Effects of weight cycling in female rats

Physiology&Behawor,Vol. 46, pp 417--421 ©Pergamon Press plc, 1989 Pnnted m the U S A

0031-9384/89 $3 00 + 00

Effects of Weight Cycling in Female Rats CELA M. ARCHAMBAULT

Department of Psychology, University of Houston Houston, TX 77204-5341 DANITA CZYZEWSKI 1

Department of Psychiatry and Behavioral Sciences Baylor College of Medicine Texas Children's Hospital, P.O. Box 20269 (1-137) Houston, TX 77225 G L E N N D. C O R D U A

Y CRUZ

Department of Psychology, University of Houston Houston, TX 77204-5341 J O H N P. F O R E Y T

Department of Medicine, Baylor College of Medicine 6535 Fannin, Mail Station F700, Houston, TX 77030 AND M A R C O J. M A R I O T T O

Department of Psychology, University of Houston Houston, TX 77204-5341 R e c e i v e d 7 S e p t e m b e r 1988

ARCHAMBAULT, C. M., D CZYZEWSKI, G. D. CORDUA Y CRUZ, J. P. FOREYT AND M. J. MARIOTTO. Effectsof weight cychng m female rats. PHYSIOL BEHAV 46(3) 417-421, 1989.--Recent reports indicate that weight cycling (repeated periods of weight gain and loss) cause an organism to become an energy conserver, meaning that the organism gains weight more quickly and loses weight more slowly dunng subsequent weight cycles. The effects of weight cychng on rates of weight gain and loss, calonc efficiency, and ad lib wheel runmng were investigated with three groups of adult female rats: 1) cycling(cycled twice); 2) maturity control (cycled once); and 3) chow control (not cycled) The cycled group evidenced weight-gain penods of 36 and 21 days, respectively, and showed a sigmficant increase in food efficiency during the second weight-gain period, relative to the fn'st There was no exqdence that maturataon was responsible for this phenomenon Time required to lose weight and ad lib wheel running were not influenced by weight cycling. These fiodmgs suggest that weight cychng may make mmntenance of normal weight more difficult and have implications for human weight-control programs Obesity

Weight cychng

Caloric efficiency

Somatic activity

Maturation

behavior. Energy conservation in previously calorie-restricted rats has been found by several researchers (4, 13, 22, 23). However,

A N I M A L models of weight cycling (repeated periods of weight gain and loss) have been useful for studying human dieting

1Requests for repnnts should be addressed to Dartita Czyzewslo, Ph.D, Texas Children's Hospital, P O Box 20269 (1-137), Houston, TX 77225.

417

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ARCHAMBAULT ET AL.

in these studies, the cycling method has not been analogous to human " d i e t s . " Brownell, Greenwood, Stellar and Shrager (6) cycled adult male rats in a manner fairly analogous to human dieting. During periods of weight gain, rats were allowed access to a high-fat diet until their mean weight increased to the mean of an obese control group. The rats were then dieted by restricting their intake of rodent chow to 50% of the intake of the normal-weight controls. Weight losses took 21 and 46 days and weight gains took 46 and 14 days during the two cycles, respectwely. Using a ratio of weight change to the number of calories consumed, the rats were found to use calories more efficiently during the second cycle. Unfortunately, the experiment failed to control for maturation. Another group of investigators (22) did find a maturity effect and not a weight cycling effect in female rats The role of physical activity in the etiology and course of obesity has produced contradictory evidence in both human and animal studies. Several studies have found obese people to be less active than those of normal weight (1, 7, 8, 18, 24), though other studies have found no differences (16,17). Additionally, Rolls and Rowe (21) found no activity level differences between female rats that were obese and those of normal weight. Even ff the obese are less active than the lean, the &rection of causahty is not clear First, reactivity may foster weight gain. However, the animal data are equivocal. Two studies found activity slowed weight gain in male rats (20,21). However, female rats, under the same con&tions, became just as obese as nonactive female rats (21). Second, obese organisms may be less active as a result of the lowered metabolic rates that accompany dieting While this effect was found in nonobese humans who were subjected to semlstarvation diets (3,14), it was not found in obese female rats who were restricted to ad lib access to rodent chow (21). Neither of these methods of caloric restriction are analogous to those most obese people use to lose weight. With the contradictory literature m this area, whether the obese are less acuve than the lean is not known In addition, the influence of weight cycling on voluntary somatic activity has not been explored. This study was a replication and an extension of Brownell et al.'s (6) work, with the addmon of the activity factor and with the maturity factor being controlled The retention was to clarify, w~thm the context of weight cychng, the relationship between rate of weight change, caloric efficiency, and activity level. METHOD

Ammals and Maintenance Conditions Twenty-seven three-month-old female Sprague-Dawley rats (Harlan Sprague-Dawley, Indianapolis, IN) were housed in individual actiwty-wheel cages (LC-34, Hazleton, Aberdeen, MD) in a temperature controlled room (24°C) illuminated from 0800 to 2000 hr. Procedure During the 40-day adaptation and the 21-day baseline periods, all animals had ad lib access to powdered Purina Rodent Chow, contained in food devices (LC-306, Hazleton, Aberdeen, MD) designed to minimize food sptllage. Throughout the course of the experiment, body weight, caloric consumption, and activity were measured every third day between 1600 and 1800 hr. On the 18th day of the baseline period, the animals' mean weight, activity, and caloric consumption data were stratified, and the animals were randomly assigned to one of three conditions: 1) cychng (CG) (cycled twice); 2) maturity control (MCG) (cycled once); 3) chow control (CCG) (not cycled). Analysis of variance showed no significant group differences in the variables used for

TABLE 1 ENERGY CONTENT AND COMPOSITION OF FOODS IN THE HIGH-CALORIE DIET

Foods Purina Rodent Chow Milk Formula High-Fat Paste

Energy (kcal)/g

Protein (%)

Carbohydrate (%)

Fat (%)

3 30 2 27 6 15

28 5 12 3 75

59 2 66 7 15 6

12 3 21 0 76 9

stratification, all Fs(2,24)<0.77, all ps>0.47 On the twenty-first day the CG began its first cycle and was switched to a high-calorie diet, consisting of ad lib access to. a milk formula of 2 parts (ml) evaporated milk, to 1 part (ml) water, and 1 part (g) sucrose, a high-fat paste of 2 parts powdered Purina Rodent Chow, to 1 part lard, and 1 part hydrogenated vegetable off (all g); and powdered Purina Rodent Chow (A. Sclafani, personal communication, May 21, 1985). Table 1 gives the energy content and major composition of these foods. The milk formula was contained in standard laboratory water bottles, and the h~gh-fat paste was contained in glass jars. When the CG reached a mean weight that was 20% above the mean weight of the CCG it was switched to a calorie-restricted &et. Attempting to make the caloric restriction as analogous as possible to weight-loss methods used by humans, the animals were given 50% of the mean amount of rodent chow being consumed daily by the CCG (6). This equalled 10 g per day, and food was given daily. The CG remained on this diet until ItS mean weight equaled the mean weight of the CCG. Upon reaching this criterion, the CG was once agam switched to the high-calorie diet as the rats began a second cycle. On the same day, the MCG was switched to the high-calorie &et for the first time. During these cycles, the procedure for both groups, for both weight-gain and weight-loss periods, was identical to that used during the CG's first cycle RESULTS

Figure 1 shows the mean body weight of the three groups of rats at each measurement point. ExamlnaUon of the weight data showed that the rats in the CG took 36 and 21 days, respectively, to reach criterion high weight. A paired comparisons t-test showed a significant difference in the weight of the rats on the 21st day of the two weight gain periods, t(8) = - 3.80, p<0.005. During the two cycles, it took 12 and 9 days, respectively, for the rats in the CG to reach the mean weight of the CCG. There was not a significant difference in weight at day 9 of the two weight-loss periods, t(8)= 1.28, p<0.24. A caloric efficiency index of the ratio of weight change over the number of calories consumed (6) was calculated to assess whether the rats in the CG had utilized energy more efficiently during the second cycle, relative to the first. Paired comparisons t-tests showed the CG's mean daily caloric intake was not slgmficantly different dunng weight-gain periods, t(8)= - 1 . 3 1 , p<0.23. (Table 2 shows the mean daily caloric consumption for each group during each period.) However, caloric efficiency increased significantly from the first to the second weight-gain period, t(8)= - 3 . 7 5 , p<0.006. During the weight-loss periods, mean dally caloric intake was also not significantly different, t ( 8 ) = - 0 17, p<0.87, and caloric efficiency was no greater during the second weight loss, compared to the first, t(8)=0.59, p<0.57. A series of planned between-group comparisons, contrasting the CG's data with that of the MCG, were used to determine the

WEIGHT CYCLING IN FEMALE RATS

419

Cycling Group

310

2?0

230 I

i

(Sl

Maturity Control • Group 310

230

2 ? (

-

C h o w Control Group

230

(s) 12

24

36

48

60

72

84

96

108

120

Days of E x p e r i m e n t

FIG 1 The effects of weight cycling on rate of weight gain and loss m female rats. S = standard diet; HC = high-calorie d]et, CR = calone-restficted diet.

effect of maturation on rate of weight gain and caloric efficiency. During its one weight gain, the MCG required 33 days to reach criterion high weight. On day 33 of both the CG's and the MCG's first weight gain, there was not a significant difference in the weight of the two groups, t(16)=0.0215, p<0.98. Although during its second weight gain, the CG gained to criterion high weight in fewer days than the MCG did during its one weight gain, the weight of the two groups was not significantly different on day 21 of these two cycles, t(16)= 1.16, p<0.26. Mean daily caloric consumption during the CG's first weight gain was not significantly different from that of the MCG during its single weight gain, t(16) = - 1.40, p<0.18, and there was not

TABLE 2 INDIVIDUAL MEAN DAILY CALORIC CONSUMPTION FOR EACH GROUP DURING EACH PERIOD

Period Basehne CG Gain 1 CG Loss 1 CG Gain 2 CG Loss 2 MCG Gain 1 MCG Loss 1

Cycled Group (CG)

Matunty Control Group (MCG)

Chow Control Group-Matched to CG

Chow Control Group-Matched to MCG

63.44

65 86

64.19

--

112.49

63.53

63.02

--

18 80

61.49

60.20

--

117 35

--

61.92

--

18 99

--

64 07

--

--

118.83

--

62 78

--

15 54

--

68.80

a significant difference in caloric efficiency, t(16) = 1.09, p<0.29. There was also not a significant difference in mean dally caloric consumption during the CG's second weight gain and the MCG's smgle weight gain, t ( 1 6 ) = - 0 . 3 4 , p<0.74. However, caloric efficiency was found to be significantly different for these two groups during these two periods, t(16) = 4.22, p<0.0007, with the CG showing greater caloric efficiency. Visual inspection of the activity data showed large day-to-day estrous-related variability in the wheel running of the rats. Consequently, to establish whether spontaneous somatic activity had changed systematically during the periods of weight gain and loss, mean daily activity data were analyzed using two 3 x 5 (groups by periods) general linear model ANOVAs for unbalanced designs. There were no significant within group or between groups differences, and no significant interactions were found, all Fs(2,4)< 1.08, all ps>0.33. Figure 2 shows the mean dally activity level for each group during each time period. In the first analysis, the data from the CCG were matched with the data from the time periods for the CG. In the second analysis, the data from the CCG were matched with the data from the first three time periods for the CG and the last two time periods for the MCG. To assess whether individual differences in caloric consumption predicted individual weight change, caloric consumption was regressed on weight change for each group during each period of the experiment. Individual caloric consumption was found to be a positive predictor of individual weight change during first weight gain for both the CG, R 2 =0.7132, F(1,7) = 17.41, p<0.004, and the MCG, R2=0.5330, F(1,7)=7.99, p<0.03. During the periods that followed first weight gain, individual caloric consumption no longer predicted individual weight change in either group, all R2s<0.0827, all Fs(1,7)<0.68, all ps>0.44. During the time period that corresponded with the CG's first weight loss, individual caloric consumptmn was a positive predictor of individual weight change m the CCG, R 2 = 0.5869, F(1,7)= 9.95, p<0.02. Individual caloric consumption did not predict individual weight change, for any of the groups, during any of the other normalweight periods, all REs<0.3687, all Fs(1,7)<4.09, all ps>0.08.

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ARCHAMBAULT E T AL.

[] • [] []

~(~

Cycled Group (CG) Maturity Control Group (MCG) Chow Control Group-Matches CG Chow Control Group-Matches MCG

X

0

s

¢,

,,-,: (s)

(s) (S)

(HC) (S) (S)

(CR) (S) (S)

(He) (S) (HC) (S)

(CR) (S) (CR) (S)

PERIODS

FIG. 2 Total mean activity for each group dunng each period S = Standard Diet Regimen, HC = High-CalorieDiet Regimen,CR = Calorie-Restricted Diet Regimen

DISCUSSION

Results suggest that gaining weight and then bemg calorie restricted makes maintenance of normal weight more difficult. Following one cycle, the rats showed marked increases in rate of weight gain and efficiency of calorie utilization. This phenomenon was observed in the CG but not the MCG, indicating that the findings are not a result of maturation. These findings are consistent with those of Brownell et al. (6). Unlike Brownell et al. (6), however, our rats did not lose weight more slowly the second time they were calorie restricted, and their increased caloric efficiency did not continue during thetr second weight loss. Gender [Brownell et al. (6) used male rats], voluntary somatic activity [Brownell et al. (6) did not use exercise wheels], and/or the interaction of these variables may account for the discrepant findings. Another variable that may account for the discrepancy is the rats' reluctance to eat the rodent chow following withdrawal of the milk formula and high-fat paste. As a result, the rats did not always consume their full daily ration. This phenomenon was particularly pronounced during the first few days of caloric restriction. Our finding that voluntary somatic activity did not decrease during calorie-restriction periods is consistent with those of Rolls and Rowe (21). The results from these two studies would seem to contradict the well established knowledge that metabolic rate drops with caloric restriction (2, 3, 5, 9, 10, 12, 14, 15, 24), as well as behavioral observations (3,14) and self-reports (14) of decreased somatic activity in normal-weight humans who are on semistarvation diets. There are a number of methodological differences which may explain the apparent contradictions. First, somatic activity is a rather inaccurate measure of total energy expenditure (11). Consequently, our and Rolls and Rowe's (21) measure of ad lib wheel running may not adequately reflect changes in metabolic rate. Second, unlike this study and that of Rolls and Rowe (21), Benedict et al. (3) and Keys et al. (14) studied humans who were of normal weight when caloric restricuon began. Thus, the differences in level of body weight when caloric restriction was initialed may account for the discrepant findings. Further, it is known that, even in rats, wheel running

does not parallel other types of activity (19). Therefore, wheel running in rats may not be a good analogue of actwlty in humans. However, because behavioral observations and self- reports are much less accurate measures than counted wheel rotations, the findings of this study and those of Rolls and Rowe (21) may be more accurate than those of Benedict et al. (3) and Keys et al. (14). Considering all of these factors, we are cautious when interpreting these results, and further research on the impact of weight cycling on activity levels is clearly indicated. Because within-rat weight variance was highly restricted during normal-weight periods, it was not surprising that individual caloric consumption did not consistently predict individual we]ght change during these periods. Because the rats exhibited large changes in weight during first weight gains, it was also not surprising that individual caloric consumption predicted individual weight change dunng these periods. What we found provocative was that individual caloric consumption no longer predicted individual weight change during the CG's second weight gain, although the rats still exhibited large changes in weight. If the process of gaining and then losing weight can cause physiological deregulation, resulting in an organism utilizing calories more efficiently and gaining weight more quickly, this process may also deregulate correspondence between caloric consumptionand amount of weight change. There are two reasons why we are cautious when interpreting these results. First, the number of rats m each group was small (nine); consequently, statistical power was weak. With a larger sample, there might have been significant findings during other time periods. Second, since a large number of analyses (fifteen) were performed, the significant results may have been found by chance. However, our findings do suggest a pattern which should be the subject of future investigation. While the results of this and the Brownell et al. (6) study are not identical, there is agreement that weight cycling has a profound influence on future patterns of weight change in rats. Although the mechanism underlying the phenomenon is unknown, it appears that gaining and then losing weight produces long-term physiological changes which facilitate obesity in rats. Whether or

WEIGHT CYCLING IN FEMALE RATS

421

not these findings are generalizable to humans is also not known. However, our findings may have implications for weight-loss programs which typically focus on caloric restriction. This method may in fact make it more difficult for an individual to maintain a normal weight. Clearly, further research on the effects of weight cycling in larger sample groups is needed. To unravel the complexities of the effects of weight cycling, this research should address the influence of gender, the role of energy expenditure (including meta-

bolic rate, forced somatic activity, and ad lib somatic activity), and level ot: obesity at the time of caloric restriction. ACKNOWLEDGEMENTS We gratefully thank the followmg individuals who assisted with this research: B. Aranda, D. Burton, S Dvoretzky, T. IOng, D. Knott, R. Reloeta, S R. Snuth, C Wait and S. Plullips. Th~sresearch was supported by Umted States Pubhc Health Service Grant No. RR-05425.

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