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O2
kinetics in old and young individuals
The Centre for Activity and Ageing, Faculty of Kinesiology, and Department of Physiology, The University of Western Ontario, London, Ontario, Canada N6A 3K7
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Chilibeck, P. D., D. H. Paterson, D. A. Cunningham, A. W. Taylor, and E. G. Noble. Muscle capillarization,
O2 diffusion distance, and
O2 kinetics in old and
young individuals. J. Appl. Physiol.
82(1): 63-69, 1997.
The relationships between muscle capillarization, estimated O2
diffusion distance from capillary to mitochondria, and
O2 uptake
(O2) kinetics
were studied in 11 young (mean age, 25.9 yr) and 9 old (mean age, 66.0 yr) adults. O2
kinetics were determined by calculating the time constants (
) for
the phase 2 O2 adjustment to and
recovery from the average of 12 repeats of a 6-min, moderate-intensity
plantar flexion exercise. Muscle capillarization was determined from
cross sections of biopsy material taken from lateral gastrocnemius.
Young and old groups had similar
O2 kinetics
(O2-on = 44 vs. 48 s;
O2-off = 33 vs. 44 s, for young and old, respectively), muscle capillarization, and
estimated O2 diffusion distances.
Muscle capillarization, expressed as capillary density or average
number of capillary contacts per fiber/average fiber area, and the
estimates of diffusion distance were significantly correlated to
O2-off kinetics in the
young (r = 
0.68 to 0.83;
P < 0.05). We conclude that
1) capillarization and
O2 kinetics during exercise
of a muscle group accustomed to everyday activity (e.g., walking) are
well maintained in old individuals, and
2) in the young, recovery of O2 after exercise is
faster, with a greater capillary supply over a given muscle fiber area
or shorter O2 diffusion distances.
aging; plantar flexion; lateral gastrocnemius
INTRODUCTION THE KINETICS of O2
uptake ( Recent studies in our laboratory (3, 9, 14) have shown that the
kinetics of METHODS Table 1.
Subject characteristics
O2)
adjustment to moderate-intensity exercise have been reported for
different exercise perturbations (e.g., supine vs. upright, arms vs.
legs) (8, 19) and in subject groups of different fitness levels (2,
10). Nevertheless, debate continues regarding the control mechanisms of
O2 kinetics. Various studies
have suggested that the limiting factor in the control of
O2 kinetics may be
the rate of response of the central circulation (21), blood flow
distribution to the active muscle (19), or the sites of metabolic
control of muscle oxidative phosphorylation (27). Hughson and Imman
(20) have used perturbations of circulatory occlusion to nonexercising
limbs or lower body negative pressure (19) to show that
O2 kinetics can be highly influenced by changes in peripheral circulation. Recent studies (34)
have used Doppler measures of arterial blood flow velocity to estimate
the rate of change in muscle blood flow in relation to
O2 kinetics during the
adjustment to or recovery from exercise. The present study was
designed to use another approach to examine the relationship of
peripheral circulation to O2
kinetics by investigating the relationship between muscle
capillarization and O2
kinetics.
O2 adjustment to
moderate-intensity cycling exercise are slower in sedentary old
compared with young individuals. However, we have shown that
O2 kinetics during ankle
plantar flexion are similar in old and young subjects (9). The plantar
flexor muscle group may be well trained in this population of old
individuals, since it is used on a daily basis during walking activity.
Babcock et al. (2) have shown that training of old individuals can
result in an improvement in
O2 kinetics to levels that
are similar to those in young subjects. The reasons for improved rate
of O2 kinetics in trained old
individuals are not clear. Improvement in the rate of peripheral
O2 delivery to working muscle may
be one factor, because muscle capillarization has been found to be
improved with endurance training (12) to levels that are similar to
those in young individuals (13). This possible relationship between
O2 kinetics and
capillarization has not been studied. Thus, the design of the present
study included studies in old and young individuals, with the
hypothesis that O2
kinetics during ankle plantar flexion would be similar in old compared with young individuals and would be related to capillarization, which
should be maintained in the plantar flexors of the old.
O2 kinetics during plantar
flexion exercise and muscle capillarization of the lateral
gastrocnemius were measured in 9 old and 11 young individuals. Subject
characteristics are listed in Table 1. Subjects were
moderately active but not well trained. Older subjects reported walking
as the primary form of exercise. These individuals were recruited from
activity classes, where group walking was performed two to three times
per week for ~30 min per day. Subjects had been participating in this
class for an average of 18 mo (with a range from 9 to 35 mo). Values
for maximal O2 uptake indicated
that subjects were of average fitness for their respective age groups
(30). All gave informed consent to participate in this study, which was
approved by the University Review Board for Research Involving Human
Subjects.
Group
n
Age, yr
Mass, kg
Height, cm
O2 max,
ml · kg
1 · min1
Young
11
25.9 ± 2.1
77.7 ± 16.4
174.5 ± 10.0
43.6 ± 9.3
Old
9
66.0 ± 6.3
70.7 ± 13.3
165.7 ± 8.8
20.6 ± 2.5
Values are means ± SD. Young group, n = 5 men, 6 women;
old group, n = 2 men, 7 women.
O2 max, maximal
O2 uptake.
O2
kinetics, subjects performed 12 6-min square-wave transitions to and
from ankle plantar flexion exercise, during three to four separate
laboratory visits. The intensity was set at 45% of peak work rate,
which averaged 1.6 and 3.4 W for old and young subjects, respectively.
This work rate could be considered moderate, as further ramp testing
determined that the work rates were below the subjects' pH
intracellular threshold, as determined by
31P-nuclear magnetic resonance
spectroscopy (28). This threshold is considered the point
at which anaerobic glycolysis is increased, as evidenced by an
increased rate of change in pH (28). A large number of transitions were
performed to improve the signal-to-noise ratio (24), in light of the
small amplitude of the O2
response with the small-muscle group exercise. Transitions were
separated by 6 min of loadless plantar flexion and were initiated
manually by the experimenter. Subjects were blinded to the initiation
and termination of square-wave changes in work rate.
O2 was measured using a
modification of the methods of Babcock et al. (3). Inspired and expired
gas flows were measured by using a low-dead space (90-ml) bidirectional
turbine (VMM 110, Alpha Technologies) calibrated by a 3.01-liter
syringe, and gas concentrations were measured by a mass spectrometer
(Airspec 2000 MGR 9N) calibrated against precision-analyzed gas
mixtures. Changes in gas concentration were aligned with gas volumes by
measuring the time delay for a square-wave bolus of gas passing the
turbine to the resulting changes in fractional gas concentrations as
measured by the mass spectrometer. Data collected every 20 ms were
converted from analog to digital format and stored for later processing by a microcomputer.
Breath-by-breath alveolar gas-exchange data were calculated using the
algorithms of Beaver et al. (5). Breath-by-breath data were
interpolated to 1 s, with square-wave repeats time aligned and
averaged. Averaged responses for each subject were fit, using a
first-order (monoexponential) model of the form
![<IT>Y</IT>(<IT>t</IT>) = a{1 − <IT>e</IT><SUP>−[(<IT>t</IT>−&dgr;)/<IT>r</IT>]</SUP>}](/content/vol82/issue1/fulltext/63/img001.gif)
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O2
at time (t); and a, 
, and are
the amplitude, time delay, and time constant of the response,
respectively. The monoexponential curves were fit from the start of the
phase 2 (20-s) portion of the
O2 response (37). Twenty
seconds is considered to be a reasonable duration of
phase 1 during the adjustment to
cycling exercise and represents the transport time for blood-borne gas-exchange signals present in the contracting muscles to be expressed
at the lung (37). During cycling exercise, there is a larger
cardiovascular, as well as metabolic, readjustment to exercise,
compared with plantar flexion exercise. Whether cardiac output and
venous return increase at the same rate during the adjustment to both
exercise tests and whether phase 1 is
the same duration are unknown. We have recently found that heart rate
kinetics during the transition to plantar flexion and
cycling exercise are similar in young individuals (11). This supports
the argument that cardiac output adjustment and phase
1 are similar in the two exercises. Solutions for a,
, and were derived from an iterative optimization computer
routine.
Muscle biopsies.
Needle biopsy samples were obtained from the lateral head of the right
gastrocnemius of each subject. These were oriented longitudinally in
embedding media, frozen in liquid
N2-cooled isopentane, and stored
in liquid N2. Frozen sections were
cut, at a width of 10 µm, on a microtome cryostat (Leitz Lauda 1720), mounted on glass coverslips, and analyzed for capillarization by
staining with periodic acid-Schiff's reagent, according to the method
of Anderson (1). Fiber type composition was determined by using the
stain for adenosinetriphosphatase activity after preincubation at pH
4.3, 4.6, and 10.3 (6). Sections were magnified and projected on an
image analyzer (Quantimet 520) for counting of capillaries and fibers.
The number of muscle fibers in sections averaged 134 ± 63 (range
44-255). Muscle capillarization was expressed as capillary density
(total number of capillaries in a section divided by the total area),
capillary-to-fiber ratio (C/F; total number of capillaries in a section
divided by the number of fibers), the average number of capillaries in
contact with each fiber (CC), and the average number of capillaries in
contact with each fiber divided by the average fiber area (CC/FA).
Average and maximal diffusion distances for
O2 from capillary to muscle fiber
were estimated, using the equations developed by Snyder (35), for capillaries distributed in random arrays
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![(capillary-to-fiber ratio)] × <RAD><RCD>average fiber cross-sectional area</RCD></RAD>](/content/vol82/issue1/fulltext/63/img003.gif)
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![(capillary-to-fiber ratio)] × <RAD><RCD>average fiber cross-sectional area</RCD></RAD>](/content/vol82/issue1/fulltext/63/img005.gif)
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O2 were calculated,
based on the O2 response
amplitude and the SD of breath-by-breath
O2 fluctuation, as
described by Lamarra et al. (24). Comparisons of
O2 were made by using a
three-factor analysis of variance (ANOVA) with age (old vs. young) and
gender (men vs. women) as between-subjects factors and repeated
measures on square-wave transients (on vs. off). Comparisons of fiber
types, capillarization, and diffusion distances were made using a
two-factor (age × gender) ANOVA. Pearson product correlations
were used to compare
O2 with measures of
muscle capillarization, diffusion distances, and fiber type
composition. P < 0.05 was accepted
as significant.
RESULTS
No effects due to gender were found for any measures. With the inclusion of only two old men, our comparison between genders is weak; this is a limitation of the present study. Using larger groups, others have found differences in capillary measures between genders, with men having a greater capillarization than women (13). For simplicity, all results are presented with subjects grouped by age (old vs. young).
O2-on and -off responses to
plantar flexion exercise for an old and young subject, along with
monoexponential fits, are depicted in Figs.
1 and 2,
respectively. Results for
O2, summarized in Table
2, showed no significant difference in
O2 between young and old,
and within age groups no difference was seen between on- and
off-kinetics. With use of the equations developed by Lamarra et al.
(24), the 95% confidence intervals, determined from the group mean
data, for estimation of O2
(for both on- and off-transients) were ±11.5 s
and ±8.4 s for old and young groups, respectively. This is based on
the O2 steady-state
amplitudes, which averaged 0.08 and 0.11 l/min for old and young
groups, respectively, and the SD of breath-by-breath fluctuations,
which averaged 0.067 l/min for both old and young groups.
O2) during on-transition to
ankle plantar flexion in an older individual, along with
monoexponential fit during phase 2 (i.e., after 20 s; O2 = 47 s). , Time constant. B: O2 during off-transition
(O2 = 37 s).
O2 during on-transition to
ankle plantar flexion in a young individual, along with monoexponential
fit during phase 2 (i.e., after 20 s;
O2 = 39 s).
B:
O2 during off-transition (O2 = 43 s).
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Muscle capillarization, fiber areas, and diffusion distances are summarized in Table 3. Fiber type composition is summarized in Table 4. No differences were found between old and young groups for any of the variables (P > 0.05).
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For combined groups, O2
was generally faster with increased muscle capillarization, with
correlations between various measures of muscle capillarization and
O2 kinetics ranging
from 0.23 to 0.59 (Table
5). Correlations for capillary
density vs. O2-off (0.48) and CC/FA vs.
O2-off (0.59) were
significant (P < 0.05). The
correlation between maximal or average diffusion distance vs.
O2-off approached
significance (P = 0.052). For
individual groups, capillary density, CC/FA, and diffusion distances
were significantly correlated with
O2-off in the young group
only (Table 5). There were no significant relationships between
O2 and capillarization for
the older group (Table 5). Figure 3 shows the individual points for the relationships of
O2-off kinetics with capillary density, CC/FA, and maximal diffusion distance. Correlations between O2
kinetics and fiber type composition (% type I) were not significant.
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O2-off and capillary
density. Young (
), r = 0.68
(P = 0.02); old (
),
r = 0.07 (NS); combined groups,
r = 0.48
(P = 0.03). Regression line is for
young group only. B: correlation
between O2-off and average
no. of capillaries in contact with each other (CC)/fiber area (FA; see
Table 3). Young (), r = 0.83
(P = 0.002); old (),
r = 0.10 (NS); combined groups,
r = 0.59
(P = 0.007). Regression line is for
young group only. C: correlation
between O2-off and
estimated O2 diffusion distance.
Young (), r = 0.68 (P = 0.02); old (),
r = 0.17 (NS); combined groups,
r = 0.44 (NS;
P = 0.052). Regression line is for
young group only.
DISCUSSION
Our finding that plantar flexion
O2 kinetics were not slower
in the group of old subjects may be due to the level of training of the
plantar flexors in this population. In an earlier study, which included
four of the nine old individuals of the present study,
O2 kinetics during cycle
ergometry were slower in the old (9), in agreement with previous
results from this laboratory (3, 14). The differences between results
may be due to the training of the muscle group tested. The plantar
flexors are used to a great extent in everyday activity (e.g., walking)
and may be relatively well trained in the old subjects. Babcock et al. (2) have shown that specific training of older subjects can substantially improve the rate of
O2 kinetics to levels similar to those of young fit individuals.
Usually, measurements of O2
kinetics have been performed during cycle exercise, as opposed to the
plantar flexion exercise used in the present study. We used plantar
flexion to compare O2
kinetics with capillarization of a specific muscle (the lateral gastrocnemius). Electromyographic (EMG) analyses have shown that cycle
exercise involves the recruitment of many muscle groups of the leg
(23); therefore, comparison of kinetics with biopsy data of one muscle
group (i.e., the vastus lateralis) may be invalid. Results from a
previous study, in which we assessed muscle recruitment with magnetic
resonance imaging and EMG, demonstrated that the lateral and medial
portions of the gastrocnemius are dominant during submaximal ankle
plantar flexion, and there is minimal contribution from other muscle
groups, such as the soleus or quadriceps (29). We therefore conclude
that O2 kinetics measured
during ankle plantar flexion reflect the exercise of the gastrocnemius and that comparisons with biopsy data from the lateral portion of this
muscle are warranted.
Our results for capillarization of the lateral gastrocnemius were very
similar to those of both the old and young groups of Coggan et al.
(13), with the exception that the C/F ratio of our group was elevated.
When capillary data were assessed across studies, it has been suggested
that the best measure to use for comparison is C/F ratio, since a
measure such as capillary density is highly influenced by muscle fiber
size, which in turn may be affected by shrinkage during histochemical
preparation techniques that vary from laboratory to laboratory (32).
The averages for each of our measures of capillarization tended to be
lower in old compared with young groups (Table 3). Whereas differences between our groups were not significant, with a larger sample size,
Coggan et al. (13) detected significant differences, with lower levels
of capillarization in lateral gastrocnemius of the old group. The
subjects of the study of Coggan et al. (13) were described as
sedentary, whereas we considered our subjects to be moderately active
and involved in walking on a regular basis. The C/F ratio (1.93; Table
3) of our young group was in the middle of the range from the
literature for C/F ratios of lateral gastrocnemius for young (range = 1.11-2.51; Refs. 7, 13, 26). C/F ratio of our old group (1.72;
Table 3) was similar to the range from two Scandinavian studies
(1.48-1.96; Refs. 15 and 16), but as mentioned, it was higher than
that of the old subjects (1.39 for old men and 0.94 for old women) of
Coggan et al. (13). Differences between studies may be due to the
training status of groups compared. Muscle capillarization appears to
be very sensitive to training in the old, as demonstrated by Coggan et
al. (12). Moderate training of older subjects resulted in substantial
increases in muscle capillarization, to levels similar to those of
their young group (13), despite the old still having substantially
lower levels of maximal O2.
The trained old subjects from the study of Coggan et al. (12) had a C/F
ratio (2.08 for men, 1.23 for women) that was closer to that of the old
individuals from the present study. The fact that most of our old
subjects performed moderate levels of walking on a daily basis could
have been a sufficient stimulus to offset any loss of capillarization
with aging.
The present data show that measures of capillarization were
significantly correlated with
O2 kinetics only when
expressed in relation to fiber area (Table 5, Fig. 3). Capillarization, expressed as CC/FA, had the strongest correlation with
O2 kinetics (Table 5, Fig.
3). This measurement gives an index of capillary supply to fiber
area, accounting for the effects of diffusion (31). Estimates of
diffusion distances, based on the equations of Snyder (35), differ in
that C/F, rather than CC, is used in relation to fiber area. As
suggested by Plyley (31), C/F and capillary density are global indices
of capillarization and yield little information on the capillary supply
of individual fibers. Therefore, CC/FA appears to offer a better
assessment of O2 delivery.
Nevertheless, measurement of capillary numbers alone may be an
oversimplification. Kinetics of O2
delivery may also be affected by branching patterns in the capillary
network, length of capillary paths, and capillary interconnections
(33), all of which would have to be measured in longitudinal as opposed to transverse sections of muscle (33). Another factor may be the rate
of capillary recruitment, which has been shown to affect O2 transport to dog gracilis
muscle at the onset of exercise (18). Estimates of diffusion distance
from capillary to cell interior, as done in this study, may be
inaccurate in assessing O2
diffusibility. Honig et al. (17) hypothesized that the principal
gradient for O2 diffusion is
across the capillary to the sarcolemma, rather than across the muscle
cell interior. Tissue gradients for
O2 are small, as myoglobin acts as
a buffer to keep PO2 relatively
uniform throughout the muscle cell (17). There may also be diffusion
interaction between muscle cells, which would complicate estimates of
diffusion from capillaries alone. The PO2 gradient from inactive to working
fibers is substantial, and the surface area for exchange is great
compared with that of capillaries (17).
We hypothesized that O2
kinetics may be related to the degree of muscle capillarization,
because it has been shown that kinetics can be highly influenced by
changes in peripheral circulation (19, 20). With increased
capillarization, diffusion distances from capillary to muscle fiber
interior are shorter (36) and there is an increased surface area for
O2 exchange (25), which together
should decrease the transport time of
O2 to mitochondria. In the present
study, correlations between
O2 kinetics and
capillarization per fiber area were in a direction indicating faster
kinetics with increased capillarization and shorter diffusion distances (Table 5). The modest correlations between simple measures of capillarization or diffusion distances and
O2 kinetics may be accounted
for by the complicating factors described above.
However, our data do reveal two important aspects to consider. First,
the findings show a significant relationship between O2 kinetics and
capillarization only in relation to the off-kinetics, not the
on-kinetics. Second, this relationship is significant in the young but
not in the old group of subjects.
The finding that capillarization was significantly correlated with
O2-off kinetics but not
O2-on kinetics suggests that O2 delivery may have a greater
influence on O2 recovery
than O2 adjustment to
exercise. This is supported by Idstrom et al. (22), who found that
the rate of recovery of phosphocreatine (PCr) after contractions of
perfused rat hindlimb was related to
O2 supply through the perfusate,
although the rate of PCr breakdown at the start of exercise was not.
Here, PCr kinetics are thought to reflect kinetics of muscle
O2 consumption (4). Tissue
gradients for O2 are small during
exercise on-transients due to myoglobin buffering (17); this may
prevent O2 transport from limiting kinetics during the adjustment to moderate exercise. Whether
O2 transport is sufficient to
prevent myoglobin desaturation and larger
O2 gradients during recovery is
unknown. If myoglobin desaturates during recovery,
O2 diffusion distance from
capillary to fiber may affect kinetics of
O2.
We hypothesized that capillarization would be lower in the old and that
this would result in slow O2
kinetics. However, we found no significant reduction in measures of
capillarization in the old and no relationship of capillarization to
O2 kinetics. O2 kinetics in the old might
be more related to mitochondrial density (27).
The findings of this study indicate the following.
1)
O2 kinetics and muscle
capillarization are well maintained in the old for a muscle group (the
plantar flexors) used extensively during everyday activity.
2) Correlations between
O2 kinetics and muscle
capillarization are strongest when capillarization is related to fiber
area, thus accounting for diffusion distances. 3) Rate of
O2 delivery is probably affected
by the interaction of many factors (i.e., capillary path lengths,
capillary branching, capillary recruitment patterns, and
O2 diffusion from adjacent muscle
cells), and estimating capacity for
O2 delivery from individual measures of capillarization may be an oversimplification.
4) Capillarization has a stronger
relationship with O2-off than
with O2-on kinetics. 5) Capillarization has a stronger
relationship with O2 kinetics in
young than in old individuals. Other factors such as mitochondrial density may control O2 kinetics in
the old.
ACKNOWLEDGEMENTS
We express our gratitude to the subjects in this study and acknowledge the laboratory assistance provided by Brad Hansen.
FOOTNOTES
Address for reprint requests: D. H. Paterson, The Centre for Activity and Ageing, The Univ. of Western Ontario, London, Ontario, Canada N6A 3K7.
Received 28 February 1996; accepted in final form 22 August 1996.
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