Vol. 83, Issue 6, 1947-1953, December 1997

Greater rate of decline in maximal aerobic capacity with age in physically active vs. sedentary healthy women

Hirofumi Tanaka¹, Christopher A. Desouza¹, Pamela P. Jones¹, Edith T. Stevenson¹, Kevin P. Davy¹, and Douglas R. Seals^1,2

¹ Human Cardiovascular Research Laboratory, Center for Physical Activity, Disease Prevention, and Aging, Department of Kinesiology, University of Colorado, Boulder 80309; and ² Divisions of Cardiology and Geriatric Medicine, Department of Medicine, Center on Aging, University of Colorado Health Sciences Center, Denver, Colorado 80262

ABSTRACT

INTRODUCTION

METHODS

RESULTS

DISCUSSION

ACKNOWLEDGEMENTS

FOOTNOTES

REFERENCES

ABSTRACT

Tanaka, Hirofumi, Christopher A. DeSouza, Pamela P. Jones, Edith T. Stevenson, Kevin P. Davy, and Douglas R. Seals. Greater rate of decline in maximal aerobic capacity with age in physically active vs. sedentary healthy women. J. Appl. Physiol. 83(6): 1947-1953, 1997.Using a meta-analytic approach, we recently reported that the rate of decline in maximal oxygen uptake (O_{2 max}) with age in healthy women is greatest in the most physically active and smallest in the least active when expressed in milliliters per kilogram per minute per decade. We tested this hypothesis prospectively under well-controlled laboratory conditions by studying 156 healthy, nonobese women (age 20-75 yr): 84 endurance-trained runners (ET) and 72 sedentary subjects (S). ET were matched across the age range for age-adjusted 10-km running performance. Body mass was positively related with age in S but not in ET. Fat-free mass was not different with age in ET or S. Maximal respiratory exchange ratio and rating of perceived exertion were similar across age in ET and S, suggesting equivalent voluntary maximal efforts. There was a significant but modest decline in running mileage, frequency, and speed with advancing age in ET. O_{2 max} (ml · kg¹ · min¹) was inversely related to age (P < 0.001) in ET (r = 0.82) and S (r = 0.71) and was higher at any age in ET. Consistent with our meta-analysic findings, the absolute rate of decline in O_{2 max} was greater in ET (5.7 ml · kg¹ · min¹ · decade¹) compared with S (3.2 ml · kg¹ · min¹ · decade¹; P < 0.01), but the relative (%) rate of decline was similar (9.7 vs 9.1%/decade; not significant). The greater absolute rate of decline in O_{2 max} in ET compared with S was not associated with a greater rate of decline in maximal heart rate (5.6 vs. 6.2 beats · min¹ · decade¹), nor was it related to training factors. The present cross-sectional findings provide additional evidence that the absolute, but not the relative, rate of decline in maximal aerobic capacity with age may be greater in highly physically active women compared with their sedentary healthy peers. This difference does not appear to be related to age-associated changes in maximal heart rate, body composition, or training factors.

aging; maximal oxygen uptake; maximal heart rate; endurance exercise training

INTRODUCTION

MAXIMAL AEROBIC CAPACITY, as assessed by maximal oxygen uptake (O_{2 max}), declines with advancing age in both men and women (1, 8, 27). This decrease reduces physical work capacity and results in older individuals working closer to maximum effort when performing a given submaximal task by reducing their functional reserve capacity (8). In addition, maximal aerobic capacity has recently been shown to be an independent risk factor for all-cause and cardiovascular disease mortality (5, 6). Therefore, the prevention or attenuation of the age-related reduction in maximal aerobic capacity via maintenance of physical activity levels with age is likely to be one of the key future goals of preventive gerontology (4).

There is some evidence in men to suggest that regularly performed vigorous endurance exercise may attenuate the loss of maximal aerobic capacity with advancing age. For example, the rate of age-related decline in O_{2 max} has been reported to be up to 50% less in endurance-trained compared with sedentary men (7, 13). In contrast, the results of recent longitudinal studies in endurance-trained men (14, 24, 32) suggest as great or greater rates of decline in maximal aerobic capacity as those previously reported in sedentary men (1, 7, 13).

The corresponding data in women appear to be similarly equivocal. Specifically, it has been reported that the rate of decline in O_{2 max} with age is lower (9, 26), unchanged (3, 22), or even greater (2, 33) in physically active compared with sedentary women. It has been suggested that small sample sizes, limited age ranges, and the lack of a sedentary control group are responsible for the conflicting results (11, 33).

To eliminate or minimize these possible limitations of previous investigations, recently we used a meta-analytic approach to address this issue. We found that the absolute rate of decline in O_{2 max} with age (i.e., ml · kg¹ · min¹ · decade¹) in healthy women is greatest in the most physically active and smallest in the least active (11). However, a well-recognized limitation of meta-analysis is the lack of experimental control due primarily to the heterogeneity of the methods used among the individual studies making up the database (21, 31). Therefore, we reasoned that a well-controlled laboratory-based study was needed to complement the findings of our previous meta-analysis.

Accordingly, the primary purpose of the present study was to further test the hypothesis that the rate of decline in O_{2 max} with age is greater in physically active than in sedentary women. Our secondary aim was to determine whether such differences in the rate of decline in O_{2 max} with age, if shown, are related to age-related changes in maximal heart rate, body composition, or training factors.

METHODS

RESULTS

Table  1.   Subject characteristics Variable Age Groups, yr r With Age P Value 20-29 30-39 40-49 50-59 >60 Sedentary subjects   n 11 11 14 20 16   Age, yr 25 ± 1  33 ± 1  45 ± 1  54 ± 1  64 ± 1    Height, cm 167 ± 2  165 ± 2  163 ± 2  167 ± 2  161 ± 2  NS   Body mass, kg 61 ± 2  65 ± 4  66 ± 3  67 ± 2  70 ± 3  0.27 <0.05   Fat-free mass, kg 44 ± 1  46 ± 1  43 ± 1  44 ± 1  46 ± 1  NS   Body fat, %  27 ± 2  28 ± 3  34 ± 1  33 ± 1  34 ± 1  0.38 <0.001 Endurance-trained subjects   n 14 21 13 23 13   Age, yr 26 ± 1  34 ± 1  45 ± 1  54 ± 1  66 ± 1    Height, cm 166 ± 1  167 ± 1  163 ± 2  166 ± 1  163 ± 2  NS   Body mass, kg 54 ± 2  55 ± 1  53 ± 2  56 ± 1  56 ± 2  NS   Fat-free mass, kg 46 ± 1  47 ± 1  45 ± 1  46 ± 1  44 ± 2  NS   Body fat, %  14 ± 1  15 ± 1  16 ± 2  19 ± 1  22 ± 1  0.51 <0.0001 Values are means ± SE; n, no. of subjects. NS, not significant.

Table  2.   Responses to maximal exercise Variable Age Groups, yr r With Age P Value 20-29 30-39 40-49 50-59 >60 Sedentary subjects   O2 max, l/min 2.1 ± 0.1  2.1 ± 0.1  1.7 ± 0.1  1.8 ± 0.1  1.6 ± 0.1   0.63 <0.0001   O2 max, ml · kg1 · min1 34.9 ± 1.4  33.7 ± 1.9  27.0 ± 1.2  26.2 ± 0.8  22.4 ± 1.2   0.71 <0.0001   O2 max, ml · FFM1 · min1 48.9 ± 1.4  47.2 ± 1.9  41.1 ± 1.4  39.6 ± 1.3  36.3 ± 1.4   0.66 <0.0001   HRmax, bpm 194 ± 4  185 ± 3  179 ± 2  175 ± 2  169 ± 3   0.69 <0.0001   RERmax 1.13 ± 0.02  1.16 ± 0.02  1.19 ± 0.02  1.17 ± 0.01  1.16 ± 0.02  NS   RPEmax 19.1 ± 0.2  19.1 ± 0.2  19.0 ± 0.3  19.3 ± 0.2  18.9 ± 0.2  NS   Emax, l/min 88.1 ± 4.7  94.9 ± 3.0  78.5 ± 3.1  80.5 ± 3.4  64.7 ± 4.1   0.51 <0.0001   O2 pulse, ml · kg1 · beat1 0.182 ± 0.010  0.182 ± 0.010  0.151 ± 0.007  0.149 ± 0.004  0.132 ± 0.007   0.57 <0.0001 Endurance-trained subjects   O2 max, l/min 3.0 ± 0.1  3.1 ± 0.1  2.7 ± 0.1  2.4 ± 0.1  1.8 ± 0.1   0.78 <0.0001   O2 max, ml · kg1 · min1 55.0 ± 1.0  55.2 ± 1.0  51.4 ± 1.8  42.7 ± 1.5  32.5 ± 1.3   0.82 <0.0001   O2 max, ml · FFM1 · min1 65.4 ± 1.3  65.8 ± 1.0  60.0 ± 1.5  55.7 ± 1.5  43.8 ± 2.0   0.78 <0.0001   HRmax, bpm 184 ± 3  183 ± 2  178 ± 1  166 ± 3  166 ± 5   0.58 <0.0001   RERmax 1.19 ± 0.02  1.17 ± 0.01  1.16 ± 0.02  1.16 ± 0.01  1.19 ± 0.02  NS   RPEmax 19.5 ± 0.2  19.2 ± 0.2  19.1 ± 0.4  19.1 ± 0.1  19.2 ± 0.3  NS   Emax, l/min 118.6 ± 4.5  117.7 ± 3.8  109.7 ± 4.1  103.3 ± 4.0  86.7 ± 5.6   0.55 <0.0001   O2 pulse, ml · kg1 · beat1 0.300 ± 0.007  0.303 ± 0.007  0.289 ± 0.010  0.247 ± 0.014  0.198 ± 0.009   0.63 <0.0001 Values are means ± SE. O2 max, maximal oxygen uptake; HRmax, maximal heart rate; RERmax, maximal respiratory exchange ratio; RPEmax, maximal rating of perceived exertion; Emax, maximal ventilation in BTPS units; FFM, fat-free mass; bpm, beats/min.

Rate of decline in O_{2 max}.

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Table  3.   Exercise training and performance data of the endurance-trained women Variable Age Groups, yr r With Age P Value 20-29 30-39 40-49 50-59 >60 Mileage, km/wk 62 ± 5  59 ± 5  49 ± 7  48 ± 3  35 ± 4   0.44 <0.0005 Frequency, days/wk 5.6 ± 0.3  5.1 ± 0.3  4.8 ± 0.3  5.3 ± 0.2  4.0 ± 0.4   0.29 <0.05 Training speed, m/min 203 ± 9  197 ± 5  194 ± 7  188 ± 5  170 ± 11   0.35 <0.001 Length of time training, yr 10.2 ± 1.2  12.1 ± 1.3  9.4 ± 1.6  18.0 ± 1.2  14.3 ± 1.5  0.35 <0.001 10-km Time, min 41 ± 1  41 ± 1  45 ± 1  50 ± 1  58 ± 2  0.81 <0.0001 %Performance 75 ± 1  76 ± 1  77 ± 1  76 ± 2  77 ± 3  NS Values are means ± SE. %Performance, % of age-adjusted world-best 10-km running times.

Correlates of the age-related decline in O_{2 max}.

Table  4.   Stepwise multiple-regression analysis for predicting factors responsible for age-related reduction in O2 max Group Predictor 1 (R2) Predictor 2 (cumulative R2) Endurance trained Age %Body fat (0.69) (0.79) Sedentary Age %Body fat (0.57) (0.77) Combined %Body fat Age (0.74) (0.82)

DISCUSSION

The primary findings of the present study are as follows. First, consistent with the results of our recent meta-analysis, the absolute, but not the relative, rate of decline in O_{2 max} with age was greater in highly physically active women compared with their sedentary peers. Second, the greater rate of decline in O_{2 max} with age in the endurance-trained women was not related to a greater rate of change in maximal heart rate, body composition, or training factors.

Using the meta-analytic approach, we recently demonstrated that the absolute rate of decline in O_{2 max} with age in healthy women increases with increasing levels of habitual endurance exercise (11). The results of the present study are consistent with these findings, indicating that the absolute rate of decline in O_{2 max} with increasing age is greater in endurance-trained than sedentary women. Moreover, the age-related rates of decline in O_{2 max} in the present study were similar to those observed in our meta-analysis (i.e., 3.2 and 3.5 in sedentary and 5.7 and 6.2 ml · kg¹ · min¹ · decade¹ in endurance-trained women, respectively). Taken together, these results indicate that endurance-trained women appear to have greater rates of decline in O_{2 max} with advancing age compared with healthy sedentary adult women. The present results also are consistent with recent findings from longitudinal studies in men (14, 24, 32).

It is not clear as to why endurance-trained women exhibit a greater rate of decline in O_{2 max} with increasing age. The results of some earlier studies indicate that changes in body composition play an important role in the age-related decline in O_{2 max} (8, 12, 20, 23). In the present study, body mass and fat-free mass were maintained across age in the endurance-trained women, whereas the sedentary women demonstrated a significant increase in body mass and body fat across age without a change in fat-free mass. The age-related increase in fat and total body mass in the sedentary women should act to increase their rate of reduction in O_{2 max} with age when expressed in milliliters per kilogram per minute per decade compared with the active women. It is also plausible to speculate that the greater rate of decline in maximal aerobic capacity in the endurance-trained women may be due to larger age-related reductions in maximal heart rate because of its effect on maximal cardiac output and, in turn, O_{2 max} via the Fick equation (13, 15). However, the rates of decline in maximal heart rate were similar between the endurance-trained and sedentary women. Thus these results suggest that factors other than body composition and maximal heart rate (namely age-related changes in maximal stroke volume and arteriovenous oxygen difference) were responsible for the greater rate of decline in O_{2 max} in the endurance-trained women.

Because of the major role that habitual physical activity plays in determining O_{2 max} (23, 25, 28), we speculated in our previous meta-analytic study that the greater rate of decline in O_{2 max} with age in the endurance-trained women could be explained in part by a marked age-related decline in their levels of training. Although the limited database of studies reporting training mileage suggested that this might have been the case, the lack of complete data precluded us from drawing any definite conclusions. In the present study, running mileage and frequency declined significantly, albeit only modestly, with age in the endurance-trained women. Thus the magnitude of decline in physical activity was greater in the endurance-trained than in the sedentary women and, therefore, could have contributed to the greater rate of decline in O_{2 max} in the former group. However, several lines of evidence suggest that reductions in exercise volume did not exert a major effect. First, the univariate correlations between O_{2 max} and both weekly training mileage (r = 0.47) and frequency (r = 0.21) were modest. Second, changes in training volume with age did not explain a significant proportion of the variance in the age-related declines in O_{2 max} in the endurance-trained women, as assessed by the stepwise multiple-regression analysis. Third, a recent study in men reported that, despite a substantially smaller age-related rate of decline in O_{2 max} compared with sedentary or fitness-trained men, elite middle-age runners experienced a 43% reduction in training volume in the 20-yr follow-up period (32). In the present study, the reduction in training volume across a similar time period was only 21%, suggesting the likelihood of an even smaller effect of reductions in training on O_{2 max}.

Exercise training intensity has been reported to exert an even stronger effect on O_{2 max} than does training volume (16). Therefore, it is reasonable to speculate that the reduction in training intensity may have contributed to the greater rate of decline in O_{2 max} in the endurance-trained women. However, the univariate correlation between O_{2 max} and training intensity (i.e., running speed), although significant, was modest (r = 0.44). In addition, stepwise multiple regression revealed that the reduction in training intensity did not explain a significant portion of the variance in the age-related reduction in O_{2 max} in the endurance-trained women. Moreover, the rate of reduction in training intensity was relatively small (i.e., approx. 3%/decade). Our results are consistent with those of one recent longitudinal study in men (32) but differ from the findings of another recent longitudinal study by Pollock and colleagues (24), which showed a significant correlation between age-related changes in maximal aerobic capacity and training intensity. Thus our data do not support an obvious relation between measures of training volume or intensity and the rate of decline in O_{2 max} with age. However, it is possible that the combined effects of the modest declines in each of these measures may have contributed significantly to the decrease in O_{2 max} with age in the endurance athletes. Such a combined training stimulus measure cannot be calculated; therefore, we cannot speculate further on this possibility.

As discussed in detail in our previous paper (11), we think that the greater rate of decline in O_{2 max} in endurance-trained women may be due to a baseline effect. That is, individuals with the higher levels of O_{2 max} as young adults demonstrate a greater rate of decline with advancing age. This argument is supported by the observation that, when the baseline effect was removed by expressing the data as relative or percent changes from mean levels at age ~25 yr, the rate of decline in O_{2 max} with age was similar in the two groups. Similar relations between baseline levels and rates of decline in O_{2 max} with age are observed between men and women (7, 11). These results suggest that the greater absolute rate of decline in O_{2 max} in endurance-trained women may be largely attributed to their higher baseline levels as young adults.

A low level of maximal aerobic capacity has recently been identified as an important risk factor for all-cause and cardiovascular disease mortality in both men and women (5, 6). In addition, O_{2 max} is the most frequently used measure of physiological functional capacity. It is important to note that, although endurance-trained women appear to have a greater rate of decline in O_{2 max} with age, their absolute levels are substantially higher than those of their sedentary peers throughout the adult age range studied. Moreover, only a few endurance-trained women had O_{2 max} values lower than 32.5 ml · kg¹ · min¹, the level below which age-adjusted mortality starts to increase in women (5, 6). Therefore, we wish to emphasize from the standpoint of preventive gerontology (4) that the endurance-trained women in the present study possess higher levels of physiological functional capacity and, based on recent epidemiological data (5, 6), lower risks of premature mortality than do sedentary women at any age.

The major limitation of the present study is its cross-sectional design. It has been noted previously that data concerning the rate of decline in maximal aerobic capacity with age differ between longitudinal and cross-sectional study designs (7, 24). However, in studies in which cross-sectional and longitudinal analyses are combined in the same subject population (18, 22, 29), the estimation of the average rate of decline in O_{2 max} with advancing age is similar with the two approaches. Nevertheless, we cannot discount the possibility that genetic or other constitutional factors may have influenced the present cross-sectional findings. Longitudinal studies will be necessary to more completely understand the relation between age-related changes in maximal aerobic capacity and habitual exercise status.

We should also emphasize that our subject inclusion criteria (e.g., limits on body mass index) as well as the fact that our subjects were volunteers (i.e., not randomly selected) likely introduced subject selection bias. Therefore, our sedentary subjects may not have been representative of the general population of women over this age range.

In conclusion, the results presented herein support our recent findings (11) that the absolute, but not the relative, rate of decline in O_{2 max} with increasing age appears to be greater in highly physically active women compared with their healthy but sedentary peers. The greater rate of decline in O_{2 max} in endurance-trained women was not associated with greater changes in body mass or composition, maximal heart rate, and/or training factors.

ACKNOWLEDGEMENTS

We thank Cyndi Long for assistance in the present study.

FOOTNOTES

Address for reprint requests: H. Tanaka, Univ. of Colorado, Dept. of Kinesiology, Campus Box 354, Boulder, CO 80309-0354 (E-mail: tanakah{at}colorado.edu).

Received 14 March 1997; accepted in final form 31 July 1997.

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