Exercise induces changes in muscle metabolism that are well documented (9,11,16,28,29,33). As either the workload or the duration of an exercise is increased, the contracting muscle must generate a greater amount of energy, thereby generating more metabolic byproducts such as lactate (11,28,29,33). The effect of the type of exercise was examined as early as 1923 when Fenn (5) found that the metabolic cost of dynamic exercise was greater than that of isometric. Subsequently, these metabolic costs were reported to be ∼50% greater for dynamic exercise (2). An increased metabolic cost and subsequent increase in metabolic byproducts might be expected to alter the osmolality of an exercised muscle, which would yield a different intracellular water content and thereby affect magnetic resonance (MR) images.
The effect of exercise upon MR images of muscle was first reported in 1983 (10) and subsequently studied with echo planar (EP) imaging in 1991 (4). These early studies demonstrated that changes in muscle images were caused almost entirely by exercise induced increases in muscle relaxation times, which are highly influenced by the muscle's water content (4). We recently reported dynamic changes in muscle transverse relaxation rates (ΔR2 (s−1), where ΔR2 = Δ(1/T2)) during and after exercise measured with a time resolution of 4 s (17). With this resolution, a distinct ΔR2 pattern was observed that included a continued increase in ΔR2 that persisted for ∼1 min after the cessation of exercise and before the muscle began to recover (17). We hypothesized that the continued increase in ΔR2 was the result of relaxation of the hydrostatic resistance that had resulted from capillary collapse (myogenic vasoconstriction) during muscle contractions (17).
As with muscle metabolism, the magnitude of exercise-induced change in an MR image is affected by the workload(or intensity) (6-8,11,13,27,29) and duration (6,17,21,27) of the exercise. The workload, a measure of how much mass the muscle contracts against relative to the maximum mass it can handle, is distinguished from the total work that a muscle performs during exercise. Blood flow to an exercising muscle is also influenced by the exercise protocol (14,15,18,20-22,34,35), and blood flow has been reported to influence the magnitude of exercise-induced change in MR images as well (3,12,17,19,23,26). The correlation between blood flow (NMR plethysmography (mL·dL−1·min−1)) and ΔR2 (s−1) under conditions of reactive hyperemia was recently established (r2 = 0.62) in a study by Toussaint et al. (32). This study concluded that there were measurable perfusion changes in the lower leg during the reactive hyperemia period following 5 min of ischemia and that these perfusion changes, the result of increased blood flow, could be reliably measured with bothΔR2 and ΔR1 (where ΔR1 = Δ(1/T1))(32). Because blood flow and MR image changes can be correlated, it is reasonable to speculate that parameters that affect blood flow might also affect MR images. The different patterns of blood flow brought about by isometric and dynamic exercise are well established (14,15,18,20,34,35), and have been observed in the both the femoral artery and the popliteal artery supplying the anterior tibialis/extensor group for dorsi-flexion exercise (34,35). It is thought to be the hydrostatic resistance to blood flow, brought about by myogenic vasoconstriction during muscle contraction, that initiates these different patterns (14,15,17,18,20,34,35). Taken as a whole, the literature suggests a pattern of blood flow response that is significantly smaller during isometric exercise than during dynamic exercise.
Most MR imaging studies have employed either an isometric exercise protocol or a dynamic exercise protocol. The known metabolic differences between the two protocols could produce different osmolalities during exercise, thereby yielding different intramuscular water contents. Additionally, the continuing ΔR2 increases immediately after exercise may result from the relaxation of myogenic vasoconstriction following muscle contraction. Either of these physiological responses could result in different MR images during isometric and dynamic exercise; however, the balance between these different factors is likely to be complex. In this study, we used echo planar imaging to compare the ΔR2 patterns (17) during and after isometric and dynamic dorsi-flexion exercise protocols at identical workloads and durations to more fully explore the contributors to exercise-induced changes in MR images.
Subjects. Twelve normal healthy adult subjects, nine male and three female, participated in this study. Subjects were 33± 3 yr of age (21-46 yr), 75 ± 2 kg weight (68-89 kg), and 176 ± 2 cm in height (168-185 cm). All subjects were screened according to exercise and dietary habits (28). Those who trained aerobically >5 d·wk−1 and/or those on specialized diets were excluded from the study. Aerobic training was defined as maintaining a heart rate above 120 bpm for a period ≥30 min. In an effort to obtain a pool of subjects that were of average physical conditioning, those subjects with sedentary lifestyles (i.e., no regular exercise habits) were also excluded from the study. In addition, subjects were screened according to the Yale-New Haven Hospital standard criteria for MR imaging. All subjects that were accepted into the study gave informed written consent according to a protocol that was reviewed and accepted by the Human Investigations Committee of Yale University School of Medicine.
Exercise protocol. Each subject performed dorsi-flexion exercise to induce MRI changes in the anterior compartment of the lower leg (anterior tibialis and extensors). Both isometric and dynamic protocols were performed on a nonmagnetic pneumatic piston/cylinder (0.5 L) exercise ergometer attached to a closed pedal apparatus to enable subjects to dorsi-flex against a constant air pressure resistance (27). The ergometer mounted directly onto a standard patient bed to allow exercise within the MR imager. By adjusting the air pressure within a supply tank (50 L) that formed an airtight link with the pneumatic cylinder via 3/8 inch (ID) braided tygon tubing, the resistance could be set to a constant workload (%MVC) (27). Exercise was then performed by rotation of the foot about the ankle with a minimum angle subtended by the dynamic contraction(27). Dorsi-flexion maximum voluntary contractions, which were assessed at least 45 min before beginning the protocol (27), were 27 ± 1 kg for the subject population (24-33 kg). So that isometric and dynamic exercise could be correlated to the effect of workload, the resistance was set to either 25% of MVC or 70% of MVC. Exercise at different workloads was performed in separate sessions. In all sessions, the duration of exercise was 1 min, 45 s.
During the dynamic exercise protocol, subjects were asked to dorsi-flex through a full range of motion (55° rotation (45° to −10°)) for 1 min, 45 s at either 25 or 70% of MVC (17,27). The air pressure within the pneumatic circuit was smaller than the actual %MVC to allow for the surface area of the piston relative to its motion through the cylinder (27). In each session, the subject lay supine and at rest in the MR imager during four baseline images (16 s). Subjects were then asked to contract two times between each single-shot imaging acquisition returning to the resting position for image recording(17). The 27 MR acquisitions occurred every 4 s, yielding an exercise duty cycle of 1 s contract/1 s relax (54 contractions = 1 min, 45 s). Following exercise, subjects lay supine and at rest while imaging continued during ∼4 min of recovery (17).
During the isometric exercise protocol, subjects were asked to dorsi-flex to the center of the range of motion (to 15°) and hold the contraction for 1 min, 45 s at a workload of either 25 or 70% of MVC. Because there is no motion during an isometric contraction, the air pressure within the pneumatic circuit was adjusted to be the same as the actual %MVC, and subjects were aided in positioning the initial contraction to the center of the range of motion. Subjects were then required only to maintain this position against the resistance for the required duration. In each session, the subject lay supine and at rest in the MR imager during ten baseline images (40 s). Subjects then dorsi-flexed and held the contraction for 1 min, 45 s (27 images). Following exercise, subjects lay supine and at rest while imaging continued during ∼4 min of recovery.
MR imaging. MR imaging was performed at 63.9 MHz on a 1.5T GE Signa system (General Electric, Milwaukee, WI) equipped with echo planar imaging (Advanced NMR Systems, Wilmington, MA). Subjects were positioned supine within the MR imager with the foot positioned in the pedal assembly of the exercise ergometer and an extremity radiofrequency(RF) coil positioned mid-calf (17,27). The RF coil was a birdcage design, which yielded uniform images throughout the entire cross-section of the lower leg. Transaxial mid-calf images were obtained using a spin-echo EP imaging sequence with a repetition time (TR) of 4 s and an echo time (TE) of 30 ms (17). The transaxial slice thickness was 1 cm with a field of view (FOV) of 20 × 40 cm and an imaging matrix of 64 × 128 (17). Before exercise, 4-10 images were collected, 27 images were collected during exercise, and following exercise 34-65 images were collected. In the dynamic exercise protocol, the images were obtained with the foot in the "unloaded" position. During exercise, contractions were timed to occur between the MR pulses. In the isometric exercise protocol resting and recovery images were obtained with the foot in the unloaded position; however, the "during exercise" images were obtained with the foot in the loaded position. In some cases, this difference of foot position resulted in a slight image registration difference. When this occurred, the first two images obtained during the initial 8 s of exercise were taken for comparison as the at rest images.
MR data analyses were performed using the same methods as reported in our previous paper (17). The change in relaxation rate owing to exercise (ΔR2) was calculated from the signal intensity within a small region-of-interest (ROI) within the exercised muscle group (<1.5 cm2). It has previously been reported that exercise-induced T2 changes in the two muscles of the anterior compartment are not significantly different (27). ΔR2 was therefore calculated for a constant TE = 30 ms within this ROI according to the following: Equation 1 where SIpre is the signal within the ROI before the start of exercise and SIpost is the signal within the ROI at each time point after the start of exercise. The TE = 30 ms was used so that the echo time would approximately equal the intrinsic resting relaxation time of the muscle, thereby producing large signal changes with exercise. The TR = 4 s was used to eliminate T1 weighting in the images (17).
To compare the amount of muscle swelling that resulted from the different exercise protocols, MR images obtained before and after 1 min, 45 s of dynamic and isometric dorsi-flexion at 25% of MVC were compared for cross-sectional area. In a subgroup of subjects (N = 8), MR images were acquired using a standard multiple spin-echo sequence(TR = 1000 ms; TE = 30, 60, 90, 120 ms; FOV = 20 cm; slice thickness = 0.5 cm, 128× 256 matrix). The ROI was determined by tracing the border of the anterior compartment before and after exercise and calculating the cross-section. The cross-sections were then compared before and after exercise (27). The changes in cross-sectional area were not significantly different between the two types of exercise (106 ± 2% of rest (isometric) and 107 ± 2% of rest (dynamic)).
Statistics. All data are presented as means ± SE of all calculatedΔR2 values. Intersubject isometric and dynamic exercise results were compared with paired two-tailed t-tests, and rates were compared with repeated measures ANOVA. Intrasubject variability, assessed by comparing ΔR2 values in ≥3 different regions within the recruited muscles (anterior tibialis and extensor) with t-tests, was found to be minor (coefficient of variation≤ ± 1.5%). Consequently, we found that propagation of error was not a source of significant contribution to the results; hence, it was not given further consideration.
The dorsi-flexion exercise protocol successfully recruited the anterior compartment of the lower leg. Figure 1, a and b, shows calculated T2 echo planar images from an individual subject derived from images obtained before and after dynamic exercise (1 min, 45 s at 70% MVC); figure 1, c and d, shows the corresponding ΔR2. Note that the darker region in 1 d indicates a decrease in the transverse relaxation rate. The exercise-inducedΔR2 values are plotted point-by-point in Figure 2a(25% of MVC) and in Figure 2b (70% of MVC). Data for the isometric portion of Figure 2b were collected before all other data andΔR2 recovery patterns were tracked for only 2.25 min of recovery. Theerror bars in the dynamic exercise portion of Figure 2a are greater than other data sets because this set represents the smallest number of trials performed, and there was a single outlying data point that was not excluded. The high variability of this set did not alter the results nor did it affect any of the statistical trials. During exercise, the time courses of ΔR2 were different for all protocols and were dependent upon the type of exercise as well as the workload. At both workloads, ΔR2 was significantly smaller at the end of 1 min, 45 s of isometric exercise when compared with dynamic exercise(−1.49 ± 0.27 s−1 (25% isometric) vs −4.21 ± 1.16 s−1 (25% dynamic) (P ≤ 0.05) and −3.39 ± 0.24s−1 (70% isometric) vs −6.44 ± 0.44s−1(70% dynamic) (P ≤ 0.01)) (Table 1). When workloads were compared (25 vs 70%), the ΔR2 values were significantly greater following both isometric (P ≤ 0.01) and dynamic (P ≤ 0.05) exercise at the heavier workload. During the first 65 ± 5 s of resting recovery immediately following all exercise protocols, ΔR2 values continued to decline. The times and magnitudes of the continued decreases in ΔR2 were not significantly different in any of the exercise protocols (Table 1). The maximum ΔR2 observed following exercise was significantly different in a comparison of the same type of exercise at different workloads (P ≤ 0.05) as well as in a comparison of isometric and dynamic exercise at identical workloads (−3.66 ± 0.30's−1 (25% isometric) vs −6.00 ± 1.24s−1 (25% dynamic) (P ≤ 0.05) and −6.02 ± 0.67s−1 (70% isometric) vs −8.55 ± 0.34s−1 (70% dynamic) (P ≤ 0.01)) (Table 1). After the ΔR2 reached a maximum, there was a steady recovery that followed a similar time course for all protocols. At both 25 and 70% of MVC, 35-65 (2 min, 15 s to 4 min, 15 s of recovery) ΔR2 time points were compared during the recovery period (isometric vs dynamic exercise). Following exercise at 25% of MVC, the mean difference in ΔR2 values of isometric versus dynamic exercise remained constant at 2.5 ± 0.04 s−1, whereas following exercise at 70% of MVC this mean difference remained constant at 3.0 ± 0.05 s−1. Rates of change in ΔR2, calculated during the first minute of exercise, during the final 45 s of exercise, during the first 65 s of recovery, and during the recovery period after 65 s, are given in Table 2 as in our previous study (17). During dynamic exercise at 25% of MVC, the rates of change in ΔR2 do not differ significantly between the initial minute and the final 45 s; however, during isometric exercise, the initial rate of change in ΔR2 (first minute) is significantly slower than the final 45 s (P ≤ 0.01). At 70% of MVC, the initial rate of change in ΔR2 (first minute) is significantly faster than the final 45 s (P ≤ 0.01) in both the dynamic and the isometric protocols. In addition, although the initial rates were similar in dynamic versus isometric exercise at 70% of MVC, the rate was significantly slower during the final 45 s of the isometric protocol (P ≤ 0.05) compared with dynamic exercise. During both periods of recovery (initial 65-s period, period after the initial 65 s), there were not significant differences in the rates of change in ΔR2 between any of the exercise/recovery protocols (isometric/dynamic at 25 and 70% of MVC).
When skeletal muscle is exercised, physical and chemical changes occur that may increase the total intramuscular water content and thereby affect the MR signal. At the onset of exercise, normal blood flow to the exercising muscle increases, owing to both an increase in cardiac output (CO) and to vasodilation (15,21,23,34,35). It may be speculated that this increased blood flow yields greater perfusion of the muscle tissue and potential expansion of the muscle's extracellular (EC) space via a fluid exchange from the blood plasma to the EC space (21,22,30,31). During exercise, contraction(the sliding together of myosin and actin filaments) causes the muscle to expand and the surrounding capillaries to collapse. It is possible that this collapse of capillaries might result in a reduction of blood flow at the fluid exchange site. Thus, the most efficient fluid exchange might be expected during the relaxation period that follows a contraction rather than during the contraction itself (3,30). Simultaneously, the metabolic response to exercise induces an osmotic pressure differential between the intracellular (IC) space and the EC space that results in passive diffusion from EC to IC spaces (31). Exercise-induced depletion of muscle glycogen and subsequent buildup of lactate may play a significant role in the net flow of water into the IC space (1,5,9,11,16,24,28,29). However, shifts in water alone do not explain the observed changes in relaxation rate because the fluid exchange rate between the IC and EC compartments is relatively fast (17). During exercise and recovery, increased muscle perfusion and osmotic pressure are likely to be coupled in a complex manner that may not be explained in simple terms. Intramuscular proteins may be the most significant relaxation agents, and exercise may affect interactions of protons at the protein-water interface.
Previous studies have demonstrated the utility of echo planar MR imaging techniques for the study of exercise-induced changes in muscle (4,6,17,32) both during and after exercise. With the improved time resolution available from single shot ΔR2 measurements, a distinct time course pattern that is duration dependent and exists both during and after exercise has been reported (17). The current study demonstrates that exercise-induced changes in the anterior compartment of the lower leg differ depending upon whether the exercise protocol is isometric or dynamic. To correlate the effect of workload and the comparison of two different types of exercise, echo planar MR images were obtained at two different workloads during and after exercise with a 4-s time resolution. At both workloads (25 and 70% of MVC) the ΔR2 values were greater with dynamic exercise than with isometric exercise. In both dynamic and isometric exercise protocols, the ΔR2 values were greater with exercise at 70% of MVC than at 25% of MVC. Although theΔR2 values were greater with dynamic exercise, the rate and amount of continued ΔR2 following exercise was not significantly different in either exercise protocol at either workload, the differences occurring during exercise. This finding demonstrates that dorsi-flexion exercise produces a distinct ΔR2 time course on echo planar MR images that is dependent upon both workload and the type of exercise.
The differences between a muscle's response to isometric exercise versus dynamic exercise apparently occur during the exercise period, as demonstrated by the different ΔR2 patterns during exercise (Fig. 2). Furthermore, these differences seem to be no longer active during the recovery period. Although the ΔR2 values are greater during recovery from exercise 70% of MVC, the rates of change of ΔR2 are not significantly different at the different workloads. This implies that both increased perfusion and osmotic pressure may be important factors controlling ΔR2 during the exercise period. During isometric exercise, the position of the foot with respect to the range of motion of dorsi-flexion is likely to be of importance. In the current study, results were less clear-cut when subjects contracted isometrically at the beginning (45 to 35° rotation of foot) or at the end (0 to −10° rotation of foot) of the range of motion. The kinesiology of isometric exercise, which may play an important role in these studies, could provide a partial explanation for the range of results reported in the literature. The relationship between capillary collapse, hydrostatic pressure, physiological response, changes in MR images, and position of the isometric contraction with respect to the range of motion has not been reported and bears further study.
The difference between rates of ΔR2 during the initial period (first minute) of exercise and during the final period (final 45 s) of exercise at 70% of MVC further supports the idea that occlusion of flow to the exercising muscle limits increases in signal intensity on MR images. Although perfusion of the muscle is not required for exercise to induce T2 increases, maximum T2 increases do not occur in the absence of perfusion (3). Because it is likely that the T2 increases seen with exercise result from changes that occur in the intracellular space, the plateau in ΔR2 seen during the 70% MVC isometric protocol may result from the limited size of the extracellular space that can be displaced by movement of fluid from the extracellular to the intracellular compartments. A recent study by Ploutz-Snyder et al. (25) supports this idea, concluding that increased extracellular fluid can account for only a minor portion of exercise-induced T2 increases. The drop in rate of ΔR2 during dynamic exercise at 70% of MVC suggests that the momentary restriction of flow with each contraction is enough to significantly reduce the movement of fluid into the intracellular space, although not to the extent of isometric exercise. When the exercise period was complete and the muscle was allowed to rest, perfusion was allowed to commence, and fluid movement from the vasculature to the extracellular space and ultimately to the intracellular space presumably was resumed producing the ΔR2 time course that was seen to be superimposable between recovery from dynamic and isometric exercise.
Muscle lactate concentrations have been measured before and after exercise using both biochemical methods (16,30,31) and 1H NMR spectroscopy (9,24) with good agreement between the two techniques. Immediately following maximal exercise to exhaustion, intramuscular lactate has been shown to increase to 25-30 mM (9,16,24,31). When the standard tissue osmolality (∼300 mOsm) is assumed, the exercise-induced increase in lactate alone (∼30 mM, (24)) can make a difference up to 10% in the osmolality of the intracellular space of a muscle. Assuming that ∼55% of a muscle's total volume is intracellular space and that 70% of this space is free water, an increase of 10 mM in lactate would yield a 1.2% increase in free water in a muscle the size of the anterior tibialis. This corresponds well with 12-18% increases in muscle T2. During ∼20 min of subsequent recovery from exercise, intramuscular lactate has been shown to approach resting concentrations in studies using both methods (9,16,24), suggesting a passive efflux of intracellular lactate resulting from shifts in muscle water ratios. Following exercise, the time course of muscle lactate recovery (9,16,24) is similar to that of muscle T2(3,27), suggesting that there may be a correlation between muscle lactate levels and T2 resulting from the role of lactate and ICW in muscle osmolality.
In summary, we have studied ΔR2 time course patterns during and after both isometric and dynamic exercise. The two workloads that we studied (25 and 70% of MVC) were matched between the two types of exercise. We observed significant differences between isometric and dynamic exercise. We further observed that the primary differences between the two exercise protocols occurred during the exercise period (Fig. 2) and that the subsequent recovery curves, although being offset, were almost identical. We postulate that postexercise recovery is more closely related to the return of osmotic pressure to a resting equilibrium owing in part to the washout of lactate from the recovering muscle. The differences in ΔR2 patterns occurred during the exercise period. We conclude that exercise-induced MR image changes are dependent not only upon the workload and duration of exercise but also upon the type of exercise.
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