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* Department of Nutrition Sciences, The University of Nevada Las Vegas, Las Vegas, NV 89154;
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 |
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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 |
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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 subjects 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 subjects 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 subjects 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):
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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
-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 |
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Total energy intake was adjusted as necessary during the free-living weeks to maintain body weight within 0.5 kg of each subjects 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 580 d) and the mean time to the final MEIAT adjustment was 52 ± 21 d (range 1995 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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26%.
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| DISCUSSION |
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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 1878 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 persons 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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| ACKNOWLEDGMENTS |
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| FOOTNOTES |
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2 Supported by National Institutes of Health 1 R29 AG13409, NIH R01-AG11811, and General Clinical Research Center grant MO1 RR10732. ![]()
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. ![]()
Manuscript received 24 November 2002. Revision accepted 9 June 2003.
| LITERATURE CITED |
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1. FDA http://www.cfsan.fda.gov/~Ird/fdahist.html (accessed 9/2/02).
2. Brown, J., Livesey, G., Roe, M., Faulks, R., Poppitt, S., Wilkinson, J. & Elia, M. (1998) Metabolizable energy of high non-starch polysaccharide-maintenance and weight-reducing diets in men: experimental appraisal of assessment systems. J. Nutr. 128:986-995.
3. Marshall, M. W. & Judd, J. T. (1982) Calculated vs. analyzed composition of four modified fat diets. J. Am. Diet. Assoc. 80:537-549.[Medline]
4. Miles, C. W., Brooks, B., Barnes, R., Marcus, W., Prather, E. S. & Bodwell, C. E. (1984) Calorie and protein intake and balance of men and women consuming self-selected diets. Am. J. Clin. Nutr. 40:1361-1367.[Abstract]
5. Miles, C. W., Webb, P. & Bodwell, C. E. (1986) Metabolizable energy of human mixed diets. Human Nutr. Appl. Nutr. 40A:333-346.
6. Stock, A. L. & Wheeler, E. F. (1972) Evaluation of meals cooked by large-scale methods: a comparison of chemical analysis and calculation from food tables. Br. J. Nutr. 27:439-448.[Medline]
7. Dallal, G. E. (1990) PC-SIZE: Consultanta program for sample size determination. The American Statistician 44:243.
8. Campbell, W., Crim, M., Young, V. & Evans, W. (1994) Increased energy requirements and changes in body composition with resistance training in older adults. Am. J. Clin. Nutr. 60:167-175.
9. Campbell, W. W., Kruskall, L. J. & Evans, W. J. (2002) Lower body versus whole body resistive exercise training and energy requirements of older men and women. Metabolism. 51:989-997.[Medline]
10. Campbell, W. W., Cyr-Campbell, D., Weaver, J. A. & Evans, W. J. (1997) Energy requirement for long-term body weight maintenance in older women. Metabolism 46:884-889.[Medline]
11. Campbell, W. W., Trappe, T. A., Jozsi, A. C., Kruskall, L. J., Wolfe, R. R. & Evans, W. J. (2002) Dietary protein adequacy and lower body versus whole body resistive training in older humans. J. Physiol. 542:631-642.
12. Campbell, W., Trappe, T., Wolfe, R. & Evans, W. (2001) The Recommended Dietary Allowance for protein may not be adequate for older people to maintain skeletal muscle. J. Gerontol. Biol. Sci. Med. Sci. 56:M373-M380.
13. Harris, J. A. & Benedict, F. G. (1919) A Biometric Study of Basal Metabolism in Man, Publication no 1919:279 Carnegie Institute of Washington Washington.
14. Roberts, S. B., Young, V. R., Fuss, P., Heyman, M. B., Fiatarone, M., Dallal, G. E., Cortiella, J. & Evans, W. J. (1992) What are the dietary energy needs of elderly adults?. Int. J. Obes. Relat. Metab. Disord. 16:969-976.[Medline]
15. McArdle, W. D., Katch, F. I. & Katch, V. L. (1991) Measurement of human energy expenditure. Exercise Physiology: Energy, Nutrition, and Human Performance 3rd ed. 1991 Lea & Febiger Philadelphia, PA.
16. Akers, R. & Buskirk, E. R. (1969) An underwater weighing system utilizing "force cube" transducers. J. Appl. Physiol. 26:649-652.
17. Wilmore, J. (1969) The use of actual, predicted and constant residual volumes in the assessment of body composition by underwater weighing. Med. Sci. Sports. Exerc. 1:87-90.
18. Siri, W. (1961) Body composition from fluid spaces and density: analysis of methods. Techniques for Measuring Body Composition 1961 National Academy of Sciences Washington, DC.
19. DiPietro, L., Caspersen, C. J., Ostfeld, A. M. & Nadel, E. R. (1993) A survey for assessing physical activity among older adults. Med. Sci. Sports. Exerc. 25:628-642.[Medline]
20. Tremblay, A., Despres, J.-P., Theriault, G., Fourier, G. & Bouchard, C. (1992) Overfeeding and energy expenditure in humans. Am. J. Clin. Nutr. 56:857-862.
21. Votruba, S., Blanc, S. & Schoeller, D. A. (2002) Pattern and cost of weight gain in previously obese women. Am. J. Physiol. 282:E923-E930.
22. FAO/WHO/UNU (1985) Energy and Protein Requirements 1985 WHO Geneva, Switzerland.
23. Khosla, T. & Billewicz, W. Z. (1964) Measurement of change in body weight. Br. J. Nutr. 18:227-239.[Medline]
24. U.S. Department of Agriculture (19761989) Human Nutrition Information Service. Composition of Foods. Agriculture Handbook No. 8 19761989 U.S. Government Printing Office Washington, DC .
25. Goranzon, H., Forsum, E. & Thilen, M. (1983) Calculation and determination of metabolizable energy in mixed diets to humans. Am. J. Clin. Nutr. 38:954-963.
26. Goranzon, H. & Forsum, E. (1987) Metabolizable energy in humans in two diets containing different sources of dietary fiber.Calculations and Analysis. J. Nutr. 117:267-273.
27. Miles, C. W., Kelsay, J. L. & Wong, N. P. (1988) Effect of dietary fiber on the metabolizable energy of human diets. J. Nutr. 118:1075-1081.
28. Wisker, E. & Feldheim, W. (1990) Metabolizable energy of diets low or high in dietary fiber from fruits and vegetables when consumed by humans. J. Nutr. 120:1331-1337.
29. Millard-Stafford, M. L., Sparling, L. B. & Dicarlo, L. J. (1992) Carbohydrate-electrolyte replacement improves distance running performance in the heat. Med. Sci. Sports. Exerc. 24:934-940.[Medline]
30. Baer, D. J., Rumpler, W. V., Miles, C. W. & Fahey, G. C. (1997) Dietary fiber decreases the metabolizable energy content and nutrient digestibility of mixed diets fed to humans. J. Nutr. 127:579-586.
31. National Academy of Sciences, Food and Nutrition Board, Institute of Medicine (2002) Dietary Reference Intakes for Energy, Carbohydrates, Fiber, Fat, Protein, and Amino Acids (Macronutrients) 2002 National Academy Press Washington, DC.
32. Miles, C. W. (1992) The metabolizable energy of diets differing in dietary fat and fiber measured in humans. J. Nutr. 122:306-311.
33. Harper, E. J. (1998) Changing perspectives in aging and energy requirements: aging and digestive function in humans, dogs, and cats. J. Nutr. 128:2632S-2635S.
34. Norgan, N. G. & Durnin, J. V. G. A. (1980) The effect of 6 weeks of overfeeding on the body weight, body composition, and energy metabolism of young men. Am. J. Clin. Nutr. 33:978-988.
35. Saltzman, E., Moriguti, J. C., Das, S. K., Corrales, A., Fuss, P., Greenberg, A. S. & Roberts, S. B. (2001) Effects of a cereal rich in soluble fiber on body composition and dietary compliance during consumption of a hypocaloric diet. J. Am. Coll. Nutr. 20:50-57.
36. Pannemans, D. E. & Westerterp, K. R. (1995) Energy expenditure, physical activity and basal metabolic rate of elderly subjects. Br. J. Nutr. 73:571-581.[Medline]
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