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© 2003 The American Society for Nutritional Sciences J. Nutr. 133:2581-2584, August 2003


Human Nutrition and Metabolism
Research Communication

The Atwater Energy Equivalents Overestimate Metabolizable Energy Intake in Older Humans: Results from a 96-Day Strictly Controlled Feeding Study

Laura J. Kruskall*,3, Wayne W. Campbell{dagger} and William J. Evans**

* Department of Nutrition Sciences, The University of Nevada Las Vegas, Las Vegas, NV 89154; {dagger} Department of Foods and Nutrition, Purdue University, West Lafayette, IN 47907; ** Nutrition, Exercise, and Metabolism Laboratory, Donald W. Reynolds Center on Aging, University of Arkansas for Medical Sciences, Little Rock, AR 72205, and the Central Arkansas Veterans Healthcare System, Geriatric Research, Education, and Clinical Center, Little Rock, AR 72205

3To whom correspondence and reprint requests should be addressed. E-mail: lakruskall{at}ccmail.nevada.edu.


    ABSTRACT
 TOP
 ABSTRACT
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
The Atwater energy equivalents of 16.7, 16.7 and 37.7 kJ/g of protein, carbohydrate and fat, respectively, are the standard values used to calculate the macronutrient intakes required to meet a person’s metabolizable energy requirement. The aim of this study was to compare in older people the measured metabolizable energy intake (MEIMEAS) required to achieve and maintain stable body weights with the MEI estimated using the Atwater energy equivalents (MEIAT). During a 96-d (14-wk) strictly controlled dietary period, 11 men and 17 women (55–78 y old) were each provided a MEIAT to maintain body weight within ± 0.5 kg of baseline weight. The MEIMEAS was determined retrospectively from the gross energy contents of food, urine and feces samples collected during week 14. Resting energy expenditure was measured using indirect calorimetry. At wk 14, MEIAT overestimated MEIMEAS by 26%. These results suggest that the Atwater energy equivalent values may overestimate the actual MEI of older people.


KEY WORDS: • energy requirement • bomb calorimetry • elderly people • Atwater energy equivalents

Food composition tables in the U.S report energy content in terms of metabolizable energy intake (MEI). The general energy conversion factors of 16.7 kJ/g of food protein or carbohydrate and 37.7 kJ/g of fat (i.e., the classic Atwater energy equivalents) are adequate for computation of the energy content of typical U.S. diets, but not of specific foods or of high fiber diets. This system is commonly used in the United States and is permitted in the Food Labeling Regulations (1).

In theory, measured MEI should be the same as that estimated using the Atwater energy equivalents. However, previous studies reported a disagreement with these values in young and middle-aged adults (26). Studies examining measured vs. calculated MEI in older adults are limited. The aim of this study was to compare directly the measured MEI with that estimated using the general Atwater energy equivalents during a long-term, strictly controlled feeding study in older men and women.


    SUBJECTS AND METHODS
 TOP
 ABSTRACT
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Men (n = 11) and women (n = 17) 55–78 y old were recruited. Subjects completed a medical history, physical examination, resting electrocardiogram, blood and urine chemistries, and a body weight history. Subjects were weight stable (± 3 kg) for at least 6 mo. Participants were free from smoking, any known acute or chronic diseases, and medications known to affect energy or protein metabolism. None of the women were receiving estrogen replacement therapy. The research protocol and consent forms were approved by the Institutional Review Board, The Pennsylvania State University, University Park, PA, and the Clinical Investigation Committee, The Pennsylvania State University, The Milton S. Hershey Medical center, Hershey, PA; all subjects gave consent.

Subjects participated in a 14-wk precisely controlled diet study at a General Clinical Research Center (GCRC) located at the Noll Physiological Research Center, The Pennsylvania State University. Subjects were randomly assigned, using separate schemes, to one of three groups: 1) sedentary, 2) lower body resistive training, and 3) whole-body resistive training. Subjects were instructed to maintain habitual physical activity levels. Power calculations [PC-SIZE: Consultant software (7)] indicated that n = 9 subjects per group would be required to detect a 15 ± 1.5% difference (80% power, P < 0.05) in energy requirement due to resistive training (8). After analyzing these data, we found that resistive training did not affect measured MEI (9). The data from the men and women in the three groups were pooled for statistical evaluation and presentation in this report.

Residency at the GCRC was required during wk 2, 3, 8 and 14, during which time the subjects were available for all testing and procedures, consumed all of their meals at the GCRC dining facility and spent the night. While not in residency, 26 of the 28 subjects lived at home and were instructed to maintain their usual lifestyles and daily physical activity patterns. For these weeks, the subjects came to the GCRC each weekday morning to be weighed and to consume breakfast. All weekday lunches and dinners, and weekend meals, were taken out. Two subjects resided at the GCRC throughout the study period.

Subjects consumed a lacto-ovo vegetarian diet that provided the Recommended Dietary Allowance (RDA) of 0.8 g protein/(kg · d), a nonprotein energy content of 60% carbohydrate and 40% fat, and sufficient dietary energy to maintain body weight. Meats were excluded from the menu because they are high protein sources that are difficult to incorporate into a lower protein meal plan. Milk- and egg-based protein represented 28.5 ± 1.2% and 10.2 ± 0.8% of total protein, respectively. We previously published a more detailed description of the 3-d rotating menu scheme, including examples of specific menus (10) and descriptions of the measures taken to enhance subject compliance to the diet (9,11). A protein intake of 0.8 g protein/(kg · d) was chosen to evaluate the adequacy of the protein RDA in older persons (11,12).

For this study, energy intake is expressed in three ways: measured metabolizable energy intake (MEIMEAS), estimated metabolizable energy intake using the Atwater energy equivalents (MEIAT) and gross energy (GE) intake. The general Atwater values were used to estimate the metabolizable energy contents of the menus; for descriptive purposes, the term MEIAT is used to represent these estimates. The term MEIMEAS is used to describe the direct measurement of metabolizable energy derived from the GE contents of the food, urine and stool samples. GE intake is the amount of combustible energy contained in the diets provided to the subjects. GE intake is greater than MEIAT and MEIMEAS. Theoretically, MEIAT and MEIMEAS are the same. In clinical practice, MEIAT is used as an estimate for MEIMEAS when an estimate of energy requirement is necessary for dietary prescription.

Initially, each subject’s MEIAT was set to equal resting energy expenditure (REE) times an activity factor of 1.7. The Harris-Benedict equations (13) were first used to estimate REE. On the basis of data from Roberts et al. (14), an activity factor of 1.70 was used. Sufficient MEIAT to maintain body weight throughout the study was provided for each subject to be in a state of energy balance. To achieve this goal, adjustments to MEIAT were made, if needed, during the free-living study weeks. An adjustment to MEIAT was made when body weight remained >0.5 kg different from the baseline weight for three consecutive days, and was made by either adding or subtracting very low protein or protein-free foods and beverages from the daily menus, while maintaining the nonprotein energy ratio at 60% carbohydrate to 40% fat. To calculate each subject’s daily MEIAT, the Atwater energy equivalents of 16.7, 16.7 and 37.7 kJ/g metabolizable energy for protein, carbohydrate and fat, respectively, were multiplied by the gram weights of the macronutrients in each menu.

Nonprotein REE was measured using indirect calorimetry at study wk 1, 2 and 14, as previously described (9). REE was calculated by multiplying the subject’s rate of oxygen uptake (L/min) by the energy equivalent associated with the nonprotein respiratory exchange ratio of the expired gas (15).

Barefoot standing height was measured to the nearest 0.1 cm with a wall-mounted stadiometer during the first week. Nude body weight was measured to the nearest 0.1 kg each weekday throughout the duration of the study after an overnight fast and after voiding (model 2181; Toledo Scale, Toledo, OH; calibrated by standard dead weight testing). The CV of the scale was 0.1%.

Body density was measured by hydrostatic weighing using a four-point transducer system (16) with simultaneous measurement of residual lung volume (17) at wk 2, 8 and 14. Total body water was determined using deuterium oxide dilution as previously described by Campbell et al. (8). The percentages of body fat, fat-free mass (FFM) and protein-mineral mass were calculated using the three-compartment model equation of Siri (18). To estimate habitual physical activity throughout the study period, The Yale Physical Activity Survey (19) was administered during wk 2, 8 and 14.

During weeks 2, 8 and 14, food, urine and fecal samples were collected. A duplicate composite of each of the three daily meals was prepared and homogenized. Four consecutive 24-h urine collections were obtained and pooled before analysis. Fecal samples (4-d) were collected between fecal dye markers and the composite feces were pooled and homogenized. Food homogenate samples were freeze-dried and pressed into pellets for combustion. GE content of all food, urine, and feces samples was determined using a bomb calorimeter (model 1261, Parr Instrument Company, Moline, IL). The calorimeter was calibrated daily as recommended by the manufacturer. The MEIMEAS for each subject at wk 14 was calculated by subtracting the GE of urine (MJ/d) and GE of feces (MJ/d) from the dietary GE intake (MJ/d), along with corrections for changes in body composition measured between week 8 and 14. The formula used to calculate MEIMEAS was as follows (20,21):



Statistical methods.

All values are expressed as means ± SEM. A one-factor (sex) ANOVA was used to determine differences between men and women in mean values for all independent variables at wk 2. A two-factor (sex) repeated-measures (time) ANOVA was used to test the main effects of sex and time, and to test for interactions of sex over time. An {alpha}-level of P < 0.05 (two-sided) was used to determine significance. Microsoft Excel 5.0 (Microsoft, Redmond, WA) software was used for all data management. Statistical evaluations were done using JMP software (version 3.2.2, SAS Institute, Cary, NC).


    RESULTS
 TOP
 ABSTRACT
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
The men and women did not differ in mean age (Table 1). The men were taller (P < 0.001) and heavier (P = 0.012); they had greater percentages of FFM (P < 0.001), total body water (P < 0.001) and protein-mineral mass (P < 0.001), and a lower percentage of body fat (P < 0.001) than the women. Over time, body weight decreased in the men and remained stable in the women (sex x time, P = 0.040). For the men, body weight decreased from wk 2 to 8, and did not change from wk 8 to 14. The changes over time in the percentage of body fat, FFM, total body water and protein-mineral mass did not differ in the men and women.


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TABLE 1 Characteristics of subjects throughout the study1

 
There was no change in estimated energy expenditure due to physical activity over the three balance periods. The values for the men at weeks 2, 8 and 14 were 2.67 ± 0.45, 2.51 ± 0.34, and 2.62 ± 0.36 MJ/d, respectively, and for the women, 3.13 ± 0.43, 2.42 ± 0.32, and 2.36 ± 0.26 MJ/d, respectively.

Total energy intake was adjusted as necessary during the free-living weeks to maintain body weight within 0.5 kg of each subject’s baseline weight. Zero adjustments were made for three subjects, one adjustment for seven subjects, two adjustments for nine subjects, three adjustments for seven subjects and four adjustments for two subjects. The mean time to the first MEIAT adjustment was 28 ± 20 d (mean ± SD; range 5–80 d) and the mean time to the final MEIAT adjustment was 52 ± 21 d (range 19–95 d).

At wk 2, the men had a higher dietary GE intake (P = 0.001), GE excretion in urine (P = 0.022) and GE excretion in feces (P = 0.002) than the women (Table 3). Dietary GE intake had to be increased over time to stabilize and maintain body weight. Greater changes were required for the men than the women (sex x time, P = 0.009). The mean increases in GE intake were 10.1 ± 2.3% in men and women combined, 17.9 ± 2.5% in men and 5.1 ± 2.9% in women. GE excretions in urine and feces did not change over time. At wk 14, dietary GE intake was higher in the men than in the women.


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TABLE 3 Gross energy (GE) of food, urine and feces in men and women during a long-term, strictly controlled feeding study1

 
For all subjects at wk 14, the mean MEIAT was 25.7 ± 3.8% higher than the mean MEIMEAS (Table 4). That is, MEIAT overestimated MEIMEAS by ~26%.


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TABLE 4 Energy intakes, REE and energy requirements of men and women at wk 14 for long-term body weight maintenance in a strictly controlled feeding study1

 

    DISCUSSION
 TOP
 ABSTRACT
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
The MEI calculated using the Atwater energy equivalents did not accurately estimate the measured MEI in these older adults. This is not consistent with the assumption that MEIAT and MEIMEAS should theoretically be the same (22). These subjects were weight stable for the last several weeks of the study. There was no change in body weight on a group basis, and there was strict control of body weight on an individual basis. The criterion of keeping subjects within 0.5 kg led to their being within 0.65% of their baseline body weight. Inherent daily variability in body weight has been reported to be 0.4–0.8% (23). Thus, during this 14-wk precisely controlled dietary experiment, we successfully kept the body weights of the subjects stable within the inherent daily variability.

The estimated MEIAT at wk 14 overestimated MEIMEAS by 26%. The need to increase energy intake from wk 2 to 8 was a result of the initial underestimation of energy intake due to the disconnect between the Atwater energy equivalents and the MEIMEAS. These findings are supported by other studies. Stock and Wheeler (6) evaluated 84 meals and found that the use of food tables using Atwater energy equivalents led to a consistent overestimation of energy content by ~20%. Miles et al. (5) examined the MEI of mixed diets in nine young and middle-aged men and women during both weight maintenance and underfeeding phases. They reported that the Atwater energy equivalents used by the USDA (24) were on average 16% higher than the measured metabolizable energy of the diets. Marshall and Judd (3) found that the energy content of four modified fat diets calculated from the U.S. food tables was almost identical to the heats of combustion determined by bomb calorimetry. Miles et al. (4) examined the energy content of self-selected diets and reported that the heats of combustion were the same as that estimated from food composition tables. The food composition tables are supposed to be metabolizable energy values and should be lower than the GE values determined by bomb calorimetry. More recently, a study examined the MEI of moderate and high nonstarch polysaccharide diets fed at maintenance and weight-reduction levels (2). The authors reported that the Atwater general energy equivalents always overestimated (although only one value was significantly different) the determined MEI consumed at weight maintenance.

It appears that the metabolizable energy content of the diet decreases as fiber intake increases (2530). The Dietary Reference Intake for total fiber is 21 g/d for women over the age of 50 y and 30 g/d for men of the same age (31). Diets providing <35 g/d of dietary fiber reported an overestimation of Atwater energy equivalents ranging from 1.1 to 4.0% (25,27,28,32). Diets providing >35 g/d reported an overestimation ranging from 4.2 to 9.4% (2529). Dietary fiber intake is not a reasonable explanation for the overestimation of Atwater energy equivalents observed in this study because the mean daily fiber intake was 28 and 24 g/d for men and women, respectively.

Another factor that may affect metabolizable energy is the ability to digest macronutrients. We do not have data to support or refute any decline in digestive function in our study population. Harper (33) reported that there is no unequivocal evidence that aging is associated with a decreased capacity for carbohydrate, protein or fat digestion. However, based on the stool energy content in our subjects, this could have been an issue. Studies in young and middle-aged adults fed mixed diets report mean stool energy contents ranging from 0.54 to 1.04 MJ/d (5,34). A recent study reported the mean stool energy content with hypoenergetic feeding of men and women aged 18–78 to be 0.49 MJ/d (35). Data on stool energy content in elderly individuals are limited. One study reported stool energy content of 26 elderly adults to be 0.57 MJ/d (36). The higher stool energy contents in our subjects may be suggestive of impaired digestive function and further research is warranted in this population.

Clinically, the apparent disconnect between the estimated MEIAT and MEIMEAS may have important applications to the energy balance and macronutrient intakes of many elderly people, especially those who receive meals planned by dietitians. However, the present data suggest that if the Atwater energy equivalents are used to estimate energy needs in older adults, these persons might be provided substantially less metabolizable energy and macronutrient intakes than required. We initially fed our subjects a MEIAT/REE ratio of 1.7 and still had to increase energy intake to prevent weight loss. To help ensure adequate energy intakes, dietitians who develop meals for older persons on the basis of the Atwater energy equivalents might use the MEIAT/REE ratios of 1.93 and 1.82 for older men and women, respectively, to estimate a person’s energy requirement. When possible, this approach should be coupled with frequent monitoring of body weight for stability. More research is required to validate the continued use of the Atwater energy equivalents for macronutrients as a means to estimate the actual metabolizable energy needs of older and elderly people.

In conclusion, the use of the classic Atwater energy equivalents to predict MEI resulted in an overestimation of energy requirement by ~26% compared with the direct measurement of MEI. Caution should be taken when relying on the Atwater energy equivalents to plan menus for older people who are at high nutritional risk. Additional measures such as regular body weights must be taken to ensure energy balance.


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TABLE 2 Macronutrient intakes of men and women during wk 14 of a controlled feeding study1

 

    ACKNOWLEDGMENTS
 
We thank the dietary and nursing staff at the GCRC, and especially the efforts of Deanna Cyr-Campbell, who developed and coordinated the preparation and distribution of the nutrient-defined menus.


    FOOTNOTES
 
1 Presented in part at Experimental Biology 2000, April 2000, San Diego, CA [Campbell W.W., Kruskall L.J. & Evans W.J. (2000) Metabolizable energy intake (MEI) for long-term body weight maintenance in older men and women. FASEB J. 14: A757 (abs.)]. Back

2 Supported by National Institutes of Health 1 R29 AG13409, NIH R01-AG11811, and General Clinical Research Center grant MO1 RR10732. Back

4 Abbreviations used: FFM, fat-free mass; GCRC, general clinical research center; GE, gross energy; MEI, metabolizable energy intake; MEIAT, estimated metabolizable intake using Atwater energy equivalents; MEIMEAS, measured metabolizable energy intake; RDA, recommended dietary allowance; REE, resting energy expenditure. Back

Manuscript received 24 November 2002. Revision accepted 9 June 2003.


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