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Original Studies |
Human Cardiovascular Research Laboratory, Center for Physical Activity, Disease Prevention, and Aging, Department of Kinesiology (R.E.V.P., P.P.J., K.P.D., C.A.D., H.T., D.R.S.), University of Colorado, Boulder, Colorado 80309; and the Department of Medicine, Divisions of Cardiology and Geriatric Medicine (D.R.S.), and the Department of Pediatrics, Center for Human Nutrition (B.M.D.), University of Colorado Health Sciences Center, Denver, Colorado 80262
Address all correspondence and requests for reprints to: Douglas R. Seals, Ph.D., Department of Kinesiology, University of Colorado, Campus Box 354, Boulder, Colorado 80309. E-mail: seals{at}spot.colorado.edu
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Abstract |
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10% lower in the
postmenopausal vs. premenopausal sedentary women (52 ±
2 vs. 57 ± 2 Cal/h; P < 0.002).
In contrast, RMRadj was not significantly different in the
premenopausal (59 ± 2 Cal/h) and postmenopausal (57 ± 1
Cal/h) distance runners. The postmenopausal swimmers had a
RMRadj (57 ± 2 Cal/h) identical to that of the
postmenopausal runners, suggesting a generalized influence of the
endurance exercise-trained state in postmenopausal women. Group
differences in RMRadj were not associated with differences
in total energy intake or composition or with plasma concentrations of
norepinephrine, T3, or T4. However, maximal
oxygen consumption (aerobic fitness) accounted for 35% of the
individual variance in RMRadj in the overall population
(r = 0.59; P < 0.001). Our results are
consistent with the concept that the age-related decline in RMR in
sedentary women is not observed in women who regularly perform
endurance exercise. The elevated level of RMR observed in middle-aged
and older exercising women may play a role in their lower levels of
body weight and fatness compared to those in sedentary women. |
Introduction |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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60–75% of daily
energy expenditure (7), decreases with age in women (8, 9) and is
thought to play an important role in the age-associated increases in
body weight and fatness. The fact that individuals with low RMR are at
greater risk for future weight gain than those with high RMR (10) is
consistent with this concept. Compared with that observed in sedentary women, the age-related increases in body weight and in total and regional body fatness are smaller or even absent in women who exercise regularly (11, 12, 13, 14). This could be due in part to their high physical activity-related energy expenditure. Additionally, the smaller age-associated increases in body mass and fat mass in highly active women could be related to a maintenance of RMR with advancing age. There is some evidence for this in men (15). Accordingly, the aim of the present investigation was to test the hypothesis that RMR declines with age in sedentary women, but not in women who perform regular endurance-type exercise.
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Subjects and Methods |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Sixty-five healthy women, aged 21–35 or 50–72 yr, were studied: 12 premenopausal and 15 postmenopausal sedentary women, 13 premenopausal and 15 postmenopausal distance runners, and 10 endurance-trained postmenopausal swimmers. The swimmers were included to establish that a higher RMR in postmenopausal runners vs. sedentary women, if observed, was related to endurance training in general (i.e. was not specific to runners).
The pre- and postmenopausal runners were matched for age-adjusted competitive performance (both groups, 74 ± 2% of age-adjusted world record times) as described previously by our laboratory (16), ran 54 ± 5 and 43 ± 3 km/week, and had been training for 9 ± 1 and 18 ± 2 yr, respectively.
The swimmers were matched to 10 postmenopausal runners for years postmenopausal (8 ± 1 yr both groups), hormone replacement use (5/group), hours of exercise per week (3.7 ± 0.5 vs. 4.2 ± 0.3 h), and relative age-adjusted competitive performance (79 ± 5% vs. 77 ± 5%). The sedentary subjects performed no regular physical activity. All subjects had been weight stable (±2 kg) during the previous 6 months.
All of the postmenopausal women were at least 2 yr postmenopausal (individual subject range, 2 to 23 yr; mean group range, 8–11 yr), and approximately half of each group were taking estrogen-based hormone supplements (eight sedentary, eight runners, and five swimmers). All premenopausal subjects were eumenorrheic, as assessed by self-report of menstrual cycles, and none was taking oral contraceptives. The range of menstrual cycle length was 21–37 days (mean cycle length, 28 days). All subjects were healthy, as assessed by medical history. Postmenopausal subjects were further evaluated for clinical evidence of cardiopulmonary disease with a physical examination and electrocardiograms during rest and maximal exercise. No subjects reported using any other medications. All subjects were nonsmokers.
The nature, purpose, and risks of the study were explained to each subject before written informed consent was obtained. The experimental protocol was approved by the human research committee at the University of Colorado-Boulder.
Body mass and composition
Total body mass was measured to the nearest 0.1 kg on a physician’s balance scale (Detecto, Webb City, MO). Body mass index (BMI) was calculated from weight and height (kg/m2). Total body density was determined by hydrodensitometry as outlined by Brozek et al. (17). Residual volume of the lungs was measured using a nitrogen dilution technique as previously outlined by Wilmore (18). Body fat percentage was then calculated using the equation of Brozek et al. (17). Fat mass and fat-free mass were estimated from the percent fat and body mass based on the two-compartmental model. The waist to hip ratio, a measure of abdominal adiposity, was determined from waist circumference, measured at the narrowest part of the torso, and hip circumference, measured at the maximal extension of the buttocks (19).
RMR
Subjects were studied after a 12-h overnight fast. RMR was
measured in the runners and swimmers 24 h after their last exercise
session. All premenopausal women were tested during the follicular
phase (days 1–10) of their menstrual cycle. Measurements were
performed between 0600–0900 h in a dimly lit room at a comfortable
temperature (23 C). Subjects remained awake in a semirecumbent
position. After a 15-min habituation period in the hood, oxygen
consumption and carbon dioxide production were measured each minute for
30 min by indirect calorimetry using a ventilated hood system
(DeltaTrac Metabolic Monitor, SensorMedics Corp., Yorba Linda, CA). RMR
was then calculated from the average of the 30 min using the Weir
formula (20). The reliability of this method was established in our
laboratory before the study by testing pilot subjects on 2 consecutive
days (n = 5). The intraclass correlation was 0.99, with a
difference of 3.5% between trials.
Aerobic fitness
Maximal oxygen consumption (VO2max) was used as a measure of aerobic fitness and was determined using an on-line computer-assisted open circuit spirometry system as previously described (16).
Estimated energy intake
Energy intake was determined from 4-day food diaries recorded for 4 consecutive days, including 3 weekdays and 1 weekend day. Each subject weighed (Dayton Hudson diet scale, 8-oz capacity) and recorded all food and beverages consumed. Three-day practice records were completed by each subject before the 4-day records, and a registered dietitian instructed each on ways to improve the accuracy of their diaries. A registered dietitian analyzed all diets for energy and macronutrient intake using the Nutritionist IV (version 3.5.2, The Hearst Corp., San Bruno, CA) computer software program.
Plasma norepinephrine and thyroid hormone concentrations
All subjects were studied at 0730 h after a 12-h fast. Blood samples were taken after subjects had rested in the supine position for 20 min. Plasma norepinephrine (NE) levels were determined by radioenzymatic assay from an antecubital venous blood sample (21). Plasma total T4 and total T3 concentrations were measured using competitive binding RIAs (22, 23).
Statistics
Group differences for most variables were determined by ANOVA. Group differences in RMR were determined by analysis of covariance, with fat mass and fat-free mass as the two covariates; the adjusted means (RMRadj) and SEs are presented. A Newman-Keuls post-hoc test for multiple comparisons was used to analyze differences among the dependent variables. When a significant interaction was not observed, specific mean comparisons were performed on the main effects. Zero order correlations were performed to determine relations between variables in the overall study population. To identify significant independent predictors of RMRadj, stepwise multiple regression analysis also was performed. Adjusted maximal oxygen consumption values (VO2maxadj), covaried for fat mass and fat-free mass, were used in correlational analyses. Because RMR did not differ between users and nonusers of hormone replacement within and across groups, subjects were pooled for all analyses. The level of statistical significance was set at P < 0.05.
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Results |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Table 1
presents selected
characteristics of the sedentary women. The postmenopausal women had
higher levels of body mass, BMI, total body fatness, and waist to hip
ratio and lower maximal oxygen consumption than the premenopausal women
(P < 0.05). Fat-free mass did not differ with age.
RMRadj was 10% lower in the postmenopausal compared
with the premenopausal women (52 ± 2 vs. 57 ± 2
Cal/h; P = 0.001; Fig. 1A). Based on analysis of diet records,
there were no significant differences in absolute carbohydrate, fat,
protein, or total estimated energy intake in the premenopausal
vs. postmenopausal women, although the postmenopausal women
had lower carbohydrate and protein intakes when expressed per kg body
mass (BM) (Table 2). Plasma
concentrations of norepinephrine, T3, and T4
also were not different in the two groups (Table 3).
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Subject characteristics for the runners are presented in Table 1
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The postmenopausal runners demonstrated higher levels of body mass and
fatness and lower maximal oxygen consumption than the premenopausal
controls (P < 0.05). Fat-free mass, BMI, and waist to
hip ratio were not different between the groups. In contrast to the
age-related difference in RMRadj observed in the sedentary
women, RMRadj was not different in the pre- and
postmenopausal runners (59 ± 2 vs. 57 ± 1 Cal/h;
Fig. 1B). Estimated absolute energy intake and composition also did not
differ with age, although the postmenopausal women had lower
carbohydrate and protein intakes when normalized per kg BM (Table 2).
No differences were observed in plasma norepinephrine, T3,
and T4 levels between the groups (Table 3).
Postmenopausal swimmers vs. runners
Table 4 presents characteristics for
the postmenopausal swimmers and the matched subgroup of postmenopausal
runners. The two groups did not differ in age, hormone replacement use,
fat-free mass, hours of exercise per week (either specific training or
other exercise), or relative performance. The swimmers demonstrated a
higher body mass, BMI, body fatness, and waist to hip ratio and lower
maximal oxygen consumption than the runners (P <
0.05). RMRadj was identical in the postmenopausal runners
and swimmers (57 ± 2 vs. 57 ± 2 Cal/h; Fig. 1C).
No group differences were observed in estimated energy intake and
composition or in plasma levels of norepinephrine, T3, or
T4.
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Significant univariate correlates of RMRadj in the
overall subject population included: VO2maxadj
(r = 0.59; P < 0.001; Fig. 2), total energy intake (r = 0.48;
P < 0.001), carbohydrate intake (r = 0.50;
P < 0.001), protein intake (r = 0.27;
P < 0.05), and training hours per week (r = 0.29;
P < 0.05). Of these variables,
VO2maxadj entered the stepwise multiple
regression analysis first and accounted for 35% of the overall
variance (P < 0.001); total energy intake was the only
other variable to enter and accounted for an additional 6% of the
variance (P < 0.05).
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Discussion |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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The differences in RMRadj observed with age in the sedentary and active women in the present study, when viewed over time, may have considerable physiological significance. Using the mean RMRadj values in calories per h for the pre- and postmenopausal women, the net age-related decline in energy expenditure would be approximately 600 Cal/week more in the sedentary compared to the exercising women. Thus, this age-related difference in energy expenditure, if uncompensated completely by a decrease in energy intake, would equate to about a 4 kg/yr greater increase in body weight in the sedentary women.
Given this, our findings may have important clinical implications. For example, body weight and fatness increase with age in women (24, 25, 26), and recent evidence indicates that even modest weight gain in women with advancing age is associated with markedly increased risks of noninsulin-dependent diabetes mellitus (27), coronary artery disease (28), and overall mortality (29, 30). We (13, 14) and others (11, 12) have shown that the age-related increases in body weight and body fatness are either smaller or absent in endurance exercise-trained compared to sedentary women. Because RMR accounts for 60–75% of daily energy expenditure and is a risk factor for future body weight gain (10), the higher RMR observed in our exercising postmenopausal women could play a role in their ability to maintain a more favorable body weight and composition with age. Moreover, meeting nutritional requirements is a problem for some older women (31). In this context, the higher RMR in physically active postmenopausal women would allow them to maintain a higher total energy intake and, therefore, have a greater likelihood of meeting their dietary needs.
Several factors not directly related to exercise have been reported to be associated with RMR in certain populations or conditions, including thyroid hormones (32, 33), total energy and macronutrient intake (34), and sympathetic nervous system activity (35, 36). In the present study, however, there was no consistent relation between RMR and any of these putative mechanisms.
Fat-free mass and fat mass are important determinants of RMR (7, 8, 33). However, we found that RMR declined with age in the sedentary, but not in the physically active, women after adjusting for these factors. Thus, our findings suggest that RMR per unit of metabolically active tissue is higher in exercise-trained vs. sedentary postmenopausal women.
In the present study, RMRadj and aerobic fitness (VO2maxadj) were positively related in the overall population (r = 0.59) as well as in the various subpopulations (r = 0.51–0.76). Aerobic fitness also was the strongest independent predictor of RMRadj, explaining 35% of the overall variance. A significant relationship between VO2max and RMR across the adult age range has been found previously in active and sedentary men (37, 38), but not in sedentary women (33). Our results indicate that aerobic fitness is significantly related to RMR among healthy females varying in age and exercise status.
We should emphasize at least three limitations of the present study. First, using a model that we have employed in the past (13, 16), we attempted to minimize constitutional differences between the pre- and postmenopausal endurance runners by matching them for age-adjusted performance. Despite this, however, because of the cross-sectional nature of our study design we cannot discount the possibility that genetic or constitutional factors influenced our findings. Secondly, it is unknown whether RMR declines significantly in endurance-trained women beyond the age range studied (i.e. beyond 72 yr of age) or at what point RMR begins to decline during the perimenopausal years (i.e. between 35–50 yr of age) in sedentary women. Lastly, we compared groups who were very different in their activity levels (i.e. sedentary and endurance-trained subjects). Thus, our results do not address the question of the minimum level of habitual exercise that is associated with a diminished age-related decline in RMR.
In conclusion, the results of the present study provide experimental evidence that is consistent with the concept that the age-related decline in RMR in sedentary women is not observed in women who regularly perform endurance exercise. The absence of a significant decline in RMR in middle-aged and older endurance-trained women may play a role in the maintenance of their lower levels of body weight and fatness compared to those in sedentary women.
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Acknowledgments |
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Footnotes |
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Received March 26, 1997.
Revised June 20, 1997.
Accepted June 27, 1997.
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References |
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