Constrained Total Energy Expenditure and Metabolic Adaptation to Physical Activity in Adult Humans

Abstract

Current obesity prevention strategies recommend increasing daily physical activity, assuming that increased activity will lead to corresponding increases in total energy expenditure and prevent or reverse energy imbalance and weight gain [1-3]. Such Additive total energy expenditure models are supported by exercise intervention and accelerometry studies reporting positive correlations between physical activity and total energy expenditure [4] but are challenged by ecological studies in humans and other species showing that more active populations do not have higher total energy expenditure [5-8]. Here we tested a Constrained total energy expenditure model, in which total energy expenditure increases with physical activity at low activity levels but plateaus at higher activity levels as the body adapts to maintain total energy expenditure within a narrow range. We compared total energy expenditure, measured using doubly labeled water, against physical activity, measured using accelerometry, for a large (n = 332) sample of adults living in five populations [9]. After adjusting for body size and composition, total energy expenditure was positively correlated with physical activity, but the relationship was markedly stronger over the lower range of physical activity. For subjects in the upper range of physical activity, total energy expenditure plateaued, supporting a Constrained total energy expenditure model. Body fat percentage and activity intensity appear to modulate the metabolic response to physical activity. Models of energy balance employed in public health [1-3] should be revised to better reflect the constrained nature of total energy expenditure and the complex effects of physical activity on metabolic physiology.

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Figures

Figure 1

Schematic of Additive total energy expenditure and Constrained total energy expenditure models. In Additive total energy expenditure models, total energy expenditure is a simple linear function of physical activity, and variation in physical activity energy expenditure (PA) determines variation in total energy expenditure. In Constrained total energy expenditure model, the body adapts to increased physical activity by reducing energy spent on other physiological activity, maintaining total energy expenditure within a narrow range.

Figure 2

A. Total energy expenditureADJ (kcal/d) and physical activity (CPM/d) in the METS sample. Boxplots indicate medians and quartiles of total energy expenditureADJ for each decile of CPM/d, and are centered on the median CPM/d value for each decile. Lowess (yellow) and ordinary least squares (gray) regression lines are shown. The change point (230 CPM/d) for the change-point regression, indicated by the vertical blue line, marks the activity level at which the slope of the total energy expenditureADJ:CPM/d regression becomes indistinguishable from zero. Total energy expenditureADJ values for three subjects exceed 3500 and are not shown; see Fig. S1C. See also Table S2 and Figures S1 and S3. B. The effect of CPM/d on Total energy expenditureADJ for subjects above increasing CPM/d thresholds. Black circles show the β value for CPM/d for subjects above a given CPM/d threshold, blue lines represent ±standard error. Analyses include manual labor. Degrees of freedom (df) are given for major CPM/d thresholds.

Figure 3

A. Total energy expenditureADJ, resting metabolic rateADJ, and activity energy expenditureADJ (kcal/d) versus physical activity (CPM/d) for the subset of subjects (n=204) with measured resting metabolic rate. Ordinary least squares regressions are shown. Resting metabolic rateADJ is not correlated with physical activity, nor are total energy expenditureADJ or activity energy expenditureADJ among subjects with physical activity above 230 CPM/d. B. Components of total energy expenditure (dotted line) modeled as a function of physical activity, using relationships shown in panel A. Resting metabolic rate is constant (1540 kcal/d). Below the change-point of 230 CPM/d, total energy expenditure = 1.12 CPM/d + 2336; above 230 CPM/d, total energy expenditure is constant (2600 kcal/d). The thermic effect of food (TEF) is calculated as 10%total energy expenditure. Activity energy expenditure (red) calculated as 0.9total energy expenditure – resting metabolic rate, is divided into two components. Activity energy expenditure1 (AEE1, solid red) increases with physical activity in a dose-dependent manner as 1.13CPM/d, the slope of the Adjusted energy expenditure vs physical activity regression for subjects below 230 CPM/d in panel A. Activity energy expenditure2 (AEE2, hatched red) is the remainder of activity energy expenditure, calculated as activity energy expenditure2 = activity energy expenditure – activity energy expenditure1. See also Figures S1 and S3.