ADAPTATION OF LOCAL MUSCLE BLOOD FLOW AND SURFACE ELECTROMYOGRAPHY TO REPEATED BOUTS OF ECCENTRIC EXERCISE MAHDI HOSSEINZADEH, OLE K. ANDERSEN, LARS ARENDT-NIELSEN, AFSHIN SAMANI, ERNEST N. KAMAVUAKO, AND PASCAL MADELEINE Center for Sensory-Motor Interaction, Department of Health Science and Technology, School of Medicine, Aalborg University, Aalborg, Denmark ABSTRACT Hosseinzadeh, M, Andersen, OK, Arendt-Nielsen, L, Samani, A, Kamavuako, EN, and Madeleine, P. Adaptation of local muscle blood flow and surface electromyography to repeated bouts of eccentric exercise. J Strength Cond Res 29(4): 1017– 1026, 2015—The aim of this randomized controlled crossover study was to investigate the effect of a bout of unaccustomed eccentric exercise (ECC) followed by a consecutive bout of the same intensity on local muscle blood flow, amplitude, and frequency of the electromyographic (EMG) signal from the exercised tibialis anterior muscle. Sixteen healthy male participants (age, 25.7 (0.6) years; body mass index 24.8 (1) kg$m22) participated in this study. Two identical bouts of high-intensity ECC were performed on the tibialis anterior muscle 7 days apart. Control sessions involving no exercise were performed 4 weeks either before or after the exercise sessions. Changes in local total blood flow [DtHb], EMG root mean square, and median power frequency were recorded during isometric maximum voluntary contraction of ankle dorsiflexion. Measurements were performed before, immediately after, and the day after both ECCs (ECC1 and ECC2). The participants rested quietly in a chair in the control session. Eccentric exercise 1 led to a significant decrease in [DtHb] on the day after (p # 0.05), whereas ECC2 did not. Median power frequency decreased significantly in ECC2 compared with ECC1 (p , 0.01). Root mean square was unchanged in all the instants. The present study showed that adaptation is depicted in the local muscle blood flow and the frequency contents of the EMG after an unaccustomed ECC inducing muscle soreness. These alterations provide a potential mechanism for a rapid adaptation, which decreases susceptibility

Address correspondence to Ole K. Andersen, [email protected] 29(4)/1017–1026 Journal of Strength and Conditioning Research Ó 2015 National Strength and Conditioning Association

of the muscle to develop further soreness in the subsequent ECC bout.

KEY WORDS local muscle blood flow, repeated bout effect, central adaptation, delayed onset muscle soreness

INTRODUCTION

E

ccentric exercise (ECC) occurs frequently in everyday activities and in athletic competitions such as downhill skiing, walking, or running. Eccentric exercise regimen focuses on the eccentric phase of muscle contraction that causes a muscle to lengthen during force exertion. Unaccustomed highintensity ECC enhances nociceptive input (17), depresses muscle force output and range of movement, increases muscle proteins such as creatine kinase and myoglobin in the circulation (5,17,33,35). Eccentric exercise can also be accompanied by delayed onset muscle soreness (DOMS) for several days after the exercise (2,5,8,35). Ultrastructural changes, damage to t-tubules, mitochondrial swelling, and increased intramuscular pressure (6,15,16) can be demonstrated after ECC. An increase in intramuscular pressure, vasodilation, and changes in water content of the muscle immediately after ECC may change the pattern of local blood flow and thereby muscle oxygenation. The effect of ECC on muscle oxygenation however is not fully understood and contradictory results have been reported in the few studies available in the literature. Ahmadi et al. (1) reported a significant increase in oxygen desaturationresaturation rate for up to 4 days after an exhaustive session of downhill walking. In contrast, Walsh et al. (36) did not report any significant changes in oxygen utilization after a 30-minute session of high-intensity ECC. Similarly, no significant change in oxygen uptake was reported after exhaustive exercise, despite a significant increase in muscle blood flow (21). Although unaccustomed ECC can induce symptoms of muscle damage, consecutive bout of the same or similar ECC performed as early as 1–2 days and up to 6 months after the first bout of ECC results in less muscle damage and VOLUME 29 | NUMBER 4 | APRIL 2015 |

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Repeated Bout Effect, Local Muscle Blood Flow and EMG Activity faster recovery of the muscle force and soreness. This phenomenon is known as repeated bout effect (RBE) (2,25). It is likely that changes in muscle fiber recruitment in presence of DOMS may also alter the pattern of muscle oxygenation. A selective damage of fast-twitch glycolytic fibers after a first bout of ECC (22) may lead to recruitment of fewer fasttwitch fibers compensated by additional slow-twitch fibers with a higher oxidative capacity potential for a repeated bout (4). Warren et al. (37) also reported that during a second bout of maximal eccentric contractions 1 week after the first, there is reduction in the electromyographic (EMG) median power frequency (MDF) with minimal change in the EMG root mean square (RMS), indicating greater reliance on slower motor units. Muthalib et al. (27), however, reported that the EMG activation (EMG amplitude) and muscle oxygenation during ECC are not different between 2 consecutive bouts of ECC. On the contrary, Wakefieldl et al. (35) reported that enhanced nociceptive input from the trapezius muscle can elevate habitual trapezius activity (“muscle tonus”) in the homonymous DOMS-afflicted region of the muscle. McHugh (25) also reported that a neural adaptation is most likely demonstrated after a first bout of ECC. This adaptation is reflected in the surface EMG by an increase in amplitude or a decrease in frequency contents after the initial bout of ECC (4,23,25,29,37). The controversial data regarding local muscle blood flow and EMG activity particularly related to RBE calls for further studies. Scientific evidence regarding RBE and its potential adaptive or protective mechanisms can be helpful for the strength and conditioning professionals who perform physical exercises to avoid injury during competitions. It can also be used by sports coaches especially in those sports involving several competitions at a short period of time like wrestling in which a fast recovery from exercise-induced soreness is of great importance. Consequently, to gain more knowledge about the adaptive or protective mechanisms related to RBE, we aimed to investigate whether local muscle blood flow, EMG MDF, and EMG RMS change after a bout of high-intensity ECC within the tibialis anterior (TA) muscle. We hypothesized that a second bout of high-intensity ECC compared with an initial ECC bout will result in an altered pattern of local muscle blood flow, a decrease in EMG MDF, and no change in EMG RMS.

METHODS Experimental Approach to the Problem

In this study, the effects of 2 bouts of high-intensity exhausting isokinetic ECC on local muscle blood flow and EMG activity during isometric maximum voluntary contraction (MVC) performed before, immediately after, and 24 hours after the ECC were investigated in a randomized controlled crossover manner. Maximum voluntary contraction force and soreness intensity were also monitored. Considering a full factorial repeated measures and using small effect size (h = 0.25), confidence level (a = 0.05), and

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desired power (80%) for 10 measurements, a test power analysis was performed and the required total sample size was calculated to be 16 subjects (G*Power 3.1.4 (12)). Experimental procedure is reported in more detail elsewhere (17). Subjects

Sixteen healthy male students voluntarily participated in the study (mean (SD); age, 25.7 (0.6) years with the age range between 18–32 years, body mass 79.9 (3.3) kg, height 179.2 (1.7) cm, body mass index 24.8 (1.0) kg.m22). All the participants were untrained and maintained normal daily activity during the course of the study, but no highintensity exercise was performed during the period of recording. None had participated in strength training for the past 6 months before this study. Participants were requested to avoid taking any anti-inflammatory medication during the study period. The inclusion criteria included the following: no pain, specifically in the lower limb before the experiment; no history of chronic pain; no caffeine and alcohol intake during the last 24 hours before each experimental session; no pain medication; and no stretch/massage exercise or any attempts to reduce soreness after exercise was allowed. The participants were verbally informed of the procedures, and they read and signed an informed consent form before participation. The study was approved by the local ethics committee (approval no. N-20070019) and conducted in accordance with the Declaration of Helsinki. Procedures

The participants were randomly divided into 2 groups and both groups underwent 2 parts (an exercise and a control part) of the experiment in a crossover design. The exercise part was conducted over 2 sessions separated by 1 week. Each session consisted of 2 consecutive days. Local muscle blood flow and EMG activity were recorded at 3 instants: before, immediately after, and the day after the ECC regimen during an isometric MVC of TA muscle of the dominant leg. The second session of ECC (ECC2) was identical to the first session (ECC1). The control session of the experiment was conducted over 4 days with 2 consecutive days during the first week (control 1) and 2 days in the following week (control 2). In the control session, instead of the ECC, the participants maintained the same posture by sitting 15 minutes quietly on the same experimental chair. The control and exercise part of the experiment were interspaced by at least 28 days (Figure 1). Measurements for each participant were done at the same time of the day. Exhausting Isokinetic Eccentric Exercise. A Kin-Com isokinetic dynamometer (Kinetic Communicator 125-AP, software version 4.03; Chattecx Corp., Chattanooga, TN, USA) with a plantar/dorsi attachment (PN. 54708) was used for the ECC of the TA muscle. After familiarization, participants performed isometric ankle dorsiflexion at their maximum

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Figure 1. Graphic illustration of the randomized controlled crossover design and timing of measurements (N = 16). NIRS = near-infrared spectroscopy; EMG = surface electromyography; ECC = high-intensity eccentric exercise of TA muscle.

force level. The dynamometer assured that during both ECCs the participants produced more than 80% of their isometric MVC force before ECC1. The participants performed 6 repetitions per set, with 20 seconds of rest inbetween the sets. The exercise continued for as many sets as required to achieve a condition where participants were no

longer able to maintain an adequate ECC ankle dorsiflexion (DF). The adequate ECC ankle DF was defined as 80% of participants’ isometric MVC force before ECC1. The number of sets, repetitions, and the intensity of the ECC ankle DF was the same across both ECCs. The participants were provided with visual feedback of the force during the ECCs

Figure 2. Maps of the percentage difference in [DtHb] at instants following the 2 bouts of ECC compared with the value before ECCs during maximum isometric MVC for the 7 NIRS channels. Grand percentage was calculated as an average (SEM) of the percentage difference of [DtHb] at all the channels.

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Repeated Bout Effect, Local Muscle Blood Flow and EMG Activity were performed with 60 seconds of rest between each repetition. The Kin-Com isokinetic dynamometer automatically provides the average of MVC force (N) during each 5 seconds. The average of the 6 repetitions was recorded as the isometric MVC force. The relative level of both ECC1 and ECC2 exercises intensity was set at 80% of the MVC force measured before ECC1 to keep similar level of exerted muscle force in both exercises. Soreness Intensity and Soreness Area. The level of soreness was assessed using a 10-cm visual analog scale, where 0 indicated “no soreness” and 10 indicated “maximal soreFigure 3. Configuration of NIRS channels the design permitted EMG electrode in between the NIRS channels on ness.” A human body chart the belly of the TA muscle. The numbers shows the exact placement of the NIRS channels 1–7. TA = tibialis consisting of a bodyline diaanterior. gram was used for outlining the soreness area. The drawand were verbally encouraged by the experimenter to mainings were scanned and processed (Vistametrix; SkillCrest, tain their maximal force. This protocol was used to induce at LLC, Tucson, AZ, USA) to quantify the area of soreness. least 50% reduction of the isometric MVC force at the measurement immediately after ECC. Local Muscle Blood Flow Evaluation by Near-Infrared Spectroscopy. Near-infrared spectroscopy (NIRS) is a noninvasive Isometric Maximum Voluntary Contractions. Participants peroptical technique that has been used to monitor local tissue formed 6 repetitions of maximum isometric DF (100% blood volume and oxygenation (14). Near-infrared spectroscopy measurements were obtained with a continuous waveMVC). The 6 repetitions of the MVC lasting 5 seconds each system (Oxymon MK III; Artinis Medical Systems BV, Elst, the Netherlands) using 2 TABLE 1. Between-day reliability indicators of [DtHb], MVC, EMG RMS, and wavelengths (850 and 760 EMG MDF.* nm). Three transmitter and 3 Measure/testing ICC SEM (same unit as the MDC (same unit as the receiver optodes were configoccasions (no. unit) measure) measure) ured in pairs to form 7 channels (Figure 2). Channels were [DtHb] (mm$L21) subdivided to medial, lateral, Between days 0.95 0.23 0.63 proximal and distal part for furBetween weeks 0.95 0.23 0.63 MVC (N) ther statistical analysis (Figures Between days 0.90 14.23 39.44 2 and 3 for the right placement Between weeks 0.83 18.55 51.41 of the channels). Near-infrared EMG RMS (mV) spectroscopy optodes were Between days 0.81 0.12 0.33 fixed in place over the midbelly Between weeks 0.78 0.13 0.36 EMG MDF (Hz) of the TA muscle (Figure 2). Between days 0.89 5.44 15.08 The interoptode distance was Between weeks 0.82 6.97 19.31 30 mm, allowing a penetration depth of approximately 15 mm *ICC = intraclass correlation coefficient; MDC = minimum detectable change. (13). The relative change in oxygenated and deoxygenated

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TABLE 2. Mean (SD) of isometric MVC force, Grand [DtHb], the RMS, and MDF of the surface EMG signal recorded over the tibialis anterior muscle, soreness, and soreness area before, immediately after, and the day after ECCs and control bouts (p # 0.05).* Control 1 N = 16 MVC force (N) Grand [DtHb] (mM$L21) Mean RMS (mV) MDF (Hz) Soreness score (0–10) Soreness area (arbitrary unit)

Before

Control 2

Day after

Before

ECC1

Day after

Before

After

256.9 (51.4) 244.5 (44.8) 259.1 (37.9) 264.3 (46.5) 257.2 (49.6)

Day after

56.8 (25.1)† 134.8 (53.3)†z

25.2 (4.5)

25.9 (5.4)

25.1 (5.1)

25.4 (4.3)

26.7 (6.1)

11.3 (3.2)†

16.7 (3.9)†z

0.9 (0.3)

1.0 (0.4)

0.9 (0.3)

1.0 (0.2)

1.1 (0.3)

1.2 (0.6)

1.3 (0.3)

123.7 (17.0) 123.8 (15.0) 126.0 (16.8) 127.0 (18.1) 123.5 (14.1) 116.3 (13.3)† 107.4 (13.2) 0.0 0.0 0.0 0.0 0.0 6.2 (2.7)† 6.6 (1.4)†z 0.0

0.0

0.0

0.0

0

0.3

0.5

ECC2 N = 16 MVC force (N) Grand [DtHb] (mM$L21) Mean RMS (mV) MDF (Hz) Soreness score (0–10) Soreness area (arbitrary unit)

Before 220.2 (58.9) 20.3 (5.0)† 1.1 (0.3) 90.2 (9.1)† 1.6 (2.2) 0.2

After 160.2 15.9 1.2 77.9 2.7

Day after

(44.2)z§ (4.6)z§ (0.3) (12.1)z§ (1.8)z 0.1

207.3 (53.2)k 21.4 (4.6)k¶ 1.2 (0.3) 86.1 (11.1)k 1.3 (0.9)k 0.0

*RMS = root mean square; MDF = median power frequency; EMG = electromyography; ECCs = eccentric exercises. †Significantly different from before ECC1. zSignificantly different from after ECC1. §Significantly different from before ECC2. kSignificantly different from day after ECC1. ¶Significantly different from after ECC2.

hemoglobin concentrations ([O2Hb] and [HHb], respectively) was expressed as micromoles (1026 mol)$per liter. Each repetition of MVC led to a trough and a peak in [O2Hb] and [HHb] recordings. The troughs and peaks were detected and the difference between the baseline value (averaged over 0.5 seconds epoch baseline before the peaks and troughs) and the corresponding value at the troughs and peaks were calculated. The differences were averaged across the repetitions of MVC and termed as [DO2Hb] and [DHHb]. A sum of [DO2Hb] and [DHHb] was also calculated to reflect the changes in total hemoglobin ([DtHb]). The [DtHb] is considered as an indirect measure of changes in the local muscle blood flow (14). A percentage of the difference between [DtHb] at instants after the bouts of ECC compared with the value before ECCs was calculated for the 7 NIRS channels. A grand percentage was calculated as an average 6 SEM of the percentage difference of [DtHb]

at all the channels. Maps of local muscle blood flow for the TA muscle were generated using the percentage difference of [DtHb] over the 7 channels. The interpolation was performed using an inverse distance weighted interpolation to obtain an image of the [DtHb] distribution map (3). Surface Electromyography. Surface EMG was collected from the TA muscle using a bipolar surface electrode configuration (Neuroline 72001k; Ambu A/S, Ballerup, Denmark). The electrodes were placed on the muscle belly along the direction of the muscle fibers (interelectrodes distance: 2 cm). A single EMG channel was recorded as similar level of activity are reported in proximal and distal muscle portion of TA (7). The reference electrode was placed on the head of the tibia. Surface EMG was amplified (between 500 and 2000 times), bandpass filtered (5–500 Hz), digitized (12 bits A/D converter), and sampled at 2 kHz. For each session of isometric VOLUME 29 | NUMBER 4 | APRIL 2015 |

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Repeated Bout Effect, Local Muscle Blood Flow and EMG Activity MVC, RMS values were estimated over 250-millisecond epochs moving in steps of 100 milliseconds. The calculated RMS values were averaged across all epochs. Similar to RMS values, MDF was estimated over 500-millisecond nonoverlapping epochs for each session of isometric MVC. The power spectrum for MDF estimation was computed using the Welch method by applying a 512 points Hanning window with 15% overlap between successive subepochs (40). Statistical Analyses

The normality of the entire data set was checked and confirmed by Shapiro-Wilk tests. Changes in average dependent variables, MVC force, mean RMS, mean MDF, [DtHb], pain/soreness scores, and pain area were compared using a linear mixed model (LMM) in SPSS (IBM SPSS Statistics version 19; IBM Corp., Armonk, NY, USA). Instants (before vs. immediately after vs. the day after), and sessions (ECC1 vs. ECC2 vs. control 1 vs. control 2) were introduced as within-subject factors of the LMM. An additional within-subject factor of channel (channels 1–7) was also added for [DtHb] recordings. To account for repeated measurements of the experiment, a repeated factor associated with the instants, sessions, and channels was added to the model. In control sessions, instead of 3 instants we had 2 instants (before vs. day after), but LMM is capable of handling such unbalanced data sets (41). Bonferroni correction for multiple comparisons was used for post hoc test. The outcome measures in the control part of the experiment were analyzed for between-day reliability using relative (intraclass correlation coefficient [ICC]) and absolute estimates (SEM, minimum detectable change [MDC]). The measurements of the control sessions over 2 consecutive days (between days), and 2 days with 7 days in-between (between weeks) from the same 16 subjects were used for ICC, SEM, and MDC assessments. SEM was calculated using the following formula (Table 1): pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi SD3ð 12ICCÞ where SD is the grand SD of the scores across all subjects (39). SEM is an indication of expected measurement error in a single individual’s score. Minimum detectable change was calculated at the 95% level using the

pffiffiffi formula: SEM 3 231:96 (39). SEM and MDC were reported using the same units as the mean values of the [DtHb], MVC, EMG RMS, and EMG MDF. In all tests, p # 0.05 was considered statistically significant. Mean (SD) are reported. A grand average of [DtHb] was measured by making an average of [DtHb] over 7 channels. A linear regression (Pearson correlation coefficient) was used to test the correlation between grand [DtHb] and MVC force or mean RMS or mean MDF.

RESULTS The between-day and between-week ICC, SEM, and MDC are reported in Table 1. Isometric Strength

A statistically significant interaction between instant and session was detected for the isometric MVC force (p , 0.001; Table 2). Maximum voluntary contraction force decreased significantly immediately after both ECC1 and ECC2 (p , 0.001 and ,0.01, respectively). The MVC force was significantly decreased the day after ECC1 (p , 0.001); however, it did not change significantly the day after ECC2. The isometric MVC force level immediately and the day after ECC2 was significantly higher compared with the same time points after ECC1 (p , 0.001 and ,0.01, respectively). Soreness Intensity and Soreness Area

A statistically significant interaction between instant and session was detected for the soreness intensity (p , 0.001). In the ECC1 session, the soreness intensity increased immediately after the exercise (p , 0.001) and the day after ECC (p , 0.001) compared with before ECC. In the ECC2 session, however, there was no significant difference between the soreness at any instants (before vs. after vs. the day after). The soreness intensity was significantly lower after the ECC2 (both immediately and the day after ECC2) compared with immediately and the day after ECC1. In both sessions, there was no significant difference between the soreness area at different instants (Table 2 and Figure 4).

Figure 4. Distribution of pain/soreness area reported following the 2 bouts of ECC exercise of the TA muscle. TA = tibialis anterior.

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For the total hemoglobin concentration [DtHb], a statistically significant interaction between instant and session was detected (p , 0.001; Table 2 and Figure 2). There was no difference between [DtHb] at baseline measures before ECC1 and at control days. The [DtHb] was significantly lower before ECC2 compared with before ECC1 (p , 0.01). In both ECC sessions, [DtHb] significantly decreased immediately after ECC compared with before ECC (p # 0.05); and then it increased the day after ECC compared with immediately after ECC (p , 0.01). In the ECC1 session, the [DtHb] was still significantly decreased the day after ECC compared with before ECC (p , 0.001). However, there was no difference between the levels of [DtHb] before and the day after ECC2. The percentage difference of [DtHb] was significantly higher at immediately and the day after ECC1 than at immediately and the day after ECC2 (p , 0.001 and ,0.001, respectively; Figure 2). Near-infrared spectroscopy channel played a significant role on [DtHb] (p # 0.05). Generally higher [DtHb] was measured over the medial part of the TA (channels 3 and 6) compared with the lateral, proximal, and distal parts. However, this difference was consistent across all measurements (p # 0.05; Figure 2). Surface Electromyography

In both ECC sessions, there was no significant difference between the mean EMG RMS at any instant (before vs. after vs. the day after). Median power frequency was similar at baseline measurement before ECC1 and at control days. A statistically significant interaction between instant and session was detected for MDF (p # 0.05). Median power frequency decreased significantly at instants of ECC2 session compared with the same instants of ECC1 (p , 0.01; Table 2). Correlations

There was a positive correlation between MVC force and the grand [DtHb] during MVC (r = 0.59, p , 0.01); a negative correlation between EMG RMS and the grand [DtHb] during MVC (r = 20.21, p , 0.01); and finally a positive correlation between MDF and the grand [DtHb] during MVC (r = 0.23, p # 0.05).

DISCUSSION As hypothesized, the unaccustomed high-intensity ECC led to a significant decrease in [DtHb] at the day after ECC1, whereas repeating the same ECC did not. There was no difference between the MDF at control sessions and ECC1 session. Median power frequency was significantly lower at ECC2 session compared with ECC1. On the contrary, no changes were seen in RMS at any instants of the study. The data support the hypothesis that the local muscle blood flow and EMG spectral contents change with ECC experience. In other words, the local muscle blood flow and EMG spectral contents are altered after an unaccustomed ECC inducing muscle soreness. These alterations could provide a potential

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mechanism for a rapid adaptation that may decrease susceptibility of the muscle to develop further soreness in the subsequent ECC bout. Principally, the ECC protocol was successful at inducing muscle soreness to TA (Figure 4). A reduction of 40% in muscle strength is regarded as one of the most valid and reliable indicators of muscle damage in humans (38). The protocol used in the present study induced a decline of 75% in muscle strength (17). It has been shown that such ECC protocol can produce DOMS, and reduction in range of motion for several days after the exercise (17,30). Hubal et al. (18) demonstrated that using a similar number of ECC contractions, large differences in muscle strength deficits were seen between participants after ECC exercise. Therefore, it is likely that different degrees of muscle damage and DOMS between different participants is an important limitation across DOMS studies. This limitation can be diminished using a protocol similar to the present study. The relevance of NIRS measurements to monitor local muscle blood flow have been established previously (34); however, it should be noted that continuous wave NIRS using 2 wavelengths (850 and 760 nm) really does not reflect the absolute [DtHb] and it is just an indirect surrogate number that correlates with local muscle blood flow (13). The percentage difference of [DtHb] immediately after ECC2 and the subsequent day was significantly lower than observed at the same time points after ECC1 (Figure 2). This pattern resembles the RBE observed for outcome measures focusing on changes in pain sensitivity (pressure pain thresholds and nociceptive withdrawal reflex threshold [NWRT]) (17,19). Moreover, the [DtHb] before ECC2 was significantly lower than it was before ECC1, which could signal that ECC2 was performed while full recovery after ECC1 was not present. This is in line with the signs of central sensitization depicted by lower NWRT after ECC1 (17). Hosseinzadeh et al. (17) reported a decrease in NWRT after the strong stimulus induced by ECC1, whereas this was not observed after ECC2. The observed modulation of the NWRT indicates hyperexcitability of the spinal nociceptive pathways as a result of ECC1-induced muscle damage. This central facilitation in response to ECC1 provided an opportunity for rapid functional plasticity that allows to accommodate with ECC2 more efficiently, hence suggesting the importance of centrally mediated changes in relation to RBE (17). Furthermore, the lack of a significant decrease of [DtHb] the day after ECC2 may indicate that RBE can be detected by NIRS independent of full recovery after ECC1. Detection of RBE before full recovery substantiates further the role of neural adaptation mechanism in RBE (25,26). In agreement with previous studies, MDF during MVC was significantly lower after consecutive bout of ECC, whereas RMS was unchanged (4,37). In parallel, MVC force decreased at the day after initial bout of ECC, whereas it returned to baseline the day after ECC2 (17). This can explain the lack of changes in RMS giving credit to VOLUME 29 | NUMBER 4 | APRIL 2015 |

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Repeated Bout Effect, Local Muscle Blood Flow and EMG Activity a hypothesis suggesting an altered recruitment after ECC1 (4). Warren et al. (37) suggested that stable RMS amplitude after the initial and the consecutive ECCs reflects similar total neural activation between 2 ECCs. Chen (4) has suggested that the lower mean power frequency during ECC at 70% MVC reflects changes in muscle fiber activation pattern associated with RBE in biceps brachii muscle. The present study reproduced similar observations in TA during maximal isometric contraction and links the findings to the blood flow. Warren et al. (37) have suggested that the decrease in MDF can be due to a shift between the recruitment of faster motor unit to the activation of slower motor units. It should, however, be noted that the use of a single bipolar surface EMG channel does not enable the extraction of neural strategies identifying the physiological mechanisms responsible for the neural control of movement (10,11). Finally, 1 could suspect that the observed changes in MDF may be due to altered frequency modulation of the EMG activity through the conducting volume because of tissue swelling, etc. Hence, an increased attenuation of the high-frequency content of the EMG signals is realistic (as the result of DOMS). However, the attenuation of high-frequency content of the EMG signal would result in a decreased signal energy that should have been detected in the EMG RMS. Because we did not observe a significant change in EMG RMS, we believe that the observed changes in MDF cannot merely be explained by altered frequency response of the conducting volume. Changes in intramuscular pressure, local blood supply, and motor unit recruitment pattern will all have an impact on [DtHb] during exercise (31). The change in the [DtHb], MVC force, and MDF could reflect a selective damage of fast-twitch glycolytic fibers after doing unaccustomed ECC1 (22). This may lead to recruitment of fewer fast-twitch fibers compensated by additional slow-twitch fibers for the repeated bout (ECC2) (37). Slow-twitch fibers have a higher oxidative capacity potential that contributes to the tissue oxygenation during consecutive ECC bouts compared with the initial bout of ECC. Better maintenance of the oxidative energy metabolism during consecutive ECC bouts could result in less muscle damage. Another interesting observation in the present study was that ECC1 led to significant higher soreness compared with ECC2 (Figure 4 and Table 2). The pain distribution report before and after both bouts of ECCs can be addressed as evidence for attainment of TA muscle damage and soreness after ECC1 (Figure 4). A theoretical model of the relationship between muscle pain and central motor drive was proposed by Mastaglia (24). Under certain circumstances, contraction-induced pain during exercise may reduce the motor drive to the active muscles and thereby reduce the level of force production and the ability to sustain it. The significant decrease of the MVC at the day after initial bout of ECC in the existence of significant DOMS and moreover no DOMS at the day after ECC2 support this hypothesis

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(Table 2). Sadamoto et al. (1983) showed that blood flow to the biceps brachii muscle was completely impeded during sustained isometric contractions at 50% MVC, because of increased intramuscular pressure (32). The [DtHb] in our study was measured at 100% MVC. Although [DtHb] does not evaluate strictly the increase and decrease of blood volume, it gives an indication of the relative change in oxygen delivery and consumption by muscle blood volume (20). Thus, during a constant muscle work at 100% MVC, the changes in muscular force can impact [DtHb]. Therefore, in this condition, [DtHb] seems to be correlated with the changes in muscle force (see Results section regarding correlations) and a marker of muscle performance (the more force production the higher [DtHb]). Demura and Nakada (9) also reported such a relationship. Given the data related to the muscle soreness, MVC force, and [DtHb], one could infer that the increased soreness after ECC1 led to a decreased central motor drive resulting in a deficit in force production. Then, this decrease in force led to less [DtHb]. Finally, getting ECC experience and rapid potential adaptation to ECC1 mitigated the amounts of soreness in the subsequent ECC that can be seen as altered local muscle blood flow pattern and frequency contents of surface EMG after ECC2. Although the set level of exerted muscle force was the same across ECC bouts, the absolute intensity of 2 ECCs might have differed. As muscle cannot produce as high a force as the initial bout while it is not fully recovered, one might anticipate that the lower extent of DOMS after the second bout of ECC could be due to lower level of exerted muscle force. However, this kind of limitation is common among most of the studies investigating RBE (28,37). Furthermore, as explained in the above, choosing the same number of sets, repetition, and the same intensity of ECC aimed at minimizing this effect.

PRACTICAL APPLICATIONS The local muscle blood flow and spectral contents of surface EMG changed following the first bout of ECC in line with our hypothesis. These changes were accompanied with signs of reduced muscle damage during the subsequent bout of ECC. The present study reproduced similar EMG activity findings but in the TA muscle and during maximal isometric contraction bridging these findings to changes in the local muscle blood flow. The relationship between the concomitant altered pattern of local muscle blood flow and frequency contents of surface EMG accompanied by the change in soreness after the unaccustomed ECC can be interpreted as a central adaptation mechanism to compensate for the peripheral changes in muscle capacity. The present study showed that preconditioning exercises consisting of high-intensity ECCs can produce protection against developing more muscle damage during subsequent bout of ECC. Therefore, clinicians, coaches, and strength and conditioning professionals are advised to emphasize preseason conditioning involving sports-specific movement

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Journal of Strength and Conditioning Research drills of ECC to induce the protective and potentially analgesic effect of ECC. Further studies on RBE targeting other body regions are necessary to investigate the underpinning mechanisms of the protective effect.

ACKNOWLEDGMENTS The authors thank Mahdieh Hosseinzadeh for assistance with preparation of the Figure 3. The results of the present study do not constitute endorsement of the product by the authors or the National Strength and Conditioning Association. No funding was received for this work from any of the following organizations: National Institutes of Health (NIH), Wellcome Trust, Howard Hughes Medical Institute (HHMI), and other(s). The authors declare that they have no conflict of interest.

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Adaptation of local muscle blood flow and surface electromyography to repeated bouts of eccentric exercise.

The aim of this randomized controlled crossover study was to investigate the effect of a bout of unaccustomed eccentric exercise (ECC) followed by a c...
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