Massage and stretching reduce spinal reflex excitability without affecting twitch contractile properties

Journal of Electromyography and Kinesiology xxx (2013) xxx–xxx

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Journal of Electromyography and Kinesiology

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Massage and stretching reduce spinal reflex excitability withoutaffecting twitch contractile properties

1050-6411/$ - see front matter � 2013 Elsevier Ltd. All rights reserved.http://dx.doi.org/10.1016/j.jelekin.2013.05.002

⇑ Corresponding author. Tel.: +1 709 864 3408; fax: +1 709 864 3979.E-mail address: [email protected] (D.G. Behm).

Please cite this article in press as: Behm DG et al. Massage and stretching reduce spinal reflex excitability without affecting twitch contractile propElectromyogr Kinesiol (2013), http://dx.doi.org/10.1016/j.jelekin.2013.05.002

David G. Behm a,⇑, Ashley Peach a, Meaghan Maddigan a, Saied Jalal Aboodarda a, Mario C. DiSanto b,Duane C. Button a, Nicola A. Maffiuletti c

a School of Human Kinetics and Recreation, Memorial University of Newfoundland, St. John’s, Newfoundland, Canada A1C 5S7b Instituto del Profesorado en Educacion Fisica, Cordoba, Argentinac Neuromuscular Research Laboratory, Schulthess Klinik, Lengghalde 2, 8008 Zurich, Switzerland

a r t i c l e i n f o a b s t r a c t

Article history:Received 19 March 2013Received in revised form 24 April 2013Accepted 9 May 2013Available online xxxx

Keywords:H-reflexM-waveMuscleTapotementElectromechanical delay

Both stretching and massage can increase range of motion. Whereas the stretching-induced increases inROM have been attributed to changes in neural and muscle responses, there is no literature investigatingthe ROM mechanisms underlying the interaction of stretch and massage. The objective of this paper wasto evaluate changes in neural and evoked muscle responses with two types of massage and static stretch-ing. With this repeated measures design, 30 s of plantar flexors musculotendinous junction (MTJ) andtapotement (TAP) massage were implemented either with or without 1 min of concurrent stretchingas well as a control condition. Measures included the soleus maximum H-reflex/M-wave (H/M) ratio,as well as electromechanical delay (EMD), and evoked contractile properties of the triceps surae. Withthe exception of EMD, massage and stretch did not significantly alter triceps surae evoked contractileproperties. Massage with and without stretching decreased the soleus H/M ratio. Both TAP conditionsprovided greater H/M ratio depression than MTJ massage while the addition of stretch provided thegreatest inhibition. Both massage types when combined with stretching increased the duration of theEMD. In conclusion, MTJ and TAP massage as well as stretching decreased spinal reflex excitability, withTAP providing the strongest suppression. While static stretching prolongs EMD, massage did not affectcontractile properties.

� 2013 Elsevier Ltd. All rights reserved.

1. Introduction

Both stretching and massage techniques have been used in anattempt to acutely increase joint range of motion (ROM). The effec-tiveness of static stretching (SS) to acutely increase ROM (Behmet al., 2001, 2004, 2006, 2011) has been attributed to both neuraland muscular factors (Behm and Chaouachi, 2011). SS-inducedmuscle changes include increases in musculotendinous unit(MTU) length and stiffness (Alter, 1996; Wilson et al., 1991) as wellas an increased tolerance to stretch (Magnusson et al., 1996). Evi-dence has also been presented to show a SS-induced reduction ofthe H-reflex amplitude, representing decreased spinal reflex excit-ability (Avela et al., 1999; Guissard et al., 1988, 2001).

The effectiveness of massage to increase ankle dorsiflexion ROMis more controversial. Three minutes of petrissage (kneadingactions) and tapotement (percussive strokes) similarly increasedankle joint ROM by 3–4% (McKechnie et al., 2007). Thirty secondsof musculotendinous junction (MTJ) massage improved hip flexor

ROM by approximately 7% (Huang et al., 2010). Dynamic soft tissuemobilization has been reported to provide greater or equal in-creases in hamstring flexibility compared to classic soft tissuemobilization or massage (Hopper et al., 2005a,b). Conversely,15 min of effleurage (circular stroking movements) and petrissagedid not increase sit and reach scores with healthy active males(Barlow et al., 2004) or adolescent soccer players (Jourkesh,2007). Fifteen minutes of petrissage did not improve ROM of hipabduction, extension, flexion and knee extension but augmentedankle dorsiflexion ROM in healthy men. Stretching in that samestudy was found to be more effective than massage to increaseROM (Wiktorsson-Moller et al., 1983).

Not all massage techniques are intended for the same purpose.Whereas techniques such as effleurage aim to promote relaxation(Weerapong et al., 2005), the objective of tapotement is to stimu-late sensory (mechanoreceptors) receptors (Morelli and Sullivan,1999; Weerapong et al., 2005). Light (Goldberg et al., 1992) anddeep (Goldberg et al., 1992) petrissage massage of the triceps suraewith one hand (Morelli et al., 1990; Sullivan et al., 1991) have allresulted in H-reflex amplitude depression with deep petrissageproviding greater inhibition than light massage. A massage

erties. J

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intervention that included effleurage, petrissage and tapotementnegatively affected isokinetic muscle strength at high speeds,which was attributed to possible increases in parasympathetic in-put and decreased afferent feedback resulting in decreased motorunit activation (Arroyo-Morales et al., 2011).

As massage techniques are transmitted to the muscle throughthe skin, the activity of the cutaneous afferents would be expectedto play a role in the excitation or inhibition of the central nervoussystem. Sayenko et al. (2009) used non-noxious electrical plantarcutaneous afferent stimulation of the heel and metatarsal regionsand reported both soleus H-reflex facilitation and inhibition withshort and long durations respectively when applied to the heel.However, both stimulation durations resulted in H-reflex depres-sion when applied to the metatarsals. Stimulation of flexor carpiradialis cutaneous afferents with single 10 ms duration pulsesfrom a probe attached to an electromagnetic vibrator producedan immediate H-reflex decline (2 ms) followed by a facilitationlasting 10 ms (Cavallari and Lalli, 1998). Hence, the H-reflex re-sponse can be quite variable dependent upon the type, durationand location of the stimulation.

As there is no information on the effect of massage on musclecontractile properties, it is unknown whether massage-induced in-creases in ROM (Huang et al., 2010; McKechnie et al., 2007) can beattributed more to mechanical or neural factors. An examination ofelectromechanical delay (EMD) would provide insights regardingchanges to musculotendinous compliance. Monitoring twitch con-tractile properties would help gauge massage-induced musclechanges in force and temporal properties. Thus one objective ofthis research was to investigate possible changes in maximal H-re-flex/M-wave (H/M) ratios as a surrogate of spinal reflex excitability(Trimble and Enoka, 1991) with combinations of SS, tapotementand MTJ massage. As the H/M ratio represents a valid indicatorof spinal-mediated neural changes to massage and SS, anotherobjective was to examine changes in twitch contractile propertieswith massage and SS to highlight neural versus muscular altera-tions. It was hypothesized that the MTJ massage technique andSS would reduce the H/M ratio whereas tapotement would in-crease the H/M ratio with no significant effect on muscle contrac-tile properties.

2. Materials and methods

Based on previously published related articles (Avela et al.,1999; Etnyre and Abraham, 2005; Goldberg et al., 1992; Guissardet al., 1988, 2001) a statistical power analysis was conducted to en-sure an alpha of 0.05 and a power of 0.8. Seventeen recreationallyactive university student participants (13 females: 169.6 ± 6.4 cm,70.3 ± 8.9 kg, 22.2 ± 0.8 years and 4 males: 180.2 ± 2.1 cm,90.5 ± 11.7 kg, 31 ± 8.4 years) from Memorial University of New-foundland volunteered for the study. All subjects were healthy

Fig. 1. Experimental Protocol. Acronyms: TAP: tapotement massage of gastrocnemius, Melectromechanical delay.

Please cite this article in press as: Behm DG et al. Massage and stretching reducElectromyogr Kinesiol (2013), http://dx.doi.org/10.1016/j.jelekin.2013.05.002

with no history of neurological impairments. A verbal overviewof procedure and purpose of the study was given to all subjects.A signed Physical Activity Readiness Questionnaire (Canadian Soci-ety for Exercise, 2003) was collected from all subjects before par-ticipation. All subjects signed written informed consent formbefore their participation in the study. Subjects were instructedto not smoke, drink alcohol, or exercise at least 6 h prior to testingand to not eat food or caffeinated beverages for at least 2 h prior totesting (Canadian Society for Exercise, 2003). The Human Investi-gation Committee of the Memorial University of Newfoundland ap-proved this study.

2.1. Experimental protocol (Fig. 1)

Participants were seated with the ankle fixed in an isometricboot apparatus (Fig. 2) equipped with strain gauges (Omega Engi-neering Inc. LCCA 250, Don Mills Ontario, Canada) (Behm et al.,2002) and were randomly subjected to the following conditionson five separate testing days: (1) MTJ massage, (2) tapotementmassage, (3) MTJ massage with stretch, (4) tapotement massagewith stretch and (5) control (no massage or stretch). Following apre-intervention test, a massage intervention was instituted for30 s (MTJ, MTJ with stretch, tapotement or tapotement withstretch), followed by another 30 s of no massage but continuedstretch position for two of the conditions (MTJ and tapotementmassage with stretch). Thirty seconds of massage was chosenbased on the Huang et al. (2010) article, which demonstrated sig-nificant (7%) increases in ROM following 30 s of MTJ massage. After60 s, the ankle joint was returned to a neutral position (for the twomassage with stretch conditions). Testing was conducted pre-test,15, 30, 45 and 60 s into the intervention period and at 1 and 2 minpost-intervention. Dependent variables included soleus H/M ratio,plantar flexors twitch contractile properties (peak torque, time topeak torque, half-relaxation time (HRT)), soleus M-wave amplitudeand electromechanical delay (EMD).

2.2. Interventions (independent variables)

A certified massage therapist provided the massage. Whileseated with knees and hips at 90�, and the right leg inserted intothe isometric boot apparatus, subjects received either MTJ ortapotement massage for 30 s. Two experimental conditions in-volved only massage with the ankle at 90� (MTJ and tapotementconditions) whereas the two other conditions involved MTJ ortapotement massage with the ankle placed in a maximal dorsi-flexed position for 60 s (first 30 s with massage and second 30 swithout massage). The ankle was in a neutral (90�) position (with-out massage) for the control condition. During the control condi-tion the massage therapist placed his hands on the triceps suraewithout movement or substantial pressure.

TJ: musculotendinous junction massage of Achilles tendon and soleus muscle, EMD:

e spinal reflex excitability without affecting twitch contractile properties. J

D.G. Behm et al. / Journal of Electromyography and Kinesiology xxx (2013) xxx–xxx 3

MTJ massage involved an effleurage (circular stroking move-ments) technique over the Achilles tendon tendon. Tapotementmassage involved a vigorous percussive stroking motion withtwo hands upon the mid-belly of the gastrocnemius (medial andlateral) at an estimated frequency of 2 Hz (1 Hz per hand). Bothmassage conditions persisted for 30 s.

2.3. Measures (dependent variables)

Measures were conducted prior to the interventions (pre-test),at 15, 30, 45 and 60 s during the interventions, and 1 and 2 minpost-interventions (no massage and no stretch). At each testingtime, we always delivered a single submaximal stimulation tothe tibial nerve (to evoke the maximal H-reflex response for the so-leus) that was systematically followed 5 s later by a single maximalstimulation (to evoke the maximal M-wave response for the soleusand twitch contractile properties for the plantar flexors).

2.4. Electrical stimulation procedures

One of the stimulating electrodes (8 � 4 cm carbon rubber elec-trodes: Diamond Athletics, Winnipeg Manitoba, Canada) wasplaced anteriorly over the tibial plateau. The optimal positioningof the electrodes over the tibial nerve to obtain the highest ampli-tude H-reflex was manipulated at the beginning of each sessionwith a probe electrode. Once this position was located, a surfaceelectrode (1-cm silver/silver chloride; MediTrace 133, Kendall,Technical products Toronto, Ontario, Canada) was taped in placeand secured with an elastic bandage. Electrodes were connectedto a high-voltage constant-current stimulator (Stimulator ModelDS7H+; Digitimer, Welwyn Garden City, Hertfordshire, UK). Theamperage (10–1000 mA) of a single square-wave pulse lasting200 ls was progressively increased until the maximum H-reflexand M-wave amplitude were achieved, and the correspondingintensities were retained. This procedure was repeated at each testsession.

Fig. 2. Photo of the boot apparatus with simulated tapotement massage.

Please cite this article in press as: Behm DG et al. Massage and stretching reducElectromyogr Kinesiol (2013), http://dx.doi.org/10.1016/j.jelekin.2013.05.002

2.5. H-reflex and M-wave recordings

The skin surface was prepared by shaving the zone, cleaningwith alcohol and removing dead epithelial cells with abrasivesandpaper. Two EMG surface electrodes (1-cm silver/silver chlo-ride; MediTrace 133, Kendall, Technical products Toronto, Ontario,Canada) with an inter-electrode distance of 2 cm were placed onthe midline of the soleus directly below the gastrocnemius–soleusintersection. The reference electrode was placed on the lateralmalleolus. EMG activity was sampled at 2000 Hz, filtered with aBlackman 61 dB band-pass filter between 10 and 500 Hz, amplified(bi-polar differential amplifier, input impedance of 2 MX, commonmode rejection ratio of 110 dB min (50/60 Hz), gain X 1000, noiseof ±5 V), and analog to digitally (A/D) converted (12 bit) (BiopacSystems Inc., DA 150: analog–digital converter MP150WSW; Holl-iston, Massachusetts) and stored on a personal computer for fur-ther analysis. The A/D unit was interfaced with the stimulatorproviding a consistent trigger to the stimulator. Off-line analysesincluded maximum H-reflex and M-wave amplitude (peak to peakamplitude from the positive to the negative voltage deflections),from which the H/M ratio was calculated.

2.6. Twitch contractile properties recordings

Plantar flexor torque was recorded by the boot apparatusequipped with strain gauge (Omega Engineering Inc. LCCA 250,Don Mills Ontario, Canada) amplified (Biopac Systems Inc., DA150: analog–digital converter MP150WSW; Holliston, Massachu-setts) and monitored online. Data were recorded at a sampling rateof 2000 Hz, and analyzed with a commercially designed softwareprogram (AcqKnowledge 3.0, Biopac Systems Inc.). Off-line analy-ses included peak twitch torque (highest amplitude), time to peaktwitch torque (duration from twitch onset to peak torque), HRT(duration from peak torque to half peak torque value), and EMD(duration from the onset of the M-wave to the onset of the twitchresponse).

2.7. Statistical analysis

We used a 2-way repeated measures ANOVA (5 � 7) with fiveconditions (MTJ, MTJ with stretch, tapotement, tapotement withstretch and control) and seven testing times (pre-intervention,15 s, 30 s, 45 s, 60 s of intervention, post-intervention 1 min andpost-intervention 2 min) as factors (SPSS 17.0 for Windows Inc.,Chicago, IL). If significant main effects of interactions were de-tected, Bonferroni-adjusted pairwise comparisons were imple-mented. Differences were considered significant at p < 0.05. Alldata are reported as mean ± SD. Reliability was calculated fromthe pre-test measures using an intraclass correlation coefficient(ICC). Standard error of the means (SEM) was also reported.

3. Results

3.1. H-reflex/M-wave (H/M) ratio

There were significant interactions with all experimental condi-tions demonstrating significantly (p < 0.0001) lower H/M ratioscompared to control at the 15 and 30 s intervention time points.In addition, both tapotement conditions (with and without stretch)had lower H/M ratios than both MTJ massage conditions (with andwithout stretch) at the 15 (p < 0.003) and 30 s (p < 0.006) timepoints. Both tapotement conditions had significantly lower H/M ra-tios than control at the 45 (p < 0.0001) and 60 s (p < 0.0001) inter-vention time point as well as the 1 min post-intervention timepoint (p = 0.02). Furthermore, at the 45 (p = 0.001) and 60 s

e spinal reflex excitability without affecting twitch contractile properties. J

Fig. 3. H-reflex/M-wave ratios. ⁄All conditions reduced significantly compared with Control; � reduced significantly compared with MTJ and MTJ-CONT; � reducedsignificantly compared with Control; – reduced significantly compared with all conditions. Mean and standard deviations are reported in the table to minimize clutter in thefigure. Acronyms: MTJ: musculotendinous junction, TAP: tapotement.

4 D.G. Behm et al. / Journal of Electromyography and Kinesiology xxx (2013) xxx–xxx

(p = 0.002) intervention time points, the tapotement with stretchcondition H/M ratio was significantly lower than both MTJ massage(with and without stretch) conditions as well as the tapotementwithout stretch condition. MTJ massage with stretch conditionexhibited lower H/M ratios than control at 45 (p < 0.0001) and60 s (p < 0.0001) intervention time points. Finally at the 2 minpost-intervention time point, tapotement with stretch had signifi-cantly (p = 0.03) lower H/M ratio than the control condition (Fig. 3).

3.2. Twitch contractile properties

There were no significant main effects or condition x time inter-action for peak twitch torque, time to peak torque, HRT and M-wave amplitude. At the 15 s intervention time point, MTJ withstretch had a significantly (p = 0.01) longer EMD duration than allother conditions. Furthermore at the 30 s time point, MTJ withstretch and tapotement with stretch EMD durations were signifi-cantly (p = 0.02) longer than MTJ control, tapotement control andcontrol conditions. Similarly, at the 60 s intervention time point,MTJ with stretch EMD duration was significantly (p = 0.03) longerthan MTJ control, tapotement control and control conditions,whereas tapotement with stretch exceeded MTJ control andtapotement control (p = 0.04). There were no significant EMD dif-ferences at 1 min post-interventions, whereas at 2 min post-inter-vention the control condition significantly (p = 0.02) exceeded TAPwith stretch condition (Fig. 4).

3.3. Reliability

The ICCs provided reliability coefficients of 0.94 (Mean:6.66 mV, 95%CI: 6.28–6.98 ± 0.82 SEM) for the H-reflex amplitude,0.86 (Mean: 28.75 ms, 95%CI: 27.1–30.4 ± 1.24 SEM) for EMD, 0.99(Mean: 29.2 N, 95%CI: 23.4–36.02 ± 4.24 SEM) for evoked twitchforce and 0.98 (Mean 0.51, 95%CI 0.45–0.57 ± 0.13 SEM) for theH/M ratios.

4. Discussion

The most important findings in the present study were that (1)a combination of massage (both tapotement and MTJ) and SS af-fected spinal reflex excitability (as witnessed by the decline in H/

Please cite this article in press as: Behm DG et al. Massage and stretching reducElectromyogr Kinesiol (2013), http://dx.doi.org/10.1016/j.jelekin.2013.05.002

M ratio), (2) tapotement massage conditions with or withoutstretch provided greater H-reflex depression than both MTJ mas-sage conditions, and (3) the addition of SS to either massage condi-tion increased the duration of the EMD during the implementationof the stretch.

Both massage techniques with and without SS attenuated theH/M ratio indicating that spinal reflex excitability (Trimble andEnoka, 1991) was reduced (likely because of decreased alpha-motoneuron excitability and/or increased presynaptic inhibition).A number of studies have reported H-reflex inhibition withstretching (Avela et al., 1999, Etnyre et al., 2005, Guissard et al.,1988, 2001) as well as massage (Goldberg et al., 1992; Sullivanet al., 1991). However, this is the first study to demonstrate theseparate and combined effects of massage on stretched versus re-laxed muscle. In Sullivan et al. study (1991), the H-reflex of petris-sage massaged triceps surae decreased approximately 43%compared to the control condition. Goldberg et al., (1992) foundthat light and deep petrissage decreased H-reflex amplitude by39% and 49% respectively. In the present study, compared to con-trol conditions, tapotement control and tapotement with stretchH/M ratios decreased 81% and 90% as compared to 54% and 60%for MTJ control and MTJ with stretch respectively. Compared tothe aforementioned petrissage studies (39–49% H-reflex depres-sion), the possibility of relatively greater inhibition with MTJ mas-sage (54–60% H/M ratio depression) may be attributed to thestimulation of the Golgi tendon organs promoting an additionalautogenic inhibitory influence. Huang et al. (2010) hypothesizedthat the increased ROM with MTJ massage might be partiallyattributed to Golgi tendon organ inhibition. Khan and Burne(2009) reported a powerful passive stretch-induced autogenicinhibition of the plantar flexors from group I tendon afferents. Theyfound that inhibition was greater with electrical stimulation at theMTJ versus muscle locations more distal to that site. Similar find-ings from the same laboratory (Burne and Lippold, 1996) usinghand muscles also demonstrated a profound reflex inhibition withelectrical stimulation over the tendons indicating a Golgi tendonorgan afferent inhibition.

Both tapotement massage conditions had significantly greaterH/M ratio decreases (81–90%) than MTJ massage (54–60%). Thereare no other studies that have examined the effect of tapotementmassage on H-reflex suppression. As tapotement is a vigorous per-cussive action, it may enable a deeper penetration into the muscle

e spinal reflex excitability without affecting twitch contractile properties. J

Fig. 4. Electromechanical Delay (EMD). ⁄Increased significantly compared with all conditions; � Increased significantly compared with MTJ-CONT, Control, TAP-CONT; �

Increased significantly compared with MTJ-CONT, TAP-CONT; – increased significantly compared with MTJ, TAP, TAP-CONT; § increased significantly compared with TAP.Mean and standard deviations are reported in the table to minimize clutter in the figure. Acronyms: MTJ: musculotendinous junction, TAP: tapotement.

D.G. Behm et al. / Journal of Electromyography and Kinesiology xxx (2013) xxx–xxx 5

and provide greater inhibition of the muscle spindles than with theless forceful effleurage actions. It has been documented for decadesthat muscle vibration can depress H-reflexes. Degail et al. (1966)reported H-reflex depression in the triceps surae with musclevibration. Whole-body vibration has also been shown to depresssoleus H-reflex activity (Sayenko et al., 2010). Vibration-inducedH-reflex inhibition of the gastrocnemius and soleus were reportedto be related to the amplitude of the vibration (Martin et al., 1986).Vibration-induced reductions in the H-reflex have been reported tobe due to presynaptic inhibition of the Ia afferents (Lapole et al.,2012). It has been suggested that petrissage massage may involvereflex inhibition from pressure sensitive receptors, cutaneous andmuscle mechanoreceptors (Goldberg et al., 1992) as well as pre-synaptic inhibition of Ia afferents (Sullivan et al., 1991). Thus, thevigorous manual percussion massage (tapotement) on the plantarflexors, which could be considered a hybrid of massage and vibra-tion provided a greater inhibitory effect than the less forceful MTJmassage.

Following the cessation of tapotement and MTJ massage, thestretched plantar flexors exhibited a considerable reduction ofthe H/M ratios (compared to control), respectively by 69% and49%. SS of the soleus in other studies has been shown to reduceH-reflex amplitude by 44% (Avela et al., 1999), 41% (Guissardet al., 1988) and 25% (Guissard et al., 2001). Even stretching dispa-rate muscles such as increasing the ROM of the hip flexors can de-press the soleus H-reflex by as much as 50% of control values(Knikou and Rymer, 2003). Similar effects have been reported withchronic SS, since a 36% decline of H-reflex amplitude has been doc-umented following 30 sessions of SS training (Guissard and Ducha-teau, 2004). The origin of such reflex depression might be relatedto presynaptic inhibition of Ia afferents by type III and IV muscleafferents (Gandevia and McKenzi, 1988; Garland and Kaufman,1995), but Avela et al. (1999) countered that it is more likely dueto a disfacilitation of, or reduction in the muscle spindles’ afferentdischarge. Fig. 2 illustrates that SS alone (45 and 60 s measures) didnot provide as much reflex inhibition as the combination of SS andmassage (15 and 30 s measures). These results suggest that thecombination of massage and stretch provides either a higher inten-sity of inhibitory influence (i.e. greater presynaptic inhibition) or agreater collection of inhibitory inputs (i.e. presynaptic inhibition

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by pressure sensitive receptors, cutaneous and muscle mechanore-ceptors, Ib afferent inhibition by Golgi tendon organs and disfacil-itation of muscle spindle discharge activity).

Similar to other published SS studies (Guissard et al., 1988,2001), the SS-induced H-reflex depression during and 30 s follow-ing MTJ massage recovered rapidly once the stretching ceased.However, the reflex inhibition with SS during and for the 30 s fol-lowing tapotement massage continued at least for 2 min after theintervention. In addition, the extent of reflex suppression was sub-stantially greater when SS continued following tapotement (69%)versus MTJ (49%). Thus, the tapotement massage contributed to agreater depression of and a more prolonged SS-induced reflexdepression. Vibration studies report that H-reflex amplitude canfully recover after 60 s of ankle flexor (Vanboxtel, 1986) andwhole-body vibration (Sayenko et al., 2010) exposure. Hence, inthe present study a combination of SS and tapotement massageprovided a prolonged and greater depression of spinal reflex excit-ability than MTJ with and without SS. The 2 min of depressedspinal reflex excitability may aid individuals when stretching aparticularly stiff muscle.

EMD was generally prolonged when massage was combinedwith stretch. MTJ with stretch had 6%, 9% and 6% longer EMD dura-tions than control at the 15 and 30 s massage and stretch interven-tion time points as well as at the 60 s stretch only interventiontime point respectively. Tapotement with stretch had 7% and 4%longer EMD durations than control at the 30 s massage and stretchintervention time point and 60 s stretch only intervention timepoints respectively. Since tapotement and MTJ without stretch(a) did not elicit prolonged EMD durations compared to control,(b) were shorter duration than both massage with stretch condi-tions and (c) showed no significant differences between massagetypes, the prolonged EMD can be attributed to the increasedROM. EMD is influenced by a number of factors including: serieselastic components, ability of the action potential to propagate,and excitation–contraction coupling (Howatson, 2010). Zhouet al. (1998) indicated that the major portion of the EMD was theduration required to stretch the series elastic components of themuscle–tendon unit (Cavanagh and Komi, 1979). Elongation ofEMD is believed to be due to mechanical stress placed on the mus-cle and increased passive tension on non-contractile structures

e spinal reflex excitability without affecting twitch contractile properties. J

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(Morgan and Proske, 2004). With no significant change in EMD(representative of compliance in the musculotendinous unit), withmassage only conditions, it would be logical to assume that in-creases in ROM seen in previous massage studies (Huang et al.,2010; McKechnie et al., 2007) would be more likely attributableto reflex inhibition. Whereas reflex inhibition has also been re-ported for the increase in ankle dorsiflexion ROM with SS (Avelaet al., 1999), increases in compliance as seen in the present studydifferentiate SS ROM increases from massage.

McKechnie et al. (2007) reported an increased ankle ROM withpetrissage massage with no deleterious effect on subsequent dropjump power measures. This finding is in opposition to the commonfinding of SS-induced performance decrements in strength, power,reaction time, balance and other measures (Behm and Chaouachi,2011). The insignificant effects of massage (MTJ and tapotement)on EMD (series elastic component compliance) and twitch contrac-tile properties (muscle force and temporal characteristics) mayhelp preserve subsequent performance capabilities while promot-ing increased ROM through reduced spinal reflex excitability. Onthe other hand, there might be a small possibility that reducedspinal excitability could delay reflex responses when stretchingvigorously leading to injury.

5. Conclusions

Combining massage and SS can reduce spinal reflex excitability(H/M ratio) without significantly affecting twitch contractile prop-erties. Greater depression of the H/M ratio was achieved withtapotement compared to MTJ massage conditions. SS increasedthe duration of the EMD whereas massage had no effect on thisproperty. Although ROM was not measured in the present research,previous accounts of increased ROM with massage may be morelikely attributed to reflex inhibition whereas SS-induced increasesin ROM may be related to both neural and mechanical factors. Acombination of massage and SS is recommended to augment thesuppression of muscle reflex excitability, with SS also increasingmuscle compliance to provide a more optimal environment forimproving ROM.

As we did not measure changes in ROM in the present study wecannot precisely elucidate the precise extent of clinical relevance.However, this study was based on our previous study by Huanget al. (2010), which showed 7% increases in ROM with 30 s of MTJmassage. The tapotement massage in the present study providedeven greater spinal reflex suppression than MTJ massage and thusit would be expected that similar or greater increases in ROM wouldbe attained with tapotement massage. These massage techniquesmay be employed immediately before stretching in an attempt torelax the muscle in an attempt to optimize the stretching effects.

6. Funding

This research was partially funded by the Holistic Health Re-search Foundation of Canada and the Natural Science and Engi-neering Research Council of Canada.

7. Conflict of Interest

There were no perceived conflicts of interest with any of theauthors of this article.

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Dr. David Behm is the Associate Dean for GraduateStudies and Research in the School of Human Kineticsand Recreation at the Memorial University of New-foundland. David’s research portfolio includes over 120articles published in peer-reviewed scientific journalsthat have been cited approximately 4000 times. Hisresearch focus has been to investigate neuromuscularresponses and adaptations to resistance training, insta-bility, stretching and other activities. David integrateshis theoretical work with a background as a competitiveathlete and coach in a variety of sport such as football(drafted in Canadian Football League), hockey (Canadianjunior hockey), baseball, tennis (provincial champion),squash (provincial champion) and others.

Ms. Ashley Peach was a graduate student in Kinesiologyat Memorial University and is currently pursuing aMasters of Occupational Therapy at McMaster Univer-sity. Ashley’s current research interests are varied as sheworks to develop her research portfolio. Ashley haspublished 2 articles in peer-reviewed scientific journalsand is currently working on another research project.Ashley’s interest in exercise physiology stemmed fromher experience as competitive athlete; she was a stu-dent-athlete in rowing at Michigan State Universityfrom 2006–2009.

Ms. Meaghan Maddigan is a Graduate Student andsessional instructor in the School of Human Kinetics andRecreation at the Memorial University of Newfound-land. Meaghan’s research portfolio includes 3 publishedarticles and 5 abstracts and conference communica-tions. Her research focus is training and ways toimprove exercise performance and adherence, investi-gation into neuromuscular responses and adaptations toresistance training, and stretching. Meaghan has abackground in competitive athletics and coaching in avariety of sports but her main passion is Softball, shewas a member of the two time Ontario Championshipwinning Western University Softball Team from 2006–2010.

Please cite this article in press as: Behm DG et al. Massage and stretching reducElectromyogr Kinesiol (2013), http://dx.doi.org/10.1016/j.jelekin.2013.05.002

Saied Jalal Aboodarda is a Ph.D. Degree holder andcurrently employed as a postdoctoral fellow in School ofHuman Kinetics and Recreation at Memorial Universityof Newfoundland, Canada. His main research interestsare Exercise Physiology, Neuromuscular Adaptations,and Sports Performance.

Mario Di Santo has been teaching at the University ofCordoba since 1989. His specific field is stretching andflexibility. He is also an associate researcher of theSchool of Human Kinetics & Recreation of MemorialUniversity of Newfoundland, Canada. Publicationsinclude two books and several articles in flexibility.

Dr. Button’s research mainly focuses on exercise neu-roscience. He has published both applied and basicresearch on how the nervous system responds to acuteand chronic activity or lack thereof. Dr. Button is also aCanadian Society for Exercise Physiology CertifiedExercise Physiologist.

Nicola A. Maffiuletti was born in Bergamo, Italy, in1973. He received the Ph.D. degree in Sport Science in2000 from the University of Burgundy in Dijon, France.He has been an Assistant Professor in the same Uni-versity (INSERM U887 Laboratory) since 2001, and iscurrently Director of the Neuromuscular Research Lab-oratory at the Schulthess Clinic in Zurich, Switzerland.His current research interests include the study ofneuromuscular function in orthopaedic patients and thephysiology of neuromuscular electrical stimulation. Heis a member of the European College of Sport Science.

e spinal reflex excitability without affecting twitch contractile properties. J