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O2 max in trained
older subjects
Department of Anesthesiology, Mayo Clinic, Rochester, Minnesota 55905
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Proctor, David N., and Michael J. Joyner. Skeletal
muscle mass and the reduction of
O2 max in trained
older subjects. J. Appl. Physiol.
82(5): 1411-1415, 1997.
The role of skeletal muscle mass in the
age-associated decline in maximal
O2 uptake (O2 max) is poorly
defined because of confounding changes in muscle oxidative capacity and
in body fat and the difficulty of quantifying active muscle mass during
exercise. We attempted to clarify these issues by
examining the relationship between several indexes of muscle mass, as
estimated by using dual-energy X-ray absorptiometry and treadmill
O2 max in 32 chronically endurance-trained subjects from four groups
(n = 8/group): young men
(20-30 yr), older men (56-72 yr), young women
(19-31 yr), and older women (51-72 yr).
O2 max per kilogram
body mass was 26 and 22% lower in the older men (45.9 vs. 62.0 ml · kg
1 · min1)
and older women (40.0 vs. 51.5 ml · kg1 · min1).
These age differences were reduced to 14 and 13%, respectively, when
O2 max was expressed
per kilogram of appendicular muscle. When appropriately adjusted for
age and gender differences in appendicular muscle mass by analysis of
covariance, whole body O2 max was 0.50 ± 0.09 l/min less (P < 0.001) in the
older subjects. This effect was similar in both genders.
These findings suggest that the reduced
O2 max seen in highly
trained older men and women relative to their younger counterparts is
due, in part, to a reduced aerobic capacity per kilogram of active
muscle independent of age-associated changes in body composition, i.e.,
replacement of muscle tissue by fat. Because skeletal muscle
adaptations to endurance training can be well maintained in older
subjects, the reduced aerobic capacity per kilogram of muscle likely
results from age-associated reductions in maximal
O2 delivery (cardiac output
and/or muscle blood flow).
gender; dual-energy X-ray absorptiometry; master athlete; exercise; maximal oxygen uptake
INTRODUCTION AGING RESULTS IN A DECLINE in maximal
O2 uptake
( The present study was designed to address many of the limitations noted
above and to test the hypothesis that
METHODS Table 1.
Subject characteristics
O2 max;
ml · kg1 · min1).
This decline has been attributed primarily to reduced maximal cardiac output, increased body fat, and reduced peripheral
O2 extraction (11, 22). Reduced
skeletal muscle mass may also contribute to the age-associated decline
in O2 max, but there are little quantitative data on the relationship between
O2 max and muscle mass
as a function of age (2, 3, 10). The available studies, which primarily
consist of O2 max and
fat-free body mass (FFM) measurements in sedentary subjects, are
difficult to interpret due to the confounding effects of age-associated
changes in body fat and muscle oxidative capacity (3, 8, 10). Additionally, many studies of the decline in
O2 max with aging, particularly in trained subjects, have not statistically adjusted (covaried) O2 max for
age or gender differences in body composition (10, 12, 22, 31).
Finally, it is unclear what relevance indicators of whole body muscle
mass (FFM, creatinine excretion) have as determinants of
O2 max when most of the
O2 consumed during
O2 max testing is used
by the limb muscles (16, 17, 21, 29). These limitations have led to
some confusion about how to best express and compare
O2 max changes with
aging (l/min, ml · kg1 · min1,
ml · kg
FFM · min1).
For these reasons, the role of skeletal muscle mass in the decline in
O2 max with
aging remains poorly defined.
O2 max per kilogram of
limb muscle is reduced in highly trained older subjects, independent of
age-associated changes in body composition. Specifically, we examined
the relationship between appendicular muscle mass, as estimated by
using dual energy X-ray absorptiometry (DXA), and treadmill
O2 max in chronically
endurance-trained subjects. Appendicular muscle mass was used to
provide a more specific estimate of the quantity of muscle recruited
during maximal treadmill running, and analysis of covariance (ANCOVA)
was performed to appropriately evaluate the impact of age and
gender differences in muscle mass on
O2 max. We studied
highly trained older men and women to minimize the potential effects of
age-related physical inactivity (i.e., reduced muscle oxidative
capacity and capillarization) and to ensure that our older subjects
were capable of reaching O2 max.
2 days/wk)
use of moderate resistance-training exercises for the upper and lower
body. Each subject gave written informed consent before the study
according to Mayo Clinic Institutional Review Board guidelines.
Men
Women
Age Effect (P Value)
Gender Effect
(P Value)
Young
Older
Young
Older
Age, yr
24 ± 4
64 ± 4
26 ± 4
61 ± 8
<0.001
NS
Height, cm
180 ± 7
178 ± 6
171 ± 5
164 ± 6
<0.05
<0.001
Weight, kg
70.9 ± 7.8
75.5 ± 10.2
60.1 ± 5.5
58.1 ± 6.6
NS
<0.001
%Fat
9.9 ± 2.5
20.0 ± 6.0
22.5 ± 4.4
28.4 ± 6.3
<0.001
<0.001
Fat-free mass, kg
64.0 ± 8.2
60.0 ± 6.1
46.4 ± 2.8
41.3 ± 2.3
<0.05
<0.001
Appendicular
muscle, kg
27.7 ± 4.1
25.1 ± 3.3
19.6 ± 2.1
16.8 ± 0.9
<0.05
<0.001
Training
yr
9 ± 3
21 ± 5
9 ± 5
19 ± 8
<0.001
NS
min/wk
444 ± 193
373 ± 184
328 ± 130
389 ± 189
NS
NS
Values are means ± SD for 8 subjects per group. %Fat, fat-free
mass, and appendicular muscle mass were each estimated by dual-energy X-ray absorptiometry. NS, not significant. P values refer to
significant main effects identified by 2-way (age × gender)
analysis of variance.
O2 max (3, 4, 7, 22,
31).
Reproducibility (intraclass correlation) of repeated DXA estimates of
appendicular muscle and FFM in a separate sample of 10 subjects (6 men,
4 women, age 25-50 yr) was 0.99 and 0.99, respectively. Mean
values for the repeated measurements on 2 different days did not differ
for appendicular muscle mass (23.7 vs. 23.9 kg;
P = 0.66) or FFM (54.7 vs. 54.9 kg;
P = 0.49). Fat mass (kg) was also
found to be highly correlated (P < 0.001) with the sum of skinfolds in the present sample of trained men
(
6; r = 0.92) and women (5;
r = 0.88) (19). The DXA instrument was
calibrated monthly by using a series of beef blocks of known
composition (Hormel, Austin, MN).
Treadmill testing.
Most of the subjects had previous experience with treadmill running.
Older subjects initially completed a Bruce treadmill test with 12-lead
electrocardiograph (ECG) and blood pressure monitoring to screen for
underlying cardiovascular abnormalities. O2 max was
subsequently determined in all subjects by using a continuous, graded
(2% every other minute) treadmill running test to exhaustion. A 5-min
warm-up was used to determine the appropriate running speed for each
subject. Treadmill speed was individually selected so that each subject
would reach exhaustion within 8-12 min, excluding warm-up (14).
O2 uptake
(O2) was measured using an
automated breath-by-breath mass spectrometry system validated against
the meteorological-balloon collection technique across a wide range of
breathing frequencies (24).
The O2 max was
defined as the average O2
over the final 60 s of the test (14). The increase in
O2 over the final 60 s
(compared with the previous percent grade) was <100 ml/min in all 16 of the older subjects and <150 ml/min in 8 of the 16 young subjects.
Thus 75% of our subjects (including all of the older subjects)
achieved a plateau in O2
during the treadmill test (14, 29). The other eight young subjects had
<70% of the expected increase in
O2 (1) over the last minute
of the test and had respiratory exchange ratio levels
>1.10. Ratings of perceived exertion ranged from 17 to
20 on the Borg 20-point scale in both the young and older groups,
suggesting a similar level of effort between age groups. Maximal heart
rate was determined from ECG (10-beat average) tracings and exceeded
95% of age-predicted values (23) in 30 of the 32 subjects.
Statistical analysis.
Age, gender, and interaction (age × gender) effects on body
composition variables and
O2 max normalized by
using ratios (e.g., ml · kg
FFM1 · min1)
were evaluated with two-way analysis of variance. Comparisons of
O2 max were also
adjusted by using measures of muscle mass as a covariate (ANCOVA). This
permitted the appropriate correction of
O2 max data for age
and gender differences in body composition (31, 32). Reproducibility of
DXA-based estimates of muscle and FFM were evaluated by using
intraclass correlation coefficients. All statistics were performed by
using the SAS statistical package. Significance was accepted at
P 
0.05.
RESULTS
O2 max (Table
2).
Treadmill O2 max was
~30% higher in men than in women when expressed as liters per
minute. However, this gender difference in
O2 max was abolished
when normalized to FFM or appendicular muscle mass. Age differences in
O2 max ranged from 22 to 26% on either an absolute (l/min) or per kilogram body weight
(ml · kg1 · min1)
basis. When age-related differences in body fat were eliminated from
the calculation of
O2 max,
O2 max per kilogram of
FFM was 16-17% lower (P < 0.001) in the older subjects. When expressed per kilogram of
appendicular muscle, older men and women had
O2 max values that were
13-14% lower (P < 0.001).
These age differences were similar in both genders, but it was apparent
that the range of muscle mass in the older women was substantially less
than it was in the other groups. Maximal heart rates averaged
20-30 beats/min lower in the older subjects.
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O2 max values (l/min)
plotted as a function of appendicular muscle mass with separate
regression lines drawn for the young and older subjects. ANCOVA
revealed that the apparent downward shift in this relationship was
significant (P < 0.001) for the
older groups, averaging 0.5 ± 0.09 l/min less than for the young
groups at a given mass of appendicular muscle. In the analysis, all
interaction terms (muscle mass × age, muscle mass × gender,
age × gender) were found to be nonsignificant
(P = 0.22-0.86). When these
interaction terms were removed from the model, the age-associated
changes in the relationship between O2 max and muscle mass
were not significantly influenced by gender
(P = 0.22). ANCOVA also revealed
significant age differences for
O2 max
expressed per kilogram of leg muscle and FFM (data not shown).
O2 max) values plotted
against appendicular muscle mass. 
, Young women; 
, young men;
, older women; 
, older men. Analysis of covariance indicated that regression line of older subjects
(O2 max = 
0.08 + 0.14 · muscle mass) was 0.5 ± 0.09 l/min less for
a given muscle mass than it was for young subjects
(O2 max = 0.42 + 0.14 · muscle mass). Age difference = 0.05 ± 0.09 l/min. This demonstrates that aerobic capacity per kilogram of
appendicular muscle is reduced in highly trained older men and women.
DISCUSSION
The major new finding of this study is that
O2 max per kilogram of
limb muscle is reduced in highly trained older men and women.
Graphically, the relationship between total body
O2 max (l/min) and
skeletal muscle mass is shifted downward in the older subjects when age
and gender differences in muscle mass are considered appropriately by
ANCOVA (Fig. 1). Because we studied chronically endurance-trained
subjects, these findings are also unlikely to be confounded by
age-associated differences in muscle quality or subject motivation.
This means that there is a reduced aerobic capacity per kilogram of
active skeletal muscle, which contributes to the reduced
O2 max seen in highly
trained older subjects.
O2 max with aging?
The possibility that skeletal muscle loss plays an important
role in the age-associated decline in
O2 max was originally suggested by Fleg and Lakatta (10). They found that the age-associated decline in O2 max
(ml · kg1 · min1)
of sedentary men and women (age 22-87 yr) was blunted by
~50% when normalized to urinary creatinine excretion, an index of
whole body muscle mass. However, these results could be confounded in at least two ways. First, none of their subjects exercised regularly, and thus it is likely that their older subjects were less physically active than were their young subjects. Because skeletal muscle O2 capacity (i.e., oxidative
enzyme activity, capillarization) and tolerance to heavy exercise are
reduced in sedentary older subjects (5, 26), it is difficult to know
how the use of sedentary subjects might affect the relationship between
O2 max and muscle mass
with aging. A second confounding aspect of the study of Fleg and
Lakatta is that it is unclear what relevance measures of whole
body muscle mass have as determinants of
O2 max when almost all
of the O2 consumed during
treadmill O2 max
testing is used by the limb muscles, especially the legs (16, 17, 21,
29).
In the present study, we attempted to clarify these issues by studying
chronically endurance-trained subjects and quantifying active muscle
mass by using regional DXA measurements. The
O2 max expressed per
kilogram body weight was 22-26% lower in the older than in the
young athletes, but
O2 max per kilogram of
appendicular muscle was only 13-14% lower (Table 2). These
differences were also seen when
O2 max was expressed
per kilogram of leg muscle (11-13% lower, data not shown). Thus
it appears that nearly one-half of the age-associated decline in
O2 max expressed per
kilogram body weight in these highly trained subjects was due to
age-associated changes in body composition, including increased body
fat and loss of appendicular muscle mass.
Because adjustment of
O2 max for FFM or
skeletal muscle mass factors out the influence of adipose tissue, our
data might be interpreted to suggest that body fat accumulation, and
not muscle loss, contributed to the decline in whole body
O2 max in these
subjects. However, it is important to recognize that the higher body
fat of the older subjects most likely represents a reciprocal loss of
lean (muscle) tissue throughout life. Although losses of muscle and
gains in fat with aging are generally less in highly trained subjects
than in the general population (18), losses in appendicular muscle mass
in these subjects (~2.7 kg) do appear to contribute importantly to
the reduced whole body O2 max values of older
endurance-trained men and women. The only exception might be elite
older male endurance athletes who can be very lean (8-15% body
fat) and whose O2 max
values expressed as liters per minute, milliliters per kilogram per
minute, and milliliters per kilogram of FFM per minute are all
similarly reduced (~10-15%) compared with young athletes having
similar absolute training and/or performance characteristics
(11, 12).
Does aerobic capacity per kilogram muscle decline in highly trained
older subjects?
To the best of our knowledge, there have been no studies of trained
older subjects that have estimated active muscle mass (e.g.,
appendicular muscle mass) or applied ANCOVA to properly adjust
O2 max for age- or
gender-based differences in body composition (31). In this context, the
present study is the first to demonstrate that there is a reduction in
aerobic capacity per unit active muscle in highly trained older men and
women (Fig. 1). This analysis showed that
O2 max averaged 0.50 l/min less per kilogram of appendicular muscle in the older subjects. A
significant age difference was also observed for
O2 max expressed per
kilogram of leg muscle (data not shown).
The reduced aerobic capacity per kilogram limb muscle could reflect
reduced O2 extraction by the
active muscles and/or reduced O2 delivery to the active muscles.
Although neither muscle biopsies nor limb
O2 extraction measurements were
obtained for the present subjects, previous studies (6, 27), including
one from our laboratory (26), have shown that muscle oxidative enzyme
activities and capillarization are similar to or higher in older
compared with young men having physiological characteristics and
training histories similar to those of the current
subjects. Although data on muscle characteristics are not
available for highly trained older women, the peripheral adaptations of
older women to endurance training are not compromised by aging (5, 28).
Therefore, it is unlikely that skeletal muscle oxidative capacity or
capillarization is responsible for the age-associated reduction in
aerobic capacity per kilogram muscle seen in our trained older
subjects. The most likely explanation of this difference is the
well-documented decline in maximal cardiac output (and presumably
reduced peak muscle blood flow and
O2 delivery) associated with
aging.
This view is consistent with earlier observations made in elite older
endurance athletes who should have maximized any peripheral adaptations
to training (9, 11, 27). In these studies, older athletes were matched
with young athletes having similar training and/or endurance
performance characteristics to examine the influence of age on
O2 max and its
physiological determinants. When this is done, there has tended to be
little difference in FFM or body fat between the young and older
groups. Consequently, O2 max in liters per
minute, milliliters per kilogram per minute, and milliliters per
kilogram of FFM per minute are reduced to a similar extent in the older
compared with young athletes. Thus it is likely that a reduced aerobic
capacity per kilogram of limb muscle also occurs in the most highly
trained and genetically gifted older subjects as a result of reduced
maximal O2 delivery.
Are there gender differences in aerobic capacity per kilogram
muscle?
When gender differences in total fat mass are factored out by
normalizing O2 max to
kilograms of FFM, the gender difference in
O2 max often disappears
(3, 7). The present study appears to be the first to document this in
highly trained young or older subjects by using region-specific
analysis of muscle mass. Aerobic capacity per kilogram of appendicular
muscle was virtually identical in this sample of highly trained men and
women (Table 2), and aging caused a similar decline in both genders.
These findings provide additional support for expressing
O2 max per unit of fat-free tissue when comparing the performance of the
cardiovascular-respiratory system of individuals who differ in body
size or composition (7, 8, 30, 31).
Summary.
The findings of the present study demonstrate that there is a reduced
aerobic capacity per kilogram of appendicular muscle in highly trained
older men and women that contributes to their reduced whole body
O2 max with aging. The
age-associated change in
O2 max per kilogram of
appendicular muscle appears to be similar in highly trained older men
and women. This difference is likely to result from reduced
O2 delivery during maximal
exercise and is independent of age-associated changes in body
composition.
ACKNOWLEDGEMENTS
We are grateful to the women and men who participated as subjects in this study. We also thank Tammy Eickoff, Darrell Loeffler, John Halliwill, Peggy Helwig, Peter Shen, and Robin Shumway for technical assistance; Dr. Peter Wollan for statistical advice; and Janet Beckman for secretarial assistance.
FOOTNOTES
Address for reprint requests: D. N. Proctor, Anesthesia Research, Mayo Clinic, 200 First St. SW, Rochester, MN 55905.
Received 10 December 1996; accepted in final form 3 January 1997.
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 S. A. Hawkins, R. A. Wiswell, and T. J. Marcell Exercise and the Master Athlete--A Model of Successful Aging? J. Gerontol. A Biol. Sci. Med. Sci., November 1, 2003; 58(11): M1009 - 1011. [Abstract] [Full Text] [PDF]
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R. T. Hepple, J. L. Hagen, D. J. Krause, and C. C. Jackson Aerobic power declines with aging in rat skeletal muscles perfused at matched convective O2 delivery J Appl Physiol, February 1, 2003; 94(2): 744 - 751. [Abstract] [Full Text] [PDF]
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A. M. Matsumoto Andropause: Clinical Implications of the Decline in Serum Testosterone Levels With Aging in Men J. Gerontol. A Biol. Sci. Med. Sci., February 1, 2002; 57(2): M76 - 99. [Full Text]
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D. N. Proctor, J. D. Miller, N. M. Dietz, C. T. Minson, and M. J. Joyner Reduced submaximal leg blood flow after high-intensity aerobic training J Appl Physiol, December 1, 2001; 91(6): 2619 - 2627. [Abstract] [Full Text] [PDF]
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R. A. Wiswell, S. A. Hawkins, S. V. Jaque, D. Hyslop, N. Constantino, K. Tarpenning, T. Marcell, and E. T. Schroeder Relationship Between Physiological Loss, Performance Decrement, and Age in Master Athletes J. Gerontol. A Biol. Sci. Med. Sci., October 1, 2001; 56(10): M618 - 626. [Abstract] [Full Text] [PDF]
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 B. J. Maron, C. G. S. Araujo, P. D. Thompson, G. F. Fletcher, A. B. de Luna, J. L. Fleg, A. Pelliccia, G. J. Balady, F. Furlanello, S. P. Van Camp, et al. Recommendations for Preparticipation Screening and the Assessment of Cardiovascular Disease in Masters Athletes : An Advisory for Healthcare Professionals From the Working Groups of the World Heart Federation, the International Federation of Sports Medicine, and the American Heart Association Committee on Exercise, Cardiac Rehabilitation, and Prevention Circulation, January 16, 2001; 103(2): 327 - 334. [Full Text] [PDF]
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J. A. Kent-Braun and A. V. Ng Skeletal muscle oxidative capacity in young and older women and men J Appl Physiol, September 1, 2000; 89(3): 1072 - 1078. [Abstract] [Full Text] [PDF]
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H. T. Yang and Y. Feng bFGF increases collateral blood flow in aged rats with femoral artery ligation Am J Physiol Heart Circ Physiol, January 1, 2000; 278(1): H85 - H93. [Abstract] [Full Text] [PDF]
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B. E. Hunt, K. P. Davy, P. P. Jones, C. A. DeSouza, R. E. Van Pelt, H. Tanaka, and D. R. Seals Role of central circulatory factors in the fat-free mass-maximal aerobic capacity relation across age Am J Physiol Heart Circ Physiol, October 1, 1998; 275(4): H1178 - H1182. [Abstract] [Full Text] [PDF]
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D. N. Proctor, P. H. Shen, N. M. Dietz, T. J. Eickhoff, L. A. Lawler, E. J. Ebersold, D. L. Loeffler, and M. J. Joyner Reduced leg blood flow during dynamic exercise in older endurance-trained men J Appl Physiol, July 1, 1998; 85(1): 68 - 75. [Abstract] [Full Text] [PDF]
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M. J. Rosen, J. D. Sorkin, A. P. Goldberg, J. M. Hagberg, and L. I. Katzel Predictors of age-associated decline in maximal aerobic capacity: a comparison of four statistical models J Appl Physiol, June 1, 1998; 84(6): 2163 - 2170. [Abstract] [Full Text] [PDF]
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D. N. Proctor, K. C. Beck, P. H. Shen, T. J. Eickhoff, J. R. Halliwill, and M. J. Joyner Influence of age and gender on cardiac output-VO2 relationships during submaximal cycle ergometry J Appl Physiol, February 1, 1998; 84(2): 599 - 605. [Abstract] [Full Text] [PDF]
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