Eur J Appl PhysiolDOI 10.1007/s00421-011-1991-3

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ORIGINAL ARTICLE

Comparison in muscle damage between maximal voluntary

and electrically evoked isometric contractions of the elbow Xexors

Marc Jubeau · Makii Muthalib · Guillaume Y. Millet ·

Nicola A. MaYuletti · Kazunori Nosaka

Received: 9 February 2011 / Accepted: 28 April 2011 Springer-Verlag 2011

Abstract This study compared between maximal voluntary(VOL) and electrically stimulated (ES) isometric contrac-tions of the elbow Xexors for changes in indirect markers ofmuscle damage to investigate whether ES would inducegreater muscle damage than VOL. Twelve non-resistance-trained men (23–39 years) performed VOL with one armand ES with the contralateral arm separated by 2 weeks in arandomised, counterbalanced order. Both VOL and ES(frequency 75 Hz, pulse duration 250 �s, maximally toleratedintensity) exercises consisted of 50 maximal isometriccontractions (4-s on, 15-s oV) of the elbow Xexors at a longmuscle length (160°). Changes in maximal voluntaryisometric contraction torque (MVC), range of motion, mus-cle soreness, pressure pain threshold and serum creatine

kinase (CK) activity were measured before, immediatelyafter and 1, 24, 48, 72 and 96 h following exercise. Theaverage peak torque over the 50 isometric contractions wasgreater (P < 0.05) for VOL (32.9 § 9.8 N m) than ES(16.9 § 6.3 N m). MVC decreased greater and recoveredslower (P < 0.05) after ES (15% lower than baseline at96 h) than VOL (full recovery). Serum CK activityincreased (P < 0.05) only after ES, and the muscles becamemore sore and tender after ES than VOL (P < 0.05). Theseresults showed that ES induced greater muscle damage thanVOL despite the lower torque output during ES. It seemslikely that higher mechanical stress imposed on theactivated muscle Wbres, due to the speciWcity of motor unitrecruitment in ES, resulted in greater muscle damage.

Keywords Electrostimulation · Muscle length · Delayed onset muscle soreness · Creatine kinase · Muscle temperature

Introduction

Unaccustomed eccentric exercise induces muscle damagethat is characterised by symptoms such as prolonged loss ofmuscle function and delayed onset muscle soreness orDOMS (Proske and Allen 2005). In some cases, muscledamage is evidenced by degeneration of muscle Wbres and/or inXammation of connective tissue surrounding muscleWbres, and increases in muscle proteins in the circulation(Paulsen et al. 2010; Raastad et al. 2010). Several studies(Aldayel et al. 2010; Jubeau et al. 2008; Mackey et al.2008) have reported that muscle damage is also inducedafter isometric contractions evoked by electrical musclestimulation (ES). For instance, Mackey et al. (2008)reported macrophage inWltration, desmin negative Wbres

Communicated by Alain Martin.

M. Jubeau · M. Muthalib · K. Nosaka (&)School of Exercise, Biomedical and Health Sciences, Edith Cowan University, 270 Joondalup Drive, Joondalup, WA 6027, Australiae-mail: k.nosaka@ecu.edu.au

M. MuthalibSchool of Human Movement Studies, Institute of Health and Biomedical Innovation, Queensland University of Technology, Brisbane, Australia

G. Y. MilletUniversité de Lyon, 42023 Saint-Étienne, France

G. Y. MilletExercise Physiology Laboratory, Jean Monnet University, Saint-Étienne, France

N. A. MaYulettiNeuromuscular Research Laboratory, Schulthess Clinic, Zurich, Switzerland

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and Z-line disruption after 180 isometric contractions of thegastrocnemius muscle evoked by ES. Aldayel et al. (2010)reported that maximal voluntary contraction (MVC)strength was decreased signiWcantly after 40 ES-evokedisometric contractions of the quadriceps (frequency 75 Hz,duration 400 �s, 5 s on–15 s oV) for 4 days, together withthe development of DOMS and increases in plasma creatinekinase (CK) activity.

Jubeau et al. (2008) compared between ES and voluntaryisometric contractions of the knee extensors at the sameforce levels. They showed that no indication of muscledamage was evident following voluntary exercise probablydue to the low intensity of force generation (»26% ofMVC); however, the ES resulted in decreases in MVCstrength, development of DOMS and increases in plasmaCK activity up to »3,600 IU L¡1. In resistance (strength)training programs, however, maximal instead of submaxi-mal voluntary isometric contractions are more often per-formed (Fleck and Kraemer 2004). When ES is used fortraining, muscles are generally stimulated at a maximallytolerable intensity that normally evokes forces of 40–60%MVC (Lieber and Kelly 1991). Thus, it is better to comparebetween ES-evoked and voluntary contractions in the pro-tocols that are used in training to clarify whether ESinduces greater muscle damage than voluntary condition.To the best of our knowledge, no previous study has com-pared the magnitude of muscle damage between repeatedES-evoked and voluntary isometric contractions when bothprotocols are performed at the respective maximal inten-sity.

It is known that muscle length is a factor inXuencingthe magnitude of eccentric exercise-induced muscle dam-age. Nosaka and Sakamoto (2001) showed that the magni-tude of muscle damage induced by eccentric exercise ofthe elbow Xexors was greater when the eccentric contrac-tions were performed for the range of motion (ROM) from100° to 180° (i.e. long muscle lengths, 180° being consid-ered full extension) compared with 50° to 130° (i.e. shortmuscle lengths). It appears that muscle length aVects themagnitude of muscle damage in isometric contractions. Ithas been shown that when repeated maximal voluntaryisometric contractions were performed at 90° of the elbowjoint angle, no signiWcant changes in MVC strength andDOMS were evident (Jones et al. 1989), but when maxi-mal voluntary isometric contractions were performed at along muscle length (elbow joint angle: 140°), MVCstrength decreased and DOMS increased signiWcantly(Jones et al. 1989; Philippou et al. 2003). It appears thatmuscle length is also a factor to inXuence the magnitudeof muscle damage in ES-evoked isometric contractions,since Nosaka et al. (2002) reported that 30 ES-evoked iso-metric contractions at the maximal tolerable intensity ofthe elbow Xexors at a short muscle length (90° elbow

angle) resulted in little or no changes in indirect markersof muscle damage. However, no previous studies haveinvestigated the eVect of ES-evoked isometric contrac-tions of the elbow Xexors at a long muscle length onmuscle damage markers.

The present study was designed to test the hypothesisthat muscle damage would be greater for ES-evoked iso-metric contractions compared with maximal voluntary iso-metric contractions when they were performed at a longmuscle length. Changes in common indirect markers ofmuscle damage were compared between ES-evoked iso-metric contractions and voluntary isometric contractions ofthe elbow Xexor muscles at long muscle length, when thetwo exercises were performed at their respective maximalintensity.

Methods

Study design

To compare between ES and maximal voluntary isometricexercise for muscle damage proWle, 12 men performed 50maximal intermittent (4-s contraction, 15-s relaxation) iso-metric contractions of the elbow Xexors at an elbow angleof 160° (full elbow extension: »180°) with one arm for theES condition and with the contralateral arm for the volun-tary condition (VOL). Each subject performed the two ses-sions separated by 2 weeks, and the order of the session (ESvs. VOL) and the use of the arm for each condition (domi-nant vs. non-dominant arm) were randomised and counter-balanced among the subjects. Among the subjects, 11 menwere right hand dominant and 1 was left hand dominantbased on the Edinburgh Handedness Inventory (OldWeld1971). Six subjects performed the ES session with the rightarm and other six subjects used the left arm for the ES.Both bouts were performed at the same time of the daybetween 8 and 12 a.m. The independent variable was thesession (ES vs. VOL), and the dependent variables includedMVC strength of the elbow Xexors during isometric con-tractions, ROM at the elbow joint, muscle soreness, pres-sure pain threshold (PPT) and serum CK activity. All of themeasurements except the blood sample for CK activitymeasures were taken from the exercised arm, and bloodsamples were taken from the non-exercised arm. The mea-surements were taken before, immediately after (except forCK) and at 1 (only for MVC), 24, 48, 72 and 96 h followingthe exercise. Muscle temperature was assessed before andimmediately after each session, since muscle temperaturehas been proposed as a mechanism to explain muscle dam-age (Armstrong 1984). Changes in the dependent variablesover time were compared between the two exercisesessions.

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Subjects

Twelve healthy men who had not been involved in anyresistance training of the elbow Xexors (either VOL or ES)for at least 6 months prior to the commencement of thestudy participated in this study. Most of the subjects hadnever experienced ES in the past. Their mean (§SD) age,height, and body mass were 31.7 § 5.1 years, 178.4§ 4.9 cm, and 80.8 § 14.0 kg, respectively. All subjectshad neither metabolic or neuromuscular disorders nor anyupper extremity muscle or joint injuries. Subjects wereasked not to perform any strenuous exercise for at least48 h prior to and during the experimental period, and not totake any medication or nutritional supplements. The studywas approved by the University Human Research EthicsCommittee, and the study was conducted in conformitywith the Declaration of Helsinki. All subjects signed a writteninformed consent form before participation in the study.

Isometric exercises

In both ES and VOL sessions, each subject was seated on apreacher arm curl bench, with the upper arm placed on thebench at 45° shoulder Xexion. The elbow joint was alignedwith the axis of the rotation of an isokinetic dynamometer(Cybex 6000, Lumex Inc., Ronkonkoma, NY, USA) oper-ated by a HUMAC-2004 software (Computer Sports Medi-cine, Inc., Stoughton, MA, USA), and the lever arm of thedynamometer was secured to the subject’s wrist in a supi-nated position at an elbow joint angle of 160°. Torque sig-nals were collected onto a data acquisition system(PowerLab16/30 with Chart 5.5.5 software, ADInstru-ments, Bella Vista, Australia) at a sampling rate of 200 Hz,and real-time visual feedback of torque signals was dis-played on a computer screen. Both ES and VOL sessionsconsisted of 50 isometric contractions, and each contractionlasted for 4-s followed by a 15-s resting period betweencontractions. In the ES condition, elbow Xexors were stim-ulated at the maximally tolerated intensity, while in theVOL condition the subjects maximally contracted theirelbow Xexor muscles against the non-movable padded wristbrace attached to the isokinetic dynamometer lever arm.The peak torque of each contraction and the torque-timeintegral that was determined as the area under the curve ofthe torque trace over the contraction duration were ana-lysed.

Electrical muscle stimulation

A portable electrical stimulator (Compex Sport-P, Medi-compex SA, Ecublens, Switzerland) was used to deliverbiphasic symmetric rectangular pulses with the followingcharacteristics: frequency 75 Hz, pulse duration 250 �s, 4 s

on (0.5 s rise time, 3.5 s steady time, and 0 s fall time) to15 s oV ratio. Three self-adhesive electrodes (Compex,Medicompex SA, Ecublens, Switzerland) were placed on thestimulated arm with two small electrodes (5 cm £ 5 cm) overthe mid-belly of the biceps brachii and brachioradialismuscles and one dispersive electrode (5 cm £ 10 cm) onthe elbow crease. Current amplitude was progressivelyincreased by the investigator over the Wrst 5 contractions toreach the maximal tolerated current level of each subject.Thereafter, current amplitude was consistently increased(for both biceps brachii and brachioradialis muscles sepa-rately) throughout the remaining 45 contractions to theindividual maximally tolerable level (pain threshold) so asto maximise muscle tension (Lieber and Kelly 1993).Current amplitude was increased from 41 § 10 to62 § 21 mA for the biceps brachii and from 39 § 9 to53 § 21 mA for the brachioradialis.

Muscle temperature

Muscle temperature was measured using a needle thermis-tor probe (model N451; Nikkiso-YSI Ltd, Tokyo, Japan)connected to a thermometer (model N550; Nikkiso-YSI).The thermistor probe (22 gauge, 70 mm) was inserted intothe belly of the biceps brachii to a depth of 15–20 mmbefore and within 1 min after both exercise bouts, and thetemperature of the muscle was recorded when it did notXuctuate more than §0.1° for 5 s.

Maximal voluntary isometric contraction strength

After a warm-up protocol consisting of 5–6 submaximal(range »25 to 75% of MVC) voluntary isometric contrac-tions, subjects performed unilateral maximal isometric con-tractions on the isokinetic dynamometer described above attwo elbow joint angles in the order from 160° to 90° usingthe exercised arm. Each contraction lasted 3 s, and the mea-surement was taken twice for each angle with a 60-s restbetween contractions and a 90-s rest between the diVerentangles (160° followed by 90°). The subjects were asked togenerate their maximal force as fast as possible without anypre-activation (Aagaard et al. 2002). The higher torque ofthe two measures was used for further analysis. If the diVer-ence in the two measures was >5%, another measure wastaken. The correlation of the muscle strength measurementsbetween the two trials was high (r = 0.99) and the variabil-ity was low (coeYcient of variation: 1.3 and 1.9% at 160°and 90°, respectively).

ROM

A plastic goniometer was used to measure the ROM of theelbow joint. ROM was calculated by subtracting the Xexed

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elbow joint angle from the relaxed elbow angle. Therelaxed elbow joint angle was determined as the anglewhen the subject was standing and asked to hang his armrelaxed by his side, while the Xexed elbow joint angle wasdetermined when subject attempted to fully Xex the elbowjoint to touch the shoulder of the same side with the palm.A semi-permanent ink pen was used to mark the followinglandmarks: the lateral epicondyle of the humerus, the acro-mion process and the mid-point of the styloid process of theulna and radius. Measurements were taken twice for eachangle and the mean value of the two measurements wasused to calculate the ROM.

Muscle soreness and tenderness

Muscle soreness was assessed using a visual analog scale(VAS) with a 100-mm horizontal line with “no pain” onone end (0 mm) and “extremely painful” on the other(100 mm). Subjects were asked to mark their pain level onthe VAS under supervision of the examiner while the corre-sponding joint was passively Xexed and extended by theinvestigator. Palpation was also applied by the investigatorusing the index and middle Wngers on Wve sites: three sitesof the biceps brachii (mid-belly, 4-cm above and below themid-belly of the biceps brachii) and the two others sitescorresponding to the mid-belly of the brachialis and bra-chioradialis. For the biceps brachii, the average value of thethree sites was used for further analysis.

PPT was recorded by an electronic algometer (SomedicAB, Sweden) with a stimulation area of 1.0 cm2 to assessmuscle tenderness (measuring range 0–1,999 kPa). Theprobe head of the algometer was placed perpendicular toWve sites: mid-belly of the biceps brachii, 4-cm above andbelow the mid-belly of the biceps brachii, mid-belly of thebrachioradialis and brachialis, in this order with approxi-mately 15-s interval between sites. For each site, pressurewas gradually applied at a rate of 50 kPa s¡1 until the sub-jects reported the Wrst feeling of noticeable pain. Thevalue (in kPa) corresponding to the amount of pressureapplied to induce pain was recorded. Three measurementswere taken from each site with approximately a 10-s restbetween measures, and the average value of the threemeasurements was used for subsequent analysis. Thevalues of the three sites of the biceps brachii were averagedfor further analysis.

Serum CK activity

Approximately 5 mL of blood was drawn by a standardvenipuncture technique from the antecubital vein. Bloodsamples were clotted at room temperature and centrifugedfor 10 min to obtain serum. Serum CK activity was deter-mined by a Hitachi Modular PT automated clinical chemistry

analyser (Hitachi, Japan) with a commercially availableRoche Diagnostics Reagent (Mannheim, Germany). Thenormal reference range of CK activity using this method is<200 IU L¡1.

Statistical analyses

After a check for normality using a Kolmogorov–Smirnovtest, changes in the dependent variables over time werecompared between ES and VOL sessions by a two-wayrepeated-measure ANOVA. When a signiWcant main eVectof session, time or an interaction (session £ time) wasfound, a Tukey’s HSD post hoc test was performed formultiple comparisons. SigniWcance was set at P < 0.05. Allvalues are presented as mean § SD.

Results

Torque during isometric exercise

As shown in Fig. 1, the normalised peak torque produced ineach contraction was always greater for VOL than ES(P < 0.001). The average peak torque over the 50 contrac-tions was also greater (P < 0.001) for VOL (74.3 § 9.5% ofpre-MVC) when compared with ES (33.6 § 8.3% of pre-MVC), and so was the total torque-time integral over thesession (5,698 § 2,031 N m s for VOL vs. 2,596 § 1,012N m s for ES).

Muscle temperature

Muscle temperature increased signiWcantly (P < 0.001)immediately after exercise from 34.5 § 0.7 to 37.9 § 0.5°Cfor ES and from 34.4 § 0.7 to 37.9 § 0.4°C for VOL,without signiWcant diVerences between the conditions(P = 0.59).

Fig. 1 Normalised changes in peak torque over 50 isometric contrac-tions in electrical stimulation (ES) and voluntary (VOL) sessions.#SigniWcantly (P < 0.05) diVerent between ES and VOL

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MVC strength

No signiWcant diVerences between ES and VOL sessionswere found for the baseline MVC strength at 90° (ES:71.5 § 16.8 N m, VOL: 71.8 § 14.1 N m, P = 0.98) and160° (50.9 § 16.7 N m, 51.8 § 13.0 N m, P = 0.86). MVCstrength decreased signiWcantly (P < 0.001) after both ESand VOL sessions (Fig. 2), and the normalised changes (i.e.»¡42% of baseline MVC) were similar between 90° and160°. However, the magnitude of the decrease in MVCstrength was greater for ES than VOL, and the recovery ofMVC strength was slower after ES than VOL (P < 0.001for 160° and P < 0.01 for 90°). In ES session, MVCstrength remained signiWcantly below the baseline at 72 and96 h post-exercise at 160° and 90°, respectively, whereasMVC strength returned to the baseline at 24 h (160°) and96 h (90°) post-exercise for VOL (Fig. 2).

ROM

The baseline ROM was similar (P = 0.31) between ES(121.5 § 7.9°) and VOL (118.8 § 4.4°). ROM was decreased(P < 0.001) after both sessions from immediately(¡8.6 § 5.1° for ES and ¡8.6 § 5.4° for VOL) to 4 daysafter exercise (¡4.6 § 7.5° for ES and ¡3.3 § 3.1% forVOL) without signiWcant diVerence in the changes betweenES and VOL (P = 0.68).

Muscle soreness and tenderness

Muscle soreness increased after both ES and VOL sessions(P < 0.001). For the palpation measures, the changes weresimilar for biceps brachii, brachialis and brachioradialis.Figure 3a shows the changes in muscle soreness upon pal-pation of the biceps brachii. Muscle soreness increased at24 h and peaked at 48 h post-exercise for both conditions,but the magnitude of muscle soreness was greater(P < 0.05) for ES than VOL at 48 h post-exercise. Themagnitude of muscle soreness upon passive Xexion andextension (Fig. 3b) was lower (P < 0.001) than that of thepalpation of the biceps brachii (Fig. 3a); however, the timecourse of changes in muscle soreness was similar to thatshown in the palpation. No signiWcant diVerences betweenES and VOL were evident (P = 0.32) for muscle sorenessupon passive Xexion and extension.

PPT for the three muscles was signiWcantly reduced afterexercise for both ES and VOL conditions (P < 0.001), sug-gesting that muscles became more tender after ES and VOLsessions. As shown in Fig. 4, the decreases in PPT weresigniWcantly greater after ES than VOL at 48–96 h post-exercise for the biceps brachii (P < 0.01 at 48 h andP < 0.001 at 72 and 96 h). The time course and the magni-tude of changes in PPT for the brachialis were similar tothat shown for the biceps brachii (P = 0.65). For thebrachioradialis, the decrease in PPT was slightly lower than

Fig. 2 Normalised changes in maximal voluntary isometric contrac-tion (MVC) strength at 160° (a) and 90° (b) before (Pre), immediatelyafter (Post), and 1, 24, 48, 72 and 96 h after exercise for electrical stim-ulation (ES) and voluntary contraction (VOL) sessions. *SigniWcantly(P < 0.05) diVerent from Pre. #SigniWcantly (P < 0.05) diVerent be-tween ES and VOL

Fig. 3 Muscle soreness assessed by a visual analog scale (VAS) uponpalpation for biceps brachii (a) and with extension of the elbow joint(b) before (Pre), immediately after (Post), and 24, 48, 72 and 96 h afterexercise for electrical stimulation (ES) and voluntary contraction(VOL) sessions. *SigniWcantly (P < 0.05) diVerent from Pre. #SigniW-cantly (P < 0.05) diVerent between ES and VOL

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that for the biceps brachii (P < 0.01) for both ES and VOLconditions. Moreover, the diVerence in PPT between ESand VOL sessions did not reach the level of signiWcance forthe brachioradialis (P = 0.17) and for the brachialis(P = 0.25).

Serum CK activity

Figure 5 shows the changes in serum CK activity after ESand VOL. A signiWcant increase in serum CK activity wasevident 4 days post-exercise only for ES.

Discussion

The main Wndings of the present study were that both maximalvoluntary and ES-evoked isometric contractions of theelbow Xexors at a long muscle length resulted in moderatebut signiWcant changes in indirect markers of muscle

damage. The magnitude of the changes was signiWcantlygreater after the ES than voluntary session for MVCstrength (both 90° and 160° elbow angle), muscle sorenessand tenderness, and serum CK activity, despite the fact thatthe torque output in the ES session was »50% smaller thanthat in the voluntary session. These results support thehypothesis that the magnitude of muscle damage would begreater for ES-evoked isometric contractions comparedwith maximal voluntary isometric contractions.

In the present study, the torque evoked by ES (e.g. from»35% of pre-MVC at the beginning of the session to»30% of pre-MVC at the end) was similar to that reportedin previous ES studies on knee extensors (Aldayel et al.2010; Jubeau et al. 2008). The ES-evoked torque remainedrelatively constant over the 50 isometric contractions(Fig. 1), because of the continuous increase in currentamplitude. The subjects were able to tolerate higher ESdose current in the progress of the session, probably due tothe subjects habituating to the electrical stimulus because ofan increase in tissue conductance resulting from increasedblood Xow and/or interstitial Xuid volume (Alon and Smith2005). ES-evoked isometric contractions even at maximallytolerable intensity generated »50% lower torque than max-imal voluntary isometric contractions. The lower torque inES can be explained by less motor unit recruitmentcompared to VOL, since ES activates preferentially superW-cial muscle Wbres adjacent to the stimulation electrodes(Vanderthommen et al. 2003), while in VOL, nearly allelbow Xexor and stabiliser muscles are likely to be acti-vated. It is also important to note that in ES, the brachialiswas unlikely to be stimulated in the present study, becausethe electrode placement mainly focused on the bicepsbrachii and brachioradialis muscles. It has been reportedthat the brachialis contributes to »25% of the elbow Xexortorque output at long muscle lengths (van Bolhuis and Gie-len 1997). This can partly explain the diVerences in torqueoutput between the two conditions.

The present study demonstrated that repeated maximalvoluntary isometric contractions at a long muscle length(160°) resulted in small but signiWcant decreases in MVCstrength and ROM, and increases in muscle soreness andtenderness. Based on the decreases in MVC strength lastingmore than 3 days (Fig. 2b), it is assumed that muscle dam-age was induced in both ES and voluntary bout, as a pro-longed decrease in muscle strength best indicates muscledamage (Warren et al. 1999). Philippou et al. (2003) alsoreported that 50 maximal voluntary isometric contractionsof the elbow Xexors at the elbow joint angle of 140°resulted in a signiWcant reduction of MVC strength (¡16%at 140° elbow angle at 24 h) as well as an increase in mus-cle soreness (peak »25 mm on a 0–100 mm VAS) and CKactivity (peak »150% increase from baseline). In the pres-ent study, no signiWcant increase in serum CK activity was

Fig. 4 Normalised changes in pressure pain threshold (PPT) of the bi-ceps brachii before (Pre), immediately after (Post), and 24, 48, 72 and96 h after exercise for electrical stimulation (ES) and voluntary con-traction (VOL) sessions. *SigniWcantly (P < 0.05) diVerent from Pre.#SigniWcantly (P < 0.05) diVerent between ES and VOL

Fig. 5 Changes in serum CK activity before (Pre) and 24, 48, 72 and96 h after exercise for electrical stimulation (ES) and voluntary (VOL)sessions. *SigniWcantly (P < 0.05) higher than Pre. #SigniWcantly(P < 0.05) diVerent between ES and VOL

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found after VOL. It seems likely that the diVerences in theduration of the contraction (4 s in the present study vs. 10 sin the Philippou et al. study) and, consequently in totalwork could explain the discrepancy.

Philippou et al. (2003) reported a signiWcantly slowerrecovery of MVC strength at a short (90°) compared to along muscle length (160°), and explained that this wasassociated with the presence of overstretched sarcomeresthat increased in series compliance of the muscle, thereforecausing a rightward shift of the force–length relationship.The present study found that recovery of MVC strengthwas slower for 90° than 160°; interestingly, this was notspeciWc to the exercise task (isometric contractions wereperformed at 160°). Desbrosses et al. (2006) reported thatthe decrease in MVC strength immediately after isometriccontractions of the knee extensors at a long muscle length(knee angle 100°; full extension 0°) was mainly associatedwith a reduction in doublet peak torque (i.e. contractile fail-ure) rather than a decrease in maximal voluntary activation(i.e. activation failure), whereas isometric exercise at ashort muscle length (knee angle 40°) induced mainly areduction in voluntary muscle activation. The authors statedthat the decrement in MVC strength after the isometric con-tractions at a long muscle length might be due to muscledamage. It appears that the decrease in MVC strength afterisometric contractions at a long muscle length is mainlyattributed to alterations at or distal to the neuromuscularjunction (e.g. impairment of excitation–contractioncoupling) rather than neural mechanisms (i.e. reduction ofvoluntary activation of muscle). Morgan et al. (2000)suggested that weaker sarcomeres were overstretched anddamaged during eccentric contractions on the descendinglimb of the sarcomere length-tension curve. The descendinglimb of the length–tension relationship starts around 100°for the elbow Xexors (van Zuylen et al. 1988). It is possiblethat the elbow joint angle used in the present study (160°)placed the weaker sarcomeres in an overstretched position,leading to ultrastructural damage. Another possibility isthat excitation–contraction coupling was impaired byisometric contractions at a long muscle length as shownin eccentric contractions (Warren et al. 2001). Further stud-ies should assess force–length and force–frequency rela-tionships in ES and VOL contractions to test the twohypotheses.

The novel Wndings of our study were that ES-evoked iso-metric contractions at a long muscle length induced greaterdecreases in MVC strength and increases in muscle sore-ness and tenderness, and serum CK activity when comparedwith maximal voluntary isometric contractions. It isunknown whether this diVerence in the magnitude of mus-cle damage persists when both ES and voluntary isometriccontractions are performed at a short and/or optimal musclelength. However, it seems likely that the diVerence in the

magnitude of muscle damage between ES-evoked andmaximal voluntary isometric contractions is minimumwhen they are performed at a short muscle length (e.g. 90°),since changes in indirect muscle damage markers are smalland short-lived (immediately after exercise only) followingES-evoked isometric contractions at 90° (Nosaka et al.2002) and maximal voluntary isometric contractions at 90°(unpublished observation).

In the present study, contraction intensity during ES was»35% of pre-MVC at the beginning and 33% of pre-MVCin average. It is important to note that the magnitude ofchanges in muscle damage markers (e.g. MVC strengthdecrement, peak serum CK activity) after ES-evoked iso-metric contractions was not correlated with the individuallevels of evoked torque relative to MVC strength during theES session (data not shown). This might suggest that theintensity of the contraction, at least for the whole musclelevel, is not the main factor responsible for the damage dur-ing ES. The increases in serum CK activity were relativelysmaller in the present study compared with our previousstudy (Jubeau et al. 2008) in which the quadriceps of bothlegs were stimulated (CK: »3,600 IU L¡1). It is likely thatthe smaller volume of muscles involved in the present study(one arm) than the previous study (two legs) can explain thesmaller increases in serum CK activity in the present study.Serum CK activity increased only at 4 days post-exercise inES. A delayed increase in CK activity in the blood is oftenobserved following submaximal eccentric exercise (Nosakaand Newton 2002; Peake et al. 2006), and it is well knownthat CK activity peaks 3–5 days after eccentric exercise ofthe elbow Xexors (Nosaka and Clarkson 1996; Nosaka andNewton 2002). Thus, it seems that the cause of increases inCK activity in the blood is the same between muscle dam-age induced by ES-evoked isometric contractions andeccentric contractions. However, it should be noted that themagnitude of changes in muscle damage markers after ES-evoked isometric contractions in the present study wasmuch smaller than that normally observed after maximalvoluntary eccentric contractions of the elbow Xexors. Forexample, Nosaka et al. (2005) reported greater decreases inMVC strength (»60% at immediately post-exercise, »50%at 4 days post-exercise) and ROM (¡25° at 2–4 days post-exercise), and a greater increase in CK activity in the blood(»16,000 IU L¡1 at 4 days post-exercise) following 24eccentric contractions of the elbow Xexors at long musclelength performed by untrained subjects.

The mechanisms underpinning muscle damage inducedby ES-evoked isometric contractions have not been fullyelucidated. It has been proposed that an elevated muscletemperature may cause damage to the structural proteins,resulting in necrosis of muscle Wbres (Armstrong 1984).However, the increase in biceps brachii muscle temperature(»3°C) was not signiWcantly diVerent between ES and

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voluntary contraction sessions. Thus, it is unlikely thatmuscle temperature is a factor to explain the greaterdamage observed after ES-evoked than maximal voluntaryisometric contractions. We suggest that the pattern of motorunit activation is responsible for the muscle damageinduced by ES exercise. It has been documented that therecruitment during ES is spatially Wxed (Gregory andBickel 2005), meaning that the same motor units are con-tinuously recruited, even after they became fatigued, thusimposing high mechanical stress to the recruited muscleWbres. In contrast, during voluntary contractions, motorunits that are fatigued might not be recruited. Moreover,since the recruitment during ES is superWcial and incom-plete (MaYuletti 2010), the volume of muscle activated byES is essentially smaller compared to maximal voluntaryisometric contractions. It can be assumed that, according toAdam’s formula (1993), the volume of muscle activatedduring ES at the beginning of the present protocol was only»26% of the total muscle, whereas it would have beennear-maximal during VOL. Moreover, in the maximal vol-untary contractions, it seems likely that all elbow Xexor andstabiliser muscles contributed to the force production, thusbetter distributing the forces over a larger activated musclevolume. Black et al. (2008) reported that ES-evoked eccen-tric contractions at 100 Hz induced greater damage thanES-evoked eccentric contraction at 25 Hz, and explainedthat this was due to greater speciWc torque in the formercondition. We can therefore speculate that the cause ofmuscle damage in ES-evoked isometric contractions is notdiVerent from that of ES-evoked eccentric contractions; thestress imposed on each muscle Wbre is the main cause ofmuscle damage in ES. Further studies are needed to com-pare the magnitude of muscle damage between eccentricand isometric contractions for the same force output peractive area.

Gregory and Bickel (2005) and Jubeau et al. (2007)stated that ES activates motor units in a random and non-selective manner, meaning that fast twitch Wbres may berecruited even at low torque levels (<40% MVC). Fasttwitch Wbres are mainly located on the superWcial regions ofa muscle (Manta et al. 1995). We can therefore assume thatboth fast and slow motor units are activated by ES, thusimposing greater mechanical stress to fast twitch Wbres fora longer period in ES than voluntary contractions. Duringrepeated maximal voluntary contractions, fast twitch Wbresmight not be recruited when fatigue is induced. This maynot occur during ES, since ES imposes a continuous con-tractile activity in the same pool of slow and fast twitchWbres for the entire exercise period. It is known that fasttwitch Wbres are more susceptible to eccentric exercise-induced muscle damage, in particular to myoWbrillar dis-ruption compared with slow twitch Wbres (Lieber et al.1991). Crameri et al. (2007) reported that ultrastructural

damage (e.g. Z-line streaming) was greater after ES-evokedeccentric contractions than maximal voluntary eccentriccontractions. They suggested that the early activation offast twitch Wbres were associated with the greater muscledamage in ES-evoked eccentric contractions. It is possiblethat ES-evoked isometric contractions also induce greaterdamage of fast twitch Wbres than maximal voluntaryisometric contractions.

To better understand the mechanisms underpinning themuscle damage induced by ES-evoked isometric contrac-tions, further studies are necessary. It would be useful todiscriminate the neural and muscular factors that are associ-ated with the greater muscle strength loss after ES-evokedthan maximal voluntary isometric contractions. The use ofmotor nerve and/or transcranial magnetic stimulationtogether with electromyography activity could be useful toinvestigate the sites of alteration (central vs. peripheral). Itis also important to examine histological changes in muscleWbres and extracellular matrix after ES-evoked and maxi-mal voluntary isometric contractions.

The Wndings of the present study may be useful for clini-cians and practitioners, since ES is used in sport trainingand rehabilitation including the treatments to restore somedegree of motor function in individuals following spinalcord injury or stroke (Bax et al. 2005; MaYuletti 2010;Vanderthommen and Duchateau 2007). If it is necessary tominimise muscle damage induced by ES, the muscle lengthat which muscles are stimulated should be considered, andit may be better to simulate the muscles at an optimal ratherthan a long length. It is important to note that isometriccontractions at a long muscle length rather than at a shortmuscle length are recommended in isometric training tominimise the joint-angle speciWcity (Fleck and Kraemer2004). Aldayel et al. (2010) showed that changes in indirectmarkers of muscle damage such as MVC strength and mus-cle soreness were attenuated after the second ES boutwhich was performed 2 weeks after an initial ES bout. Ithas also been reported that submaximal non-damagingeccentric contractions confer protective eVect againsthigher intensity eccentric contractions (Lavender andNosaka 2008). Thus, it is possible to attenuate potentialmuscle damage induced by ES by “pre-conditioning”muscles.

Conclusion

This study showed that isometric contractions at a longmuscle length induced moderate but signiWcant muscledamage to the elbow Xexors. Comparatively, muscle dam-age is greater in electrically induced isometric contractionsat maximally tolerable intensity despite lower torque outputthan maximal voluntary isometric contractions. It appears

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that the speciWcity of muscle activation in ES, inducing agreater force per activated muscle Wbres, is responsible forthe greater muscle damage in ES compared with voluntarycontractions.

Acknowledgments The authors express their gratitude to Dr. JulienGondin (CRMBM, UMR CNRS 6612, University of the Mediterra-nean) for his valuable comments to our paper.

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