A decline in resting energy expenditure (REE) beyond that predicted from changes in body composition has been noted following dietary-induced weight loss. However, it is unknown whether a compensatory downregulation in REE also accompanies exercise (EX)-induced weight loss, or whether this adaptive metabolic response influences energy intake (EI).
Thirty overweight and obese women (body mass index (BMI)=30.6±3.6 kg/m2) completed 12 weeks of supervised aerobic EX. Body composition, metabolism, EI and metabolic-related hormones were measured at baseline, week 6 and post intervention. The metabolic adaptation (MA), that is, difference between predicted and measured REE was also calculated post intervention (MApost), with REE predicted using a regression equation generated in an independent sample of 66 overweight and obese women (BMI=31.0±3.9 kg/m2).
Although mean predicted and measured REE did not differ post intervention, 43% of participants experienced a greater-than-expected decline in REE (−102.9±77.5 kcal per day). MApost was associated with the change in leptin (r=0.47; P=0.04), and the change in resting fat (r=0.52; P=0.01) and carbohydrate oxidation (r=−0.44; P=0.02). Furthermore, MApost was also associated with the change in EI following EX (r=−0.44; P=0.01).
Marked variability existed in the adaptive metabolic response to EX. Importantly, those who experienced a downregulation in REE also experienced an upregulation in EI, indicating that the adaptive metabolic response to EX influences both physiological and behavioural components of energy balance.
Although a reduction in resting energy expenditure (REE) following dietary energy restriction is well documented,1 it has been suggested that some individuals experience a greater-than-expected decline in REE based on changes in fat mass (FM) and fat-free mass (FFM).2 This compensatory downregulation in REE is thought to be an autoregulatory response that acts to attenuate the prescribed energy deficit and protect against sustained weight loss.3 Importantly, this adaptive response in energy expenditure is characterised by marked individual variability4 and may help explain the disparity between predicted and actual weight loss observed during weight-loss interventions.5 However, it should be noted that the existence and clinical importance of such adaptive thermogenesis during weight loss has been contested.6, 7
The adaptive suppression of REE during weight loss is thought to result from a downregulation in sympathetic nervous system activity, which is mediated through weight-induced changes in thyroid hormones8, 9 and in particular, leptin.10, 11 However, although leptin influences the regulation of energy expenditure and energy intake (EI), the impact of adaptive thermogenesis on EI during weight loss has not been examined. Furthermore, although adaptive thermogenesis has been established following dietary-induced weight loss, its existence during exercise (EX)-induced weight loss (that is, EX alone) has yet to be examined. This is of importance, as the biological and behavioural responses to dietary- and EX-induced weight loss may differ. Therefore, this study aimed to examine the extent of adaptive thermogenesis during EX-induced weight loss and its effect on compensatory eating during 12 weeks of supervised aerobic EX.
Materials and methods
Thirty overweight and obese women (body mass index (BMI)=30.6±3.6 kg/m2) participated in the present study. Participants were recruited from the University of Leeds, UK, and surrounding areas using poster advertisements and recruitment emails. Participants were physically inactive (⩽2 h per week of EX over the previous 6 months), weight stable (±2 kg for the previous 3 months), non-smokers and not taking medication known to effect metabolism or appetite. All participants provided written informed consent before taking part, and ethical approval was granted by the Institute of Psychological Sciences Ethics Board, University of Leeds, and the Leeds West NHS Research Ethics Committee (09/H1307/7).
Participants completed a 12-week supervised aerobic EX programme (EX) designed to expend 2500 kcal per week. Body composition, REE, EI and fasting glucose, insulin and leptin were measured at baseline, week 6 and post intervention. To disclose any change in REE that could not be explained by changes in body composition, the difference between predicted and measured REE was calculated during EX. To predict REE, a regression equation based on FM and FFM was generated in an independent reference population of 66 sedentary women, matched for age and body composition (BMI=31.0±3.9 kg/m2).
Participants in EX completed a 12-week aerobic EX programme, expending 500 kcal per session at 70% of age-predicted maximum heart rate (that is, 220—age), 5 days per week. All EX sessions were supervised in the research laboratory, and participants could choose from a range of EX modes (running, cycling or rowing stepping). Individual EX prescriptions were calculated using standard stoichiometric equations,12 based on the relationship between heart rate and VO2/VCO2 during a maximal incremental treadmill test. To account for changes in cardiovascular fitness during the intervention, the incremental test was performed at baseline, week 6 and post intervention, with the EX prescription adjusted accordingly. To verify and record the duration and intensity of EX, participants wore heart rate monitors during each session (Polar RS400, Polar, Kempele, Finland). Total EX-induced energy expenditure during the intervention was 27 960±3479 kcal, which represented >98% of the prescribed EX-induced energy expenditure.
At baseline, week 6 and post intervention, REE, body composition and maximal aerobic capacity (VO2peak) were measured in the morning (0700–0900 h) following an overnight fast (2200–0000 h). Baseline measures were taken before the start of EX (that is, in a sedentary state), whereas post-intervention measures were taken during the week following the completion of EX (with a minimum of 48 h between the final EX session). On arrival, REE was initially measured using an indirect calorimeter fitted with a ventilated hood (GEM, Nutren Technology Ltd, Cheshire, UK), using the procedures outlined by The American Dietetic Association.13 Participants remained awake but motionless in a supine position for 45 min, with REE calculated using the Weir equation14 from respiratory data averaged over the final 30 min of assessment. The non-protein respiratory exchange ratio was calculated as the ratio of VCO2 to VO2, whereas fat and carbohydrate (CHO) oxidation rates were calculated using standard stoichiometric equations.12 These calculations were based on the assumption that nitrogen excretion was negligible.
Following the measurement of REE, body composition was measured using air-displacement plethysmography (BOD POD Body Composition System, Life Measurement, Inc., Concord, CA, USA). After voiding, participants were weighed (to the nearest 0.01 kg) and instructed to sit in the BOD POD. Measurements were then taken according to manufacturers’ instructions, with thoracic gas volumes estimated using the manufacturer’s software. Finally, VO2peak was determined using a validated maximal incremental treadmill test,15 with expired air (Sensormedics Vmax29, Sensormedics Corporation, Yorba Linda, CA, USA) and heart rate (Polar RS400, Polar) continoulsy measured. Respiratory and heart rate data from the incremental treadmill test were also used to determine the relationship between VO2/VCO2 and heart rate during EX, and used alongside standard stoichiometric equations12 to calculate individual EX prescriptions.
Metabolic- and appetite-related hormones
Fasting glucose, insulin and leptin were measured at baseline, week 6 and post intervention in a subsample of 20 participants who completed EX. Fasting venous blood samples were collected into EDTA-containing monovette tubes. After collection, blood samples were centrifuged for 10 min at 4 °C at 3500 r.p.m. and were immediately pipetted into eppendorf tubes and stored at −80° C until analysis. Insulin and leptin were analysed using a magnetic bead based multiples kit (Millipore, Billerica, MA, USA). Insulin sensitivity was calculated using the homeostatic model of assessment.16
Assessment of food intake
Food intake was measured at baseline, week 6 and post intervention using a laboratory-based test meal protocol. At each time point, participants completed two meal days (separated by at least 1 day) in which they consumed test meals at 4-hourly intervals during the day that were either high (>50% of energy from fat) or low in fat (<20% of the energy from fat). The order of these days was randomised and counterbalanced, and no EX was performed on these days. The mean proportion of energy contributed by fat, protein and carbohydrate to total daily EI during the high-fat meal days was 54.4%, 7.9% and 37.7%, respectively. During the low-fat meal days, the mean proportion of energy contributed by fat, protein and carbohydrate to total daily EI was 19.3%, 8.3% and 72.4%, respectively. During these meal days, participants consumed only the foods/drinks provided to them, but ad libitum water consumption was permitted. Meals consisted of an individualised energy breakfast (ad libitum at baseline and then fixed at baseline levels for the remainder of EX), a fixed energy lunch (800 kcals) and ad libitum dinner meal. After the dinner meal, participants were free to leave the research unit but were given an ad libitum snack box of foods to consume if desired during the evening. A detailed description of the foods provided can be found elsewhere.17
All meals consumed in the research unit were eaten in isolation, with participants instructed to eat as much or as little as they wanted until comfortably full (during ad libitum meal consumption). Food was provided in excess of expected consumption, with participants able to request further food and water if required. EI was calculated by weighing the food before and after consumption to the nearest 0.1 g, and with reference to the manufacturers’ energy values. To calculate test meal EI, the energy equivalences used for protein, fat and carbohydrate were 4, 9 and 3.75 kcal/g, respectively. Before commencing the study, participants completed a food preference questionnaire, and if they strongly disliked any of the test foods they were excluded if a suitable alternative (matched for macronutrient composition) could not be found.
Calculation of the metabolic adaptation
In order to predict REE during the intervention, a regression equation was generated from an independent sample of overweight and obese women (reference (REF)). This REF population did not include individuals who participated in EX, and REE and body composition were measured in REF using the same procedures described in the present study. As can be seen in Tables 1 and 2, no differences existed between REF and EX at baseline in terms of age, body composition, REE or respiratory exchange ratio. Initially, age, FM and FFM were entered as independent variables into a stepwise multiple regression model, based on previous findings indicating these variables to be independent determinants of REE.18 In the present study, FM and FFM were retained in the model (probability of F to enter, P<0.05) and the following predictive equation was constructed:
This equation was then used to predict REE at week 6 and post intervention, using the measured values of FM and FFM at these time points. To disclose any adaptations in REE not accounted for by changes in FM and FFM, the residual between predicted and measured REE (that is, the metabolic adaptation (MA)) was then calculated at week 6 (MA6) and post intervention (MApost).
Classification of positive and negative MA
In order to highlight the impact of the adaptive response in REE on the physiological and behavioural responses to weight loss, the direction of the post-intervention difference between predicted and measured REE was used to classify participants as either experiencing a negative MA, that is, a greater-than-predicted decline in REE, or a positive MA, that is, a change in REE equal to or greater than the predicted decline.
Data are reported as mean±s.d. throughout. Statistical analyses were performed using IBM SPSS for windows (IBM, Chicago, IL, USA; Version 20). The contribution of age, FM and FFM to the observed between-subject variation in REE within REF was examined by stepwise multiple linear regression (probability of F to enter, P<0.05). Changes in body composition and metabolism were examined using one-way repeated measures analysis of variance, with group (that is, positive or negative MA) entered as a between-subject factor. To examine changes in EI on the high- and low-fat probe days, a two-way analysis of variance (time × condition) with repeated measures was used. Where appropriate, Greenhouse–Geisser probability levels were used to adjust for sphericity and Bonferroni adjustments were applied to control for multiple post-hoc comparisons. The average EI (EIave) during the high- and low-fat meal days was also calculated at baseline, week 6 and post intervention. After controlling for baseline differences between predicted and measured REE, partial correlations were used to test the associations between MA6 and MApost, and substrate oxidation, EI, fasting glucose and insulin. Similarly, hierarchical multiple regression was used to test the associations between MA6 and MApost, and fasting leptin (after controlling for change in FM).
Changes in body composition and food intake
Compared with baseline values, body mass (P=0.034) and FM (P=0.004) were significantly lower post intervention, whereas the increase in FFM following EX failed to reach significance (P=0.057). However, examination of the individual responses in body composition revealed marked individual variability (Figure 1), with the change in BM and FM ranging from −7.7 to+3.8 kg and from −8.4 to +2.0 kg, respectively. Similarly, the change in FFM ranged from −1.8 to+3.1 kg. This variability could not be explained by differences in total EX-induced energy expenditure, with simple linear regression indicating that differences in total EX-induced energy expenditure only account for 4% (F(1, 29)=1.165, P=0.290; R2=0.04) and <1% (F(1, 29)=0.082, P=0.776; R2=0.00) of the variance in the change in BM and FM, respectively.
Post-intervention values of EIHF and EILF (or EIave) did not differ from baseline (individual P-values>0.05), but EI was significantly higher during the high-fat meal days than during the low-fat meal days (P<0.001; Table 1).
As can be seen in Table 2, measured REE did not differ significantly from baseline at week 6 (P=0.070) or post intervention (P=0.247). Similarly, post-intervention values of resting RQ (P=0.081), resting fat oxidation (P=0.252) or CHO oxidation (P=0.174), fasting glucose (P=0.451), fasting insulin (P=0.657) or the homeostatic model of assessment index (P=0.108) did not change significantly from baseline. However, there was a significant decline in fasting leptin following EX (P=0.041).
Although predicted and measured REE did not differ at week 6 (P=0.465) or post intervention (P=0.710; Table 2), the proportion of variance accounted for by the predictive equation decreased from 70% at baseline (r=0.84; R2=0.70; P<0.001) to 30% post intervention (r=0.55; R2=0.30; P=0.002; Figure 2). Indeed, examination of the individual responses in MApost revealed marked between-subject variability, with 43% (n=13) of participants experiencing a greater-than-expected decline in REE following EX (mean decline=−102.9±77.5 kcal per day). Furthermore, those who experienced a negative MA, that is, a greater-than-predicted decline in REE (n=13) exhibited attenuated losses in body mass (42% difference: −1.1±2.5 vs −1.9±2.9 kg) and FM (27% difference: −1.9±2.1 vs −2.6±2.7 kg) following EX as compared with those experiencing a positive MA, that is, a change in REE equal to or greater than predicted (n=17; mean increase in REE=129.5±113.5 kcal per day).
The MA, resting substrate oxidation and leptin
After controlling for the change in FM, hierarchical multiple regression indicated that the change in fasting leptin following EX was positively correlated with MA6 (r=0.81; R2=0.44; P<0.001) and MApost (r=0.46; R2=0.21; P=0.048), such that a greater decline in leptin was associated with a greater compensatory downregulation in REE (n=20). Furthermore, those who experienced a negative MA exhibited larger reductions in leptin following EX (mean reduction=−20.3%) than those who experienced a positive MA (mean reduction=−3.5%). MApost was positively associated with the change in resting fat oxidation following EX (r=0.53; P=0.005), with a compensatory downregulation in REE associated with an attenuated increase in resting fat oxidation. Changes in resting fat (r=0.59; P=0.012) and CHO oxidation (r=−0.61; P=0.009) following EX were also associated with the change in fasting leptin (independent of changes in FM and FFM). Furthermore, the associations between the MA (that is, MA6 and MApost), fasting leptin and resting fat oxidation remained after controlling for baseline differences in predicted REE (using hierarchical multiple regression).
The MA and food intake
MApost was negatively associated with the change in EIHF (r=−0.54; R2=0.24; P=0.003) and EIave following EX (r=−0.45; R2=0.20; P=0.015; Figure 3), such that a compensatory downregulation in REE was associated with increased food intake following EX. Again, these associations between MApost and food intake remained after controlling for baseline differences in predicted REE. Furthermore, changes in EIHF (+79.7±338.3 vs −342.7±256.3 kcal per day; P=0.001) and EIave (−34.0±296.2 vs −257.9±255.7 kcal per day; P=0.038) following EX differed significantly between those who experienced a negative and positive MA, respectively.
This study aimed to examine the extent of adaptive thermogenesis during EX-induced weight loss, and whether this adaptive metabolic response influenced both EI and EE. Here we have demonstrated that despite the overall preservation of FFM and REE, marked individual variability existed in the MA to EX-induced weight loss. Indeed, 43% of individuals experienced a greater-than-predicted decline in REE following the EX intervention, which could not be explained by changes in FM and FFM. Importantly, those individuals who experienced a compensatory downregulation of REE also experienced a concomitant upregulation in food intake following the EX intervention.
Although adaptive thermogenesis has been disclosed following dietary-induced weight loss, whether a similar compensatory response in REE exists following EX-induced weight loss has not previously been examined. Importantly, we show here that marked individual variability existed in the adaptive metabolic response in REE following EX. Although the mean values of predicted and measured REE did not differ post intervention, 43% of individuals experienced a decline in REE that was greater than would be expected based on the changes in body composition (mean decline: −102.9±77.5 kcal per day). This adaptive metabolic response occurred despite a mean weight loss of only −1.3±2.7 kg following the intervention. However, consistent with previous findings,19, 20, 21 the group changes in body composition masked marked individual variability (Figure 1). Therefore, these data indicate that in some individuals, EX-induced weight loss is characterised by a compensatory downregulation in REE that moderates the capacity of chronic EX to reduce body weight. Indeed, large differences existed in the loss of body mass (42%) and FM (27%) between those who experienced a negative and positive MA.
In agreement with studies examining dietary-induced weight loss,11, 22, 23 the compensatory downregulation in REE observed in the present study was associated with the change in fasting leptin following EX (independent of changes in FM). Baseline fasting leptin concentrations decreased by 13% during EX and this decline was related to the change in FM. However, the change in leptin was also related to MA6 and MApost, such that a greater decline in leptin following EX was associated with a greater compensatory downregulation in REE (independent of FM). Leptin has been causally implicated in dietary-induced adaptive thermogenesis, as decreased levels of circulating leptin have been shown to decrease sympathetic nervous system activity and EE.24 Indeed, it has been suggested that in those who experience an adaptive suppression of REE, weight loss and the weight-reduced state is interpreted by the brain as one of relative leptin deficiency, despite an actual surplus of stored energy, that is, FM.25
Another important feature of the adaptive metabolic response to EX was that individuals who experienced a greater-than-expected decline in REE also demonstrate a reduced ability to upregulate resting fat oxidation in response to the EX intervention. Taken together, the changes in energy expenditure and substrate oxidation would favour the defence of body weight rather than promote weight loss. Indeed, the change in resting respiratory exchange ratio has been shown to be an independent predictor of the change in FM following chronic aerobic EX,20 whereas a greater reliance on CHO oxidation at rest has been shown to predict future weight gain.26, 27, 28 As the changes in resting substrate oxidation were strongly associated with the change in leptin in the present study, the relationship between MApost and the changes in resting substrate oxidation may again relate to a leptin-induced blunting of sympathetic nervous system activity, as the sympathetic nervous system is known to regulate both substrate oxidation and energy expenditure.29
A strength of the present study was the objective measurement of food intake alongside body composition and metabolism. Importantly, this approach disclosed novel relationships between the adaptive metabolic response to EX and food intake. Indeed, a major finding was that a compensatory downregulation in REE was also associated with upregulation in food intake during EX. Indeed, significant differences existed in the change in EI between those who experienced negative or positive MAs. Although MApost was not associated with the change in EILF, this probably reflects the varying energy density of the two conditions, that is, a smaller change in the amount consumed would have had a larger effect on daily EI under the high-fat rather than the low-fat condition. It should also be noted that food intake was measured during this study using a laboratory-based test meal protocol. Although this approach allowed for the sensitive measurement of volitional intake (free from contamination from external factors), it is acknowledged that laboratory-based feeding protocols do not necessarily reflect food intake in the (more turbulent) free-living environment.
Importantly, a downregulation in REE and upregulation in EI in susceptible individuals would act synergistically to attenuate any EX-induced energy deficit. However, although these data are suggestive of a coordinated adaptive metabolic and behavioural response in some individuals, further studies are required to determine the mechanisms underlying this relationship. However, leptin may again be central to this, as exogenous leptin administration has not only been shown to reverse the adaptive suppression of REE in weight-reduced individuals30 but also the decline in satiation associated with weight maintenance.31
In the present study, MApost was characterised by a marked individual variability. Although this variability will in part reflect errors in the measurement and prediction of REE, the fact that MApost was associated with a range of independent metabolic and behavioural variables suggests that this variance was primarily biologically driven (rather than due to methodological caprice). Indeed, a noticeable characteristic of dietary-induced adaptive thermogenesis is the large individual variability observed.4 It should also be noted that body composition was measured using a two-compartmental model in the present study and, as such, it was not possible to examine how changes in the composition of FFM, or in the distribution of different fat depots, influenced the MA.
In summary, these data indicate that marked variability exists in the MA to chronic aerobic EX (that is, MApost), with some individuals experiencing a greater-than-expected decline in REE following EX-induced weight loss. Importantly, those individuals who experienced a compensatory downregulation in REE also experienced a concomitant upregulation in food intake. This coordinated adaptive response in susceptible individuals would act synergistically to attenuate perturbations to energy balance, favouring the defence of body weight rather than promoting weight loss. As such, these findings may help explain why some individuals lose less weight than expected following chronic aerobic EX. Furthermore, although the underlying mechanisms still need to be determined, the change in leptin may have a role in the compensatory downregulation of REE and promotion of food intake.
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This research was supported by BBSRC grant numbers BBS/B/05079 and BB/G005524/1 (DRINC), EU FP7 Full4Health (266408) and the Stockholm county council (ALF).
The authors declare no conflict of interest.
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Cite this article
Hopkins, M., Gibbons, C., Caudwell, P. et al. The adaptive metabolic response to exercise-induced weight loss influences both energy expenditure and energy intake. Eur J Clin Nutr 68, 581–586 (2014). https://doi.org/10.1038/ejcn.2013.277
- exercise-induced weight loss
- energy intake
- resting energy expenditure
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