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J Appl Physiol 92: 2303-2308, 2002. First published January 11, 2002; doi:10.1152/japplphysiol.01124.2001
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Vol. 92, Issue 6, 2303-2308, June 2002

Changes in maximal aerobic capacity with age in endurance-trained women: 7-yr follow-up

Iratxe Eskurza1, Anthony J. Donato1, Kerrie L. Moreau1, Douglas R. Seals1,2, and Hirofumi Tanaka1

1 Human Cardiovascular Research Laboratory, Department of Kinesiology and Applied Physiology, University of Colorado at Boulder, Boulder 80309; and 2 Divisions of Cardiology and Geriatric Medicine, Department of Medicine, University of Colorado Health Sciences Center, Denver, Colorado 80262


    ABSTRACT
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

On the basis of cross-sectional data, we previously reported that the absolute, but not the relative (%), rate of decline in maximal oxygen consumption (VO2 max) with age is greater in endurance-trained compared with healthy sedentary women. We tested this hypothesis by using a longitudinal approach. Eight sedentary (63 ± 2 yr at follow-up) and 16 endurance-trained (57 ± 2) women were reevaluated after a mean follow-up period of 7 yr. At baseline, VO2 max was ~70% higher in endurance-trained women (48.1 ± 1.7 vs. 28.1 ± 0.8 ml · kg-1 · min-1 · yr-1). At follow-up, body mass, fat-free mass, maximal respiratory exchange ratio, and maximal rating of perceived exertion were not different from baseline in either group. The absolute rate of decline in VO2 max was twice as great (P < 0.01) in the endurance-trained (-0.84 ± 0.15 ml · kg-1 · min-1 · yr-1) vs. sedentary (-0.40 ± 0.12 ml · kg-1 · min-1 · yr-1) group, but the relative rates of decline were not different (-1.8 ± 0.3 vs. -1.5 ± 0.4% per year). Differences in rates of decline in VO2 max were not related to changes in body mass or maximal heart rate. However, among endurance-trained women, the relative rate of decline in VO2 max was positively related to reductions in training volume (r = 0.63). Consistent with this, the age-related reduction in VO2 max in a subgroup of endurance-trained women who maintained or increased training volume was not different from that of sedentary women. These longitudinal data indicate that the greater decrease in maximal aerobic capacity with advancing age observed in middle-aged and older endurance-trained women in general compared with their sedentary peers is due to declines in habitual exercise in some endurance-trained women. Endurance-trained women who maintain or increase training volume demonstrated age-associated declines in maximal aerobic capacity not different from healthy sedentary women.

maximal oxygen consumption; functional capacity


    INTRODUCTION
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

MAXIMAL AEROBIC CAPACITY is an important indicator of physiological functional capacity and is known to decrease with advancing age (2, 13, 14, 18). The decrease in maximal aerobic capacity with age has a number of physiological and clinical implications as it is associated with increased risks for cardiovascular and all-cause mortality (1) and disability (21), and reductions in cognitive function (20), quality of life (21), and independence (21).

With the number of older adults rapidly increasing, the question of how rates of decline in maximal aerobic capacity with age may differ among populations is of obvious importance. In this context, largely on the basis of cross-sectional data in men, for many years it was suggested that the rate of decline in maximal aerobic capacity with age in endurance exercise-trained adults was only approximately half of that observed in healthy sedentary controls (7, 9, 11). In contrast to this view, on the basis of cross-sectional comparisons, we recently reported that the absolute (ml · kg-1 · min-1 · yr-1) decrease in maximal oxygen consumption (VO2 max) across subject age actually was greater in endurance-trained compared with healthy sedentary women, although the relative (% per year) decreases were similar (6, 18). However, because of well-recognized limitations associated with cross-sectional study designs (4), these findings need to be confirmed with a longitudinal study.

On the basis of the important influence of habitual physical activity on VO2 max (3, 9, 14) and correlational data from our cross-sectional comparisons (6, 18), we speculated in its previous reports (6, 18) that the greater absolute rate of decline in VO2 max with age in the endurance-trained women in general could be attributable to reductions in training. However, the limited and cross-sectional nature of the available data precluded drawing any definite conclusion on this issue.

Accordingly, in the present investigation, we prospectively tested the hypothesis that the absolute rate of age-related decline in maximal aerobic capacity is greater in endurance-trained than in sedentary healthy middle-aged and older women. If so, we also sought to determine whether the greater rate of decline in maximal aerobic capacity in endurance-trained women was associated with declines in exercise training. To do so, we retested sedentary and endurance-trained women a mean of 7 yr after originally studying them (5, 16, 17).


    METHODS
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INTRODUCTION
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RESULTS
DISCUSSION
REFERENCES

Subjects. We studied 24 women: 8 sedentary and 16 endurance trained aged 40-78 yr. All subjects were apparently healthy and free of overt cardiovascular diseases, as assessed by medical history questionnaire. Irrespective of training status, women >50 yr of age were further evaluated by physical examination and resting and maximal exercise electrocardiograms. All of the subject were normotensive (<140/90 mmHg), nonobese (body mass index of <30kg/m2), and nonsmokers. None of the women were taking medications, other than hormone-replacement therapy, that could affect cardiovascular function. Before participation, verbal and written explanations of the nature, purpose, and risks of the study were administered. In turn, subjects gave their written, informed consent to participate in this investigation. This study was reviewed and approved by the Human Research Committee of the University of Colorado at Boulder.

All the subjects were initially tested in years 1993-1994 (5, 16, 17) and subsequently reevaluated in 2000, with a mean follow-up period of 7 yr. At the initial testing, all endurance-trained women had placed in the top 10 for their age group in Bolder Boulder road race (the second largest 10-km road race in the United States). When these women were reevaluated in 2000, they were still actively competing in running road races. None of the sedentary subjects engaged in any type of endurance training during the follow-up period. Their sedentary status was documented by questionnaire as well as VO2 max values.

Measurements. VO2 max was assessed with on-line computer-assisted open-circuit spiromery during continuous incremental treadmill exercise as described in detail previously (5, 16-18). Gas fractions were analyzed with a Perkin-Elmer MGA-1100 mass spectrometer (Pomona, CA) previously calibrated with standard gases of known concentrations. Expired air volume was measured either with a turbine (VMM-2, Interface Associates, Laguana Niguel, CA) or a pneumotachometer (Hans Rudolph, Kansas City, MO). There were no differences between these two systems when ventilation and oxygen uptake were analyzed simultaneously. These machines were calibrated against 3- or 7-liter syringes before and after each session. Heart rates were continuously monitored with an electrocardiogram.

After a 6- to 10-min warm-up period, each subject ran (endurance-trained women) or walked (sedentary women) at a comfortable speed that corresponded to 70-80% of age-predicted maximal heart rate. Treadmill grade was increased 2.5% every 2 min until volitional exhaustion. At the end of each stage, subjects were asked to rate their perception of effort by using a Borg scale (6-20 scale). Each treadmill test lasted between 8 and 12 min. Maximal heart rate was defined as the highest value recorded from electrocardiogram recordings during the test. To ensure that each subject attained VO2 max, at least three of the following four criteria were met by each subject: 1) a plateau in oxygen uptake with increasing exercise intensity, 2) a respiration exchange ratio of at least 1.15, 3) an achievement of the age-predicted maximal heart rate (±10 beats/min), and 4) a rating of perceived exertion of at least 18 units (10). The same individualized protocol was used at the baseline and follow-up periods.

Body mass was measured with a physician's balance scale (Detecto, Webb City, MO) to the nearest 0.1 kg. Body fat percent was estimated from the sum of five-site skinfold measurements with a Lange caliper. Fat-free mass was subsequently calculated as the difference between total body mass and estimated fat mass. Waist circumference was measured at the umbilicus, and hip circumference was determined at the maximum circumference of the buttocks. Measurements of plasma lipid and lipoprotein concentrations were performed by the General Clinical Research Center Core Laboratory at the University of Colorado Health Sciences Center as previously described (16, 17). Arterial blood pressure was measured by a conventional mercury sphygmomanometer after at least 10 min of rest under quiet, comfortable laboratory conditions (16, 17).

Detailed information was obtained from each subject regarding her training records. Endurance-trained women recorded their running intensity, mileage, duration, frequency, and characteristics of training (e.g., long slow distance, interval training) on a daily basis continuously for 2 wk. The same questionnaire was used at the baseline and follow-up periods. Additionally, to minimize the potential influence of seasonal variations in training levels, the reevaluation of the endurance-trained women was conducted at a similar time of the year in their competitive season to that in the initial evaluation. Physical activity levels of the sedentary subjects were estimated by using the Stanford Physical Activity Questionnaire (15).

Statistics. Analysis of variance with repeated measures (group × time) was used to determine differences in the dependent variables in each group before and after the follow-up period. When indicated by a significant F value, a post hoc test using the Newman-Keuls method was performed to identify significant differences among mean values. Univariate correlation and regression analyses were used to determine associations between dependent variables. All data are reported as means ± SE. Statistical significance was set at P < 0.05.


    RESULTS
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INTRODUCTION
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RESULTS
DISCUSSION
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Subject characteristics. Table 1 presents mean values for selected subject characteristics. At baseline, sedentary women had significantly higher body mass, body mass index, body fat, hip circumference, and waist-to-hip ratio compared with endurance-trained women. Height and fat-free mass decreased and body mass index and body fat percentage increased over the follow-up period in both groups (P < 0.05); there were no significant differences in these changes between the two groups. No significant changes were observed in blood pressure and plasma cholesterol and lipid levels in either group. Physical activity levels of the sedentary women did not change (32 ± 1 kcal/day at baseline and 35 ± 1 at follow-up; P = not significant).

                              
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Table 1.   Selected subject characteristics

VO2 max at baseline and during follow-up. At baseline, VO2 max was higher (P < 0.01) in endurance-trained compared with sedentary women (Fig. 1). When expressed in absolute terms, the rate of decline in VO2 max over the follow-up period was 110% greater (P < 0.05) in endurance-trained (-0.84 ± 0.15 ml · kg-1 · min-1 · yr-1) compared with sedentary (-0.40 ± 0.12 ml · kg-1 · min-1 · yr-1) women. In contrast, the relative rate of decline in VO2 max over the same period was not different between endurance-trained (-1.8 ± 0.3% per year) and sedentary (-1.5 ± 0.4% per year) women (P = 0.59). Age-related declines in maximal heart rate and oxygen pulse also were not different in the two groups (Table 2). In both groups, respiratory exchange ratio and rating of perceived exertion at VO2 max were not different at baseline and follow-up, suggesting similar voluntary maximal efforts at the two testing points.


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Fig. 1.   Absolute (A) and relative (B) rates of decline in maximal oxygen consumption (VO2 max) with increasing age. Delta , change. Numbers in parentheses indicate baseline VO2 max values ± SE. *P < 0.05 vs. sedentary subjects. dagger P < 0.05 vs. sedentary subjects' baseline value.


                              
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Table 2.   Exercise hemodynamic and performance characteristics

Correlates of changes in VO2 max over the follow-up period. In the pooled subject population, changes in VO2 max were related to corresponding changes in maximal oxygen pulse (r = 0.42; P < 0.01). Among sedentary women, changes in VO2 max were not related to any measure. As illustrated in Fig. 2, among endurance-trained women, changes in VO2 max were positively related to decreases in running mileage (r = 0.63) and more modestly with running (weekly) frequency (r = 0.42) (P < 0.01) but not with changes in running intensity (r = -0.03; P = 0.93).


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Fig. 2.   Relation between Delta VO2 max and running mileage.

Subgroup analysis: effects of training volume. To gain further insight into the role of reductions in training volume with age on the decline in VO2 max, we divided the endurance-trained women into those who maintained or increased (n = 6) and those who reduced (n = 10) their baseline training volume (Table 3). The two subgroups did not differ significantly in baseline levels of VO2 max. The reduction in VO2 max over the follow-up period was significantly greater in the subgroup of endurance-trained women who reduced their training volume (-1.04 ± 0.16 ml · kg-1 · min-1 · yr-1) compared with the other two groups but was not different (P = 0.62) between the subgroup of endurance-trained women who maintained/increased training volume (-0.52 ± 0.20 ml · kg-1 · min-1 · yr-1) and the sedentary women (Fig. 3). Among the sedentary women and endurance-trained women who maintained/increased their training volume (i.e., groups that exhibited similar rates of reduction in VO2 max with age), changes in VO2 max were not significantly related to changes in any other variable.

                              
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Table 3.   Selected subject characteristics of endurance-trained women: subgroup analyses



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Fig. 3.   Absolute rates of decline in VO2 max in endurance-trained women who reduced and who maintained/increased their baseline training volume. Numbers in parentheses indicate baseline VO2 max values ± SE. *P < 0.05 vs. the other two groups.


    DISCUSSION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

For the last decade, our laboratory has been investigating the modulatory influence of regular physical activity on age-related reductions in VO2 max in women. As an initial step, we used a meta-analytic approach to address this issue (6) and found that, in marked contrast to the prevailing view in men (7, 9, 11), the absolute rate of decline in VO2 max across age was greatest in the most physically active and smallest in the least active women (6). Because of the well-recognized limitations of meta-analysis, we next performed a well-controlled laboratory-based study (18) and obtained findings consistent with those of our prior meta-analysis. However, to provide more definitive insight into the relation between age-related changes in maximal aerobic capacity and habitual exercise status, we conducted the present longitudinal investigation.

The key findings of this new study are as follows. First, in the overall sample of the endurance-trained women in their 50s and 60s, the absolute but not relative rate of decline in VO2 max with age was greater than that in healthy sedentary women. Second, endurance-trained women who maintained/increased their training volume demonstrated a rate of decline in VO2 max over a 7-yr period that is not different from their sedentary peers. These longitudinal data confirm our previous cross-sectional observations (6, 18) that the decrease in maximal aerobic capacity with advancing age is greater in endurance-trained women in general compared with their sedentary peers. However, the present results extend importantly our previous findings by demonstrating that the greater decline in VO2 max in the overall sample of endurance-trained subjects is due to reductions in training volume in some of the women. Thus, among healthy women aged 34-78 yr, the endurance exercise-trained state is associated only with an accelerated rate of decline in maximal aerobic capacity (compared with sedentary women) when training volume decreases.

During the development of the present manuscript, the results of a longitudinal analysis of age-related reductions in VO2 max in endurance-trained women aged 40-73 yr were published (8). They reported age-related rates of decline in VO2 max ranging from -0.4 to -0.9 ml · kg-1 · min-1 · yr-1 in female masters athletes (8). These rates of decline in VO2 max are similar to those we obtained in our endurance-trained women and appear to be greater than the rates previously reported in sedentary controls (2, 6), but no sedentary control group was included.

Regarding "physiological" mechanisms, it has been hypothesized that the decline in VO2 max with age in trained and untrained adults may be influenced by the corresponding reduction in maximal heart rate (7). However, consistent with our previous cross-sectional results (6, 18, 19), there was no obvious association between reductions in maximal heart rate and habitual exercise status. These findings suggest that other factors, including declines in maximal stroke volume, skeletal muscle oxidative capacity, and/or pulmonary function (e.g., maintenance of arterial oxygen concentrations), may be responsible for explaining group differences in the absolute rate of decline in VO2 max with age. Moreover, we wish to emphasize that more than one mechanism may be responsible for population-specific differences in the rate of decline in VO2 max with age. The fact that the rates of decline were similar in the sedentary controls and endurance-trained women who maintained/increased training volume suggests the possibility of a common mechanism (or mechanisms), perhaps related to fundamental biological aging processes. On the other hand, the greater rate of decline in VO2 max in the endurance-trained women who decreased their training volume is consistent with the superimposition of one or more additional mechanisms, perhaps linked to processes associated with deconditioning per se. Definitive mechanistic insight into these issues will need to be obtained from future longitudinal studies.

Our series of findings in women (6, 18) differ from the results of our recent meta-analysis in men (22). In the latter investigation, we found that both absolute and relative rates of decline in VO2 max with age were not different between sedentary and endurance-trained men (22). These gender-related differences are in agreement with the previously mentioned cross-sectional study by Ogawa et al. (12). Although they studied distinct groups of young and older men and women, manual construction of a linear regression line with the use of their mean data reveals that the absolute rate of decline in VO2 max was ~50% greater in the endurance-trained compared with the sedentary women, whereas such differences were absent in men (12). It is not clear why there appears to be a sex difference in the age-related reduction in VO2 max between sedentary and endurance-trained healthy adults. Based on the present study's findings, it is plausible to hypothesize that some endurance-trained women may experience a greater rate of decline in training volume compared with their male counterparts. A well-controlled laboratory-based study would be required to properly test this hypothesis.

In conclusion, the results of the present longitudinal study support our recent cross-sectional findings that, in the overall sample of endurance-trained women, the absolute, but not relative, rate of decline in VO2 max with age was greater in endurance-trained compared with healthy sedentary women. However, our data also indicate that the greater age-associated rate of decline in VO2 max in the overall sample of endurance-trained women appears to be due to those who reduced their training (running) volume. Thus, among healthy women aged 34-78 yr, the endurance exercise-trained state only is associated with an accelerated rate of decline in maximal aerobic capacity (compared with sedentary women) when training volume decreases.


    ACKNOWLEDGEMENTS

We thank Susan Evans, Cyndi Long, and Edith Stevenson for technical assistance in the present study.


    FOOTNOTES

This study was supported by National Institute on Aging Grants AG-00847 and AG-13038, and the Basque Government.

Address for reprint requests and other correspondence: H. Tanaka, Dept. of Kinesiology and Health Education, Univ. of Texas at Austin, Austin, TX 78712 (E-mail: htanaka{at}mail.utexas.edu).

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

First published January 11, 2002;10.1152/japplphysiol.01124.2001

Received 9 November 2001; accepted in final form 9 January 2002.


    REFERENCES
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

1.   Blair, SN, Kohl HW, Paffenbarger RS, Clark DG, Cooper KH, and Gibbons LW. Physical fitness and all-cause mortality: a prospective study of men and women. JAMA 262: 2395-2401, 1989.

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3.   Coyle, EF, Hemmert MK, and Coggan AR. Effects of detraining on cardiovascular responses to exercise: role of blood volume. J Appl Physiol 60: 95-99, 1986.

4.   Dehn, MM, and Bruce RA. Longitudinal variations in maximal oxygen intake with age and activity. J Appl Physiol 33: 805-807, 1972.

5.   Evans, SL, Davy KP, Stevenson ET, and Seals DR. Physiological determinants of 10-km performance in highly trained female runners of different ages. J Appl Physiol 78: 1931-1941, 1995.

6.   FitzGerald, MD, Tanaka H, Tran ZV, and Seals DR. Age-related decline in maximal aerobic capacity in regularly exercising vs. sedentary females: a meta-analysis. J Appl Physiol 83: 160-165, 1997.

7.   Hagberg, JM. Effect of training on the decline of VO2 max with aging. Fed Proc 46: 1830-1833, 1987.

8.   Hawkins, SA, Marcell TJ, Victoria Jaque S, and Wiswell RA. A longitudinal assessment of change in VO2 max and maximal heart rate in master athletes. Med Sci Sports Exerc 33: 1744-1750, 2001.

9.   Heath, GW, Hagberg JM, Ehsani AA, and Holloszy JO. A physiological comparison of young and older endurance athletes. J Appl Physiol 51: 634-640, 1981.

10.   Howley, ET, Bassett DR, and Welch HG. Criteria for maximal oxygen uptake: review and commentary. Med Sci Sports Exerc 27: 1292-1301, 1995.

11.   Kasch, FW, Boyer JL, Camp SPV, Verity LS, and Wallace JP. The effect of physical activity and inactivity on aerobic power in older men (a longitudinal study). Phys Sportsmed 18: 73-83, 1990.

12.   Ogawa, T, Spina RJ, Martin WH, Kohrt WM, Schechtman KB, Holloszy JO, and Ehsani AA. Effects of aging, sex, and physical training on cardiovascular responses to exercise. Circulation 86: 494-503, 1992.

13.   Robinson, S. Experimental studies of physical fitness in relation to age. Arbeitsphysiol 10: 251-323, 1938.

14.   Robinson, S. Training and physiological aging in man. Fed Proc 32: 1628-1634, 1973.

15.   Sallis, JF, Haskell WL, Wood PD, Fortmann SP, Rogers T, Blair SN, and Paffenbarger RS. Physical activity assessment methodology in the Five-City Project. Am J Epidemiol 121: 91-106, 1985.

16.   Stevenson, ET, Davy KP, and Seals DR. Maximal aerobic capacity and total blood volume in highly trained middle-aged and older female endurance athletes. J Appl Physiol 77: 1691-1696, 1994.

17.   Stevenson, ET, Davy KP, and Seals DR. Hemostatic, metabolic, and androgenic risk factors for coronary heart disease in physically active and less active postmenopausal women. Arterioscler Thromb 15: 669-677, 1995.

18.   Tanaka, H, DeSouza CA, Jones PP, Stevenson ET, Davy KP, and Seals DR. Greater rate of decline in maximal aerobic capacity with age in physically active vs. sedentary healthy women. J Appl Physiol 83: 1947-1953, 1997.

19.   Tanaka, H, Monahan KD, and Seals DR. Age-predicted maximal heart rate revisited. J Am Coll Cardiol 37: 153-156, 2001.

20.   Van Boxtel, MPJ, Paas FGW, Houx PJ, Adam JJ, Teeken JC, and Jolles J. Aerobic capacity and cognitive performance in a cross-sectional aging study. Med Sci Sports Exerc 29: 1357-1365, 1997.

21.   WHO Study Group. Aging and Working Capacity. Geneva: World Health Organization, 1993.

22.   Wilson, TM, and Tanaka H. Meta-analysis of the age-associated decline in maximal aerobic capacity in men: relation to training status. Am J Physiol Heart Circ Physiol 278: H829-H834, 2000.


J APPL PHYSIOL 92(6):2303-2308
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