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(EI), total daily EE and body weight in six lean women using a within-subject, repeated measures design. METHOD: Subjects were each studied three times ...
International Journal of Obesity (2002) 26, 866–869 ß 2002 Nature Publishing Group All rights reserved 0307–0565/02 $25.00 www.nature.com/ijo

SHORT COMMUNICATION The effect of graded levels of exercise on energy intake and balance in free-living women{ RJ Stubbs1*, A Sepp1, DA Hughes1, AM Johnstone1, N King3, G Horgan2 and JE Blundell3 1

The Rowett Research Institute, Bucksburn, Aberdeen, UK; 2Biomathematics and Statistics, The Rowett Research Institute, Bucksburn, Aberdeen, UK; and 3BioPsychology Group, Psychology Department, University of Leeds, Leeds, UK AIM: We assessed the effect of graded increases in exercised-induced energy expenditure (EE) on appetite, daily energy intake (EI), total daily EE and body weight in six lean women using a within-subject, repeated measures design. METHOD: Subjects were each studied three times during 7 day treatments, corresponding to no-exercise (control; Nex; 0 MJ=day), medium exercise level (Mex;  1.9 MJ=day) and high exercise level (Hex;  3.4 MJ=day), with 2 day maintenance beforehand. Subjects self-weighed ad libitum food intake. EE was assessed by continual heart rate monitoring. During waking hours subjects recorded hourly sensations of hunger and appetite. RESULTS: EE amounted to 9.2, 11.0 and 12.1 MJ=day (F (2, 10) ¼ 5.67; P ¼ 0.023 (s.e.d. ¼ 0.87)) on the Nex, Mex and Hex treatments, respectively. The corresponding values for EI were 8.9, 9.2 and 10.0 MJ=day (F (2, 10) ¼ 4.80; P ¼ 0.035 (s.e.d. ¼ 0.36)). There were very weak treatment effects on hunger. Weight loss was significantly different from zero on the Mex and Hex treatments. CONCLUSION: Markedly increasing EE through exercise produced significant but partial compensations in EI (  33% of EE due to exercise). Accurate adjustments of El to acute increases in EE are likely to take weeks rather than days. International Journal of Obesity (2002) 26, 866 – 869. doi:10.1038=sj.ijo.0801874 Keywords: exercise; appetite; human; energy balance; feeding behaviour

Introduction, materials and methods Sedentary lifestyles are believed important in predisposing people to obesity and increased physical activity is often recommended as a strategy for controlling energy balance (EB).1 Few studies have quantified the exact relationship between energy intake (EI), expenditure (EE) and EB in ad libitum feeding subjects undergoing various exercise interventions.2 Of those that have, methodologies have varied considerably (see King et al,2 for a review). To understand the relationship between changing EE through physical activity and patterns of food intake with reference to the general population it is important to inter-relate a number of studies,

*Correspondence: RJ Stubbs, The Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen AB21 9SB, UK. E-mail: [email protected] { Part of this work was presented as an abstract at the Nutrition Society Summer Symposium, University of Surrey, Guildford, June 1998. Received 15 May 2000; revised 2 July 2001; accepted 12 July 2001

using similar methodologies. This study has been designed as one of a series, using methodologies which allow crosscomparison between these and previous work.3 – 9 This particular study was designed to continually monitor over 7 days EI, EE (both total and exercise-induced) and motivation to eat in the same women exposed to no (Nex), moderate (Mex) or high levels of exercise (Hex)-induced EE. Six women, mean (s.e.m.) age 23.0 (0.6) y; weight 58.4 (3.3) kg; height 1.65 (0.02) m; body mass index (BMI) 21.4 (1.0) kg=m2; resting metabolic rate (RMR) 5.66 (0.17) MJ=day; extrapolated VO2max 33.41 (2.49) ml=min=kg were recruited by advertisement. During the 2 days prior to the beginning of the study they underwent a medical examination and were trained in the study procedures. Height and RMR were recorded as described previously.10 Subjects’ restraint (DEBQ11) ranged between 1.1 and 3.3 with a mean of 2.3 (s.e.m. ¼ 0.3). The study was approved by the Joint Grampian Health Board and University of Aberdeen Ethical Committee. Subjects were each studied three times in a 9 day protocol, corresponding to: sedentary routine, ie no additional exercise (control; Nex; 0 MJ=day; moderate exercise, ie two

Graded levels of exercise RJ Stubbs et al

40 min exercise sessions per day (Mex; 21.4 kJ=kg=day); high levels of exercise, ie three 40 min exercise sessions per day (Hex; 42.8 kJ=kg=day). The order of treatments was randomised and each was separated by at least one week. On days 1 – 2 of each treatment period, subjects consumed a controlled maintenance diet. Throughout the subsequent 7 days subjects had ad libitum access to their normal daily diet. They weighed all food items and fluids on PETRA (portable electronic tape recording automated) scales12 and recorded their food intake and the time of eating in food diaries. On the Mex and Hex treatments subjects exercised throughout days 3 – 9 inclusive, at the prescribed intensity and duration using a bicycle ergometer (Tunturi E850, Tunturi, Finland) in the exercise suite of the Human Nutrition Unit. During the study EE was assessed by continuously monitoring heart rate (HR, Polar sports tester, Polar Electro, Finland), using the FLEX method.13 Subjects wore the heart rate monitor (HRM) during waking hours over the whole 9 days of each study period. Body weight was recorded each morning before eating and after voiding. Subjects wore the same clothing when being weighed. Energy and nutrient intakes were calculated using the Diet 5 programme (Robert Gordon University, Aberdeen) which is based on current UK food tables.14 Changes in subjective appetite, hunger and satiety and other aspects of mood were assessed hourly, during waking hours throughout days 1 – 9, using visual analogue scales (VAS) on a palm-top computer as previously described.15 Subjects also completed an End of Day Questionnaire, which assessed retrospectively perceptions of mood, alertness, liveliness, hunger, thirst and preoccupation with thoughts of food throughout the day. Energy and nutrient intakes and EE were analysed by analysis of variance with treatment and day as factors and subject and run as blocking factors. A square-root transformation was applied to the VAS for subjective ratings, in order to satisfy assumptions of normality, and then the data were analysed by analysis of variance with subject, run, day and time as blocking factors and exercise, day and time as treatment factors. Similarly, to satisfy assumptions of normality, a logarithmic transformation was applied to data from end-of-day questionnaires and the data were then analysed by analysis of variance with subject, run and day as blocking factors and exercise and day as treatment factors. Changes in body weight from day 1 to day 10 were analysed by analysis of variance to test for treatment effects. For each treatment, t-tests were used to test for significant difference from zero in body weight change over each manipulation period. Where appropriate, simple linear regressions were conducted to examine temporal trends across the 7 days of each treatment. All analysis was performed using the Genstat 5 statistical program (Genstat 5 Rothamsted Experimental Station, Harpenden, UK).

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Results The actual energy cost of exercise amounted to 0, 1.9 and 3.4 MJ=day respectively (Table 1). This led to significant elevations in total daily EE on going from the Nex, Mex and Hex treatments. Subjects expended on average (s.e.m.) 1.63, (0.06), 1.95, (0.09) and 2.14 (0.06) times RMR, respectively. After subtracting the energy cost of exercise, total daily non-exercise EE amounted to 9.2, 9.0 and 8.7 MJ=day on the Nex, Mex and Hex treatments, respectively. These women did not compensate for the increased energy cost of exercise by resting more at other times in the day. Regression analysis showed that, on average, daily EE decreased by 70.3 MJ on the Hex (t ¼ 72.6; P ¼ 0.046) and Mex (t ¼ 73.3; P ¼ 0.022) treatments, but not the Nex treatment. Subjects consumed (mean (s.e.m.)) 1.58 (0.05), 1.64 (0.05) and 1.78 (0.07) times RMR on the Nex, Mex and Hex treatments, respectively. There was no significant difference in daily intakes of protein between the treatments; the difference in EI was due to elevations of fat and carbohydrate intake (Table 1). EB, estimated from EI minus EE, became more negative and significantly different from zero on the Mex and Hex treatments. Using a value of 26.2 MJ=kg for the energy cost of weight loss16 gave estimates of energy imbalance amounting to 71.3, 71.8 and 72.9 MJ=day. These estimates are within  1 MJ=day of the estimates of EB from EI minus EE data, albeit systematically more negative. There were no significant treatment or day effects for hourly-rated hunger, fullness, prospective consumption, thirst, preoccupation with thoughts of food, tiredness, tension or contentment. However the effect for contentment almost reached significance. Subjects were more content on the Mex treatment than on the other two treatments. When considering the end of day questionnaire there was a significant effect for hunger, thirst, depression, contentedness and tiredness (Table 2).

Table 1 Mean daily energy expenditure, energy and macronutrient intakes, energy balance and body weight changes for the six women during each treatment Nex Total EE (MJ=day) Exercise EE (MJ=day) Non exercise EE (MJ=day) Energy intake (MJ) Energy intake from food (MJ) Energy intake from drinks (MJ) Energy balance (MJ) Protein intake (MJ) Carbohydrate intake (MJ) Fat intake (MJ) Weight change (kg)

Mex

Hex

F (2,10)

P

9.2 11.0 12.1 5.67 0.023 0.0 1.9 3.4 244.41 < 0.001 9.2 9.0 8.7 0.25 0.780 8.9 9.2 10.0 4.80 0.035 8.0 8.2 9.1 4.34 0.044 0.9 1.0 0.9 0.58 0.575 70.3 71.7 72.1 1.44 0.281 1.3 1.3 1.4 1.00 0.402 4.9 5.1 5.4 4.69 0.037 2.7 2.8 3.2 4.10 0.050 { 70.4 70.5 70.8* 1.65 0.240

s.e.d. 0.87 0.16 6.77 0.36 0.38 0.19 1.11 0.07 0.18 0.18 0.23

*t ¼ 72.04; P ¼ 0.097; {t ¼ 73.04; P ¼ 0.029. Tests based on one-sample t-test of whether the slope of weight over time differed from zero.

International Journal of Obesity

Graded levels of exercise RJ Stubbs et al

868 Table 2 Average end of day ratings of mood and motivation to eat for the six female subjects on each treatment

Alert Lively Hungry Thirsty Preoccupationa b Cravings 1 c Cravings 2 Depressed Bored Anxious Full Desire to eat Prospective consumption Tired Tense Contentment Lethargic

Nex (mm)

Mex (mm)

Hex (mm)

F (2, 10)

P

s.e.d.

56 55 44 49 39 14 17 23 21 21 49 51 62 39 28 60 26

63 58 57 54 50 15 22 12 19 14 53 66 72 42 17 70 25

55 55 58 62 50 18 23 14 16 11 47 61 66 55 14 62 26

1.05 0.15 7.98 6.08 3.75 0.28 0.20 6.08 2.52 3.13 0.34 3.42 3.35 4.01 3.11 5.58 0.29

0.385 0.859 0.008 0.019 0.061 0.761 0.818 0.019 0.130 0.088 0.723 0.074 0.077 0.053 0.089 0.024 0.757

5.97 5.96 3.99 3.87 4.89 4.62 8.37 3.71 4.45 4.24 6.45 5.59 3.95 6.12 6.28 3.04 5.26

For each parameter (eg Alert) the question asked how ‘alert’ have you been feeling today? Two extreme states were anchored at either end of the visual analogue scale ‘not at all’ and ‘extremely’. a Preoccupation with thoughts of food. b ‘How often today have you experienced strong cravings to eat particular foods?’ c ‘How strong have any cravings to eat particular types of foods been?’

Discussion and conclusions This particular study simultaneously examined in detail over the course of 7 days, motivation to eat and mood, EI, EE (both due to exercise and total daily EE) and indices of EB. Few studies have examined the effect of exercise on EI over this time period and of those that have, none have incorporated all of the measures used here. In the present study six lean young women underwent 0, 1.9 and 3.4 MJ=day of aerobic exercise. This significantly elevated daily EE from 1.63 to 1.95 and 2.14RMR. Deducting the energy expended in prescribed exercise from total daily EE suggested that subjects did not on average decrease non-exercise EE as the level and intensity of exercise increased. However, regression of total daily EE over the course of each treatment period showed average daily EE decreased by 0.3 MJ=day on the Mex and Hex treatments, indicating that subjects were also showing compensatory adjustments in EE as each intervention progressed. This may have been due to fatigue since in longer-term protocols, leisure time EE does not decrease. EI rose from 1.58 to 1.64 and 1.78RMR which were only significantly different between the Nex and Hex treatments, indicating only partial  30% compensation of EI for exercise-induced increases in EE. It may be that the significant tendency to compensate in these women may be due to a loss of restraint since subjects knew they had expended so much energy. Nonetheless the significant but small increase in hunger (only detected using the End of Day Questionnaire) across treatments is consistent with a weak elevation International Journal of Obesity

in EI. While EI began to track EE as EE rose, this had no effect on protein intake during the study. Subjective hunger and appetite did not change greatly across treatments. Differences between sedentary and exercise treatments approached significance for hourly questionnaires and were significant for the end of day questionnaire. This again suggests a mild increase in the motivation to eat. Subjects lost weight as the EE due to exercise increased. The majority of studies examining the effect of exercise on EI show poor compensation in the short to medium term.2 – 9 The results of this present study add to these findings by showing that that large increases in EE due to exercise have modest but significant effects on motivation to eat and EI in lean women over the course of 7 days. This suggests that coupling of EI to systematic graded elevations in exercise-induced EE would take a number of weeks to achieve equilibrium. Alternatively, a relaxation of cognitive restraint among lean women may explain the partial compensation.

References 1 Department of Health. Obesity. Reversing the increasing problem of obesity in England. Report from the Nutrition and Physical Activity Task Forces. Department of Health: London; 1995. 2 King NA, Tremblay A, Blundell JE. Effects of exercise on appetite control: implications for energy balance. Med Sci Sports Exerc 1997; 29: 1076 – 1089. 3 Woo R, Garrow J, Pi-Sunyer F. Effect of exercise on spontaneous calorie intake in obesity. Am J Clin Nutr 1982; 36: 470 – 477. 4 Woo R, Pi-Sunyer F. Effect of increased physical activity on voluntary intake in lean women. Metabolism 1985; 34: 836 – 841. 5 Woo R, Garrow J. Voluntary food intake during prolonged exercise in obese woman. Am J Clin Nutr 1982; 36: 478 – 484. 6 King NA, Snell L, Smith RD, Blundell JE. Effects of short-term exercise on appetite responses in unrestrained females. Eur J Clin Nutr 1996; 50: 663 – 667. 7 King NA, Lluch A, Stubbs RJ, Blundell JE. High dose exercise does not increase hunger or energy intake in free living males. Eur J Clin Nutr 1997; 51: 478 – 483. 8 Dionne I, Johnson M, White MD, St-Pierre S, Tremblay A. Acute effect of exercise and low-fat diet on energy balance in heavy men. Int J Obes Relat Metab Disord 1997; 21: 413 – 416. 9 Tremblay A, Almeras N, Boer J, Kranenbarg EK, Despres JP. Diet composition and postexercise energy balance. Am J Clin Nutr 1994; 59: 975 – 979. 10 Johnstone AM, Stubbs RJ, Harbron CG. Effect of overfeeding macronutrients on day-to-day food intake in man. Eur J Clin Nutr 1996; 50: 418 – 430. 11 Van strein TV, Frijters JER, Bergers GPA, Defares PB. The Dutch Eating Behaviour Questionnaire (DEBQ) for assessment of restraint, emotional and external eating behaviour. Int J Eat Disord 1986; 5: 295 – 315. 12 Bingham SA, Cummings JH, Murgatroyd PR. PETRA: a new device for weighed dietary intakes. 13th International Congress on Nutrition, 1985, 126 (Abstract). 13 Ceesay SM, Prentice AM, Day KC, Murgatroyd PR, Goldberg GR, Scott W, Spurr GB. The use of heart rate monitoring in the estimation of energy expenditure: a validation study using indirect whole-body calorimetry. Br J Nutr 1989; 61: 175 – 186. 14 B Holand, AA Welch, ID Unwin, DH Buss, AA Paul, DAT Southgate (eds). McCance & Widdowson’s The composition of foods, 5th edn. HMSO: London; 1991.

Graded levels of exercise RJ Stubbs et al 15 Stratton RJ, Stubbs RJ, Hughes D, King N, Blundell JE, Elia M. Comparison of the traditional paper visual analogue scale questionnaire with an Apple Newton electronic appetite rating system (EARS) in free living subjects feeding ad libitum. Eur J Clin Nutr 1998; 52: 737 – 741.

16 Forbes GF, Brown MR, Welle SL, Lipindski BA. Deliberate overfeeding in women and men: energy cost and composition of the weight gain. Br J Nutr 1986; 56: 1 – 9.

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