Obesity and physical activity - Nature

International Journal of Obesity (1999) 23, Suppl 1, 59±64 ß 1999 Stockton Press All rights reserved 0307±0565/99 $12.00 http://www.stockton-press.co.uk/ijo

Obesity and physical activity KR Westerterp*1 1

Department of Human Biology, Maastricht University, The Netherlands

OBJECTIVES: Three aspects of obesity and physical activity are reviewed: whether the obese are inactive; how the activity level can be increased; and which are the effects of an increase in physical activity in combination with a reduction of energy intake. METHOD: The focus is on an objective approach that is, activity associated energy expenditure as measured with doubly labelled water. RESULTS: Activity associated energy expenditure increases with body mass index while the average physical activity level does not change. The majority of obese subjects is moderately active. An increase in the activity level of obese subjects is limited by the ability to perform exercise of higher intensity. Training programs obese subjects can cope with are until now not rewarded by weight loss. A possible loss in fat mass is compensated by a gain in fat-free mass. CONCLUSIONS: Obese subjects can only reach a signi®cant weight loss with an energy restricted diet. Mild energy restriction will already result in very signi®cant weight loss when one complies with the diet. An increase in physical activity is necessary to compensate for the reduction in activity induced energy expenditure and should be facilitated by the lower body mass. Keywords: energy expenditure; energy intake; doubly-labelled water; fat mass; fat-free mass

Introduction

Are the obese inactive?

Obesity is often associated with a low level of physical activity. Many people think that one of the causes of obesity is that people sit most of the day. The ®rst question we will try to answer is whether there is evidence for a difference in the level of physical activity between obese and non-obese subjects. Obesity can be treated by inducing a negative energy balance, either by increasing physical activity or be reducing energy intake. The second and third question therefore is, respectively, how can the activity level be increased in obese subjects and what is the effect of an increase in physical activity in combination with a reduction of energy intake. Discussing obesity and physical activity needs a de®nition of both items. Obesity can be quanti®ed as weight corrected for height, the body mass index (BMI, kg=m2), or fat mass corrected for height, the fat mass index, or fat mass as a fraction of body mass. Physical activity is not easily quanti®ed. Measures range from self report to activity-associated energy expenditure. One obviously wants an objective approach and therefore can not rely on self report. Here, the focus is on activityassociated energy expenditure as measured with doubly-labelled water.

The doubly-labelled water method allows accurate measurement of average daily metabolic rate (ADMR) under unrestricted conditions over 1 ± 3 week intervals to assess the relation between physical activity and obesity. In Maastricht, we have applied the method, since 1983, in humans.1 Table 1 shows characteristics of 226 subjects measured since then in our laboratory, excluding the following characteristics: age < 20 y and > 50 y, an intervention in energy intake, an intervention in physical activity including athletic performance, pregnancy, lactation and disease. Basal metabolic rate (BMR) was measured with a ventilated hood or in a respiration chamber. Body composition was measured with isotope dilution. Figure 1 shows ADMR as a function of BMI. The lower limit of ADMR clearly increases with BMI from < 5 MJ=d in somebody with the lowest BMI of 12.5 kg=m2 to > 15 MJ=d in the morbid obese, a threefold difference. It is obvious from this ®gure that the lower limit of energy expenditure, that is, energy expenditure at a minimal physical activity, increases with body size. The upper limit is set by body size and physical capacity. Here, we see a steep increase in the lower range of BMI from 5 MJ=d in somebody with the lowest BMI of 12.5 kg=m2 to a value of about 20 MJ=d in somebody with a BMI of 22.5 kg=m2. Higher values can be reached in a selection of the population, such as endurance athletes.2 The energy expenditure associated with physical activity was calculated as ADMR minus diet-induced energy expenditure, assumed to be 10% of ADMR, and minus BMR. Figure 2 shows activity-associated

*Correspondence: Dr KR Westerterp, Department of Human Biology, Maastricht University, PO Box 616, 6200 MD Maastricht, The Netherlands. Email [email protected]

Obesity and physical activity KR Westerterp

60 Table 1 Characteristics of the subjects

Age (y) Height (m) Body mass (kg) Body mass index (kg=m2) Fat mass (kg) Fat-free mass (kg) BMR (MJ=d) ADMR (MJ=d) ADMR=BMR

Women (n 101) mean s.d. range

Men (n 125) mean s.d. range

32 1.67 73 26.4

8 20 ± 49 0.06 1.54 ± 1.81 24 38 ± 164 8.1 12.5 ± 55.3

34 1.80 82 25.4

7 20 ± 48 0.06 1.64 ± 1.97 20 58 ± 216 5.6 19.4 ± 61.7

26 47 6.3 10.9 1.75

17 1 ± 85 8 33 ± 79 1.2 3.6 ± 10.8 2.2 4.7 ± 18.4 0.22 1.07 ± 2.57

20 62 7.7 13.6 1.79

14 3 ± 129 8 48 ± 93. 1.3 5.4 ± 12.7 2.3 9.7 ± 21.5 0.23 1.23 ± 2.57

*BMR, basal metabolic rate; ADMR, average daily metabolic rate.

Figure 2 Activity associated energy expenditure (AEE) as a function of body mass index (BMI) in 226 subjects (Table 1) with the calculated linear regression line (AEE (MJ=d) 0.38 BMI (kg=m2) r 0.17, P < 0.01).

Figure 1 Average daily metabolic rate as a function of body mass index in 226 subjects (Table 1). The dotted lines denote the lower and upper limits.

energy expenditure as a function of BMI. As expected, there is a wide scatter, the activity-induced energy expenditure being the most variable component of ADMR. It ranges from 1 ± 10 MJ=d and there is a slight but signi®cant increase with BMI (P < 0.01), overweight subjects spending on average more energy for physical activity. The physical activity level (PAL) of a subject can be calculated by expressing ADMR as a multiple of BMR (PAL ADMR=BMR) or by adjustment of ADMR for BMR as suggested by Carpenter et al.8 Figure 3 shows the physical activity level expressed in both ways and plotted as a function of BMI. Whichever of the two methods is used, the physical activity level is independent of BMI, a result that has been con®rmed with a tri-axial accelerometer for movement registration in a sub-group of the subjects in current analysis.3 An explanation for the fact that energy expenditure associated with physical activity

increases with BMI while the PAL for the same population does not is that the latter is corrected for differences in body size by expressing ADMR as a multiple of BMR. Someone with a larger body mass needs more energy for an activity than someone with a lower body mass, especially when the activity involves movement of the body mass. It is impossible to recommend a generalisable coef®cient for adjusting energy expenditure associated with physical activity for body size.4 Dividing by body mass power 1 de®nitely overcorrects for body size as the majority of the activities for the average subject involve only limb movements. Prentice et al 4 calculated an exponent of 0.51 for a 24 h activity pattern in a respiration chamber including ADL activities, stepping and cycling. Dividing by BMR, as done in the PAL calculation, probably is a justi®ed intermediate. BMR in the population of the current analysis was a function of body mass power 0.63 (BMR 0.443 body mass0.63, r 2 0.69). There are at least four meta-analyses of the relation between body mass or body fatness and physical activity as derived from doubly-labelled water.4 ± 7 Westerterp et al 5 analysed 96 existing data sets with observations on body composition and PAL of healthy subjects age 19 ± 48 y. Fat-free mass and fat mass were related to PAL. In a regression analysis fat mass explained 53 and 40% of the variation in fatfree mass in females and males, respectively. Adding PAL to the model raised the explained variation in fatfree mass in females to 62%. In contrast with females, there was an independent relationship between PAL and fat mass in males, such that a higher PAL was


physical activity and it was suggested that a low physical activity is a permissive factor for obesity. Prentice et al 4 analysed 319 data sets of healthy subjects age 18 ± 64 y. Results were analysed according to four categories: < 25.0, 25.0 ± 29.9, 30.0 ± 35.0 and > 35.0 kg=m2. PAL remained constant across the three lowest BMI groups indicating similar levels of physical activity. There was a non-signi®cant decrease in PAL in the most obese men and women. Westerterp and Goran7 analysed data sets of 290 healthy subjects age 18 ± 49 y. Physical activity was quanti®ed by adjustment of ADMR for BMR as suggested by Carpenter et al. 8 The result was a gender difference of the relation between physical activity and body fatness. In males, there was a signi®cant inverse crosssectional relationship between activity-energy expenditure and body fatness, whereas no such relationship was apparent in females. Summarizing, activity associated energy expenditure increases with BMI while the average PAL does not change. In contrast, on average, women with a higher PAL have a higher fat-free mass while men with a higher PAL have a lower fat mass.

How can the activity level be increased?

Figure 3 Physical activity level as a function of body mass index in 226 subjects (Table 1), (A) physical activity level calculated as average daily metabolic rate (ADMR) divided by basal metabolic rate (BMR); (B) physical activity level calculated as the residual of the ADMR ± BMR relation.

related to a lower fat mass. It was concluded that there is a relation between PAL and fat-free mass under normal living conditions though fat mass obscures the relation, especially in males. When subjects lose fat mass they also lose fat-free mass, an effect that partly explains why an increase in PAL does not prevent the loss of fat-free mass when the loss of fat mass is high as in persons on weight-reducing diets (see below, last section) Schulz and Schoeller6 analysed 259 existing data sets with observations on body fatness and physical activity. The relationship between physical activity, here expressed as non-basal energy expenditure divided by body mass (ADMR 7 BMR)=kg, and body fatness (fat mass divided by body mass) was highly signi®cant. Fatness increased with decreasing

It is very dif®cult to increase the activity level in the obese. First of all, increasing the level of habitual activity requires a change of life style. Secondly, increasing the activity level in the obese does not imply a change from a sedentary life style. Many obese subjects are already moderately active (see section on `Are the obese inactive'). Thirdly, obese subjects are limited in the ability to perform exercise of higher intensity. Finally, exercise is not rewarded by weight loss. Here, controlled exercise programs are described without restriction of energy intake. Five available studies were reviewed recently2 with respect to the effect of exercise training on spontaneous physical activity and on ADMR. Two studies used jogging as a means of increasing physical activity, the other three included indoor exercises, stationary cycling on a cycle ergometer and weight-training, in a limited number of sessions per week. Jogging certainly is not the exercise mode of choice for obese subjects. We studied the effect of an increase in physical activity on energy balance and body composition in subjects not participating in any sport before the start of the experiment and prepared to run a half-marathon competition after 44 weeks.9 Of 370 respondents to an advertisement in the local media, 16 women and 16 men, aged 28 ± 41 y and with a BMI of 19.4 ± 26.4 kg=m2, were selected. During the study nine subjects withdrew on being unable to keep up with the training program. They all dropped out within 20 weeks of the start of the training. Reasons

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mass. The male participants of the jogging training with the higher percentage body fat were the only subjects losing more fat than gaining fat-free mass. Summarizing, the majority of obese subjects is moderately active. An increase in the activity level of obese subjects is limited by the ability to perform exercise of higher intensity. Training programs with which obese subjects can cope have until now not been rewarded by weight loss. A possible loss in fat mass is compensated by a gain in fat-free mass.

Effects of an increase in physical activity in combination with a reduction of energy intake

Figure 4 Body mass index of subjects who completed and who withdrew from a training to run a half-marathon.

for giving up were `not enough time to join the training' (n 3), injuries (n 5) and not able to keep up with the training (n 1). Figure 4 gives the BMI values of the subjects who completed (BMI 19.4 ± 25.7) and who withdrew (BMI 23.4 ± 26.4). All dropouts had a BMI above the group mean of 22.9 kg=m2. Although manifestly obese subjects were excluded by the selection criteria, most subjects with a BMI > 24 kg=m2 could not cope with the training. Weight-training is an exercise mode that is suitable for a wide variety of target groups including the obese. Van Etten et al 10 did training studies in men with a BMI up to 30 kg=m2 without dropouts. Blaak et al 11 successfully trained obese boys with more than 30% body fat, with daily one-hour cycling bouts at 50 ± 60% of VO2max. Obviously, the increase in PAL is a function of the training mode and training volume. The jogging training, four sessions of 20 ± 60 min=week, resulted in an increase in PAL in the successful subjects of 1.68 0.18 to 2.13 0.19 (P < 0.0001). The weight training, two sessions of 60 min=week, resulted in a PAL increase from 1.76 0.14 to 1.92 0.18 (P < 0.01), and the cycling training, ®ve sessions of 60 min=week, resulted in a PAL increase from 1.77 0.15 to 2.04 0.15 (P < 0.01). Changes in body mass were not large in any of the three studies. The jogging training did not result in a signi®cant body mass change in women and resulted in a 1.3 kg body mass loss in men (P < 0.01) at 40 weeks. The weight training resulted in an unaltered body mass after 18 weeks, and the cycling training had no effect on body mass either. There were consistent changes in body composition, however; losses in fat mass were compensated by early equivalent gains in fat-free

As shown above, exercise training can reduce body mass and fat mass but the resultant changes are small. The same seems to hold for the combination of exercise training with energy restriction. During diet-induced weight loss, added exercise results in little further weight loss. The idea of a combination of exercise training with energy restriction is that the exercise will accelerate fat loss and maintain fat-free mass and thus prevent a decline in resting metabolic rate. Indeed, aerobic exercise provides some conservation of fat-free mass during weight loss as shown in a meta-analysis of 21 studies by Garrow and Summerbell.12 It was hypothesized that a subject with 10 kg excess weight has 2.5 kg excess fat-free mass. Men losing 10 kg by dieting alone and by dieting plus exercise lost, respectively, 2.9 and 1.7 kg, and women, respectively, 2.2 and 1.7 kg. Part of the conservation of fat-free mass was suggested to occur through maintaining glycogen and water, implicating no preventative effect on the diet-induced decline in resting metabolic rate. Ballor and Poehlman13 analysed 33 studies on the extent to which exercise training and=or diet-induced weight loss affect resting metabolic rate. Weight loss programs of the included studies averaged 12 weeks and the overall weight loss was about 12 kg. The weight loss resulted in a consistent decrease in resting metabolic rate of 0.85 MJ=d with no exercise training effects. The change in resting metabolic rate was proportional to the magnitude of the weight reduction (r 0.66, P < 0.01). Weight loss systematically results in a reduction of resting metabolic rate, even when the weight loss results from a reduction in fat mass while fat-free mass remains the same or is increased, as shown by a study of the effect of chronic exercise.9 Body mass decreased during the 40-week training program with an average of (mean s.d.) 1.0 1.7 kg (P < 0.01) while fat-free mass increased by 2.7 1.5 kg (P < 0.001) and fat mass decreased by 3.7 2.1 kg (P < 0.01). Sleeping metabolic rate decreased from (mean s.d.) 6.46 0.62 to 6.32 0.61 MJ=d


(P < 0.01). The decrease of body mass explained 38% of the variance in the decrease in sleeping metabolic rate. Thus, an exercise induced increase in fat-free mass did not result in an increase in resting metabolic rate. There was an indication of the opposite effect, a decreasing resting metabolic rate as a defence mechanism in the maintenance of body mass. The addition of exercise to an energy restricted diet results in little further weight loss. Exercise does not reverse the weight loss-induced depression of resting metabolic rate and weight loss is not different for groups undergoing dietary restriction and dietary restriction plus exercise. The latter implicates that the direct cost of the exercise training is compensated by a reduction of activity associated energy expenditure outside the training sessions. Two studies compared activity-associated energy expenditure before and after dietary restriction and dietary restriction plus exercise, as measured with doubly labelled water. Racette et al 15 designed diets to promote a weight loss of 1 kg=week for 12 weeks by prescribing a diet with 75% of measured resting metabolic rate in the diet-only group and added the calculated energy costs of the exercise for the diet plus exercise group to create a comparable energy de®cit. They observed a maintenance of ADMR in the exercise group ( 0.1 1.2 MJ=d, n.s.) while ADMR decreased in the diet-only group ( 7 1.4 1.0 MJ=d, P < 0.01). Kempen et al 16 provided all subjects with an identical low-energy formula diet providing 2 MJ=d for 4 weeks, followed by 4 weeks 1.4 MJ=d of the formula diet supplemented with a free choice of food to 3.5 MJ=d. They observed a comparable decrease of ADMR of 7 0.9 1.0 MJ=d (P < 0.05) and 7 1.4 1.3 MJ=d (P < 0.01) in the diet plus exercise and the diet-only group, respectively. ADMR dropped signi®cantly, and to a similar extent, at both treatments suggesting no net effect of the exercise training on the activity associated energy expenditure. Explanations for the relatively minor or non-existent effect of the addition of exercise to an energyrestricted diet are a low compliance to the exercise prescription and=or a negative effect of exercise training on dietary compliance. Racette et al 15 calculated that there was an increase of 0.3 MJ=d of activity-associated energy expenditure over and above the 0.4 MJ=d of the supervised exercise sessions, that is an increase instead of a decrease in physical activity outside the exercise periods. However, before the intervention, subjects in the diet plus exercise group had a lower activity induced energy expenditure than the diet-only group and both groups reached the same value, that is activity level, during the intervention. Kempen et al 16 observed no difference in activity-induced energy expenditure between the two groups, starting from the same activity level before the intervention (Figure 5). With respect to dietary compliance both studies observed that exercise enhances compliance. Calculated intake, doubly labelled water measured energy expenditure minus

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Figure 5 Average daily metabolic rate as a function of sleeping metabolic rate in obese subjects before weight loss (regression line) and after eight weeks weight loss by an energy restricted diet only (open symbols) of by the energy restricted diet plus exercise (closed symbols).

mobilized energy from body stores, was 1.1 and 1.5 times the prescribed intake of about 5 MJ=d in the diet plus exercise and diet only group, respectively, in the study of Racette et al.15 Kempen et al 16 observed values of 2.0 and 2.5 times the prescribed intake of 2.75 MJ=d in the diet plus exercise and diet only group, respectively. Amongst the suggested explanations for the improved compliance in the exercise group are an increased contact with the subjects during the supervised exercise sessions.17 The overall conclusion is that the size of the exercise intervention only has a minor or no effect on the activity level of the subjects and consequently does not result in additional weight loss. Finally there are some studies showing the effect of energy restriction on physical activity. Velthuis-te Wierik et al 18 observed the effect of a moderately energy-restricted diet on energy metabolism in non-obese men (BMI, 24.9 1.9 kg=m2). For 10 weeks subjects received a diet with 67% of their measured ADMR during weight maintenance. The consequent weight loss was 7.4 1.7 kg and the activity level (ADMR=BMR) went down from 1.85 0.37 to 1.65 0.29 (P 0.06), that is there was a tendency for a reduction of physical activity by reducing energy intake. Bouten et al 19 measured physical activity in subjects voluntarily reducing energy intake resulting in underweight, that is subjects with anorexia nervosa. Subjects with a BMI 5 17 kg=m2 were equally or more active compared with control subjects, while subjects with a BMI < 17 kg=m2 were equally or less active compared


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with control subjects. Thus, undereating may cause a decrease in daily physical activity. Exercise training in obese subjects does not seem to promote weight loss. What are the bene®cial effects of exercise for obese subjects, being on average moderately active and having a limited ability to perform exercise? The answer probably is that a high level of energy turnover, that is a high level of physical activity, promotes weight maintenance. Regulation of energy balance is likely to be better at a higher energy turnover. Obviously one can eat more when one is physically active, without getting into a positive energy balance. There are speculations that exercise reduces perceived hunger in obese subjects and there is evidence that exercise increases fat oxidation at a high-fat diet. Obese subjects can only reach a signi®cant weight loss with an energy restricted diet. Mild energy restriction will already result in very signi®cant weight loss when one complies with the diet. An increase in physical activity is necessary to compensate for the reduction in activity induced energy expenditure and should be facilitated by the lower body mass. References

1 Westerterp KR, De Boer JO, Saris WHM, Schoffelen PFM, Ten Hoor F. Measurement of energy expenditure using doubly labelled water. Int J Sports Med 1984; 5: 74 ± 75. 2 Westerterp KR. Alterations in energy balance with exercise. Am J Clin Nutr 1998; 6 (Suppl): S970 ± S974 3 Westerterp KR, Bouten CVC. Physical activity assessment: comparison between movement registration and doubly labelled water method. Z ErnaÈhrungswiss 1997; 36: 263 ± 267. 4 Prentice AM, Black AE, Coward WA, Cole TJ. Energy expenditure in overweight and obese adults in af¯uent societies: an analysis of 319 doubly-labelled water measurements. Int J Obes 1996; 50: 93 ± 97. 5 Westerterp KR, Meijer GAL, Kester ADM, Wouters L, Ten Hoor F. Fat-free mass as a function of fat mass and habitual activity level. Int J Sports Med 1992; 13: 163 ± 166. 6 Schulz LO, Schoeller DA. A compilation of total daily energy expenditures and body weights in healthy adults. Am J Clin Nutr 1994; 60: 676 ± 681.

7 Westerterp KR, Goran M. Relationship between physical activity related energy expenditure and body composition: a gender difference. Int J Obes 1997; 21: 184 ± 188. 8 Carpenter WH, Poehlman ET, O'Connell M, Goran MI. In¯uence of body composition and resting metabolic rate on variation in total energy expenditure: a meta-analysis. Am J Clin Nutr 1995; 61: 4 ± 10. 9 Westerterp KR, Meijer GAL, Janssen EME, Saris WHM, Ten Hoor F. Long term effect of physical activity on energy balance and body composition. Br J Nutr 1992; 68: 21 ± 30. 10 Van Etten LMLA, Westerterp KR, Verstappen FJT, Boon BJB, Saris WHM. Effect of an 18-wk weight-training program on energy expenditure and physical activity. J Appl Physiol 1997; 82: 298 ± 304. 11 Blaak EE, Westerterp KR, Bar-Or O, Wouters LJM, Saris WHM. Effect of training on total energy expenditure and spontaneous activity in obese boys. Am J Clin Nutr 1992; 55: 777 ± 782. 12 Garrow JS, Summerbell CD. Meta-analysis: effect of exercise, with or without dieting, on body composition of overweight subjects. Eur J Clin Nutr 1995; 49: 1 ± 10. 13 Ballor DL, Poehlman ET. A meta-analysis of the effects of exercise and=or dietary restriction on resting metabolic rate. Eur J Appl Physiol 1995; 71: 535 ± 542. 14 Westerterp KR, Meijer GAL, Schoffelen P, Janssen EME. Body mass, body composition and sleeping metabolic rate before, during and after endurance training. Eur J Appl Physiol 1994; 69: 203 ± 208. 15 Racette SB, Schoeller DA, Kushner RF, Neil KM, HelingIaffaldano K. Effects of aerobic exercise and dietary carbohydrate on energy expenditure and body composition during weight reduction in obese women. Am J Clin Nutr 1995; 61: 486 ± 494. 16 Kempen KPG, Saris WHM, Westerterp KR. Energy balance during 8 weeks energy-restrictive diet with and without exercise in obese females. Am J Clin Nutr 1995; 62: 722 ± 729. 17 Racette SB, Schoeller DA, Kushner RF, Neil KM. Exercise enhances dietary compliance during moderate energy restriction in obese women. Am J Clin Nutr 1995; 62: 345 ± 349. 18 Velthuis-te Wierik EJM, Westerterp KR, Van den Berg H. Impact of a moderately energy-restricted diet on energy metabolism and body composition in non-obese men. Int J Obes 1995; 19: 318 ± 324. 19 Bouten CVC, Van Marken Lichtenbelt WD, Westerterp KR. In¯uence of body mass index on daily physical activity in anorexia nervosa. Med Sci Sports Exerc 1996; 28: 967 ± 973.