The effects of exercise training on skeletal muscle mitochondrial oxidative capacity have been well known for several years (21). Skeletal muscle contractile activity initiates several cellular signals that result in increased nuclear and mitochondrial gene transcription, followed by translation into mitochondrial proteins (24). Over time, repeated bouts of exercise result in increased mitochondrial enzyme concentrations and activities (14,19,23), which have been termed mitochondrial biogenesis. In contrast, lack of physical activity, aging, and several pathological conditions are associated with reduced mitochondrial function (28,29,31).
Historically, skeletal muscle mitochondrial function has been measured using muscle tissue samples that require surgical removal (21–23). The concentration and activity levels of key mitochondrial enzymes such as citrate synthase or succinate dehydrogenase (SDH) are commonly used as a measure of mitochondrial function (14,19,23). A major limitation of these assays is that mitochondrial function is inferred from a very small amount of tissue and the evaluation of a single mitochondrial enzyme. High-resolution respirometry can provide more information about the specific function of the various complexes in the electron transport chain, but the isolated tissue used is subjected to nonphysiological conditions (i.e., higher oxygen concentrations). Noninvasive assessments of mitochondrial function have advantages for testing human subjects. In vivo techniques allow for repeated measurements with little, if any, discomfort while circulatory and other regulatory systems remain intact. Phosphorus magnetic resonance spectroscopy is the most commonly used in vivo technique for assessing mitochondrial function (6).
Recent advances in optical spectroscopy have led to improved optical devices and applications for studying muscle physiology (12). Near-infrared spectroscopy (NIRS) has been used to measure various aspects of muscle physiology, including muscle blood flow and perfusion (10), muscle oxygen consumption (9,10,33), and muscle oxygenation (1,15). The recovery of muscle oxygen consumption (mV˙O2) after exercise, measured with NIRS, has been used as an index of skeletal muscle oxidative capacity (5,36). Recently, this method has been improved by correcting for the small changes in observed heme concentrations that often occur during these measurements (38). Recent studies have shown the approach to be reproducible and that the increase in muscle metabolic rate needed for the study can be produced with either voluntary exercise or electrical stimulation (37). Furthermore, a recent study from our laboratory demonstrated that NIRS-measured skeletal muscle mitochondrial capacity of endurance-trained cyclists was higher than sedentary control subjects, and that the relative magnitude of difference in mitochondrial capacity was similar to more established techniques (4).
The purpose of this study was to use NIRS measurements of the recovery rate of mV˙O2 after exercise to measure changes in skeletal muscle mitochondrial capacity induced by endurance exercise training and detraining. It was hypothesized that mitochondrial capacity would increase with endurance exercise training and would return to baseline with detraining.
MATERIALS AND METHODS
Nine healthy college-age men and women volunteered to participate in this study (five men/four women; mean ± SD: age = 23 ± 2.3 yr, height = 172.4 ± 9.8 cm, weight = 63.4 ± 12.5 kg). Participants were included if they had not been diagnosed with any chronic disease known to influence muscle metabolism, were not taking medications that could alter muscle mitochondrial function, or were not currently performing forearm exercise training more than 1 d·wk−1. The study was conducted with the approval of the institutional review board at the University of Georgia (Athens, GA) and was carried out in accordance with the Declaration of Helsinki (2008). All participants gave written informed consent before testing.
This was a longitudinal study design where participants performed 4 wk of unilateral wrist flexor exercise of the nondominant arm. The wrist flexor muscles were chosen because they are not involved in locomotion and should be reasonably untrained in comparison with the musculature of the thigh or calf. The dominant arm was not trained and served as the control arm. NIRS measurements of mitochondrial capacity were made every 3–7 d throughout the length of the study. Maximal voluntary isometric contractions (MVIC) were performed once per week to determine the appropriate weight for exercise training and testing (∼30% MVIC).
Wrist flexion exercise was performed 5 d·wk−1 for 4 wk (20 total sessions) on the nondominant arm only. Each session consisted of continuous wrist flexion exercise for 30 min. Participants performed the exercise on a padded flat surface with the elbow at 90° of flexion. Gloves were provided to prevent any discomfort to the hands or skin. Participants trained with dumbbell weights adjusted to approximately 30% MVIC. Progressive increases in the contraction frequency occurred as tolerated, with the goal of inducing the largest change in mitochondrial capacity. Participants began training with a contraction frequency of 0.3–0.5 Hz (600–900 contractions per session) and increases to 1.0–1.2 Hz (1800–2160 contractions per session). During the final 1 min of the each exercise training session, participants performed a high-intensity “sprint”, which consisted of performing wrist flexions at a maximal rate. This 1-min period was included in an attempt to maximize the stimulus for mitochondrial biogenesis (11). After the 20th session of exercise, participants were instructed to not perform any forearm exercise for the remaining duration of the study.
NIRS testing was performed on both the experimental (training) and the control arm every 3–7 d throughout both the training and the detraining portions of the study. Each participant was placed supine on a padded table with the tested arm extended (90° from the body). For each testing session, the NIRS protocol was performed on both the control and experimental arm, which last approximately 45 min. The NIRS probe was placed over the superficial wrist flexor muscles (flexor carpi radialis, palmaris longus, and flexor carpi ulnaris) approximately 2–3 cm distal to the medial epicondyle of the humerus. A blood pressure cuff (Hokanson SC5, Bellevue, WA) was placed proximally to the elbow joint and was attached to rapid cuff-inflation system (Hokanson E20 cuff inflator) powered by a 30-gallon commercial air compressor (Husky VT6315, Kenosha, WI).
NIRS signals were obtained using a continuous wave NIRS device (Oxymon MK III; Artinis Medical Systems, The Netherlands). The probe was set for one source-detector separation distance after the measurement of adipose tissue thickness (ATT). The source-detector distance was set to the closest available distance (choices available were 25, 30, 35, 40, 45, and 50 mm) that was at least twice the ATT. ATT was measured at the site of the NIRS probe using B-mode ultrasound (LOGIQe; GE HealthCare, USA). NIRS data were collected at 10 Hz. NIRS signals that represent oxygenated (O2Hb) and deoxygenated (HHb) hemoglobin/myoglobin were corrected for blood volume changes as previously described (38). Once corrected, the Hbdifference signal was calculated from the difference of O2Hb and HHb, which effectively increases the signal to noise ratio.
The NIRS protocol used was based on a previous study (4). All NIRS measurements were made using the calculated Hbdifference signal (difference between O2Hb and HHB, after correction for blood volume shifts). Resting muscle oxygen consumption (mV˙O2) was measured as the decline in muscle oxygenation (Hbdifference signal) during inflation of a blood pressure cuff to 250–300 mm Hg. Two resting measurements were made using 30 s of arterial occlusion. Resting mV˙O2 was calculated using simple linear regression with the first 20 s of each occlusion (200 data points). After the resting measurements, mitochondrial capacity was measured as the rate of recovery of mV˙O2 after voluntary wrist flexion exercise. Short duration (∼10 s) wrist flexion exercise (30% MVIC) was used to increase mV˙O2. A series of short duration arterial occlusions was performed immediately after the exercise. The cuff protocol is as follows: cuffs 1–10 = 3 s on, 3 s off; cuffs 11–15 = 7 s on, 7 s off; cuffs 16–20 = 10 s on, 10 s off; cuffs 21+ = 10 s on, 20 s off. This cuffing protocol was designed to optimize our ability to characterize the recovery of mV˙O2 while minimizing any discomfort to the participants. The exercise/cuff protocol was performed twice, and the two tests were averaged. An ischemia/hyperemia calibration was used to normalize NIRS signals as previously described (37). Briefly, 5 s of voluntary wrist flexion exercise was performed, followed by inflation of the blood pressure cuff to 250–300 mm Hg for 3–6 min (until the NIRS signals plateau). Upon release of the cuff, a 1- to 3-min period of hyperemia occurred. This calibration was used to scale the NIRS signals to this “physiological” range.
Calculation of muscle oxygen consumption
mV˙O2 was calculated as the slope of change in Hbdifference signal during the arterial occlusion using simple linear regression. The postexercise repeated measurements of mV˙O2 were fit to a monoexponential curve according to the following formula:
For this equation, y represents relative mV˙O2 during the arterial occlusion, End is the mV˙O2 immediately after the cessation of exercise, Delta is the change in mV˙O2 from rest to end exercise, t is time, and k is the fitting rate constant. The recovery rate constant (k) of mV˙O2 after exercise is proportional to the maximal oxidative capacity. We choose to report the NIRS rate constant because this value is directly proportional to mitochondrial capacity. Time constants can be calculated as 1 / rate constant.
Data are presented as means ± SD. Statistical analyses were performed using SPSS 19.0 (IBMm®, Armonk, NY). A two-way mixed-model ANOVA with a within-subjects factor (time) and between-subjects factor (control arm vs training arm) was performed on the NIRS rate constants. When a significant interaction effect was found, a post hoc analysis was performed using pairwise comparisons of the main effect (time) with a Bonferroni adjustment. An a priori power calculation was performed using G*Power 3 (Heinrich Heine, Düsseldorf, Germany) and yielded a total sample size of 6 based on the interaction term for repeated ANOVA with a 20% improvement in mitochondrial capacity, α = 0.05, and power (1 − β) = 0.8.
All participants completed the testing and exercise training without any adverse events. The physical characteristics of the participants in this study are shown in Table 1. All participants increased the number of contractions performed throughout the training portion of the study (session 1, ∼800 ± 160 contractions; session 20, ∼1800 ± 130 contractions; P < 0.001). Weekly training progression for the group is shown in Table 2. Resting mV˙O2 was not altered by training (P = 0.790) and was not different between control and training arms (0.29%·s−1 ± 0.03%·s−1 vs 0.31%·s−1 ± 0.02%·s−1, P = 0.461). MVIC did not change over time in either the control arm (P = 0.833) or the training arm (P = 0.537).
NIRS mitochondrial capacity
Representative NIRS raw data and the recovery kinetics of mV˙O2 are shown in Figures 1A and 1B for descriptive purposes. All participants showed improvements in skeletal muscle oxidative capacity in the endurance trained wrist flexors, as indicated by an increase in the rate constant (k) for the recovery of mV˙O2 (P < 0.001) (Fig. 2). There was no change in the rate constant (k) in the control arm (P = 0.757) (Fig. 2). The mean coefficient of variation for the NIRS rate constant in the control arm was 10.4% (range = 6%–16%). A two-way ANOVA found a main effect of group, F(1,160) = 22.7, P < 0.001, indicating that the trained and control arm NIRS rate constants were different. There was also a significant main effect for time, F(9,160) = 4.54, P < 0.001, indicating that the NIRS rate constants changed over time. The interaction effect (time × group) was also significant (F 9,160 = 3.085, P = 0.002). Post hoc analysis of the interaction was performed using pairwise comparisons (control arm vs training arm) with a Bonferroni correction. These pairwise comparisons found significant differences (P < 0.05) in the NIRS rate constants between the control arm and the training arm at the time points 3–6, as well as significant differences (P < 0.05) between time points 3–6 and baseline (time = 0) for the training arm only (Fig. 2). We also found that the initial (baseline) NIRS rate constant was not different between the dominant and the nondominant arms (1.17 ± 0.23 vs 1.15 ± 0.21, P = 0.717). The normalized changes in mitochondrial capacity (percent change from baseline) are shown in Figure 3. We found a wide range of improvement in mitochondrial capacity in this study (31%–151%). Because of this wide range in responses to training protocol, we conducted a regression analysis to determine the relationship between the improvement (percent change) and the initial mitochondrial capacity (rate constant at baseline). This relationship was significant (F 1,8 = 7.447, P = 0.029, r = −0.718). The initial (end-exercise) mV˙O2 also increased with exercise training. The initial mV˙O2 from the first testing session was 4.45%·s−1 ± 1.88%·s−1 and peaked at 6.67%·s−1 ± 1.34%·s−1 in testing session 5 (P = 0.09).
We also calculated rates of adaptation and deadaptation in mitochondrial oxidative capacity using the NIRS data. During the exercise training, the mean change in mitochondrial capacity increase linearly over time, reaching a peak improvement of approximately 64% ± 37% measured approximately 48–72 h after the last training session. Individual training and detraining responses are shown in Table 3. Pooled training and detraining responses were characterized with linear regression and monoexponential decay functions, respectively (Fig. 3). A rapid decline in mitochondrial capacity occurred during the detraining portion of the study, which was well characterized by a monoexponential decay (Fig. 3). The calculated half-time for the decay in the NIRS rate constant was 7.7 d. There was no significant difference between the starting mitochondrial capacity and the mitochondrial capacity after 5 wk of detraining (P = 1.000).
This study found that mitochondrial capacity measured by NIRS improved with exercise endurance training and returned to baseline values with detraining. We are not aware of previous studies that have used the rate constant (k) for the recovery of mV˙O2 measured with NIRS to assess training and detrained in skeletal muscle. The magnitude and the rate of adaptation in mitochondrial capacity found in this study are in agreement with previous studies which used in vitro measurements from muscle biopsies (14,16,18,19,21,39) and in vivo measurements of phosphocreatine resynthesis (13,35). Moreover, the time course of deadaptation is also consistent with previous studies (2,7,20,27,30,35). The ability to detect training and detrained-induced changes support the validity of NIRS-based measurements as a technique for assessing mitochondrial oxidative capacity.
In this study, we report a 64% ± 37% increase in mitochondrial oxidative capacity (indicated by the rate constant for the recovery of mV˙O2) in response to 4 wk of endurance exercise training of the wrist flexor muscles. It is difficult to compare the relative magnitudes of increase in mitochondrial capacity to previous studies because of methodological differences in both the measurement of mitochondrial function and the exercise training protocols. However, the magnitude of change is within the expected range from previous studies. For example, Gollnick et al. (14) reported a 95% increase in SDH activity after 5 months of cycling exercise training in the vastus lateralis muscle. After 2 months of unilateral cycling exercise training, Henriksson (19) reported a 27% increase in SDH activity in the vastus lateralis muscle. Shorter duration exercise training also causes increased mitochondrial function. Spina et al. (39) found that 7–10 d of endurance cycling exercise (˜2 h·d−1) increased citrate synthase (CS) concentrations by approximately 30% in the vastus lateralis muscle. A similar study by Green et al. (18) was published a few years earlier. The authors of this study reported that 10–12 d of endurance exercise increased SDH and CS activities by 14% and 23%, respectively, in the vastus lateralis muscle, although these changes were not considered statistically significant. Exercise training-induced increases in mitochondrial capacity have also been reported using the in vivo phosphorus magnetic resonance spectroscopy (13,34,35).
Participants in the current study performed continuous wrist flexion exercise for 30 min·d−1, 5 d·wk−1, for 4 wk. Progressive increases in the exercise intensity were made as tolerated by the participants (∼2 fold increase in contraction number per training session by the end of the study). The short duration of training, in combination with the increasing stimulus, resulted in a linear increase in mitochondrial capacity during the training portion. This relationship is not unexpected as Green et al. (17) found a linear increase in SDH activity through 6 wk of cycling exercise training. Previous studies have suggested that a fixed and unchanging training stimulus might result in a first-order increase in oxidative capacity with a similar rates of adaptation and deadaptation, which would level off given the appropriate training duration (2,11,40).
The participants in this study had a wide range of responses to the exercise training (31%–151% improvement). The heterogeneity in responses to exercise training was consistent with previous studies suggesting genetic influences on training responses (3). Although our study was not designed to determine the mechanisms behind this wide range, several factors could influence the magnitude of change in mitochondrial capacity. We did find a statistically significant relationship between the baseline mitochondrial capacity (NIRS rate constant) and the percent improvement, which accounted for approximately 50% of the variance in the percent improvement. This suggests that greater improvements were seen in the participants with the lowest rate constant at baseline. Another potential factor could be differences in the training intensity between participants (11). There were small differences in the number of contractions performed between participants, but all participants increased the number of contractions performed. We did not find a statistically significant relationship between the magnitude of improvement and either the number of contractions performed or the rate of increase in training intensity (i.e., rate of increase in the number of contractions). It is possible that the difference in training intensity between participants was not large enough to detect an effect on the magnitude of adaptation. In addition, there are numerous wrist flexor muscles capable of contributing to the exercise; thus, the motor unit recruit patterns (of the superficial wrist flexor muscles where the NIRS device was placed) during training are unknown. We also found no gender differences in the magnitude of improvement in mitochondrial oxidative capacity, consistent with previous reports (32).
Skeletal muscle mitochondrial capacity declined rapidly after the cessation of exercise training. We characterized this decline by fitting the group data to a monoexponential decay function and calculated the half-time to be 7.7 d. All participants roughly followed this time course, given the expected variation in NIRS rate constants (∼10%–15%). Both the exponential pattern and the rate of decline in mitochondrial capacity are consistent with previous studies using in vitro techniques. Booth and Holloszy (2) reported that the half-times for the turnover of cytochrome c in fast and slow rat muscles were 7 and 8 d, respectively. This rapid decline in mitochondrial enzyme concentration/activity in human skeletal muscle has been shown to be somewhere between 2 and 6 wk (7,20,25–27,30).
In the current study, NIRS was used to measure the rate of recovery of muscle oxygen consumption after exercise. The rate constant for the recovery is proportional to mitochondrial oxidative capacity, such that higher rate constants are related to higher maximal rates of oxygen consumption (i.e., state 3 respiration). The relative contributions of myoglobin and hemoglobin to the NIRS signal remains controversial (8). However, with the NIRS device used in the current study (as well as all commercially available NIRS devices), the separation of the hemoglobin and myoglobin absorption spectra is not possible. Future studies are needed to determine whether the contributions of hemoglobin and myoglobin influence the current measurements, but these studies will require a device that can separate the absorption spectra of these two heme sources.
In conclusion, this study reports changes in skeletal muscle mitochondrial oxidative capacity in response to endurance exercise training and detraining measured in the wrist flexor muscles with NIRS. Both the magnitude and the time course of changes in mitochondrial capacity were consistent with previous studies using both in vitro and in vivo methods. NIRS-based assessments of mitochondrial capacity have previously been shown to be reproducible, independent of the type or magnitude of exercise needed to perform the measurements and to detect differences in training status in cross-sectional studies. In addition, the NIRS measurements are inexpensive, portable, and easy to perform. Future studies could use NIRS to examine mitochondrial capacity in both research and clinical settings, especially when repeated-measures on human participants are of interest.
The authors thank the participants of this study for their enthusiastic commitment to this study.
This study was funded in part by the National Institutes of Health (grant no. HD-039676) and the University of Georgia Graduate School intramural grants.
The authors report no conflicts of interest.
The results of the present study do not constitute endorsement by the American College of Sports Medicine.
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Keywords:© 2013 American College of Sports Medicine
NIRS; MITOCHONDRIAL CAPACITY; OXIDATIVE METABOLISM; ENDURANCE TRAINING; DETRAINING