Original Communication The energy expenditure of ... - Nature

European Journal of Clinical Nutrition (2001) 55, 1059–1067 ß 2001 Nature Publishing Group All rights reserved 0954–3007/01 $15.00 www.nature.com/ejcn

Original Communication The energy expenditure of postmenopausal women classified as restrained or unrestrained eaters GP Bathalon1{, NP Hays1{, MA McCrory1, AG Vinken1, KL Tucker1, AS Greenberg1, C Castaneda1 and SB Roberts1* 1

Jean Mayer USDA Human Nutrition Research Center on Aging at Tufts University, Boston, Massachusetts, USA

Objective: Restrained eating is a common dietary practice among individuals who are attempting to prevent weight gain, but little is known about differences in energy physiology and regulation between restrained and unrestrained eaters. We investigated this issue in non-obese free-living postmenopausal women classified as longterm restrained (n ¼ 26) or unrestrained (n ¼ 34) eaters group matched for body mass index (BMI). Measurements: Measurements were made of total energy expenditure (TEE), resting energy expenditure (REE), body composition, reported leisure time activity, maximal aerobic capacity (VO2max) and weight change during the study period. In addition, physical activity level (PAL) and nonexercise activity thermogenesis (NEAT) were calculated from measured variables. Results: There were no significant differences between the groups in body composition, weight change, aerobic capacity or total leisure time activity. Relationships between fat-free mass (FFM) and both REE and TEE, and the relationship between work load and energy expenditure in the test of maximal oxygen consumption, were also not different between groups. However, restrained eaters had a significantly lower PAL (equal to TEE=REE, 1.72 0.04 vs 1.84 0.04, P < 0.05). In addition, in multiple regression models predicting NEAT, NEAT was significantly lower in restrained eaters than unrestrained eaters and there was a positive relationship between NEAT and weight change in unrestrained eaters but no relationship in restrained eaters (P < 0.05). Conclusions: In contrast to a previous report, we found no significant difference in TEE between restrained and unrestrained eaters. PAL was slightly lower in restrained eaters, apparently due to reduced NEAT, and restrained eaters also lacked the positive association between NEAT and body weight change seen in unrestrained eaters. This latter finding, if confirmed in future studies, could help explain an increased susceptibility of restrained eaters to weight gain. Sponsorship: NIH grants AG12829, DK46124 and T32AG00209, and US Cooperative Agreement number 581950-9-001. Descriptors: energy metabolism; total energy expenditure; resting energy expenditure; doubly labeled water; respiratory quotient; body composition European Journal of Clinical Nutrition (2001) 55, 1059–1067

Introduction *Correspondence: SB Roberts, Energy Metabolism Laboratory, Jean Mayer USDA Human Nutrition Research Center on Aging at Tufts University, 711 Washington St, Boston, MA 02111, USA. E-mail: [email protected] { Current address for GPB: Military Nutrition Division, US Army Research Institute of Environmental Medicine, Natick, MA 01760, USA. The first two authors made similar contributions. Guarantors: GP Bathalon and SB Roberts. Contributors: GPB and SBR were responsible for design of the study and wrote the manuscript; NPH, GPB and ASG were particularly responsible for conduct of study and data analysis, with additional help from AGV and CC. MAM helped with statistical analysis and interpretation of the data and KLT also helped with interpretation of the data. All authors have approved the manuscript. Received 14 August 2000; revised 8 May 2001; accepted 10 May 2001

Twenty-five years ago, the psychological construct ‘dietary restraint’ was introduced by Herman and Mack (1975) to describe the high degree of self-control in eating exhibited by some women attempting to consciously restrict energy intake to prevent weight gain or promote weight loss. Results from several studies (Laessle et al, 1989; Westenhoefer et al, 1990; Klesges et al, 1992; Schweiger et al, 1992; Barr et al, 1994; de Castro, 1995; Lawson et al, 1995; Lindroos et al, 1997) have indicated that restrained eaters report consuming significantly less dietary energy than unrestrained eaters (who are defined as individuals who eat as much food as they want). One interpretation of this finding is that restrained eaters have reduced energy requirements relative to unrestrained eaters of similar body

Dietary restraint and energy metabolism GP Bathalon et al

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mass, a factor that could help explain an increased susceptibility to weight gain. Recently, however, some (Bingham et al, 1995; Bathalon et al, 2000) though not all (Tuschl et al, 1990) studies of the accuracy of dietary reporting in different groups have suggested that restrained eaters under-report energy intake to a greater extent than unrestrained eaters. Thus, the question of whether energy requirements are persistently decreased in individuals practicing dietary restraint remains unclear. There is also controversy regarding the association between dietary restraint and energy expenditure. One study of total energy expenditure (TEE) in young women reported significantly lower TEE, by 2.59 MJ=day (620 kcal=day), in restrained eaters compared to unrestrained eaters (Tuschl et al, 1990). However, the period of time over which dietary restraint had been practiced was not documented in that study, and the lower energy expenditure was only apparent after statistical adjustment of the data for both height and body composition (assessed by bioelectrical impedance). In apparent contrast to the study of Tuschl et al (1990), Poehlman et al (1991) and Lawson et al (1995) reported no significant association between the degree of dietary restraint and resting energy expenditure (REE, the major component of energy requirements), but TEE was not measured in those investigations. We therefore conducted a study to investigate TEE and components of energy expenditure in healthy postmenopausal women classified as chronically restrained or unrestrained eaters, specifically to test the hypothesis that long-term dietary restraint is associated with significantly reduced TEE. We further speculated that the reduced TEE would be due to reduced nonexercise activity thermogenesis (NEAT), a recently-coined term encompassing all energy expenditure other than for REE and intentional exercise (Levine et al, 1999). We anticipated that these results would help resolve the specific controversy over energy conservation in restrained eaters, and would also provide information relevant to the general question of whether adaptive variations in NEAT play a quantitatively important role in energy regulation in well-nourished individuals. Subjects and methods Subjects The subjects were 60 healthy postmenopausal women classified as restrained or unrestrained eaters who reported stable body weight and dietary restraint over the past 10 y (Table 1). Eating Inventory (Stunkard & Messick, 1985) scores of 5 or 13 for restraint were used to classify the eating styles of the women as highly unrestrained or highly restrained, respectively. These cut-off points are the 25th and 75th percentiles of restraint scores in a large study of women of a similar age range living in the Boston, MA, area (Hays et al, 2001). The subjects were free from known disorders that may affect energy intake or energy metabolism, including diabetes, cancer, coronary heart disease, European Journal of Clinical Nutrition

Table 1 Subject characteristics Unrestrained

Restrained

n 26 34 59.4 0.6 Age (y) 60.3 0.6a Weight (kg) 63.8 1.7 64.0 1.5 Height (cm) 164.4 1.2 160.8 1.1* 2 23.6 0.6 24.8 0.5 Body mass index (kg=m ) Weight change during study (g=day) 732.5 12.6** 727.9 9.8*** Waist circumference (cm) 80.9 1.7 81.4 1.3 Fat (percentage by weight) 35.3 1.2 36.6 1.6 Fat-free mass (kg) 40.9 0.8 40.2 1.0 Beta-hydroxybutyric acid (mg=dl) 1.9 0.1 1.8 0.1 a x s.e.m. *Significantly different from unrestrained eaters, P < 0.05. **,***Significantly different from 0: **P < 0.05; ***P < 0.01.

eating disorders, depression, alcoholism, inflammatory disorders and endocrine, hepatic, renal or thyroid dysfunction. Additional exclusion criteria included smoking, reported endurance training (participation in sports or athletic training) of > 6 h per week, being on a formal weight control diet during the past year, history of hypertension, vegetarian diet, psychiatric disorders, and current or recent use of any medications known to affect energy intake or energy expenditure. In addition, groups were group matched for body mass index (BMI). The study was conducted in the Metabolic Research Unit at the Jean Mayer USDA Human Nutrition Research Center on Aging at Tufts University with ethical approval from the New England Medical Center=Tufts University Human Investigations Review Committee. Written informed consent was given by each subject prior to study participation. Study protocol The study was conducted over an 18 day period. After an overnight fast and familiarization of the subjects with all testing equipment, REE was measured on the morning of study day 1 and a fasting blood sample was taken. Then body weight, body composition, maximal aerobic capacity (VO2max), and anthropometric variables were measured, and in 57 subjects the Minnesota Leisure Time Physical Activity questionnaire was also completed (Taylor et al, 1978; Folsom et al, 1986). Subjects started a doubly labeled water measurement of TEE on the same day. They were then discharged from the research center and were instructed to lead their usual life at home without gaining or losing weight. They returned to the center on the morning of study day 9 to deliver urine samples for the doubly labeled water study, provide a second fasting blood sample, and have their weight measured. They also returned on the morning of study day 11 to repeat the measurements of REE, weight and anthropometric variables, to provide a urine sample for the doubly labeled water study, and to receive instruction on keeping a 7 day weighed food record (Bathalon et al, 2000). Subjects were then discharged and during study days 11 – 17 recorded all food and beverages consumed and continued collecting urine samples until day 15. On study day 18 they


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returned urine samples and the 7 day food record to the center. Measurements of TEE Total energy expenditure was measured over a 14 day period. For this measurement, a mixed dose of 2H218O containing 0.12 g=kg body weight of H218O and 0.07 g=kg body weight of 2H2O was given orally between 07:45 and 08:30 am on study day 1 after an overnight fast and collection of two baseline urine specimens. The dose was followed by two 25 ml rinses of tap water. Subjects then fasted for 4 h and urine specimens were collected at 3, 4 and 5 h after isotope administration. On subsequent study days, the subjects led their usual life at home, and urine specimens from the second or later void of the day were collected by the subject and stored in airtight storage tubes in their home freezer. Abundances of 2H and 18O, in dilutions of the isotope doses and in seven urine specimens (baseline, 5 h and study days 2, 3, 10, 14 and 15) were analyzed using isotope-ratio mass spectrometry as described elsewhere (Roberts et al, 1990). On average, triplicate analyses of each sample were performed for 2H and duplicate analyses for 18O abundances. Values for TEE were calculated from the doubly labeled water data by using a modification of the equations of Roberts et al (1990) incorporating the recommended assumption of a fixed ratio of dilution spaces (2H2O:H218O) of 1.0342 in all subjects with a standard fractionation correction for older individuals (Roberts et al, 1992). The calculations were performed using DLW software (Dallal & Roberts, 1991). Values for TEE were calculated from rates of carbon dioxide production by using Weir’s equation (Weir, 1949), with estimates for respiratory quotient (RQ) assumed to equal the food quotient determined from reported macronutrient intakes in the 7 day weighed food intake record (Black et al, 1986). Please note that inaccurate food records have only a very small impact on the accuracy of TEE (Surrao et al, 1998). Resting energy expenditure VO2 and VCO2 were measured on study days 1 and 11 under thermoneutral temperature conditions, after a 12 h overnight fast, and at least 36 h after strenuous exercise. After subjects rested supine for 30 min, measurements of expired gases were taken for a 30 min period following a 10 min equilibration phase. The subjects were instructed to relax and avoid hyperventilation, fidgeting and sleeping during measurements, which were made using a ventilatedhood indirect calorimeter (Deltatrac; Sensor-Medics Corporation, Yorba Linda, CA) calibrated using gases of known concentration. The calorimeter was also monitored in alcohol burn tests at regular intervals during the study and values for VO2 and VCO2 recovery averaged 100 1% of expected. Values for REE were calculated from VO2 and VCO2 using Weir’s equation (Weir, 1949). Duplicate measures of REE were obtained in 56 of the 60 subjects. When available, the mean of two REE measurements was used in the data analysis.

Maximal aerobic capacity Maximal aerobic capacity (VO2max) was determined in the early afternoon of study day 1, approximately 2 h after a light lunch, in 56 of the subjects. Subjects pedaled on an electrically braked cycle ergometer (Corival model 400 Lode Ergometer, Quinton Instrument Co., Seattle, WA) at an average 60 rpm, with increasingly higher workloads until exhaustion, using a standard Bruce protocol (Vogel et al, 1986). Subjects cycled for 2 min at an initial power rating of 50 W, and then output was increased by 25 W every minute until volitional fatigue while a pedal frequency of 40 – 60 rpm was maintained. During the test, volunteers breathed through a low-resistance mouthpiece while wearing a nose-clip. Expired gases were collected and analyzed for O2 and CO2 concentrations (for n ¼ 49, Applied Electrochemistry Analyzer S-3A for O2 and Beckman LB-2 Analyzer for CO2; for n ¼ 7 Sensormedics Vmax 229LV, Yorba Linda, CA) and for volume (for n ¼ 49, Parkinson-Cowan CD-4 dry gasometer; for n ¼ 7, Sensormedics Vmax 229LV, Yorba Linda, CA). The maximum oxygen uptake was defined as the mean of two successive values that did not differ by more that 0.2 l=min when the RQ was > 1.1. Body composition and anthropometry Body density was determined by hydrostatic weighing with repeated measurements taken until at least three values for body fat percentage agreed within 1% (Bathalon et al 1995). Residual lung volume was then measured on land using an oxygen dilution technique (Wilmore, 1969) in which direct nitrogen analysis of expired air was determined (Med Science Model 505 Nitralyzer, St Louis, MO). For this measurement, each subject sat in a chair and a maximum of four trials were made. Values agreeing within 150 ml were averaged and used in subsequent calculations (Bathalon et al, 1995; Wilmore, 1969). Body fat percentage was calculated using the Siri equation (Siri, 1961). Two restrained volunteers were unable to complete the hydrostatic weighing procedure. In these cases, results from dualenergy X-ray absorptiometry (model Lunar DPX, software version 3.6Z, Lunar Corporation, Madison, WI) were used because there were no significant differences between measures of body composition (fat-free mass (FFM) and body fat percentage) by the two methods in this population (data not shown). Body weight was measured to 0.1 kg using an electronic load cell scale (model 8138 Toledo Weight-Plate; Bay State Scale Co, Cambridge, MA), with the subjects wearing preweighed gowns. Body weight change during the study was calculated as d117d1 weights. Height was measured to 0.1 cm using a wall mounted stadiometer. Waist circumference at the level of the umbilicus was measured in triplicate using standard techniques (Lohman et al, 1998). Blood samples Blood was drawn by venipuncture after a 12 h fast with the serum stored at 780 C prior to analysis. Serum European Journal of Clinical Nutrition


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b-hydroxybutyric acid (a measure of acute fasting) was measured by enzymatic reaction (Sigma Diagnostics, St Louis, MO) by automated analysis (Cobas Fara II, Roche Diagnostic Systems, Montclair, NJ).

Table 2 Energy expenditure, VO2max, and reported time spent devoted to physical activity in postmenopausal women classified as unrestrained or restrained eaters

Calculated energy variables and statistical analyses Three variables were calculated from TEE. Energy expenditure for physical activity and arousal (EEPA) was calculated as 0.9TEE7REE. Physical activity level (PAL) was calculated as TEE=REE. Nonexercise activity thermogenesis (NEAT) was calculated as 0.9TEE7(REE þ energy expenditure for physical activity) for 57 subjects (the ones for whom leisure time activity data were available), where energy expenditure for physical activity in this case was predicted from the Minnesota Leisure Time Physical Activity Questionnaire described above. Values are expressed as mean s.e.m. The Shapiro – Wilk test was used to examine the normality of each variable. In order to take into account the fact that multiple responses were being studied, Hotelling’s T-squared was used to test for differences in mean responses on all outcomes between restrained and unrestrained groups. Differences between groups in individual variables were further analyzed using Student’s independent t-test (normal distribution) or Mann – Whitney U-test (non-normal distribution). Levene’s test for equality of group variances was used to assess equal variances with the reported P reflecting whether the assumption of equal variances was achieved. The Pearson product – moment coefficient of correlation (r) was used to assess associations between variables. Analysis of variance and multiple regression analysis were used to determine the associations between variables in restrained vs unrestrained subjects. Differences between restrained and unrestrained groups in these associations were determined by including an interaction term between group and the independent variable of interest. Analysis of covariance (ANCOVA) was also used when necessary to control for confounders. Statistical significance was accepted at P < 0.05. The calculations were performed using SPSS 10.0 for Windows (SPSS Inc., Chicago, IL).

TEE (MJ=day) REE (MJ=day) EEPA (MJ=day) NEAT (MJ=day) Physical activity level (TEE=REE) Fasting RQ Maximum oxygen uptake VO2max (l=min) VO2max (ml kg=FFM=min) Reported physical activity (min=day) Light leisure time activity Moderate leisure time activity Heavy leisure time activity Total leisure time activity Reported physical activity (MJ=day) Total leisure time activity

Results Restrained subjects were significantly shorter than unrestrained subjects, but were not significantly different in age, BMI, body fatness, or waist circumference (Table 1). In addition, although there was a range of individual body weight fluctuations, there was no significant difference in measured weight change between the groups, an expected finding since subjects were instructed to eat normally and not deliberately gain or lose weight. Levels of b-hydroxybutyric acid were within the normal range and were not different between groups. Hotelling’s T-squared demonstrated that the two groups differed significantly in the mean responses to variables listed in Table 2 (P ¼ 0.0092). In absolute terms TEE, REE, EEPA, NEAT and fasting RQ were not significantly difEuropean Journal of Clinical Nutrition

Unrestrained

Restrained

9.49 0.23 5.18 0.10 3.37 0.19 2.1 0.2 1.84 0.04 0.85 0.01

8.96 0.26 5.21 0.08 2.86 0.20 1.7 0.2 1.72 0.04* 0.87 0.01

1.45 0.05 35.45 1.18

1.39 0.04 35.06 1.11

17.0 4.0 40.2 9.5 7.3 2.3 64.6 10.5

20.6 3.8 28.3 10.1 21.4 4.4* 70.5 11.8

1.2 0.2

1.4 0.2

a

x s.e.m. TEE, total energy expenditure; REE, resting energy expenditure; EEPA, energy expenditure for physical activity and arousal; NEAT, nonexercise activity thermogenesis; RQ, respiratory quotient. *Significantly different from unrestrained eaters: P < 0.05.

ferent between groups, though the restrained eaters had lower absolute mean values for TEE (P ¼ 0.07 by onetailed t-test) and NEAT (P ¼ 0.11 by one-tailed t-test) (Table 2). TEE adjusted for height was also not significantly different between groups (TEE of unrestrained eaters was 9.31 0.25 MJ, TEE of restrained eaters was 9.10 0.22 MJ=day). In addition, maximal aerobic capacity (VO2max) and energy expenditure for activity calculated from the Minnesota Leisure Time Physical Activity Questionnaire were not significantly different between groups. However, restrained eaters did have a significantly lower PAL (P < 0.05), and TEE adjusted for REE was almost significantly lower (P ¼ 0.07 by two-tailed t-test). Reported duration of heavy activity (such as swimming, stair climbing or snow skiing) was significantly higher in restrained eaters, but reported duration of light and moderate activities (such as brisk walking, dancing and gardening) was not significantly different between the groups. Taken together, the total reported time spent in leisure activities did not differ significantly between groups. The relationship between energy expenditure and workload during the test of maximal oxygen consumption (for workloads that all subjects performed) is shown in Figure 1. In this analysis, only data from the last 30 s of each workload period was used, to ensure subjects were in steady-state to the maximum possible extent. As seen, there was no significant difference between the groups at 50, 75 or 100 W power, and a similar lack of difference between the groups was found when VO2 was adjusted for weight or FFM in ANCOVA (data not shown). Table 3 summarizes Pearson correlation coefficients for relationships between variables in the restrained and unrestrained eaters. As shown, for all subjects combined TEE was


1063 Table 3 Pearson correlations (r) between energy expenditure and biological variables in postmenopausal women classified as unrestrained or restrained eaters Unrestrained TEE and Weight (kg) Fat-free mass (kg) Fat mass (kg) Resting energy expenditure (MJ=day) VO2max (l=min) VO2max=FFM (l=min=kg) Weight change (g=day) REE and Weight (kg) Fat-free mass (kg) Fat mass (kg) VO2max (l=min) VO2max=FFM (l=min=kg) Weight change (g=day) EEPA and Weight (kg) Fat-free mass (kg) Fat mass (kg) Resting energy expenditure (MJ=day) VO2max (l=min) VO2max=FFM (l=min=kg) Weight change (g=day) NEAT and Weight (kg) Fat-free mass (kg) Fat mass (kg) Resting energy expenditure (MJ=day) VO2max (l=min) VO2max=FFM (l=min=kg) Weight change (g=day)

Restrained

Total

0.07 0.20 70.05 0.41*

0.39* 0.56** 0.09 0.63**

0.27* 0.46** 0.03 0.52**

70.05 70.15 0.11

0.48*** 70.05 70.08

0.31* 70.07 70.01

0.65** 0.51*** 0.53*** 0.14 70.21 70.07

0.61** 0.68** 0.28 0.51*** 70.11 70.17

0.63** 0.60** 0.38*** 0.34* 70.16 70.12

70.27 70.05 70.33 70.09

0.23 0.40* 70.01 0.36*

0.03 0.26* 70.14 0.16

70.12 70.05 0.15

0.38* 70.01 70.02

0.21 70.02 0.04

70.21 70.17 70.16 70.23

0.41* 0.29 0.25 0.35*

0.16 0.14 0.10 0.09

Figure 1 Relationship between workload and energy expenditure at submaximal rates of work during the measurement of maximal oxygen consumption in women classified as unrestrained (open circle) and restrained (solid circle) eaters (solid line is for unrestrained eaters, dotted line for restrained eaters). Values shown are for work loads that all subjects were able to complete, and data from the last 30 s of each workload period (described in Methods) is used. There was no significant difference between the groups at any workload by ANOVA.

Significant relationships: *P < 0.05; **P < 0.001; ***P < 0.01. TEE, total energy expenditure; REE, resting energy expenditure; EEPA, energy expenditure for physical activity and arousal; NEAT, nonexercise activity thermogenesis; FFM, fat-free mass.

most strongly related to REE and FFM; REE was most strongly related to initial weight and FFM; EEPA was related to FFM. In addition, EEPA was related to FFM and REE in restrained eaters but not unrestrained eaters. NEAT was related to weight and REE in restrained eaters but no relationships with NEAT were significant in unrestrained eaters. In general, associations between energy and other variables tended to be stronger in restrained eaters than unrestrained eaters. Pearson correlation coefficients also showed a negative association between weight change and leisure time physical activity in unrestrained eaters (r ¼ 70.43, P ¼ 0.04) and no relationship in restrained eaters (r ¼ 70.02, P ¼ 0.92). The relationship between FFM and both TEE and REE are shown in Figures 2 and 3, respectively. Multiple regression analysis was also used to determine associations of REE, TEE, EEPA and NEAT with body composition and related parameters (weight, fat, FFM,

Dweight, VO2max and reported leisure time activity) as potential independent variables. The best fitting model for predicting REE contained both FFM and fat mass as significant variables (r2 ¼ 0.53, P < 0.001), and there was no significant effect of restraint status either as an independent variable (P ¼ 0.67) or as an interaction term with either body composition parameter. For TEE and EEPA there were no multiple regression models in which two or more independent variables were significant predictors. Concerning the other energy expenditure variables, NEAT was significantly predicted by a model containing weight, Dweight, restraint status and an interaction between restraint status and Dweight (r2 ¼ 0.14, P < 0.01), and the relationships between NEAT and weight change in the two groups are shown in Figure 4. The equations generated from the model for predicting NEAT were: NEAT in unrestrained eaters (MJ=day) ¼ 0.414 þ 0.03053*weight þ 0.012191*weight change; NEAT in restrained eaters

70.28 70.12 0.38

0.05 70.22 70.06

70.07 70.18 0.11

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Figure 2 Scatterplot showing the association between total energy expenditure and fat-free mass in postmenopausal women classified as unrestrained (open circle, UNR) or restrained (solid circle, RES) eaters (solid line is for unrestrained eaters, dotted line for restrained eaters). Slopes for the two groups were not significantly different by ANOVA.

(MJ=day) ¼ 70.332 þ 0.03053*weight70.001809*weight change, where weight is in kg, weight change in g=day. Discussion The results of this study suggest that, compared to unrestrained eaters who were not significantly different in body composition, restrained eaters with comparable levels of

Figure 3 Scatterplot showing the association between resting energy expenditure and fat-free mass in postmenopausal women classified as unrestrained (open circle, UNR) or restrained (solid circle, RES) eaters (solid line is for unrestrained eaters, dotted line for restrained eaters).

fitness and reported leisure time physical activity had no significant difference in TEE even after adjusting for height differences between the groups. This result contrasts with a previous report of very low TEE in restrained eaters compared to unrestrained eaters (Tuschl et al, 1990). Since energy intake equals energy expenditure in subjects maintaining energy balance, our results also suggest that postmenopausal restrained eaters are not self-restricting their energy intake into a range where metabolic adaptation

Figure 4 Scatterplot showing the association between nonexercise activity thermogenesis (NEAT) and weight change in postmenopausal women classified as unrestrained (open circle) or restrained (solid circle) eaters (solid line is for unrestrained eaters, dotted line for restrained eaters). In a multiple regression analysis (r2 ¼ 0.14, P < 0.01) with weight, weight change and restraint status as independent variables, restraint status was a significant predictor of NEAT (P ¼ 0.03) and there was an interaction between weight change and restraint status (P ¼ 0.048). European Journal of Clinical Nutrition


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occurs. The significance of this latter finding relates to the issue that animal models have consistently suggested beneficial anti-aging effects of dietary energy restriction when the extent of restriction is severe enough to have a measurable impact on such parameters as REE (Weindruch & Walford, 1988; Roberts et al, 2000). The results of the present study suggest that restrained eaters are not an appropriate model in which to investigate the possible anti-aging effects of human dietary restriction. The restrained eaters in our study did have a lower PAL ratio (1.72 vs 1.84), and a different relationship between calculated NEAT and body weight change; however, all the differences between the groups were relatively small; in the case of PAL, values for both groups were at the upper end of the range for ‘moderate’ activity (World Health Organization, 1985). Concerning the PAL ratio, our finding of slightly reduced PAL in restrained eaters is consistent in direction with the observation of Tuschl et al (1990), who reported reduced TEE in restrained eaters compared to unrestrained eaters after adjustment for group differences in height and body composition. However, the reduced energy expenditure in that study (Tuschl et al, 1990) was a substantial 25% (adjusted values) whereas ours was equivalent to only a 6% difference in TEE (and only 2% after adjusting for differences in height between the groups). It is possible that the large difference in TEE between the groups of Tuschl et al (1990) was due to lower strenuous physical activity in the restrained eaters, because physical activity was not assessed independently in that study. Consistent with that suggestion and with our own results, Verboeket-van de Venne et al (1994) found no significant difference in unadjusted 24 h energy expenditure between young restrained and unrestrained female students measured in a respiration chamber in which physical activity was necessarily restricted by the confined nature of the chamber. It is also important to note that the reduced PAL in restrained eaters in our study was apparently not due to altered REE, or reduced leisure time physical activity as quantified by questionnaire. As reported by Poehlman et al (1991) and Lawson et al (1995) for younger restrained eaters, REE, reported total leisure time activity and maximal aerobic capacity did not differ between the groups. Moreover, our restrained eaters did not have reduced energy expenditure for defined workloads between 50 and 100 W, suggesting equivalent energy costs of standardized physical activities in the two groups. A further possible difference between our study and that of Tuschl et al (1990) is that we documented weight change during the study period when weight was supposed to be maintained constant. The weight loss of our subjects was small ( 30 g=day) and if the subjects of Tuschl et al (1990) were in significant energy imbalance this could also have reduced TEE (Saltzman & Roberts, 1995). The observation that, compared to unrestrained eaters, restrained eaters have slightly reduced PAL but comparable levels of fitness and leisure time physical activity implies that the component of energy expenditure most affected by restrained eating might be NEAT, or nonexercise activity

thermogenesis. NEAT is a term that includes both spontaneous energy expenditure for fidgeting=non-accountable movement and thermogenesis different from that usual during postprandial metabolism, and is suggested to be one of the mechanisms by which genetically lean individuals may avoid excess weight gain (Levine et al, 1999). In our study, changes in NEAT may also include a component of energy expenditure due to changes in occupation-related activity, since this was not specifically quantified (please note, however, that women in both groups had similar occupations). We therefore compared our values for NEAT between the groups, using reported leisure time activity to provide data on physical activity. Unadjusted mean values for NEAT were lower in restrained eaters compared to unrestrained eaters but not significantly so. However, in models predicting NEAT from spontaneous weight change during the study and restraint status and controlled for initial weight, NEAT was significantly lower in restrained eaters and the relationship between weight change and NEAT was significantly different among the groups. Specifically, there was a positive relationship between NEAT and weight change in unrestrained eaters, and no relationship seen in restrained eaters. Concerning NEAT and energy regulation in our unrestrained individuals, the linear regression of NEAT and body weight change suggested that an approximate 1.3 MJ change in NEAT would be associated with a 6 MJ change in body energy (assuming weight change has an average energy content of 16 kJ=g — see Saltzman & Roberts, 1995). An alternative way of expressing these data is that NEAT was equivalent to 22% of the sum of changes in NEAT and body energy, which is an approximation of the energy intake imbalance if other components of energy expenditure do not change substantially with body weight change. The value of 22% is consistent with data from a previous study of ours, suggesting that the adaptive capacity of TEE is 15 – 30% of the change in energy intake during positive or negative energy balance, with perhaps a greater capacity for energy expenditure to decrease during undereating than to increase during overfeeding (Saltzman & Roberts, 1996). In their original paper on NEAT, Levine et al (1999) reported much higher values for percentage of excess energy intake during overeating that is channeled into energy expenditure (54%, with NEAT being the principal component). It is possible that differences between the studies in methodology (most notably, the þ 4.2 MJ=day overfeeding regimen, and the use of activity monitors) or the use of subjects with different susceptibilities to weight gain may have contributed to the different results, but this issue cannot be resolved at the present time and further research is needed. It is also important to recognize that a study larger than ours might detect a significant non-linear relationship between NEAT and weight change, which could have important implications for the role of NEAT in usual energy regulation. In restrained eaters, the lack of a relationship between NEAT and spontaneous weight change implied that there was no decrease in NEAT energy expenditure during European Journal of Clinical Nutrition


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negative energy balance and similarly no increase in NEAT during positive energy balance. This latter suggestion indicates an increased efficiency of weight gain during overeating. This is because during periods of overeating, increased NEAT would help attenuate excess body weight gain, and no increase in NEAT must be associated with increased energy deposition. The tendency to not increase NEAT during positive energy balance would potentially be counterbalanced by a smaller reduction in NEAT (and hence greater body energy loss) during negative energy balance. Viewed from this perspective, a lack of NEAT responsiveness can be considered a potentially contributing factor to the perceived increase in susceptibility to weight gain in restrained eaters. As a separate issue, it is also interesting to note that the capacity for adaptive thermogenesis in general may decline with age (Saltzman & Roberts, 1996), suggesting that those restrained eaters who are successfully able to adapt to lower levels of NEAT, such as the non-overweight restrained subjects in our study, may theoretically be at reduced risk of ageassociated weight gain. It is important to note that there are some significant general limitations in the calculation of NEAT. In particular the use of reported values for leisure time physical activity in the calculation, as in our study, to adjust TEE for defined physical activity may be problematic. Although there is no clearly superior alternative procedure for calculating NEAT (since the main alternative is use of activity monitors to predict physical activity, and activity monitors may detect fidgeting as well as defined physical activities, and hence count some percentage of NEAT as energy expenditure for physical activity), the possibility exists that one group misreported physical activity to a greater extent than another and that this biased the result. The fact that both reported physical activity and aerobic capacity were not significantly different between groups in our study would argue against this possibility. It is also important to note that correlational studies such as that reported here cannot distinguish between cause and effect, and thus the question of whether NEAT abnormalities caused or resulted from a pattern of restrained eating is not yet resolved. In summary, the results of this study suggest that there is no significant difference in TEE between healthy postmenopausal women classified as long-term restrained or unrestrained eaters. The restrained eaters did have a slightly reduced PAL level compared to unrestrained eaters matched for body composition. However, the differences between the groups were small and apparently due to reduced NEAT. Restrained eaters also had reduced NEAT responsiveness to changes in body weight, a finding that may help to explain their increased perception of susceptibility to weight gain. Further studies are needed to investigate in greater detail the role of NEAT in energy regulation, and the long-term consequences of dietary restraint for both energy regulation and health.


Acknowledgements —We gratefully thank the volunteers who participated in the study. We also acknowledge the expert assistance given by the recruiting department and the nursing staff of the Metabolic Research Unit for their professional assistance in data collection and care of the volunteers.

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