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Changes in transverse relaxation time of quadriceps femoris muscles after active recovery exercises with different intensities a

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Takahiro Mukaimoto , Syun Semba , Yosuke Inoue & Makoto Ohno a

Research Institute for Sport Science, Nippon Sport Science University, Tokyo, Japan

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Graduate School of Health and Sport Science, Nippon Sport Science University, Tokyo, Japan Published online: 10 Jan 2014.

Click for updates To cite this article: Takahiro Mukaimoto, Syun Semba, Yosuke Inoue & Makoto Ohno (2014) Changes in transverse relaxation time of quadriceps femoris muscles after active recovery exercises with different intensities, Journal of Sports Sciences, 32:8, 766-775, DOI: 10.1080/02640414.2013.855803 To link to this article: http://dx.doi.org/10.1080/02640414.2013.855803

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Journal of Sports Sciences, 2014 Vol. 32, No. 8, 766–775, http://dx.doi.org/10.1080/02640414.2013.855803

Changes in transverse relaxation time of quadriceps femoris muscles after active recovery exercises with different intensities

TAKAHIRO MUKAIMOTO1, SYUN SEMBA2, YOSUKE INOUE1 & MAKOTO OHNO2 1

Research Institute for Sport Science, Nippon Sport Science University, Tokyo, Japan and 2Graduate School of Health and Sport Science, Nippon Sport Science University, Tokyo, Japan

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(Accepted 11 October 2013)

Abstract The purpose of this study was to examine the changes in the metabolic state of quadriceps femoris muscles using transverse relaxation time (T2), measured by muscle functional magnetic resonance (MR) imaging, after inactive or active recovery exercises with different intensities following high-intensity knee-extension exercise. Eight healthy men performed recovery sessions with four different conditions for 20 min after high-intensity knee-extension exercise on separate days. During the recovery session, the participants conducted a light cycle exercise for 20 min using a cycle (50%, 70% and 100% of the lactate threshold (LT), respectively: active recovery), and inactive recovery. The MR images of quadriceps femoris muscles were taken before the trial and after the recovery session every 30 min for 120 min. The percentage changes in T2 for the rectus femoris and vastus medialis muscles after the recovery session in 50%LT and 70%LT were significantly lower than those in either inactive recovery or 100%LT. There were no significant differences in those for vastus lateralis and vastus intermedius muscles among the four trials. The percentage changes in T2 of rectus femoris and vastus medialis muscles after the recovery session in 50%LT and 70%LT decreased to the values before the trial faster than those in either inactive recovery or 100%LT. Those of vastus lateralis and vastus intermedius muscles after the recovery session in 50%LT and 70%LT decreased to the values before the trial faster than those in 100%LT. Although the changes in T2 after active recovery exercises were not uniform in exercised muscles, the results of this study suggest that active recovery exercise with the intensities below LT are more effective to recover the metabolic state of quadriceps femoris muscles after intense exercise than with either intensity at LT or inactive recovery. Keywords: recovery exercise, active rest, transverse relaxation time, metabolic state, blood lactate concentration

Introduction Conventionally, low-intensity aerobic exercise during recovery from intense exercise, called active recovery exercise, is utilised for rapid recovery from fatigue. It has been widely demonstrated in humans that lactate accumulation is closely associated with muscle fatigue and endurance (Fairchild et al., 2003; Jacobs, 1986; Tesch & Wright, 1983). In previous studies, it has been reported that active recovery exercise results in more rapid lactate decrease from the blood and muscle than inactive recovery (Ahmaidi et al., 1996; Ainsworth, Serfass, & Leon, 1993; Bangsbo, Graham, Johansen, & Saltin, 1994; Dodd, Powers, Callender, & Brooks, 1984). As the exercise intensity increases, so does the blood flow; therefore, the transport of lactate to the heart and skeletal muscles increases because the heart (Åstrand, Rodahl, Dahl, & Strømme, 2003) and skeletal muscles (i.e. type Ι muscle fibres) (Brooks,

2001; Gladden, 2000) are major lactate-uptake sites. Also, active recovery exercise with a moderate intensity after intense exercise could enhance lactate metabolism within the previously exercised muscles by oxidation and/or glyconeogenesis or increase the efflux of lactate from these muscles and its transport to other tissues for oxidation or synthesis to glucose. Conversely, exercise intensity above the anaerobic threshold and/or lactate threshold (LT) causing lactate accumulation is likely to offset the influence of lactate uptake on lactate disappearance (Rowell, 1974; Stamford, Weltman, Moffatt, & Sady, 1981). With regard to the optimal exercise intensity for active recovery, previous studies have indicated that active recovery exercise at intensities ranging between 29% and 40% of maximum oxygen uptake : (VO2 max) (Stamford et al., 1981) or the level of LT (McLellan & Skinner, 1982) is most effective for promoting blood lactate decrease. However, active

Correspondence: Takahiro Mukaimoto, Research Institute for Sport Science, Nippon Sport Science University, 7-1-1 Fukasawa, setagaya-ku, Tokyo 158–8508, Japan. E-mail: [email protected] © 2013 Taylor & Francis

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Metabolic state of quadriceps femoris muscles after active rest recovery exercise with intensities ranging between : 60% and 80% of VO2max is no more effective than inactive recovery. On the other hand, Dupont, Moalla, Guinhouya, Ahmaidi, and Berthoin (2004) and Dupont, Moalla, Matran, and Berthoin (2007) investigated the local regulation in muscles with a repeated series of moderate recovery exercise, detected by near-infrared spectroscopy. They reported that the mean rate of decrease in oxy-haemoglobin with active recovery exercise with moderate intensity was significantly faster (Dupont et al., 2004), and deoxy-haemoglobin variations were significantly higher in active recovery conditions with low intensity (Dupont et al., 2007), compared with inactive recovery. In addition, Koizumi et al. (2011) reported that active recovery exercise with moderate exercise intensity for 20 min resulted in a higher muscle oxygenation level in the vastus lateralis. Thus, it has been suggested that active recovery would enable the blood flow to be higher from previously exercised muscle, which would increase O2 supply and phosphorylcreatine re-synthesis in local muscles (Bogdanis, Nevill, Lakomy, Graham, & Louis, 1996; Dorado, Sanchis-Moysi, & Calbet, 2004). However, no studies have examined the effects of active recovery exercises with different intensities on the metabolic state of individual muscles (e.g. quadriceps femoris muscles). In recent years, exercise-induced transverse relaxation time (T2), measured using muscle functional magnetic resonance imaging (mfMRI), has been used to assess patterns of muscle activation (Adams, Duvoisin, & Dudley, 1992; Fisher, Meyer, Adams, Foley, & Potchen, 1990) or metabolic state (Prior, Ploutz-Snyder, Cooper, & Meyer, 2001; Vandenborne et al., 2000) from superficial and deep regions of muscles, noninvasively. T2 is a quantitative measurement of a basic biophysical property that leads to signal contrast shift on MRI. This has been used to infer which muscles were used during the activity and the extent of their contribution. Moreover, it has been demonstrated that the magnitudes of exercise-induced elevations in T2 are directly related to integrated electromyogram activity (Adams et al., 1992), isometric torque induced by electromyostimulation (Adams, Harris, Woodard, & Dudley, 1993), increases in exercise intensity (Adams et al., 1992, 1993; Fisher et al., 1990) and the metabolic state of skeletal muscle (Prior et al., 2001; Vandenborne et al., 2000). Thus, exerciseinduced contrast shifts in mfMRI have been used to reflect activation and/or metabolic state in working muscles. However, mfMRI has never been applied to assess muscle metabolic characteristics of previously exercised quadriceps femoris muscles after active recovery exercises at the level of LT or below it.

Therefore, the purpose of the present study was to examine the changes in the metabolic state of quadriceps femoris muscles using mfMRI after inactive rest or active recovery exercises with different intensities following high-intensity knee-extension exercise. We hypothesised that active recovery exercise at an intensity below LT would result in a faster recovery from intense exercise of the metabolic state in quadriceps femoris muscles, compared with those at an intensity at LT or inactive recovery, because a delay of recovery in blood lactate would be associated with that in T2 values.

Materials and methods Participants Eight healthy men of similar age, physique and physical activity level were recruited to participate in this study. All participants were physically active and trained recreationally with sufficient experience of resistance and aerobic exercises (at least 2 days ∙ week–1 in 6 months prior to the study), but did not have any experience of competitive sports. None of the participants was a smoker, habitual drinker or took any medications, ergogenic supplements, or nutritional supplements known to affect energy metabolism or exercise performance. Before this experiment, the procedure, purpose, risks and benefits associated with this study were explained and written informed consent was obtained. The procedures of the study were reviewed and approved by the Ethical Review Board of Nippon Sport Science University and undertaken in accordance with the Declaration of Helsinki. The physical characteristics of the participants are presented in Table I.

Experimental schedule All participants visited the laboratory for six times during the experimental period. During the first visit, body composition was determined using Table I. Physical characteristics of participants (n = 8). Age (years) Height (cm) Body weight (kg) Body mass index (kg · m−2) Percent body fat (%) Knee extension 1-RM (kg) : VO2peak (ml · kg−1 · min−1) HRpeak (beats · min−1) : VO2 on LT (ml · kg−1 · min−1) HR on LT (beats · min−1)

25.8 168.6 66.4 23.3 16.7 38.8 48.8 193.5 23.8 112.4

± ± ± ± ± ± ± ± ± ±

2.1 4.2 4.8 1.2 2.4 5.4 3.2 1.1 2.0 9.9

Notes: Values are means ± standard deviation. 1-RM = one-repeti: tion maximum, VO2 = oxygen uptake, HR = heart rate, LT = lactate threshold.

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bioelectrical impedance analysis (Inner Scan BC600, TANITA Co., Tokyo, Japan). Subsequently, each participant performed a one-repetition maximum (1-RM) strength test of bilateral knee-extension exercise using an isotonic exercise machine (PROTEUS STUDIO-2000, PROTEUS, Taiwan). Before 1-RM was assessed, a warm-up that included 10–15 repetitions at 50% of the participant’s perceived 1-RM was undertaken. Following a period of rest for 3 min, the participants carried out a 1-RM estimation test. The initial load was set to participant’s estimated 1-RM, and increased by 5 kg after each successful attempt until the 1-RM value was identified. Each trial was separated by an interval time of 3 min. The 1-RM was defined as the maximum amount of weight lifted during one full range of motion without a bounce. The range of motion in each set of exercises was from 90° to 0° (0° at full extension). During the: second visit, participants performed the LT and VO2peak test by a graded exercise test on a cycle ergometer (AEROBIKE800, COMBI, Japan). This test was conducted for the calculation of the exercise intensity of the active recovery commensurate with each participant’s aerobic ability. Blood lactate concentration was measured every 2 min using a lactate analyser (Lactate : Pro LT − 1710, ARKRAY, Japan), and VO2 was collected continuously in a breath-by-breath manner using a portable cardiopulmonary exercise system (METAMAX3B, CORTEX, Germany). The participants started cycling at 50 W for the first 5 min, and the power output was increased by 20 W every 2 min until maximum volitional exhaustion (American College of Sports Medicine, 2006). The test was terminated when the participant failed to maintain the prescribed pedalling frequency of : 50 rpm or reached a plateau in VO2. The LT was defined as the intensity at which blood lactate concentration begins to increase curvilinearly with the increasing workload (Kindermann, Simon, & Keul, 1979). That is, a computerised two-linear regression analysis was performed to locate the intersection of the line of the blood lactate concentration versus workload from which the estimate LT values were identified. Then, the workload of the following three active recovery exercises was calculated based on the estimated LT. During visits three to six, in a random order, the participants performed the following four conditions of recovery after bilateral high-intensity knee-extension exercise described below: (1) inactive recovery on a chair; (2) active recovery exercise at 50% of the LT (50%LT); (3) active recovery exercise at 70% of the LT (70%LT); and (4) active recovery exercise at 100% of the LT (100%LT). All participants performed all trials with at least 4 days between the trials within a period of 4 weeks. Each trial was performed between 08:00 and 13:00 h

after an overnight fasting of 12 h. Participants were requested not to participate in any vigorous activities on the day before each trial. They were also instructed to refrain from ingesting alcohol and caffeine. The experiments were conducted in a laboratory with air-conditioning and room temperature and relative humidity were maintained at 23–24°C and 50–60%, respectively, throughout the experiments. Regimens of knee-extension exercise and recovery session The experimental procedure is shown in Figure 1. The participants rested on a comfortable chair for 10 min, and then MR images of the right femur of the participants were taken. Subsequently, the kneeextension exercise was performed with six sets using an isotonic exercise machine, with a 1 min resting period between each trial. The exercise intensity of knee-extension exercise was set to 80% of the 1-RM for each participant according to the previously established 1-RM. The relative intensity (%1-RM) of the exercise was calculated with reference to a repetitive movement conversion table (Carmer & Coburn, 2004) utilising previously determined values of 1-RM. The range of motion in each set of exercises was from 90° to 0° (0° at full extension). Each set was continued until maximum exhaustion. The participants were instructed to maintain a constant speed of 1 s in the lifting phase and 2 s in the lowering phase, with no pause between the phases. To facilitate a constant speed of movement during each phase, a digital metronome was used. The three active recovery sessions were performed with the prescribed constant workload by a cycle ergometer. The workloads in each active recovery exercise were determined : by linear regression of the data obtained during VO2peak test. The pedalling

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Figure 1. Experimental procedure. Note: 1-RM = one-repetition maximum, IR = inactive recovery on a chair, LT = lactate threshold, RPE = ratings of perceived exertion, : VO2 = oxygen uptake, HR = heart rate, La = blood lactate concentration, MRI = magnetic resonance imaging.

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Metabolic state of quadriceps femoris muscles after active rest frequency was set at 60 rpm. All participants conducted a recovery session under the prescribed conditions for 20 min. The duration of the recovery session was determined on the basis of previous studies (Hermansen & Osnes, 1972; Koizumi et al., 2011). Subsequently, MR images of the right femur of the participants were taken within 10 min after the recovery session, and they then rested on a comfortable chair for 120 min. MR images were taken every 30 min to determine the T2 value. In the inactive recovery trial, they rested for the same time throughout the active recovery exercise session. The seated participants were instructed to stay unmoved as much as possible. In addition, they indicated their ratings of perceived exertion on Borg’s 15-point rating scale (Noble, Borg, Jacobs, Ceci, & Kaiser, 1983) immediately after the knee-extension exercise and every 5 min in the recovery session. Measurement of blood lactate concentration Blood samples were collected before and immediately after the knee-extension exercise, and at 0, 30, 60, 90 and 120 min after the recovery session. Five microlitres of blood was taken from a fingertip and immediately analysed for blood lactate concentration using a lactate analyser. Measurement of expired gas and heart rate Expired gas was collected continuously to determine : : VO2, carbon dioxide production (VCO2) and ventilation volume in a breath-by-breath manner using a portable cardiopulmonary exercise system. Similarly, heart rate was measured continuously using a wireless heart rate monitor (POLAR, Finland) throughout the recovery session. The obtained values were converted into average values for each minute using expired gas analytical software (MetaSoft, CORTEX, Germany). The values obtained during the exercise were averaged every 1 min, and mean VO2 throughout the recovery session for 20 min was then calculated to compare the magnitude of cardiorespiratory stress among the four conditions of recovery session. Appropriate calibrations of the O2 and CO2 sensors and the volume transducer were conducted before each trial. MR imaging and analysis The mfMRI was detected by a 0.3-T AIRIS scanner (Hitachi Medical Co., Japan) as performed in previous studies (Adams et al., 1993; Akima, Kinugasa, & Kuno, 2005; Kinugasa et al., 2006). Seven 10mm-thick trans-axial T2-weighted images (repetition time = 1600 ms; echo time = 30 and 60 ms; matrix = 256 × 256; field of view = 240 mm;

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number of excitations = 1; scan time = 5 min 7 s) of the right thigh spaced 30 mm apart were collected with a 40-cm-diameter extremity coil. By using padded restraints, the participant’s right thigh was stabilised in a supine position with the knee and ankle at 0° (full extension) and 0° (anatomical position). The right limb was all participants’ dominant side. The participants were fully rested before the first scan. The fourth image corresponded to the 50% level from the greater trochanter to the lateral intercondylar tuberculum. Ink marks on the thigh were aligned with cross-hairs of the imager for a similar positioning of the thigh in the magnet bore over the repeating scans. mfMR images were transferred to a personal computer for calculation of T2 by AquariusNetStation Version 1.5 (TERARECON, Inc., Foster City, CA, USA). After a series of spatial calibration, five regions of interest (1–1.5 cm2) per individual quadriceps femoris muscles (rectus femoris, vastus medialis, vastus lateralis and vastus intermedius muscles) were defined to calculate a mean T2 value at seven slices. We also focused on excluding non-contractile tissues, such as aponeurosis, membranes, vessels, fat, nerves, and the femur from the regions of interest. T2 was calculated for each pixel within the regions of interest from the following formula: T2 = (ta − tb)/In(ia/ib), where ta and tb are the spinecho collection times, In is the natural log, and ia and ib are the signal intensities (Adams et al., 1993; Akima et al., 2005). The coefficients of variation for resting T2 values of quadriceps femoris muscles before knee-extension exercise were 3.9% in rectus femoris muscle, 3.6% in vastus medialis muscle, 3.8% in vastus lateralis muscle and 3.5% in vastus intermedius muscle. No significant difference was observed in the resting T2 values of quadriceps femoris muscles before knee-extension exercise among the four trials (data not shown).

Statistical analysis The data are presented as means ± standard deviation. A one-way analysis of variance (ANOVA) with repeated measures was used to examine differences in ratings of perceived exertion and physiological responses during recovery sessions among the four trials. A two-way (trial × time) ANOVA with repeated measures was used to determine the interaction and main effects in blood lactate concentration and T2 values after recovery sessions among the four trials. When ANOVA revealed significant interaction or main effect, post hoc analysis was performed using Scheffé’s multiple comparison test. For all statistical tests, P < 0.05 was considered significant.

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Results Blood lactate concentration (mmol/l)

There were no significant changes among each participant in height, body weight and 1-RM over the course of the experiment. The average value of the load throughout the six sets of knee-extension exercise in all trials was 29.8 ± 4.1 kg · set −1. The rating of perceived exertion immediately after the kneeextension exercise in all trials was 15.0 ± 1.3 (arbitrary unit). Blood lactate concentration and T2 values for quadriceps femoris muscles immediately after the six sets of the knee-extension exercise in all trials were significantly greater than the resting values before the knee-extension exercise. On the other hand, there were no significant differences among the four trials in blood lactate concentration and T2 values for quadriceps femoris muscles immediately after the knee-extension exercise. Table II shows the workload in active recovery exercise using a cycle ergometer, and ratings of perceived exertion and physiological responses during the recovery session under the four different conditions. Ratings of perceived exertion were the averages of values determined every 5 min in the recovery session for 20 min. The ratings of perceived exertion in 70%LT and 100%LT were significantly higher than in inactive recovery and 50%LT (P < 0.05), and those in 100%LT were significantly higher than : in 70%LT (P < 0.05). The VO2 and heart rate over the recovery session for 20 min in 100%LT were significantly greater than those in the other trials (100%LT > 70% LT > 50%LT > inactive recovery, P < 0.05). The ventilation volume in 100%LT was significantly greater than those in the other trials (P < 0.05), and those in 50%LT and 70%LT were significantly greater than that in inactive recovery (P < 0.05). No significant difference was observed between 50%LT and 70%LT. In contrast, the blood lactate concentrations immediately after the recovery session in 50%LT and 70%LT were significantly lower than in inactive recovery or 100%LT

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Figure 2. Blood lactate concentration before and after knee-extension exercise, and after the recovery session of four different conditions. Notes: Values are means ± standard deviation. IR = inactive recovery on a chair, LT = lactate threshold. Arrow line (→) significant difference (P < 0.05) from resting values before kneeextension exercise. a Significant difference (P < 0.05) between 50%LT and IR, b Significant difference (P < 0.05) between 50%LT and 100% LT, aaSignificant difference (P < 0.05) between 70%LT and IR, bb Significant difference (P < 0.05) between 70%LT and 100%LT.

(P < 0.05), whereas no significant difference was observed between 50%LT and 70%LT. Figure 2 shows blood lactate concentration before and after the knee-extension exercise, and after the recovery session of the four different conditions. The blood lactate concentration was found to be significantly higher from immediately after the recovery session to 30 min after the recovery session in 100% LT (P < 0.05), and at immediately after the recovery session in the other three trials (P < 0.05), than the resting value before the knee-extension exercise. The only significant differences in blood lactate concentrations among the four recovery conditions were observed immediately after the recovery session.

Table II. Workload in active recovery exercise by cycle ergometer, and ratings of perceived exertion and physiological responses during recovery session of four different conditions. IR Workload (W) RPE (Arbitrary unit) : VO2 (ml · kg−1 · min−1) −1 HR : (beats · min ) VE (l · min−1) La* (mmol · l−1)

9.1 4.4 66.6 9.6 2.7

– ± ± ± ± ±

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1.8 0.3 8.1 1.2 0.3bc

50.5 9.1 16.5 94.8 25.7 2.2

± ± ± ± ± ±

11.1 1.7 1.9a 5.6a 3.0a 0.5

70%LT 69.2 11.1 18.5 103.2 28.4 2.3

± ± ± ± ± ±

15.3b 1.7ab 2.8ab 8.1ab 4.1a 0.5

100%LT 93.3 12.5 22.9 112.3 34.2 3.2

± ± ± ± ± ±

21.2bc 1.7abc 2.7abc 11.0abc 4.1abc 0.8bc

Notes: Values are means on a chair, LT = lactate threshold, RPE = ratings of : : ± standard deviation. IR = inactive recovery perceived exertion, VO2 = oxygen uptake, HR = heart rate, V E = ventilation volume, La = blood lactate concentration, * values which was obtained immediately after recovery session, aSignificant difference (P < 0.05) from IR, bSignificant difference (P < 0.05) from 50%LT, cSignificant difference (P < 0.05) from 70%LT.

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Figure 3. Percentage change in T2 values of quadriceps femoris muscles, before and after knee-extension exercise, and after the recovery session of four conditions. Notes: Values are means ± standard deviation. RF = rectus femoris; VM = vastus medialis; VL = vastus lateralis; VI = vastus intermedius; IR = inactive recovery on a chair; LT = lactate threshold. Arrow line (→) significant difference (P < 0.05) from resting values before knee-extension exercise. aSignificant difference (P < 0.05) between 50%LT and IR, bSignificant difference (P < 0.05) between 50%LT and 100%LT, aa Significant difference (P < 0.05) between 70%LT and IR, bbSignificant difference (P < 0.05) between 70%LT and 100%LT.

Figure 3 shows percentage change in T2 values for rectus femoris, vastus medialis, vastus lateralis and vastus intermedius muscles, before and after the knee-extension exercise and after the recovery session under the four conditions. The percentage changes in T2 for the rectus femoris and vastus medialis muscles were found to be significantly higher from immediately after the recovery session to 60 min after the recovery session in 100%LT (P < 0.05), from immediately after the recovery session to 30 min after the recovery session in inactive recovery (P < 0.05) and at immediately after the recovery session in 50%LT and 70%LT, than the resting value before the knee-extension exercise. The percentage changes in T2 for the vastus lateralis and vastus intermedius muscles were found to be significantly higher from immediately after the recovery session to 60 min after the recovery session in

100%LT, and from immediately after the recovery session to 30 min after the recovery session in the other three trials. Upon comparison among the four recovery conditions, the percentage changes in T2 for the rectus femoris muscle were found to be significantly lower from immediately after the recovery session to 60 min after the recovery session in 50%LT and 70%LT than in 100%LT (P < 0.05). In addition, the percentage changes in T2 for the rectus femoris muscle were found to be significantly lower at 30 min and 60 min after the recovery session in 50%LT and 70%LT than in inactive recovery (P < 0.05). The percentage changes in T2 for the vastus medialis muscle were found to be significantly lower from immediately after the recovery session to 30 min after the recovery session in 50%LT and 70%LT than in 100%LT (P < 0.05). No significant

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differences in the percentage change in T2 for the vastus lateralis and vastus intermedius muscles were observed at any time point among the four trials.

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Discussion Although previous studies have evaluated physiological responses in active recovery exercise of different intensities by changes in blood lactate concentration (Greenwood, Moses, Bernardino, Gaesser, & Weltman, 2008; McLellan & Skinner, 1982; Stamford et al., 1981), little is known about the metabolic state in individual exercised muscles after active recovery. Thus, we examined changes in blood lactate concentration and metabolic state in quadriceps femoris muscles using mfMRI signal changes after moderate active recovery cycle exercise standardised by each LT level, following a highintensity knee-extension exercise. Bogdanis et al. (1996) conducted two maximum 30 s cycle ergometer sprints separated by 4 min and showed improved mean power output with active recovery compared with inactive recovery in the second sprint. However, in their study, the performance significantly decreased in the second sprint compared with the first sprint in both active and inactive recoveries. Hermansen and Osnes (1972) reported that a complete recovery of pH in the muscle from intense exercise requires a rest interval of approximately 30 min, in the case of inactive recovery. On the other hand, Koizumi et al. (2011) reported that active recovery exercise for 20 min resulted in a higher muscle oxygenation level during the second exercise, concomitant with a decreased blood lactate concentration. Furthermore, the authors reported that no reduction in performance of the second compared with the first exercise was shown in both active and inactive recovery for 20 min, and suggested that a rest interval of 20 min was appropriate for assessing the effects of active recovery compared to the natural recovery process with time. For this reason, in the present study, the duration of the recovery session was set to 20 min. Many previous studies have reported that active recovery exercise results in a more rapid lactate decrease from the blood and muscle than inactive recovery (Ahmaidi et al., 1996; Ainsworth et al., 1993; Bangsbo et al., 1994; Dodd et al., 1984); additionally, the rapid lactate decrease after active recovery exercise is more effective at an intensity below LT than above LT (Greenwood et al., 2008; McLellan & Skinner, 1982; Stamford et al., 1981). In the present study, on comparison among the four recovery conditions, the blood lactate concentration was found to be significantly lower immediately after the recovery session in 50%LT and 70%LT than in inactive recovery and 100%LT (Figure 2). On the

other hand, there were no significant differences in the blood lactate concentration between 50%LT and 70%LT, and between inactive recovery and 100% LT. Intense exercises prior to active recovery exercise in previous studies have been performed until exhaustion at an exercise intensity above (Fairchild : et al., 2003) or close to VO2max (McLellan & Skinner, 1982), using a cycle ergometer. In the present study, although the knee-extension exercise prior to the active recovery exercise was conducted until exhaustion or maximum repetition with a high resistance load, blood lactate concentration before the active recovery exercise was lower in the present study than in previous studies. In the previous studies on the effect of active recovery exercise, the cycle exercise which consists of a complex pattern of knee extension and flexion motions was often used for main intensive exercise before recovery treatment. During the cycle exercise, not only quadriceps femoris muscles but also flexor and adductor muscles are engaged (Watanabe, Katayama, Ishida, & Akima, 2009). A previous study reported that the flexor and adductor muscles each occupy approximately 25% of the thigh in healthy individuals. In comparison, the knee extensor muscles occupy approximately 50% of the thigh (Akima et al., 2007). The total muscle volume involved plays the absolute role in power output during exercise (Fukunaga et al., 2001), and is closely associated with the amount of the glycolytic metabolism in each muscle, which should produce a higher level of blood lactate concentration. Thus, it is of necessity that the increase in the blood lactate concentration during knee-extension exercise was lower than during the cycle exercise in the previous studies. Nevertheless, the results in the present study showed the marked difference in the blood lactate concentration among the four recovery conditions, which would indicate the inclusive manner of the moderate active recovery irrespective of the total amount of the metabolites from the intensive exercise. In this study, the percentage changes in T2 for rectus femoris and vastus medialis muscles after the recovery session with 50%LT and 70%LT returned to the resting level faster than those in inactive recovery and 100%LT. In addition, the percentage changes in T2 for vastus lateralis and vastus intermedius after the recovery session with 50%LT, 70% LT and inactive recovery returned to the resting level faster than those in 100%LT. High-intensity resistance exercise leads to local accumulation of metabolites such as lactate and protons. The resulting pH change inhibits glycolytic enzymes such as lactate dehydrogenase and phosphofructokinase, and muscular contraction might be impaired (Karlsson, Hulten, & Sjodin, 1974). It has been reported that the exercise-induced T2 increase results from

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Metabolic state of quadriceps femoris muscles after active rest osmotically driven shifts of water that increase the volume of intracellular space and from intracellular acidification resulting from metabolic end products (Patten, Meyer, & Fleckenstein, 2003; Prior et al., 2001). Kinugasa et al. (2006) suggested that perfusion is one of the factors underlying the exerciseinduced T2 changes. The perfusion of exercising muscle under conditions of metabolite accumulation would provide the water necessary to expand the extracellular fluid volume of contracting muscle further, thereby further increasing T2 found (Kinugasa et al., 2006; Prior et al., 2001). In contrast, active recovery exercise following intense resistance exercise may promote muscle pump action and induce efflux of metabolites in the muscles, associated with increased blood flow (Bangsbo, Johansen, Graham, & Saltin, 1993; Bogdanis et al., 1996). Relating the T2 values, it has been reported that the pattern of signal intensity on T2-weighted MRI during the recovery period of a maximum voluntary contraction task is closely related to the total myoglobin/haemoglobin signal detected by near-infrared spectroscopy (Kuboki et al., 2001). Dupont et al. (2004) examined the changes of muscle oxygenation level during active recovery or inactive recovery between intermittent exercises until exhaustion, and reported that the oxygenated myoglobin/haemoglobin concentration level was lower in the active condition than in the inactive condition. In addition, Bangsbo et al. (1994) investigated the effect of lowintensity exercise on lactate metabolism during the first 10 min of recovery exercise from exhaustive knee-extension exercise. The authors showed that the leg O2 consumption level was increased and the muscle lactate was decreased during the recovery period. During the active recovery period, the O2 supply can increase in exercising muscle tissues, and therefore the input and output would tend to be imbalanced, showing a lower muscle oxygenation level. During active recovery exercise, O2 supply and consumption would increase in the exercising muscles, although O2 consumption is restrained in the higher intensity active recovery exercise above LT. In addition, it is considered that the active recovery exercise below LT promotes reductions of metabolites such as lactate and protons in the aerobic metabolism system, simultaneously with the promotion of O2 supply and consumption for exercising muscles (Åstrand et al., 2003; Gladden, 2000). Therefore, it is speculated that rapid recovery of T2 in exercised muscles from intense exercise was observed after exercise in the active recovery exercises below LT, compared with that in the active recovery exercise at 100%LT or on inactive rest. It has been shown that quadriceps femoris muscles are the principal muscles that generate knee-

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extension torque (Levangie & Norkin, 2001). Previous studies have reported that, in the structure of the quadriceps femoris muscles, the activity of each muscle is not necessarily uniform (Akima, Foley, Prior, Dudley, & Meyer, 2002; Akima, Takahashi, Kuno, & Katsuta, 2004; Ebenbichler et al., 1998). Ebenbichler et al. (1998) suggested that the activation pattern of rectus femoris muscle in submaximal isometric knee-extension exercise is different from those in the three vasti muscles. In the present study, the percentage change in the T2 for the rectus femoris muscle was significantly smaller in 50%LT and 70%LT than in inactive recovery, at 30 and 60 min after the recovery session, and in 100% LT, immediately and 30 and 60 min after the recovery session. Percentage change in the T2 for vastus medialis muscle was significantly smaller in 50%LT and 70%LT than in 100%LT immediately and 30 min after the recovery session. On the other hand, in terms of the percentage change in T2 for vastus medialis and vastus intermedius muscles, no significant differences were observed among the four different recovery conditions. It has been suggested that the mono-articular vasti muscles are responsible for force and power generation around the knee joint, while the bi-articular rectus femoris muscle predominantly controls net torque at the hip and knee joints, and transfers power between the hip and knee joints (Doorenbosch, Welter, & van Ingen Schenau, 1997; Jacobs, Bobbert, & van Ingen Schenau, 1996). Moreover, some studies have reported that rectus femoris muscle was the most activated among the individual quadriceps femoris muscles after isokinetic knee-extension exercises (Akima et al., 2004). It has been reported that three vasti muscles, namely, vastus lateralis, vastus medialis, and vastus intermedius muscles, are synergistic muscles (Nichols, Cope, & Abelew, 1999). It has been demonstrated that there are strong monosynaptic Ia linkages among the three vasti muscles, but linkages between individual vasti muscles and rectus femoris muscle are weaker (Nichols et al., 1999). In the present study, percentage change in T2 of rectus femoris muscle after the knee-extension exercise showed the highest values; therefore, the responses on T2 of rectus femoris muscle might also be sensitive to active recovery exercise compared with the other three muscles (Figure 3). On the other hand, in terms of the percentage change in T2 of the vastus lateralis muscle in this study, no significant differences were observed among the four different recovery conditions. Some recent studies reported that vasti muscles, especially vastus lateralis muscle, were the most activated among the femoral muscles across constant workload cycling exercise (Reid, Foley, Jayaraman, Prior, & Meyer, 2001) and sprint cycling (Akima

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T. Mukaimoto et al.

et al., 2005; Takahashi et al., 2002). Therefore, it is speculated that recovery of T2 in vastus lateralis muscle after the recovery session was not influenced by the intensity of the active recovery exercise or inactive rest because body fluid containing the metabolites should shift within the proper working muscles. As regards the T2 values of the vastus medialis muscle, Akima et al. (2005) reported that the vastus medialis muscle appears to be much more important for cycling exercise to maintain power output based on results of a stepwise linear regression analysis. Indeed, in the present study, the power output in vastus medialis muscle could be greater during the active recovery exercise at 100%LT than the other recovery sessions. Thus, it is considered that T2 of vastus medialis muscle after active recovery exercise at 100%LT was significantly higher than those at 50% and 70%, although there was no significant difference compared with inactive recovery. No significant differences among the four recovery conditions were observed in T2 of vastus intermedius muscle at any point in time after the recovery sessions. These results might be partly explained by different blood flow and/or metabolic state within the quadriceps femoris muscles (Miura, McCully, & Chance, 2003; Moritani, Sherman, Shibata, Matsumoto, & Shinohara, 1992). Vastus intermedius muscle tends to be higher in terms of the ratio of slow twitch fibbers than the three other synergists (Johnson, Polgar, Weightman, & Appleton, 1973). Moreover, Hannukainen et al. (2006) demonstrated using positron emission tomography that the perfusion and free fatty acid uptake levels were higher in vastus intermedius muscle than in the other three synergists. Considering the above-mentioned physiological characteristics of vastus intermedius muscle, this muscle has the greatest capacity for aerobic metabolism than the other three synergists, and thereby efficiently consumes the metabolites in the recovery period. Thus, it is considered that the recovery of T2 in vastus intermedius muscle was not influenced by the exercise intensity in the active recovery exercise. However, as we did not measure blood flow or metabolites in the muscles, whether the above-mentioned physiological responses in individual muscles occurred in the present study is unclear. Consequently, further investigations are required to resolve these issues. In conclusion, we examined changes in the metabolic state of quadriceps femoris muscles from T2 values on mfMRI after inactive rest or active recovery exercises with different intensities following an intense knee-extension exercise. Although the change of T2 after active recovery exercise was not uniform in the exercised muscles, the results of this study suggested that active recovery exercise with below LT intensities are more effective to recover the metabolic condition in

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