the diet and a growth allowance according to age.30 Body Composition The deuterium oxide (2H2O) dilution method36 was used to assess total body water and FFM according to the appropriate hydration indices.37 Oral dose administered under fasting conditions was 0.2 g/kg of deuterium with 99.9% enrichment.38 Only children with urinary sphincter control were studied. Urine samples were collected on the dosing day. Samples were analyzed for deuterium enrichment by continuous flow mass spectrometry (Hydra, Europa Scientific, Crewe, Cheshire, UK). Statistical Analysis Means, standard deviations (SDs), correlation coefficients, and t test were performed with Excel 5.0. P ⬍ 0.05 was considered statistically significant, and Statistica 4.5 for Windows was used. Fisher’s exact test was performed to assess the association between micronutrient supplementation, laboratory assessments, enzyme supplementation, and nutrition status.

20% were above the 90th centile. Triceps skinfold indicated that 26.6% control and 33.4% CF children were below the 10th centile. Excess triceps fat stores (⬎90th centile) was found on 6.7% of control children and 13.4% of CF children. Body composition assessed by a validated method such as deuterated water showed no differences between groups. On the contrary, body composition between CF and control children were remarkably similar (Table II). Anthropometric estimates of body fat (percentage and kilograms) and FFM (kg) by Slaughter’s equations did not differ from the deuterium values, except for percentage of body fat, where a mean difference of 6% was observed in the control group. A positive association between triceps and body fat (%) was obtained by deuterium in CF and controls (r ⫽ 0.75 and 0.86, respectively). Body composition by deuterium was very close to reference values based on height and weight for each individual according to Fomon et al.39 and Deurenberg et al.40 Micronutrient Status Hair zinc levels were normal in 86.7% of CF children (mean, 153.8 ⫾ 46.8 ␮g/dL); only two children (13%) were classified as

TABLE II. COMPARISON OF BODY COMPOSITION OF CF CHILDREN AND CONTROL CHILDREN BASED ON ANTHROPOMETRY* AND DEUTERIUM†

RESULTS As expected, there were no differences in general and nutritional characteristics between the two groups of children (Table I). Both groups were remarkably similar with respect to age, weight, and height. Nutrition status was within the normal range for weight for height (W/H) and height for age (H/A). No differences were observed in the amount of body fat from skinfold thickness. According to the W/H index, 53.3% of the CF children were eutrophic (Z score within ⫾1 SD), 20% were overweight (between ⫹1 and ⫹2 SD), 13.3% were obese (⬎2 SD), and 13.3% were nutritionally at risk (⫺1 to ⫺2 SD). Similarly, height versus age was normal in 66.6% of children, 13.3% were between ⫺1 and ⫺2 SD, and 20% were stunted. Arm circumference distribution in controls was between the 25th and 75th centiles of the NCHS standard. This was not the case in CF children, 26.6% of whom were below the 10th centile and

Body fat (%) Anthropometry Deuterium Fat mass (kg) Anthropometry Deuterium Fat-free mass (kg) Anthropometry Deuterium

CF (n ⫽ 15)‡

Control (n ⫽ 15)‡

P

14.0 ⫾ 6.6 13.0 ⫾ 6.0

11.0 ⫾ 2.6 19.0 ⫾ 4.9

NS NS

4.0 ⫾ 1.6 4.0 ⫾ 1.8

3.0 ⫾ 0.9 5.0 ⫾ 1.6

NS NS

24.0 ⫾ 9.2 22.0 ⫾ 7.3

21.0 ⫾ 6.2 20.0 ⫾ 6.2

NS NS

* Calculated with equations by Slaughter et al.27 † Deuterium ⫽ hydration coefficient according to Fomon et al.39 ‡ Values are mean ⫾ standard deviation. CF, cystic fibrosis; NS, not significant

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Nutrition Volume 20, Number 2, 2004 TABLE III. RESTING METABOLIC RATE OF CF AND CONTROL SUBJECTS CF (n ⫽ 15)*

REEa Measured (24 h) Predicted (24 h) Measured (per kg) REE/kg FFMc

Control (n ⫽ 15)†

kcal

MJ

kcal

MJ

P

1127 ⫾ 220† (858–1615) 997 ⫾ 274 (783–1554) 47 ⫾ 14 (30–86) 53.4 ⫾ 9.4 (32.7–65)

4.71 ⫾ 0.9 (3.6–6.7) 4.16 ⫾ 1.1 (3.2–6.5) 0.19 ⫾ 0.06 (0.1–0.4) 0.22 ⫾ 0.04 (0.1–0.3)

1108 ⫾ 191† (872–1491) 1085 ⫾ 106 (856–1592) 53 ⫾ 11 (29–64) 56.8 ⫾ 8.1 (48–65.6)

4.63 ⫾ 0.8 (3.6–6.2) 4.57 ⫾ 0.4 (3.5–6.6) 0.22 ⫾ 0.5 (0.1–0.3) 0.23 ⫾ 0.03 (0.2–0.3)

NS NS NS NS

* Mean ⫾ standard deviation (range). † No significant differences from predicted REE CF, cystic fibrosis; FFM, fat-free mass by deuterium dilution; NS, not significant; REE, resting energy expenditure

zinc deficient (⬍100 ␮g/dL). There was no relation between hair zinc content and nutrition status by the W/H index. Mean plasma tocopherol was 7.0 ⫾ 3.6 mg/L, with only two children classified as tocopherol deficient. Retinol was normal in all but three children (cutoff value, 300 mg/L); mean plasma levels were 424.3 ⫾ 125 ␮g/dL. Biochemical Determinations Hemoglobin, albumin, plasma proteins, and glycemia were normal in all children. Cholesterol, GOT, and GPT were above the normal ranges in 26.6%, 9.0%, and 9.0% of children, respectively. Alkaline phosphatases were elevated in all CF children. Carotene, prothrombin, and calcium were below acceptable levels in 46%, 15.4%, and 6.6% of children, respectively.

in both groups. REE and FFM were strongly associated (r ⫽ 0.85) in the entire group. Total Energy Expenditure On average, CF children spent 6.5 ⫾ 1.5 MJ/d (1552 ⫾ 359 kcal/d) and had a sedentary physical activity pattern corresponding to 1.5 ⫾ 0.3 times the REE (Table IV). The CF children spent most of the daytime on sedentary activities (89%) and very little on light to moderate activities. Total energy expenditure (TEE) was highly correlated to FFM by deuterium (r ⫽ 0.79) and energy intake (r ⫽ 0.48). Mean energy intake was equivalent to 141 ⫾ 36% of estimated TEE, representing an excess of 2.3 ⫾ 1.9 MJ/d (560 ⫾ 468 kcal/d) or 0.1 ⫾ 0.1 MJ/kg of body weight (26 ⫾ 25 kcal/kg).

DISCUSSION Food Intake The mean energy intake of CF patients was in excess of the estimated requirements according to the 1996 IDECG,30 reaching 127 ⫾ 21% on average and ranging from 100% to 161%. Total energy intake comprised 16% protein, 55% carbohydrate, and 29% fat. Micronutrient intakes for vitamins B1 and B2, niacin, and vitamin C were, on average, within the RDA for healthy children. Vitamins A and E were in excess of the recommended intake for normal children but were insufficient for CF children, whose intake ranged from 363 to 909 ␮g/d of retinol equivalents and 70 to 200 mg/d of ␣-tocopherol equivalents (68% for vitamin A and 100% for vitamin E). Calcium, iron, and magnesium were adequate. Average zinc intake was below the RDA (intake 6.4 ⫾ 3 mg/d versus RDA 10 to 15 mg/d).

Our study agrees with results reported by others who found that REE in ambulatory CF children, with light or moderate lung dysfunction (non-oxygen dependent), is similar to expected values1,18 or slightly increased, without significant differences in relation to their control group, matched by nutrition status and sex.1,41 Other studies have reported larger differences reaching 21% to 52% excess in REE, but their measured REE was compared with formulas.22,27 The use of equations such as Harris-

TABLE IV. TEE AND ENERGY BALANCE IN THE CHILDREN WITH CYSTIC FIBROSIS Mean ⫾ SD (range)

Resting Metabolic Rate There were no significant differences between groups with respect to total REE (kcal/d), REE/kg of body mass, or corrected by FFM (Table III). Measured REE values were similar to the estimates of the Food and Agriculture Organization (FAO)/World Health Organization (WHO) equations in both groups, reaching on average 105% in CF and 103% in controls. Individual REE values are shown in Figure 1. There is a great similarity between the matched CF and control comparisons. On average, they differed by 0.41 MJ (98 kcal), with most of the differences being approximately 0.418 ⫾ 0.5 MJ (100 ⫾ 137 kcal) or less. Only one pair had larger differences reaching 1.14 MJ (273 kcal). Resting metabolic rate was associated with nutrition status as measured by W/H (r ⫽ ⫺0.46) and triceps skinfold (r ⫽ ⫺0.54)

kcal Estimated TEE (24 h) TEE (per kg) Physical activity (24 h) TEE/REE (PAL) Intake (24 h) Balance (%)

1552 ⫾ 359† (951–2261) 64 ⫾ 18 (40–114) 255 ⫾ 138 (97–644) 1.5 ⫾ 0.3 (0.8–1.7) 2112 ⫾ 462† (1414–3346) 141 ⫾ 36 (82–230)

MJ 6.48 ⫾ 1.5 (3.9–9.4) 0.26 ⫾ 0.07 (0.1–0.5) 1.0 ⫾ 0.57 (0.4–2.7) 1.5 ⫾ 0.3 (0.8–1.7) 8.8 ⫾ 1.92 (5.9–13.9) 141 ⫾ 36 (82–230)

† Estimated TEE versus intake, P ⫽ 0.001. PAL, physical activity level; REE, resting energy expenditure; TEE, total energy expenditure

Nutrition Volume 20, Number 2, 2004 Benedict,42 FAO/WHO,43 and Schofield44 have been shown to have a limited application in children, particularly ill ones.45 The greater error was for the Harris-Benedict, which was found to overestimate REE by 13% to 52%, and the other two equations underestimated REE by 16% to 12%, respectively.45 This study attempted to control all factors usually involved in REE increment such as acute infection, severe chronic lung disease (O2 dependent), and the use of bronchodilators before the measurement.1,19 The lack of control for these factors can partly explain the observed differences in REE in relation to other studies. Another explanation for differences among studies could be related to the fact that not many, including our study, have controlled by genotype characteristics. CF homozygous children have been reported to have higher REE increments than CF heterozygous children.22,46 Nevertheless, other investigators have found that higher than expected REEs are not explained by genotype. This is the case for Davies et al.47 and Bines et al.16 who found that energy expenditure did not respond to genotype differences in children followed for 1 y. The high correlation obtained for FFM (by deuterium) and REE confirms that FFM is the most important determinant of energy expenditure under resting conditions. This has been reinforced by several investigators who questioned the use of body weight as a proper expression to detect metabolic changes in ill patients. The precise measurement of body composition was found to be crucial in these type of studies. Additional evidence was obtained by Allen et al.48 in well-nourished children similar in age to those in our study. They used multiple regression analyses to show that 78% of REE variation is due to FFM (r2 ⫽ 0.84 and 0.77 in males and females, respectively). Other factors such as pancreatic insufficiency and liver disease together have explained 84% of the REE variance. Despite the fact that FFM did not differ between males and females, females showed higher energy expenditure when compared with CF males and control females. Thus, sex differences in REE remain to be explained by other factors at the cellular level, early pubertal onset, or others.49 Our study did not have this problem because CF subjects were matched with controls by sex (except case no. 15 in Figure 1, where the control is female and the CF subject is male). Arm circumference showed that about 25% of CF children had deficits (⬍10th centile) and 20% had excess (⬎90th centile), whereas neither deficit nor excess was found for control children. This situation did not agree with the results obtained from the deuterium test or triceps skinfold. The most likely explanation for this finding is some degree of muscle mass reduction because arm skinfold thicknesses were the same. It does not mean a lower FFM in the whole body. On the contrary, CF children had a slightly higher FFM (by about 2 kg) when compared with control children as assessed by more robust measurements such as body composition by deuterated water. TEE has been found to be 25% to 27% higher in CF than in control children, whereas other studies have found no differences. These inconsistent results20,50 seem to respond to clinical and genotypic variations among the studied children and to the use of different methods to estimate TEE, e.g., heart rate monitoring, doubly labeled water, and activity records. Studies performed in young adult CF patients have shown no differences in TEE when assessed by doubly labeled water.51 Another relevant study using doubly labeled water was done in clinically normal infants followed throughout the first year of life.47 These researchers found that CF children did not differ from controls in the first 2 mo, but by the age of 12 mo CF infants had 19% higher TEE (113 versus 97 kJ · kg⫺1 FFM · d⫺1, respectively). Daily physical activity showed that 86.6% of children were involved in sedentary activities, with little time devoted to moderate or intense activity. The same has been found in wellnourished Chilean children of the same age groups when using a similar activity recall method52,53 indicating that these children were equally inactive (TEE/REE range, 1.42–1.50). Even though

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physical activity estimates obtained by recall are limited by its reliability and accuracy, this is the most practical way to classify physical activity in children. Its limitations can be greatly reduced by the use of trained observers. In our study this information was gathered by one of the authors (S.V.). Information on physical activity patterns in CF children is scarce, and exercise is rarely prescribed despite the finding that it improves respiratory exchange. Thus, exercise incorporated into the physiotherapy program is indicated.54,55 Energy intake on average was 127% of estimated requirements, but much greater, 141%, when compared with the estimated TEE. Although the excess in energy intake agrees with recommendations for CF children,33 this level of energy intake is considered inappropriate for patients in a condition similar to ours. Based on their energy expenditure, our children were in positive energy balance, which could partly explain why important proportions of CF children was overweight and obese (20% and 13%, respectively). Methodologic errors are certainly involved in dietary assessments, but dietary intake and nutrition status point in the same direction. Certainly another way of explaining this issue is to assume that excess energy intake is wasted through higher fecal losses. In our study, this was probably true for 25% of CF children in whom Sudan⫹⫹ was found. This finding however, was not associated with nutrition status. Other sources to explain excess energy disposal is the thermic effect of food and energy for growth requirements; nevertheless, these two are always too small to produce a great impact. This study, however, considered both variables to calculate CF children’s energy requirements. Energy supplied by carbohydrate (55 ⫾ 4%), fat (29 ⫾ 3%), and protein (15 ⫾ 3) was within the recommended range for healthy children, in accordance with other studies in CF children,56 –58 but do not satisfy the recommended 40% fat for CF children,33,59 based on supposedly higher-than-normal fecal fat losses. In relation to micronutrients, zinc intake was inadequate in 64% of children, which agrees with similar studies on CF children56,58,60 and those in Chilean healthy children.61,62 Zinc nutrition status as assessed by hair content showed normal values in the majority of cases (86.7%). Considering that nearly half of the study group had zinc supplementation, it is necessary to question how appropriate the nutritional recommendation is or how reliable the hair zinc content is for zinc nutrition assessment. With regard to the presence of pancreatic insufficiency, the degree of biliary salt alterations, and liver plus gallbladder dysfunction in CF children, it is expected that fat-soluble vitamin deficiency would need to be corrected with appropriate supplementation.63 Wilson et al. reported that these vitamins were deficient in 35% of their patients. Six of our patients were supplemented with vitamins A, E, and K. Serum vitamin A and E levels were normal in the majority of cases. Routine assessment of vitamins A and E and minerals such as iron and zinc are recommended at least once a year for CF patients.33 We conclude that energy requirements for CF children are similar to those for normal healthy children. Their food intake, in particular energy intake, was higher than their requirements, emphasizing the urgent need to reassess nutritional recommendations for these patients to avoid overweight and obesity.

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