Journal ofGerontologx: BIOLOGICAL SCIENCES
Copyright 1991 by The Gerontological Society of America
1991, Vol. 46, No. 2.B54-58
Relation of Age and Physical Exercise Status on Metabolic Rate in Younger and Older Healthy Men Eric T. Poehlman,1 Christopher L. Melby,2 and Stephen F. Badylak3 'Division of Endocrinology, Metabolism and Nutrition, College of Medicine, University of Vermont. department of Food Science and Human Nutrition, Colorado State University. 3 Biomedical Engineering Center, Purdue University.
of fatness and leanness, which are regulated THEby extremes fluctuations in energy balance, are important health concerns in the aging population. Little is known, however, regarding the effect of regular participation in physical exercise on metabolic rate in aging man. Previous research has focused on the impact of exercise-training on resting energy metabolism in younger men. For example, young endurance athletes have been reported to have a higher resting metabolic rate (RMR) relative to inactive subjects (Poehlman et al., 1988, 1989; Tremblay et al., 1985, 1986). However, others have observed no meaningful differences in RMR between active and sedentary individuals (Davis et al., 1983; Hill et al., 1984; LeBlanc et al., 1984). The thermic effect of a meal test (TEM) is also reported to be affected by the level of physical exercise in younger men. Energy expenditure following ingestion of a meal or a glucose challenge is blunted in highly trained young males (LeBlanc et al., 1984; Poehlman et al., 1988, 1989; Tremblay et al., 1985), and increased in sedentary individuals who undergo moderate exercise-training (Davis et al., 1983). More recently, an "inverted-U" curve has characterized the association between maximal aerobic fitness and TEM (Poehlman et al., 1989). Differences in subject size, classification of trained and untrained individuals, and the timing of the indirect calorimetry measurements relative to the last exercise bout may contribute to discrepant results among investigators who have examined the association between RMR, TEM, and physical exercise (Poehlman, 1989). Resting metabolic rate declines with age (Calloway and Zanni, 1980; Dill etal., 1967;Golay etal., 1983, Keyset al., 1973; Robinson et al., 1975; Shock et al., 1963; Tzankoff and Norris, 1977, 1978). Several investigators, but not all (Tuttle et al., 1953), have reported an age-related decline in TEM (Golay et al., 1982, 1983; Morgan and York, 1983). These phenomena may contribute to the reduction in energy needs with age and a propensity to gain fat mass. It is unclear, however, whether the inverse relationship between B54
age and metabolic rate (RMR and TEM) is an immutable consequence of the aging process or is subject to the influence of regular participation in physical exercise. The objective of the present study was to compare RMR and TEM in sedentary younger and older men with individuals of similar age who regularly participated in aerobic exercise. MATERIALS AND METHODS
Subjects. — Twenty young (18-34 yr) and 16 older (50-78 yr) males in excellent general health participated in this study. Their physical characteristics are listed in Table 1. Volunteers had: no clinical symptoms of heart disease; a resting blood pressure < 140/90 mm/Hg; no family medical history of diabetes and/or obesity; they were weight stable within the past year ( ± 2 kg) and were presently not taking any medications. One inactive older individual was a light smoker, but had not smoked 12 hr prior to testing. Volunteers were instructed to maintain their normal dietary habits for 3 days prior to testing and did not exercise for at least 24 hours prior to the measurement of metabolic rate. There were four groups in the study defined by age and habitual level of physical exercise as assessed from an exercise history questionnaire: (a) an active younger group (n = 10) comprising runners with a frequency of running at least 3 times per week, an average of 24 ± 6 km per week; (b) an active older group (n — 9) comprising runners averaging 28 ± 7 km per week for at least 12 yr; (c) a sedentary younger group (n = 10); and (d) a sedentary older group (n = 7) that did not participate in any form of regular endurance exercise or conditioning activities. The written informed consent of all volunteers was obtained, and the experimental protocol was approved by the Committee on Human Research. Body fat was estimated from body density by underwater weighing with the Siri (1956) equation. Residual lung volume was assessed by the method of Wilmore et al. (1980). Fat-free
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We examined the influence of age and habitual physical exercise level on resting metabolic rate (RMR) and thermic effect of a meal test (TEM) by studying sedentary and physically active younger and older men. RMR was measured using a ventilated hood and TEM for 180 min after ingestion of a liquid meal. RMR, adjustedfor fat-free weight (FFW) and percent body fat, was lower in sedentary older men relative to the other three groups. TEM (kcahl80 min-1) was highest in active younger (77.3 ± 3.7) and active older men (69.8 ±7.0) relative to sedentary younger (53.1 ± 4.0) and sedentary older men (51.5 ± 6.9). TEM was not related to age or body composition. A sedentary life style in older men may be associated with a lower RMR, independent of FFW and percent body fat, relative to younger men and older men who regularly exercise. Participation in physical exercise, regardless of age, is associated with a higher TEM.
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AGE, EXERCISE, AND METABOLIC RATE
Table 1. Physical Characteristics of Sedentary and Active, Younger and Older Men, Mean ± SEM
Variable Age, yr Height, cm Weight, kg % Body fat Fat-free weight, kg Body mass indexb
Sedentary Younger (n = 10) (1)
Active Younger (n = 10) (2)
Sedentary Older (n = 7) (3)
Active Older (n = 9) (4)
24.1 ± 1.7 (18 to 34) 177.4 ± 2.5 72.3 ± 2.1 14.2 ± 1.2
22.9 ± 0.8 (18 to 28) 179.5 ± 2.3 77.0 ± 2.7 13.6 ± 1.4
63.0 ± 3.3 (53 to 78) 179.2 ± 2.6 83.1 ± 3.6 20.4 ± 1.7
57.9 ± 2.7 (50 to 73) 177.7 ± 3.2 75.7 ± 3.2 15.5 ± 1.4
62.2 ± 7.6 23.0 ± 0.6
66.4 ± 2.2 24.0 ± 0.9
66.0 ± 2.4 26.0 ± 1.5
63.8 ± 2.3 23.9 ± 0.4
2 x 2 ANOVAa
NS< Interaction; 1 vs 3; p < .05 Age;p < .01 Activity; p < .06 NS NS
a
weight (FFW) was estimated as total body weight minus fat weight. Resting metabolic rate and thermic effect of a meal test. — At least 24 hours after the last exercise session, RMR and TEM were established for each subject after a 12-hour fast by indirect calorimetry using a ventilated-hood system (Sensormedics, Anaheim, CA). This method and its reliability have been previously described (Poehlman et al., 1988). Briefly, volunteers were acquainted with the hood system one day prior to conducting the measurements. On the day of testing, subjects were transported to the laboratory and RMR measurements were begun at 0630hr. A 30-min habituation period in the hood preceded a 30-min collection period for measurement of baseline RMR. Thereafter, the hood was removed and the subjects consumed a liquid meal (Sustacal, Mead Johnson, Evansville, IN) with an energy content of 10 kcal'kg FFW"1 and a mixed nutrient composition of 24% protein, 55% carbohydrate, and 21% fat. The subject was then returned to the hood and TEM was measured continuously for the next 180 min and results averaged for 30-min periods. The stability of our measurements following ingestion of a noncaloric solution has previously been documented (Poehlman et al., 1988). Energy expenditure was calculated by the Weir formula (1949). Heart rate was monitored continuously by a single-lead electrocardiogram. Blood pressure was taken at 30-min intervals with a pressure cuff and mercury sphygmomanometer. Statistics. — A 2 x 2 analysis of variance (ANOVA) tested for the main effects of age (older vs younger), physical exercise status (active vs sedentary), and interactions for the physical characteristics of the volunteers. RMR data were analyzed using a 2-way analysis of covariance model with fat-free weight and percent body fat as the two covariates. This allows for the removal of a linear effect of fat-free weight and percent body fat on RMR in testing for the main effect of age and level of physical exercise. An analysis of covariance (ANCOVA) for repeated measures, using percent body fat and fat-free weight as the covariates, tested for the main effects of age and physical activity status on TEM. Adjustment for differences in fat-free weight and percent
body fat, however, did not change the TEM results. Therefore, unadjusted mean values are presented. The Tukey-Kramer post hoc test for multiple comparisons, which corrects for unequal subject sizes, tested for the source of significant interactions. The total increase in postprandial energy expenditure during the 180-min period was calculated by subtracting basal RMR from the mean postprandial metabolic rate and then multiplying by 180 min, as previously described (Poehlman et al., 1988). Percent increases in TEM are expressed relative to the energy content of the meal. All values are represented as means ± SE. RESULTS
No differences in age within the younger and older groups were noted between the active and sedentary men (Table 1). Sedentary younger men weighed less (p < .05) than sedentary older men. Older men had a greater percent body fat (p < .05) than younger men. A borderline main effect was noted for physical activity (p < .06), indicative of the lower percent body fat in active younger and active older men. No significant differences were noted among the groups for standing height, fat-free weight (FFW), and body mass index. Resting metabolic rate (RMR), respiratory exchange ratio (RER), blood pressure, and heart rate in the four groups are listed in Table 2. An effect of age, but not physical activity, was found for unadjusted RMR (kcalmihr1), indicative of the lower RMR (p < .05) in older men relative to younger men. A significant main effect of age (p < .01) and a significant interaction (p < .05) effect were found following the adjustment of RMR for differences in FFW and percent body fat using analysis of covariance. The interaction was due to the lower adjusted RMR in the sedentary older men relative to the other three groups. No differences among groups were found for fasting RER and blood pressure. An effect of physical activity was noted for resting heart rate indicative of the lower heart rate (p < .05) in active men relative to sedentary men. The time course of the thermic effect of the meal test (TEM) among the four groups is shown in Figure 1. As expected, a significant increase in metabolic rate after meal consumption was noted in all groups (p < .01). A significant main effect of activity (p < .01) but not age was noted, indicating that physically active men, regardless of age, had a
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2 X 2 analysis of variance (ANOVA) was performed with age (younger vs older) and physical activity level (active vs sedentary) as grouping factors; values in parentheses are ranges. b Body mass index = wt (kg)/ht (m)2 C NS = nonsignificant
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POEHLMAN ET AL.
Table 2. Resting Metabolic Rate (RMR) and Postabsorptive Respiratory Exchange Ratio, Blood Pressure, and Heart Rate in Sedentary and Active, Younger and Older Men, Mean ± SEM
Variable 1
RMR (kcal'min- ) Adjusted RMRa
Respiratory exchange ratio Systolic blood pressure (mm/Hg) Diastolic blood pressure (mm/Hg) Resting heart rate (bpm)
Sedentary Younger (n = 10) (1)
Active Younger (n = 10) (2)
Sedentary Older (« = 7) (3)
Active Older (n = 9) (4)
1.16 ± 0.04 1.20 ± 0.03
1.16 ± 0.04 1.15 ± 0.03
1.04 ± 0.03 0.97 ± 0.05
1.08 ± 0.04 1.09 ± 0.04
0.79 117 76 59
± ± ± ±
0.01 3.0 2.0 2.0
0.81 115 75 56
± ± ± ±
0.81 119 76 57
0.01 1.0 3.0 2.0
± ± ± ±
0.02 5.0 3.0 2.0
0.79 112 74 50
± ± ± ±
0.04 2.0 3.0 2.0
2 x 2 ANOVA Age; p < .05
Age;p< .01 3 vs \;p< .01 3 vs2;/?< .01 3 v s 4 ; p < .05 NSb NS NS Activity; p < .05
higher TEM than sedentary men. Total TEM (kcal»180 min"1) was higher (—40%) in active younger (77.0 ± 3.7) and active older men (69.8 ± 7.0) relative to sedentary younger (53.1 ± 4.0) and sedentary older men (51.5 ± 6.9). Similar results were found when TEM was expressed as a percent increase in metabolic rate relative to the caloric content of the meal ([caloric load/total TEM kcaM80 min"1 min] x 100%). Percent TEM was higher in active younger men (11.7 ± 0.6%) and active older men (10.9 ± 0.9%) relative to sedentary younger men (8.7 ± 0.8%) and sedentary older men (7.9 ± 1.2%) (data not shown in figure form). Adjustment of TEM using the covariates of percent body fat and FFW did not alter the aforementioned results. As expected, the RER increased in all groups after meal consumption (p < .01), but no significant differences were noted among groups. The mean postprandial RER was 0.88 ± 0.01 in sedentary younger men, 0.90 ± 0.01 in active younger men, 0.88 ± 0.02 in sedentary older men, and 0.85 ± 0.02 in active older men. A significant increase in heart rate (p < .01) was noted after meal ingestion. An age effect (p < .01) was noted for postprandial heart rate. The mean postprandial heart rate was lower in sedentary older (61 ± 2 ) and active older men (57 ± 3) relative to younger sedentary (70 ± 2) and younger active men (67 ± 3) (data not shown in table form). Systolic blood pressure increased after meal consumption (p < .01), but no significant differences were found among groups. The mean postprandial systolic blood pressure was 121 ± 3 for sedentary younger men, 120 ± 2 for active younger men, 120 ± 4 for sedentary older men, and 115 ± 4 for active older men. No changes in response to the meal or differences among groups were found for diastolic blood pressure. The mean postprandial diastolic blood pressure was 75 ± 2 for sedentary younger men, 74 ± 3 for active men, 77 ± 3 for sedentary older men, and 73 ± 2 for active older men (data not shown in table form). A significant linear correlation was noted between RMR and FFW (r = .57; p < .01). No relation was noted between RMR and percent body fat (r = -.05). No significant association was noted between TEM and FFW (r = .26) and between TEM and percent body fat (r = .08).
TOTAL POSTPRANDIAL ENERGY EXPENDITURE
• o • C
0
30
60
Younger Inactive Younger Active Older Inactive Older Active
90
120
150
180
Postprandial Time (min)
Figure 1. Increase in postprandial energy expenditure for active and sedentary, younger and older men after ingestion of a liquid meal. The inset shows the total postprandial energy expenditure (kcaM80 min-1) in the four groups.
DISCUSSION
We examined the impact of age and activity level on RMR and TEM in younger and older individuals who regularly participated in aerobic exercise relative to sedentary volunteers. We recruited active older and younger men with similar exercise habits (i.e., frequency of exercise participation and distance run per week). We controlled for differences in adiposity and FFW among individuals using covariance analysis. Resting metabolic rate. — We noted a lower RMR (—8%), uncorrected for body size (kcal'min-1), in older men relative to younger men. This is concordant with other crosssectional (Calloway and Zanni, 1980; Shock et al., 1963; Tuttle et al., 1953; Tzankoff and Norris, 1977; Tzankoff and Norris, 1978) and longitudinal studies (Dill et al., 1967; Keys et al., 1973) in which an age-related decline in RMR was noted. The magnitude of the decline in RMR in older men relative to the younger men compares favorably with the rate of decline of —2% per decade reported by Keys et al.
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"Adjusted RMR are values after analysis of covariance with fat-free weight and percent body fat as covariates. b NS = nonsignificant.
AGE, EXERCISE, AND METABOLIC RATE
Thermic effect of a meal. — Although TEM represents a smaller fraction of 24h energy expenditure (—10%), it is thought to be important in the long-term control of energy balance (Danforth, 1981). In the present study, regardless of age, individuals who regularly participated in aerobic exercise had a higher TEM (—40%) relative to inactive men. The higher TEM in moderately active younger individuals has previously been reported (Davis et al., 1983; Hill et al., 1984; Poehlman et al., 1989). We have extended these previous findings to include active older men. In fact, the magnitude of TEM was comparable between active younger men and active older men. The higher TEM persists when data were analyzed either as total energy expenditure for 3 hours; as the integrated area under the postprandial response curve; or
as a percent increase in energy expenditure relative to the caloric load. Lundholm et al. (1986) reported a higher TEM (-56%) in well-trained older men compared to inactive older men but did not consider younger men in their study. Our results do not indicate a difference in the relative amounts of substrate oxidation as a possible explanation for differences in TEM, as fasting and postprandial values of RER were similar among the four groups. On a speculative note, perhaps differences in the energetics of substrate cycling (i.e., total lipid recycling) induced by chronic physical activity contribute to the higher TEM in active individuals. We did not observe an effect of age on TEM in this study, as TEM was similar between inactive younger and older men, as well as between active younger and older men. Some investigators (Golay et al., 1982, 1983), but not all (Tuttle et al., 1953) have suggested that aging is associated with a lower energy expenditure after a meal or glucose ingestion, which may be related to an impairment of glucose uptake (Golay et al., 1982, 1983). Divergent results among investigators may relate to the energy content and nutrient mix of the meal challenge, duration of the postprandial measurements, and the degree of insulin resistance in the older population. TEM (kcaM80 mhr1), unlike RMR, was not significantly related to an index of body composition in this study. Associations between TEM and fat-free weight (r = .26) and percent body fat (r = .08) were nonsignificant. This would argue against the need to standardize postprandial thermogenesis to an index of body size and suggest that TEM is not dependent on body composition in normal weight younger and older males. A cause-and-effect relation between physical activity and its influence on RMR and TEM cannot be established from this study. RMR exhibits a genetic influence (Fontaine et al., 1985), and sensitivity of the adaptive response of RMR and TEM to short-term exercise training has also been shown to be genotype dependent (Poehlman et al., 1986). Long-term exercise intervention studies are needed to more critically examine changes in RMR and TEM with chronic participation in physical activity in older persons. ACKNOWLEDGMENTS
Dr. Poehlman's work is supported by a grant from the National Institute of Aging (AG-07857), the American Association of Retired Persons (AARP) Andrus Foundation, and in part by the General Clinical Research Center at the University of Vermont (NIH RR-109). Dr. Poehlman is a recipient of the 1990 Nation W. Shock New Investigator Award presented by The Gerontological Society of America Biological Sciences Section. The authors thank Lauri LoPresto, Paul Arciero, and Joe Sagorsky for their technical assistance. Appreciation is extended to Dr. Elliot Danforth, Jr., Dr. Michael I. Goran, and David Van Houten for their constructive criticisms of the manuscript. Address correspondence to Dr. Eric T. Poehlman, Division of Endocrinology, Metabolism and Nutrition, College of Medicine, University of Vermont, Burlington, VT 05405. REFERENCES
Calloway, D. H.; Zanni, E. Energy requirements and energy expenditure of elderly men. Am. J. Clin. Nutr. 33:2088-2092; 1980. Cohn, S. H.; Vartsky, D.; Yasumura, S.; Sawitsky, A.; Zanzi, I.; Vaswani, A.; Ellis, K. J. Compartmental body composition based on total-body
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(1973), when considering the four-decade difference between younger and older men in the present study. When comparing individuals of different age, level of physical exercise and body composition, RMR must be standardized to a suitable index of body size. It has been suggested that fat-free weight is the appropriate reference unit because it most closely quantifies the mass of the active tissues (Cunningham, 1980; Keys et al., 1973; Ravussin et al., 1986). Our results support the significant relation between RMR and FFW (r = .57; p < .01). The lower order correlation between FFW and RMR relative to other studies (Cunningham, 1980; Ravussin et al., 1986) is probably reflective of the homogeneity of our subjects with respect to FFW. RMR was lower in older men when differences in percent body fat and FFW were taken into account using covariance analysis (Table 2). These findings support those of Fukagawa et al. (1990), who also found that differences in fat-free weight cannot fully account for the lower RMR in older persons. The age effect was strongly influenced by the lower RMR in sedentary older men who displayed a ~ 11 % and — 17% lower RMR relative to physically active older men and younger men, respectively. No differences in adjusted RMR were noted between sedentary and younger active men. The higher RMR in active older men relative to sedentary older men suggests that regular participation in aerobic exercise may attenuate the age-related decline in RMR. Previous authors who have examined the effects of aging on RMR have not considered the level of physical activity as a factor influencing metabolic rate (Keys et al., 1973; Shock et al., 1963; Tzankoff and Norris, 1977, 1978). The etiology of the lower RMR in sedentary older men cannot be determined from the present study. With advancing age, skeletal muscle occupies an increasingly smaller percentage of FFW (Cohn et al., 1980). Thus despite a similar quantity of FFW relative to the other groups, the skeletal mass component may be reduced in sedentary older men and contribute to the lower RMR. This implies, on the other hand, that regular physical exercise may attenuate the loss of skeletal mass in older men, as evidenced by the higher RMR in active older men. These results need to be confirmed with a larger sample size using measures of body composition that more accurately discriminate between skeletal muscle and nonmuscle compartments in younger and older individuals.
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Poehlman, E. T.; Melby C. L.; Badylak, S. F. Resting metabolic rate and postprandial thermogenesis in highly trained and untrained males. Am. J. Clin. Nutr. 47:793-798; 1988. Poehlman, E. T.; Melby, C. L.; Badylak, S. F.; Calles, J. Aerobicfitnessand resting energy expenditure in young adult males. Metabolism 38:85-90; 1989. Ravussin, E.; Lillioja, S.; Anderson, T. E.; Christin, L.; Bogardus, C. Determinants of 24-hour energy expenditure in man. Methods and results using a respiratory chamber. J. Clin. Invest. 78:1568-1578; 1986. Robinson, S.; Dill, D. B.; Tzankoff, S. P.; Wagner, J. A.; Robinson, R. D. Longitudinal studies of aging in 37 men. J. Appl. Physiol. 38:263-267; 1975. Shock, N. W.; Watkin, D. M.; Yiengst, M. J.; Norris, A. H.; Gaffney, G. W.; Gregerman, R. I.; Falzone, J. A. Age differences in the water content of the body as related to basal oxygen consumption in males. J. Gerontol. 18:1-8; 1963. Siri, W. E. The gross composition of the body. Adv. Biol. Med. Phys. 4:239-280; 1956. Tremblay, A.; Fontaine, E.; Nadeau, A. Contribution of postexercise increment in glucose storage to variations in glucose-induced thermogenesis in endurance athletes. Can. J. Physiol. Pharmacol. 63:1165-1169; 1985. Tremblay, A.; Fontaine, E.; Poehlman, E. T.; Mitchell, D.; Perron, L.; Bouchard, C. The effect of exercise-training on resting metabolic rate in lean and moderately obese individuals. Int. J. Obesity 10:511-517; 1986. Tuttle, W. W.; Horvath, S. M.; Presson, L. F.; Daum, K. Specific dynamic action of protein in men past 60 years of age. J. Appl. Physiol. 5:631— 634; 1953. Tzankoff, S. P.; Norris, A. J. Effect of muscle mass decrease on age-related BMR changes. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 43:1001-1006; 1977. Tzankoff, S. P.; Norris, A. H. Longitudinal changes in basal metabolism in man. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 45:536539;1978. Weir, J. B. de V. New methods for calculating metabolic rate with special reference to protein. J. Physiol. 109:1-9; 1949. Wilmore, J. H.; Vodak, P. A.; Parr, R. B.; Girandola, R. N.; Billing, J. E. Further simplification of a method of residual lung volume. Med. Sci. Sports Exerc. 12:216-218; 1980. Received August 23', 1989 Accepted April 17, 1990
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nitrogen, potassium, and calcium. Am. J. Physiol. 239:E524—E53O; 1980. Cunningham, J. J. A reanalysis of the factors influencing basal metabolic rate in normal adults. Am. J. Clin. Nutr. 33:2372-2374; 1980. Danforth, E. Jr. Dietary-induced thermogenesis: control of energy expenditure. Life Sci. 28:1821-1827; 1981. Davis, J. R.; Tagliaferro, A. R.; Kertzer, R.; Gerardo, T; Nichols, J.; Wheeler, J. Variations in dietary-induced thermogenesis and body fatness with aerobic capacity. Eur. J. Appl. Physiol. 50:319-329; 1983. Dill, D. B.; Robinson, S.; Ross, J. C. A longitudinal study of 16 champion runners. J. Sports Med. 7:4-27; 1967. Fukagawa, N. K.; Bandini, L. G.; Young, J. B. Effect of age on body composition and resting metabolic rate. Am. J. Physiol. 259:E233E238; 1990. Fontaine, E.; Savard, R.; Tremblay, A.; Poehlman, E.; Bouchard, C. Resting metabolic rate in monozygotic and dizygotic twins. Acta Genet. Med. Gemellol. 34:41-47; 1985. Golay, A.; Schutz, Y.; Meyer, H. U.; Thiebaud, D.; Churchod, B.; Maeder, E.; Felber, J. P.; Jequier, E. Glucose-induced thermogenesis in nondiabetic and diabetic obese subjects. Diabetes: 31:1023-1028; 1982. Golay, A.; Schutz, Y.; Broquet, C ; Moeri, R.; Felber, J. P.; Jequier, E. Decreased thermogenic response to an oral glucose load in older subjects. J. Am. Geriatr. Soc. 31:144-148; 1983. Hill, J. O.; Heymsfield, S. B.; McMannus III, C ; DiGirolamo, M. Meal size and thermic response to food in male subjects as a function of maximum aerobic capacity. Metabolism 33:743-749; 1984. Keys, A.; Taylor, H. L.; Grande, F. Basal metabolism and age of adult man. Metabolism 22:579-587; 1973. LeBlanc, J.; Diamond, P.; Cote, P.; Labrie, A. Hormonal factors on reduced postprandial heat production of exercise-trained subjects. J. Appl. Physiol. 56:772-776; 1984. Lundholm, K.; Holm, G.; Lindmark, L.; Larsson, B.; Sjostrom, L.; Bjorntorp, P. Thermogenic effect of food in physically well-trained elderly men. Eur. J. Appl. Physiol. 55:486-492; 1986. Morgan, J. B.; York, D. A. Thermic effect of feeding in relation to energy balance in elderly men. Ann. Nutr. Metab. 27:71-77; 1983. Poehlman, E. T. A review: Exercise and its influence on resting energy metabolism in man. Med. Sci. Sports Exerc. 21:515-525; 1989. Poehlman, E. T.; Tremblay, A.; Nadeau, A.; Dussault, J.; Theriault, G.; Bouchard, C. Heredity and changes in hormones and metabolic rates with short-term training. Am. J. Physiol. 250:E711-717; 1986.
Copyright 1991 by The Gerontological Society of America
1991, Vol. 46, No. 2.B54-58
Relation of Age and Physical Exercise Status on Metabolic Rate in Younger and Older Healthy Men Eric T. Poehlman,1 Christopher L. Melby,2 and Stephen F. Badylak3 'Division of Endocrinology, Metabolism and Nutrition, College of Medicine, University of Vermont. department of Food Science and Human Nutrition, Colorado State University. 3 Biomedical Engineering Center, Purdue University.
of fatness and leanness, which are regulated THEby extremes fluctuations in energy balance, are important health concerns in the aging population. Little is known, however, regarding the effect of regular participation in physical exercise on metabolic rate in aging man. Previous research has focused on the impact of exercise-training on resting energy metabolism in younger men. For example, young endurance athletes have been reported to have a higher resting metabolic rate (RMR) relative to inactive subjects (Poehlman et al., 1988, 1989; Tremblay et al., 1985, 1986). However, others have observed no meaningful differences in RMR between active and sedentary individuals (Davis et al., 1983; Hill et al., 1984; LeBlanc et al., 1984). The thermic effect of a meal test (TEM) is also reported to be affected by the level of physical exercise in younger men. Energy expenditure following ingestion of a meal or a glucose challenge is blunted in highly trained young males (LeBlanc et al., 1984; Poehlman et al., 1988, 1989; Tremblay et al., 1985), and increased in sedentary individuals who undergo moderate exercise-training (Davis et al., 1983). More recently, an "inverted-U" curve has characterized the association between maximal aerobic fitness and TEM (Poehlman et al., 1989). Differences in subject size, classification of trained and untrained individuals, and the timing of the indirect calorimetry measurements relative to the last exercise bout may contribute to discrepant results among investigators who have examined the association between RMR, TEM, and physical exercise (Poehlman, 1989). Resting metabolic rate declines with age (Calloway and Zanni, 1980; Dill etal., 1967;Golay etal., 1983, Keyset al., 1973; Robinson et al., 1975; Shock et al., 1963; Tzankoff and Norris, 1977, 1978). Several investigators, but not all (Tuttle et al., 1953), have reported an age-related decline in TEM (Golay et al., 1982, 1983; Morgan and York, 1983). These phenomena may contribute to the reduction in energy needs with age and a propensity to gain fat mass. It is unclear, however, whether the inverse relationship between B54
age and metabolic rate (RMR and TEM) is an immutable consequence of the aging process or is subject to the influence of regular participation in physical exercise. The objective of the present study was to compare RMR and TEM in sedentary younger and older men with individuals of similar age who regularly participated in aerobic exercise. MATERIALS AND METHODS
Subjects. — Twenty young (18-34 yr) and 16 older (50-78 yr) males in excellent general health participated in this study. Their physical characteristics are listed in Table 1. Volunteers had: no clinical symptoms of heart disease; a resting blood pressure < 140/90 mm/Hg; no family medical history of diabetes and/or obesity; they were weight stable within the past year ( ± 2 kg) and were presently not taking any medications. One inactive older individual was a light smoker, but had not smoked 12 hr prior to testing. Volunteers were instructed to maintain their normal dietary habits for 3 days prior to testing and did not exercise for at least 24 hours prior to the measurement of metabolic rate. There were four groups in the study defined by age and habitual level of physical exercise as assessed from an exercise history questionnaire: (a) an active younger group (n = 10) comprising runners with a frequency of running at least 3 times per week, an average of 24 ± 6 km per week; (b) an active older group (n — 9) comprising runners averaging 28 ± 7 km per week for at least 12 yr; (c) a sedentary younger group (n = 10); and (d) a sedentary older group (n = 7) that did not participate in any form of regular endurance exercise or conditioning activities. The written informed consent of all volunteers was obtained, and the experimental protocol was approved by the Committee on Human Research. Body fat was estimated from body density by underwater weighing with the Siri (1956) equation. Residual lung volume was assessed by the method of Wilmore et al. (1980). Fat-free
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We examined the influence of age and habitual physical exercise level on resting metabolic rate (RMR) and thermic effect of a meal test (TEM) by studying sedentary and physically active younger and older men. RMR was measured using a ventilated hood and TEM for 180 min after ingestion of a liquid meal. RMR, adjustedfor fat-free weight (FFW) and percent body fat, was lower in sedentary older men relative to the other three groups. TEM (kcahl80 min-1) was highest in active younger (77.3 ± 3.7) and active older men (69.8 ±7.0) relative to sedentary younger (53.1 ± 4.0) and sedentary older men (51.5 ± 6.9). TEM was not related to age or body composition. A sedentary life style in older men may be associated with a lower RMR, independent of FFW and percent body fat, relative to younger men and older men who regularly exercise. Participation in physical exercise, regardless of age, is associated with a higher TEM.
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Table 1. Physical Characteristics of Sedentary and Active, Younger and Older Men, Mean ± SEM
Variable Age, yr Height, cm Weight, kg % Body fat Fat-free weight, kg Body mass indexb
Sedentary Younger (n = 10) (1)
Active Younger (n = 10) (2)
Sedentary Older (n = 7) (3)
Active Older (n = 9) (4)
24.1 ± 1.7 (18 to 34) 177.4 ± 2.5 72.3 ± 2.1 14.2 ± 1.2
22.9 ± 0.8 (18 to 28) 179.5 ± 2.3 77.0 ± 2.7 13.6 ± 1.4
63.0 ± 3.3 (53 to 78) 179.2 ± 2.6 83.1 ± 3.6 20.4 ± 1.7
57.9 ± 2.7 (50 to 73) 177.7 ± 3.2 75.7 ± 3.2 15.5 ± 1.4
62.2 ± 7.6 23.0 ± 0.6
66.4 ± 2.2 24.0 ± 0.9
66.0 ± 2.4 26.0 ± 1.5
63.8 ± 2.3 23.9 ± 0.4
2 x 2 ANOVAa
NS< Interaction; 1 vs 3; p < .05 Age;p < .01 Activity; p < .06 NS NS
a
weight (FFW) was estimated as total body weight minus fat weight. Resting metabolic rate and thermic effect of a meal test. — At least 24 hours after the last exercise session, RMR and TEM were established for each subject after a 12-hour fast by indirect calorimetry using a ventilated-hood system (Sensormedics, Anaheim, CA). This method and its reliability have been previously described (Poehlman et al., 1988). Briefly, volunteers were acquainted with the hood system one day prior to conducting the measurements. On the day of testing, subjects were transported to the laboratory and RMR measurements were begun at 0630hr. A 30-min habituation period in the hood preceded a 30-min collection period for measurement of baseline RMR. Thereafter, the hood was removed and the subjects consumed a liquid meal (Sustacal, Mead Johnson, Evansville, IN) with an energy content of 10 kcal'kg FFW"1 and a mixed nutrient composition of 24% protein, 55% carbohydrate, and 21% fat. The subject was then returned to the hood and TEM was measured continuously for the next 180 min and results averaged for 30-min periods. The stability of our measurements following ingestion of a noncaloric solution has previously been documented (Poehlman et al., 1988). Energy expenditure was calculated by the Weir formula (1949). Heart rate was monitored continuously by a single-lead electrocardiogram. Blood pressure was taken at 30-min intervals with a pressure cuff and mercury sphygmomanometer. Statistics. — A 2 x 2 analysis of variance (ANOVA) tested for the main effects of age (older vs younger), physical exercise status (active vs sedentary), and interactions for the physical characteristics of the volunteers. RMR data were analyzed using a 2-way analysis of covariance model with fat-free weight and percent body fat as the two covariates. This allows for the removal of a linear effect of fat-free weight and percent body fat on RMR in testing for the main effect of age and level of physical exercise. An analysis of covariance (ANCOVA) for repeated measures, using percent body fat and fat-free weight as the covariates, tested for the main effects of age and physical activity status on TEM. Adjustment for differences in fat-free weight and percent
body fat, however, did not change the TEM results. Therefore, unadjusted mean values are presented. The Tukey-Kramer post hoc test for multiple comparisons, which corrects for unequal subject sizes, tested for the source of significant interactions. The total increase in postprandial energy expenditure during the 180-min period was calculated by subtracting basal RMR from the mean postprandial metabolic rate and then multiplying by 180 min, as previously described (Poehlman et al., 1988). Percent increases in TEM are expressed relative to the energy content of the meal. All values are represented as means ± SE. RESULTS
No differences in age within the younger and older groups were noted between the active and sedentary men (Table 1). Sedentary younger men weighed less (p < .05) than sedentary older men. Older men had a greater percent body fat (p < .05) than younger men. A borderline main effect was noted for physical activity (p < .06), indicative of the lower percent body fat in active younger and active older men. No significant differences were noted among the groups for standing height, fat-free weight (FFW), and body mass index. Resting metabolic rate (RMR), respiratory exchange ratio (RER), blood pressure, and heart rate in the four groups are listed in Table 2. An effect of age, but not physical activity, was found for unadjusted RMR (kcalmihr1), indicative of the lower RMR (p < .05) in older men relative to younger men. A significant main effect of age (p < .01) and a significant interaction (p < .05) effect were found following the adjustment of RMR for differences in FFW and percent body fat using analysis of covariance. The interaction was due to the lower adjusted RMR in the sedentary older men relative to the other three groups. No differences among groups were found for fasting RER and blood pressure. An effect of physical activity was noted for resting heart rate indicative of the lower heart rate (p < .05) in active men relative to sedentary men. The time course of the thermic effect of the meal test (TEM) among the four groups is shown in Figure 1. As expected, a significant increase in metabolic rate after meal consumption was noted in all groups (p < .01). A significant main effect of activity (p < .01) but not age was noted, indicating that physically active men, regardless of age, had a
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2 X 2 analysis of variance (ANOVA) was performed with age (younger vs older) and physical activity level (active vs sedentary) as grouping factors; values in parentheses are ranges. b Body mass index = wt (kg)/ht (m)2 C NS = nonsignificant
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Table 2. Resting Metabolic Rate (RMR) and Postabsorptive Respiratory Exchange Ratio, Blood Pressure, and Heart Rate in Sedentary and Active, Younger and Older Men, Mean ± SEM
Variable 1
RMR (kcal'min- ) Adjusted RMRa
Respiratory exchange ratio Systolic blood pressure (mm/Hg) Diastolic blood pressure (mm/Hg) Resting heart rate (bpm)
Sedentary Younger (n = 10) (1)
Active Younger (n = 10) (2)
Sedentary Older (« = 7) (3)
Active Older (n = 9) (4)
1.16 ± 0.04 1.20 ± 0.03
1.16 ± 0.04 1.15 ± 0.03
1.04 ± 0.03 0.97 ± 0.05
1.08 ± 0.04 1.09 ± 0.04
0.79 117 76 59
± ± ± ±
0.01 3.0 2.0 2.0
0.81 115 75 56
± ± ± ±
0.81 119 76 57
0.01 1.0 3.0 2.0
± ± ± ±
0.02 5.0 3.0 2.0
0.79 112 74 50
± ± ± ±
0.04 2.0 3.0 2.0
2 x 2 ANOVA Age; p < .05
Age;p< .01 3 vs \;p< .01 3 vs2;/?< .01 3 v s 4 ; p < .05 NSb NS NS Activity; p < .05
higher TEM than sedentary men. Total TEM (kcal»180 min"1) was higher (—40%) in active younger (77.0 ± 3.7) and active older men (69.8 ± 7.0) relative to sedentary younger (53.1 ± 4.0) and sedentary older men (51.5 ± 6.9). Similar results were found when TEM was expressed as a percent increase in metabolic rate relative to the caloric content of the meal ([caloric load/total TEM kcaM80 min"1 min] x 100%). Percent TEM was higher in active younger men (11.7 ± 0.6%) and active older men (10.9 ± 0.9%) relative to sedentary younger men (8.7 ± 0.8%) and sedentary older men (7.9 ± 1.2%) (data not shown in figure form). Adjustment of TEM using the covariates of percent body fat and FFW did not alter the aforementioned results. As expected, the RER increased in all groups after meal consumption (p < .01), but no significant differences were noted among groups. The mean postprandial RER was 0.88 ± 0.01 in sedentary younger men, 0.90 ± 0.01 in active younger men, 0.88 ± 0.02 in sedentary older men, and 0.85 ± 0.02 in active older men. A significant increase in heart rate (p < .01) was noted after meal ingestion. An age effect (p < .01) was noted for postprandial heart rate. The mean postprandial heart rate was lower in sedentary older (61 ± 2 ) and active older men (57 ± 3) relative to younger sedentary (70 ± 2) and younger active men (67 ± 3) (data not shown in table form). Systolic blood pressure increased after meal consumption (p < .01), but no significant differences were found among groups. The mean postprandial systolic blood pressure was 121 ± 3 for sedentary younger men, 120 ± 2 for active younger men, 120 ± 4 for sedentary older men, and 115 ± 4 for active older men. No changes in response to the meal or differences among groups were found for diastolic blood pressure. The mean postprandial diastolic blood pressure was 75 ± 2 for sedentary younger men, 74 ± 3 for active men, 77 ± 3 for sedentary older men, and 73 ± 2 for active older men (data not shown in table form). A significant linear correlation was noted between RMR and FFW (r = .57; p < .01). No relation was noted between RMR and percent body fat (r = -.05). No significant association was noted between TEM and FFW (r = .26) and between TEM and percent body fat (r = .08).
TOTAL POSTPRANDIAL ENERGY EXPENDITURE
• o • C
0
30
60
Younger Inactive Younger Active Older Inactive Older Active
90
120
150
180
Postprandial Time (min)
Figure 1. Increase in postprandial energy expenditure for active and sedentary, younger and older men after ingestion of a liquid meal. The inset shows the total postprandial energy expenditure (kcaM80 min-1) in the four groups.
DISCUSSION
We examined the impact of age and activity level on RMR and TEM in younger and older individuals who regularly participated in aerobic exercise relative to sedentary volunteers. We recruited active older and younger men with similar exercise habits (i.e., frequency of exercise participation and distance run per week). We controlled for differences in adiposity and FFW among individuals using covariance analysis. Resting metabolic rate. — We noted a lower RMR (—8%), uncorrected for body size (kcal'min-1), in older men relative to younger men. This is concordant with other crosssectional (Calloway and Zanni, 1980; Shock et al., 1963; Tuttle et al., 1953; Tzankoff and Norris, 1977; Tzankoff and Norris, 1978) and longitudinal studies (Dill et al., 1967; Keys et al., 1973) in which an age-related decline in RMR was noted. The magnitude of the decline in RMR in older men relative to the younger men compares favorably with the rate of decline of —2% per decade reported by Keys et al.
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"Adjusted RMR are values after analysis of covariance with fat-free weight and percent body fat as covariates. b NS = nonsignificant.
AGE, EXERCISE, AND METABOLIC RATE
Thermic effect of a meal. — Although TEM represents a smaller fraction of 24h energy expenditure (—10%), it is thought to be important in the long-term control of energy balance (Danforth, 1981). In the present study, regardless of age, individuals who regularly participated in aerobic exercise had a higher TEM (—40%) relative to inactive men. The higher TEM in moderately active younger individuals has previously been reported (Davis et al., 1983; Hill et al., 1984; Poehlman et al., 1989). We have extended these previous findings to include active older men. In fact, the magnitude of TEM was comparable between active younger men and active older men. The higher TEM persists when data were analyzed either as total energy expenditure for 3 hours; as the integrated area under the postprandial response curve; or
as a percent increase in energy expenditure relative to the caloric load. Lundholm et al. (1986) reported a higher TEM (-56%) in well-trained older men compared to inactive older men but did not consider younger men in their study. Our results do not indicate a difference in the relative amounts of substrate oxidation as a possible explanation for differences in TEM, as fasting and postprandial values of RER were similar among the four groups. On a speculative note, perhaps differences in the energetics of substrate cycling (i.e., total lipid recycling) induced by chronic physical activity contribute to the higher TEM in active individuals. We did not observe an effect of age on TEM in this study, as TEM was similar between inactive younger and older men, as well as between active younger and older men. Some investigators (Golay et al., 1982, 1983), but not all (Tuttle et al., 1953) have suggested that aging is associated with a lower energy expenditure after a meal or glucose ingestion, which may be related to an impairment of glucose uptake (Golay et al., 1982, 1983). Divergent results among investigators may relate to the energy content and nutrient mix of the meal challenge, duration of the postprandial measurements, and the degree of insulin resistance in the older population. TEM (kcaM80 mhr1), unlike RMR, was not significantly related to an index of body composition in this study. Associations between TEM and fat-free weight (r = .26) and percent body fat (r = .08) were nonsignificant. This would argue against the need to standardize postprandial thermogenesis to an index of body size and suggest that TEM is not dependent on body composition in normal weight younger and older males. A cause-and-effect relation between physical activity and its influence on RMR and TEM cannot be established from this study. RMR exhibits a genetic influence (Fontaine et al., 1985), and sensitivity of the adaptive response of RMR and TEM to short-term exercise training has also been shown to be genotype dependent (Poehlman et al., 1986). Long-term exercise intervention studies are needed to more critically examine changes in RMR and TEM with chronic participation in physical activity in older persons. ACKNOWLEDGMENTS
Dr. Poehlman's work is supported by a grant from the National Institute of Aging (AG-07857), the American Association of Retired Persons (AARP) Andrus Foundation, and in part by the General Clinical Research Center at the University of Vermont (NIH RR-109). Dr. Poehlman is a recipient of the 1990 Nation W. Shock New Investigator Award presented by The Gerontological Society of America Biological Sciences Section. The authors thank Lauri LoPresto, Paul Arciero, and Joe Sagorsky for their technical assistance. Appreciation is extended to Dr. Elliot Danforth, Jr., Dr. Michael I. Goran, and David Van Houten for their constructive criticisms of the manuscript. Address correspondence to Dr. Eric T. Poehlman, Division of Endocrinology, Metabolism and Nutrition, College of Medicine, University of Vermont, Burlington, VT 05405. REFERENCES
Calloway, D. H.; Zanni, E. Energy requirements and energy expenditure of elderly men. Am. J. Clin. Nutr. 33:2088-2092; 1980. Cohn, S. H.; Vartsky, D.; Yasumura, S.; Sawitsky, A.; Zanzi, I.; Vaswani, A.; Ellis, K. J. Compartmental body composition based on total-body
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(1973), when considering the four-decade difference between younger and older men in the present study. When comparing individuals of different age, level of physical exercise and body composition, RMR must be standardized to a suitable index of body size. It has been suggested that fat-free weight is the appropriate reference unit because it most closely quantifies the mass of the active tissues (Cunningham, 1980; Keys et al., 1973; Ravussin et al., 1986). Our results support the significant relation between RMR and FFW (r = .57; p < .01). The lower order correlation between FFW and RMR relative to other studies (Cunningham, 1980; Ravussin et al., 1986) is probably reflective of the homogeneity of our subjects with respect to FFW. RMR was lower in older men when differences in percent body fat and FFW were taken into account using covariance analysis (Table 2). These findings support those of Fukagawa et al. (1990), who also found that differences in fat-free weight cannot fully account for the lower RMR in older persons. The age effect was strongly influenced by the lower RMR in sedentary older men who displayed a ~ 11 % and — 17% lower RMR relative to physically active older men and younger men, respectively. No differences in adjusted RMR were noted between sedentary and younger active men. The higher RMR in active older men relative to sedentary older men suggests that regular participation in aerobic exercise may attenuate the age-related decline in RMR. Previous authors who have examined the effects of aging on RMR have not considered the level of physical activity as a factor influencing metabolic rate (Keys et al., 1973; Shock et al., 1963; Tzankoff and Norris, 1977, 1978). The etiology of the lower RMR in sedentary older men cannot be determined from the present study. With advancing age, skeletal muscle occupies an increasingly smaller percentage of FFW (Cohn et al., 1980). Thus despite a similar quantity of FFW relative to the other groups, the skeletal mass component may be reduced in sedentary older men and contribute to the lower RMR. This implies, on the other hand, that regular physical exercise may attenuate the loss of skeletal mass in older men, as evidenced by the higher RMR in active older men. These results need to be confirmed with a larger sample size using measures of body composition that more accurately discriminate between skeletal muscle and nonmuscle compartments in younger and older individuals.
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