AJCN North Carolina Research Campus
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Purchase Article
Right arrow View Shopping Cart
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Kashyap, S.
Right arrow Articles by Schulze, K. F
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Kashyap, S.
Right arrow Articles by Schulze, K. F
Agricola
Right arrow Articles by Kashyap, S.
Right arrow Articles by Schulze, K. F
American Journal of Clinical Nutrition, Vol. 74, No. 3, 374-380, September 2001
© 2001 American Society for Clinical Nutrition

Original Research Communication

Effects of quality of energy on substrate oxidation in enterally fed, low-birth-weight infants1,2

Sudha Kashyap, Helen M Towers, Rakesh Sahni, Kiyoko Ohira-Kist, Kirsten Abildskov and Karl F Schulze

1 From the Division of Neonatal-Perinatal Medicine, Department of Pediatrics, Babies and Children's Hospital, College of Physicians and Surgeons, Columbia University, New York.

2 Reprints not available. Address correspondence to S Kashyap, Department of Pediatrics, College of Physicians & Surgeons, Columbia University, 630 West 168th Street, New York, NY 10032. E-mail: sk48{at}columbia.edu.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Carbohydrate and fat may differ in their ability to support energy-requiring physiologic processes, such as protein synthesis and growth. If so, varying the constituents of infant formula might be therapeutically advantageous.

Objective: We tested the hypothesis that low-birth-weight infants fed a diet containing 65% of nonprotein energy as carbohydrate oxidize relatively more carbohydrate and relatively less protein than do infants fed an isoenergetic, isonitrogenous diet containing 35% of nonprotein energy as carbohydrate.

Design: Sixty-two low-birth-weight infants weighing from 750 to 1600 g at birth were assigned randomly and blindly to receive 1 of 5 formulas that differed only in the quantity and quality of nonprotein energy. Formula containing 544 kJ•kg-1•d-1 with either 50%, 35%, or 65% of nonprotein energy as carbohydrate was administered to control subjects, group 1, and group 2, respectively. Groups 3 and 4 received gross energy intakes of 648 kJ•kg-1•d-1 with 35% and 65% of nonprotein energy as carbohydrate. Protein intake was targeted at 4 g•kg-1•d-1. Substrate oxidation was estimated from biweekly, 6-h measurements of gas exchange and 24-h urinary nitrogen excretion.

Results: Carbohydrate oxidation was positively (r = 0.71, P < 0.0001) and fat oxidation was negatively (r = –0.46, P < 0.001) correlated with carbohydrate intake. Protein oxidation was negatively correlated with carbohydrate oxidation (r = –0.42, P < 0.001). Fat oxidation was not correlated with protein oxidation. Protein oxidation was less in infants receiving 65% of nonprotein energy as carbohydrate than in groups receiving 35% nonprotein energy as carbohydrate.

Conclusion: These data support the hypothesis that energy supplied as carbohydrate is more effective than energy supplied as fat in sparing protein oxidation in enterally fed low-birth-weight infants.

Key Words: Low-birth-weight infants • substrate oxidation • oxygen consumption • carbon dioxide production • respiratory quotient • energy expenditure • nonprotein energy


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The current goal of nutritional management of preterm infants, as recommended by the American Academy of Pediatrics (1), is to achieve a postnatal growth approximating that of a normal fetus of the same postconceptional age. Although rates of weight gain similar to or greater than the intrauterine rate have been achieved by feeding preterm infants enriched diets (2–6), invariably, these diets lead to a disproportionate increase in body fat. The reasons for this postnatal failure to maintain the high fetal rates of protein synthesis relative to fat deposition are not known. One difference between fetal and neonatal life is the relatively greater dependence of the fetus on carbohydrate rather than fat as a source of energy. If the fetus is relatively more dependent on carbohydrate than fat, then it is possible that the same is true of infants of comparable maturity after birth. There is some evidence that, joule for joule, use of carbohydrate as an energy source is more effective in supporting protein accretion than use of fat (7–10). There are investigators, however, who assert that this effect is transient (11). This hypothesis remains untested in enterally fed, low-birth-weight (LBW) infants. Should there be significant differences in the growth-supporting effects of fat and carbohydrate, these differences might be exploited in the design of formulas for premature infants and human milk supplements.

Many studies have investigated the effect of varying the source of nonprotein energy on substrate use in parenterally fed, newborn infants (12, 13). However, the consequences of variations in the quality of nonprotein energy have not been investigated in enterally fed, preterm infants. In adults, substrate oxidation is dependent on the relative proportions of carbohydrate and fat in the diet (14, 15). The purpose of the present study was to test the hypothesis that LBW infants fed diets containing 65% of nonprotein energy as carbohydrate oxidize relatively more carbohydrate and relatively less protein than do infants fed isoenergetic, isonitrogenous diets containing 35% nonprotein energy as carbohydrate.


   SUBJECTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Experimental design
LBW infants without gastrointestinal, renal, or severe pulmonary disease and who weighed between 750 and 1600 g at birth were stratified by birth weight into 1 of 3 ranges: 750–1000, 1001–1300, or 1301–1600 g. The infants were then randomly assigned by a blind draw to receive 1 of 4 experimental formulas or a control formula. All formulas were designed to provide protein intakes of 4 g•kg–1•d–1 when fed at 180 mL•kg–1•d–1. The control formula and formulas 1 and 2 were designed to provide 502 kJ•kg–1•d–1 when fed at the same volume. The carbohydrate and fat contents of the formulas were varied to provide 35% of nonprotein energy as carbohydrate in formula 1, 65% of nonprotein energy in formula 2, and 50% of nonprotein energy in the control formula. Formulas 3 and 4 were designed to provide higher energy intakes of 628 kJ•kg-1•d–1 when fed at 180 mL•kg–1•d–1, with nonprotein energy as 35% and 65% from carbohydrate. All formulas were made specifically for this study by Ross Laboratories (Columbus, OH). Formula bottles were number coded and the investigators were not informed of the code until the study was completed. The protein content of the formulas was modified bovine milk protein with a ratio of whey protein to casein of 60:40. The carbohydrate content of the formulas was composed of equal amounts of lactose and corn syrup solids, and fat was provided as a mixture of coconut, soy, and safflower oils. The electrolyte, mineral, and vitamin contents of the formulas were similar and met recommended dietary intakes (1). The measured energy content of the formulas were slightly higher than what was planned in the study design. The actual macronutrient intakes of the 5 groups are shown in Table 1Go. Protein concentrations in the specially designed formulas varied, which resulted in a slightly lower absolute protein intake by the infants randomly assigned to group 4 than in infants in group 3.


View this table:
[in this window]
[in a new window]
  		TABLE 1 Dietary intakes of study groups1
 
The study was approved by the Institutional Review Board of the College of Physicians and Surgeons of Columbia University. Written, informed parental consent was obtained before infants were enrolled in the study.

Experimental protocol
Shortly after enrollment and as soon as medically permitted, the infants were transferred to the General Clinical Research Center, where they remained until discharge. The assigned formula was administered as soon as enteral feedings could be tolerated by the infant. The volume of the formula was increased as tolerated until the desired intake of 180 mL•kg–1•d–1 was achieved. This volume was then maintained throughout the study until the infant's weight reached 2200 g or until the infant was discharged from the hospital. During this time, infants were cared for in servo-controlled, single-walled incubators under thermoneutral conditions. The formulas were administered either by orogastric tube or, if tolerated, by nipple. Vitamin E [25 mg (25 IU)] and a mixture of vitamins A [450 µg (1500 IU)], C (35 mg), and D [10 µg (400 IU)] were administered daily once feedings were established. The volume of formula intake, nitrogen excretion, oxygen consumption (O2), and carbon dioxide production (CO2) were monitored serially from the time full feeds were tolerated until discharge. The study period ranged from 13 to 54 d ( ± SD: 26.1 ± 10.2 d) for the control group, from 13 to 47 d (25.9 ± 10.3 d) for group 1, from 14 to 48 d (25.3 ± 10.3 d) for group 2, from 13 to 37 d (25.4 ± 7.2 d) for group 3, and from 14 to 37 d (21.9 ± 7.7 d) for group 4.

Measurement of gaseous metabolism
Once infants had been receiving full enteral feedings for >=72 h, gaseous metabolism was measured every 2 wk until discharge. Each study began immediately after the feeding at 0800, was interrupted for the 1100 feeding, and then continued until the infant was ready for the 1400 feeding. Data from >=150 consecutive minutes were collected during each interfeed period.

O2 and CO2 were measured in a whole-body respirometer by use of flow-through indirect calorimetry. The oxygen concentration of dried gas exiting the respirometer was measured with a Servomex OA 1100 paramagnetic oxygen analyzer (Sybron, Norwood, MA). The concentration of carbon dioxide in the exiting gas was measured with a Beckman LB-2 infrared carbon dioxide analyzer (SensorMedics, Yorba Linda, CA). Air flow through the system was measured with a linear mass flow meter (Matheson, East Rutherford, NJ). Analog outputs from all sensors were digitized at 25 Hz with the use of a Labmaster analog-to-digital converter (Scientific Solutions, Solon, Ohio) and logged to a dedicated AST 286 PC microcomputer (AST, Hong Kong). During each study, the respirometer was warmed indirectly by an overhead radiant heater, servo-controlled to maintain an abdominal skin temperature of 36.5°C. Electrical and gas standard calibrations were performed during each study. The performance of this system was validated (16) and the bench accuracy established at ± 2.2% for both CO2 and O2.

Offline processing with special purpose software was used to correct the raw digital data for drift, transform the data using the appropriate calibration standards, correct measurements to standard temperature and pressure, correct the flow for differences in respiratory exchange, and integrate the signals on a continuous minute-to-minute basis. Measurements of O2 and CO2 were then normalized to body weight and logged as means for each minute. Mean measurements were then calculated for each feeding interval and for each study.

Studies were conducted every 2 wk. Of the 62 infants, 46 participated in 2 studies, 11 participated in 3 studies, and 5 infants participated in 1 study. Measurements for each infant were then averaged to yield a single estimate of O2, CO2, and a respiratory quotient (RQ) for the entire period of full enteral intake.

Urinary nitrogen excretion
Seventy-two–hour urine collections spanning the measurements of gaseous metabolism were obtained every 2 wk. The methods used for collecting and analyzing urinary nitrogen excretion were described previously (3). The mean urine volume was slightly but significantly less in the infants receiving the higher-energy diets (111 ± 7.3, 110 ± 7.6, and 108 ± 10.4 mL•kg-1•d -1 in the control group and groups 1 and 2, and 102 ± 11.3 and 102 ± 6.5 mL•kg-1•d -1 in groups 3 and 4, respectively). The variability in the urine volume within groups ranged from 6.5% to 11%. Sex did not influence the urine volume collected.

Calculation of substrate oxidation
Net substrate oxidation was calculated by using the classic theory and equations of Lusk (17, 18). The O2 and CO2 in the combustion of glucose and fat can be computed accurately from their stoichiometry by assuming the fatty acid composition of the triacylglycerols. Comparable although slightly less accurate values for O2 and CO2 by oxidizing protein were estimated empirically by Magnus-Levy (19). The errors that result from the assumptions about the composition of fatty acids and the quality of protein are thought to be small when the composition of dietary fat and protein does not vary appreciably (20, 21). Infants fed the study formula, unlike free-feeding adults, received similar amounts of substrate within each study group. In general, the equations were nearly exact for the calculation of net lipid, glucose, and protein oxidation rates and for the calculation of net lipid synthesis from glucose.

These equations must be interpreted differently whenever net lipogenesis from carbohydrate is known to occur (20–25). When nonprotein respiratory quotients are >1.0, ie, when net lipogenesis is thought to occur, fat oxidation is a negative value and thus, measured carbohydrate oxidation and true carbohydrate oxidation differ by the glucose equivalent of the fat synthesized. Under these conditions, true carbohydrate oxidation is less than measured carbohydrate oxidation (22, 25). It is also known that lipogenesis can occur in some tissues at a nonprotein RQ of <1.0 (22–25). Thus, the calculated carbohydrate oxidation rate represents the true carbohydrate oxidation rate, the amount of glucose converted to fat during lipogenesis, and an unknown but negligible contribution from gluconeogenesis. The equations used in the calculations (22) are listed below:


(1)

where CO2 and O2 are in L•kg-1•d -1 and urinary N is in g•kg-1•d -1.


(2)


(3)

where urinary N is equal to nitrogen excretion in g•kg-1•d -1 and 6.25 is the conversion factor for converting nitrogen to protein.

Data analysis
Mean values for all variables were computed from all data obtained from each infant. Effects of the quality of energy intake on metabolic gas exchange and substrate oxidation rates were then analyzed by group. Data were analyzed using analysis of variance. When the analysis of variance was significant, post hoc analyses were performed with specific contrasts incorporated into the model (26). The comparisons were limited to outcomes at high compared with low carbohydrate intake at both gross energy intakes.

To determine the relation of carbohydrate and fat intake with carbohydrate and fat oxidation, regression analysis of oxidation rates against intake was performed. The correlation between carbohydrate and fat oxidation and protein oxidation was also estimated by linear regression of the rate of protein oxidation against the rates of carbohydrate and fat oxidation.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Gaseous metabolism was measured in 62 of the 68 infants randomly assigned. Two infants were withdrawn from the protocol because they developed a patent ductus arteriosus requiring fluid restriction (one infant each from groups 1 and 4) and 2 were withdrawn after developing necrotizing enterocolitis (one infant each from groups 2 and 3). One infant's formula (from group 1) was inadvertently changed before the infant completed the protocol, and another infant (from group 4) completed other aspects of the study but was not measured for gaseous metabolism. All of the formulas were well tolerated by the infants. Characteristics of the study groups were not significantly different (Table 2Go).


View this table:
[in this window]
[in a new window]
  		TABLE 2 Characteristics of the study population1
 
Data that summarize the bioenergetics of the study populations are shown in Table 3Go. As anticipated, the mean energy balances (energy stored) of infants in groups 3 and 4, ie, the high energy intake groups (648 kJ•kg-1•d -1), were greater than the energy balances of infants in groups 1 and 2, the lower energy intake groups (544 kJ•kg-1•d -1). Despite the higher rate of energy expenditure, the infants in group 4 who received 65% of their nonprotein energy as carbohydrate retained more energy than did the infants in group 3 who received 65% of their nonprotein energy intake as fat. At the lower energy intake there was no difference in energy expenditure between the groups. However, the infants on the high carbohydrate diet had a higher energy balance than those on the high fat formula. The groups consuming high intakes of fat (groups 1 and 3) lost more energy via excreta than did the infants with high intakes of carbohydrate (groups 2 and 4) and the infants in the control group.


View this table:
[in this window]
[in a new window]
  		TABLE 3 Energy balance data of the study groups1
 
As anticipated, the mean CO2 and the RQ were significantly higher in infants consuming high intakes of carbohydrate at both gross energy intakes (Table 4Go). There was no significant difference in O2 between the groups. Mean urinary nitrogen excretion of infants in groups consuming high amounts of carbohydrate was significantly less than that of infants consuming the high-fat formulas.


View this table:
[in this window]
[in a new window]
  		TABLE 4 Metabolic gas exchange and urinary nitrogen excretion of the study groups1
 
The results of the substrate oxidation calculations are shown in Table 5Go. As expected, carbohydrate oxidation increased with carbohydrate intake. Thus, groups receiving 65% of the nonprotein energy as carbohydrate, ie, groups 2 and 4, oxidized carbohydrate at greater rates than did the groups receiving only 35% of nonprotein energy as carbohydrate (groups 1 and 3). Likewise, fat oxidation varied inversely with carbohydrate intake (r = 0.46, P < 0.001). Consistent with the hypothesis, protein oxidation at both gross energy intakes was less in groups receiving 65% of nonprotein energy as carbohydrate. The protein oxidation of the control group at an energy intake of 544 kJ•kg-1•d -1 was intermediate.


View this table:
[in this window]
[in a new window]
  		TABLE 5 Macronutrient oxidation rates of the study groups1
 
The regression relations of carbohydrate intake with both carbohydrate and fat oxidation are shown in Figure 1Go. As carbohydrate intake increased, carbohydrate oxidation increased (r = 0.71, P < 0.0001) and fat oxidation decreased. In this study, by design, carbohydrate and fat intake were closely related. Carbohydrate intake was a superior predictor of carbohydrate and fat oxidation. Inclusion of fat intake in the regression did not improve the regression relation. As noted above, at nonprotein RQs >1, carbohydrate oxidation included true carbohydrate oxidation and carbohydrate used in fat synthesis.



View larger version (12K):
[in this window]
[in a new window]
  		FIGURE 1. Regression relation of carbohydrate oxidation (n = 62; y = 4.064 + 0.601x; r = 0.71; P < 0.0001) and fat oxidation (n = 46; y = 3.676 -0.145x; r = -0.46; P < 0.001) with carbohydrate intake. At a respiratory quotient >1, the measured carbohydrate oxidation includes true carbohydrate oxidation and carbohydrate used in fat synthesis (negative fat synthesis).

 
The correlations between protein oxidation and both carbohydrate and fat oxidation are shown in Figure 2Go. Protein oxidation was inversely correlated with carbohydrate oxidation but was not correlated with fat oxidation.



View larger version (12K):
[in this window]
[in a new window]
  		FIGURE 2. Correlation of protein oxidation with carbohydrate and fat oxidation. There was a significant negative correlation between protein and carbohydrate oxidation (n = 62; r = -0.42; P < 0.001), whereas the correlation between protein and fat oxidation was not significant (n = 46; P = 0.39). Sixteen patients with a respiratory quotient >=1 were not included when plotting protein against fat oxidation because there was no occurrence of net fat oxidation.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Measurements of metabolic gas exchange and 72-h urinary nitrogen excretion obtained prospectively in a double-blind, randomized study of healthy, growing LBW infants were used to estimate the rates of carbohydrate, fat, and protein oxidation. The results indicate that the rate of protein oxidation is less when 65% of nonprotein energy is supplied as carbohydrate and 35% is supplied as fat than when the proportions are reversed. This was true at gross energy intakes of 544 and 648 kJ•kg-1•d -1. In the infants studied, carbohydrate intake was noted to have a significant, positive relation with carbohydrate oxidation and a negative relation with fat oxidation. Protein oxidation decreased significantly as carbohydrate oxidation increased, but was not related to fat oxidation. Considered together, these data support the hypothesis that, in healthy, enterally fed LBW infants, carbohydrate is more effective than is fat in reducing the oxidation of protein.

In the present study, the higher metabolizable energy intake in the high-carbohydrate diet groups confounds the group comparison for the specific effect of quality of energy on protein oxidation. There was too little variation in metabolizable energy to permit within group analysis between metabolizable energy and protein oxidation. As expected, metabolizable energy intake of the infants correlated significantly with protein oxidation (r = 0.53, P < 0.0001). However, the effect of carbohydrate intake on protein oxidation was apparent with or without metabolizable energy as a covariate in the analysis of variance.

This decrease in protein oxidation (ie, increase in protein stores) with increasing carbohydrate intake at a constant protein intake is consistent with reports in adults of enhanced protein retention when carbohydrate is the primary energy substrate in both enteral (7, 8) and parenteral diets (9). Although greater nitrogen retention with increasing energy intake was reported in enterally fed (3, 27) and parenterally fed (28) LBW infants, knowledge regarding possible differential effects of carbohydrate compared with fat (quality of nonprotein energy) on nitrogen retention in enterally fed LBW infants has been lacking. Published reports of nonprotein energy effects on nitrogen retention are limited to parenterally fed infants, and results have been inconsistent. Investigators reported increased (10), unchanged (13, 29, 30), and decreased (12) nitrogen retention with high carbohydrate intakes. A study investigating the administration of a high-fat formula to premature infants with bronchopulmonary dysplasia reported no difference in nitrogen retention of infants receiving a high-fat compared with a high-carbohydrate diet (31). In contrast, we observed higher rates of nitrogen retention (444.1 ± 22.1 compared with 420.2 ± 23.7 mg•kg-1•d -1 in groups 2 and 1, respectively, and 459.2 ± 20.4 compared with 438.7 ± 26.3 mg•kg-1•d-1 in groups 4 and 3, respectively) and weight gain (23.2 ± 2.9 compared with 20.2 ± 1.8 g•kg-1•d-1 in groups 2 and 1, respectively, and 24.9 ± 2.4 compared with 20.7 ± 2.3 g•kg-1•d -1 in groups 4 and 3, respectively) in infants fed the high-carbohydrate diets at both gross energy intakes (32). However, infants fed the high-energy, high-carbohydrate diet had increased fat deposition as evidenced by the significantly greater increase in skinfold thickness (1.70 ± 0.47 compared with 0.93 ± 0.38 mm/wk in groups 4 and 3, respectively).

The direct correlation of increasing carbohydrate oxidation with increasing carbohydrate intake observed in the present study of enterally fed LBW infants has also been observed in enterally fed adults (15, 33) and parenterally fed infants (12, 13, 34). The diminished fat oxidation with increasing carbohydrate intake and the enhanced fat oxidation with increasing fat intake observed in this study was also noted in some studies (12, 14) but not in others (35, 36).

The conclusions of the present study must be interpreted in light of the study population, experimental design, experimental methodology, and assumptions made in estimating substrate oxidation rates from metabolic gas exchange and urinary nitrogen excretion. The study subjects were healthy, growing LBW infants who were receiving full enteral intakes. The dietary intervention was meticulously controlled, and the experimental protocol spanned a substantial period of time (study duration was a mean of 25 ± 9 d). We carefully validated the indirect calorimeter and defined the error in the use of 6-h studies to predict total daily gas exchange (16, 37, 38). Multiple serial measurements were obtained in most of these infants to further reduce the sampling error associated with these measurements. Among the limitations of the study design was that the diets were designed with a fixed inverse relation between carbohydrate and fat intake; thus, the carbohydrate and fat intakes were not truly independent of each other.

Although thought to be both theoretically and empirically sound, the interpretation of substrate oxidation values as measured by indirect calorimetry is sensitive to both methodologic errors and erroneous assumptions. The assumptions underlying the classic technique for calculating macronutrient oxidation from gas exchange are thought to be most secure when applied to long-term net oxidation rates (21). However, these assumptions may not hold when experimental conditions are not rigidly controlled. For example, when the sampling period is brief, the effects of potentially confounding variables, such as variations in the quality of the diet, physical activity of the infant, and changes in the physical environment (eg, temperature and humidity), need to be adequately controlled. CO2, O2, and RQ all vary significantly depending on the time elapsed after feeding, the amount of food, and, as shown here, the composition of the food (37, 39). Thus, estimates of oxidation rates made from short periods of measurement without control of the aforementioned variables could be inaccurate. As we and others have shown, inclusion of 2 full feeding periods can eliminate most of the variability related to feeding, physical activity, and sleep state (38, 40).

This randomized, prospective investigation of the effects of carbohydrate compared with fat, when fed at 2 isonitrogenous gross energy intakes, on the substrate oxidation of enterally fed LBW infants showed a significant positive relation between carbohydrate intake and carbohydrate oxidation and an inverse relation between fat oxidation and carbohydrate intake. There was less protein oxidation at both gross energy intakes in groups receiving 65% of nonprotein energy as carbohydrate. Within the limitations of the theory and the methodology, these data support the hypothesis that carbohydrate is more effective than is fat in sparing protein oxidation in enterally fed LBW infants. However, because of the increased metabolic load of carbon dioxide and the lack of evidence for the safety of carbohydrate-enriched dietary intakes in LBW infants, particularly regarding the enhanced release of insulin when such diets are given over prolonged periods of time, recommendations for specific enrichment of preterm infant formulas with carbohydrate cannot be made without further evaluation.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. American Academy of Pediatrics Committee on Nutrition. Nutritional needs of preterm infants. In: Kleinman RE, ed. Pediatric nutrition handbook. Elk Grove Village, IL: American Academy of Pediatrics, 1998:55–87.
  2. Schulze K, Stefanski M, Masterson J, Spinnazola R, Dell R, Heird W. Energy expenditure, energy balance and composition of weight gain in low birth weight infants fed diets of different energy and protein content. J Pediatr 1987;110:753–9.[Medline]
  3. Kashyap S, Schulze K, Forsyth M, et al. Growth nutrient retention and metabolic response in low-birth-weight infants fed varying intakes of protein and energy. J Pediatr 1988;113:713–21.[Medline]
  4. Reichman B, Chessex P, Putet G, et al. Diet, fat accretion and growth in premature infants. N Engl J Med 1981;305:1495–500.[Abstract]
  5. Whyte RK, Haslam R, Vlainic C, et al. Energy balance and nitrogen balance in growing low birth weight infants fed human milk or formula. Pediatr Res 1983;17:891–8.[Medline]
  6. Catzeflis C, Schutz Y, Micheli J-L, Welsch C, Arnaud MJ, Jequier E. Whole body protein synthesis and energy expenditure in very low birth weight infants. Pediatr Res 1985;19:679–87.[Medline]
  7. Munro HN. General aspects of the regulation of protein metabolism by diet and by hormones. III. Influence of dietary carbohydrate and fat on protein metabolism. In: Munro HN, Allison JB, eds. Regulation of protein metabolism in mammalian protein metabolism. Vol 1. New York: Academic Press, 1964:412–47.
  8. Richardson DP, Waylar AH, Scrimshaw NS, Young VR. Quantitative effect of an isoenergetic exchange of fat for carbohydrate on dietary protein utilization in healthy young men. Am J Clin Nutr 1979;32: 2217–26.[Free Full Text]
  9. Long JM, Wilmore DW, Mason AD, Pruit BA. Effect of carbohydrate and fat intake on nitrogen excretion during total intravenous feeding. Ann Surg 1977;185:417–22.[Medline]
  10. Chessex P, Gagne G, Pineault M, Vaucher J, Bisaillon S, Brisson G. Metabolic and clinical consequences of changing from high glucose to high fat regimens in parenterally fed newborn infants. J Pediatr 1989;115:992–7.[Medline]
  11. Jeejeebhoy KN, Anderson GH, Nakhooda AF, Greenberg GR, Sanderson I, Marliss EB. Metabolic studies in total parenteral nutrition with lipid in man: comparison with glucose. J Clin Invest 1976;57:125–36.
  12. Salas-Salvado J, Molina J, Figueras J, Masso J, Marti-Henneberg C, Jimenez R. Effect of the quality of infused energy on substrate utilization in the newborn receiving total parenteral nutrition. Pediatr Res 1993;33:112–7.[Medline]
  13. Van Aerde JEE, Sauer PJJ, Pencharz PB, Smith JM, Swyer PR. Effect of replacing glucose with lipid on the energy metabolism of newborn infants. Clin Sci 1989;76:581–8.[Medline]
  14. Verboeket-van de Venne WPHG, Westerterp KR, Hoor F. Substrate utilization in man: effects of dietary fat and carbohydrate. Metabolism 1994;43:152–6.[Medline]
  15. Roy HJ, Lovejoy JC, Keenan MJ, Bray GA, Windhauser MM, Wilson JK. Substrate oxidation and energy expenditure in athletes and nonathletes consuming isoenergetic high- and low-fat diets. Am J Clin Nutr 1998;67:405–11.[Abstract]
  16. Schulze K, Kairam R, Stefanski M, Sciacca B, James LS. Continuous measurement of minute ventilation and gaseous metabolism of newborn infants. J Appl Physiol 1981;50:1098–103.[Abstract/Free Full Text]
  17. Lusk G. Analysis of the oxidation of mixtures of carbohydrate and fat. J Biol Chem 124;54:41–2.
  18. Lusk G. The Atwater-Rosa respiration calorimeter. In: Lusk G, ed. The elements of the science of nutrition. 4th ed. Philadelphia: WB Saunders Co, 1928:61–74.
  19. Magnus-Levy A. The physiology of metabolism. In: von Noorden C, ed. Metabolism and practical medicine. Vol 1. London: Heinemann, 1907:190.
  20. Livesey G, Elia M. Estimation of energy expenditure, net carbohydrate utilization, and net fat oxidation and synthesis by indirect calorimetry: evaluation of errors with special reference to the detailed composition of fuels. Am J Clin Nutr 1988;47:608–28.[Abstract/Free Full Text]
  21. Elia M, Livesey G. Theory and validity of indirect calorimetry during net lipid synthesis. Am J Clin Nutr 1988;47:591–607.[Abstract/Free Full Text]
  22. Frayn KN. Calculation of substrate oxidation rate in vivo from gaseous exchange. J Appl Physiol 1983;55:628–34.[Abstract/Free Full Text]
  23. Ferrannini E. The theoretical bases of indirect calorimetry: a review. Metabolism 1988;37:287–301.[Medline]
  24. Sinclair JC. Discussion: energy needs during infancy. In: Foman SJ, Heird WC, eds. Energy and protein needs during infancy. Orlando, FL: Academic Press Inc, 1986:41–51.
  25. Glamour TS, McCullough AJ, Sauer PJ, Kalhan SC. Quantification of carbohydrate oxidation by respiratory gas exchange and isotopic tracers. Am J Physiol 1995;268:E789–96.[Abstract/Free Full Text]
  26. Netter J, Wasserman W. Applied linear statistical models, regressions, analysis of variance and experimental designs. Homewood, IL: Richard D Irwin Inc, 1974:535–6.
  27. Kashyap S, Schulze KF, Ramakrishnan R, Dell RB, Heird WC. Evaluation of a mathematical model for predicting the relationship between protein and energy intakes of low birth weight infants and the rate and composition of weight gain. Pediatr Res 1994;35:704–12.[Medline]
  28. Zlotkin S, Bryan M, Anderson G. Intravenous nitrogen and energy intakes required to duplicate in utero nitrogen accretion in prematurely born human infants. J Pediatr 1981;99:115–20.[Medline]
  29. Pineault M, Chessex P, Bisaillon S, Brisson G. Total parenteral nutrition in the newborn: impact of the quality of infused energy on nitrogen metabolism. Am J Clin Nutr 1988;47:298–304.[Abstract/Free Full Text]
  30. Pencharz PB, Beesley J, Sauer PJ. Total body protein turnover in parenterally fed neonates: effects of energy source studied by using 15N glycine and 13C leucine. Am J Clin Nutr 1989;50:1395–400.[Abstract/Free Full Text]
  31. Pereira GR, Baumgart S, Bennett MJ, et al. Use of high-fat formula for premature infants with bronchopulmonary dysplasia: metabolic, pulmonary, and nutritional studies. J Pediatr 1994;124:605–11.[Medline]
  32. Kashyap S, Ohira-Kist K, Abildskov K, et al. The effects of quality of energy intake on growth and metabolic response of enterally fed low birth weight infants. Pediatr Res (in press).
  33. Acheson KJ, Schutz Y, Bessard T, Ananthraman K, Flatt JP, Jequier E. Glycogen storage capacity and de novo lipogenesis during massive carbohydrate overfeeding in man. Am J Clin Nutr 1988;48:240–7.[Abstract/Free Full Text]
  34. Sauer PJ, Van Aerde JE, Pencharz PB, Smith JM, Swyer PR. Glucose oxidation rates in newborn infants measured with indirect calorimetry and [U-13C]glucose. Clin Sci (Colch) 1986 70:587–93.
  35. Schutz Y, Flatt JP, Jequier E. Failure of dietary fat intake to promote fat oxidation: a factor favoring the development of obesity. Am J Clin Nutr 1989;50:307–14.[Abstract/Free Full Text]
  36. Thomas CD, Peters JC, Reed GW, Abumrad NN, Sun M, Hill JO. Nutrient balance and energy expenditure during ad libitum feeding of high-fat and high-carbohydrate diets in humans. Am J Clin Nutr 1992;55:934–42.[Abstract/Free Full Text]
  37. Schulze K, Kairam R, Stefanski M, Sciacca B, James LS. Spontaneous variability in gaseous metabolism, minute ventilation and heart rate in low birth weight infants. Pediatr Res 1981;15:1111–6.[Medline]
  38. Schulze K, Stefanski M, Masterson J, et al. An analysis of the variability in estimates of bioenergetic variables in low birth weight infants. Pediatr Res 1986;20:422–7.[Medline]
  39. Sahni R, Towers HM, Kashyap S, Ohira-Kist K, Saluja D, Schulze KF. Effects of variations in carbohydrate intake on post prandial gas exchange and respiratory frequency of low birth weight infants. Pediatr Res 1999;45:318A (abstr).
  40. Bell EF, Rios GR, Wilmoth PK. Estimation of 24-hour energy expenditure from shorter measurement periods in premature infants. Pediatr Res 1986;20:646–9.[Medline]
Received for publication June 30, 2000. Accepted for publication January 3, 2001.




This article has been cited by other articles:


Home page
 Biol Res NursHome page
K. Pridham, A. Bhattacharya, S. Thoyre, D. Steward, J. Bamberger, J. Wells, C. Green, F. Greer, P. Green-Sotos, and M. O'Brien
Exploration of the Contribution of Biobehavioral Variables to the Energy Expenditure of Preterm Infants
Biol Res Nurs, January 1, 2005; 6(3): 216 - 229.
[Abstract] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Purchase Article
Right arrow View Shopping Cart
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Kashyap, S.
Right arrow Articles by Schulze, K. F
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Kashyap, S.
Right arrow Articles by Schulze, K. F
Agricola
Right arrow Articles by Kashyap, S.
Right arrow Articles by Schulze, K. F

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS