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O2 peak and the
capillary supply to skeletal muscle
Department of Physiology, Graduate Department of Community Health, and Department of Physical Therapy, University of Toronto, Toronto, Ontario, Canada M5S 3J7
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Hepple, R. T., S. L. M. Mackinnon, J. M. Goodman, S. G. Thomas, and M. J. Plyley. Resistance and aerobic training in older
men: effects on
O2 peak and the
capillary supply to skeletal muscle. J. Appl.
Physiol. 82(4): 1305-1310, 1997.
Both aerobic training (AT) and resistance training (RT) may increase aerobic power
(O2 peak) in the
older population; however, the role of changes in the capillary supply
in this response has not been evaluated. Twenty healthy
men (age 65-74 yr) engaged in either 9 wk of lower body RT
followed by 9 wk of AT on a cycle ergometer (RT
AT group) or 18 wk of AT on a cycle ergometer (ATAT group). RT was performed
three times per week and consisted of three sets of four exercises at
6-12 repetitions maximum. AT was performed three
times per week for 30 min at 60-70% heart rate
reserve. O2 peak was increased
after both RT and AT (P < 0.05).
Biopsies (vastus lateralis) revealed that the number of capillaries per fiber perimeter length was increased after both AT and RT
(P < 0.05), paralleling the changes
in O2 peak, whereas
capillary density was increased only after AT
(P < 0.01). These results, and the
finding of a significant correlation between the change in capillary
supply and O2 peak
(r = 0.52), suggest the possibility that similar mechanisms may be involved in the increase of
O2 peak after
high-intensity RT and AT in the older population.
capillaries; aerobic power; aging; oxygen flux
INTRODUCTION THE HYPOTHESIS that the capillary supply to skeletal
muscle may play a vital role in determining aerobic metabolic function is supported by work with animal models (22), young athletic humans
(17), and investigations suggesting that muscle diffusing capacity
limits maximal oxygen consumption
( METHODS
O2) (27). In
this respect, aging and inactivity have been found to result in a
reduction of the capillary supply to skeletal muscle (3) and a
reduction in whole body aerobic power
(O2 peak) (31), whereas
aerobic training (AT) of sedentary older persons is associated with an increase in both
O2 peak and the
capillary supply (4). Because high-intensity resistance
training (RT) has also been suggested to increase the
O2 peak in this
population (8), an examination of the role of the capillary changes,
relative to the increases in
O2 peak observed with
both types of training, would seem to be warranted. Consistent with
this line of reasoning we recently demonstrated that RT in older men is
associated not only with an increased
O2 peak but
also with an increase in the capillary supply to the skeletal muscle
fibers (13). Furthermore, given the significance that has
been ascribed to the changes in muscle function with aging, it is
possible that there may be a synergistic effect of a combined RT and AT
program. To examine these issues, we compared the effects of a
sequential RT and AT program with those of an exclusively AT program in
a group of healthy older men, focusing on the changes in
O2 peak and changes in
muscle capillary supply.
150 Torr; diastolic blood pressure 90 Torr), and had been
nonsmokers for at least 10 yr before beginning the study. While none of
the subjects participated in regimented physical training before
starting the study, most engaged in periodic low-intensity physical
activity consisting of golf, tennis, and/or walking two or
fewer times per week. All subjects were informed of the procedures,
risks, and benefits, and they gave written consent for participation in
the study.
AT)
underwent 9 wk of RT designed to increase the muscle strength of the
lower body, followed by 9 wk of AT (programs described in
RT and
AT). The second group
(ATAT) underwent two consecutive 9-wk periods of AT (i.e., 18 wk total).
RT.
Each subject in the RTAT group participated in a RT program
three times per week for 9 wk. Each training session consisted of a
warm-up and cool-down series of stretching exercises and three sets of
four resistance exercises, performed on each leg separately and at an
intensity regularly adjusted to elicit fatigue within 6-12
repetitions (i.e., 6-12 repetitions maximum) on Universal weight
machines. On the basis of the reported effect of circuit-types of RT as
an AT stimulus in a young adult population (25), a minimum of 2 min of
recovery were taken between each exercise to prevent a circuit-training
benefit.
AT.
The subjects participated in AT on a cycle ergometer, for 30 min, three
times per week, for either 9 (RTAT group) or 18 wk (ATAT group). The exercise intensity was determined by using the modified Karvonen formula (18). Heart rate was measured at 5-min
intervals with the aid of heart rate monitors (Polar), and logs were
maintained to monitor subject compliance and progress.
O2 peak.
The O2 peak was
assessed before training was begun (T1), after 9 wk of training (T2),
and after 18 wk of training (T3) on an electrically braked cycle
ergometer (Collins Pedalmate) fitted with toe clips, by using an
incremental protocol to voluntary exhaustion under the supervision of a
physician. Subjects were given a 5-min warm-up at 50 W, followed by 5 min at 100 W. After a brief recovery of 5 min, individuals were brought
to maximum effort by using step increases in power output, beginning at
75 W (2 min) and progressing to 100 W (2 min), with subsequent power output increments of 16.7 W/min to fatigue. The criteria
used for acceptance of
O2 peak values as a
maximum included two or more of 1) a
heart rate greater than or equal to age-predicted maximum (±10
beats/min), 2) a respiratory
exchange ratio (RER = CO2
production/O2) 
1.10, or
3) a change in
O2 85 ml with an increase
in power output (i.e., one-half of the predicted rise in
O2 with an increase in
power output). Heart rate was monitored continuously from a V5 tracing
displayed on a built-in oscilloscope of the ECG-defibrillator
(Physiocontrol, Lifepak 9P). Blood pressure was monitored by using an
automated inflation system (Dynamap vital signs monitor, model 1846 SX), and gas analysis was performed with a metabolic cart (Morgan)
on-line with a microcomputer. Ventilatory volumes were assessed with a
ventilation monitor (Morgan Ventilometer Mark 2) connected to a
pneumotachograph on the inspiratory arm of the mouthpiece. Expired
gases were sampled and analyzed via an infrared
CO2 monitor (Jaeger
CO2-Test) and an
O2 analyzer (Ametek S3-A), which
utilized a stabilized zirconia cell heated to 750°C.
Muscle biopsy.
Percutaneous needle biopsies of the vastus lateralis of the dominant
leg were performed before the training program was begun according to
the method of Bergstrom (2), as adapted by Mubarak et al. (24). Samples
were obtained midway between the iliac crest and the upper border of
the patella, at a depth of 2-3 cm. The subsequent samples (i.e.,
after training: T2 and T3) were taken at a distance of 2 cm from the
original incision and at the same depth to minimize variation due to
muscle inhomogeneities (13). Local anesthetic (2% Xylocaine) was
administered to the subject before the incision. Muscle samples were
mounted in cross section in an embedding medium (OCT), immersed in
liquid isopentane cooled in liquid nitrogen, and stored at
80°C for subsequent histochemical analysis.
Histochemical analysis.
Specimens were sectioned to a thickness of 10 µm on a cryostat,
mounted on albumin-coated slides, and kept at 20°C until fixation. Histochemical processing was done within 1 wk of sectioning. The sections were first fixed for 5 min in a Guth and Samaha (10) fixative at room temperature and then incubated for 1 h at 36°C in
a Pb-adenosinetriphosphatase staining medium to simultaneously stain
for both fiber types and capillaries (28). No subtypes of the type II
fiber population are revealed with this method in human tissue.
Morphometry.
Muscle sections were viewed under a light microscope, on-line with a
microcomputer and an image-analysis system (Mocha, Jandel Scientific).
Capillaries were quantified manually from the microscope on each fiber
to estimate the folowing indexes: 1)
the number of capillaries around a fiber [capillary contacts
(CC)], 2) the capillary-to-fiber ratio on an individual-fiber basis
(C/Fi), and
3) the number of fibers sharing each
capillary [sharing factor (SF); Ref. 26; Fig.
1]. Quantitation of the
capillary supply was performed on 25 fibers of each type by randomly
selecting a fiber in an artifact-free region (free of connective tissue and demonstrating a uniform staining intensity among fibers of a given
type) and counting the closest 25 neighboring fibers of each type (4).
Fiber area (FA) and perimeter (P)
were measured with the image-analysis system and commercial software
(Mocha), calibrated to transform the number of pixels (viewed on a
computer monitor) into micrometers. Fiber type distributions were
determined by counting all of the fibers in a section [315 ± 26 (SE) muscle fibers; range 220-504 fibers]. All
quantitative analyses were performed blind by a single observer.
) + (1 × 1/2) = 2.17.
To examine the potential for blood-tissue exchange, the capillary density (CD) and the capillary-to-fiber perimeter exchange (CFPE) index (12) were calculated. The CD was calculated by using the fiber as the reference space, as described previously (6). The CFPE index was used to obtain an index of the size of the capillary-to-fiber interface and was determined from the following equation
|
RESULTS
O2 peak.
O2 peak data are based
on 10 subjects in the RTAT group at each time point while the
ATAT group
O2 peak data are based on 10 subjects at each of T1 and T2 and on 9 subjects at T3 (1 subject
dropped out after the T2 assessment). The RTAT group demonstrated significant increases in the
O2 peak after both RT
and AT (P < 0.05; Table
1). Body mass did not change
throughout the study in this group, and thus the pattern of the
alterations in mass-specific
O2 peak did not differ
from that observed for the absolute measures. There was also an
increase in the peak power output after both phases of training in the
RTAT group (P < 0.05), but
neither peak heart rate nor RER measured at exhaustion was found to
change with training.
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AT group also demonstrated a significant
increase in the
O2 peak after the first
9 wk of AT (P < 0.05) and a small, not statistically significant, increase in the second 9-wk period of
AT. However, because of the decrease of body mass from T1 to T3 in this
group, the mass-specific
O2 peak was
significantly increased after both 9 and 18 wk of training
(P < 0.05) in this group. There was
also a significant increase in the peak workload attained at exhaustion
after the first 9 wk of AT (P < 0.01). No further increase in the peak workload was observed in the
second 9 wk of training, consistent with the data for absolute
O2 peak. As was also
observed in the RTAT group, there were no significant differences in the peak heart rate or the peak RER attained at exhaustion. Due, in part, to considerable interindividual variation in the training response, the magnitude of the improvement in absolute O2 peak was
not significantly different between groups at either T2 or T3.
Muscle structure.
The morphometric data are presented in Table
2. Whereas 9 subjects
consented to the biopsy procedures at all three time points in the
RTAT group, the data in the ATAT group are based on
seven subjects at the T1 assessment, five at T2 (2 samples had
insufficient tissue for analysis), and seven at T3. The fiber type
distribution did not differ significantly across time points,
exhibiting a coefficient of variation of 9.1 ± 2.2% from T1 to T3.
The percentage of type I fibers was 59 ± 2% for the RTAT
group and 57 ± 6% for the ATAT group (average of
all 3 time points).
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AT group have been presented
previously (13) and are included here for comparison. Briefly, there
were significant increases in both the cross-sectional area and
P (P < 0.05) of the muscle fibers after RT (i.e., T1 to T2). These
alterations in fiber size were accompanied by a significant increase in
CC (P < 0.05) and the
C/Fi
(P < 0.05) and no change in the SF.
Whereas there was no change in CD after the RT period, the CFPE index
was significantly increased (indicative of a larger capillary-to-fiber
surface; P < 0.05).
After AT in the RTAT group (i.e., from T2 to T3), there were
significant reductions in both the cross-sectional area
(P < 0.05) and
P (P < 0.05) of the muscle fibers, which returned to values that were not
significantly different from those at T1. The reduction of the fiber
size after AT was associated with no further change in CC or in the
C/Fi, beyond the values that were observed after RT. As a result, there was a significant increase in the
CD (P < 0.01) and a further increase
in the CFPE index (P < 0.05) after
AT in this group.
The ATAT group demonstrated no significant alterations in
either the cross-sectional area or P
of the muscle fibers after 9 or 18 wk of AT. In contrast, there were
significant increases in CC (P < 0.05) and the C/Fi
(P < 0.05) and no significant change in the SF, after 18 wk of AT. After 9 wk of AT, both the CD and the
CFPE index increased (P < 0.01),
with no further changes in the second 9-wk phase of AT.
DISCUSSION
We found that in a population of older men, 9 wk of high-intensity RT
of the legs followed by 9 wk of AT on a cycle ergometer resulted in similar changes in both the
O2 peak and
the size of the capillary-fiber interface as did 18 wk of AT on a cycle ergometer. Both RT and AT resulted in significant increases in the
O2 peak and the
capillary supply to the skeletal muscle, suggesting similarities in the
mechanism of these training responses. In addition, it is noteworthy
that the changes in the CFPE index (related to the capillary-to-fiber
surface) paralleled the changes in
O2 peak as a
consequence of both RT and AT, whereas CD (related to diffusion
distances) was altered only after the AT.
O2 peak was reasonable.
In addition, it is noteworthy that there were no differences between
groups with respect to the number of subjects attaining the criteria
for determination of
O2 peak, nor were there
differences between testing periods (11), indicating that similar
efforts were put forth by the subjects at each testing period.
It is apparent from Tables 1 and 2 that there was a slight
(nonsignificant) difference in muscle fiber size and body mass between
groups before training, which, in theory, could have had an impact on
the adaptation to training. However, because the pattern of change in
fiber size and capillary number (i.e., whether there was an increase,
decrease, or maintenance with training) was not related to the initial
fiber size or body mass (unpublished observations), it seems unlikely
that these differences between groups had any bearing on the training
response.
O2 peak changes
after RT and/or AT.
The changes in absolute
O2 peak (l/min)
represented 17 and 16% of the initial values in the RTAT and
ATAT groups, respectively, comparable with recent studies of AT
in this population, where 7-38% increases in
O2 peak have been
observed (1, 19, 21). In a comparision of the responses between the two
groups, the similarity of training response suggests prior RT does not
have a synergistic effect on subsequent AT. It is also clear that RT alone provided a reasonably effective training stimulus for improving O2 peak, in agreement
with the results reported previously for high-intensity RT in this
population (8). While the RTAT group performed only one-half
the AT of the ATAT group, it is not apparent what the nature
and amount of stimulus delivered at the muscle tissue level might be.
It is possible that, despite probable differences in motor unit
recruitment between RT and AT [although we found no differences
in either the pattern or magnitude of adaptation between type I and
type II muscle fibers between resistance and AT (11)], RT may
have provided an "aerobic-like" stimulus to adaptation in these
older adults with respect to the adaptive process at the muscle level.
This possibility will be evaluated in light of the changes in capillary
supply that were observed.
Alterations in muscle morphometry: implications for blood-tissue
exchange.
Utilization of capillary measurements related to FA and
P on transverse sections of muscle
tissue provides a means of examining the significance of alterations in
the morphometric profile on the capacity for the different processes
that capillaries serve in blood-tissue exchange (12). Specifically,
there is evidence to suggest that the FA-based measurements of the
capillary supply (which relate to diffusion distances), such as the CD,
may relate better to the delivery of fuel substrates (7) to muscle
fibers and to the removal of waste products (30) from muscle fibers (i.e., processes that rely primarily on passive diffusion). In contrast, indexes of the capillary-to-fiber surface, such as the capillary-to-fiber P ratio (23) and
the CFPE index (12), may provide more relevant information regarding
the capacity for oxygen flux and the transport of substances from blood
that rely on carrier- or receptor-mediated processes at the muscle
fiber membrane (i.e., hormones, glucose, etc.).
As we have reported previously (13), the RT period resulted in a
maintenance of the CD but significantly increased the CFPE index,
indicating a larger surface area was available for exchange between the
capillaries and muscle fibers after the RT (i.e., T1)1
and suggesting there may be an increased capacity for oxygen flux after
the RT. In the subsequent period of AT, the increases in the CD and
CFPE index were due exclusively to a reduction in the fiber size rather
than an increase in capillary number from T2 to T3 in the RTAT
group, indicating no new capillary development occurred in this period.
This response may indicate that the muscle fiber hypertrophy evident
after the RT was not necessary for the AT period (because it was not
maintained) and that, as a consequence of the reduction of fiber size
and the resulting increase in capillary supply, there was no need for a
further increase in the number of capillaries.
In contrast, the ATAT group, after two consecutive 9-wk periods
of AT on a cycle ergometer, demonstrated a significant increase in
capillary number at T3 (i.e., CC and
C/Fi) with no change in fiber
size, resulting in an increased CD and an increased CFPE index at both
T2 and T3. The net result, however, is that both RT and AT were
associated with adaptations in the capillary supply that indicate the
potential for an increased capacity for oxygen flux (i.e., an increased
size of the capillary-to-fiber surface), and this similarity may help
explain the means by which
O2 peak is augmented
through these training paradigms in this population. Specifically, we
observed that the CFPE index was increased after both resistance and
AT, paralleling the increase in
O2 peak, whereas the CD
was increased only after AT. It is also relevant that the magnitude of
changes in capillary supply did not differ between groups, again
suggesting prior RT did not potentiate but rather complemented the
subsequent adaptation to AT in these subjects.
Role of the capillary supply in whole body
O2 peak.
There is mounting evidence that the capillary supply plays an important
role in determining the maximal rate of oxygen flux at the
muscle-capillary interface (15, 16, 22). A large number of studies have
suggested that the maximal O2
is limited by diffusive processes between the blood and tissues (14,
27), consistent with an important role for the capillary supply to skeletal muscle in this response. Of course, if there is an
optimization of structure and function, as proposed by others (20), we
would expect the capillary supply to be matched to the
O2 peak without necessarily implying a limitation per se.
Stepwise multiple-regression analysis revealed that the CFPE index
explained 40% of the variance in
O2 peak and
that addition of the CD to the regression equation did not
significantly improve the prediction. Figure
2 illustrates the relationship between the
capillary supply, as defined by the CD and the CFPE index, and
O2 peak across all time
points for all subjects. The training did not appear to alter the
nature of the relationships that were observed (i.e., the slopes of the
regressions were similar before and after training). In the
consideration of Fig. 2, it is important to recognize that there is
considerable evidence that strongly suggests it is not the diffusion
distance per se that is the most crucial aspect of the capillary supply
with respect to oxygen flux but rather the size of the
capillary-to-fiber surface (15, 22, 29). Thus the observation that the
CFPE index (an index of the capillary-to-fiber surface) explained a
larger proportion of the variance in
O2 peak than did the CD
(a determinant of diffusion distance) would tend to support this
hypothesis.
O2 peak)
when all of data points are combined
[O2 peak = 15.7 + (2.7558 × CFPE index);
r = 0.63, P < 0.01].
B: relationship between capillary
density and O2 peak
when all data points are combined
[O2 peak = 22.6 + (0.0178 × capillary density); r = 0.44, P < 0.01]. caps,
Capillaries.
A relationship between the capillary supply and
O2 peak has
been documented previously in young adult humans (17); however, our
investigation is the first to describe a relationship between the
capillary supply and
O2 peak in the older
population. While it is clear that other factors (e.g., metabolic
adjustments, cardiac output, etc.) must account for a large portion of
the variance in O2 peak
in this population, our findings suggest that the role of the capillary
supply to muscle fibers is also important to whole body aerobic
function in the older population. In this respect, it is most pertinent
that when the change in
O2 peak (ml/min) was
plotted as a function of the change in the capillary supply (i.e., CFPE
index) for all subjects, a moderate relationship was found
(r = 0.52, P < 0.01), indicating that the
individuals with the greatest increase in the capillary supply tended
also to have the greatest increase in
O2 peak. Comparison of
the slopes of these responses between groups revealed that the
relationship between the capillary supply and
O2 peak was the same,
irrespective of training modality. In contrast, the plot of the change
in O2 peak vs. the
change in CD was not significant (P = 0.07).
Conclusions.
We observed that a program of 9 wk of RT followed by 9 wk of AT
produced a similar increase in
O2 peak (l/min) as did
18 wk of AT in a population of older men. In conjunction with the changes in O2 peak, we
observed significant increases in the capillary-to-fiber surface
interface (as reflected in an increased CFPE index) after both RT and
AT, whereas the CD was significantly increased only after
AT. When the
O2 peak was regressed
as a function of the capillary supply, the CFPE index was found to explain a greater proportion of the variance in
O2 peak than did the
other indexes of the capillary supply. These observations support the
utility of the CFPE index in providing an indication of the capacity
for oxygen flux between the capillaries and muscle fibers and support
an important role for the capillaries in the O2 peak response in the
older population. They also suggest the possibility that high-intensity
RT and AT, by increasing the capillary supply to the skeletal muscle
fibers, may operate through similar mechanisms to increase the
O2 peak in the older
population.
ACKNOWLEDGEMENTS
We thank Dr. D. Richards for assistance in the screening and for
supervising the O2 peak
evaluations of the subjects. We also thank the subjects for the
generous donation of their time and effort.
FOOTNOTES
Address for reprint requests: R. T. Hepple, Div. of Physiology, Dept. of Medicine, 0623A, 9500 Gilman Dr., Univ. of California, San Diego, La Jolla, CA 92093-0623.
Received 23 September 1996; accepted in final form 19 December 1996.
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