Original Article
Changes in Energy Expenditure Resulting from Altered Body Weight
N Engl J Med 1995; 332:621-628March 9, 1995
- Abstract
Background
No current treatment for obesity reliably sustains weight loss, perhaps because compensatory metabolic processes resist the maintenance of the altered body weight. We examined the effects of experimental perturbations of body weight on energy expenditure to determine whether they lead to metabolic changes and whether obese subjects and those who have never been obese respond similarly.
Methods
We repeatedly measured 24-hour total energy expenditure, resting and nonresting energy expenditure, and the thermic effect of feeding in 18 obese subjects and 23 subjects who had never been obese. The subjects were studied at their usual body weight and after losing 10 to 20 percent of their body weight by underfeeding or gaining 10 percent by overfeeding.
Results
Maintenance of a body weight at a level 10 percent or more below the initial weight was associated with a mean (±SD) reduction in total energy expenditure of 6±3 kcal per kilogram of fat-free mass per day in the subjects who had never been obese (P<0.001) and 8±5 kcal per kilogram per day in the obese subjects (P<0.001). Resting energy expenditure and nonresting energy expenditure each decreased 3 to 4 kcal per kilogram of fat-free mass per day in both groups of subjects. Maintenance of body weight at a level 10 percent above the usual weight was associated with an increase in total energy expenditure of 9±7 kcal per kilogram of fat-free mass per day in the subjects who had never been obese (P<0.001) and 8±4 kcal per kilogram per day in the obese subjects (P<0.001). The thermic effect of feeding and nonresting energy expenditure increased by approximately 1 to 2 and 8 to 9 kcal per kilogram of fat-free mass per day, respectively, after weight gain. These changes in energy expenditure were not related to the degree of adiposity or the sex of the subjects.
Conclusions
Maintenance of a reduced or elevated body weight is associated with compensatory changes in energy expenditure, which oppose the maintenance of a body weight that is different from the usual weight. These compensatory changes may account for the poor long-term efficacy of treatments for obesity.
Media in This Article
Figure 3
Total and Resting Energy Expenditure According to Fat-free Mass at the Initial Weight and after a Gain or Loss in Weight.Figure 2
Mean (±SD) Observed-minus-Predicted Total Energy Expenditure (Shaded Bars) Based on the Regression of Total Energy Expenditure in a Model with a Variable Combining Fat-free Mass and Fat Mass in the Same Subjects at Their Initial Weight.Article Activity
- Article
Obesity is a common and intractable problem in some modern societies. Body weight is normally regulated by integrated, coordinate effects on food intake and energy expenditure.1 The high rate of recidivism among obese people who lose weight may reflect the operation of such regulatory processes.2-4
In humans, total energy expenditure is accounted for by resting energy expenditure (approximately 60 percent of total energy expenditure), which is the metabolic cost of processes such as the maintenance of transmembrane ion gradients and resting cardiopulmonary activity; the thermic effect of feeding (approximately 10 percent of total energy expenditure), which is the energy expended in the digestion, transport, and deposition of nutrients; and nonresting energy expenditure (approximately 30 percent of total energy expenditure), which is all the remaining expenditure of energy, mainly in the form of physical activity.5 In an earlier study, we found a persistent 28 percent decrease in the energy expended per unit of body-surface area in formerly obese patients with a stable reduced weight,6 suggesting a metabolic resistance to the maintenance of a reduced body weight. The present study was designed to examine the components of energy expenditure during the maintenance of usual and altered body weight in obese subjects and subjects who had never been obese.
Methods
Subjects
Eighteen obese subjects (11 women and 7 men; mean [±SD] age, 29±10 years [range, 21 to 45]) and 23 subjects who had never been obese (7 women and 16 men; mean age, 26±10 years [range, 19 to 41]) were recruited through physicians' referrals or advertisements (Table 1Table 1
Characteristics and Body Composition of Subjects at Initial and Altered Weights.). All subjects were at their maximal lifetime weight and had maintained this weight within a range of 2 kg for at least six months. None were taking medications or on special diets. Subjects whose body-mass index (expressed as the weight in kilograms divided by the square of the height in meters) was higher than 28.0 were classified as obese.7 All subjects had normal findings on physical examination and laboratory evaluations, including thyroid-function tests, complete blood count, tests for hepatitis A and B and human immunodeficiency virus infection, biochemical tests, and urinalysis. Six of the obese subjects and two of those who had never been obese smoked 2 to 10 cigarettes daily throughout the study. The protocol was approved by the Rockefeller University Hospital Institutional Review Board, and written informed consent was obtained from all the subjects.Study Design
The subjects were admitted to the Clinical Research Center at Rockefeller University and fed a liquid formula (40 percent fat [corn oil], 45 percent carbohydrate [glucose polymer], and 15 percent protein [casein hydrolysate]) supplemented with 5.0 g of iodized sodium chloride, 1.9 g of potassium ions as a potassium salt, and 2.5 g of calcium carbonate per day, 1 mg of folic acid twice weekly, and 36 mg of ferrous iron every other day. The mean caloric content of this formula, measured with a bomb calorimeter, was 1.36 kcal per gram. With the use of standard digestibility quotients, the content of metabolizable calories was 1.25 kcal per gram.8 Fecal calorie and urinary nitrogen losses were measured at all weight plateaus to confirm that they did not change (see below). The caloric intake was adjusted until the body weight was constant (slope of the regression line of body weight [grams] vs. time [days], <10 g per day) for at least 14 days. All subjects then underwent studies of energy expenditure and body composition during approximately a 10-day period while continuing to ingest the same quantity of dietary formula. Body composition was analyzed by hydrodensitometry9; stool and urine samples, collected for eight days, were analyzed to determine fecal calorie loss (by bomb calorimetry) and urinary nitrogen excretion10; and resting energy expenditure and the thermic effect of feeding were determined by indirect calorimetry with the use of a Beckman MMC Horizon Metabolic Cart (Beckman Instruments, Fullerton, Calif.) with a ventilated hood fitted snugly around the subject's neck11 (and unpublished data).
Resting energy expenditure at 8 a.m. in the postabsorptive state was calculated from oxygen consumption corrected for the respiratory quotient and the daily rate of nitrogen excretion based on the nitrogen content of the dietary formula and the rate of urinary nitrogen excretion. To measure the thermic effect of feeding, at 9 a.m. the subjects were given dietary formula with a caloric content equal to 60 percent of the 24-hour resting energy expenditure measured that morning. Oxygen consumption and carbon dioxide production were measured in the hood calorimeter for 30 minutes 2 and 4 hours after the feeding. The area of the polygon whose base is the prefeeding value of resting energy expenditure and whose other vertexes are resting energy expenditure at 9 a.m., 11 a.m., and 1 p.m. represents the increase in energy expenditure during the four hours after ingestion of food; this area was used to calculate the percentage of calories oxidized after ingestion of the formula.
Since no technique is available for the direct measurement of nonresting energy expenditure, we calculated this component of energy expenditure as the difference between total energy expenditure and the sum of the resting components of total energy expenditure: nonresting energy expenditure = total energy expenditure - (resting energy expenditure + thermic effect of feeding). In a subgroup of subjects studied at multiple weight plateaus, total energy expenditure was also determined by the differential excretion rates12 of two stable isotopes of water (2H2O and H2 18O) and by indirect calorimetry performed at the Clinical Diabetes and Nutrition Section, National Institute of Diabetes and Digestive and Kidney Diseases (Phoenix, Ariz.), in a respiration chamber equipped with wall-mounted radar detectors to monitor physical activity.13 These subjects also underwent measurement of body composition by isotope dilution12 and by dual-photon absorptiometry14 to validate the caloric titration and hydrodensitometric methods used in the study (unpublished data).
After the completion of studies at their initial weight, 11 of the obese subjects and 13 of the subjects who had never been obese (hereafter referred to as nonobese) were given the maximally tolerated amount of self-selected foods (generally 5000 to 8000 kcal per day) until they had gained 10 percent of their initial body weight (Figure 1Figure 1
Study Design.). No formula was ingested during the period of weight gain, which ranged from 4 to 6 weeks in the nonobese subjects and from 6 to 10 weeks in the obese subjects. At the new weight plateau, the dietary formula was reinstated, and the quantity of formula was titrated to maintain the weight. When the weight had been stable for at least 14 days, the studies of energy expenditure and body composition, described above, were repeated. Eight obese women who had undergone and maintained a 10 percent weight gain were then fed 800 kcal per day of the formula until they had returned to their initial weight. They were given the same number of kilocalories of formula that had been required to maintain their initial weight, and the studies of energy metabolism were repeated once their weight had been stabilized.After the initial-weight studies described above, 9 obese subjects and 11 nonobese subjects were fed 800 kcal of the dietary formula per day until their body weight had been reduced to a level that was 10 percent below their initial weight (Figure 1). (Eight of the obese and one of the nonobese subjects had previously undergone studies after a 10 percent gain in weight.) The period of weight loss ranged from 4 to 7 weeks for the nonobese subjects and from 6 to 14 weeks for the obese subjects. When the subjects had lost 10 percent of their initial weight, the formula was reinstated and adjusted to maintain the weight for at least 14 days; the studies described above were then repeated. Ten obese subjects who had undergone initial-weight studies (seven of whom were also studied after a 10 percent weight loss) were fed 800 kcal of dietary formula per day until they had lost 20 percent of their initial weight. The studies described above were performed after their weight had stabilized at the lower level.
Resting energy expenditure was determined in some subjects at the end of each period of weight gain or loss, when the intended level of weight had been achieved (10 percent higher or lower than the initial weight or after a return to the initial weight) but the subjects were still gaining or losing weight. These studies were performed to assess the degree to which the metabolic status was carried over from a period of changing weight to a period of stable weight.
Statistical Analysis
The results are presented as means ±SD. Energy expenditure at each weight plateau is expressed as the absolute number of kilocalories per day, as well as the number per kilogram of fat-free mass, to allow comparisons among different groups of subjects at the same weight plateau and among different weight plateaus for the same subject. The thermic effect of feeding and fecal calorie loss are expressed as percentages of ingested calories that were oxidized and lost in stool, respectively. Comparisons of energy expenditure in the same subjects at different weight plateaus were made by a one-way analysis of variance with repeated measures.15 The effects of sex and adiposity on measures of energy expenditure at different weight plateaus were determined by a multivariate analysis of variance with repeated measures15 in which sex and adiposity were treated as dichotomous variables (male vs. female and nonobese vs. obese).
At the usual body weight, resting energy expenditure is closely correlated with measures of metabolic mass (e.g., fat-free mass).13 Regression lines relating energy expenditure to metabolic mass do not have zero intercepts.5 Thus, subjects with values on the same regression line can have different values for the ratio of energy expenditure to metabolic mass. To correct for this possibility, regression equations relating measures of energy expenditure to fat-free mass and fat mass at the initial weight were calculated at that weight and used to determine the predicted value of energy expenditure in the same subject at each new weight plateau. The observed-minus-predicted values were then tested against the null hypothesis that the observed-minus-predicted value was 0, to determine whether the observed values differed significantly from the predicted values for each subject. All statistical tests were two-tailed.
Results
Energy Expenditure
The rates of energy expenditure changed in both the obese and the nonobese subjects after changes in body weight (Table 2Table 2
Measures of 24-Hour Energy Expenditure. and Figure 2Figure 2Mean (±SD) Observed-minus-Predicted Total Energy Expenditure (Shaded Bars) Based on the Regression of Total Energy Expenditure in a Model with a Variable Combining Fat-free Mass and Fat Mass in the Same Subjects at Their Initial Weight. and Figure 3Figure 3Total and Resting Energy Expenditure According to Fat-free Mass at the Initial Weight and after a Gain or Loss in Weight.). A 10 percent increase or decrease in the usual weight was accompanied by a 16 percent increase or 15 percent decrease, respectively, in 24-hour total energy expenditure corrected for body composition. Fat-free mass was significantly related to total energy expenditure, resting and nonresting energy expenditure, and the thermic effect of feeding. Fat mass was significantly related to total and resting energy expenditure.In agreement with the results of other studies,16 total energy expenditure and resting energy expenditure, expressed as kilocalories per kilogram of fat-free mass per day, were significantly higher in the obese subjects than in the nonobese subjects, whereas the thermic effect of feeding was lower in the obese subjects than in the nonobese subjects.17,18 The higher resting energy expenditure in the obese subjects probably reflects increased cardiorespiratory work related to chest-wall weight and a larger mass of adipose tissue. Smokers did not differ significantly from nonsmokers for any of the measures. Fecal calorie and urinary nitrogen losses, expressed as percentages of ingested calories and protein, respectively, were not significantly affected by changes in body weight and did not differ significantly according to sex or prior adiposity.
Effects of Weight Gain
Total energy expenditure, nonresting energy expenditure, and the thermic effect of feeding were significantly higher after a 10 percent gain in weight than at the initial weight. Stabilization of body weight after a 10 percent gain resulted in significant increases in observed-minus-predicted values for total energy expenditure, nonresting energy expenditure, and the thermic effect of feeding (Table 2). The magnitude of these changes was not affected by sex or initial adiposity. In 14 subjects (7 obese and 7 nonobese), the percentage of time spent in motion during a 23-hour period, measured in a respiration chamber, did not differ significantly between the initial weight (9.1±2.0 percent) and the 10 percent higher weight (8.6±2.1 percent, P = 0.47).
Return to Initial Weight
Eight obese women were studied at their initial weight, at a weight 10 percent higher than their initial weight, and after a return to their initial weight. No significant differences in body composition or in any aspect of energy expenditure were noted between the time of the initial-weight study and the return to the initial weight (Table 1 and Table 2).
Effects of Weight Loss
Total energy expenditure and nonresting and resting energy expenditure were significantly lower at weights 10 and 20 percent below the initial weight than at the initial weight (Table 2). Stabilization of body weight at a level 10 percent below the initial weight was associated with negative observed-minus-predicted values for total energy expenditure and nonresting and resting energy expenditure. Stabilization of body weight at a level 20 percent below the initial weight was associated with negative observed-minus-predicted values for total energy expenditure and nonresting energy expenditure. The magnitude of these changes was not significantly related to sex or initial adiposity. There were no significant differences in energy expenditure at weights 10 and 20 percent below the initial weight, suggesting that the maximal adaptation to the maintenance of a reduced body weight was already attained at the 10 percent level. Among eight subjects (six nonobese and two obese) the mean percentage of time spent in motion in the respiratory chamber was 9.2±2.0 percent at the initial weight and 9.4±1.8 percent after a 10 percent loss in weight (P = 0.52).
Static Weight Maintenance versus Dynamic Weight Change
The high degree of weight stability among the subjects (mean rate of weight change during the 10-day testing periods, -1.2 g per day) suggests that body composition was constant during weight maintenance. When weight and body composition are stable, the respiratory quotient reflects mainly the composition of the diet. As expected, the processes of weight gain and loss resulted in increases and decreases, respectively, in the respiratory quotient. However, the respiratory quotient did not differ significantly from the quotient for the dietary formula (0.85) at any of the weight plateaus, indicating that the subjects were in caloric balance at each plateau, without a carryover effect of weight loss or gain on caloric requirements or substrate use.
The effects of weight gain and loss on energy metabolism were also assessed by comparing resting energy expenditure at the end of the dynamic phase of weight change with that at the end of the period of maintenance of the same weight (Table 3Table 3
Comparison of Resting Energy Expenditure and Respiratory Quotient at the End of a Period of Weight Gain or Loss and during Maintenance of the Altered Weight.). The process of increasing weight by overfeeding was accompanied by approximately 12 percent more resting energy expenditure than a 10 percent weight gain maintained for 14 days. Conversely, the process of losing weight on a diet of 800 kcal per day resulted in 10 to 15 percent less resting energy expenditure than a stabilized weight loss of 10 percent.Body Composition
A 10 percent gain in weight resulted in increases in adipose tissue and fat-free body mass, and a weight loss of 10 percent resulted in significant decreases in both these measures. These changes in body composition, expressed as the change in the percentage of body fat, were statistically significant within all subgroups of subjects. There was no evidence that sex or prior adiposity affected the distribution of weight gained or lost between fat mass and fat-free mass (Table 1). There was a trend for the obese subjects to gain a lower percentage of weight as fat than the nonobese subjects (P = 0.11) and to lose a higher percentage of weight as fat (P = 0.13).
Discussion
We found that energy expenditure adjusted for metabolic mass increased with a weight gain and decreased with a weight loss. These changes in energy expenditure were evident during periods of stable altered body weight and were in a direction tending to return the subject to his or her initial weight; their magnitude was similar in nonobese and obese subjects. After a 10 percent gain in weight, the increase in total energy expenditure reflected a large increase in the absolute number of kilocalories of nonresting energy expenditure per day and a small increase in the absolute number of kilocalories per day attributed to the thermic effect of feeding. After a 10 or 20 percent loss in weight, the decline in total energy expenditure reflected similar decreases in both nonresting and resting energy expenditure.
In some studies, energy expenditure has been higher than that predicted for metabolic mass during weight gain or maintenance of a higher body weight in nonobese subjects.19 In other studies,20,21 such an increase has not occurred. Resting energy expenditure declines during a period of weight loss,22 but whether a similar decline occurs when weight loss has stabilized is the subject of considerable debate.23-26 Likewise, there is a lack of agreement concerning the effect of weight reduction on total energy expenditure; both decreases (of 8 to 22 percent) and no change or increases (of approximately 9 percent, as compared with the values for weight-matched nonobese controls) have been reported.27-29
Several considerations are important in drawing conclusions from our findings. The alterations in energy expenditure do not reflect carryovers from the dynamic periods of weight change, since the measures of energy expenditure at the initial weight and after a return to that weight were similar, the anticipated changes in resting energy expenditure occurred during periods of weight change, and respiratory quotients at the various weight plateaus equaled that predicted for a stable weight while subjects were ingesting the dietary formula. Subtle shifts in body composition during periods of stable weight could have masked differences in energy expenditure among the weight plateaus. Such changes are unlikely, since they would have led to discrepancies between total energy expenditure as measured by formula titration and total energy expenditure as measured by elimination rates for 2H2O and H2 18O. Yet these two measures were highly correlated and did not differ significantly at any weight plateau (unpublished data). In addition, respiratory quotients during all periods of stable weight equaled that predicted on the basis of the nutrient composition of the formula diet, suggesting that there was no net storage or catabolism of fat.
Although we did not examine the permanence of these changes in rates of energy expenditure, a reduced level of energy expenditure has been reported to persist in subjects who have maintained a reduced body weight for periods ranging from six months to more than four years.6 The aspect of body composition that mediates or signals these changes in energy expenditure is not known. In our study, the largest changes in body composition with weight alteration occurred in fat mass. A substantial body of literature suggests that the mass of adipose tissue or the size of adipocytes is the aspect of body composition that is regulated,30 but the feedback mechanism for the effect of fat mass on energy metabolism is not known. A candidate gene for such a signal from fat has recently been cloned.31
The metabolic variable most affected by weight change was nonresting energy expenditure. Since it was not measured directly, the nature of the changes in this variable cannot be identified. Differences in the energy needed to move a larger or smaller body mass account for only some of the differences in energy expenditure, as suggested by Weigle and Brunzell, in whose study lost weight was replaced with backpack loads.32 This cannot be the entire explanation, however, since obese and lean subjects at their usual body weight have nearly equal nonresting energy expenditure, corrected for both fat-free mass and fat mass. One possibility is that the efficiency with which skeletal muscle performs mechanical work is different at different weight plateaus (decreased with a 10 percent gain in weight and increased with a 10 percent loss). The efficiency of muscular work before and after weight gain does not change, nor does the energy expenditure associated with moderate exercise.33,34 The effect of a change in weight on the energy expended during mild physical exertion, however, has not been systematically studied, and this minimal level of exertion may be most representative of the physical activity of sedentary adults. The possibility that changes in skeletal muscle have a role in mediating the alterations in energy expenditure that occur with weight loss may be the reason exercise is helpful in maintaining a reduced body weight.
Body weight in adults is remarkably stable for long periods of time. In the Framingham Study the body weight of the average adult increased by only 10 percent over a 20-year period.35 Such a fine balance is evidence of the presence of regulatory systems for body weight.4,36 Whatever the mechanism (or mechanisms), the weight at which regulation occurs differs from one person to another, and these differences are almost certainly due in part to genetic37,38 and developmental39 influences.
Our results have immediate implications for the clinical management of obesity. Many obese people who lose weight have metabolic alterations similar to those observed in our subjects. The reduction in energy expenditure to a level 15 percent below that predicted for body composition, as a result of a 10 percent (or larger) decrease in body weight, is large when one considers that an average daily intake of 2500 kcal would be associated with a positive energy balance of approximately 375 kcal per day. In addition, the sense of hunger or dysphoria that may accompany this state of reduced energy expenditure will promote increased food intake, further widening the gap between energy output and intake.3 Physicians should be aware that for some obese patients the achievement of what is considered to be a more healthful body weight may be accompanied by metabolic alterations that make it difficult to maintain the lower weight. Nevertheless, the beneficial effect of even a modest weight loss on lipid and carbohydrate metabolism in obese patients40,41 justifies persistent efforts at weight reduction and maintenance of a reduced body weight for the treatment of obesity.
Supported in part by grants from the National Institutes of Health (DK30583 and GCRCRR00102) and the Weight Watchers Foundation. During part of the study period, Dr. Rosenbaum was an Amparo Rugarcia Clinical Scholar, and Dr. Leibel was an Established Investigator of the American Heart Association.
We are indebted to Drs. Elio Presta, Streamson C. Chua, and Lisa C. Hudgins, Mr. David Markel, Ms. Rachael Kolb, Ms. Eileen Mullen, Ms. Jennifer Ziedonis, Ms. Alice Murphy, and the members of the nursing staff of the Rockefeller University Hospital Clinical Research Center for their help with the care of the subjects; to Ms. Cynthia Seidman and her staff of research dietitians for supervising the preparation and testing of the dietary formula; to Drs. Steven Heymsfield and Steven Lichtman at St. Luke's–Roosevelt Hospital Medical Center for supervising the body-composition studies; to Dr. Eric Ravussin at the National Institute of Diabetes and Digestive and Kidney Diseases in Phoenix, Arizona, for supervising the chamber respirometry studies and for his helpful suggestions on the manuscript; and to Dr. Dwight Matthews and Mr. Chuck Gilker for performing the mass spectrometric analysis of urine for 2H2O and H2 18O.
Source Information
From the Laboratory of Human Behavior and Metabolism, Rockefeller University, 1230 York Ave., New York, NY 10021, where reprint requests should be addressed to Dr. Leibel.
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