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Changes in energy metabolism in response to 48 h of overfeeding and fasting in Caucasians and Pima Indians

Abstract

OBJECTIVE: Differences in the metabolic response to overfeeding and starvation may confer susceptibility or resistance to obesity in humans. To further examine this hypothesis, we assessed the changes in 24 h energy metabolism in response to short-term overfeeding and fasting in Caucasians (C) and Pima Indians (I), a population with a very high propensity for obesity.

METHODS: We measured the changes in 24 h energy expenditure (24 -EE) and 24 h respiratory quotient (24-RQ) in response to 48 h of mixed diet overfeeding (100% above energy requirements) and fasting in a whole body respiratory chamber in 14 male subjects (7 C/7 I, age 30±6 y, mean±s.d.). Results were compared to a 24 h measurement under eucaloric conditions.

RESULTS: Mean 24-EE increased in response to overfeeding and decreased in response to fasting (all changes P<0.01), with no differences between C (+9.1% and −9.1%) and I (+8.6% and −9.6%). Similarly, mean 24-RQ increased/decreased in response to overfeeding/fasting, respectively (all changes P<0.01), again with no differences between C (+0.06 and −0.05) and I (+0.05 and −0.05). The changes in 24-EE in response to overfeeding and fasting were positively correlated (r=0.70, P<0.01), whereas those in 24-RQ were not (r=0.40, NS).

CONCLUSIONS: Pima Indians do not appear to have an impaired metabolic response to short-term overfeeding and fasting that could explain their propensity for obesity. Individuals with a large increase in energy expenditure in response to overfeeding appear to have a small decrease in energy expenditure in response to starvation (spendthrift phenotype) and vice versa (thrifty phenotype).

Introduction

The Pima Indians of Arizona have one of the highest reported prevalence rates of obesity in the world.1,2 The etiologic mechanisms predisposing this population to obesity are largely unknown. Although low rates of energy expenditure3 and fat oxidation4 are predictive of future weight gain in Pima Indians, comparative studies with Caucasians revealed no abnormalities in either measure when assessed under eucaloric conditions.5

Studies in rodents suggest that susceptibility to obesity may be determined not only by variations in energy metabolism under eucaloric conditions, but also by differences in the metabolic response to alterations in energy intake.6,7,8,9,10,11 In the late 1970s and early 1980s, Rothwell and Stock6,7 in their pioneering overfeeding experiments in rodents demonstrated that when lean rats were voluntarily overeating on a cafeteria diet, they were able to largely resist weight gain by responding to the increased energy intake with an almost equivalent increase in energy expenditure (diet-induced thermogenesis, DIT). At the same time, other studies revealed that the capacity to increase DIT was defective in various animal models of obesity and that these animals gained substantially more weight than their lean counterparts when overfed by the same amount of calories.8,9,10,11 These intriguing findings in rodents led to the hypothesis that inter-individual differences in the metabolic response to altered energy intake, ie, in energy efficiency, might explain, in part, why some humans appear to gain weight more easily than others.12

Numerous over- and underfeeding studies have been undertaken to examine the metabolic responses to altered energy intake in humans.13,14,15,16,17,18,19,20,21,22,23,24,25,26,27 Although these studies confirmed that individuals differ in their metabolic susceptibility to weight gain and weight loss13,14,15,16,21,23,26 and provided evidence that this interindividual variation may in part be genetically determined,21 results were inconclusive as to whether DIT might be relevant to the development of obesity in humans. While some human studies suggested that part of the excess energy intake during overfeeding must have been dissipated by an increase in energy expenditure,13,14,15,16,19,21 others found no evidence for such a compensatory thermogenic mechanism.21,25,27 In this respect, it is important to remember that, in most of these studies, subjects were overfed for several weeks and that the occurrence or not of DIT was inferred from comparing the amount of excess energy consumed with the resulting increase in body weight using standard estimates for the energy cost of weight gain.28 Most,18,19,22,23,24,25 but not all15 human studies with direct measurement of energy metabolism indicate that, in response to short-term over- and underfeeding, energy expenditure increases and decreases, respectively. These studies give only limited information, however, as to whether these metabolic responses differ between lean and obese individuals16,18,19 or between populations with different propensity for obesity. Moreover, since only a few studies included a combined over- and underfeeding regimen,17,23,24 it is not clear how the metabolic responses to over- and underfeeding relate to one another within the same individuals.

In the present study, we measured the changes in 24 h energy metabolism in response to short-term overfeeding and fasting in a respiratory chamber in lean and obese Caucasians and Pima Indians. We hypothesized that, although Pima Indians do not have lower rates of energy expenditure than Caucasians under eucaloric conditions,5 they might have an impaired metabolic response to overfeeding and/or starvation that could explain their propensity for weight gain. A second aim was to examine how the metabolic responses to over- and underfeeding relate to one another within the same individuals.

Subjects and methods

Subjects

Fourteen male subjects, seven Caucasians and seven Pima Indians participated in this study (Table 1). Each ethnic group comprised of three lean and four obese individuals with obesity defined by a body mass index (BMI)>30 kg/m2. Subjects were between 18 and 45 y of age, nondiabetic according to a 75 g oral glucose tolerance test and healthy according to a physical examination and routine laboratory tests. No subject smoked or took medications at the time of the study. The study protocol was approved by the Institutional Review Board of the National Institute of Diabetes and Digestive and Kidney Diseases and by the Tribal Council of the Gila River Indian Community and all subjects provided written informed consent prior to participation.

Table 1 Physical and metabolic characteristics of the study population

All subjects were admitted for approximately 3 weeks to the metabolic ward of the Clinical Diabetes and Nutrition Section of the National Institutes of Health in Phoenix, AZ, where they were fed a weight-maintaining diet (50%, 30% and 20% of daily calories provided as carbohydrate, fat and protein, respectively) and abstained from strenuous exercise. After at least 3 days on the weight-maintaining diet, subjects spent 24 h in a respiratory chamber for the assessment of baseline 24 h energy metabolism and 24 h energy requirement (Figure 1). During this baseline evaluation, subjects were fed an amount of calories estimated to achieve energy balance.29 Subsequently, subjects underwent three further evaluations in the respiratory chamber. These evaluations each lasted for 48 h and were separated by 3 day periods on a weight maintaining diet on the metabolic ward (Figure 1). During each of the three 48 h evaluations in the respiratory chamber, subjects underwent, in randomized order, one of three different dietary interventions. On one occasion, subjects were fed 100% of their energy requirements according to the baseline evaluation in the respiratory chamber (eucaloric feeding). On another occasion, no food was provided except for caffeine-free diet sodas, which were allowed ad libitum (0% of energy requirement, fasting) and on a third occasion, subjects were fed 200% of their energy requirement (overfeeding) (Figure 1). The macronutrient composition of the diet served in the chamber was constant and the same as that of the weight maintaining diet served on the unit.

Figure 1
figure1

Changes (mean±s.d.) in 24 h energy expenditure, sleeping metabolic rate, physical activity energy expenditure, and 24 h respiratory quotient in 14 male subjects (seven Caucasians and seven Pima Indians) in response to 48 h of fasting (F), eucaloric feeding (EF), and 100% mixed-diet overfeeding (OF) in a respiratory chamber (BL=baseline evaluation).

Methods

Body composition was estimated at baseline by hydrodensitometry with simultaneous assessment of residual lung volume by helium dilution30 and calculation of percentage body fat as described before.31 The measurement of energy expenditure and substrate oxidation in the respiratory chamber has previously been described.32 In brief, volunteers entered the chamber at 7:45 am after an overnight fast and remained therein for 24 h or 48 h. Meals were provided at 8:00 am, 11:30 am, 5:00 pm and an evening snack (8:00 pm). The rate of energy expenditure was measured continuously, calculated for each 15 min interval and then averaged for the first and second 24 h interval (24-EE). Spontaneous physical activity (SPA) was detected by radar sensors and expressed as percentage of time over the 24 h period, in which activity was detected.32 Sleeping metabolic rate (SMR) was defined as the average energy expenditure of all 15 min periods between 11:30 pm and 5 am during which SPA was <1.5%. Physical activity energy expenditure (PA-EE) was calculated by multiplying SPA values by the slope of the regression line of energy expenditure vs SPA.32 Carbon dioxide production (VCO2) and oxygen consumption (VO2) were calculated for every 15 min interval and averaged for the first and second 24 h interval. The 24 h respiratory quotient (24-RQ) was calculated as the ratio of 24 h VCO2 and 24 h VO2. From the 24 h energy intake, 24-EE and 24-RQ, the substrate balances were calculated as described.32

Statistical analyses

Statistical analyses were performed using the procedures of the SAS Institute (Cary, NC). The baseline characteristics were compared between Caucasians and Pima Indians and between the lean and obese subgroups using general linear regression models with adjustment for age. The changes in 24-EE, SMR, PA-EE and 24-RQ in response to fasting, eucaloric feeding and overfeeding were calculated as the absolute and relative (%) differences between the mean 24-EE, SMR, PA-EE and 24-RQ during the 48 h of fasting, eucaloric feeding and overfeeding (averaged from the first and second day of each chamber evaluation) and the 24-EE, SMR, PA-EE and 24-RQ at baseline. Paired t-tests were used to assess whether 24-EE, SMR, PA-EE and 24-RQ were significantly different between the first and second day within the 48 h fasting, eucaloric feeding, and overfeeding periods or between the 48 h fasting, eucaloric feeding, and overfeeding periods and the baseline evaluation. General linear regression models were used to test whether changes in 24-EE, SMR, PA-EE or 24-RQ in response to overfeeding and fasting differed between Caucasians and Pima Indians and between the lean and obese subgroups. The relationships between the changes in 24-EE, SMR, PA-EE and 24-RQ in response to fasting and overfeeding were assessed by simple linear regression analysis with calculation of Pearson correlation coefficients.

Results

The anthropometric and metabolic characteristics of the study population are summarized in Table 1. Caucasians were significantly taller than Pima Indians, whereas neither body weight and composition nor any of the variables of 24 h energy metabolism at baseline differed between the two ethnic groups. By design, body weight, BMI and percentage body fat were greater in the obese than in the lean subgroup, as were age-adjusted 24-EE, SMR and PA-EE, but not 24-RQ.

24 h energy expenditure

In response to the 48 h of fasting and overfeeding, mean 24-EE decreased (by−9.4±5.1%,−315±211 kcal/day) and increased (by+8.8±5.0%,+266±158 kcal/day), respectively (both P<0.001; Figure 1). During the 48 h of eucaloric feeding, mean 24 -EE was not significantly different from baseline (Figure 1). The decrease/increase in 24-EE was almost completely established during the first 24 h of fasting/overfeeding with no further decrease/increase during the second 24 h (Figure 1). The mean decrease/increase in 24-EE in response to overfeeding/fasting, respectively, was not different between Caucasians and Pima Indians or between the lean and obese subgroups (Figure 2). The changes in 24-EE in response to fasting and overfeeding varied substantially among individuals and were positively related, ie individuals with the smallest decrease in 24-EE in response to fasting tended to have the greatest increase in 24-EE in response to overfeeding and vice versa (Figure 3).

Figure 2
figure2

Changes in 24 h energy expenditure, sleeping metabolic rate, physical activity energy expenditure, and 24 h respiratory quotient in response to 48 h of fasting (open bars) and 100% mixed-diet overfeeding (filled bars) in Caucasians vs Pima Indians and in the lean vs obese subgroups.

Figure 3
figure3

Relationship between the metabolic responses to 48 h fasting and the metabolic responses to 48 h mixed diet overfeeding in 14 male subjects seven Caucasians (open circles) and 7 Pima Indians (filled circles).

Sleeping metabolic rate

In response to the 48 h of fasting and overfeeding, mean SMR decreased (by−4.4±7.6%,−107±150 kcal/day, P=0.05) and increased (by +18.1±5.6%,+351±113 kcal/day, P<0.0001), respectively (Figure 1). During the 48 h of eucaloric feeding, mean SMR was not significantly different from baseline (Figure 1). As with 24-EE, the decrease/increase in SMR was almost completely established during the first 24 h of fasting/overfeeding with no further decrease/increase during the second 24 h (Figure 1). The mean increase in SMR in response to overfeeding was not different between Caucasians and Pima Indians or between the lean and obese subgroups (Figure 2). In response to fasting, mean SMR decreased in Pima Indians and in the obese subgroup, but not in Caucasians or in the lean subgroup (Figure 2). The latter finding, however, was mainly due to two lean Caucasians who showed an increase in SMR in response to fasting whereas all other 12 subjects experienced a decrease (Figure 3). As with 24-EE, the changes in SMR in response to fasting and overfeeding varied substantially among individuals and were positively related, ie individuals with the smallest decrease in SMR in response to fasting tended to have the greatest increase in SMR in response to overfeeding and vice versa (Figure 3).

Physical-activity energy expenditure (PA-EE)

In response to the 48 h of fasting, eucaloric feeding, and overfeeding, there were no significant changes in mean PA-EE, neither in the entire study population (Figure 1), nor in the Caucasian/Pima Indian or lean/obese subgroups (Figure 2). No change was detected in PA-EE from the first and second day of fasting, eucaloric feeding or overfeeding (Figure 1) The changes in PA-EE in response to fasting and overfeeding varied substantially among individuals and were not significantly related with one another (Figure 3).

24-h respiratory quotient

In response to the 48 h of fasting and overfeeding, mean 24-RQ decreased (by −0.052±0.019) and increased (by +0.052±0.022), respectively (both P<0.0001; Figure 1). During the 48 h of eucaloric feeding, mean 24-RQ was not significantly different from baseline (Figure 1). The 24-RQ continued to decrease/increase during the 48 h of fasting/overfeeding, ie the decrease/increase in 24-RQ on the second 24 h of fasting/overfeeding was greater than the decrease/increase on the first 24 h (Figure 1). The mean decrease/increase in 24-RQ was not different between Caucasians and Pima Indians or between the lean and obese subgroups (Figure 2). The changes in 24-RQ in response to fasting and overfeeding varied substantially among individuals and were not significantly related with one another (Figure 3).

Energy and substrate balances and body weight

The negative energy balance induced by fasting (−2850±1233 kcal/day) was accounted for by negative carbohydrate, fat and protein balances (−822±147, −1728±462 and −300±49 kcal/day respectively, all P<0.0001). Conversely, the positive energy balance induced by overfeeding (+2689±1393 kcal/day) was accounted for by positive carbohydrate, fat and protein balances (+850±197, +1034±376 and+805±211 kcal/day, respectively, all P<0.0001). Body weight did not change significantly in response to the 48 h of fasting (−0.2±0.4 kg, NS) or overfeeding (+0.4±0.3 kg, NS).

Discussion

Adaptive increases and decreases in energy expenditure in response to altered energy intake play an important role in body weight homeostasis in rodents,6,7,8,9,10,11 but whether interindividual variation in the metabolic response to altered energy intake also plays a role in the pathophysiology of obesity in humans remains controversial.28 In the present study, we addressed this issue by examining the changes in 24-EE and substrate oxidation in response to short-term overfeeding and fasting in lean and obese Caucasians and Pima Indians, a population with one of the highest reported prevalence rates of obesity in the world.1,2 Although our results confirm that humans have the ability to respond to overfeeding and fasting with an increase and decrease in energy expenditure, respectively, and that these adaptive changes vary considerably among individuals, we found no evidence for an impaired metabolic response in Pima Indians compared to Caucasians or in obese vs lean individuals that could explain their different propensity for weight gain. Our results indicate, however, that the metabolic responses to overfeeding and fasting might be related to one another such that individuals with the greatest increase in energy expenditure upon overfeeding tend to have the smallest decrease in energy expenditure upon fasting (spendthrift phenotype) and vice versa (thrifty phenotype).

The finding that 24-EE increased in response to short-term overfeeding agrees with previous reports13,14,15,16,19,21 and confirms, once more, that the capacity to dissipate excessive energy as heat is fairly limited in humans. In fact, 100% overfeeding for 48 h in the present study led to a 9% increase in 24-EE, ie an average of only 530 of the 6330 excess kcal consumed during the 48 h overfeeding period could be dissipated. This capacity to increase energy expenditure appears to be of similar magnitude as in other large mammals such as pig33 or sheep,34 but substantially smaller than in rodents, which in response to overfeeding are able to dissipating a much larger proportion (75%) of the excess energy.6,7 The increase in energy expenditure in response to excess energy intake in rodents is largely mediated by increased thermogenesis in brown adipose tissue,6,7 which in humans decreases with age and is scarce in adulthood.35 This could also explain why elderly people appear to have an impaired increase in energy expenditure in response to overfeeding.25 Although the well-known methodological limitations in quantifying the thermic effect of food and physical activity-related energy expenditure in a respiratory chamber36 prevented us from delineating the exact contributions of these factors to the overall increase in 24-EE in this small number of subjects, our results indicate that the major effect was attributable to an increase in SMR. In agreement with the study by Dauncey,17 SMR was increased by as much as 19% in the present study, indicating that the effect of overfeeding to increase metabolic rate was sustained for at least 12 h and in fact most prominent in the postabsorptive period. In accordance with findings by Roberts et al,20 overfeeding induced no detectable change in PA-EE. While recognizing the methodological limitations in quantifying PAEE in the chamber, we conclude that in the short-term, increased fidgeting is probably not a major adaptation to a positive energy balance in humans. In response to the 48 h of fasting, 24-EE decreased by approximately the same amount (9%) as the increase induced by overfeeding. On average, it appears that the decrease in SMR in response to fasting was less pronounced than the decrease in 24-EE (Figure 1) and even absent in lean individuals and in Caucasians (Figure 2). Although this finding seems to agree with the study by Dauncey,17 it was largely attributable to two lean Caucasians who showed a paradoxical increase in SMR in response to fasting. By definition, the lack of a thermic effect of food must also have contributed to the overall decrease in 24-EE in response to fasting. The finding that 24-RQ increased in response overfeeding and decreased in response to fasting was highly anticipated and indicates that substrate oxidation shifted towards carbohydrate oxidation in response to a positive energy balance, and towards fat oxidation in response to a negative energy balance. In contrast to the changes in energy expenditure, these shifts in substrate oxidation continued throughout the 48 h periods, presumably because of the changes in body glycogen stores. Jebb et al,24 who followed the metabolic responses to over- and underfeeding continuously for 12 days in a respiratory chamber showed that changes in substrate balances continue over several days.

We had hypothesized that compared to Caucasians, Pima Indians might have a smaller increase in energy expenditure in response to overfeeding and/or a larger decrease in energy expenditure in response to fasting which could have contributed to their propensity to weight gain. The present results indicate that at least in the short-term, this does not appear to be the case. Whether ethnic differences in the metabolic adaptation to long-term weight gain contribute to the high propensity for obesity in Pima Indians remains unknown, although this hypothesis would be supported by our recent observations that sympathetic nervous system activity does not increases with increasing adiposity in Pima Indians,37 as the case in Caucasians, and that Pima Indians show only a marginal metabolic adaptation to long-term weight changes.38 Finally, findings by Roberts et al20 suggest that the major metabolic adaptation to overfeeding in humans might not be an increase in energy expenditure, but rather a subsequent decrease in voluntary energy and fat intake following overfeeding. It is thus possible that an inadequate or absent adaptive decrease in energy intake after periods of overeating contributes to the propensity for weight gain in Pima Indians.

Since Caucasians and Pima Indians had similar metabolic responses to overfeeding and starvation in the present study, we conducted a second subgroup analysis in which we divided the study population into a lean and obese subgroup. Based on results by Glick et al,15 which suggested that overfeeding may lead to increased basal metabolic rate in lean, but not in obese individuals, we hypothesized that obese individuals might have an abnormal metabolic response to altered energy intake that could have contributed to their development of obesity in the first place. As with the ethnic comparison, however, we found no evidence to support this hypothesis since neither the response in energy expenditure nor that in substrate oxidation differed between the lean and obese subgroups. Thus, even severely obese individuals (max. BMI 67 kg/m2 in the present study) seem to have normal metabolic responses to overfeeding and fasting. While this agrees with previous findings by Webb and Annis,18 who also found normal metabolic responses to overfeeding in obese individuals, it is important to remember that cross-sectional comparisons between lean and obese individuals cannot exclude the possibility that abnormal metabolic responses exist in the pre-obese state that then normalize as obesity develops.

The assessment of metabolic responses to both overfeeding and fasting within the same individuals in the present study allowed us to examine how these responses relate to one another. We found that the changes in both 24-EE and SMR to overfeeding and fasting were positively related such that individuals with the greatest increase in energy expenditure upon overfeeding tended to have the smallest decrease in energy expenditure upon fasting and vice versa. Similar results were obtained when the values from the 48 h period of eucaloric feeding instead of those from the initial 24 h baseline period were used for calculating the changes in response to overfeeding and fasting (data not shown). The physiological explanation for these relations remains uncertain, but could involve different responses of the sympathetic nervous system, thyroid hormones, leptin, or uncoupling protein expression.38,39 Regardless of the underlying mechanism, if confirmed, our finding would support the concept that there are some individuals with a ‘thrifty’ phenotype (those with a small increase in energy expenditure upon overfeeding and a large decrease in energy expenditure in response to fasting) and others with a more ‘spendthrift’ phenotype (those with a large increase in energy expenditure upon overfeeding and a small decrease in energy expenditure upon fasting). Whether this is in fact the case and if so, whether the former group of individuals is more predisposed to obesity (‘easy gainers/hard losers’) while the later group is more resistant (‘hard gainers/easy losers’) remains to be established.

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Acknowledgements

The authors wish to thank the subjects for their participation. We also gratefully acknowledge Mrs Carol Massengill and the nurses of the Clinical Research Unit as well as Dr Ennette Larson and the staff of the metabolic kitchen for their care of the patients in the studies and the Clinical Diabetes and Nutrition Section technical staff, particularly Mr Tom Anderson, for assisting in the chamber measurements.

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Correspondence to C Weyer.

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Weyer, C., Vozarova, B., Ravussin, E. et al. Changes in energy metabolism in response to 48 h of overfeeding and fasting in Caucasians and Pima Indians. Int J Obes 25, 593–600 (2001). https://doi.org/10.1038/sj.ijo.0801610

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Keywords

  • energy metabolism
  • diet-induced thermogenesis
  • respiratory chamber
  • metabolic adaptation
  • ethnicity

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