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Departments of 1 Physiology, 2 Radiology, and 3 Kinesiology, Michigan State University, East Lansing, Michigan 48824
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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The increase in nuclear magnetic resonance
transverse relaxation time (T2) of muscle water measured by
magnetic resonance imaging after exercise has been correlated with work
rate in human subjects. This study compared the T2 increase
in thigh muscles of trained (cycling
O2 max = 54.4 ± 2.7 ml
O2 · kg
1 · min1,
mean ± SE, n = 8, 4 female) vs. sedentary
(31.7 ± 0.9 ml
O2 · kg1 · min1,
n = 8, 4 female) subjects after cycling exercise for 6 min at 50 and 90% of the subjects' individually determined
O2 max. There was no significant
difference between groups in the T2 increase measured in
quadriceps muscles within 3 min after the exercises, despite the fact
that the absolute work rates were 60% higher in the trained group
(253 ± 15 vs. 159 ± 21 W for the 90% exercise). In both
groups, the increase in T2 of vastus muscles was twofold greater after the 90% exercise than after the 50% exercise. The recovery of T2 after the 90% exercise was significantly
faster in vastus muscles of the trained compared with the sedentary
group (mean recovery half-time 11.9 ± 1.2 vs. 23.3 ± 3.7 min). The results show that the increase in muscle T2
varies with work rate relative to muscle maximum aerobic power, not
with absolute work rate.
muscle recruitment; muscle functional magnetic resonance imaging; cycling exercise; transverse relaxation time
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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THE 1h nuclear magnetic resonance transverse relaxation time (T2) of muscle water increases during exercise (8, 9). The T2 increase is easily measured by conventional magnetic resonance imaging (MRI) methods and has been used in many studies as an index of the intensity of muscle recruitment during various exercises (6, 10, 21). This application of muscle MRI is largely based on empirical studies of relatively homogeneous groups of healthy subjects, in which there was a good correlation between the T2 increase vs. integrated surface EMG and contraction rate or force during voluntary exercise (1, 12, 19).
The underlying biophysical cause of the T2 increase in exercised muscle is not fully understood. Saab et al. (22) recently showed that the T2 increase in human muscle coincides with a shift of signal amplitude between two intracellular relaxation components, which may arise from intracellular fluid compartments with different intrinsic relaxation rates. Additional studies suggest that the uptake or redistribution of fluid within muscle is driven by the accumulation of osmotically active metabolites, such as inorganic phosphate (Pi) and lactate, during exercise. For example, in rat hindlimb muscles stimulated at various rates, the T2 increase is greatest in a muscle region characterized by relatively low oxidative capacity and blood flow and by high glycolytic capacity in which Pi and lactate accumulation during stimulation are known to be relatively high (20). Similarly, there is a good correlation between the T2 increase and the extent of phosphocreatine (PCr) hydrolysis and muscle acidification immediately after exercise in human muscle, although the T2 change recovers more slowly after exercise compared with these metabolic changes (5, 23).
It is well known that the extent of Pi and lactate accumulation in muscle during exercise depends on power output relative to the maximum aerobic power of the muscle (17). Therefore, if the T2 increase during exercise results from the osmotic effect of metabolite accumulation, then it should depend on power relative to the peak aerobic power of the recruited muscles rather than on absolute power per se. The purpose of this study was to compare the T2 increase after cycling exercise in thigh muscles of trained vs. sedentary subjects. The results show that the T2 increase in the recruited muscles depends on power relative to peak aerobic power. Furthermore, the recovery of muscle T2 after high-intensity exercise is faster in subjects with greater aerobic capacity. These results have important practical implications for the use of muscle T2 as an index of muscle activity during exercise.
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METHODS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Subject selection and characterization. Sixteen subjects (18-30 yr old, 8 female) were recruited from the academic community. The study was approved by the University Committee on Research Involving Human Subjects, and each subject gave informed, written consent. Subjects were selected for either the trained or the sedentary group on the basis of their self-reported activity levels. Subjects who reported participation in cycling or other aerobic training >5 h/wk were assigned to the trained group; subjects in the sedentary group reported no regular participation in aerobic exercise.
Maximum oxygen consumption (O2 max) of
the subjects during cycling exercise was determined by an incremental
stage protocol. Subjects pedaled at a cadence of 60-90 rpm on a
cycle ergometer (Sensormedics Ergo-metrics 800S) for a 3-min warm-up period at 25 W. Thereafter, the power level was increased by 30 W every
3 min, while respiratory volume, PO2,
PCO2, and O2
were recorded on a Sensormedics 2900 metabolic cart. This ergometer automatically varies the resistance inversely with variations in
pedaling frequency to provide a uniform power at each stage. The
subjects continued this progressive protocol until exhaustion or until
unable to maintain the frequency >60 rpm.
O2 max was the highest
O2 recorded during a completed workload.
Exercise and imaging protocol.
Subjects abstained from exercise for 24 h before each of two
exercise-imaging sessions conducted 1 wk apart and by use of the same
cycle ergometer used during the O2 max
measurements. Each exercise session consisted of pedaling at 60-90
rpm for 2 min at 25 W, followed by 6 min of pedaling at either 50 or
90% of the power corresponding to 100% of the subject's
O2 max. These exercises were conducted
in a hallway adjacent to the scanner room, subjects were positioned in
the magnet, and scanning was begun within 1 min after completion of the exercise.
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Statistics.
The half-time for T2 recovery after exercise
(T1/2) in individual muscles was estimated by fitting the
recovery time course to a three-parameter exponential model using the
Marquardt-Levenberg algorithm
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(1) |
T2(t) is
the change in T2 at time t after exercise
compared with before exercise, T2(t = 0)
is the fitted T2 at the time immediately after the end
of the exercise, and T2(t = 
) is the
fitted baseline T2. All results are reported as means ± SE. Comparisons between groups and muscles were performed by two-way
ANOVA followed by Tukey's procedure or by Student's t-test
with Bonferroni adjustment for multiple comparisons at the
P < 0.05 level of significance.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Characteristics of the subjects are shown in Table
2. The two groups were not significantly
different in age, weight, height, or body mass index. The cycling
O2 max and peak aerobic power (power at
100% O2 max) were 72 and 60% greater in the trained compared with the sedentary group, respectively. There
was a trend toward greater thigh muscle cross-sectional area in the
trained group; however, this difference was small compared with the
difference in peak aerobic power, such that the ratio of power to
muscle cross-sectional area was still 46% higher in the trained group.
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Figure 1 shows illustrative magnitude images from a sedentary and a
trained subject before and after completion of the 90% exercise.
Two-way ANOVA indicated that there were significant differences in
preexercise T2 between different muscles in the thigh
(two-way ANOVA, muscle effect, P < 0.05) and a small
but significant overall difference in T2 between muscles of
the sedentary vs. the trained group but no significant muscle × group interaction term. These minor differences in preexercise
T2 very likely reflect variations in interfasicular fat
content between groups or between muscles, inasmuch as the
T2 of fat (45-50 ms) is higher than that of resting
muscle (11). For example, as shown in Fig.
2, the biceps femoris muscle in the
preexercise images of the sedentary subject of Fig. 1 includes many
more higher intensity pixels compared with the trained subject. This
difference is associated with greater skewing of the distribution of
pixel T2 toward higher values in the sedentary compared
with the trained subject (Fig. 2B).
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The bars in Fig. 3 show the change in
T2 (T2, post- minus preexercise) measured
within 3 min after the exercises for 10 muscles of the thigh. The
T2 increase after the 50% exercise was greatest in the
single-joint knee extensors (vastus lateralis, vastus intermedius, and
vastus medialis). In both groups of subjects, the T2 change in these muscles was twofold greater after the 90% exercise compared with the 50% exercise. After the 90% exercise, T2 was
also significantly elevated in the rectus femoris and in several of the
posterior thigh muscles, in particular the sartorius, adductor magnus,
and gracilis. In these muscles, the T2 increase was three-
to eightfold greater after the 90% compared with the 50% exercise.
These changes were also similar in the two groups of subjects. For
example, in the posterior muscles of both groups, the T2
increase after the 90% exercise was greatest in the sartorius and
intermediate in the semitendinous, whereas there was no significant
T2 increase in the biceps femoris muscle in either group.
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Figure 4 shows the time course of
recovery of T2 after the exercises in the vastus lateralis
muscle. In the trained group, there was no significant difference in
the half-time for recovery after the 50% vs. the 90% exercise (Table
3). However, recovery was significantly
slower after the 90% exercise in sedentary group compared both with
the trained group and with the sedentary group after the 50% exercise.
Similar differences in T2 recovery between groups were
observed in the other muscles of the thigh after the 90% exercise
(data not shown). Despite this difference in T2 recovery time, there was no significant difference between groups in the fitted
T2 increase immediately after the exercises
[T2(t = 0) of Eq. 1, Table
3]. The baseline parameter [T2(t = )] was not significantly different from zero in either group.
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Figure 5 shows the relationship between
the T2 increase in the vastus lateralis muscle immediately
after the exercises [T2(t = 0)] vs.
absolute power (W/cm2 thigh muscle) and also vs. power as a
percentage of the subjects' maximum aerobic power. When the results
from both groups are considered, it is clear that the T2
increase is more closely related to relative than to absolute power
output. Consideration of Fig. 3 shows that qualitatively similar
relationships would be obtained by use of the T2 data from
the other vastus muscles or by use of the T2 change
averaged across all of the muscles in the thigh.
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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The main result of this study is that the T2 increase in exercised muscles of human subjects depends on exercise intensity relative to maximum aerobic power and not on absolute work rate per se. It is well known that the extent of muscle PCr hydrolysis and lactic acid accumulation also depend on exercise intensity relative to muscle peak aerobic power. Therefore, this result is consistent with the hypothesis that that the T2 increase is caused by fluid shifts associated with the net accumulation of osmotically active metabolites during exercise. Similar conclusions were drawn from a recent study of rat triceps surae muscles after electrical stimulation, in which the T2 increase varied inversely with the known aerobic capacity of the muscles (20). Of course, it is not possible to determine from this or previous studies whether the difference between trained vs. sedentary subjects is primarily due to differences in the intrinsic properties of muscle fibers (e.g., fiber type, mitochondrial content, glycogenolytic capacity) or to differences in flow capacity or cardiovascular fitness. Just as for other measures of metabolic stress in muscle (e.g., acidosis, net nucleotide degradation), the increase in T2 in exercised muscle likely depends on both intrinsic and systemic factors.
The practical implication of this result is that the T2 increase observed in human muscles during exercise cannot be used to directly compare muscle activity across different individuals unless some independent measure of muscle aerobic capacity is available. Similarly, decreased postexercise T2 after training cannot be used to infer that training decreased the extent of muscle recruitment (18), unless other evidence shows that the training did not alter the muscle's aerobic capacity. Furthermore, considering the possibility that different muscles within a subject might differ in aerobic capacity, it may not always be possible to use T2 changes to compare the activity between muscles within a subject. For example, considered in isolation, the results of this study at the 50% intensity level suggest that both groups used their vastus muscles to a greater extent than the rectus femoris or posterior muscles during cycling at moderate intensity. However, in the absence of some other measurement, this conclusion could, in principle, be criticized on the grounds that the vastus muscles might have lower aerobic capacity than the other muscles in the thigh. On the other hand, when the results at both exercise intensities are considered, it does seem reasonable to conclude that both groups of subjects increased recruitment of the rectus femoris and posterior muscles relative to the vastus muscles during high- compared with moderate-intensity cycling.
A secondary result of this study is that the recovery of muscle T2 after intense exercise is significantly faster in subjects with higher aerobic capacity. Similarly, after electrical stimulation, T2 recovery was faster in rat triceps surae muscles characterized by high aerobic capacity (20). Again, this difference may depend both on intrinsic properties of the muscle (e.g, on the rate of PCr resynthesis) and on systemic factors such as blood flow and the rate of lactate clearance. The practical implication of this result is that muscle functional MRI measurements should be obtained during or as soon as possible after the exercise under study. Alternatively, inasmuch as the recovery of T2 is well described by an exponential fit, several measurements should be made during recovery and the results extrapolated to the time immediately after the exercise.
Interestingly, a previous study by Le Rumeur et al. (16)
concluded that the T2 increase was greater in vastus
muscles of highly trained compared with moderately active or sedentary
subjects after 15 min of cycling exercise at the same relative
workloads (as estimated from heart rate) and that recovery of
T2 was slower in the highly trained subjects. The reason
for the discrepancy between that study and this one is not clear.
However, neither maximum heart rate, cycling
O2 max, nor muscle cross-sectional area
was measured in that study. Therefore, it may be that the relative
workload was higher in the trained compared with the other groups.
Richardson et al. (21) previously used MRI to compare the recruitment of thigh muscles during cycling with knee extension exercises. The cycling result in that study is qualitatively similar to the result after the 90% exercise in this study, although in that study the relative T2 increases (expressed as %resting T2) were slightly greater in the gracilis and adductor magnus compared with the vastus muscles. In addition, the T2 changes observed in that study were roughly one-half those observed in this study. This difference is likely due to the shorter exercise duration used in that study (2-2.5 min).
Finally, some studies have suggested that differences in relaxation times (T2 and/or T1) of resting muscles might be used to distinguish muscles with different fiber type or mitochondrial content (4, 7, 15). Although in this study T2 was significantly shorter in muscles of the trained compared with those of the sedentary group , the differences were small (~0.5 ms, Table 2) and comparable to the variance of the measurements. Therefore, it is unlikely that the training status of individual subjects could be reliably distinguished by this difference. On the other hand, the higher interfascicular and intermuscular fat content of sedentary compared with trained subjects is readily apparent (Fig. 1) and can be quantified by both spectroscopic (3) and image thresholding methods (14). These more direct measurements of muscular fat are likely to provide a better correlate of muscle training status than minor variations in relaxation times measured at rest.
In summary, the T2 increase in thigh muscles after cycling exercise depends on exercise intensity relative to peak aerobic power. Functional MRI measurements based on the T2 increase can be a useful method for visualizing the pattern of muscle activity during exercise (6, 10, 21) or electrical stimulation (2). However, because the T2 increase depends on additional factors such as muscle metabolic and flow capacity, it is not a direct measure of muscle recruitment. Instead, these measurements provide a high-resolution map of relative metabolic stress within the imaged muscles.
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ACKNOWLEDGEMENTS |
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This study was supported by National Institutes of Health Grant AR-43903.
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FOOTNOTES |
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Address for reprint requests and other correspondence: R. A. Meyer, Dept. of Physiology, Giltner Hall, Michigan State University, East Lansing, MI 48824 (E-mail: ram{at}pslsun.psl.msu.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.
Received 8 August 2000; accepted in final form 4 October 2000.
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REFERENCES |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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) and trained (
) subjects. All values
are mean ± SE, n = 8.