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ARTICLE Twitch mechanical properties after repeated eccentric exercise of the elbow flexors Damian Janecki, Anna Jaskólska, Jarosław Marusiak, Renata Andrzejewska, and Artur Jaskólski
Abstract: The purpose of this study was to assess if the protective adaptation after eccentric exercise affects changes of twitch contractile properties of the biceps brachii muscle. Maximal isometric torque (MVC), twitch contractile properties, muscle soreness, and relaxed elbow angle (RANG) assessments were measured in 12 untrained, right-handed male volunteers (age, 23 ± 2 years; height, 182 ± 5 cm; mass, 75 ± 7 kg) before, immediately after, 48 h, and 120 h following each bout of eccentric exercise that consisted of 30 repetitions of lowering a dumbbell adjusted to 75% of each individual’s maximal isometric torque of the right elbow flexors. MVC, peak twitch torque, maximal rate of twitch torque development, maximal rate of relaxation, muscle soreness, and RANG changes were significantly attenuated after the second bout of eccentric exercise when compared with the first bout. In contrast, time to twitch peak torque and half relaxation time did not change significantly after both the first and the second bout. The findings indicate that the mechanisms responsible for rapid adaptation affect some twitch mechanical properties such as peak torque, maximal rate of torque development, and maximal rate of relaxation but not time to peak torque and half relaxation time. Key words: repeated bout effect, lengthening contraction, contractile properties, electrical stimulation. Résumé : Dans cette étude on évalue si l’adaptation a` caractère protecteur après un exercice pliométrique exerce une influence sur la modification des propriétés contractiles de la secousse du muscle biceps brachial. On mesure le moment de force isométrique maximale (« MVC »), les propriétés contractiles de la secousse, la douleur musculaire et l’angle du coude relâché (« RANG ») chez douze volontaires masculins droitiers et non entraînés (23 ± 2 ans, 182 ± 5 cm, 75 ± 7 kg), et ce, avant, immédiatement après, puis 48 h et 120 h après chaque série d’exercices pliométriques consistant en 30 répétitions de l’abaissement d’un haltère dont la charge équivaut a` 75 % du moment de force isométrique maximale des fléchisseurs du coude droit du volontaire. À la suite de la deuxième série d’exercices pliométriques, on observe une diminution significative du MVC, du moment de force de pointe de la secousse, du taux de développement maximal de la secousse, du taux maximal de relaxation, de la douleur musculaire et du RANG comparativement a` la première série. Par contre, on n’observe pas de modifications significatives du moment de pointe de la secousse et du temps de demi-relaxation après la première et la seconde série. D’après ces observations, les mécanismes a` la base de l’adaptation rapide exercent une influence sur quelques propriétés mécaniques de la secousse (moment de force de pointe, taux de développement maximal de la secousse, taux maximal de relaxation), mais pas sur le temps de développement du moment de force de pointe et le temps de demi-relaxation. [Traduit par la Rédaction] Mots-clés : effet de répétition, contraction avec étirement, propriétés contractiles, stimulation électrique.
Introduction Unaccustomed eccentric exercise (ECC), which involves the active lengthening of muscle during tasks such as walking downhill, results in muscle damage that can produce long-lasting effects on muscle function. In particular, the consequences of this muscle damage include a decline in maximum force generated by the muscle, delayed onset muscle soreness development (DOMS), and the decrease in relaxed elbow angle (RANG) (Chen et al. 2007; Clarkson et al. 1992; Janecki et al. 2011; Jaskólski et al. 2007; Starbuck and Eston 2012). If the same eccentric exercise (or eccentrically biased task) is repeated again after recovery, the symptoms of previously occurred damage are markedly reduced (e.g., significantly faster recovery of muscle strength and RANG, and smaller development of muscle soreness) in what is described as the repeated bout effect and the mechanisms responsible for this phenomenon are divided into 3 main theories: cellular, mechanical, and neural (McHugh 2003).
Twitch mechanical response obtained after electrical stimulation could be used to assess muscle function without direct involvement of the central nervous system and therefore can be a useful method for estimation a contribution of peripheral contractile properties related to muscle force drop because of eccentric exercise and provides information about peripheral mechanisms associated with the repeated bout effect. Electrical stimulation has been used to examine various aspects of muscle function; e.g., changes associated with fatigue (Smith and Newham 2007), length-tension relation after exercise induced muscle damage (Prasartwuth et al. 2006), the effects of ECC training (Michaut et al. 2004; Pensini et al. 2002), and muscle immobilization (Duchateau and Hainaut 1987; Sayers et al. 2003). Kamandulis et al. (2010) have used electrical stimulation to evoke superimposed twitch and tetanic contraction after 2 separate bouts of eccentric exercise in quadriceps femoris muscle and concluded that repeated bout effect is not associated with changes in voluntary activation and depends mainly on peripheral adaptation. In this study we examined resting twitch contractile properties of
Received 7 March 2013. Accepted 29 June 2013. D. Janecki, A. Jaskólska, J. Marusiak, R. Andrzejewska, and A. Jaskólski. Department of Kinesiology, Faculty of Physiotherapy, University School of Physical Education, Wroclaw 51-612, Poland. Corresponding author: Damian Janecki (e-mail: [email protected]). Appl. Physiol. Nutr. Metab. 39: 74–81 (2014) dx.doi.org/10.1139/apnm-2013-0097
Published at www.nrcresearchpress.com/apnm on 16 July 2013.
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the biceps brachii muscle after the first and the second bout of ECC separated by 2–3 weeks hiatus to assess specific changes associated with the protective adaptation process. It has been reported that immediate decreases in contractile properties after a bout of ECC occur and it could be ascribed to physiological fatigue (Sahlin and Ren 1989). The papers of Sayers et al. (2003) and Prasartwuth et al. (2005, 2006) reported that twitch torque decrease may occur longer than 1 week after ECC (9 and 8 days, respectively). That could be explained by prolonged excitation–contraction system impairment and structural myofibrils disruption (Proske and Morgan 2001). Previous studies, which incorporated twitch recordings after ECC, evaluated changes in contractile properties only after a single bout of ECC 5 and when the second bout was performed after eccentric training period (Michaut et al. 2004; Pensini et al. 2002). However, there is no such study on repeated bout effect that we believe reflects one of the most fundamental skeletal muscle adaptations. Thus the better understanding of this phenomenon is of practical importance for sport medicine and human movement science. Therefore, the first aim of this study was to check if the rapid adaptation that develops after ECC affects twitch properties such as peak torque, maximal rate of torque development, contraction time, maximal rate of relaxation, and half relaxation time. The second aim was to compare which of them better represents peripheral mechanisms related to changes in muscle force production after eccentric contractions. We hypothesized that changes in twitch contractile properties that occur after the first bout of ECC would be attenuated after the second bout as a result of repeated bout effect.
Materials and methods Subjects Twenty untrained, right-handed male volunteers (age, 24 ± 3 years; height, 181 ± 7 cm; body mass, 77 ± 7 kg) that gave their written consent prior to the study, which was approved by the ethics committee of the University School of Physical Education (Wroclaw, Poland) and complied with the Helsinki Declaration, took part in this investigation. Some of the subjects were familiarized with resistance training but did not perform any resistance exercise at least for 6 months before this study. The participants did not have any neuromuscular disorders and were free from any injuries of the upper limbs. All subjects were instructed to keep their normal diet and not to take any anti-inflammatory drugs as they could have some influence on mechanisms of recovery associated with repeated bout effect (Depner et al. 2010; Shimomura et al. 2010). Experimental overview A within-group repeated measures design was used to determine changes in twitch contractile properties after 2 bouts of eccentric exercise separated by 2–3 weeks. Maximal isometric torque (MVC), twitch contractile properties, muscle soreness, and RANG assessments were collected before, immediately after, 48 h, and 120 h following each bout of eccentric exercise. The sequence of measurements was always in the same order: RANG assessment, muscle soreness evaluation, twitch properties, and MVC tasks. This order was chosen to avoid the potential influence of maximal torque development on subsequent measurements (e.g., MVC effect on twitch potentiation) (Vandervoort et al. 1983). Maximal isometric torque The maximal isometric torque of the elbow flexors of the right arm at 90° elbow joint angle was measured with the BIODYNA dynamometer (designed and built by Warsaw Technical University in Poland (Ke˛dzior et al. 1987)). The device consists of a chair with seat belts for stabilization, a column, and moveable arm with wrist handle. The wrist handle has the high sensitivity force transducer (SML-200; Interface, Scottsdale, Ariz., USA) inbuilt on 1 side
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and movable plate for the wrist stabilization from the other side (Fig. 1). The adjustable wrist handle allows setting the lever arm individually to ensure that during maximal voluntary contraction measurements, force is exerted by the subject’s wrist against the force transducer at the level of styloid processes of the radius and ulna. The wrist handle placement on the lever arm was recorded before the first measure and used as the site for the wrist handle setting on each subsequent measurement. The torque applied at the elbow was calculated by multiplying the measured force by the perpendicular distance between force transducer and the center of rotation of the elbow. Before the study began, the MSL-200 force transducer was calibrated on 2 different lever arms of the dynamometer using weights of known mass (0.5, 1, 2, 5, and 10 kg) and the calibration was linear within the tested range. An angle was measured with a precision potentiometer connected to the lever arm of the dynamometer. Tests were conducted with the participants seated with their back supported and their shoulders and torso were stabilized by the seatbelts. The right arm was positioned perpendicular to the trunk in the long axis of the shoulder. The arm and forearm were flexed at 90° of the elbow joint and held in a horizontal plane with the forearm in a supinated position. The forearm was held immobile between the force transducer and the stabilizing plate within the wrist handle. The rotation axis of the elbow joint was always at the rotation axis of the equipment. Participants were instructed to exert the maximal elbow flexion as fast and hard as possible when a sound signal was emitted by a computer and to release (relax) the force as fast as they could at the second signal (3 s later) (Jaskólska et al. 2003). The peak force of each 3-s test was determined. Subjects developed the MVC 3 times with 120 s of rest between attempts. To ensure that the participants maximally activated their muscles, they had to achieve MVC within a 10% difference on 3 consecutive contractions. If the subject did not achieve the required force, the trial was disregarded and measure was repeated after 180 s. The mean force from 3 appropriate attempts was calculated as a representative score. The average value of the 3 trials was used for the MVC because the average value is more reproducible and reliable than the maximal value of a single trial (Heinonen et al. 1994). Twitch contractile properties Twitch responses were collected using the same force transducer used for MVC assessment. Electrical stimulations (0.1 ms, constant current; model S88K, Astro-Med Inc., Grass Instrument Division) were delivered to the motor point of the biceps brachii muscle by the surface gel pad cathode located at previously determined motor point between the anterior edge of the deltoid muscle and the elbow crease and a surface carbon rubber anode placed over the distal tendon of the biceps brachii muscle. In both occasions before ECC the motor point was located using the same procedure. Intensity of stimulation was set 10% above the level required to evoke a resting twitch of maximal amplitude. Stimulator intensity needed to obtain maximal twitch amplitude in some cases was different and the value of this parameter was established before each measurement session for each subject separately. A series of 3 single stimuli at 5-s intervals were delivered to the relaxed muscle before each MVC trial (a total of 9 stimuli were delivered) to avoid twitch potentiation by a previous maximal contraction (Vandervoort et al. 1983). The following parameters were recorded and averaged from 3 twitch traces (twitch with highest amplitude in each MVC trial was analyzed): peak twitch torque (TT; Nm), maximal rate of twitch torque development (RTD; Nm·s−1), time to peak torque (TPT; ms), maximal rate of relaxation (REL; Nm·s−1), and twitch half relaxation time (HRT; ms). Maximal RTD was extracted from 10 ms with the maximal slope of the moment-time curve of the ascending limb of trace; Published by NRC Research Press
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Fig. 1. Experimental setup for the BIODYNA system to measure elbow flexion torque.(A) Force transducer; (B) anode; (C) cathode.
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continuous line representing “no pain” at one end (0 mm) and “very painful” at the other (100 mm). The point where testing end of the probe was placed was marked by permanent, waterproof marker to ensure repeatability of the place where the measures on the muscle were done. Data for muscle soreness are presented in millimeters. RANG RANG was determined by handle goniometer. Measurements were done with the arm relaxed along the side of the body during standing. A permanent marker was used to identify the lateral middle point of the humerus, the lateral axis point of elbow joint, and the lateral middle point between radius and ulna for the goniometer placements. Data for RANG are presented in degrees. Statistics Data were analyzed using SPSS 14.0. Dependent variables (MVC, DOMS, RANG, TT, TPT, RTD, REL, HRT) were analyzed by 2-way ANOVA (2 bout × 4 time; 8 test sessions) for repeated measures with a Bonferroni post hoc procedure used to find a specific difference between bouts and measurement time. The test–retest reproducibility was estimated by coefficient of variation (CV). Measurements performed before each bout were taken to analysis for test vs. retest. CV was calculated from mean values of 3 repetitions obtained before each bout of ECC. A significance level was set at p < 0.05. All data are presented as means ± SD.
similarly REL was extracted from 10 ms with the maximal slope of the moment-time curve of the descending limb of trace. Eccentric exercise Subjects performed the first bout of eccentric exercise (ECC1) of the right elbow flexors using a dumbbell. The load was adjusted to ⬃75% of each individual’s MVC taken at an elbow angle of 90° (MVC ranged from 74 to 115 Nm and loads applied during exercise ranged from 15 to 22 kg). This level of load was chosen as it was the highest value that allowed finishing the protocol by most of the subjects. The task for the subjects was to lower the dumbbell from an elbow flexed (⬃50°) to the elbow fully extended position (⬃180°) in 5 s, keeping the velocity as constant as possible, by following the examiner’s counting “zero” for the beginning and “1, 2, 3, 4, and 5” for the movement. The researcher has given instructions to the subjects on how to perform exercise correctly but if necessary, additional corrections were given during exercise performance. After each eccentric action, the examiner removed the load, and the arm was returned to the start position. The movement was repeated every 45 s for 30 repetitions and this long interval was chosen to minimize the effect of fatigue. The cadence and exercise velocity were controlled using metronome and stopwatch. All participants performed the second bout of eccentric exercise (ECC2) with the same arm using the same dumbbell 2– 3 weeks after the first bout, because we were waiting until MVC returned at least to 90% of the pre-ECC value. The protocol for ECC2 was identical to that of ECC1 and performed under examiner’s supervising. Pain assessment DOMS was evaluated in the same position as MVC assessment before strength measurements were performed. The device used to assess pain consists of a probe with pressure transducer (to obtain the pressure in the range from 0.25–2 kg) and a handle. Investigator grasped the handle and put the testing end of the probe on the central part of the biceps brachii muscle and pressed until the pressure of 2 kg was achieved. The maximal value of pressure was chosen to ensure the exposure of even minimal pain sensation that could occur after ECC. After that the investigator released the device and the subjects were asked to indicate the level of soreness on a visual analog scale consisting of 100 mm
Results Two-factorial ANOVA for repeated measures showed a significant (p < 0.05) effect for measurement time, bout, and the interaction of both for MVC, DOMS, RANG, TT, TPT, and RTD. Only TPT and HRT did not change significantly. Specific differences between time and (or) bouts were revealed by Bonferroni post hoc procedure. Figure 2 provides data for MVC changes after repeated eccentric exercise. There was a significant decrease (p < 0.05) in MVC immediately after and 48 h after ECC1 (MVC reduced from 85 ± 12 to 61 ± 14 and 58 ± 15 Nm, respectively; mean ± SD; p < 0.05). The second bout of eccentric exercise caused a significant decrease in MVC immediately after ECC only (from 81 ± 14 to 60 ± 16 Nm, respectively; mean ± SD; p < 0.05). Moreover the magnitude of the decrease of the MVC in measurement performed at 48 and 120 h after ECC2 was significantly smaller when compared with respective time points after ECC1. There was no significant difference (p > 0.05) between mean MVC values for test–retest reproducibility, and CV was 18% before ECC1 vs. 23% before ECC2. Figure 3 provides data for muscle soreness developed after each exercise bout. Subjective pain sensation increased significantly (p < 0.05) in all measurements after ECC1. The second bout resulted in significantly reduced pain perception in muscle soreness compared with the first bout at 48 and 120 h after ECC2 (p < 0.05). There was no significant difference (p > 0.05) between mean muscle soreness values for test–retest reproducibility, and CV was 119% before ECC1 vs. 144% before ECC2. Figure 4 provides data for RANG changes after repeated eccentric exercise Resting elbow angle decreased from 152 ± 4° before ECC to 137 ± 6°, 137 ± 5°, 144 ± 7° (immediately after, 48 h, and 120 h after exercise, respectively; mean ± SD; p < 0.05). The second bout of eccentric exercise decreased RANG immediately after exercise only (from 152 ± 3° to 143 ± 4°). There was no significant difference (p > 0.05) between mean values for test–retest reproducibility, and CV for RANG was 3% before ECC1 vs. 2% before ECC2. The ECC1 reduced peak twitch torque from 21.3 ± 4.1 to 12.5 ± 3.1 Nm, 13.7 ± 4.2 Nm, 15.8 ± 4.2 Nm (before, immediately after, 48 h and 120 h after eccentric exercise, respectively; mean ± SD; p < 0.05). The ECC2 caused a significant decrease in TT immediately after exercise only (from 19.9 ± 3.5 to 12.7 ± 2.9 Nm; mean ± SD; p < 0.05). Moreover, the values of TT performed 48 and 120 h Published by NRC Research Press
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Fig. 2. Changes in maximal isometric torque of the elbow flexors muscles before (pre), immediately after (post), and 48–120 h following the first bout of eccentric exercise and the second bout of eccentric exercise 2–3 weeks later. *, Significant (p < 0.05) difference compared with pre; †, significant (p < 0.05) difference compared with the first bout. ECC1 and ECC2, first and second bouts of eccentric exercise, respectively; h, hours after exercise; MVC, maximal isometric torque. Data are presented as means ± SD.
Fig. 3. Changes in soreness of the biceps brachii muscle before (pre), immediately after (post), and 48–120 h following the first bout of eccentric exercise and the second bout of eccentric exercise 2–3 weeks later. *, Significant (p < 0.05) difference compared with pre; †, significant (p < 0.05) difference compared with the first bout. DOMS, delayed onset muscle soreness development; ECC1 and ECC2, first and second bouts of eccentric exercise, respectively; h, hours after exercise. Data are presented as means and ± SD.
after ECC2 were significantly higher (p < 0.05) when compared with respective time points after ECC1 (Fig. 5). There was no significant difference (p > 0.05) between TT mean values for test– retest reproducibility, and CV was 31% before ECC1 vs. 29% before ECC2. The maximal rate of twitch torque development decreased after ECC1 from 388 ± 97 to 221 ± 57 Nm·s−1 immediately after eccentric exercise and remained significantly lower (p < 0.05) up to 120 h (295 ± 94 Nm·s−1; Fig. 6). The value of RTD after ECC2 decreased
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Fig. 4. Changes in elbow angle before (pre), immediately after (post), and 48–120 h following the first bout of eccentric exercise and the second bout of eccentric exercise 2–3 weeks later. ECC1 and ECC2, first and second bouts of eccentric exercise, respectively; h, hours after exercise; RANG, relaxed elbow angle. *, Significant (p < 0.05) difference compared with pre. Data are presented as means ± SD.
Fig. 5. Changes in twitch torque before (pre), immediately after (post), and 48–120 h following the first bout of eccentric exercise and the second bout of eccentric exercise 2–3 weeks later. *, Significant (p < 0.05) difference compared with pre; †, significant (p < 0.05) difference compared with the first bout. ECC1 and ECC2, first and second bouts of eccentric exercise, respectively; h, hours after exercise; TT, peak twitch torque. Data are presented as means ± SD.
significantly immediately after exercise only (from 371 ± 92 to 252 ± 58 Nm·s−1). Moreover decrease in RTD at 48 and 120 h after ECC2 was smaller when compared with ECC1 (Fig. 6). There was no significant difference (p > 0.05) between RTD mean values for test–retest reproducibility, and CV was 30% before ECC1 vs. 32% before ECC2. Figure 7 provides a graphic description for time to twitch peak torque after 2 bouts of eccentric exercise. There were no significant differences (p > 0.05) in TPT after each bout of ECC. There was no significant difference (p > 0.05) between TPT mean values for Published by NRC Research Press
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Fig. 6. Changes in maximal rate of twitch torque development before (pre), immediately after (post), and 48–120 h following the first bout of eccentric exercise and the second bout of eccentric exercise 2–3 weeks later. *, Significant (p < 0.05) difference compared with pre; †, significant (p < 0.05) difference compared with the first bout. ECC1 and ECC2, first and second bouts of eccentric exercise, respectively; h, hours after exercise; RTD, maximal rate of twitch torque development. Data are presented as means ± SD.
Fig. 7. Changes in time to twitch peak torque before (pre), immediately after (post), and 48–120 h following the first bout of eccentric exercise and the second bout of eccentric exercise 2–3 weeks later. There were no significant (p > 0.05) differences between both measurement time and exercise bouts. ECC1 and ECC2, first and second bouts of eccentric exercise, respectively; h, hours after exercise; TPT, time to peak torque. Data are presented as means ± SD.
test–retest reproducibility, and CV was 8.9% before ECC1 vs. 8.6% before ECC2. Maximal rate of twitch relaxation decreased after ECC1 from 150 ± 36 to 90 ± 28 Nm·s−1 immediately after eccentric exercise and remained significantly lower (p < 0.05) up to 120 h after ECC (Fig. 8). The value of REL after ECC2 decreased significantly only immediately after exercise (from 142 ± 23 to 86 ± 23 Nm·s−1) Moreover, decrease in REL at 48 and 120 h after ECC2 was smaller when
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Fig. 8. Changes in maximal rate of twitch relaxation before (pre), immediately after (post), and 48–120 h following the first bout of eccentric exercise and the second bout of eccentric exercise 2–3 weeks later. *, Significant (p < 0.05) difference compared with pre; †, significant (p < 0.05) difference compared with the first bout. ECC1 and ECC2, first and second bouts of eccentric exercise, respectively; h, hours after exercise; REL, maximal rate of relaxation. Data are presented as means ± SD.
compared with ECC1 (Fig. 8). There was no significant difference (p > 0.05) between REL mean values for test–retest reproducibility, and CV was 30% before ECC1 vs. 32% before ECC2. Figure 9 presents data for twitch half relaxation time after 2 bouts of eccentric exercise. There were no significant differences (p > 0.05) in HRT after each bout of ECC. There was no significant difference (p > 0.05) between HRT mean values for test–retest reproducibility, and CV was 19% before ECC1 vs. 21% before ECC2.
Discussion The ECC1 protocol that we used was appropriate to induce a rapid adaptation mechanism. Faster MVC recovery, smaller changes in RANG, and significantly reduced muscle soreness after ECC2 demonstrate evidence of the repeated bout effect. The first bout of eccentric exercise reduced MVC immediately after ECC with further decrement 48 h later. Muscle strength loss observed immediately after the exercise could be attributed to metabolic fatigue (Sahlin and Ren 1989; Smith and Newham 2007) and to decrease in voluntary activation process (Kamandulis et al. 2010; Prasartwuth et al. 2005). Prolonged impairment of force generating capacity could be due to both neural process and contractile apparatus failure. Based on the twitch interpolation technique Prasartwuth et al. (2005, 2006) concluded that voluntary activation impairment after eccentric exercise of the elbow flexors occurs during the first 24 h after exercise bout. However, prolonged force deficit is mainly attributed to mechanical myofibrills disruption accompanied by impairment of the excitation–contraction coupling system, which occurs several days after ECC (Ingalls et al. 1998; Proske and Morgan 2001). Initial injury leads to local inflammatory response, which is, at least in part, responsible for development of delayed onset muscle soreness (Smith 1991). Our results of significant and prolonged RANG decrease are consistent with other studies that have used it as indirect marker of exerciseinduced muscle damage (Chen et al. 2007; Starbuck and Eston 2012). It has been hypothesized that some fibers affected by ECC may develop an injury contracture because of uncontrolled sarcoplasmic calcium increase resulting from damage of the sarcoreticular membrane (Whitehead et al. 2001). These changes may be responsible for the increase in muscle passive stiffness, which in turn could be reflected by RANG decrease observed in our study. Published by NRC Research Press
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Fig. 9. Changes in twitch half relaxation time before (pre), immediately after (post), and 48–120 h following the first bout of eccentric exercise and the second bout of eccentric exercise 2–3 weeks later. There were no significant (p > 0.05) differences between both measurement time and exercise bouts. ECC1 and ECC2, first and second bouts of eccentric exercise, respectively; h, hours after exercise; HRT, twitch half relaxation time. Data are presented as means ± SD.
Faster MVC recovery, attenuated RANG decrease, and reduced soreness perception after ECC2 are consistent with previous studies, where the application of the 1 damaging bout of eccentric exercise conferred protection against the second bout and mechanisms of this phenomenon were described previously (Chan et al. 2012; Chen et al. 2007; Clarkson et al. 1992; Ebbeling and Clarkson 1989; Janecki et al. 2011). The new finding of this study is that the rapid adaptation that occurs after eccentric exercise is also related to some twitch contractile properties such as rate of torque development and peak torque but not to contraction time and half relaxation time changes. These results confirm the hypothesis that the repeated bout effect is evident for some contractile properties. This is the first report of changes in twitch contractile properties after 2 separate bouts of eccentric exercise. TT and RTD decreases were significantly smaller after ECC2 compared with ECC1. This was in line with our hypothesis. In contrast, TPT and HRT remained unchanged after either bout. Our protocol, consisting of 30 submaximal eccentric contractions, resulted in immediate and prolonged decreases in TT, which is in agreement with previous studies measuring this parameter (Prasartwuth et al. 2006; Smith 1991; Smith and Newham 2007). Those results could be due to mechanical sarcomeres disruption (Proske and Morgan 2001) and the damage to muscle membranes that leads to excitation–contraction coupling system impairment (Ingalls et al. 1998). Data obtained during stimulated contractions of the mouse muscle confirm that decrease of the peak sarcoplasmic calcium concentration occurs, which, at least in part, could be the reason for the inability to fully activate the contractile apparatus (Balnave and Allen 1995; Ingalls et al. 1998). Decrease in contractile capacity could be ascribed to changes in length–tension relation that occur after ECC (Jones et al. 1997; Prasartwuth et al. 2006). The rightward shift that occurs after ECC-induced damage could be explained by the “popping” sarcomere hypothesis (Proske and Morgan 2001) where during lengthening contraction some weak and unstable sarcomeres are overstretched beyond their myofilament overlap. This hypothesis has been supported by studies on animal and human
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muscles (Jones et al. 1997; Whitehead et al. 1998). The presence of overstretched or disrupted sarcomeres may increase the series compliance of the muscle, thus leading to the rightward shift in length–tension relation (Gregory et al. 2007). Although we measured TT at 90° only, the potential contribution of the abovementioned shift on force generation capacity decrease cannot be excluded. After ECC2, the values of TT decreased significantly only immediately after exercise and were significantly higher than respective values after ECC1. Faster twitch torque recovery after the second bout of eccentric exercise could be attributed to rapid adaptation mechanisms that occurs after the initial bout of eccentric exercise and is related to muscle repair and (or) rebuilt processes (Lapointe et al. 2002) such as removal of destroyed sarcomeres and cell membrane strengthening (Morgan and Allen 1999), increase in collagen synthesis (Lapier et al. 1995), existing myofibrils remodeling (Yu et al. 2003; Yu et al. 2004), and structural protein reorganization (Lehti et al. 2007). Those mechanisms may lead to a better muscle resistance to eccentric contractions; thus, the susceptibility of the muscle tissue to damage is smaller and therefore TT recovery is faster after ECC2 when compared with ECC1. Both ECC sessions resulted in significant reduction in RTD immediately after exercise. However, when comparing RTD changes at 48–120 h after both ECC1 and ECC2 it appeared that after the second bout it recovers significantly faster (p < 0.05). This could be related to the repeated bout effect. This hypothesis is supported by the lack of significant changes in RTD noted from 48 h after ECC2. The decreases in RTD in our study are in agreement with the previous findings that reported immediate (Michaut et al. 2004) and prolonged changes in this parameter after ECC (Sayers et al. 2003). RTD depends mainly on transient sarcoplasmic calcium increase (Wahr and Rall 1997) and fiber-type (myosin heavy chain (MHC) isoform) composition (Harridge et al. 1995). Eccentric exercise leads to various changes that affect previously mentioned factors. Among them are (i) failure in the excitation–contraction coupling system because of damage of the sarcoreticular membrane, which leads to an increase of the resting sarcoplasmic calcium concentration and thus leads to lower calcium release during muscle excitation (Ingalls et al. 1998); and (ii) myofibrills organization disruption that may impair the actino-myosin crossbridge function (Michaut et al. 2004). As the type II MHC isoforms have elevated cross-bridge cycle transition rate (Harridge et al. 1995), the predominance of this protein is an important intrinsic muscle factor determining RFD (Harridge et al. 1996). Nardone and Schieppati (1988) reported selective activation of fast motor units during eccentric contractions in humans. The results from a cat model experiment (Brockett et al. 2002) indicated that ECCinduced muscle damage occurs in type II fibers mainly (which have significant content of type II MHC isoforms). If the same occurs also in humans, their damage should affect strongly RTD. Gregory et al. (2007) hypothesized that the mentioned disruption of the sarcomeres could also lead to increase in muscle series compliance. In this situation it would need more time to fully take up of the extra compliance during twitch, which in turn could impair both TT and RTD. Similar to TT, changes in RTD were attenuated after the second bout of eccentric exercise and could be ascribed to an adaptation that leads to strengthening and (or) rebuilding of the muscle fibers especially susceptible to eccentric damage (Lapointe et al. 2002). Because those fibers are mainly type II (Brockett et al. 2002) their adaptation results in a faster RTD recovery that occurs after ECC2. There was a lack of differences in TPT after each bout of eccentric exercise. The results provided by Sayers et al. (2003) and Prasartwuth et al. (2005) revealed that significant decreases in TPT occur only immediately after ECC and recovery in this parameter is much faster than the other contractile properties. Initial decrease in TPT, reported by Sayers et al. (2003) and Prasartwuth et al. (2005), without prolonged changes suggest that mechanisms Published by NRC Research Press
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responsible for TPT are affected by physiological fatigue mainly and are less or not susceptible to ECC-induced muscle damage. The contrary results of changes immediately after ECC seen in our study could be explained by the different ECC protocol that we used. In the protocol of Prasartwuth et al. (2005) the subjects performed ECC until isometric maximal voluntary contraction dropped by 40%, which required 50 to 350 repetitions for most participants with 6 s of rest between repetitions in series that consisted of 50 repetitions with 30 s of rest between sets. In the study of Sayers et al. (2003) the subjects performed 2 sets of 25 maximal contractions with 5 min and 12 s of rest, respectively. In our protocol we applied 30 submaximal eccentric contractions with 45-s intervals between each repetition to minimize the effect of fatigue. Shorter rest periods between repetitions and a greater number of contractions could result in greater physiological fatigue changes observed in those studies, which in turn may be responsible for the decreases in TPT immediately after ECC when compared with our results. Another explanation for the lack of changes in this parameter may be because of decreases in twitch torque. Although RTD was lower, the decrease in twitch torque caused by that time to peak torque did not change significantly. Both ECC sessions resulted in significant reduction in REL immediately after exercise. However, when comparing REL changes at 48–120 h after both ECC1 and ECC2, it appeared that after the second bout it recovered significantly faster (p < 0.05). This could be related to the repeated bout effect. This hypothesis is supported by the lack of significant changes in REL noted from 48 h after ECC2. Wahr and al. (1998) suggested that the rate of relaxation depends on cross-bridge dissociation kinetics related to calcium reuptake rate by the sarcoplasmic reticulum and the speed of this process can be affected by fatigue (Green et al. 2011). The results of this study provide evidence that specific changes associated with prolonged disturbance of intracellural calcium homeostasis, which occur after ECC (Whitehead et al. 2001), may affect REL. Therefore, it seems that REL is sensitive to muscle damage after ECC. This hypothesis is supported by faster REL recovery after ECC2, indicating that this parameter reflects repeated bout effect (which is associated with a smaller muscle damage). There was a lack of differences in HRT both between time points after exercise and ECC bouts. Similarly as for TPT, Sayers et al. (2003) and Prasartwuth et al. (2005) revealed that significant decreases in HRT occur only during the first hours after ECC, which suggests that this parameter is affected mainly by physiological fatigue. Although REL and HRT are often used interchangeably (Michaut et al. 2004; Pensini et al. 2002; Prasartwuth et al. 2006; Sayers et al. 2003; Wahr et al. 1998), our data suggests that REL is more sensitive than HRT for specific changes that occur after ECC, which could be explained by a different effect of twitch torque decrease on those parameters. Since the maximal rate of relaxation was slower, the decrease in twitch torque resulted in a lack of changes in the net time of HRT. This novel result should be taken into account when analyzing these parameters in experiments incorporating eccentric exercise. In conclusion, the findings of the present study indicate that the repeated bout effect is evident for some twitch contractile properties such as the peak torque, the maximal rate of torque development, and the maximal rate of relaxation. These findings reflect peripheral adaptation mechanisms that at least in part have an effect on maximal isometric torque changes after eccentric exercise. However, specific muscle damage after ECC used in our protocol did not affect the time to twitch peak torque and the half relaxation time, which should be take into account in future studies on twitch contractile properties changes after eccentric exercise.
Appl. Physiol. Nutr. Metab. Vol. 39, 2014
Acknowledgements This work was supported by National Science Centre Grant DEC-2011/01/N/NZ7/00012.
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ARTICLE Twitch mechanical properties after repeated eccentric exercise of the elbow flexors Damian Janecki, Anna Jaskólska, Jarosław Marusiak, Renata Andrzejewska, and Artur Jaskólski
Abstract: The purpose of this study was to assess if the protective adaptation after eccentric exercise affects changes of twitch contractile properties of the biceps brachii muscle. Maximal isometric torque (MVC), twitch contractile properties, muscle soreness, and relaxed elbow angle (RANG) assessments were measured in 12 untrained, right-handed male volunteers (age, 23 ± 2 years; height, 182 ± 5 cm; mass, 75 ± 7 kg) before, immediately after, 48 h, and 120 h following each bout of eccentric exercise that consisted of 30 repetitions of lowering a dumbbell adjusted to 75% of each individual’s maximal isometric torque of the right elbow flexors. MVC, peak twitch torque, maximal rate of twitch torque development, maximal rate of relaxation, muscle soreness, and RANG changes were significantly attenuated after the second bout of eccentric exercise when compared with the first bout. In contrast, time to twitch peak torque and half relaxation time did not change significantly after both the first and the second bout. The findings indicate that the mechanisms responsible for rapid adaptation affect some twitch mechanical properties such as peak torque, maximal rate of torque development, and maximal rate of relaxation but not time to peak torque and half relaxation time. Key words: repeated bout effect, lengthening contraction, contractile properties, electrical stimulation. Résumé : Dans cette étude on évalue si l’adaptation a` caractère protecteur après un exercice pliométrique exerce une influence sur la modification des propriétés contractiles de la secousse du muscle biceps brachial. On mesure le moment de force isométrique maximale (« MVC »), les propriétés contractiles de la secousse, la douleur musculaire et l’angle du coude relâché (« RANG ») chez douze volontaires masculins droitiers et non entraînés (23 ± 2 ans, 182 ± 5 cm, 75 ± 7 kg), et ce, avant, immédiatement après, puis 48 h et 120 h après chaque série d’exercices pliométriques consistant en 30 répétitions de l’abaissement d’un haltère dont la charge équivaut a` 75 % du moment de force isométrique maximale des fléchisseurs du coude droit du volontaire. À la suite de la deuxième série d’exercices pliométriques, on observe une diminution significative du MVC, du moment de force de pointe de la secousse, du taux de développement maximal de la secousse, du taux maximal de relaxation, de la douleur musculaire et du RANG comparativement a` la première série. Par contre, on n’observe pas de modifications significatives du moment de pointe de la secousse et du temps de demi-relaxation après la première et la seconde série. D’après ces observations, les mécanismes a` la base de l’adaptation rapide exercent une influence sur quelques propriétés mécaniques de la secousse (moment de force de pointe, taux de développement maximal de la secousse, taux maximal de relaxation), mais pas sur le temps de développement du moment de force de pointe et le temps de demi-relaxation. [Traduit par la Rédaction] Mots-clés : effet de répétition, contraction avec étirement, propriétés contractiles, stimulation électrique.
Introduction Unaccustomed eccentric exercise (ECC), which involves the active lengthening of muscle during tasks such as walking downhill, results in muscle damage that can produce long-lasting effects on muscle function. In particular, the consequences of this muscle damage include a decline in maximum force generated by the muscle, delayed onset muscle soreness development (DOMS), and the decrease in relaxed elbow angle (RANG) (Chen et al. 2007; Clarkson et al. 1992; Janecki et al. 2011; Jaskólski et al. 2007; Starbuck and Eston 2012). If the same eccentric exercise (or eccentrically biased task) is repeated again after recovery, the symptoms of previously occurred damage are markedly reduced (e.g., significantly faster recovery of muscle strength and RANG, and smaller development of muscle soreness) in what is described as the repeated bout effect and the mechanisms responsible for this phenomenon are divided into 3 main theories: cellular, mechanical, and neural (McHugh 2003).
Twitch mechanical response obtained after electrical stimulation could be used to assess muscle function without direct involvement of the central nervous system and therefore can be a useful method for estimation a contribution of peripheral contractile properties related to muscle force drop because of eccentric exercise and provides information about peripheral mechanisms associated with the repeated bout effect. Electrical stimulation has been used to examine various aspects of muscle function; e.g., changes associated with fatigue (Smith and Newham 2007), length-tension relation after exercise induced muscle damage (Prasartwuth et al. 2006), the effects of ECC training (Michaut et al. 2004; Pensini et al. 2002), and muscle immobilization (Duchateau and Hainaut 1987; Sayers et al. 2003). Kamandulis et al. (2010) have used electrical stimulation to evoke superimposed twitch and tetanic contraction after 2 separate bouts of eccentric exercise in quadriceps femoris muscle and concluded that repeated bout effect is not associated with changes in voluntary activation and depends mainly on peripheral adaptation. In this study we examined resting twitch contractile properties of
Received 7 March 2013. Accepted 29 June 2013. D. Janecki, A. Jaskólska, J. Marusiak, R. Andrzejewska, and A. Jaskólski. Department of Kinesiology, Faculty of Physiotherapy, University School of Physical Education, Wroclaw 51-612, Poland. Corresponding author: Damian Janecki (e-mail: [email protected]). Appl. Physiol. Nutr. Metab. 39: 74–81 (2014) dx.doi.org/10.1139/apnm-2013-0097
Published at www.nrcresearchpress.com/apnm on 16 July 2013.
Janecki et al.
the biceps brachii muscle after the first and the second bout of ECC separated by 2–3 weeks hiatus to assess specific changes associated with the protective adaptation process. It has been reported that immediate decreases in contractile properties after a bout of ECC occur and it could be ascribed to physiological fatigue (Sahlin and Ren 1989). The papers of Sayers et al. (2003) and Prasartwuth et al. (2005, 2006) reported that twitch torque decrease may occur longer than 1 week after ECC (9 and 8 days, respectively). That could be explained by prolonged excitation–contraction system impairment and structural myofibrils disruption (Proske and Morgan 2001). Previous studies, which incorporated twitch recordings after ECC, evaluated changes in contractile properties only after a single bout of ECC 5 and when the second bout was performed after eccentric training period (Michaut et al. 2004; Pensini et al. 2002). However, there is no such study on repeated bout effect that we believe reflects one of the most fundamental skeletal muscle adaptations. Thus the better understanding of this phenomenon is of practical importance for sport medicine and human movement science. Therefore, the first aim of this study was to check if the rapid adaptation that develops after ECC affects twitch properties such as peak torque, maximal rate of torque development, contraction time, maximal rate of relaxation, and half relaxation time. The second aim was to compare which of them better represents peripheral mechanisms related to changes in muscle force production after eccentric contractions. We hypothesized that changes in twitch contractile properties that occur after the first bout of ECC would be attenuated after the second bout as a result of repeated bout effect.
Materials and methods Subjects Twenty untrained, right-handed male volunteers (age, 24 ± 3 years; height, 181 ± 7 cm; body mass, 77 ± 7 kg) that gave their written consent prior to the study, which was approved by the ethics committee of the University School of Physical Education (Wroclaw, Poland) and complied with the Helsinki Declaration, took part in this investigation. Some of the subjects were familiarized with resistance training but did not perform any resistance exercise at least for 6 months before this study. The participants did not have any neuromuscular disorders and were free from any injuries of the upper limbs. All subjects were instructed to keep their normal diet and not to take any anti-inflammatory drugs as they could have some influence on mechanisms of recovery associated with repeated bout effect (Depner et al. 2010; Shimomura et al. 2010). Experimental overview A within-group repeated measures design was used to determine changes in twitch contractile properties after 2 bouts of eccentric exercise separated by 2–3 weeks. Maximal isometric torque (MVC), twitch contractile properties, muscle soreness, and RANG assessments were collected before, immediately after, 48 h, and 120 h following each bout of eccentric exercise. The sequence of measurements was always in the same order: RANG assessment, muscle soreness evaluation, twitch properties, and MVC tasks. This order was chosen to avoid the potential influence of maximal torque development on subsequent measurements (e.g., MVC effect on twitch potentiation) (Vandervoort et al. 1983). Maximal isometric torque The maximal isometric torque of the elbow flexors of the right arm at 90° elbow joint angle was measured with the BIODYNA dynamometer (designed and built by Warsaw Technical University in Poland (Ke˛dzior et al. 1987)). The device consists of a chair with seat belts for stabilization, a column, and moveable arm with wrist handle. The wrist handle has the high sensitivity force transducer (SML-200; Interface, Scottsdale, Ariz., USA) inbuilt on 1 side
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and movable plate for the wrist stabilization from the other side (Fig. 1). The adjustable wrist handle allows setting the lever arm individually to ensure that during maximal voluntary contraction measurements, force is exerted by the subject’s wrist against the force transducer at the level of styloid processes of the radius and ulna. The wrist handle placement on the lever arm was recorded before the first measure and used as the site for the wrist handle setting on each subsequent measurement. The torque applied at the elbow was calculated by multiplying the measured force by the perpendicular distance between force transducer and the center of rotation of the elbow. Before the study began, the MSL-200 force transducer was calibrated on 2 different lever arms of the dynamometer using weights of known mass (0.5, 1, 2, 5, and 10 kg) and the calibration was linear within the tested range. An angle was measured with a precision potentiometer connected to the lever arm of the dynamometer. Tests were conducted with the participants seated with their back supported and their shoulders and torso were stabilized by the seatbelts. The right arm was positioned perpendicular to the trunk in the long axis of the shoulder. The arm and forearm were flexed at 90° of the elbow joint and held in a horizontal plane with the forearm in a supinated position. The forearm was held immobile between the force transducer and the stabilizing plate within the wrist handle. The rotation axis of the elbow joint was always at the rotation axis of the equipment. Participants were instructed to exert the maximal elbow flexion as fast and hard as possible when a sound signal was emitted by a computer and to release (relax) the force as fast as they could at the second signal (3 s later) (Jaskólska et al. 2003). The peak force of each 3-s test was determined. Subjects developed the MVC 3 times with 120 s of rest between attempts. To ensure that the participants maximally activated their muscles, they had to achieve MVC within a 10% difference on 3 consecutive contractions. If the subject did not achieve the required force, the trial was disregarded and measure was repeated after 180 s. The mean force from 3 appropriate attempts was calculated as a representative score. The average value of the 3 trials was used for the MVC because the average value is more reproducible and reliable than the maximal value of a single trial (Heinonen et al. 1994). Twitch contractile properties Twitch responses were collected using the same force transducer used for MVC assessment. Electrical stimulations (0.1 ms, constant current; model S88K, Astro-Med Inc., Grass Instrument Division) were delivered to the motor point of the biceps brachii muscle by the surface gel pad cathode located at previously determined motor point between the anterior edge of the deltoid muscle and the elbow crease and a surface carbon rubber anode placed over the distal tendon of the biceps brachii muscle. In both occasions before ECC the motor point was located using the same procedure. Intensity of stimulation was set 10% above the level required to evoke a resting twitch of maximal amplitude. Stimulator intensity needed to obtain maximal twitch amplitude in some cases was different and the value of this parameter was established before each measurement session for each subject separately. A series of 3 single stimuli at 5-s intervals were delivered to the relaxed muscle before each MVC trial (a total of 9 stimuli were delivered) to avoid twitch potentiation by a previous maximal contraction (Vandervoort et al. 1983). The following parameters were recorded and averaged from 3 twitch traces (twitch with highest amplitude in each MVC trial was analyzed): peak twitch torque (TT; Nm), maximal rate of twitch torque development (RTD; Nm·s−1), time to peak torque (TPT; ms), maximal rate of relaxation (REL; Nm·s−1), and twitch half relaxation time (HRT; ms). Maximal RTD was extracted from 10 ms with the maximal slope of the moment-time curve of the ascending limb of trace; Published by NRC Research Press
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Fig. 1. Experimental setup for the BIODYNA system to measure elbow flexion torque.(A) Force transducer; (B) anode; (C) cathode.
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continuous line representing “no pain” at one end (0 mm) and “very painful” at the other (100 mm). The point where testing end of the probe was placed was marked by permanent, waterproof marker to ensure repeatability of the place where the measures on the muscle were done. Data for muscle soreness are presented in millimeters. RANG RANG was determined by handle goniometer. Measurements were done with the arm relaxed along the side of the body during standing. A permanent marker was used to identify the lateral middle point of the humerus, the lateral axis point of elbow joint, and the lateral middle point between radius and ulna for the goniometer placements. Data for RANG are presented in degrees. Statistics Data were analyzed using SPSS 14.0. Dependent variables (MVC, DOMS, RANG, TT, TPT, RTD, REL, HRT) were analyzed by 2-way ANOVA (2 bout × 4 time; 8 test sessions) for repeated measures with a Bonferroni post hoc procedure used to find a specific difference between bouts and measurement time. The test–retest reproducibility was estimated by coefficient of variation (CV). Measurements performed before each bout were taken to analysis for test vs. retest. CV was calculated from mean values of 3 repetitions obtained before each bout of ECC. A significance level was set at p < 0.05. All data are presented as means ± SD.
similarly REL was extracted from 10 ms with the maximal slope of the moment-time curve of the descending limb of trace. Eccentric exercise Subjects performed the first bout of eccentric exercise (ECC1) of the right elbow flexors using a dumbbell. The load was adjusted to ⬃75% of each individual’s MVC taken at an elbow angle of 90° (MVC ranged from 74 to 115 Nm and loads applied during exercise ranged from 15 to 22 kg). This level of load was chosen as it was the highest value that allowed finishing the protocol by most of the subjects. The task for the subjects was to lower the dumbbell from an elbow flexed (⬃50°) to the elbow fully extended position (⬃180°) in 5 s, keeping the velocity as constant as possible, by following the examiner’s counting “zero” for the beginning and “1, 2, 3, 4, and 5” for the movement. The researcher has given instructions to the subjects on how to perform exercise correctly but if necessary, additional corrections were given during exercise performance. After each eccentric action, the examiner removed the load, and the arm was returned to the start position. The movement was repeated every 45 s for 30 repetitions and this long interval was chosen to minimize the effect of fatigue. The cadence and exercise velocity were controlled using metronome and stopwatch. All participants performed the second bout of eccentric exercise (ECC2) with the same arm using the same dumbbell 2– 3 weeks after the first bout, because we were waiting until MVC returned at least to 90% of the pre-ECC value. The protocol for ECC2 was identical to that of ECC1 and performed under examiner’s supervising. Pain assessment DOMS was evaluated in the same position as MVC assessment before strength measurements were performed. The device used to assess pain consists of a probe with pressure transducer (to obtain the pressure in the range from 0.25–2 kg) and a handle. Investigator grasped the handle and put the testing end of the probe on the central part of the biceps brachii muscle and pressed until the pressure of 2 kg was achieved. The maximal value of pressure was chosen to ensure the exposure of even minimal pain sensation that could occur after ECC. After that the investigator released the device and the subjects were asked to indicate the level of soreness on a visual analog scale consisting of 100 mm
Results Two-factorial ANOVA for repeated measures showed a significant (p < 0.05) effect for measurement time, bout, and the interaction of both for MVC, DOMS, RANG, TT, TPT, and RTD. Only TPT and HRT did not change significantly. Specific differences between time and (or) bouts were revealed by Bonferroni post hoc procedure. Figure 2 provides data for MVC changes after repeated eccentric exercise. There was a significant decrease (p < 0.05) in MVC immediately after and 48 h after ECC1 (MVC reduced from 85 ± 12 to 61 ± 14 and 58 ± 15 Nm, respectively; mean ± SD; p < 0.05). The second bout of eccentric exercise caused a significant decrease in MVC immediately after ECC only (from 81 ± 14 to 60 ± 16 Nm, respectively; mean ± SD; p < 0.05). Moreover the magnitude of the decrease of the MVC in measurement performed at 48 and 120 h after ECC2 was significantly smaller when compared with respective time points after ECC1. There was no significant difference (p > 0.05) between mean MVC values for test–retest reproducibility, and CV was 18% before ECC1 vs. 23% before ECC2. Figure 3 provides data for muscle soreness developed after each exercise bout. Subjective pain sensation increased significantly (p < 0.05) in all measurements after ECC1. The second bout resulted in significantly reduced pain perception in muscle soreness compared with the first bout at 48 and 120 h after ECC2 (p < 0.05). There was no significant difference (p > 0.05) between mean muscle soreness values for test–retest reproducibility, and CV was 119% before ECC1 vs. 144% before ECC2. Figure 4 provides data for RANG changes after repeated eccentric exercise Resting elbow angle decreased from 152 ± 4° before ECC to 137 ± 6°, 137 ± 5°, 144 ± 7° (immediately after, 48 h, and 120 h after exercise, respectively; mean ± SD; p < 0.05). The second bout of eccentric exercise decreased RANG immediately after exercise only (from 152 ± 3° to 143 ± 4°). There was no significant difference (p > 0.05) between mean values for test–retest reproducibility, and CV for RANG was 3% before ECC1 vs. 2% before ECC2. The ECC1 reduced peak twitch torque from 21.3 ± 4.1 to 12.5 ± 3.1 Nm, 13.7 ± 4.2 Nm, 15.8 ± 4.2 Nm (before, immediately after, 48 h and 120 h after eccentric exercise, respectively; mean ± SD; p < 0.05). The ECC2 caused a significant decrease in TT immediately after exercise only (from 19.9 ± 3.5 to 12.7 ± 2.9 Nm; mean ± SD; p < 0.05). Moreover, the values of TT performed 48 and 120 h Published by NRC Research Press
Janecki et al.
Fig. 2. Changes in maximal isometric torque of the elbow flexors muscles before (pre), immediately after (post), and 48–120 h following the first bout of eccentric exercise and the second bout of eccentric exercise 2–3 weeks later. *, Significant (p < 0.05) difference compared with pre; †, significant (p < 0.05) difference compared with the first bout. ECC1 and ECC2, first and second bouts of eccentric exercise, respectively; h, hours after exercise; MVC, maximal isometric torque. Data are presented as means ± SD.
Fig. 3. Changes in soreness of the biceps brachii muscle before (pre), immediately after (post), and 48–120 h following the first bout of eccentric exercise and the second bout of eccentric exercise 2–3 weeks later. *, Significant (p < 0.05) difference compared with pre; †, significant (p < 0.05) difference compared with the first bout. DOMS, delayed onset muscle soreness development; ECC1 and ECC2, first and second bouts of eccentric exercise, respectively; h, hours after exercise. Data are presented as means and ± SD.
after ECC2 were significantly higher (p < 0.05) when compared with respective time points after ECC1 (Fig. 5). There was no significant difference (p > 0.05) between TT mean values for test– retest reproducibility, and CV was 31% before ECC1 vs. 29% before ECC2. The maximal rate of twitch torque development decreased after ECC1 from 388 ± 97 to 221 ± 57 Nm·s−1 immediately after eccentric exercise and remained significantly lower (p < 0.05) up to 120 h (295 ± 94 Nm·s−1; Fig. 6). The value of RTD after ECC2 decreased
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Fig. 4. Changes in elbow angle before (pre), immediately after (post), and 48–120 h following the first bout of eccentric exercise and the second bout of eccentric exercise 2–3 weeks later. ECC1 and ECC2, first and second bouts of eccentric exercise, respectively; h, hours after exercise; RANG, relaxed elbow angle. *, Significant (p < 0.05) difference compared with pre. Data are presented as means ± SD.
Fig. 5. Changes in twitch torque before (pre), immediately after (post), and 48–120 h following the first bout of eccentric exercise and the second bout of eccentric exercise 2–3 weeks later. *, Significant (p < 0.05) difference compared with pre; †, significant (p < 0.05) difference compared with the first bout. ECC1 and ECC2, first and second bouts of eccentric exercise, respectively; h, hours after exercise; TT, peak twitch torque. Data are presented as means ± SD.
significantly immediately after exercise only (from 371 ± 92 to 252 ± 58 Nm·s−1). Moreover decrease in RTD at 48 and 120 h after ECC2 was smaller when compared with ECC1 (Fig. 6). There was no significant difference (p > 0.05) between RTD mean values for test–retest reproducibility, and CV was 30% before ECC1 vs. 32% before ECC2. Figure 7 provides a graphic description for time to twitch peak torque after 2 bouts of eccentric exercise. There were no significant differences (p > 0.05) in TPT after each bout of ECC. There was no significant difference (p > 0.05) between TPT mean values for Published by NRC Research Press
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Fig. 6. Changes in maximal rate of twitch torque development before (pre), immediately after (post), and 48–120 h following the first bout of eccentric exercise and the second bout of eccentric exercise 2–3 weeks later. *, Significant (p < 0.05) difference compared with pre; †, significant (p < 0.05) difference compared with the first bout. ECC1 and ECC2, first and second bouts of eccentric exercise, respectively; h, hours after exercise; RTD, maximal rate of twitch torque development. Data are presented as means ± SD.
Fig. 7. Changes in time to twitch peak torque before (pre), immediately after (post), and 48–120 h following the first bout of eccentric exercise and the second bout of eccentric exercise 2–3 weeks later. There were no significant (p > 0.05) differences between both measurement time and exercise bouts. ECC1 and ECC2, first and second bouts of eccentric exercise, respectively; h, hours after exercise; TPT, time to peak torque. Data are presented as means ± SD.
test–retest reproducibility, and CV was 8.9% before ECC1 vs. 8.6% before ECC2. Maximal rate of twitch relaxation decreased after ECC1 from 150 ± 36 to 90 ± 28 Nm·s−1 immediately after eccentric exercise and remained significantly lower (p < 0.05) up to 120 h after ECC (Fig. 8). The value of REL after ECC2 decreased significantly only immediately after exercise (from 142 ± 23 to 86 ± 23 Nm·s−1) Moreover, decrease in REL at 48 and 120 h after ECC2 was smaller when
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Fig. 8. Changes in maximal rate of twitch relaxation before (pre), immediately after (post), and 48–120 h following the first bout of eccentric exercise and the second bout of eccentric exercise 2–3 weeks later. *, Significant (p < 0.05) difference compared with pre; †, significant (p < 0.05) difference compared with the first bout. ECC1 and ECC2, first and second bouts of eccentric exercise, respectively; h, hours after exercise; REL, maximal rate of relaxation. Data are presented as means ± SD.
compared with ECC1 (Fig. 8). There was no significant difference (p > 0.05) between REL mean values for test–retest reproducibility, and CV was 30% before ECC1 vs. 32% before ECC2. Figure 9 presents data for twitch half relaxation time after 2 bouts of eccentric exercise. There were no significant differences (p > 0.05) in HRT after each bout of ECC. There was no significant difference (p > 0.05) between HRT mean values for test–retest reproducibility, and CV was 19% before ECC1 vs. 21% before ECC2.
Discussion The ECC1 protocol that we used was appropriate to induce a rapid adaptation mechanism. Faster MVC recovery, smaller changes in RANG, and significantly reduced muscle soreness after ECC2 demonstrate evidence of the repeated bout effect. The first bout of eccentric exercise reduced MVC immediately after ECC with further decrement 48 h later. Muscle strength loss observed immediately after the exercise could be attributed to metabolic fatigue (Sahlin and Ren 1989; Smith and Newham 2007) and to decrease in voluntary activation process (Kamandulis et al. 2010; Prasartwuth et al. 2005). Prolonged impairment of force generating capacity could be due to both neural process and contractile apparatus failure. Based on the twitch interpolation technique Prasartwuth et al. (2005, 2006) concluded that voluntary activation impairment after eccentric exercise of the elbow flexors occurs during the first 24 h after exercise bout. However, prolonged force deficit is mainly attributed to mechanical myofibrills disruption accompanied by impairment of the excitation–contraction coupling system, which occurs several days after ECC (Ingalls et al. 1998; Proske and Morgan 2001). Initial injury leads to local inflammatory response, which is, at least in part, responsible for development of delayed onset muscle soreness (Smith 1991). Our results of significant and prolonged RANG decrease are consistent with other studies that have used it as indirect marker of exerciseinduced muscle damage (Chen et al. 2007; Starbuck and Eston 2012). It has been hypothesized that some fibers affected by ECC may develop an injury contracture because of uncontrolled sarcoplasmic calcium increase resulting from damage of the sarcoreticular membrane (Whitehead et al. 2001). These changes may be responsible for the increase in muscle passive stiffness, which in turn could be reflected by RANG decrease observed in our study. Published by NRC Research Press
Janecki et al.
Fig. 9. Changes in twitch half relaxation time before (pre), immediately after (post), and 48–120 h following the first bout of eccentric exercise and the second bout of eccentric exercise 2–3 weeks later. There were no significant (p > 0.05) differences between both measurement time and exercise bouts. ECC1 and ECC2, first and second bouts of eccentric exercise, respectively; h, hours after exercise; HRT, twitch half relaxation time. Data are presented as means ± SD.
Faster MVC recovery, attenuated RANG decrease, and reduced soreness perception after ECC2 are consistent with previous studies, where the application of the 1 damaging bout of eccentric exercise conferred protection against the second bout and mechanisms of this phenomenon were described previously (Chan et al. 2012; Chen et al. 2007; Clarkson et al. 1992; Ebbeling and Clarkson 1989; Janecki et al. 2011). The new finding of this study is that the rapid adaptation that occurs after eccentric exercise is also related to some twitch contractile properties such as rate of torque development and peak torque but not to contraction time and half relaxation time changes. These results confirm the hypothesis that the repeated bout effect is evident for some contractile properties. This is the first report of changes in twitch contractile properties after 2 separate bouts of eccentric exercise. TT and RTD decreases were significantly smaller after ECC2 compared with ECC1. This was in line with our hypothesis. In contrast, TPT and HRT remained unchanged after either bout. Our protocol, consisting of 30 submaximal eccentric contractions, resulted in immediate and prolonged decreases in TT, which is in agreement with previous studies measuring this parameter (Prasartwuth et al. 2006; Smith 1991; Smith and Newham 2007). Those results could be due to mechanical sarcomeres disruption (Proske and Morgan 2001) and the damage to muscle membranes that leads to excitation–contraction coupling system impairment (Ingalls et al. 1998). Data obtained during stimulated contractions of the mouse muscle confirm that decrease of the peak sarcoplasmic calcium concentration occurs, which, at least in part, could be the reason for the inability to fully activate the contractile apparatus (Balnave and Allen 1995; Ingalls et al. 1998). Decrease in contractile capacity could be ascribed to changes in length–tension relation that occur after ECC (Jones et al. 1997; Prasartwuth et al. 2006). The rightward shift that occurs after ECC-induced damage could be explained by the “popping” sarcomere hypothesis (Proske and Morgan 2001) where during lengthening contraction some weak and unstable sarcomeres are overstretched beyond their myofilament overlap. This hypothesis has been supported by studies on animal and human
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muscles (Jones et al. 1997; Whitehead et al. 1998). The presence of overstretched or disrupted sarcomeres may increase the series compliance of the muscle, thus leading to the rightward shift in length–tension relation (Gregory et al. 2007). Although we measured TT at 90° only, the potential contribution of the abovementioned shift on force generation capacity decrease cannot be excluded. After ECC2, the values of TT decreased significantly only immediately after exercise and were significantly higher than respective values after ECC1. Faster twitch torque recovery after the second bout of eccentric exercise could be attributed to rapid adaptation mechanisms that occurs after the initial bout of eccentric exercise and is related to muscle repair and (or) rebuilt processes (Lapointe et al. 2002) such as removal of destroyed sarcomeres and cell membrane strengthening (Morgan and Allen 1999), increase in collagen synthesis (Lapier et al. 1995), existing myofibrils remodeling (Yu et al. 2003; Yu et al. 2004), and structural protein reorganization (Lehti et al. 2007). Those mechanisms may lead to a better muscle resistance to eccentric contractions; thus, the susceptibility of the muscle tissue to damage is smaller and therefore TT recovery is faster after ECC2 when compared with ECC1. Both ECC sessions resulted in significant reduction in RTD immediately after exercise. However, when comparing RTD changes at 48–120 h after both ECC1 and ECC2 it appeared that after the second bout it recovers significantly faster (p < 0.05). This could be related to the repeated bout effect. This hypothesis is supported by the lack of significant changes in RTD noted from 48 h after ECC2. The decreases in RTD in our study are in agreement with the previous findings that reported immediate (Michaut et al. 2004) and prolonged changes in this parameter after ECC (Sayers et al. 2003). RTD depends mainly on transient sarcoplasmic calcium increase (Wahr and Rall 1997) and fiber-type (myosin heavy chain (MHC) isoform) composition (Harridge et al. 1995). Eccentric exercise leads to various changes that affect previously mentioned factors. Among them are (i) failure in the excitation–contraction coupling system because of damage of the sarcoreticular membrane, which leads to an increase of the resting sarcoplasmic calcium concentration and thus leads to lower calcium release during muscle excitation (Ingalls et al. 1998); and (ii) myofibrills organization disruption that may impair the actino-myosin crossbridge function (Michaut et al. 2004). As the type II MHC isoforms have elevated cross-bridge cycle transition rate (Harridge et al. 1995), the predominance of this protein is an important intrinsic muscle factor determining RFD (Harridge et al. 1996). Nardone and Schieppati (1988) reported selective activation of fast motor units during eccentric contractions in humans. The results from a cat model experiment (Brockett et al. 2002) indicated that ECCinduced muscle damage occurs in type II fibers mainly (which have significant content of type II MHC isoforms). If the same occurs also in humans, their damage should affect strongly RTD. Gregory et al. (2007) hypothesized that the mentioned disruption of the sarcomeres could also lead to increase in muscle series compliance. In this situation it would need more time to fully take up of the extra compliance during twitch, which in turn could impair both TT and RTD. Similar to TT, changes in RTD were attenuated after the second bout of eccentric exercise and could be ascribed to an adaptation that leads to strengthening and (or) rebuilding of the muscle fibers especially susceptible to eccentric damage (Lapointe et al. 2002). Because those fibers are mainly type II (Brockett et al. 2002) their adaptation results in a faster RTD recovery that occurs after ECC2. There was a lack of differences in TPT after each bout of eccentric exercise. The results provided by Sayers et al. (2003) and Prasartwuth et al. (2005) revealed that significant decreases in TPT occur only immediately after ECC and recovery in this parameter is much faster than the other contractile properties. Initial decrease in TPT, reported by Sayers et al. (2003) and Prasartwuth et al. (2005), without prolonged changes suggest that mechanisms Published by NRC Research Press
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responsible for TPT are affected by physiological fatigue mainly and are less or not susceptible to ECC-induced muscle damage. The contrary results of changes immediately after ECC seen in our study could be explained by the different ECC protocol that we used. In the protocol of Prasartwuth et al. (2005) the subjects performed ECC until isometric maximal voluntary contraction dropped by 40%, which required 50 to 350 repetitions for most participants with 6 s of rest between repetitions in series that consisted of 50 repetitions with 30 s of rest between sets. In the study of Sayers et al. (2003) the subjects performed 2 sets of 25 maximal contractions with 5 min and 12 s of rest, respectively. In our protocol we applied 30 submaximal eccentric contractions with 45-s intervals between each repetition to minimize the effect of fatigue. Shorter rest periods between repetitions and a greater number of contractions could result in greater physiological fatigue changes observed in those studies, which in turn may be responsible for the decreases in TPT immediately after ECC when compared with our results. Another explanation for the lack of changes in this parameter may be because of decreases in twitch torque. Although RTD was lower, the decrease in twitch torque caused by that time to peak torque did not change significantly. Both ECC sessions resulted in significant reduction in REL immediately after exercise. However, when comparing REL changes at 48–120 h after both ECC1 and ECC2, it appeared that after the second bout it recovered significantly faster (p < 0.05). This could be related to the repeated bout effect. This hypothesis is supported by the lack of significant changes in REL noted from 48 h after ECC2. Wahr and al. (1998) suggested that the rate of relaxation depends on cross-bridge dissociation kinetics related to calcium reuptake rate by the sarcoplasmic reticulum and the speed of this process can be affected by fatigue (Green et al. 2011). The results of this study provide evidence that specific changes associated with prolonged disturbance of intracellural calcium homeostasis, which occur after ECC (Whitehead et al. 2001), may affect REL. Therefore, it seems that REL is sensitive to muscle damage after ECC. This hypothesis is supported by faster REL recovery after ECC2, indicating that this parameter reflects repeated bout effect (which is associated with a smaller muscle damage). There was a lack of differences in HRT both between time points after exercise and ECC bouts. Similarly as for TPT, Sayers et al. (2003) and Prasartwuth et al. (2005) revealed that significant decreases in HRT occur only during the first hours after ECC, which suggests that this parameter is affected mainly by physiological fatigue. Although REL and HRT are often used interchangeably (Michaut et al. 2004; Pensini et al. 2002; Prasartwuth et al. 2006; Sayers et al. 2003; Wahr et al. 1998), our data suggests that REL is more sensitive than HRT for specific changes that occur after ECC, which could be explained by a different effect of twitch torque decrease on those parameters. Since the maximal rate of relaxation was slower, the decrease in twitch torque resulted in a lack of changes in the net time of HRT. This novel result should be taken into account when analyzing these parameters in experiments incorporating eccentric exercise. In conclusion, the findings of the present study indicate that the repeated bout effect is evident for some twitch contractile properties such as the peak torque, the maximal rate of torque development, and the maximal rate of relaxation. These findings reflect peripheral adaptation mechanisms that at least in part have an effect on maximal isometric torque changes after eccentric exercise. However, specific muscle damage after ECC used in our protocol did not affect the time to twitch peak torque and the half relaxation time, which should be take into account in future studies on twitch contractile properties changes after eccentric exercise.
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Acknowledgements This work was supported by National Science Centre Grant DEC-2011/01/N/NZ7/00012.
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