resting metabolic rate is lower in women than in men · man. resting metabolic rate is lower in...

Resting metabolic rate is lower in women than in men

PAUL J. ARCIERO, MICHAEL I. GORAN, AND ERIC T. POEHLMAN Baltimore Veterans Affairs Medical Center, Division of Gerontology and Geriatric Research Education and Clinical Center, University of Maryland, Baltimore, Maryland 21201; and Division of Endocrinology, Metabolism, and Nutrition, Department of Medicine, College of Medicine, University of Vermont, Burlington, Vermont 05405

ARCIERO,PAUL J., MICHAEL I. GORAN,ANDERIC T. POEHL- MAN. Resting metabolic rate is lower in women than in men. J. Appl. Physiol. 75(6): 2514-2520, 1993.-This study examined gender differences in resting metabolic rate (RMR) across a broad age spectrum after controlling for differences in body composition and aerobic fitness. Three hundred twenty-eight healthy men (17-80 yr) and 194 women (W-81 yr) volunteers were characterized for RMR, body composition, physical activity, peak oxygen consumption (peak VO,), anthropometrics, and energy intake. Measured RMR was 23% higher (P -c 0.01) in men (1,740 & 194 kcal/day) than in women (1,348 t 125 kcal/day). Multiple regression analysis showed that 84% of individual variation in RMR was explained by fat-free mass, fat mass, peak VO,, and gender. After controlling for differences in fat-free mass, fat mass, and peak VO,, a lower RMR (3%; P < 0.01) persisted in women (1,563 t 153 kcal/day) compared with men (1,613 t 127 kcal/day). Adjusted RMR in premenopausal (P < 0.01) and postmenopausal (P < 0.05) women was lower than in men of a similar age. Our results support a lower RMR in women than in men that is independent of differences in body composition and aerobic fitness.

gender; fat-free mass; peak oxygen consumption; fat mass

RESTING METABOLIC RATE (RMR) accounts for the largest component (60-75%) of total daily energy expenditure (13) and therefore plays a significant role in the regulation of energy balance. A low RMR has been shown to be a significant predictor for subsequent weight gain in Southwestern American Indians (30), which underscores its important role in the regulation of body energy re- serves.

To our knowledge, it is unknown whether gender influences RMR. Men generally display a higher absolute RMR than women because of their larger quantity of fat-free mass. The question of interest, however, is whether RMR is different in men and women independent of differences in body composition.

Although several studies have examined potential gender differences in RMR, they have been limited by small sample sizes (3, 11, 16, 18, 20, 29, 34). A recent study by Ferraro et al. (9) in 114 men and 121 women, however, did find that 24-h sedentary energy expenditure, but not RMR, was lower in the women than in the men after adjusting for differences in body composition. The primary purpose of this study was to retrospectively analyze data to examine gender differences in RMR in a large cohort of healthy men and women spanning a broad range of age, body mass, aerobic fitness, and adiposity. A

secondary goal was to compare RMR in pre- and postmenopausal women with men of a similar age to examine the possibility that menopausal status influences gender-related differences in RMR.

MATERIALS AND METHODS

Subjects

Three hundred twenty-eight healthy men (17-80 yr) and 194 healthy women (18-81 yr) were examined in this study. Some of the data from this cohort have been previously published (22, 24), although gender differences in RMR have not been examined. Subjects were excluded from participation in the study for the following reasons: 1) clinical evidence of coronary heart disease (e.g., ST segment depression >l mm at rest or exercise) or cardio- myopathy, 2) hypertension (resting blood pressure >140/90 mmHg), 3) medications that could affect cardiovascular function or metabolic rate, 4) medical history of diabetes, 5) instability of body weight during the preced- ing year (a change of >2 kg), 6) exercise-limiting noncar- disc disease (arthritis, peripheral vascular disease, cere- bral vascular disease), or 7) history of oophorectomy. Menopausal status for each female volunteer was determined by questionnaire and was assigned a dummy value based on three levels (1 = premenopausal, 2 = perimenopausal, 3 = postmenopausal) as previously performed (1, 24). No women were presently taking estrogen replace- ment therapy. All premenopausal women were tested between days 5-12 during the follicular phase to standard- ize measurements during the same phase of the menstrual cycle. Menstrual status was not determined by chemical analysis. The experimental procedures used in this study were approved by the Committee on Human Research for the Medical Sciences at the University of Vermont. Written informed consent was obtained from each subject before investigation.

Outline of Experimental Protocol

All volunteers were admitted to the Clinical Research Center the afternoon before their metabolic testing between 1400 and 1600 h. Subjects were fed a standardized l,OOO-kcal mixed meal (15% protein, 30% fat, 55% carbo- hydrate) at -1730 h and thereafter were given practice with the ventilated hood to reduce any concern or appre- hension with testing conditions. After a 12-h overnight fast in which volunteers slept in the Clinical Research Center, the following tests were performed the next

2514 0161-7567/93 $2.00 Copyright 0 1993 the American Physiological Society

RESTING METABOLIC RATE IN MEN AND WOMEN 2515

morning in sequence: RMR, underwater weighing for body composition determination, anthropometrics, and test of peak oxygen consumption (peak Oo,). These methods, as well as their reproducibility in our laboratory, have been previously described (23). However, because the data were collected over several years, updated values for the reproducibility of the major outcome variables are presented.

Subject Characterization

RMR was established for each subject by indirect calorimetry for 45 min using the ventilated hood technique. If volunteers regularly participated in exercise, metabolic tests were performed 36-48 h after the last exercise bout. RMR was measured in the same room in which the subjects slept. Recent work from our laboratory has shown that outpatient measurements of RMR are 8% higher when compared with measurements performed under inpatient conditions (4). Thus, to obtain the lowest RMR value in normal volunteers, inpatient measurement procedures are preferred. The intraclass correlation and co- efficient of variation (CV) for RMR determined using test-retest in 17 male volunteers was 0.90 and 4.3%, re- spectively, in our laboratory performed in volunteers between 1988 and 1990. These values compare favorably with recent test-retest data in eight older male volunteers, yielding an intraclass correlation of 0.91 and a CV of 3.9% recently obtained in our laboratory.

Body fat was estimated from b by underwater weighing, with

OdY density as measured ultaneous measure-

ment of residual lung volume by the helium dilution method using the formula of Siri (32). Fat-free mass was estimated as total body weight minus fat weight. Pre- vious reproducibility measures for the estimation of per- cent body fat reached 0.98, and the CV was 4.9% (25). Recent test-retest conditi .ons of six older female volu n- teers yi .elded an intraclass car relation of 0.94 and a CV of 4.1%. Fat distribution was estimated from the ratio of the waist and hip circumference.

The energy cost of leisure time physical activity within the past year was assessed in a structured interview using the Minnesota Leisure Time Physical Activity Question- naire (33). Peak Voz was measured by a progressive and continuous treadmill test to volitional fatigue in all 522 volunteers. The highest 00, for 1 min during the test was recorded as the peak VO,. Earlier (1988-1990) test-retest conditions for peak VO, in men (n = 25) yielded an intraclass correlation of 0.94 and a CV of 3.8% in our laboratory (25). More recent test-retest data in seven older men yielded an intraclass correlation of 0.95 and a CV of 3.9%. Energy and macronutrient intakes were estimated from 3-day (2 weekdays and 1 weekend day) food diaries (21). However, it is likely that individuals underreported their true energy intake, as previously shown in our (13) and other (15) laboratories.

Statistical Analysis

Means, SDS, and ranges for each v pariable were calcu- lated. Differences between men and women for the de-

TABLE 1. Physical characteristics in total group of men and women

Men Women (n = 328) P (n = 194)

Age, Yr 42.0t19.2 NS 45.0t16.9 (17-80) (18-81)

Height, cm 177.0t7.1 <O.Ol 163.8t6.6 (162-200) (146-182)

Weight, kg 77.6tll.l <O.Ol 61.9t8.6 (55.9-122.5) (45.4-106.5)

Body mass index, kg/m2 24.823.2 <O.Ol 23.lk3.0 (18.2-37.9) (17.5-37.4)

Body fat, % 15.9k7.3 co.01 24.6t7.7 (2.3-39.4) (8.4-47.6)

Fat-free mass, kg 64.8~18.2 co.01 46.3t5.4 (48.4-98.3) (35.1-66.0)

Fat mass, kg 12.7t7.3 <O.Ol 15.626.5 (1.7-47.3) (4.9-50.7)

Waist-to-hip ratio 0.89t0.06 <O.Ol 0.7720.07 (0.78-1.07) (0.57-1.28)

Leisure time activity, kcal/day 434t241 <O.Ol 36lt231 (loo-1,517) (77-1,278)

Peak VO,, llmin 3.50t0.94 <O.Ol 2.20t0.62 (1.3-6.1) (1.0-4.0)

Self-reported energy intake, kcallday 2,808+801 <O.Ol 1,830+455

(1,144-7,019) (994-3,376)

Values are means ~fr SD; ranges given in parentheses. Peak i702, peak oxygen consumption; body composition was estimated from hydrodensitometry; leisure time activity was assessed from a structured interview; self-reported energy intake was estimated from a 3day food diary.

pendent variables were determined by an independent t test. Pearson product-moment correlation coefficients were used to assess the degree of association between pairs of variables. Stepwise multiple regression analysis using all measured variables was applied to the total group of men and women volunteers to determine the variables contributing to the variation in RMR.

After the independent factors that contribute to variation in RMR were determined, analysis of covariance was employed to test for differences in the adjusted means of RMR between men and women. The parallelism of the regression lines between men and women using fat-free mass, fat mass, peak VO,,~and body fat distribution as covariates were compared by a test of homogeneity of slopes, and no violations were noted.

The influence of menopausal status on gender-related differences in RMR was analyzed by subdividing women into premenopausal and postmenopausal subsets. Briefly, all premenopausal women (n = 105) were assigned a dummy value of 1, which corresponded to women 147 yr, whereas postmenopausal women (n = 75) were given a value of 3, which corresponded to women >48 yr. There- after, the cutoff age points for women were applied to the men so that appropriate age-matched comparisons between men and women could be made. Perimenopausal women (n = 14) were excluded from this subanalysis.

RESULTS

Total Group

Subject characteristics. Table 1 shows differences in the physical characteristics of the total group of men and

2516 RESTING METABOLIC RATE IN MEN AND WOMEN

TABLE 2. Pearson product correlation coefficients of men, women, and total group

Resting Metabolic Rate

Men Women Total group (n = 328) (n = 194) (n = 522)

Fat-free mass, kg 0.74* 0.90* 0.90* Peak 60,, llmin 0.66* 0.55* 0.79* Weight, kg 0.57* 0.54" 0.74* Energy intake, kcal/day 0.31* 0.27* 0.5F Waist-to-hip ratio -0.08 0.07 0.46* Age, Yr -0.40* -0.35* -0.31* Leisure time activity, kcal/day 0.20* 0.22* 0.24* Fat mass, kg 0.03 -0.02 -0.13*

Fat-free mass and fat mass were estimated from hydrodensitometry; resting metabolic rate was measured from indirect calorimetry. *P < 0.01.

women. These volunteers represent a wide range of age, body composition, peak VO,, physical activity level, and energy intake. There was no age difference between the men and women volunteers. Body weight was 20% greater in men than in women, primarily due to a greater quantity of fat-free mass. Women were 19% fatter (P < 0.01) and 17% less physically active in their leisure time as measured from a physical activity questionnaire (P < 0.01). Men displayed a 37% higher absolute peak VO, (P < 0.01) than women. Women reported an energy intake of -1,000 kcal/day less than men (P < 0.01).

RMR. Table 2 displays the Pearson product-moment correlation coefficients among the physical characteristics and metabolic variables with measured RMR in the total group and when separated by gender. In general, the magnitude of association between RMR and the independent variables is similar in both the sexes. As expected, fat-free mass was the highest correlate with RMR in the total group of 522 volunteers. Figure 1 shows the significant linear relationship between RMR and fat- free mass in the total group.

Stepwise regression analysis was performed to determine which factor(s) explains significant amounts of variation in RMR. In the total data set, variation in RMR was best explained by four variables: fat-free mass (? = 81%; P < O.Ol), peak vo2 (partial ? = 2%; P < 0.05), fat mass (partial 1-2 = 0.05%; P < 0.05), and gender (partial ? = 0.05%; P < 0.05). The regression equation to predict RMR in our total cohort of men and women is as follows: RMR (kcal/day) = 13.7 (fat-free mass, kg) + 3.3 (fat mass, kg) + 74 (peak VO,, l/min) - 50 (gender; 0 = men, 1 = women) + 596 (? = 0.84, P < 0.01, standard error of the estimate = 106.5 kcal/day).

Adjusted RMR. Figure 2 shows the results of analysis of covariance that was performed on the total group (n = 522) using gender as the grouping variable. Figure 2 shows the comparison between men and women for the absolute measured RMR and the adjusted RMR values after controlling. for differences in fat-free mass, fat mass, and peak VO,. The rationale for using these variables as covariates were their identification as independent factors that accounted for a significant amount of variation in RMR.

As expected, men showed a 23% higher measured

RMRthanwomen (Fig. 2A; 1,740 t 199vs.1,348 t 125 kcal/day; P < 0.01). A 3% higher adjusted RMR (1,613 t 127 vs. 1,563 t 153 kcal/day; P < 0.01) persisted in men after controlling for differences in fat-free mass, fat mass, and peak VO, (Fig. 2B). There was no difference in fasting respiratory quotient between men (0.810 t 0.046) and women (0.816 t 0.044) (P > 0.05).

Subset Analysis

A subset analysis was performed to examine whether gender differences in RMR persisted in pre- and postmenopausal women when compared with a group of men of similar age. In the subset analysis, premenopausal women showed a 24% lower measured RMR compared with younger men (1,377 t 115 vs. 1,811 t 198 kcal/day; P < 0.01; Fig. 3A). A 4% lower adjusted RMR persisted in the premenopausal women compared with the group of men (1,618 t 143 vs. 1,681 t 125 kcal/day; P < 0.01; Fig. 3B, Table 3). Similarly, the postmenopausal women exhibited a 21% lower measured RMR (1,291 t 106 kcal/day for women vs. 1,638 t 171 kcal/day for men; P < 0.01; Fig. 3C) and a 5% lower adjusted RMR (1,469 t 199 kcal/day for women vs. 1,539 t 174 kcal/day for men; P < 0.05; Fig. 30, Table 3) than their male coun- terparts. There were no differences in RMR between the pre- and postmenopausal women after adjusting for differences in body composition and peak VO, (1,348 t 61 vs. 1,344 t 69 kcal/day; P = 0.74). Thus, the lower RMR in women persisted throughout the age range in this study.

DISCUSSION

The purpose of this study was to examine differences in RMR between men and women after controlling for differences in body composition and aerobic fitness level. The major findings of this study are that 1) RMR is 3% lower (50 kcal/day) in women than in men after differences in body composition and peak VO, are taken into account and 2) a lower RMR was found in both premenopausal and postmenopausal women when compared with men of similar ages.

As expected, measured RMR was 23% higher in men than in women. This difference can be explained primarily by the larger quantity of fat-free mass in the men compared with the women (Table 1, Fig. 1). Our laboratory (22, 24) and others (9, 29) have consistently shown that fat-free mass accounts for the greatest source of variation in RMR in humans. Furthermore, the slope (20.3 t 0.4 kcal/day) and y-intercept (418 t 26 kcal/day) of our regression equation of RMR and fat-free mass (Fig. 1) compares favorably with those of others (5,6,8, 17, 19, 28).

The present study found that the quantity of fat mass and the aerobic fitness level of the individual were also important factors in explaining additional variation in RMR independent of fat-free mass. The independent contribution of fat mass is in agreement with previous work from our laboratory (22) and others (9,12,16) but


2500

RMR (kcal/d) = 418 + 20.3 (FFM) v 4 2 /

r = 0.81 0 /

0

1000

3; 6-b 9; Fat-free mass (kg)

. 1 in contrast with yet others (29). Furthermore, this study confirms our previous work that showed that aerobic fitness (peak VO,) is an additional independent factor explaining variation in RMR (22).

FIG. 1. Linear relationship between resting metabolic rate (RMR) and fat- free mass in 522 healthy men and women (17-81 yr). Fat-free mass was determined by underwater weighing, and RMR was measured by indirect calorimetry using ventilated hood system. P < 0.01; standard error of estimate = 115 kcallday.

v

0

males (

females

t-1=328)

(n=19 4)

110

The question of interest, however, is whether RMR is different between men and women independent of differences in body composition and cardiovascular fitness. In our large data set, women showed a 3% lower adjusted RMR compared with men after controlling for differences in body composition and peak 00,. Because this is the largest study (n = 522) to date that has examined gender differences in RMR across a broad age range (18- 81 yr), it is likely that we could detect small, but biologi- cally meaningful, differences in RMR that otherwise might have been ignored in studies using smaller sample sizes. We performed a power analysis and found that 102 males and 102 females are needed to detect the 50-kcal/ day (3%) difference at an alpha error of 0.05 and statistical power of 80%. Previous investigations (3, 11, 16, 18, 20, 29, 34), using smaller sample sizes, have not found gender differences in RMR. Because the seven afore- mentioned studies did not test large numbers of subjects (range of n = lo-177), it is possible that a type II error contributed to the absence of small, but important, gender differences in RMR.

The question of interest is whether a difference of 50 kcal/day has significant clinical implications in the long- term regulation of energy balance. Because of the large contribution of RMR to total daily energy expenditure (13), it is possible that small gender-related differences may have a significant long-term effect on the regulation

of body weight and composition. For example, Ravussin et al. (30) showed that a lower adjusted RMR of 71 kcal/ day in a group of 15 subjects resulted in a weight gain of >lO kg over a 4-yr time span. It is interesting to note that our observed gender difference of 50 kcal/day approxi- mates that found in the individuals that subsequently gained weight in the study by Ravussin et al. However, because our data are cross sectional and not prospective, we cannot address the issue of subsequent gain in body weight and adipose tissue stores in our female population.

Recently, Ferraro et al. (9) found a 44-kcal/day lower adjusted RMR in females after data were normalized for fat-free mass, fat mass, and age. However, the difference in RMR in the Ferraro et al. study was not significant despite a large sample size (n = 235). Although these findings may appear inconsistent with our power analysis, the variation (SE = 49 kcal/day) of the adjusted RMR value was actually larger than the mean RMR value (44 kcal/day) in the work of Ferraro et al. The large variation in RMR measurement may reflect their rela- tively short measurement period (9-15 min) compared with that of the present study (45 min). The study of Cunningham (6) also failed to detect a gender-related difference despite a large sample size (n = 233). However, the data were obtained from the work of Harris and Ben- edict (14), which has since been found to significantly overestimate (7, 17) and underestimate (2, 10,ZO) RMR in today’s current populations. Furthermore, in the study of Cunningham, lean body mass was estimated from a prediction equation and not directly measured.

2518

2000

s : a 0 r 1000 a > a

500

0

RESTING METABOLIC RATE IN MEN AND WOMEN

T (PcO.01)

I

MEASURED RMR ADJUSTED RMR A B

Because previous studies (1,9) have shown that menopausal status influences RMR, we divided our female population into two subsets based on menopausal status to compare pre- and postmenopausal women with men of similar ages. As expected, measured RMR was lower in the women in both groups compared with the men. How-

Although this investigation cannot elucidate the mech- anism(s) for the lower RMR in women compared with men, several possibilities should be considered. Na+- K+-ATPase activity has been shown to be reduced in

ever, the lower adjusted RMR in pre- and postmeno- women compared with men (31 ), and we h .ave recently pausal women persisted even after normalizing for body reported that a lower Na+-K+ activity is related to a composition and fitness. In addition, there were no dif- lower RMR, independent of difference& fat-free weight ferences in RMR between pre- and postmenopausal (26). Our laboratory has previously shown that a re- women after adjustments for differences in body compo- strained eating pattern in females was a significant fac- sition and physical fitness were taken into account. Col- tor contributing to a reduced RMR and higher levels of lectively, these findings confirm that the lower RMR in body fat (27). Differences in skeletal muscle metabolism women compared with men is independent of meno- may also be implicated in gender-related differences in

2250

$1500 x

a > 1250 a

1000

750

500

FIG. 2. Difference in RMR between men and women for total group (n = 522). A: measured RMR for men [1,740 t 199 (SD) kcal/day] vs. women (1,348 & 125 kcal/day). B: adjusted RMR values after controlling for fat-free mass, fat m-ass, and peak oxygen consumption (VO,) for men (1,613 t 127 kcal/day) vs. women (1,563 t 153 kcal/

day).

pausal status and body composition and persists throughout a large age range.

‘PcO.01) (P<

FIG. 3. A: difference in measured 0.05) RMR between men [l&311 k 198 (SD)

kcal/day] and premenopausal women of similar age (1,377 & 115 kcal/day) (n = 299). B: adjusted RMR after statistical adjustment for fat-free mass, fat mass, and peak VO, in younger men (1,681 * 125 kcal/day) vs. women (1,618 t 143 kcallday) (n = 299). C: difference in measured RMR between older men (1,638 -t 171 kcal/day) and postmenopausal women of similar age (1,291 t 106 kcal/day) (n = 209). D: RMR after

’ statistical adjustment for fat-free mass, fat mass, and peak VO, in older men (1,539 t 174 kcal/day) vs. women (1,469 t 199 kcal/day) (n = 209).

MEASURED ADJUSTED MEASURED ADJUSTED

A B C D


TABLE 3. Comparison of adjusted resting metabolic rate

Total group 522 1,613&127 -co.01 1,563+153 Younger group 299 1,681+125 <O.Ol 1,618+143 Older group 209 1,539+174 -co.05 1,469&199

Values are adjusted means t SD of resting metabolic rate in kcal/ day. Adjusted resting metabolic rate refers to resting metabolic rate values after controlling for differences in body composition and peak VO, between men and women volunteers using analysis of covariance. Younger group was comprised of premenopausal women (147 yr), and older group was comprised of postmenopausal women (248 yr). Cutoff age points for women were applied to men to allow for appropriate comparisons.

RMR, although previous findings do not support a gender effect when adjustments were made for skeletal muscle mass (35).

It is important to point out several aspects of our study that reinforce the validity of our findings. These procedures include 1) the measurement of RMR on an inpatient basis removed at least 48 h from the last bout of exercise, 2) the standardization of measurement procedures during the follicular phase of the menstrual cycle, 3) the habituation of all subjects to the ventilated hood, and 4) a large sample size of well-characterized healthy individuals.

We conclude that women have a lower metabolic rate than men, which does not appear to be explained by differences in body composition, fitness level, menopausal status, or age. A lower RMR in women for their metabolic size represents a gender-specific difference in resting energy expenditure.

We thank all the volunteers who participated in this study. We also thank Phil Ades, the Cardiac Rehabilitation staff, Shane Katzman- Rooks, Dr. Andrew Gardner, and the General Clinical Research Center staff for their assistance.

E. T. Poehlman is supported by National Institute of Aging Grant AG-07857, National Institute of Aging Research Career and Develop- ment Award K04-AG-00564, the American Association of Retired Per- sons Andrus Foundation, and a Biomedical Research Grant from the University of Vermont. M. I. Goran is supported by a grant from Ameri- can Diabetes Association, the National Institute of Child Health and Human Development, and US Department of Agriculture. This work was supported in part by General Clinical Research Center Grant RR- 109.

Address for reprint requests: E. T. Poehlman, Baltimore Veterans Affairs Medical Center, Division of Gerontology/GRECC, Univ. of Maryland, Baltimore, MD 21201.

Received 1 June 1993; accepted in final form 20 July 1993.

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2. ARCIERO, P. J., M. I. GORAN, A. W. GARDNER, P. A. ADES, R. S. TYZBIR, AND E. T. POEHLMAN. A practical equation to predict resting metabolic rate in older males. Metabolism 42: 950-957, 1993.

3. ASTRUP, A., G. THORBEK, J. LIND, AND B. ISAKSSON. Prediction of 24-h energy expenditure and its components from physical characteristics and body composition in normal-weight humans. Am. J. Clin. Nutr. 52: 777-783, 1990.

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