clinical study the effect of neuromuscular electrical stimulation...

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Hindawi Publishing Corporation BioMed Research International Volume 2013, Article ID 802534, 9 pages http://dx.doi.org/10.1155/2013/802534 Clinical Study The Effect of NeuroMuscular Electrical Stimulation on Quadriceps Strength and Knee Function in Professional Soccer Players: Return to Sport after ACL Reconstruction J. Taradaj, 1,2 T. Halski, 3 M. Kucharzewski, 4 K. Walewicz, 1 A. Smykla, 1 M. Ozon, 1 L. Slupska, 3,5 R. Dymarek, 3,6 K. Ptaszkowski, 3,7 J. Rajfur, 3 and M. Pasternok 3 1 Department of Physiotherapy Basics, Academy of Physical Education in Katowice, Mikolowska Street 72, 40-065 Katowice, Poland 2 Department of Medical Biophysics, Medical University of Silesia in Katowice, Medykow Street 18, 40-752 Katowice, Poland 3 Department of Physiotherapy, Public Higher Professional Medical School in Opole, Katowicka Street 68, 40-060 Opole, Poland 4 Department of Descriptive and Topographic Anatomy, Medical University of Silesia in Zabrze, Jordana Street 19, 41-808 Zabrze, Poland 5 Department of Physiotherapy, University of Medicine in Wroclaw, Grunwaldzka Street 2, 50-355 Wrocław, Poland 6 Department of Nervous System Diseases, University of Medicine in Wroclaw, Bartla Street 5, 51-618 Wrocław, Poland 7 Department of Gynecology and Obstetrics, University of Medicine in Wroclaw, Bartla Street 5, 51-618 Wrocław, Poland Correspondence should be addressed to J. Taradaj; [email protected] Received 8 September 2013; Revised 9 October 2013; Accepted 13 November 2013 Academic Editor: Brad J. Schoenfeld Copyright © 2013 J. Taradaj et al. is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. e aim of this study was to assess the clinical efficacy and safety of NMES program applied in male soccer players (aſter ACL reconstruction) on the quadriceps muscle. e 80 participants (NMES = 40, control = 40) received an exercise program, including three sessions weekly. e individuals in NMES group additionally received neuromuscular electrical stimulation procedures on both right and leſt quadriceps (biphasic symmetric rectangular pulses, frequency of impulses: 2500 Hz, and train of pulses frequency: 50 Hz) three times daily (3 hours of break between treatments), 3 days a week, for one month. e tensometry, muscle circumference, and goniometry pendulum test (follow-up aſter 1 and 3 months) were applied. e results of this study show that NMES (in presented parameters in experiment) is useful for strengthening the quadriceps muscle in soccer athletes. ere is an evidence of the benefit of the NMES in restoring quadriceps muscle mass and strength of soccer players. In our study the neuromuscular electrical stimulation appeared to be safe for biomechanics of knee joint. e pathological changes in knee function were not observed. is trial is registered with Australian and New Zealand Clinical Trials Registry ACTRN12613001168741. 1. Introduction One key goal of successful anterior cruciate ligament (ACL) reconstruction is return to sports. Athletes who sustain ACL tears require successful reconstruction in order to continue participating in cutting and pivoting sports. e two most commonly reported treatment options for ACL injuries in sport is surgical operation and physical therapy management [1]. Quadriceps muscle weakness aſter anterior cruciate lig- ament (ACL) reconstruction is a serious problem, but the mechanisms underlying these chronic strength deficits are not clear. For example, Krishnan and Williams [2] examined quadriceps strength in people 2–15 years aſter ACL recon- struction and tested the hypothesis that chronic quadriceps weakness is related to levels of voluntary quadriceps muscle activation, antagonistic hamstrings moment, and peripheral changes in muscle. Knee extensor strength and activation were evaluated in 15 ACL reconstructed and 15 matched uninjured control subjects using an interpolated triplet tech- nique. Electrically evoked contractile properties were used to evaluate peripheral adaptations in the quadriceps muscle.

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Page 1: Clinical Study The Effect of NeuroMuscular Electrical Stimulation …downloads.hindawi.com/journals/bmri/2013/802534.pdf · 2019. 7. 31. · (ii) single-leg plyometrics, cutting/pivoting

Hindawi Publishing CorporationBioMed Research InternationalVolume 2013 Article ID 802534 9 pageshttpdxdoiorg1011552013802534

Clinical StudyThe Effect of NeuroMuscular Electrical Stimulation onQuadriceps Strength and Knee Function in Professional SoccerPlayers Return to Sport after ACL Reconstruction

J Taradaj12 T Halski3 M Kucharzewski4 K Walewicz1 A Smykla1 M Ozon1

L Slupska35 R Dymarek36 K Ptaszkowski37 J Rajfur3 and M Pasternok3

1 Department of Physiotherapy Basics Academy of Physical Education in Katowice Mikolowska Street 7240-065 Katowice Poland

2Department of Medical Biophysics Medical University of Silesia in Katowice Medykow Street 18 40-752 Katowice Poland3Department of Physiotherapy Public Higher Professional Medical School in Opole Katowicka Street 68 40-060 Opole Poland4Department of Descriptive and Topographic Anatomy Medical University of Silesia in Zabrze Jordana Street 1941-808 Zabrze Poland

5Department of Physiotherapy University of Medicine in Wroclaw Grunwaldzka Street 2 50-355 Wrocław Poland6Department of Nervous System Diseases University of Medicine in Wroclaw Bartla Street 5 51-618 Wrocław Poland7Department of Gynecology and Obstetrics University of Medicine in Wroclaw Bartla Street 5 51-618 Wrocław Poland

Correspondence should be addressed to J Taradaj jtaradajawfkatowicepl

Received 8 September 2013 Revised 9 October 2013 Accepted 13 November 2013

Academic Editor Brad J Schoenfeld

Copyright copy 2013 J Taradaj et alThis is an open access article distributed under the Creative CommonsAttribution License whichpermits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

The aim of this study was to assess the clinical efficacy and safety of NMES program applied in male soccer players (after ACLreconstruction) on the quadriceps muscle The 80 participants (NMES = 40 control = 40) received an exercise program includingthree sessions weekly The individuals in NMES group additionally received neuromuscular electrical stimulation procedureson both right and left quadriceps (biphasic symmetric rectangular pulses frequency of impulses 2500Hz and train of pulsesfrequency 50Hz) three times daily (3 hours of break between treatments) 3 days a week for one month The tensometry musclecircumference and goniometry pendulum test (follow-up after 1 and 3 months) were applied The results of this study show thatNMES (in presented parameters in experiment) is useful for strengthening the quadriceps muscle in soccer athletes There isan evidence of the benefit of the NMES in restoring quadriceps muscle mass and strength of soccer players In our study theneuromuscular electrical stimulation appeared to be safe for biomechanics of knee jointThe pathological changes in knee functionwere not observed This trial is registered with Australian and New Zealand Clinical Trials Registry ACTRN12613001168741

1 Introduction

One key goal of successful anterior cruciate ligament (ACL)reconstruction is return to sports Athletes who sustain ACLtears require successful reconstruction in order to continueparticipating in cutting and pivoting sports The two mostcommonly reported treatment options for ACL injuries insport is surgical operation and physical therapy management[1]

Quadriceps muscle weakness after anterior cruciate lig-ament (ACL) reconstruction is a serious problem but the

mechanisms underlying these chronic strength deficits arenot clear For example Krishnan and Williams [2] examinedquadriceps strength in people 2ndash15 years after ACL recon-struction and tested the hypothesis that chronic quadricepsweakness is related to levels of voluntary quadriceps muscleactivation antagonistic hamstrings moment and peripheralchanges in muscle Knee extensor strength and activationwere evaluated in 15 ACL reconstructed and 15 matcheduninjured control subjects using an interpolated triplet tech-nique Electrically evoked contractile properties were usedto evaluate peripheral adaptations in the quadriceps muscle

2 BioMed Research International

Antagonistic hamstrings moments were predicted using apractical mathematical model Knee extensor strength andevoked torque at rest were significantly lower in the recon-structed legs (Plt 005) Voluntary activation and antagonistichamstrings activity were similar across legs and betweengroups (P gt 005) Regression analyzes indicated that side-to-side differences in evoked torque at rest explained 71 of theknee extensor strength differences by side (P lt 0001)

Adams et al [3] noticed that quadriceps strength deficitis significant after ACL injury ranging from 15 to 40(followup was obtained 502 patients at a mean of 141years postoperatively) Regression analysis showed that themost statistically significant factor related to lower subjectivescores was lack of normal knee extension and loss of normalflexion

Neuromuscular electrical stimulation (NMES) is theapplication of electrical current to elicit a muscle contractionand seems to be helpful for strengthening the musclesUse of NMES for orthopedic and neurologic rehabilitationhas grown significantly in recent years and seems to bedocumented [1 4ndash7]

The neurophysiologic principles on which the treatmentis based have been studied in animal and human subjectsA nerve action potential may be elicited by a ldquocommandrdquooriginating in the motor cortex of the brain or by anelectrically induced stimulus at the periphery In eithercase the mechanism of action potential propagation andrelease of synaptic transmitter substance is the same Afundamental difference between the twomechanisms and theresultant muscle contraction exists in the recruitment orderof individual motor units [7]

During a voluntary muscle contraction smaller motorunits composed primarily of type I (slow twitch fibers)fatigue-resistant fibers tend to be recruited first Differentmotor units are recruited asynchronously As some are relax-ing others are contracting and constant tension of themuscleis maintained During electrical stimulation such as NMES(especially for 50ndash70Hz frequencies) composed primarily oftype II (fast twitch fibers) readily fatigable fibers are recruitedfirst because their (larger diameter) motor nerves have lowthresholds to electrical excitation [8 9] Motor units ofsimilar thresholds lying superficially beneath the stimulatingelectrodes will be recruited simultaneously As they begin tofatigue tension in the muscle will begin to decrease unlessthe intensity of the stimulus is increased recruiting additionalmotor unitswith higher thresholds orwith similar thresholdsbut more remote locations [9] Excessive fatigue can beminimized during electrically induced muscle contractionby limiting the frequency at which the stimulus is appliedand the duration of the contraction Adequate rest periodsbetween contractions will increase the likelihood that subse-quent muscle contractions will be sufficiently strong In theliterature there are lots of theories (historical and modern)on mechanism of generating the action potential and musclenerve conducting electronic propagation Hodgkin-Huxleytheory patch claim technique or theory of channel activation[9 10]

The goal of improving human performance in sport andexercise has been an extremely interesting topic for coaches

athletic trainers physical therapists exercise physiologistsand athletes alike Unfortunately the utility of the NMESfor sport application still remains controversial For exam-ple while many research studies find muscle strength andrecovery after physical effort significantly improved byNMES[3 4 11ndash14] a few do not [8 15 16] It is also unclear whetherthe NMES is completely safe Some authors maintain thatNMES could induce muscle damage or influence on functionand biomechanics of the near articulations of the stimulatedmuscles [17]

Bax et al [18] presented a systematic review andmetaanalysis of randomized controlled trials to determinewhether NMES is an effective modality for strength aug-mentation of the quadriceps femoris A full content searchfor randomized controlled trials was performed in MedlineEmbase Cinahl the Cochrane Controlled Trials RegisterFand the PhysicalTherapy EvidenceDatabase Onlymaximumvolitional isometric or isokinetic muscle torque in Nm wasused as main outcome measure and final conclusions areunclear Authors stated that further research should bedirected toward identifying the clinical impact at activity andparticipation levels and the optimal stimulation parametersof this modality Well-prepared and documented prospec-tive controlled studies are needed

The objective of this study was to assess the efficacy andsafety of NMES program applied in soccer players (after ACLreconstruction) on the quadricepsmuscleThe primary studyendpoint was a comparison of the change in muscle strengthbetween the stimulated and control groups The secondaryend point was the analysis between groups of the changeof quadriceps muscle circumference and other measuredparameters as predictors of safety (whether there are anypathological changes in knee function) after NMES therapy

2 Materials and Methods

All participants provided informed consent to this projectthat was approved by the Local Institutional Review Boardof theMedical University of Silesia in Katowice Poland Trialis registered in Australian and New Zealand Clinical TrialsRegistry (ACTRN12613001168741)

21 Participants and Randomization The 80 professionalmale soccer players (The Soccer Academymdashten soccer clubsfrom 2nd and 3rd Polish League) participated in experimentsto measure the clinical effectiveness and safety of electricalstimulation Participating subjects met the following inclu-sion criteria

(1) They underwent arthroscopy surgery as follows ini-tially an anteromedial incision was made on the proximaltibia and the gracilis and semitendinosus tendons weredetached from their insertions on tibia Subsequently thetendons were removed to fashion the graft for ACL recon-struction A tibial canal was established through this canalthe femoral canal was created under arthroscopy guideFinally the graft was passed through the canals as a singlebundle

(2) They spent 6 months after operation

BioMed Research International 3

(3) They received the same rehabilitation program beforeNMES procedures week 1 (CPM Machinemdashstart at 0ndash30degrees and increase with not less than 10 degrees per dayPROM Wall Slides Seated Active Assistive Knee FlexionProne Dangle Passive resting extension with heel propPatellar Mobilizations SLR x3 Flexion Adduction Abduc-tion HamstringCalf Stretches Ankle Pumps Gait TrainingHome Exercise Program-2 or 3 times per day) Week 2ndash4 (Scar MobilizationMassage Proprioceptive Neuromus-cular Facilitation Progressive Resistive Exercises Man-ualMachine resisted leg press BalanceProprioception Iso-metric Knee extension 90ndash60∘ Stationary Bike Minisquatsprogress up to 90∘ Step ups Retro TreadmillStairmasterHip abductionexternal rotation) and week 4ndash16 (FunctionalStrengthening Proprioceptive Neuromuscular FacilitationProgressive Resistive Exercises ManualMachine resisted legpress BalanceProprioception Squats to 90 degrees Singleleg squats Step ups Retro TreadmillStairmaster and ReviewHome Exercise Program 2 times per day) Week 16ndash24(Continue strength endurance proprioception progressionBegin double-leg hopping jogging and agility drills)

(4) They provided written informed consent to partici-pate in the study

Subjects with the following conditions were not allowedto participate or were excluded from the study

(1) women(2) soccer practice for less than 3 years (share of the

league for at least three years)(3) bone fracture in the last 2 years(4) chronic sprain ankle(5) a history of Achilles tendon injuryParticipants were randomly allocated to the groups

Computer-generated random numbers were sealed insequentially numbered envelopes and the group allocationwas independent of the time and person delivering thetreatment The physician (research coordinator) whoallocated the subjects to groups had 80 envelopes eachcontaining a piece of paper marked with either group A(NMES) or B (control) The physician would select andopen an envelope in the presence of a physiotherapist tosee the symbol and would then direct the patient to thecorresponding group Another physiotherapist collected thedata and coded them into an Excel database The ldquoblindedrdquoresults were transferred to a Statistica version 100 databaseby a technician The research coordinator had no contactwith and could not identify the soccer players

22 Procedures All participants received an exercise pro-gram including three sessions (Mondays Wednesdays andFridays) weekly for one month

(i) double-leg hopping jogging agility drills and freerunning

(ii) single-leg plyometrics cuttingpivoting drills withstutter step pattern high intensity aerobicanaerobicsport specific training and advanced lower extremitystrengthening

I

T

Figure 1 NMES impulse shape and characteristics Legends Basefrequency 2500Hz burst frequency 50Hz on 10ms off 10msincreasingdecreasing ramp shape

(iii) triple hop for distance single hop for distance lateralhop 1210158401015840 times 1210158401015840 squares separated by 1210158401015840 of hops (inbox) and unilateral vertical jump

Weight training exercise in the gym was prohibitedThe individuals in group A additionally received neu-

romuscular electrical stimulation procedures on both rightand left quadriceps (two electrodes on themuscle attachmentsites) A portable electrical stimulator (Ionoson PhysiomedGermany) delivered biphasic symmetric rectangular pulses(frequency of impulses 2500Hz train of pulses frequency50Hz) The stimulus output is interrupted every 10ms tocreate ldquoburstsrdquo of stimulation every second The 10ms offperiodwas not detectable by the subject A total of 10maximalcontractions sustained for 10 seconds each with a 50 secondoff time defined a treatment session (according to methodol-ogy of stimulation prepared by Yakov Kots in year 1989 [10]mdashcalled in literature ldquoRussian stimulationrdquo and recognized asone of the types of the NMESmdashFigure 1) The intensity wasbetween 55 and 67mA (mean of 5889mA) Stimulation wasperformed with a current which produced strong visiblemotion effects Electrodes were made of conductive carbonrubber (8 times 6 cm) Before application of electrodes the skinwas cleaned by use of alcohol The total time of singleprocedure was 30 minutes Quadriceps was stimulated at 60∘of knee flexion The procedures were repeated three timesdaily (3 hours of break between treatments) 3 days a week(Tuesdays Thursdays and Saturdays) for one month

23 Measures Measurements of muscle strength were per-formed by a tensometer (Accuro Sumer Poland) The ten-someter was composed of resistance lever roller and elec-tronic momentum meter (Figure 2) The spectrum of mea-surement was between 0 and 500 Newton meters (Nm) Themagnitudes of force moment were converted into Newtons(N) The tested legs were at 60∘ of knee flexion (we observedmaximal strength of muscle when individuals were preparedto the measurements)

Change of muscle circumference was measured by aldquotailor taperdquo 10 cm above the patella on the quadriceps The

4 BioMed Research International

Figure 2 Tensometry

measurements were performed before and after experiment(the measurements were in a supine position before the firstand after the last NMES procedure)

The goniometry pendulum test was composed of aperipheral device and a personal computer with softwareTheperipheral device consisted of a goniometry compass and aninterface system-transducer cooperated with the computerThe goniometry compass was composed of two thin metalarms (Figures 3(a) and 3(b)) One of the arms (immobile) wasfixed in a special outlet that allowed changing the angle andlengthThemobile armwas connected to the athletersquos legThemotion of the compasswasmeasured by aminioptoelectronictransducer The position of the transducer was measured(with a resolution of 12 bytes (B) on one revolution) andcoded in a range from 0∘ to 360∘ (exact to 0088∘) Thesignal was transmitted to the interface The software allowedreadings of 100 positions of the compass per second

Using the pendulum test the spectrum (range) and easeof motion in knee (whether the movement was smoothphysiological and free in examined axis) were measured anddetermined by the following parameters

119899 number of oscillations119905 whole time of oscillations119879 period of oscillations (119879 = 119905119899)120582 logarithmdecrement of suppression (120582 = ln119883

21198834

where 1198832is a second amplitude during oscillations

and1198834is a fourth amplitude during oscillations

120573 suppression index (120573 = 120582119879)

The number of oscillations (119899) and whole time of oscil-lations (119905) described the ease of knee motion The periodof oscillations (119879) and suppression parameters (120582 and 120573)assessed the spectrum of knee motion (Figure 4) Thegoniometry pendulum test was performed for analysis ofNMES safety (to assess whether an increase in muscle massand strength will change in the mechanics of the knee joint)

24 Follow-Up The goniometry pendulum test was repeated1 and 3 months after the study (79 athletes were measured infollowup and only one participant fromgroupBwas excludedbecause of femoral neck fracture) The following procedure

was performed for analysis of electrical stimulation safety inlong term results

25 Statistical Analysis The chi-squared independence test(greatest reliability level) and parametric 119905-test were usedfor analysis of indicators which characterized individualsin both comparative groups The normal distribution waschecked by Shapiro-Wilk (for the null hypothesis that asample came from a normally distributed population) andthe chi-squared test (when the null hypothesis was true alsoconsider that a chi-squared test is a test in which this isasymptotically true meaning that the sampling distribution-if the null hypothesis is true can be made to approximate achi-squared distribution as closely as desired by making thesample size large enough) Recalling that the null hypothesisis that the population is normally distributed if the 119875-valueis less than the chosen alpha level then the null hypothesisis rejected (ie one concludes that the data are not from anormally distributed population)

If the 119875-value is greater than the chosen alpha levelthen one does not reject the null hypothesis that the datacame from a normally distributed population (according tostatistical estimation the population over 30ndash35 is needed forfurther analysis of normal distribution so we had to includeabout 80 participants in two groups in this study and use theparametric tests) Analyzed distributions appeared normaland we received the Gauss decay in all comparisons

The parameters before and after study were comparedin groups by parametric 119905-test (for dependent variables)Differences in parameters between groups were evaluatedwith 119905-test (for the independent variables) for comparisonsof experimental and follow-up results we used analysis ofvariance ANOVA to analyze the differences between groupmeans and their associated procedures (such as ldquovaria-tionrdquo among and between groups) In ANOVA setting theobserved variance in a particular variable is partitioned intocomponents attributable to different sources of variation

Two-sided 119875 values of less than 005 were considered tobe statistically significant

3 Results

The groups studied were homogeneous in terms of allparticipant characteristics (Table 1) and initial muscle powerand knee biomechanical parameters After experiment thestrength of quadriceps on the operated side in group A(NMES) increased from 6459 to 8934N (287 119875 = 0001)and in group B (control) it increased from 6486 to only6698N (46 119875 = 004) The comparison after 1-monththerapy of relative changes of the muscle strength betweenboth groups showed a significant difference in favor of stim-ulation (287 versus 46 119875 = 0002 and 95 confidenceinterval) The strength of quadriceps on nonoperated side ingroup A increased from 8401 to 10898N (301 119875 = 0003)and in group B increased from 8404 to only 8852N (46119875 = 004) The comparison after 1-month therapy of relativechanges of the muscle strength between both groups showed

BioMed Research International 5

(a) (b)

Figure 3 (a) and (b) are Goniometry pendulum test

Figure 4 Exampled data from pendulum test (sinusoidal wave ofpendulum movement) Legends (lambda) 120582 logarithm decrementof suppression (beta)120573 suppression index (Okreswahan)119879 periodof oscillations (Liczba wahan) 119899 number of oscillations (Czaswahan) 119905 whole time of oscillations

a significant difference in favor of stimulation (301 versus46 119875 = 0002 and 95 confidence interval)

In NMES group on the operated side quadriceps circum-ference increased from 565 to 579 cm (14 119875 = 003) andin group B it increased from 562 to 571 cm (06 119875 = 005)The comparison after amonth of treatment of relative changesof the muscle circumference between both groups showeda significant difference in favor of stimulation (14 versus06 119875 = 004 and 95 confidence interval) On the non-operated side quadriceps circumference increased from 581to 593 cm (11119875 = 003) and in group B increased from 577to 582 cm (04 119875 = 004) The comparison after a monthtreatment of relative changes of the muscle circumferencebetween both groups showed a significant difference in favorof NMES (11 versus 04 119875 = 004 and 95 confidenceinterval)

The comparison of all parameters measured usinggoniometry pendulum test in group A and B did not indicateany significant difference and also in the followup (after 1 and3 months after the end of study)mdashTables 2 and 3

4 Discussion

The results of this study showed that NMES is effective formuscle training in sport (we observed intensive increaseof power and mass of quadriceps muscle after one monththerapy) which corresponds with some research studiesHowever experiments in the literature are usually basedon small number of participants unclear randomization(researchers do not use validated methods of randomizationsuch as a computer or marked envelopes only physiciandecides the allocation of participants) lack of inclusion andexclusion criteria and no assessment of the safety of NMESapplication in sport [11 13 14 19]

Paillard et al [11] in their study observed the effectsof different types of NMES programs on vertical jumpperformance Twenty-seven healthy trained male students insports-sciences were recruited and randomized into threegroups The control group (C group 119899 = 8) did notperform NMES training Two other groups underwent 3training sessions a week for over 5 weeks on the quadricepsfemoris musclemdashF group (119899 = 9) stimulation with an80Hz current for 15min for improving muscle strength Egroup (119899 = 10) stimulation with a 25Hz current for 60minfor improving muscle endurance The height of the verticaljump was measured before NMES training (test 1) and oneweek (test 2) and five weeks (test 3) after the end of theprograms The results showed that the height of the verticaljump significantly increased in both the F and E groupsbetween tests 1 and 2 (5 cm and 3 cm resp) Results of test3 showed that both groups preserved their gains In authorsopinion aNMES training program improvesmuscle strength

British researchers [19] observed prolonged NMES insedentary adults Fifteen healthy subjects (10 men 5 women)with a sedentary lifestyle completed a 6-week training pro-gram during which they completed an average of 29 1-hourof NMES sessions The form NMES used by the subjects wascapable of eliciting a cardiovascular exercise responsewithoutloading the limbs or joints It achieved this bymeans of induc-ing rapid rhythmical contractions in the large leg musclesA crossover study design was employed with subjects under-going their habitual activity levels during the nontraining

6 BioMed Research International

Table 1 Characteristics of individuals from group A and B

Group A Group B Level ofsignificance

Number ofparticipants 40 40 lowastlowast

119875 gt 005

Age (years)Range 17ndash29 17ndash29

lowast

119875 gt 005Mean 224 213SD 578 567

Operated kneeRight 26 23

lowastlowast

119875 gt 005

Left 14 17Height (cm)

Range 171ndash193 170ndash186lowast

119875 gt 005Mean 1803 1765SD 754 811

Weight (kg)Range 71ndash80 63ndash100

lowast

119875 gt 005Mean 738 709SD 576 712

BMI (kgm2)Range 192ndash258 203ndash289

lowast

119875 gt 005Mean 224 234SD 422 303

Muscle strength(N)

Operated 5784ndash7013 5675ndash6899

lowastlowast

119875 gt 005

Range 6459 6486Mean 346 386SD

NonoperatedRange 8214ndash8798 8315ndash8897Mean 8401 8404SD 234 279

Duration of career(how long soccerplayers practicetheir discipline) inyears

Range 34ndash105 33ndash85lowast

119875 gt 005Mean 54 48SD 246 189

lowastthe 119905-test lowastlowastthe 1205942-test

phase of the studyThe training effect was evaluated bymeansof a treadmill test to determine peak aerobic capacity peakoxygen consumption Vo

2 a 6-minutes walking distance test

and measurement of body mass index (BMI) and quadricepsmuscle strength At baseline the mean values for peak Vo

2

6-min walking distance quadriceps strength and BMI were

246 lmin 4933m 3608N and 269 kgm2 respectivelyAfter training subjects demonstrated statistically significantimprovements in all variables except BMI PeakVo

2increased

by an average of 024 lmin (119875 lt 005) walking distanceincreased by 366m (119875 lt 0005) and quadriceps strengthincreased by 875N (119875 lt 0005) These results suggest thatNMES can be used in sedentary adults to improve musclestrength

Snyder-Mackler et al [13] included 85 patients to treatwith highintensity NMES high-level volitional exercise low-intensity NMES or combined high and lowintensity NMESAll treatment was performed isometrically with the knee in65 degrees of flexion All of the patients participated in anintensive programof closed-kinetic-chain exercise After fourweeks of treatment the strength of the quadriceps femorismuscle and the kinematics of the knee during stance phasewere measured Quadriceps strength averaged 70 or moreof the strength on the uninvolved side in the two groupsthat were treated with high-intensity NMES (either aloneor combined with low-intensity NMES) 57 in the groupthat was treated with high-level volitional exercise and 5in the group that was treated with low-intensity NMES Thekinematics of the knee joint were directly and significantly(119875 lt 005) correlated with the strength of the quadriceps

Other researchers [14] presented 27 healthy subjects(mean age 234 years) volunteered for the study and wererandomly assigned to 1 of 3 groups control group (noNMES)group 2 (NMES 2 times per week) and group 3 (NMES3 times per week) Groups 2 and 3 received NMES (10minutes per session) over a 4-week period for a total of 8and 12 NMES training sessions respectively The isometricquadriceps femoris muscle force produced during NMESwas monitored during each treatment minute The force ofthe quadriceps femoris was assessed prior to the first weekand at the start of weeks 2 3 and 4 of the 4-week trainingprogram with a final measurement after the fourth week (5total measurements) for all subjects Only the mean percentchange in quadriceps power before and after the 4 weeks oftraining with NMES between the control group and group 3was significantly different (119875 = 0021)

In our research we studied motion and function param-eters in knee without analysis of inflammatory reaction orquadriceps muscle damage

A review of the literature can be found to have onlyone article about muscle pathologies after NMES applicationVanderthommen et al [17] studied the effects on musclefunction of an electrical stimulation bout applied unilaterallyon thigh muscles in healthy male volunteers One group(ES group 119899 = 10) received consecutively 100 isometriccontractions of quadriceps and 100 isometric contractions ofhamstrings (on-off ratio 6-6 s) induced by neuromuscularelectrical stimulations (NMES) Changes in muscle torquemuscle soreness (VAS) muscle stiffness and serum creatinekinase (CK) activity were assessed before the NMES exercise(preex) as well as 24 h 48 h and 120 h after the bout Asecond group (control group 119899 = 10) was submitted tothe same test battery as the stimulation group and with thesame time-frame The between group comparison indicateda significant increase in VAS scores and in serum levels of CK

BioMed Research International 7

Table 2 Goniometry pendulum test in group A

Parameter Before therapy After therapyFollowup

Level of significance1 month 3 monthsMean SD Mean SD Mean SD Mean SD

120582

Operated 057 019 056 016 055 020 055 022 119875 gt 005

Nonoperated 047 018 045 019 046 022 046 022 lowast(in all comparisons)120573 [sminus1]

Operated 077 030 077 028 074 022 075 030 119875 gt 005

Non-operated 057 030 056 031 053 023 054 030 lowast(in all comparisons)119879 [s]

Operated 089 030 094 030 095 027 093 030 119875 gt 005

Non-operated 095 022 099 019 099 019 098 021 lowast(in all comparisons)119899

Operated 332 122 332 143 331 121 332 125 119875 gt 005

Non-operated 478 122 487 145 486 121 487 121 lowast(in all comparisons)119905 [s]

Operated 207 122 207 152 212 110 213 121 119875 gt 005

Non-operated 304 120 304 145 301 113 301 113 lowast(in all comparisons)lowastAnalysis of variance ANOVALegends120582 logarithm decrement of suppression (more than 065 is pathology of I Outebridge degree of the articular cartilage) 120573 suppression index (more than 085is pathology of I Outebridge degree of the articular cartilage) 119879 period of oscillations (less than 075 is pathology of I Outebridge degree of the articularcartilage) 119899 number of oscillations (less than 300 is pathology of I Outebridge degree of the articular cartilage) and 119905 whole time of oscillations (less than150 is pathology of I Outebridge degree of the articular cartilage)

Table 3 Goniometry pendulum test in group B

Parameter Before therapy After therapyFollowup

Level of significance1 month 3 monthsMean SD Mean SD Mean SD Mean SD

120582

Operated 055 021 058 019 056 022 055 020 119875 gt 005

Nonoperated 048 021 043 019 044 022 045 020 lowast(in all comparisons)120573 [sminus1]

Operated 075 032 076 021 075 022 075 028 119875 gt 005

Non-operated 058 027 057 028 055 025 054 028 lowast(in all comparisons)119879 [s]

Operated 087 034 090 035 090 029 090 030 119875 gt 005

Non-operated 095 019 097 019 097 019 099 020 lowast(in all comparisons)119899

Operated 335 131 333 138 333 130 333 130 119875 gt 005

Non-operated 475 131 479 139 480 141 480 141 lowast(in all comparisons)119905 [s]

Operated 211 103 209 104 210 111 211 101 119875 gt 005

Non-operated 310 128 311 125 311 111 310 109 lowast(in all comparisons)lowastAnalysis of variance ANOVALegends120582 logarithm decrement of suppression (more than 065 is pathology of I Outebridge degree of the articular cartilage) 120573 suppression index (more than 085is pathology of I Outebridge degree of the articular cartilage) 119879 period of oscillations (less than 075 is pathology of I Outebridge degree of the articularcartilage) 119899 number of oscillations (less than 300 is pathology of I Outebridge degree of the articular cartilage) and 119905 whole time of oscillations (less than150 is pathology of I Outebridge degree of the articular cartilage)

8 BioMed Research International

only in the ES group In the ES group changes were morepronounced in hamstrings than in quadriceps and peakedat 48 h (quadriceps VAS scores = 220 plusmn 1 (0 at preex)hamstrings VAS scores = 315 plusmn 214 (0 at preex) hip flexionangle = 62 plusmn 5∘ (75 plusmn 6∘ at preex) CK activity = 3021 plusmn2693 IU sdot l minus 1 (136 plusmn 50 IU sdot l minus 1 at preex) The results of thestudy suggested the occurrence of muscle damage that couldhave been induced by the physiologically incorrect musclerecruitment inNMES and the resulting overratedmechanicalstress

In our study the NMES appeared to be safe for biome-chanics of knee joint Based on our previous experience wecan strongly recommend the goniometry pendulum test asuseful diagnostic method in physical therapy process [20]The purpose of this clinical study was to assess low frequencylow intensity magnetic fields in the enhancement of thephysical rehabilitation of patients after knee endoprosthesissurgery The study included 62 patients who underwent totalknee arthroplasty Group A consisted of 32 patients who werephysically rehabilitated Group B consisted of 30 patients whowere physically rehabilitated and treated additionally withpulsing magnetic fields (5mT 30Hz 20min once a day 5days weekly)Therapy lasted for 3 weeks for both groupsTherehabilitation process was evaluated using a goniometer ten-someter goniometry pendulum test Lysholm scale for kneefunction and a visual analogue scale (VAS) questionnaire forpain and activityThe pendulum test appeared very useful forprecise observation of biomechanical changes in knee jointduring therapy process The physical therapy decreased thelogarithm decrement of suppression (120582) by about 79 ingroup A and 96 in group B suppression index (120573) decreasedabout 11 in group A and 133 in group B The period ofoscillations increased by 49 in group A and 4 in group Bnumber of oscillations (119899) increased by 221 in group A and206 in group B The whole time of oscillations increased of298 in group A and 245 in group B

In our study we did not observe both early and longterm results (goniometry pendulum testour research is thefirst attempt in literature of using this apparatus in sport)any pathological changes in knee function after increasingthe strength and mass of quadriceps in use of NMESThe progress in muscle parameters did not have influencepathologically on knee function

41 Limitations of Study In our study soccer players aftera month of therapy with NMES + rehabilitation or onlyrehabilitation program (7 months after ACL reconstruc-tion) returned to sport and league competition what couldinterfere with follow-up observation We were not able todemonstrate a relationship between the pendulum test andmuscle dysfunction either in the study or from previousresearch using a similar protocol correlated with markersof muscle damage We tried to use objective measurementmethods but we did not collect data related to functionaloutcomes of which there are some they could have chosen(triple-hop crossover-hop and jump-landing test)

5 Conclusion

The results of this study show that NMES (presented parame-ters in experiment) is useful for strengthening the quadricepsmuscle in soccer athletes There is an evidence the benefit ofthe NMES in restoring quadriceps muscle mass and strengthof soccer players In our study the neuromuscular electricalstimulation appeared to be safe for biomechanics of kneejoint The pathological changes in knee function were notobserved

Conflict of Interests

The authors would like to certify that they have no commer-cial associations with the manufacturers of the equipmentdescribed in the paper or other conflict of interests

References

[1] S C Petterson R L Mizner J E Stevens et al ldquoImprovedfunction from progressive strengthening interventions aftertotal knee arthroplasty a randomized clinical trial with animbedded prospective cohortrdquo Arthritis Care and Research vol61 no 2 pp 174ndash183 2009

[2] C Krishnan and G N Williams ldquoFactors explaining chronicknee extensor strength deficits after ACL reconstructionrdquo Jour-nal of Orthopaedic Research vol 29 no 5 pp 633ndash640 2011

[3] D Adams D S Logerstedt A Hunter-Giordano M J Axeand L Snyder-Mackler ldquoCurrent concepts for anterior cruciateligament reconstruction a criterion-based rehabilitation pro-gressionrdquo Journal of Orthopaedics and Sports Physical Therapyvol 42 no 7 pp 601ndash614 2012

[4] J E Stevens-Lapsley J E Balter P Wolfe D G Eckhoff andW M Kohrt ldquoEarly neuromuscular electrical stimulation toimprove quadriceps muscle strength after total knee arthro-plasty a randomized controlled trialrdquo Physical Therapy vol 92no 2 pp 210ndash226 2012

[5] G J Yun M H Chun J Y Park and B R Kim ldquoThesynergic effects of mirror therapy and neuromuscular electricalstimulation for hand function in stroke patientsrdquo Annals ofRehabilitation Medicine vol 35 no 3 pp 316ndash322 2011

[6] R J Walls G McHugh D J OrsquoGorman N M Moyna and JM OrsquoByrne ldquoEffects of preoperative neuromuscular electricalstimulation on quadriceps strength and functional recovery intotal knee arthroplasty A pilot studyrdquo BMC MusculoskeletalDisorders vol 14 no 11 article 119 2010

[7] Y Guan P W Wacnik F Yang et al ldquoSpinal cord stimulation-induced analgesia electrical stimulation of dorsal column anddorsal roots attenuates dorsal horn neuronal excitability inneuropathic ratsrdquo Anesthesiology vol 113 no 6 pp 1392ndash14052010

[8] T Arakawa A Katada H Shigyo et al ldquoElectrical stimulationprevents apoptosis in denervated skeletal musclerdquo NeuroReha-bilitation vol 27 no 2 pp 147ndash154 2010

[9] M R Gersh Electrotherapy in Rehabilitation ContemporaryPerspectives in Rehabilitation (Book 7) FA Davis CompanyPhiladelphia Pa USA 1994

[10] J H Kim M L Trew A J Pullan and O Rohrle ldquoSimulatinga dual-array electrode configuration to investigate the influence

BioMed Research International 9

of skeletal muscle fatigue following functional electrical stim-ulationrdquo Computers in Biology and Medicine vol 42 no 9 pp915ndash924 2012

[11] T Paillard F Noe N Bernard P Dupui and C HazardldquoEffects of two types of neuromuscular electrical stimulationtraining on vertical jump performancerdquo Journal of Strength andConditioning Research vol 22 no 4 pp 1273ndash1278 2008

[12] I Vivodtzev R Debigare P Gagnon et al ldquoFunctional andmuscular effects of neuromuscular electrical stimulation inpatients with severe COPD a randomized clinical trialrdquo Chestvol 141 no 3 pp 716ndash725 2012

[13] L Snyder-Mackler A Delitto S L Bailey and S W StralkaldquoStrength of the quadriceps femoris muscle and functionalrecovery after reconstruction of the anterior cruciate ligamentA prospective randomized clinical trial of electrical stimula-tionrdquo Journal of Bone and Joint Surgery A vol 77 no 8 pp 1166ndash1173 1995

[14] M G Parker M J Bennett M A Hieb A C Hollar and A ARoe ldquoStrength response in human quadriceps femoris muscleduring 2 neuromuscular electrical stimulation programsrdquo Jour-nal of Orthopaedic and Sports Physical Therapy vol 33 no 12pp 719ndash726 2003

[15] J W Bellew Z Beiswanger E Freeman C Gaerte and JTrafton ldquoInterferential and burst-modulated biphasic pulsedcurrents yield greater muscular force than Russian currentrdquoPhysiotherapy Theory and Practice vol 28 no 5 pp 384ndash3902012

[16] A Mysliwiec E Saulicz M Kuszewski M Kokosz and TWolny ldquoAssessment of the influence of Saunders tractionand transcutaneous electrical nerve stimulation on hand gripforce in patients with neck painrdquo Ortopedia TraumatologiaRehabilitacja vol 13 no 1 pp 37ndash44 2011

[17] M Vanderthommen M Triffaux Ch Demoulin J MCrielaard and J L Croisier ldquoAlteration of muscle functionafter electrical stimulation bout of knee extensors and flexorsrdquoJournal of Sports Science andMedicine vol 11 pp 592ndash599 2012

[18] L Bax F Staes and A Verhagen ldquoDoes neuromuscular electri-cal stimulation strengthen the quadriceps femoris A systematicreview of randomised controlled trialsrdquo SportsMedicine vol 35no 3 pp 191ndash212 2005

[19] P Banerjee B Caulfield L Crowe and A Clark ldquoProlongedelectrical muscle stimulation exercise improves strength andaerobic capacity in healthy sedentary adultsrdquo Journal of AppliedPhysiology vol 99 no 6 pp 2307ndash2311 2005

[20] E Błaszczak A Franek J Taradaj JWiduchowski and J Klim-czak ldquoAssessment of the efficacy and safety of low frequencylow intensity magnetic fields in patients after knee endopros-thesis plasty Part 2 a clinical studyrdquo Bioelectromagnetics vol30 no 2 pp 152ndash158 2009

Submit your manuscripts athttpwwwhindawicom

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Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 2: Clinical Study The Effect of NeuroMuscular Electrical Stimulation …downloads.hindawi.com/journals/bmri/2013/802534.pdf · 2019. 7. 31. · (ii) single-leg plyometrics, cutting/pivoting

2 BioMed Research International

Antagonistic hamstrings moments were predicted using apractical mathematical model Knee extensor strength andevoked torque at rest were significantly lower in the recon-structed legs (Plt 005) Voluntary activation and antagonistichamstrings activity were similar across legs and betweengroups (P gt 005) Regression analyzes indicated that side-to-side differences in evoked torque at rest explained 71 of theknee extensor strength differences by side (P lt 0001)

Adams et al [3] noticed that quadriceps strength deficitis significant after ACL injury ranging from 15 to 40(followup was obtained 502 patients at a mean of 141years postoperatively) Regression analysis showed that themost statistically significant factor related to lower subjectivescores was lack of normal knee extension and loss of normalflexion

Neuromuscular electrical stimulation (NMES) is theapplication of electrical current to elicit a muscle contractionand seems to be helpful for strengthening the musclesUse of NMES for orthopedic and neurologic rehabilitationhas grown significantly in recent years and seems to bedocumented [1 4ndash7]

The neurophysiologic principles on which the treatmentis based have been studied in animal and human subjectsA nerve action potential may be elicited by a ldquocommandrdquooriginating in the motor cortex of the brain or by anelectrically induced stimulus at the periphery In eithercase the mechanism of action potential propagation andrelease of synaptic transmitter substance is the same Afundamental difference between the twomechanisms and theresultant muscle contraction exists in the recruitment orderof individual motor units [7]

During a voluntary muscle contraction smaller motorunits composed primarily of type I (slow twitch fibers)fatigue-resistant fibers tend to be recruited first Differentmotor units are recruited asynchronously As some are relax-ing others are contracting and constant tension of themuscleis maintained During electrical stimulation such as NMES(especially for 50ndash70Hz frequencies) composed primarily oftype II (fast twitch fibers) readily fatigable fibers are recruitedfirst because their (larger diameter) motor nerves have lowthresholds to electrical excitation [8 9] Motor units ofsimilar thresholds lying superficially beneath the stimulatingelectrodes will be recruited simultaneously As they begin tofatigue tension in the muscle will begin to decrease unlessthe intensity of the stimulus is increased recruiting additionalmotor unitswith higher thresholds orwith similar thresholdsbut more remote locations [9] Excessive fatigue can beminimized during electrically induced muscle contractionby limiting the frequency at which the stimulus is appliedand the duration of the contraction Adequate rest periodsbetween contractions will increase the likelihood that subse-quent muscle contractions will be sufficiently strong In theliterature there are lots of theories (historical and modern)on mechanism of generating the action potential and musclenerve conducting electronic propagation Hodgkin-Huxleytheory patch claim technique or theory of channel activation[9 10]

The goal of improving human performance in sport andexercise has been an extremely interesting topic for coaches

athletic trainers physical therapists exercise physiologistsand athletes alike Unfortunately the utility of the NMESfor sport application still remains controversial For exam-ple while many research studies find muscle strength andrecovery after physical effort significantly improved byNMES[3 4 11ndash14] a few do not [8 15 16] It is also unclear whetherthe NMES is completely safe Some authors maintain thatNMES could induce muscle damage or influence on functionand biomechanics of the near articulations of the stimulatedmuscles [17]

Bax et al [18] presented a systematic review andmetaanalysis of randomized controlled trials to determinewhether NMES is an effective modality for strength aug-mentation of the quadriceps femoris A full content searchfor randomized controlled trials was performed in MedlineEmbase Cinahl the Cochrane Controlled Trials RegisterFand the PhysicalTherapy EvidenceDatabase Onlymaximumvolitional isometric or isokinetic muscle torque in Nm wasused as main outcome measure and final conclusions areunclear Authors stated that further research should bedirected toward identifying the clinical impact at activity andparticipation levels and the optimal stimulation parametersof this modality Well-prepared and documented prospec-tive controlled studies are needed

The objective of this study was to assess the efficacy andsafety of NMES program applied in soccer players (after ACLreconstruction) on the quadricepsmuscleThe primary studyendpoint was a comparison of the change in muscle strengthbetween the stimulated and control groups The secondaryend point was the analysis between groups of the changeof quadriceps muscle circumference and other measuredparameters as predictors of safety (whether there are anypathological changes in knee function) after NMES therapy

2 Materials and Methods

All participants provided informed consent to this projectthat was approved by the Local Institutional Review Boardof theMedical University of Silesia in Katowice Poland Trialis registered in Australian and New Zealand Clinical TrialsRegistry (ACTRN12613001168741)

21 Participants and Randomization The 80 professionalmale soccer players (The Soccer Academymdashten soccer clubsfrom 2nd and 3rd Polish League) participated in experimentsto measure the clinical effectiveness and safety of electricalstimulation Participating subjects met the following inclu-sion criteria

(1) They underwent arthroscopy surgery as follows ini-tially an anteromedial incision was made on the proximaltibia and the gracilis and semitendinosus tendons weredetached from their insertions on tibia Subsequently thetendons were removed to fashion the graft for ACL recon-struction A tibial canal was established through this canalthe femoral canal was created under arthroscopy guideFinally the graft was passed through the canals as a singlebundle

(2) They spent 6 months after operation

BioMed Research International 3

(3) They received the same rehabilitation program beforeNMES procedures week 1 (CPM Machinemdashstart at 0ndash30degrees and increase with not less than 10 degrees per dayPROM Wall Slides Seated Active Assistive Knee FlexionProne Dangle Passive resting extension with heel propPatellar Mobilizations SLR x3 Flexion Adduction Abduc-tion HamstringCalf Stretches Ankle Pumps Gait TrainingHome Exercise Program-2 or 3 times per day) Week 2ndash4 (Scar MobilizationMassage Proprioceptive Neuromus-cular Facilitation Progressive Resistive Exercises Man-ualMachine resisted leg press BalanceProprioception Iso-metric Knee extension 90ndash60∘ Stationary Bike Minisquatsprogress up to 90∘ Step ups Retro TreadmillStairmasterHip abductionexternal rotation) and week 4ndash16 (FunctionalStrengthening Proprioceptive Neuromuscular FacilitationProgressive Resistive Exercises ManualMachine resisted legpress BalanceProprioception Squats to 90 degrees Singleleg squats Step ups Retro TreadmillStairmaster and ReviewHome Exercise Program 2 times per day) Week 16ndash24(Continue strength endurance proprioception progressionBegin double-leg hopping jogging and agility drills)

(4) They provided written informed consent to partici-pate in the study

Subjects with the following conditions were not allowedto participate or were excluded from the study

(1) women(2) soccer practice for less than 3 years (share of the

league for at least three years)(3) bone fracture in the last 2 years(4) chronic sprain ankle(5) a history of Achilles tendon injuryParticipants were randomly allocated to the groups

Computer-generated random numbers were sealed insequentially numbered envelopes and the group allocationwas independent of the time and person delivering thetreatment The physician (research coordinator) whoallocated the subjects to groups had 80 envelopes eachcontaining a piece of paper marked with either group A(NMES) or B (control) The physician would select andopen an envelope in the presence of a physiotherapist tosee the symbol and would then direct the patient to thecorresponding group Another physiotherapist collected thedata and coded them into an Excel database The ldquoblindedrdquoresults were transferred to a Statistica version 100 databaseby a technician The research coordinator had no contactwith and could not identify the soccer players

22 Procedures All participants received an exercise pro-gram including three sessions (Mondays Wednesdays andFridays) weekly for one month

(i) double-leg hopping jogging agility drills and freerunning

(ii) single-leg plyometrics cuttingpivoting drills withstutter step pattern high intensity aerobicanaerobicsport specific training and advanced lower extremitystrengthening

I

T

Figure 1 NMES impulse shape and characteristics Legends Basefrequency 2500Hz burst frequency 50Hz on 10ms off 10msincreasingdecreasing ramp shape

(iii) triple hop for distance single hop for distance lateralhop 1210158401015840 times 1210158401015840 squares separated by 1210158401015840 of hops (inbox) and unilateral vertical jump

Weight training exercise in the gym was prohibitedThe individuals in group A additionally received neu-

romuscular electrical stimulation procedures on both rightand left quadriceps (two electrodes on themuscle attachmentsites) A portable electrical stimulator (Ionoson PhysiomedGermany) delivered biphasic symmetric rectangular pulses(frequency of impulses 2500Hz train of pulses frequency50Hz) The stimulus output is interrupted every 10ms tocreate ldquoburstsrdquo of stimulation every second The 10ms offperiodwas not detectable by the subject A total of 10maximalcontractions sustained for 10 seconds each with a 50 secondoff time defined a treatment session (according to methodol-ogy of stimulation prepared by Yakov Kots in year 1989 [10]mdashcalled in literature ldquoRussian stimulationrdquo and recognized asone of the types of the NMESmdashFigure 1) The intensity wasbetween 55 and 67mA (mean of 5889mA) Stimulation wasperformed with a current which produced strong visiblemotion effects Electrodes were made of conductive carbonrubber (8 times 6 cm) Before application of electrodes the skinwas cleaned by use of alcohol The total time of singleprocedure was 30 minutes Quadriceps was stimulated at 60∘of knee flexion The procedures were repeated three timesdaily (3 hours of break between treatments) 3 days a week(Tuesdays Thursdays and Saturdays) for one month

23 Measures Measurements of muscle strength were per-formed by a tensometer (Accuro Sumer Poland) The ten-someter was composed of resistance lever roller and elec-tronic momentum meter (Figure 2) The spectrum of mea-surement was between 0 and 500 Newton meters (Nm) Themagnitudes of force moment were converted into Newtons(N) The tested legs were at 60∘ of knee flexion (we observedmaximal strength of muscle when individuals were preparedto the measurements)

Change of muscle circumference was measured by aldquotailor taperdquo 10 cm above the patella on the quadriceps The

4 BioMed Research International

Figure 2 Tensometry

measurements were performed before and after experiment(the measurements were in a supine position before the firstand after the last NMES procedure)

The goniometry pendulum test was composed of aperipheral device and a personal computer with softwareTheperipheral device consisted of a goniometry compass and aninterface system-transducer cooperated with the computerThe goniometry compass was composed of two thin metalarms (Figures 3(a) and 3(b)) One of the arms (immobile) wasfixed in a special outlet that allowed changing the angle andlengthThemobile armwas connected to the athletersquos legThemotion of the compasswasmeasured by aminioptoelectronictransducer The position of the transducer was measured(with a resolution of 12 bytes (B) on one revolution) andcoded in a range from 0∘ to 360∘ (exact to 0088∘) Thesignal was transmitted to the interface The software allowedreadings of 100 positions of the compass per second

Using the pendulum test the spectrum (range) and easeof motion in knee (whether the movement was smoothphysiological and free in examined axis) were measured anddetermined by the following parameters

119899 number of oscillations119905 whole time of oscillations119879 period of oscillations (119879 = 119905119899)120582 logarithmdecrement of suppression (120582 = ln119883

21198834

where 1198832is a second amplitude during oscillations

and1198834is a fourth amplitude during oscillations

120573 suppression index (120573 = 120582119879)

The number of oscillations (119899) and whole time of oscil-lations (119905) described the ease of knee motion The periodof oscillations (119879) and suppression parameters (120582 and 120573)assessed the spectrum of knee motion (Figure 4) Thegoniometry pendulum test was performed for analysis ofNMES safety (to assess whether an increase in muscle massand strength will change in the mechanics of the knee joint)

24 Follow-Up The goniometry pendulum test was repeated1 and 3 months after the study (79 athletes were measured infollowup and only one participant fromgroupBwas excludedbecause of femoral neck fracture) The following procedure

was performed for analysis of electrical stimulation safety inlong term results

25 Statistical Analysis The chi-squared independence test(greatest reliability level) and parametric 119905-test were usedfor analysis of indicators which characterized individualsin both comparative groups The normal distribution waschecked by Shapiro-Wilk (for the null hypothesis that asample came from a normally distributed population) andthe chi-squared test (when the null hypothesis was true alsoconsider that a chi-squared test is a test in which this isasymptotically true meaning that the sampling distribution-if the null hypothesis is true can be made to approximate achi-squared distribution as closely as desired by making thesample size large enough) Recalling that the null hypothesisis that the population is normally distributed if the 119875-valueis less than the chosen alpha level then the null hypothesisis rejected (ie one concludes that the data are not from anormally distributed population)

If the 119875-value is greater than the chosen alpha levelthen one does not reject the null hypothesis that the datacame from a normally distributed population (according tostatistical estimation the population over 30ndash35 is needed forfurther analysis of normal distribution so we had to includeabout 80 participants in two groups in this study and use theparametric tests) Analyzed distributions appeared normaland we received the Gauss decay in all comparisons

The parameters before and after study were comparedin groups by parametric 119905-test (for dependent variables)Differences in parameters between groups were evaluatedwith 119905-test (for the independent variables) for comparisonsof experimental and follow-up results we used analysis ofvariance ANOVA to analyze the differences between groupmeans and their associated procedures (such as ldquovaria-tionrdquo among and between groups) In ANOVA setting theobserved variance in a particular variable is partitioned intocomponents attributable to different sources of variation

Two-sided 119875 values of less than 005 were considered tobe statistically significant

3 Results

The groups studied were homogeneous in terms of allparticipant characteristics (Table 1) and initial muscle powerand knee biomechanical parameters After experiment thestrength of quadriceps on the operated side in group A(NMES) increased from 6459 to 8934N (287 119875 = 0001)and in group B (control) it increased from 6486 to only6698N (46 119875 = 004) The comparison after 1-monththerapy of relative changes of the muscle strength betweenboth groups showed a significant difference in favor of stim-ulation (287 versus 46 119875 = 0002 and 95 confidenceinterval) The strength of quadriceps on nonoperated side ingroup A increased from 8401 to 10898N (301 119875 = 0003)and in group B increased from 8404 to only 8852N (46119875 = 004) The comparison after 1-month therapy of relativechanges of the muscle strength between both groups showed

BioMed Research International 5

(a) (b)

Figure 3 (a) and (b) are Goniometry pendulum test

Figure 4 Exampled data from pendulum test (sinusoidal wave ofpendulum movement) Legends (lambda) 120582 logarithm decrementof suppression (beta)120573 suppression index (Okreswahan)119879 periodof oscillations (Liczba wahan) 119899 number of oscillations (Czaswahan) 119905 whole time of oscillations

a significant difference in favor of stimulation (301 versus46 119875 = 0002 and 95 confidence interval)

In NMES group on the operated side quadriceps circum-ference increased from 565 to 579 cm (14 119875 = 003) andin group B it increased from 562 to 571 cm (06 119875 = 005)The comparison after amonth of treatment of relative changesof the muscle circumference between both groups showeda significant difference in favor of stimulation (14 versus06 119875 = 004 and 95 confidence interval) On the non-operated side quadriceps circumference increased from 581to 593 cm (11119875 = 003) and in group B increased from 577to 582 cm (04 119875 = 004) The comparison after a monthtreatment of relative changes of the muscle circumferencebetween both groups showed a significant difference in favorof NMES (11 versus 04 119875 = 004 and 95 confidenceinterval)

The comparison of all parameters measured usinggoniometry pendulum test in group A and B did not indicateany significant difference and also in the followup (after 1 and3 months after the end of study)mdashTables 2 and 3

4 Discussion

The results of this study showed that NMES is effective formuscle training in sport (we observed intensive increaseof power and mass of quadriceps muscle after one monththerapy) which corresponds with some research studiesHowever experiments in the literature are usually basedon small number of participants unclear randomization(researchers do not use validated methods of randomizationsuch as a computer or marked envelopes only physiciandecides the allocation of participants) lack of inclusion andexclusion criteria and no assessment of the safety of NMESapplication in sport [11 13 14 19]

Paillard et al [11] in their study observed the effectsof different types of NMES programs on vertical jumpperformance Twenty-seven healthy trained male students insports-sciences were recruited and randomized into threegroups The control group (C group 119899 = 8) did notperform NMES training Two other groups underwent 3training sessions a week for over 5 weeks on the quadricepsfemoris musclemdashF group (119899 = 9) stimulation with an80Hz current for 15min for improving muscle strength Egroup (119899 = 10) stimulation with a 25Hz current for 60minfor improving muscle endurance The height of the verticaljump was measured before NMES training (test 1) and oneweek (test 2) and five weeks (test 3) after the end of theprograms The results showed that the height of the verticaljump significantly increased in both the F and E groupsbetween tests 1 and 2 (5 cm and 3 cm resp) Results of test3 showed that both groups preserved their gains In authorsopinion aNMES training program improvesmuscle strength

British researchers [19] observed prolonged NMES insedentary adults Fifteen healthy subjects (10 men 5 women)with a sedentary lifestyle completed a 6-week training pro-gram during which they completed an average of 29 1-hourof NMES sessions The form NMES used by the subjects wascapable of eliciting a cardiovascular exercise responsewithoutloading the limbs or joints It achieved this bymeans of induc-ing rapid rhythmical contractions in the large leg musclesA crossover study design was employed with subjects under-going their habitual activity levels during the nontraining

6 BioMed Research International

Table 1 Characteristics of individuals from group A and B

Group A Group B Level ofsignificance

Number ofparticipants 40 40 lowastlowast

119875 gt 005

Age (years)Range 17ndash29 17ndash29

lowast

119875 gt 005Mean 224 213SD 578 567

Operated kneeRight 26 23

lowastlowast

119875 gt 005

Left 14 17Height (cm)

Range 171ndash193 170ndash186lowast

119875 gt 005Mean 1803 1765SD 754 811

Weight (kg)Range 71ndash80 63ndash100

lowast

119875 gt 005Mean 738 709SD 576 712

BMI (kgm2)Range 192ndash258 203ndash289

lowast

119875 gt 005Mean 224 234SD 422 303

Muscle strength(N)

Operated 5784ndash7013 5675ndash6899

lowastlowast

119875 gt 005

Range 6459 6486Mean 346 386SD

NonoperatedRange 8214ndash8798 8315ndash8897Mean 8401 8404SD 234 279

Duration of career(how long soccerplayers practicetheir discipline) inyears

Range 34ndash105 33ndash85lowast

119875 gt 005Mean 54 48SD 246 189

lowastthe 119905-test lowastlowastthe 1205942-test

phase of the studyThe training effect was evaluated bymeansof a treadmill test to determine peak aerobic capacity peakoxygen consumption Vo

2 a 6-minutes walking distance test

and measurement of body mass index (BMI) and quadricepsmuscle strength At baseline the mean values for peak Vo

2

6-min walking distance quadriceps strength and BMI were

246 lmin 4933m 3608N and 269 kgm2 respectivelyAfter training subjects demonstrated statistically significantimprovements in all variables except BMI PeakVo

2increased

by an average of 024 lmin (119875 lt 005) walking distanceincreased by 366m (119875 lt 0005) and quadriceps strengthincreased by 875N (119875 lt 0005) These results suggest thatNMES can be used in sedentary adults to improve musclestrength

Snyder-Mackler et al [13] included 85 patients to treatwith highintensity NMES high-level volitional exercise low-intensity NMES or combined high and lowintensity NMESAll treatment was performed isometrically with the knee in65 degrees of flexion All of the patients participated in anintensive programof closed-kinetic-chain exercise After fourweeks of treatment the strength of the quadriceps femorismuscle and the kinematics of the knee during stance phasewere measured Quadriceps strength averaged 70 or moreof the strength on the uninvolved side in the two groupsthat were treated with high-intensity NMES (either aloneor combined with low-intensity NMES) 57 in the groupthat was treated with high-level volitional exercise and 5in the group that was treated with low-intensity NMES Thekinematics of the knee joint were directly and significantly(119875 lt 005) correlated with the strength of the quadriceps

Other researchers [14] presented 27 healthy subjects(mean age 234 years) volunteered for the study and wererandomly assigned to 1 of 3 groups control group (noNMES)group 2 (NMES 2 times per week) and group 3 (NMES3 times per week) Groups 2 and 3 received NMES (10minutes per session) over a 4-week period for a total of 8and 12 NMES training sessions respectively The isometricquadriceps femoris muscle force produced during NMESwas monitored during each treatment minute The force ofthe quadriceps femoris was assessed prior to the first weekand at the start of weeks 2 3 and 4 of the 4-week trainingprogram with a final measurement after the fourth week (5total measurements) for all subjects Only the mean percentchange in quadriceps power before and after the 4 weeks oftraining with NMES between the control group and group 3was significantly different (119875 = 0021)

In our research we studied motion and function param-eters in knee without analysis of inflammatory reaction orquadriceps muscle damage

A review of the literature can be found to have onlyone article about muscle pathologies after NMES applicationVanderthommen et al [17] studied the effects on musclefunction of an electrical stimulation bout applied unilaterallyon thigh muscles in healthy male volunteers One group(ES group 119899 = 10) received consecutively 100 isometriccontractions of quadriceps and 100 isometric contractions ofhamstrings (on-off ratio 6-6 s) induced by neuromuscularelectrical stimulations (NMES) Changes in muscle torquemuscle soreness (VAS) muscle stiffness and serum creatinekinase (CK) activity were assessed before the NMES exercise(preex) as well as 24 h 48 h and 120 h after the bout Asecond group (control group 119899 = 10) was submitted tothe same test battery as the stimulation group and with thesame time-frame The between group comparison indicateda significant increase in VAS scores and in serum levels of CK

BioMed Research International 7

Table 2 Goniometry pendulum test in group A

Parameter Before therapy After therapyFollowup

Level of significance1 month 3 monthsMean SD Mean SD Mean SD Mean SD

120582

Operated 057 019 056 016 055 020 055 022 119875 gt 005

Nonoperated 047 018 045 019 046 022 046 022 lowast(in all comparisons)120573 [sminus1]

Operated 077 030 077 028 074 022 075 030 119875 gt 005

Non-operated 057 030 056 031 053 023 054 030 lowast(in all comparisons)119879 [s]

Operated 089 030 094 030 095 027 093 030 119875 gt 005

Non-operated 095 022 099 019 099 019 098 021 lowast(in all comparisons)119899

Operated 332 122 332 143 331 121 332 125 119875 gt 005

Non-operated 478 122 487 145 486 121 487 121 lowast(in all comparisons)119905 [s]

Operated 207 122 207 152 212 110 213 121 119875 gt 005

Non-operated 304 120 304 145 301 113 301 113 lowast(in all comparisons)lowastAnalysis of variance ANOVALegends120582 logarithm decrement of suppression (more than 065 is pathology of I Outebridge degree of the articular cartilage) 120573 suppression index (more than 085is pathology of I Outebridge degree of the articular cartilage) 119879 period of oscillations (less than 075 is pathology of I Outebridge degree of the articularcartilage) 119899 number of oscillations (less than 300 is pathology of I Outebridge degree of the articular cartilage) and 119905 whole time of oscillations (less than150 is pathology of I Outebridge degree of the articular cartilage)

Table 3 Goniometry pendulum test in group B

Parameter Before therapy After therapyFollowup

Level of significance1 month 3 monthsMean SD Mean SD Mean SD Mean SD

120582

Operated 055 021 058 019 056 022 055 020 119875 gt 005

Nonoperated 048 021 043 019 044 022 045 020 lowast(in all comparisons)120573 [sminus1]

Operated 075 032 076 021 075 022 075 028 119875 gt 005

Non-operated 058 027 057 028 055 025 054 028 lowast(in all comparisons)119879 [s]

Operated 087 034 090 035 090 029 090 030 119875 gt 005

Non-operated 095 019 097 019 097 019 099 020 lowast(in all comparisons)119899

Operated 335 131 333 138 333 130 333 130 119875 gt 005

Non-operated 475 131 479 139 480 141 480 141 lowast(in all comparisons)119905 [s]

Operated 211 103 209 104 210 111 211 101 119875 gt 005

Non-operated 310 128 311 125 311 111 310 109 lowast(in all comparisons)lowastAnalysis of variance ANOVALegends120582 logarithm decrement of suppression (more than 065 is pathology of I Outebridge degree of the articular cartilage) 120573 suppression index (more than 085is pathology of I Outebridge degree of the articular cartilage) 119879 period of oscillations (less than 075 is pathology of I Outebridge degree of the articularcartilage) 119899 number of oscillations (less than 300 is pathology of I Outebridge degree of the articular cartilage) and 119905 whole time of oscillations (less than150 is pathology of I Outebridge degree of the articular cartilage)

8 BioMed Research International

only in the ES group In the ES group changes were morepronounced in hamstrings than in quadriceps and peakedat 48 h (quadriceps VAS scores = 220 plusmn 1 (0 at preex)hamstrings VAS scores = 315 plusmn 214 (0 at preex) hip flexionangle = 62 plusmn 5∘ (75 plusmn 6∘ at preex) CK activity = 3021 plusmn2693 IU sdot l minus 1 (136 plusmn 50 IU sdot l minus 1 at preex) The results of thestudy suggested the occurrence of muscle damage that couldhave been induced by the physiologically incorrect musclerecruitment inNMES and the resulting overratedmechanicalstress

In our study the NMES appeared to be safe for biome-chanics of knee joint Based on our previous experience wecan strongly recommend the goniometry pendulum test asuseful diagnostic method in physical therapy process [20]The purpose of this clinical study was to assess low frequencylow intensity magnetic fields in the enhancement of thephysical rehabilitation of patients after knee endoprosthesissurgery The study included 62 patients who underwent totalknee arthroplasty Group A consisted of 32 patients who werephysically rehabilitated Group B consisted of 30 patients whowere physically rehabilitated and treated additionally withpulsing magnetic fields (5mT 30Hz 20min once a day 5days weekly)Therapy lasted for 3 weeks for both groupsTherehabilitation process was evaluated using a goniometer ten-someter goniometry pendulum test Lysholm scale for kneefunction and a visual analogue scale (VAS) questionnaire forpain and activityThe pendulum test appeared very useful forprecise observation of biomechanical changes in knee jointduring therapy process The physical therapy decreased thelogarithm decrement of suppression (120582) by about 79 ingroup A and 96 in group B suppression index (120573) decreasedabout 11 in group A and 133 in group B The period ofoscillations increased by 49 in group A and 4 in group Bnumber of oscillations (119899) increased by 221 in group A and206 in group B The whole time of oscillations increased of298 in group A and 245 in group B

In our study we did not observe both early and longterm results (goniometry pendulum testour research is thefirst attempt in literature of using this apparatus in sport)any pathological changes in knee function after increasingthe strength and mass of quadriceps in use of NMESThe progress in muscle parameters did not have influencepathologically on knee function

41 Limitations of Study In our study soccer players aftera month of therapy with NMES + rehabilitation or onlyrehabilitation program (7 months after ACL reconstruc-tion) returned to sport and league competition what couldinterfere with follow-up observation We were not able todemonstrate a relationship between the pendulum test andmuscle dysfunction either in the study or from previousresearch using a similar protocol correlated with markersof muscle damage We tried to use objective measurementmethods but we did not collect data related to functionaloutcomes of which there are some they could have chosen(triple-hop crossover-hop and jump-landing test)

5 Conclusion

The results of this study show that NMES (presented parame-ters in experiment) is useful for strengthening the quadricepsmuscle in soccer athletes There is an evidence the benefit ofthe NMES in restoring quadriceps muscle mass and strengthof soccer players In our study the neuromuscular electricalstimulation appeared to be safe for biomechanics of kneejoint The pathological changes in knee function were notobserved

Conflict of Interests

The authors would like to certify that they have no commer-cial associations with the manufacturers of the equipmentdescribed in the paper or other conflict of interests

References

[1] S C Petterson R L Mizner J E Stevens et al ldquoImprovedfunction from progressive strengthening interventions aftertotal knee arthroplasty a randomized clinical trial with animbedded prospective cohortrdquo Arthritis Care and Research vol61 no 2 pp 174ndash183 2009

[2] C Krishnan and G N Williams ldquoFactors explaining chronicknee extensor strength deficits after ACL reconstructionrdquo Jour-nal of Orthopaedic Research vol 29 no 5 pp 633ndash640 2011

[3] D Adams D S Logerstedt A Hunter-Giordano M J Axeand L Snyder-Mackler ldquoCurrent concepts for anterior cruciateligament reconstruction a criterion-based rehabilitation pro-gressionrdquo Journal of Orthopaedics and Sports Physical Therapyvol 42 no 7 pp 601ndash614 2012

[4] J E Stevens-Lapsley J E Balter P Wolfe D G Eckhoff andW M Kohrt ldquoEarly neuromuscular electrical stimulation toimprove quadriceps muscle strength after total knee arthro-plasty a randomized controlled trialrdquo Physical Therapy vol 92no 2 pp 210ndash226 2012

[5] G J Yun M H Chun J Y Park and B R Kim ldquoThesynergic effects of mirror therapy and neuromuscular electricalstimulation for hand function in stroke patientsrdquo Annals ofRehabilitation Medicine vol 35 no 3 pp 316ndash322 2011

[6] R J Walls G McHugh D J OrsquoGorman N M Moyna and JM OrsquoByrne ldquoEffects of preoperative neuromuscular electricalstimulation on quadriceps strength and functional recovery intotal knee arthroplasty A pilot studyrdquo BMC MusculoskeletalDisorders vol 14 no 11 article 119 2010

[7] Y Guan P W Wacnik F Yang et al ldquoSpinal cord stimulation-induced analgesia electrical stimulation of dorsal column anddorsal roots attenuates dorsal horn neuronal excitability inneuropathic ratsrdquo Anesthesiology vol 113 no 6 pp 1392ndash14052010

[8] T Arakawa A Katada H Shigyo et al ldquoElectrical stimulationprevents apoptosis in denervated skeletal musclerdquo NeuroReha-bilitation vol 27 no 2 pp 147ndash154 2010

[9] M R Gersh Electrotherapy in Rehabilitation ContemporaryPerspectives in Rehabilitation (Book 7) FA Davis CompanyPhiladelphia Pa USA 1994

[10] J H Kim M L Trew A J Pullan and O Rohrle ldquoSimulatinga dual-array electrode configuration to investigate the influence

BioMed Research International 9

of skeletal muscle fatigue following functional electrical stim-ulationrdquo Computers in Biology and Medicine vol 42 no 9 pp915ndash924 2012

[11] T Paillard F Noe N Bernard P Dupui and C HazardldquoEffects of two types of neuromuscular electrical stimulationtraining on vertical jump performancerdquo Journal of Strength andConditioning Research vol 22 no 4 pp 1273ndash1278 2008

[12] I Vivodtzev R Debigare P Gagnon et al ldquoFunctional andmuscular effects of neuromuscular electrical stimulation inpatients with severe COPD a randomized clinical trialrdquo Chestvol 141 no 3 pp 716ndash725 2012

[13] L Snyder-Mackler A Delitto S L Bailey and S W StralkaldquoStrength of the quadriceps femoris muscle and functionalrecovery after reconstruction of the anterior cruciate ligamentA prospective randomized clinical trial of electrical stimula-tionrdquo Journal of Bone and Joint Surgery A vol 77 no 8 pp 1166ndash1173 1995

[14] M G Parker M J Bennett M A Hieb A C Hollar and A ARoe ldquoStrength response in human quadriceps femoris muscleduring 2 neuromuscular electrical stimulation programsrdquo Jour-nal of Orthopaedic and Sports Physical Therapy vol 33 no 12pp 719ndash726 2003

[15] J W Bellew Z Beiswanger E Freeman C Gaerte and JTrafton ldquoInterferential and burst-modulated biphasic pulsedcurrents yield greater muscular force than Russian currentrdquoPhysiotherapy Theory and Practice vol 28 no 5 pp 384ndash3902012

[16] A Mysliwiec E Saulicz M Kuszewski M Kokosz and TWolny ldquoAssessment of the influence of Saunders tractionand transcutaneous electrical nerve stimulation on hand gripforce in patients with neck painrdquo Ortopedia TraumatologiaRehabilitacja vol 13 no 1 pp 37ndash44 2011

[17] M Vanderthommen M Triffaux Ch Demoulin J MCrielaard and J L Croisier ldquoAlteration of muscle functionafter electrical stimulation bout of knee extensors and flexorsrdquoJournal of Sports Science andMedicine vol 11 pp 592ndash599 2012

[18] L Bax F Staes and A Verhagen ldquoDoes neuromuscular electri-cal stimulation strengthen the quadriceps femoris A systematicreview of randomised controlled trialsrdquo SportsMedicine vol 35no 3 pp 191ndash212 2005

[19] P Banerjee B Caulfield L Crowe and A Clark ldquoProlongedelectrical muscle stimulation exercise improves strength andaerobic capacity in healthy sedentary adultsrdquo Journal of AppliedPhysiology vol 99 no 6 pp 2307ndash2311 2005

[20] E Błaszczak A Franek J Taradaj JWiduchowski and J Klim-czak ldquoAssessment of the efficacy and safety of low frequencylow intensity magnetic fields in patients after knee endopros-thesis plasty Part 2 a clinical studyrdquo Bioelectromagnetics vol30 no 2 pp 152ndash158 2009

Submit your manuscripts athttpwwwhindawicom

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Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 3: Clinical Study The Effect of NeuroMuscular Electrical Stimulation …downloads.hindawi.com/journals/bmri/2013/802534.pdf · 2019. 7. 31. · (ii) single-leg plyometrics, cutting/pivoting

BioMed Research International 3

(3) They received the same rehabilitation program beforeNMES procedures week 1 (CPM Machinemdashstart at 0ndash30degrees and increase with not less than 10 degrees per dayPROM Wall Slides Seated Active Assistive Knee FlexionProne Dangle Passive resting extension with heel propPatellar Mobilizations SLR x3 Flexion Adduction Abduc-tion HamstringCalf Stretches Ankle Pumps Gait TrainingHome Exercise Program-2 or 3 times per day) Week 2ndash4 (Scar MobilizationMassage Proprioceptive Neuromus-cular Facilitation Progressive Resistive Exercises Man-ualMachine resisted leg press BalanceProprioception Iso-metric Knee extension 90ndash60∘ Stationary Bike Minisquatsprogress up to 90∘ Step ups Retro TreadmillStairmasterHip abductionexternal rotation) and week 4ndash16 (FunctionalStrengthening Proprioceptive Neuromuscular FacilitationProgressive Resistive Exercises ManualMachine resisted legpress BalanceProprioception Squats to 90 degrees Singleleg squats Step ups Retro TreadmillStairmaster and ReviewHome Exercise Program 2 times per day) Week 16ndash24(Continue strength endurance proprioception progressionBegin double-leg hopping jogging and agility drills)

(4) They provided written informed consent to partici-pate in the study

Subjects with the following conditions were not allowedto participate or were excluded from the study

(1) women(2) soccer practice for less than 3 years (share of the

league for at least three years)(3) bone fracture in the last 2 years(4) chronic sprain ankle(5) a history of Achilles tendon injuryParticipants were randomly allocated to the groups

Computer-generated random numbers were sealed insequentially numbered envelopes and the group allocationwas independent of the time and person delivering thetreatment The physician (research coordinator) whoallocated the subjects to groups had 80 envelopes eachcontaining a piece of paper marked with either group A(NMES) or B (control) The physician would select andopen an envelope in the presence of a physiotherapist tosee the symbol and would then direct the patient to thecorresponding group Another physiotherapist collected thedata and coded them into an Excel database The ldquoblindedrdquoresults were transferred to a Statistica version 100 databaseby a technician The research coordinator had no contactwith and could not identify the soccer players

22 Procedures All participants received an exercise pro-gram including three sessions (Mondays Wednesdays andFridays) weekly for one month

(i) double-leg hopping jogging agility drills and freerunning

(ii) single-leg plyometrics cuttingpivoting drills withstutter step pattern high intensity aerobicanaerobicsport specific training and advanced lower extremitystrengthening

I

T

Figure 1 NMES impulse shape and characteristics Legends Basefrequency 2500Hz burst frequency 50Hz on 10ms off 10msincreasingdecreasing ramp shape

(iii) triple hop for distance single hop for distance lateralhop 1210158401015840 times 1210158401015840 squares separated by 1210158401015840 of hops (inbox) and unilateral vertical jump

Weight training exercise in the gym was prohibitedThe individuals in group A additionally received neu-

romuscular electrical stimulation procedures on both rightand left quadriceps (two electrodes on themuscle attachmentsites) A portable electrical stimulator (Ionoson PhysiomedGermany) delivered biphasic symmetric rectangular pulses(frequency of impulses 2500Hz train of pulses frequency50Hz) The stimulus output is interrupted every 10ms tocreate ldquoburstsrdquo of stimulation every second The 10ms offperiodwas not detectable by the subject A total of 10maximalcontractions sustained for 10 seconds each with a 50 secondoff time defined a treatment session (according to methodol-ogy of stimulation prepared by Yakov Kots in year 1989 [10]mdashcalled in literature ldquoRussian stimulationrdquo and recognized asone of the types of the NMESmdashFigure 1) The intensity wasbetween 55 and 67mA (mean of 5889mA) Stimulation wasperformed with a current which produced strong visiblemotion effects Electrodes were made of conductive carbonrubber (8 times 6 cm) Before application of electrodes the skinwas cleaned by use of alcohol The total time of singleprocedure was 30 minutes Quadriceps was stimulated at 60∘of knee flexion The procedures were repeated three timesdaily (3 hours of break between treatments) 3 days a week(Tuesdays Thursdays and Saturdays) for one month

23 Measures Measurements of muscle strength were per-formed by a tensometer (Accuro Sumer Poland) The ten-someter was composed of resistance lever roller and elec-tronic momentum meter (Figure 2) The spectrum of mea-surement was between 0 and 500 Newton meters (Nm) Themagnitudes of force moment were converted into Newtons(N) The tested legs were at 60∘ of knee flexion (we observedmaximal strength of muscle when individuals were preparedto the measurements)

Change of muscle circumference was measured by aldquotailor taperdquo 10 cm above the patella on the quadriceps The

4 BioMed Research International

Figure 2 Tensometry

measurements were performed before and after experiment(the measurements were in a supine position before the firstand after the last NMES procedure)

The goniometry pendulum test was composed of aperipheral device and a personal computer with softwareTheperipheral device consisted of a goniometry compass and aninterface system-transducer cooperated with the computerThe goniometry compass was composed of two thin metalarms (Figures 3(a) and 3(b)) One of the arms (immobile) wasfixed in a special outlet that allowed changing the angle andlengthThemobile armwas connected to the athletersquos legThemotion of the compasswasmeasured by aminioptoelectronictransducer The position of the transducer was measured(with a resolution of 12 bytes (B) on one revolution) andcoded in a range from 0∘ to 360∘ (exact to 0088∘) Thesignal was transmitted to the interface The software allowedreadings of 100 positions of the compass per second

Using the pendulum test the spectrum (range) and easeof motion in knee (whether the movement was smoothphysiological and free in examined axis) were measured anddetermined by the following parameters

119899 number of oscillations119905 whole time of oscillations119879 period of oscillations (119879 = 119905119899)120582 logarithmdecrement of suppression (120582 = ln119883

21198834

where 1198832is a second amplitude during oscillations

and1198834is a fourth amplitude during oscillations

120573 suppression index (120573 = 120582119879)

The number of oscillations (119899) and whole time of oscil-lations (119905) described the ease of knee motion The periodof oscillations (119879) and suppression parameters (120582 and 120573)assessed the spectrum of knee motion (Figure 4) Thegoniometry pendulum test was performed for analysis ofNMES safety (to assess whether an increase in muscle massand strength will change in the mechanics of the knee joint)

24 Follow-Up The goniometry pendulum test was repeated1 and 3 months after the study (79 athletes were measured infollowup and only one participant fromgroupBwas excludedbecause of femoral neck fracture) The following procedure

was performed for analysis of electrical stimulation safety inlong term results

25 Statistical Analysis The chi-squared independence test(greatest reliability level) and parametric 119905-test were usedfor analysis of indicators which characterized individualsin both comparative groups The normal distribution waschecked by Shapiro-Wilk (for the null hypothesis that asample came from a normally distributed population) andthe chi-squared test (when the null hypothesis was true alsoconsider that a chi-squared test is a test in which this isasymptotically true meaning that the sampling distribution-if the null hypothesis is true can be made to approximate achi-squared distribution as closely as desired by making thesample size large enough) Recalling that the null hypothesisis that the population is normally distributed if the 119875-valueis less than the chosen alpha level then the null hypothesisis rejected (ie one concludes that the data are not from anormally distributed population)

If the 119875-value is greater than the chosen alpha levelthen one does not reject the null hypothesis that the datacame from a normally distributed population (according tostatistical estimation the population over 30ndash35 is needed forfurther analysis of normal distribution so we had to includeabout 80 participants in two groups in this study and use theparametric tests) Analyzed distributions appeared normaland we received the Gauss decay in all comparisons

The parameters before and after study were comparedin groups by parametric 119905-test (for dependent variables)Differences in parameters between groups were evaluatedwith 119905-test (for the independent variables) for comparisonsof experimental and follow-up results we used analysis ofvariance ANOVA to analyze the differences between groupmeans and their associated procedures (such as ldquovaria-tionrdquo among and between groups) In ANOVA setting theobserved variance in a particular variable is partitioned intocomponents attributable to different sources of variation

Two-sided 119875 values of less than 005 were considered tobe statistically significant

3 Results

The groups studied were homogeneous in terms of allparticipant characteristics (Table 1) and initial muscle powerand knee biomechanical parameters After experiment thestrength of quadriceps on the operated side in group A(NMES) increased from 6459 to 8934N (287 119875 = 0001)and in group B (control) it increased from 6486 to only6698N (46 119875 = 004) The comparison after 1-monththerapy of relative changes of the muscle strength betweenboth groups showed a significant difference in favor of stim-ulation (287 versus 46 119875 = 0002 and 95 confidenceinterval) The strength of quadriceps on nonoperated side ingroup A increased from 8401 to 10898N (301 119875 = 0003)and in group B increased from 8404 to only 8852N (46119875 = 004) The comparison after 1-month therapy of relativechanges of the muscle strength between both groups showed

BioMed Research International 5

(a) (b)

Figure 3 (a) and (b) are Goniometry pendulum test

Figure 4 Exampled data from pendulum test (sinusoidal wave ofpendulum movement) Legends (lambda) 120582 logarithm decrementof suppression (beta)120573 suppression index (Okreswahan)119879 periodof oscillations (Liczba wahan) 119899 number of oscillations (Czaswahan) 119905 whole time of oscillations

a significant difference in favor of stimulation (301 versus46 119875 = 0002 and 95 confidence interval)

In NMES group on the operated side quadriceps circum-ference increased from 565 to 579 cm (14 119875 = 003) andin group B it increased from 562 to 571 cm (06 119875 = 005)The comparison after amonth of treatment of relative changesof the muscle circumference between both groups showeda significant difference in favor of stimulation (14 versus06 119875 = 004 and 95 confidence interval) On the non-operated side quadriceps circumference increased from 581to 593 cm (11119875 = 003) and in group B increased from 577to 582 cm (04 119875 = 004) The comparison after a monthtreatment of relative changes of the muscle circumferencebetween both groups showed a significant difference in favorof NMES (11 versus 04 119875 = 004 and 95 confidenceinterval)

The comparison of all parameters measured usinggoniometry pendulum test in group A and B did not indicateany significant difference and also in the followup (after 1 and3 months after the end of study)mdashTables 2 and 3

4 Discussion

The results of this study showed that NMES is effective formuscle training in sport (we observed intensive increaseof power and mass of quadriceps muscle after one monththerapy) which corresponds with some research studiesHowever experiments in the literature are usually basedon small number of participants unclear randomization(researchers do not use validated methods of randomizationsuch as a computer or marked envelopes only physiciandecides the allocation of participants) lack of inclusion andexclusion criteria and no assessment of the safety of NMESapplication in sport [11 13 14 19]

Paillard et al [11] in their study observed the effectsof different types of NMES programs on vertical jumpperformance Twenty-seven healthy trained male students insports-sciences were recruited and randomized into threegroups The control group (C group 119899 = 8) did notperform NMES training Two other groups underwent 3training sessions a week for over 5 weeks on the quadricepsfemoris musclemdashF group (119899 = 9) stimulation with an80Hz current for 15min for improving muscle strength Egroup (119899 = 10) stimulation with a 25Hz current for 60minfor improving muscle endurance The height of the verticaljump was measured before NMES training (test 1) and oneweek (test 2) and five weeks (test 3) after the end of theprograms The results showed that the height of the verticaljump significantly increased in both the F and E groupsbetween tests 1 and 2 (5 cm and 3 cm resp) Results of test3 showed that both groups preserved their gains In authorsopinion aNMES training program improvesmuscle strength

British researchers [19] observed prolonged NMES insedentary adults Fifteen healthy subjects (10 men 5 women)with a sedentary lifestyle completed a 6-week training pro-gram during which they completed an average of 29 1-hourof NMES sessions The form NMES used by the subjects wascapable of eliciting a cardiovascular exercise responsewithoutloading the limbs or joints It achieved this bymeans of induc-ing rapid rhythmical contractions in the large leg musclesA crossover study design was employed with subjects under-going their habitual activity levels during the nontraining

6 BioMed Research International

Table 1 Characteristics of individuals from group A and B

Group A Group B Level ofsignificance

Number ofparticipants 40 40 lowastlowast

119875 gt 005

Age (years)Range 17ndash29 17ndash29

lowast

119875 gt 005Mean 224 213SD 578 567

Operated kneeRight 26 23

lowastlowast

119875 gt 005

Left 14 17Height (cm)

Range 171ndash193 170ndash186lowast

119875 gt 005Mean 1803 1765SD 754 811

Weight (kg)Range 71ndash80 63ndash100

lowast

119875 gt 005Mean 738 709SD 576 712

BMI (kgm2)Range 192ndash258 203ndash289

lowast

119875 gt 005Mean 224 234SD 422 303

Muscle strength(N)

Operated 5784ndash7013 5675ndash6899

lowastlowast

119875 gt 005

Range 6459 6486Mean 346 386SD

NonoperatedRange 8214ndash8798 8315ndash8897Mean 8401 8404SD 234 279

Duration of career(how long soccerplayers practicetheir discipline) inyears

Range 34ndash105 33ndash85lowast

119875 gt 005Mean 54 48SD 246 189

lowastthe 119905-test lowastlowastthe 1205942-test

phase of the studyThe training effect was evaluated bymeansof a treadmill test to determine peak aerobic capacity peakoxygen consumption Vo

2 a 6-minutes walking distance test

and measurement of body mass index (BMI) and quadricepsmuscle strength At baseline the mean values for peak Vo

2

6-min walking distance quadriceps strength and BMI were

246 lmin 4933m 3608N and 269 kgm2 respectivelyAfter training subjects demonstrated statistically significantimprovements in all variables except BMI PeakVo

2increased

by an average of 024 lmin (119875 lt 005) walking distanceincreased by 366m (119875 lt 0005) and quadriceps strengthincreased by 875N (119875 lt 0005) These results suggest thatNMES can be used in sedentary adults to improve musclestrength

Snyder-Mackler et al [13] included 85 patients to treatwith highintensity NMES high-level volitional exercise low-intensity NMES or combined high and lowintensity NMESAll treatment was performed isometrically with the knee in65 degrees of flexion All of the patients participated in anintensive programof closed-kinetic-chain exercise After fourweeks of treatment the strength of the quadriceps femorismuscle and the kinematics of the knee during stance phasewere measured Quadriceps strength averaged 70 or moreof the strength on the uninvolved side in the two groupsthat were treated with high-intensity NMES (either aloneor combined with low-intensity NMES) 57 in the groupthat was treated with high-level volitional exercise and 5in the group that was treated with low-intensity NMES Thekinematics of the knee joint were directly and significantly(119875 lt 005) correlated with the strength of the quadriceps

Other researchers [14] presented 27 healthy subjects(mean age 234 years) volunteered for the study and wererandomly assigned to 1 of 3 groups control group (noNMES)group 2 (NMES 2 times per week) and group 3 (NMES3 times per week) Groups 2 and 3 received NMES (10minutes per session) over a 4-week period for a total of 8and 12 NMES training sessions respectively The isometricquadriceps femoris muscle force produced during NMESwas monitored during each treatment minute The force ofthe quadriceps femoris was assessed prior to the first weekand at the start of weeks 2 3 and 4 of the 4-week trainingprogram with a final measurement after the fourth week (5total measurements) for all subjects Only the mean percentchange in quadriceps power before and after the 4 weeks oftraining with NMES between the control group and group 3was significantly different (119875 = 0021)

In our research we studied motion and function param-eters in knee without analysis of inflammatory reaction orquadriceps muscle damage

A review of the literature can be found to have onlyone article about muscle pathologies after NMES applicationVanderthommen et al [17] studied the effects on musclefunction of an electrical stimulation bout applied unilaterallyon thigh muscles in healthy male volunteers One group(ES group 119899 = 10) received consecutively 100 isometriccontractions of quadriceps and 100 isometric contractions ofhamstrings (on-off ratio 6-6 s) induced by neuromuscularelectrical stimulations (NMES) Changes in muscle torquemuscle soreness (VAS) muscle stiffness and serum creatinekinase (CK) activity were assessed before the NMES exercise(preex) as well as 24 h 48 h and 120 h after the bout Asecond group (control group 119899 = 10) was submitted tothe same test battery as the stimulation group and with thesame time-frame The between group comparison indicateda significant increase in VAS scores and in serum levels of CK

BioMed Research International 7

Table 2 Goniometry pendulum test in group A

Parameter Before therapy After therapyFollowup

Level of significance1 month 3 monthsMean SD Mean SD Mean SD Mean SD

120582

Operated 057 019 056 016 055 020 055 022 119875 gt 005

Nonoperated 047 018 045 019 046 022 046 022 lowast(in all comparisons)120573 [sminus1]

Operated 077 030 077 028 074 022 075 030 119875 gt 005

Non-operated 057 030 056 031 053 023 054 030 lowast(in all comparisons)119879 [s]

Operated 089 030 094 030 095 027 093 030 119875 gt 005

Non-operated 095 022 099 019 099 019 098 021 lowast(in all comparisons)119899

Operated 332 122 332 143 331 121 332 125 119875 gt 005

Non-operated 478 122 487 145 486 121 487 121 lowast(in all comparisons)119905 [s]

Operated 207 122 207 152 212 110 213 121 119875 gt 005

Non-operated 304 120 304 145 301 113 301 113 lowast(in all comparisons)lowastAnalysis of variance ANOVALegends120582 logarithm decrement of suppression (more than 065 is pathology of I Outebridge degree of the articular cartilage) 120573 suppression index (more than 085is pathology of I Outebridge degree of the articular cartilage) 119879 period of oscillations (less than 075 is pathology of I Outebridge degree of the articularcartilage) 119899 number of oscillations (less than 300 is pathology of I Outebridge degree of the articular cartilage) and 119905 whole time of oscillations (less than150 is pathology of I Outebridge degree of the articular cartilage)

Table 3 Goniometry pendulum test in group B

Parameter Before therapy After therapyFollowup

Level of significance1 month 3 monthsMean SD Mean SD Mean SD Mean SD

120582

Operated 055 021 058 019 056 022 055 020 119875 gt 005

Nonoperated 048 021 043 019 044 022 045 020 lowast(in all comparisons)120573 [sminus1]

Operated 075 032 076 021 075 022 075 028 119875 gt 005

Non-operated 058 027 057 028 055 025 054 028 lowast(in all comparisons)119879 [s]

Operated 087 034 090 035 090 029 090 030 119875 gt 005

Non-operated 095 019 097 019 097 019 099 020 lowast(in all comparisons)119899

Operated 335 131 333 138 333 130 333 130 119875 gt 005

Non-operated 475 131 479 139 480 141 480 141 lowast(in all comparisons)119905 [s]

Operated 211 103 209 104 210 111 211 101 119875 gt 005

Non-operated 310 128 311 125 311 111 310 109 lowast(in all comparisons)lowastAnalysis of variance ANOVALegends120582 logarithm decrement of suppression (more than 065 is pathology of I Outebridge degree of the articular cartilage) 120573 suppression index (more than 085is pathology of I Outebridge degree of the articular cartilage) 119879 period of oscillations (less than 075 is pathology of I Outebridge degree of the articularcartilage) 119899 number of oscillations (less than 300 is pathology of I Outebridge degree of the articular cartilage) and 119905 whole time of oscillations (less than150 is pathology of I Outebridge degree of the articular cartilage)

8 BioMed Research International

only in the ES group In the ES group changes were morepronounced in hamstrings than in quadriceps and peakedat 48 h (quadriceps VAS scores = 220 plusmn 1 (0 at preex)hamstrings VAS scores = 315 plusmn 214 (0 at preex) hip flexionangle = 62 plusmn 5∘ (75 plusmn 6∘ at preex) CK activity = 3021 plusmn2693 IU sdot l minus 1 (136 plusmn 50 IU sdot l minus 1 at preex) The results of thestudy suggested the occurrence of muscle damage that couldhave been induced by the physiologically incorrect musclerecruitment inNMES and the resulting overratedmechanicalstress

In our study the NMES appeared to be safe for biome-chanics of knee joint Based on our previous experience wecan strongly recommend the goniometry pendulum test asuseful diagnostic method in physical therapy process [20]The purpose of this clinical study was to assess low frequencylow intensity magnetic fields in the enhancement of thephysical rehabilitation of patients after knee endoprosthesissurgery The study included 62 patients who underwent totalknee arthroplasty Group A consisted of 32 patients who werephysically rehabilitated Group B consisted of 30 patients whowere physically rehabilitated and treated additionally withpulsing magnetic fields (5mT 30Hz 20min once a day 5days weekly)Therapy lasted for 3 weeks for both groupsTherehabilitation process was evaluated using a goniometer ten-someter goniometry pendulum test Lysholm scale for kneefunction and a visual analogue scale (VAS) questionnaire forpain and activityThe pendulum test appeared very useful forprecise observation of biomechanical changes in knee jointduring therapy process The physical therapy decreased thelogarithm decrement of suppression (120582) by about 79 ingroup A and 96 in group B suppression index (120573) decreasedabout 11 in group A and 133 in group B The period ofoscillations increased by 49 in group A and 4 in group Bnumber of oscillations (119899) increased by 221 in group A and206 in group B The whole time of oscillations increased of298 in group A and 245 in group B

In our study we did not observe both early and longterm results (goniometry pendulum testour research is thefirst attempt in literature of using this apparatus in sport)any pathological changes in knee function after increasingthe strength and mass of quadriceps in use of NMESThe progress in muscle parameters did not have influencepathologically on knee function

41 Limitations of Study In our study soccer players aftera month of therapy with NMES + rehabilitation or onlyrehabilitation program (7 months after ACL reconstruc-tion) returned to sport and league competition what couldinterfere with follow-up observation We were not able todemonstrate a relationship between the pendulum test andmuscle dysfunction either in the study or from previousresearch using a similar protocol correlated with markersof muscle damage We tried to use objective measurementmethods but we did not collect data related to functionaloutcomes of which there are some they could have chosen(triple-hop crossover-hop and jump-landing test)

5 Conclusion

The results of this study show that NMES (presented parame-ters in experiment) is useful for strengthening the quadricepsmuscle in soccer athletes There is an evidence the benefit ofthe NMES in restoring quadriceps muscle mass and strengthof soccer players In our study the neuromuscular electricalstimulation appeared to be safe for biomechanics of kneejoint The pathological changes in knee function were notobserved

Conflict of Interests

The authors would like to certify that they have no commer-cial associations with the manufacturers of the equipmentdescribed in the paper or other conflict of interests

References

[1] S C Petterson R L Mizner J E Stevens et al ldquoImprovedfunction from progressive strengthening interventions aftertotal knee arthroplasty a randomized clinical trial with animbedded prospective cohortrdquo Arthritis Care and Research vol61 no 2 pp 174ndash183 2009

[2] C Krishnan and G N Williams ldquoFactors explaining chronicknee extensor strength deficits after ACL reconstructionrdquo Jour-nal of Orthopaedic Research vol 29 no 5 pp 633ndash640 2011

[3] D Adams D S Logerstedt A Hunter-Giordano M J Axeand L Snyder-Mackler ldquoCurrent concepts for anterior cruciateligament reconstruction a criterion-based rehabilitation pro-gressionrdquo Journal of Orthopaedics and Sports Physical Therapyvol 42 no 7 pp 601ndash614 2012

[4] J E Stevens-Lapsley J E Balter P Wolfe D G Eckhoff andW M Kohrt ldquoEarly neuromuscular electrical stimulation toimprove quadriceps muscle strength after total knee arthro-plasty a randomized controlled trialrdquo Physical Therapy vol 92no 2 pp 210ndash226 2012

[5] G J Yun M H Chun J Y Park and B R Kim ldquoThesynergic effects of mirror therapy and neuromuscular electricalstimulation for hand function in stroke patientsrdquo Annals ofRehabilitation Medicine vol 35 no 3 pp 316ndash322 2011

[6] R J Walls G McHugh D J OrsquoGorman N M Moyna and JM OrsquoByrne ldquoEffects of preoperative neuromuscular electricalstimulation on quadriceps strength and functional recovery intotal knee arthroplasty A pilot studyrdquo BMC MusculoskeletalDisorders vol 14 no 11 article 119 2010

[7] Y Guan P W Wacnik F Yang et al ldquoSpinal cord stimulation-induced analgesia electrical stimulation of dorsal column anddorsal roots attenuates dorsal horn neuronal excitability inneuropathic ratsrdquo Anesthesiology vol 113 no 6 pp 1392ndash14052010

[8] T Arakawa A Katada H Shigyo et al ldquoElectrical stimulationprevents apoptosis in denervated skeletal musclerdquo NeuroReha-bilitation vol 27 no 2 pp 147ndash154 2010

[9] M R Gersh Electrotherapy in Rehabilitation ContemporaryPerspectives in Rehabilitation (Book 7) FA Davis CompanyPhiladelphia Pa USA 1994

[10] J H Kim M L Trew A J Pullan and O Rohrle ldquoSimulatinga dual-array electrode configuration to investigate the influence

BioMed Research International 9

of skeletal muscle fatigue following functional electrical stim-ulationrdquo Computers in Biology and Medicine vol 42 no 9 pp915ndash924 2012

[11] T Paillard F Noe N Bernard P Dupui and C HazardldquoEffects of two types of neuromuscular electrical stimulationtraining on vertical jump performancerdquo Journal of Strength andConditioning Research vol 22 no 4 pp 1273ndash1278 2008

[12] I Vivodtzev R Debigare P Gagnon et al ldquoFunctional andmuscular effects of neuromuscular electrical stimulation inpatients with severe COPD a randomized clinical trialrdquo Chestvol 141 no 3 pp 716ndash725 2012

[13] L Snyder-Mackler A Delitto S L Bailey and S W StralkaldquoStrength of the quadriceps femoris muscle and functionalrecovery after reconstruction of the anterior cruciate ligamentA prospective randomized clinical trial of electrical stimula-tionrdquo Journal of Bone and Joint Surgery A vol 77 no 8 pp 1166ndash1173 1995

[14] M G Parker M J Bennett M A Hieb A C Hollar and A ARoe ldquoStrength response in human quadriceps femoris muscleduring 2 neuromuscular electrical stimulation programsrdquo Jour-nal of Orthopaedic and Sports Physical Therapy vol 33 no 12pp 719ndash726 2003

[15] J W Bellew Z Beiswanger E Freeman C Gaerte and JTrafton ldquoInterferential and burst-modulated biphasic pulsedcurrents yield greater muscular force than Russian currentrdquoPhysiotherapy Theory and Practice vol 28 no 5 pp 384ndash3902012

[16] A Mysliwiec E Saulicz M Kuszewski M Kokosz and TWolny ldquoAssessment of the influence of Saunders tractionand transcutaneous electrical nerve stimulation on hand gripforce in patients with neck painrdquo Ortopedia TraumatologiaRehabilitacja vol 13 no 1 pp 37ndash44 2011

[17] M Vanderthommen M Triffaux Ch Demoulin J MCrielaard and J L Croisier ldquoAlteration of muscle functionafter electrical stimulation bout of knee extensors and flexorsrdquoJournal of Sports Science andMedicine vol 11 pp 592ndash599 2012

[18] L Bax F Staes and A Verhagen ldquoDoes neuromuscular electri-cal stimulation strengthen the quadriceps femoris A systematicreview of randomised controlled trialsrdquo SportsMedicine vol 35no 3 pp 191ndash212 2005

[19] P Banerjee B Caulfield L Crowe and A Clark ldquoProlongedelectrical muscle stimulation exercise improves strength andaerobic capacity in healthy sedentary adultsrdquo Journal of AppliedPhysiology vol 99 no 6 pp 2307ndash2311 2005

[20] E Błaszczak A Franek J Taradaj JWiduchowski and J Klim-czak ldquoAssessment of the efficacy and safety of low frequencylow intensity magnetic fields in patients after knee endopros-thesis plasty Part 2 a clinical studyrdquo Bioelectromagnetics vol30 no 2 pp 152ndash158 2009

Submit your manuscripts athttpwwwhindawicom

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Disease Markers

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Research and TreatmentAIDS

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Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 4: Clinical Study The Effect of NeuroMuscular Electrical Stimulation …downloads.hindawi.com/journals/bmri/2013/802534.pdf · 2019. 7. 31. · (ii) single-leg plyometrics, cutting/pivoting

4 BioMed Research International

Figure 2 Tensometry

measurements were performed before and after experiment(the measurements were in a supine position before the firstand after the last NMES procedure)

The goniometry pendulum test was composed of aperipheral device and a personal computer with softwareTheperipheral device consisted of a goniometry compass and aninterface system-transducer cooperated with the computerThe goniometry compass was composed of two thin metalarms (Figures 3(a) and 3(b)) One of the arms (immobile) wasfixed in a special outlet that allowed changing the angle andlengthThemobile armwas connected to the athletersquos legThemotion of the compasswasmeasured by aminioptoelectronictransducer The position of the transducer was measured(with a resolution of 12 bytes (B) on one revolution) andcoded in a range from 0∘ to 360∘ (exact to 0088∘) Thesignal was transmitted to the interface The software allowedreadings of 100 positions of the compass per second

Using the pendulum test the spectrum (range) and easeof motion in knee (whether the movement was smoothphysiological and free in examined axis) were measured anddetermined by the following parameters

119899 number of oscillations119905 whole time of oscillations119879 period of oscillations (119879 = 119905119899)120582 logarithmdecrement of suppression (120582 = ln119883

21198834

where 1198832is a second amplitude during oscillations

and1198834is a fourth amplitude during oscillations

120573 suppression index (120573 = 120582119879)

The number of oscillations (119899) and whole time of oscil-lations (119905) described the ease of knee motion The periodof oscillations (119879) and suppression parameters (120582 and 120573)assessed the spectrum of knee motion (Figure 4) Thegoniometry pendulum test was performed for analysis ofNMES safety (to assess whether an increase in muscle massand strength will change in the mechanics of the knee joint)

24 Follow-Up The goniometry pendulum test was repeated1 and 3 months after the study (79 athletes were measured infollowup and only one participant fromgroupBwas excludedbecause of femoral neck fracture) The following procedure

was performed for analysis of electrical stimulation safety inlong term results

25 Statistical Analysis The chi-squared independence test(greatest reliability level) and parametric 119905-test were usedfor analysis of indicators which characterized individualsin both comparative groups The normal distribution waschecked by Shapiro-Wilk (for the null hypothesis that asample came from a normally distributed population) andthe chi-squared test (when the null hypothesis was true alsoconsider that a chi-squared test is a test in which this isasymptotically true meaning that the sampling distribution-if the null hypothesis is true can be made to approximate achi-squared distribution as closely as desired by making thesample size large enough) Recalling that the null hypothesisis that the population is normally distributed if the 119875-valueis less than the chosen alpha level then the null hypothesisis rejected (ie one concludes that the data are not from anormally distributed population)

If the 119875-value is greater than the chosen alpha levelthen one does not reject the null hypothesis that the datacame from a normally distributed population (according tostatistical estimation the population over 30ndash35 is needed forfurther analysis of normal distribution so we had to includeabout 80 participants in two groups in this study and use theparametric tests) Analyzed distributions appeared normaland we received the Gauss decay in all comparisons

The parameters before and after study were comparedin groups by parametric 119905-test (for dependent variables)Differences in parameters between groups were evaluatedwith 119905-test (for the independent variables) for comparisonsof experimental and follow-up results we used analysis ofvariance ANOVA to analyze the differences between groupmeans and their associated procedures (such as ldquovaria-tionrdquo among and between groups) In ANOVA setting theobserved variance in a particular variable is partitioned intocomponents attributable to different sources of variation

Two-sided 119875 values of less than 005 were considered tobe statistically significant

3 Results

The groups studied were homogeneous in terms of allparticipant characteristics (Table 1) and initial muscle powerand knee biomechanical parameters After experiment thestrength of quadriceps on the operated side in group A(NMES) increased from 6459 to 8934N (287 119875 = 0001)and in group B (control) it increased from 6486 to only6698N (46 119875 = 004) The comparison after 1-monththerapy of relative changes of the muscle strength betweenboth groups showed a significant difference in favor of stim-ulation (287 versus 46 119875 = 0002 and 95 confidenceinterval) The strength of quadriceps on nonoperated side ingroup A increased from 8401 to 10898N (301 119875 = 0003)and in group B increased from 8404 to only 8852N (46119875 = 004) The comparison after 1-month therapy of relativechanges of the muscle strength between both groups showed

BioMed Research International 5

(a) (b)

Figure 3 (a) and (b) are Goniometry pendulum test

Figure 4 Exampled data from pendulum test (sinusoidal wave ofpendulum movement) Legends (lambda) 120582 logarithm decrementof suppression (beta)120573 suppression index (Okreswahan)119879 periodof oscillations (Liczba wahan) 119899 number of oscillations (Czaswahan) 119905 whole time of oscillations

a significant difference in favor of stimulation (301 versus46 119875 = 0002 and 95 confidence interval)

In NMES group on the operated side quadriceps circum-ference increased from 565 to 579 cm (14 119875 = 003) andin group B it increased from 562 to 571 cm (06 119875 = 005)The comparison after amonth of treatment of relative changesof the muscle circumference between both groups showeda significant difference in favor of stimulation (14 versus06 119875 = 004 and 95 confidence interval) On the non-operated side quadriceps circumference increased from 581to 593 cm (11119875 = 003) and in group B increased from 577to 582 cm (04 119875 = 004) The comparison after a monthtreatment of relative changes of the muscle circumferencebetween both groups showed a significant difference in favorof NMES (11 versus 04 119875 = 004 and 95 confidenceinterval)

The comparison of all parameters measured usinggoniometry pendulum test in group A and B did not indicateany significant difference and also in the followup (after 1 and3 months after the end of study)mdashTables 2 and 3

4 Discussion

The results of this study showed that NMES is effective formuscle training in sport (we observed intensive increaseof power and mass of quadriceps muscle after one monththerapy) which corresponds with some research studiesHowever experiments in the literature are usually basedon small number of participants unclear randomization(researchers do not use validated methods of randomizationsuch as a computer or marked envelopes only physiciandecides the allocation of participants) lack of inclusion andexclusion criteria and no assessment of the safety of NMESapplication in sport [11 13 14 19]

Paillard et al [11] in their study observed the effectsof different types of NMES programs on vertical jumpperformance Twenty-seven healthy trained male students insports-sciences were recruited and randomized into threegroups The control group (C group 119899 = 8) did notperform NMES training Two other groups underwent 3training sessions a week for over 5 weeks on the quadricepsfemoris musclemdashF group (119899 = 9) stimulation with an80Hz current for 15min for improving muscle strength Egroup (119899 = 10) stimulation with a 25Hz current for 60minfor improving muscle endurance The height of the verticaljump was measured before NMES training (test 1) and oneweek (test 2) and five weeks (test 3) after the end of theprograms The results showed that the height of the verticaljump significantly increased in both the F and E groupsbetween tests 1 and 2 (5 cm and 3 cm resp) Results of test3 showed that both groups preserved their gains In authorsopinion aNMES training program improvesmuscle strength

British researchers [19] observed prolonged NMES insedentary adults Fifteen healthy subjects (10 men 5 women)with a sedentary lifestyle completed a 6-week training pro-gram during which they completed an average of 29 1-hourof NMES sessions The form NMES used by the subjects wascapable of eliciting a cardiovascular exercise responsewithoutloading the limbs or joints It achieved this bymeans of induc-ing rapid rhythmical contractions in the large leg musclesA crossover study design was employed with subjects under-going their habitual activity levels during the nontraining

6 BioMed Research International

Table 1 Characteristics of individuals from group A and B

Group A Group B Level ofsignificance

Number ofparticipants 40 40 lowastlowast

119875 gt 005

Age (years)Range 17ndash29 17ndash29

lowast

119875 gt 005Mean 224 213SD 578 567

Operated kneeRight 26 23

lowastlowast

119875 gt 005

Left 14 17Height (cm)

Range 171ndash193 170ndash186lowast

119875 gt 005Mean 1803 1765SD 754 811

Weight (kg)Range 71ndash80 63ndash100

lowast

119875 gt 005Mean 738 709SD 576 712

BMI (kgm2)Range 192ndash258 203ndash289

lowast

119875 gt 005Mean 224 234SD 422 303

Muscle strength(N)

Operated 5784ndash7013 5675ndash6899

lowastlowast

119875 gt 005

Range 6459 6486Mean 346 386SD

NonoperatedRange 8214ndash8798 8315ndash8897Mean 8401 8404SD 234 279

Duration of career(how long soccerplayers practicetheir discipline) inyears

Range 34ndash105 33ndash85lowast

119875 gt 005Mean 54 48SD 246 189

lowastthe 119905-test lowastlowastthe 1205942-test

phase of the studyThe training effect was evaluated bymeansof a treadmill test to determine peak aerobic capacity peakoxygen consumption Vo

2 a 6-minutes walking distance test

and measurement of body mass index (BMI) and quadricepsmuscle strength At baseline the mean values for peak Vo

2

6-min walking distance quadriceps strength and BMI were

246 lmin 4933m 3608N and 269 kgm2 respectivelyAfter training subjects demonstrated statistically significantimprovements in all variables except BMI PeakVo

2increased

by an average of 024 lmin (119875 lt 005) walking distanceincreased by 366m (119875 lt 0005) and quadriceps strengthincreased by 875N (119875 lt 0005) These results suggest thatNMES can be used in sedentary adults to improve musclestrength

Snyder-Mackler et al [13] included 85 patients to treatwith highintensity NMES high-level volitional exercise low-intensity NMES or combined high and lowintensity NMESAll treatment was performed isometrically with the knee in65 degrees of flexion All of the patients participated in anintensive programof closed-kinetic-chain exercise After fourweeks of treatment the strength of the quadriceps femorismuscle and the kinematics of the knee during stance phasewere measured Quadriceps strength averaged 70 or moreof the strength on the uninvolved side in the two groupsthat were treated with high-intensity NMES (either aloneor combined with low-intensity NMES) 57 in the groupthat was treated with high-level volitional exercise and 5in the group that was treated with low-intensity NMES Thekinematics of the knee joint were directly and significantly(119875 lt 005) correlated with the strength of the quadriceps

Other researchers [14] presented 27 healthy subjects(mean age 234 years) volunteered for the study and wererandomly assigned to 1 of 3 groups control group (noNMES)group 2 (NMES 2 times per week) and group 3 (NMES3 times per week) Groups 2 and 3 received NMES (10minutes per session) over a 4-week period for a total of 8and 12 NMES training sessions respectively The isometricquadriceps femoris muscle force produced during NMESwas monitored during each treatment minute The force ofthe quadriceps femoris was assessed prior to the first weekand at the start of weeks 2 3 and 4 of the 4-week trainingprogram with a final measurement after the fourth week (5total measurements) for all subjects Only the mean percentchange in quadriceps power before and after the 4 weeks oftraining with NMES between the control group and group 3was significantly different (119875 = 0021)

In our research we studied motion and function param-eters in knee without analysis of inflammatory reaction orquadriceps muscle damage

A review of the literature can be found to have onlyone article about muscle pathologies after NMES applicationVanderthommen et al [17] studied the effects on musclefunction of an electrical stimulation bout applied unilaterallyon thigh muscles in healthy male volunteers One group(ES group 119899 = 10) received consecutively 100 isometriccontractions of quadriceps and 100 isometric contractions ofhamstrings (on-off ratio 6-6 s) induced by neuromuscularelectrical stimulations (NMES) Changes in muscle torquemuscle soreness (VAS) muscle stiffness and serum creatinekinase (CK) activity were assessed before the NMES exercise(preex) as well as 24 h 48 h and 120 h after the bout Asecond group (control group 119899 = 10) was submitted tothe same test battery as the stimulation group and with thesame time-frame The between group comparison indicateda significant increase in VAS scores and in serum levels of CK

BioMed Research International 7

Table 2 Goniometry pendulum test in group A

Parameter Before therapy After therapyFollowup

Level of significance1 month 3 monthsMean SD Mean SD Mean SD Mean SD

120582

Operated 057 019 056 016 055 020 055 022 119875 gt 005

Nonoperated 047 018 045 019 046 022 046 022 lowast(in all comparisons)120573 [sminus1]

Operated 077 030 077 028 074 022 075 030 119875 gt 005

Non-operated 057 030 056 031 053 023 054 030 lowast(in all comparisons)119879 [s]

Operated 089 030 094 030 095 027 093 030 119875 gt 005

Non-operated 095 022 099 019 099 019 098 021 lowast(in all comparisons)119899

Operated 332 122 332 143 331 121 332 125 119875 gt 005

Non-operated 478 122 487 145 486 121 487 121 lowast(in all comparisons)119905 [s]

Operated 207 122 207 152 212 110 213 121 119875 gt 005

Non-operated 304 120 304 145 301 113 301 113 lowast(in all comparisons)lowastAnalysis of variance ANOVALegends120582 logarithm decrement of suppression (more than 065 is pathology of I Outebridge degree of the articular cartilage) 120573 suppression index (more than 085is pathology of I Outebridge degree of the articular cartilage) 119879 period of oscillations (less than 075 is pathology of I Outebridge degree of the articularcartilage) 119899 number of oscillations (less than 300 is pathology of I Outebridge degree of the articular cartilage) and 119905 whole time of oscillations (less than150 is pathology of I Outebridge degree of the articular cartilage)

Table 3 Goniometry pendulum test in group B

Parameter Before therapy After therapyFollowup

Level of significance1 month 3 monthsMean SD Mean SD Mean SD Mean SD

120582

Operated 055 021 058 019 056 022 055 020 119875 gt 005

Nonoperated 048 021 043 019 044 022 045 020 lowast(in all comparisons)120573 [sminus1]

Operated 075 032 076 021 075 022 075 028 119875 gt 005

Non-operated 058 027 057 028 055 025 054 028 lowast(in all comparisons)119879 [s]

Operated 087 034 090 035 090 029 090 030 119875 gt 005

Non-operated 095 019 097 019 097 019 099 020 lowast(in all comparisons)119899

Operated 335 131 333 138 333 130 333 130 119875 gt 005

Non-operated 475 131 479 139 480 141 480 141 lowast(in all comparisons)119905 [s]

Operated 211 103 209 104 210 111 211 101 119875 gt 005

Non-operated 310 128 311 125 311 111 310 109 lowast(in all comparisons)lowastAnalysis of variance ANOVALegends120582 logarithm decrement of suppression (more than 065 is pathology of I Outebridge degree of the articular cartilage) 120573 suppression index (more than 085is pathology of I Outebridge degree of the articular cartilage) 119879 period of oscillations (less than 075 is pathology of I Outebridge degree of the articularcartilage) 119899 number of oscillations (less than 300 is pathology of I Outebridge degree of the articular cartilage) and 119905 whole time of oscillations (less than150 is pathology of I Outebridge degree of the articular cartilage)

8 BioMed Research International

only in the ES group In the ES group changes were morepronounced in hamstrings than in quadriceps and peakedat 48 h (quadriceps VAS scores = 220 plusmn 1 (0 at preex)hamstrings VAS scores = 315 plusmn 214 (0 at preex) hip flexionangle = 62 plusmn 5∘ (75 plusmn 6∘ at preex) CK activity = 3021 plusmn2693 IU sdot l minus 1 (136 plusmn 50 IU sdot l minus 1 at preex) The results of thestudy suggested the occurrence of muscle damage that couldhave been induced by the physiologically incorrect musclerecruitment inNMES and the resulting overratedmechanicalstress

In our study the NMES appeared to be safe for biome-chanics of knee joint Based on our previous experience wecan strongly recommend the goniometry pendulum test asuseful diagnostic method in physical therapy process [20]The purpose of this clinical study was to assess low frequencylow intensity magnetic fields in the enhancement of thephysical rehabilitation of patients after knee endoprosthesissurgery The study included 62 patients who underwent totalknee arthroplasty Group A consisted of 32 patients who werephysically rehabilitated Group B consisted of 30 patients whowere physically rehabilitated and treated additionally withpulsing magnetic fields (5mT 30Hz 20min once a day 5days weekly)Therapy lasted for 3 weeks for both groupsTherehabilitation process was evaluated using a goniometer ten-someter goniometry pendulum test Lysholm scale for kneefunction and a visual analogue scale (VAS) questionnaire forpain and activityThe pendulum test appeared very useful forprecise observation of biomechanical changes in knee jointduring therapy process The physical therapy decreased thelogarithm decrement of suppression (120582) by about 79 ingroup A and 96 in group B suppression index (120573) decreasedabout 11 in group A and 133 in group B The period ofoscillations increased by 49 in group A and 4 in group Bnumber of oscillations (119899) increased by 221 in group A and206 in group B The whole time of oscillations increased of298 in group A and 245 in group B

In our study we did not observe both early and longterm results (goniometry pendulum testour research is thefirst attempt in literature of using this apparatus in sport)any pathological changes in knee function after increasingthe strength and mass of quadriceps in use of NMESThe progress in muscle parameters did not have influencepathologically on knee function

41 Limitations of Study In our study soccer players aftera month of therapy with NMES + rehabilitation or onlyrehabilitation program (7 months after ACL reconstruc-tion) returned to sport and league competition what couldinterfere with follow-up observation We were not able todemonstrate a relationship between the pendulum test andmuscle dysfunction either in the study or from previousresearch using a similar protocol correlated with markersof muscle damage We tried to use objective measurementmethods but we did not collect data related to functionaloutcomes of which there are some they could have chosen(triple-hop crossover-hop and jump-landing test)

5 Conclusion

The results of this study show that NMES (presented parame-ters in experiment) is useful for strengthening the quadricepsmuscle in soccer athletes There is an evidence the benefit ofthe NMES in restoring quadriceps muscle mass and strengthof soccer players In our study the neuromuscular electricalstimulation appeared to be safe for biomechanics of kneejoint The pathological changes in knee function were notobserved

Conflict of Interests

The authors would like to certify that they have no commer-cial associations with the manufacturers of the equipmentdescribed in the paper or other conflict of interests

References

[1] S C Petterson R L Mizner J E Stevens et al ldquoImprovedfunction from progressive strengthening interventions aftertotal knee arthroplasty a randomized clinical trial with animbedded prospective cohortrdquo Arthritis Care and Research vol61 no 2 pp 174ndash183 2009

[2] C Krishnan and G N Williams ldquoFactors explaining chronicknee extensor strength deficits after ACL reconstructionrdquo Jour-nal of Orthopaedic Research vol 29 no 5 pp 633ndash640 2011

[3] D Adams D S Logerstedt A Hunter-Giordano M J Axeand L Snyder-Mackler ldquoCurrent concepts for anterior cruciateligament reconstruction a criterion-based rehabilitation pro-gressionrdquo Journal of Orthopaedics and Sports Physical Therapyvol 42 no 7 pp 601ndash614 2012

[4] J E Stevens-Lapsley J E Balter P Wolfe D G Eckhoff andW M Kohrt ldquoEarly neuromuscular electrical stimulation toimprove quadriceps muscle strength after total knee arthro-plasty a randomized controlled trialrdquo Physical Therapy vol 92no 2 pp 210ndash226 2012

[5] G J Yun M H Chun J Y Park and B R Kim ldquoThesynergic effects of mirror therapy and neuromuscular electricalstimulation for hand function in stroke patientsrdquo Annals ofRehabilitation Medicine vol 35 no 3 pp 316ndash322 2011

[6] R J Walls G McHugh D J OrsquoGorman N M Moyna and JM OrsquoByrne ldquoEffects of preoperative neuromuscular electricalstimulation on quadriceps strength and functional recovery intotal knee arthroplasty A pilot studyrdquo BMC MusculoskeletalDisorders vol 14 no 11 article 119 2010

[7] Y Guan P W Wacnik F Yang et al ldquoSpinal cord stimulation-induced analgesia electrical stimulation of dorsal column anddorsal roots attenuates dorsal horn neuronal excitability inneuropathic ratsrdquo Anesthesiology vol 113 no 6 pp 1392ndash14052010

[8] T Arakawa A Katada H Shigyo et al ldquoElectrical stimulationprevents apoptosis in denervated skeletal musclerdquo NeuroReha-bilitation vol 27 no 2 pp 147ndash154 2010

[9] M R Gersh Electrotherapy in Rehabilitation ContemporaryPerspectives in Rehabilitation (Book 7) FA Davis CompanyPhiladelphia Pa USA 1994

[10] J H Kim M L Trew A J Pullan and O Rohrle ldquoSimulatinga dual-array electrode configuration to investigate the influence

BioMed Research International 9

of skeletal muscle fatigue following functional electrical stim-ulationrdquo Computers in Biology and Medicine vol 42 no 9 pp915ndash924 2012

[11] T Paillard F Noe N Bernard P Dupui and C HazardldquoEffects of two types of neuromuscular electrical stimulationtraining on vertical jump performancerdquo Journal of Strength andConditioning Research vol 22 no 4 pp 1273ndash1278 2008

[12] I Vivodtzev R Debigare P Gagnon et al ldquoFunctional andmuscular effects of neuromuscular electrical stimulation inpatients with severe COPD a randomized clinical trialrdquo Chestvol 141 no 3 pp 716ndash725 2012

[13] L Snyder-Mackler A Delitto S L Bailey and S W StralkaldquoStrength of the quadriceps femoris muscle and functionalrecovery after reconstruction of the anterior cruciate ligamentA prospective randomized clinical trial of electrical stimula-tionrdquo Journal of Bone and Joint Surgery A vol 77 no 8 pp 1166ndash1173 1995

[14] M G Parker M J Bennett M A Hieb A C Hollar and A ARoe ldquoStrength response in human quadriceps femoris muscleduring 2 neuromuscular electrical stimulation programsrdquo Jour-nal of Orthopaedic and Sports Physical Therapy vol 33 no 12pp 719ndash726 2003

[15] J W Bellew Z Beiswanger E Freeman C Gaerte and JTrafton ldquoInterferential and burst-modulated biphasic pulsedcurrents yield greater muscular force than Russian currentrdquoPhysiotherapy Theory and Practice vol 28 no 5 pp 384ndash3902012

[16] A Mysliwiec E Saulicz M Kuszewski M Kokosz and TWolny ldquoAssessment of the influence of Saunders tractionand transcutaneous electrical nerve stimulation on hand gripforce in patients with neck painrdquo Ortopedia TraumatologiaRehabilitacja vol 13 no 1 pp 37ndash44 2011

[17] M Vanderthommen M Triffaux Ch Demoulin J MCrielaard and J L Croisier ldquoAlteration of muscle functionafter electrical stimulation bout of knee extensors and flexorsrdquoJournal of Sports Science andMedicine vol 11 pp 592ndash599 2012

[18] L Bax F Staes and A Verhagen ldquoDoes neuromuscular electri-cal stimulation strengthen the quadriceps femoris A systematicreview of randomised controlled trialsrdquo SportsMedicine vol 35no 3 pp 191ndash212 2005

[19] P Banerjee B Caulfield L Crowe and A Clark ldquoProlongedelectrical muscle stimulation exercise improves strength andaerobic capacity in healthy sedentary adultsrdquo Journal of AppliedPhysiology vol 99 no 6 pp 2307ndash2311 2005

[20] E Błaszczak A Franek J Taradaj JWiduchowski and J Klim-czak ldquoAssessment of the efficacy and safety of low frequencylow intensity magnetic fields in patients after knee endopros-thesis plasty Part 2 a clinical studyrdquo Bioelectromagnetics vol30 no 2 pp 152ndash158 2009

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 5: Clinical Study The Effect of NeuroMuscular Electrical Stimulation …downloads.hindawi.com/journals/bmri/2013/802534.pdf · 2019. 7. 31. · (ii) single-leg plyometrics, cutting/pivoting

BioMed Research International 5

(a) (b)

Figure 3 (a) and (b) are Goniometry pendulum test

Figure 4 Exampled data from pendulum test (sinusoidal wave ofpendulum movement) Legends (lambda) 120582 logarithm decrementof suppression (beta)120573 suppression index (Okreswahan)119879 periodof oscillations (Liczba wahan) 119899 number of oscillations (Czaswahan) 119905 whole time of oscillations

a significant difference in favor of stimulation (301 versus46 119875 = 0002 and 95 confidence interval)

In NMES group on the operated side quadriceps circum-ference increased from 565 to 579 cm (14 119875 = 003) andin group B it increased from 562 to 571 cm (06 119875 = 005)The comparison after amonth of treatment of relative changesof the muscle circumference between both groups showeda significant difference in favor of stimulation (14 versus06 119875 = 004 and 95 confidence interval) On the non-operated side quadriceps circumference increased from 581to 593 cm (11119875 = 003) and in group B increased from 577to 582 cm (04 119875 = 004) The comparison after a monthtreatment of relative changes of the muscle circumferencebetween both groups showed a significant difference in favorof NMES (11 versus 04 119875 = 004 and 95 confidenceinterval)

The comparison of all parameters measured usinggoniometry pendulum test in group A and B did not indicateany significant difference and also in the followup (after 1 and3 months after the end of study)mdashTables 2 and 3

4 Discussion

The results of this study showed that NMES is effective formuscle training in sport (we observed intensive increaseof power and mass of quadriceps muscle after one monththerapy) which corresponds with some research studiesHowever experiments in the literature are usually basedon small number of participants unclear randomization(researchers do not use validated methods of randomizationsuch as a computer or marked envelopes only physiciandecides the allocation of participants) lack of inclusion andexclusion criteria and no assessment of the safety of NMESapplication in sport [11 13 14 19]

Paillard et al [11] in their study observed the effectsof different types of NMES programs on vertical jumpperformance Twenty-seven healthy trained male students insports-sciences were recruited and randomized into threegroups The control group (C group 119899 = 8) did notperform NMES training Two other groups underwent 3training sessions a week for over 5 weeks on the quadricepsfemoris musclemdashF group (119899 = 9) stimulation with an80Hz current for 15min for improving muscle strength Egroup (119899 = 10) stimulation with a 25Hz current for 60minfor improving muscle endurance The height of the verticaljump was measured before NMES training (test 1) and oneweek (test 2) and five weeks (test 3) after the end of theprograms The results showed that the height of the verticaljump significantly increased in both the F and E groupsbetween tests 1 and 2 (5 cm and 3 cm resp) Results of test3 showed that both groups preserved their gains In authorsopinion aNMES training program improvesmuscle strength

British researchers [19] observed prolonged NMES insedentary adults Fifteen healthy subjects (10 men 5 women)with a sedentary lifestyle completed a 6-week training pro-gram during which they completed an average of 29 1-hourof NMES sessions The form NMES used by the subjects wascapable of eliciting a cardiovascular exercise responsewithoutloading the limbs or joints It achieved this bymeans of induc-ing rapid rhythmical contractions in the large leg musclesA crossover study design was employed with subjects under-going their habitual activity levels during the nontraining

6 BioMed Research International

Table 1 Characteristics of individuals from group A and B

Group A Group B Level ofsignificance

Number ofparticipants 40 40 lowastlowast

119875 gt 005

Age (years)Range 17ndash29 17ndash29

lowast

119875 gt 005Mean 224 213SD 578 567

Operated kneeRight 26 23

lowastlowast

119875 gt 005

Left 14 17Height (cm)

Range 171ndash193 170ndash186lowast

119875 gt 005Mean 1803 1765SD 754 811

Weight (kg)Range 71ndash80 63ndash100

lowast

119875 gt 005Mean 738 709SD 576 712

BMI (kgm2)Range 192ndash258 203ndash289

lowast

119875 gt 005Mean 224 234SD 422 303

Muscle strength(N)

Operated 5784ndash7013 5675ndash6899

lowastlowast

119875 gt 005

Range 6459 6486Mean 346 386SD

NonoperatedRange 8214ndash8798 8315ndash8897Mean 8401 8404SD 234 279

Duration of career(how long soccerplayers practicetheir discipline) inyears

Range 34ndash105 33ndash85lowast

119875 gt 005Mean 54 48SD 246 189

lowastthe 119905-test lowastlowastthe 1205942-test

phase of the studyThe training effect was evaluated bymeansof a treadmill test to determine peak aerobic capacity peakoxygen consumption Vo

2 a 6-minutes walking distance test

and measurement of body mass index (BMI) and quadricepsmuscle strength At baseline the mean values for peak Vo

2

6-min walking distance quadriceps strength and BMI were

246 lmin 4933m 3608N and 269 kgm2 respectivelyAfter training subjects demonstrated statistically significantimprovements in all variables except BMI PeakVo

2increased

by an average of 024 lmin (119875 lt 005) walking distanceincreased by 366m (119875 lt 0005) and quadriceps strengthincreased by 875N (119875 lt 0005) These results suggest thatNMES can be used in sedentary adults to improve musclestrength

Snyder-Mackler et al [13] included 85 patients to treatwith highintensity NMES high-level volitional exercise low-intensity NMES or combined high and lowintensity NMESAll treatment was performed isometrically with the knee in65 degrees of flexion All of the patients participated in anintensive programof closed-kinetic-chain exercise After fourweeks of treatment the strength of the quadriceps femorismuscle and the kinematics of the knee during stance phasewere measured Quadriceps strength averaged 70 or moreof the strength on the uninvolved side in the two groupsthat were treated with high-intensity NMES (either aloneor combined with low-intensity NMES) 57 in the groupthat was treated with high-level volitional exercise and 5in the group that was treated with low-intensity NMES Thekinematics of the knee joint were directly and significantly(119875 lt 005) correlated with the strength of the quadriceps

Other researchers [14] presented 27 healthy subjects(mean age 234 years) volunteered for the study and wererandomly assigned to 1 of 3 groups control group (noNMES)group 2 (NMES 2 times per week) and group 3 (NMES3 times per week) Groups 2 and 3 received NMES (10minutes per session) over a 4-week period for a total of 8and 12 NMES training sessions respectively The isometricquadriceps femoris muscle force produced during NMESwas monitored during each treatment minute The force ofthe quadriceps femoris was assessed prior to the first weekand at the start of weeks 2 3 and 4 of the 4-week trainingprogram with a final measurement after the fourth week (5total measurements) for all subjects Only the mean percentchange in quadriceps power before and after the 4 weeks oftraining with NMES between the control group and group 3was significantly different (119875 = 0021)

In our research we studied motion and function param-eters in knee without analysis of inflammatory reaction orquadriceps muscle damage

A review of the literature can be found to have onlyone article about muscle pathologies after NMES applicationVanderthommen et al [17] studied the effects on musclefunction of an electrical stimulation bout applied unilaterallyon thigh muscles in healthy male volunteers One group(ES group 119899 = 10) received consecutively 100 isometriccontractions of quadriceps and 100 isometric contractions ofhamstrings (on-off ratio 6-6 s) induced by neuromuscularelectrical stimulations (NMES) Changes in muscle torquemuscle soreness (VAS) muscle stiffness and serum creatinekinase (CK) activity were assessed before the NMES exercise(preex) as well as 24 h 48 h and 120 h after the bout Asecond group (control group 119899 = 10) was submitted tothe same test battery as the stimulation group and with thesame time-frame The between group comparison indicateda significant increase in VAS scores and in serum levels of CK

BioMed Research International 7

Table 2 Goniometry pendulum test in group A

Parameter Before therapy After therapyFollowup

Level of significance1 month 3 monthsMean SD Mean SD Mean SD Mean SD

120582

Operated 057 019 056 016 055 020 055 022 119875 gt 005

Nonoperated 047 018 045 019 046 022 046 022 lowast(in all comparisons)120573 [sminus1]

Operated 077 030 077 028 074 022 075 030 119875 gt 005

Non-operated 057 030 056 031 053 023 054 030 lowast(in all comparisons)119879 [s]

Operated 089 030 094 030 095 027 093 030 119875 gt 005

Non-operated 095 022 099 019 099 019 098 021 lowast(in all comparisons)119899

Operated 332 122 332 143 331 121 332 125 119875 gt 005

Non-operated 478 122 487 145 486 121 487 121 lowast(in all comparisons)119905 [s]

Operated 207 122 207 152 212 110 213 121 119875 gt 005

Non-operated 304 120 304 145 301 113 301 113 lowast(in all comparisons)lowastAnalysis of variance ANOVALegends120582 logarithm decrement of suppression (more than 065 is pathology of I Outebridge degree of the articular cartilage) 120573 suppression index (more than 085is pathology of I Outebridge degree of the articular cartilage) 119879 period of oscillations (less than 075 is pathology of I Outebridge degree of the articularcartilage) 119899 number of oscillations (less than 300 is pathology of I Outebridge degree of the articular cartilage) and 119905 whole time of oscillations (less than150 is pathology of I Outebridge degree of the articular cartilage)

Table 3 Goniometry pendulum test in group B

Parameter Before therapy After therapyFollowup

Level of significance1 month 3 monthsMean SD Mean SD Mean SD Mean SD

120582

Operated 055 021 058 019 056 022 055 020 119875 gt 005

Nonoperated 048 021 043 019 044 022 045 020 lowast(in all comparisons)120573 [sminus1]

Operated 075 032 076 021 075 022 075 028 119875 gt 005

Non-operated 058 027 057 028 055 025 054 028 lowast(in all comparisons)119879 [s]

Operated 087 034 090 035 090 029 090 030 119875 gt 005

Non-operated 095 019 097 019 097 019 099 020 lowast(in all comparisons)119899

Operated 335 131 333 138 333 130 333 130 119875 gt 005

Non-operated 475 131 479 139 480 141 480 141 lowast(in all comparisons)119905 [s]

Operated 211 103 209 104 210 111 211 101 119875 gt 005

Non-operated 310 128 311 125 311 111 310 109 lowast(in all comparisons)lowastAnalysis of variance ANOVALegends120582 logarithm decrement of suppression (more than 065 is pathology of I Outebridge degree of the articular cartilage) 120573 suppression index (more than 085is pathology of I Outebridge degree of the articular cartilage) 119879 period of oscillations (less than 075 is pathology of I Outebridge degree of the articularcartilage) 119899 number of oscillations (less than 300 is pathology of I Outebridge degree of the articular cartilage) and 119905 whole time of oscillations (less than150 is pathology of I Outebridge degree of the articular cartilage)

8 BioMed Research International

only in the ES group In the ES group changes were morepronounced in hamstrings than in quadriceps and peakedat 48 h (quadriceps VAS scores = 220 plusmn 1 (0 at preex)hamstrings VAS scores = 315 plusmn 214 (0 at preex) hip flexionangle = 62 plusmn 5∘ (75 plusmn 6∘ at preex) CK activity = 3021 plusmn2693 IU sdot l minus 1 (136 plusmn 50 IU sdot l minus 1 at preex) The results of thestudy suggested the occurrence of muscle damage that couldhave been induced by the physiologically incorrect musclerecruitment inNMES and the resulting overratedmechanicalstress

In our study the NMES appeared to be safe for biome-chanics of knee joint Based on our previous experience wecan strongly recommend the goniometry pendulum test asuseful diagnostic method in physical therapy process [20]The purpose of this clinical study was to assess low frequencylow intensity magnetic fields in the enhancement of thephysical rehabilitation of patients after knee endoprosthesissurgery The study included 62 patients who underwent totalknee arthroplasty Group A consisted of 32 patients who werephysically rehabilitated Group B consisted of 30 patients whowere physically rehabilitated and treated additionally withpulsing magnetic fields (5mT 30Hz 20min once a day 5days weekly)Therapy lasted for 3 weeks for both groupsTherehabilitation process was evaluated using a goniometer ten-someter goniometry pendulum test Lysholm scale for kneefunction and a visual analogue scale (VAS) questionnaire forpain and activityThe pendulum test appeared very useful forprecise observation of biomechanical changes in knee jointduring therapy process The physical therapy decreased thelogarithm decrement of suppression (120582) by about 79 ingroup A and 96 in group B suppression index (120573) decreasedabout 11 in group A and 133 in group B The period ofoscillations increased by 49 in group A and 4 in group Bnumber of oscillations (119899) increased by 221 in group A and206 in group B The whole time of oscillations increased of298 in group A and 245 in group B

In our study we did not observe both early and longterm results (goniometry pendulum testour research is thefirst attempt in literature of using this apparatus in sport)any pathological changes in knee function after increasingthe strength and mass of quadriceps in use of NMESThe progress in muscle parameters did not have influencepathologically on knee function

41 Limitations of Study In our study soccer players aftera month of therapy with NMES + rehabilitation or onlyrehabilitation program (7 months after ACL reconstruc-tion) returned to sport and league competition what couldinterfere with follow-up observation We were not able todemonstrate a relationship between the pendulum test andmuscle dysfunction either in the study or from previousresearch using a similar protocol correlated with markersof muscle damage We tried to use objective measurementmethods but we did not collect data related to functionaloutcomes of which there are some they could have chosen(triple-hop crossover-hop and jump-landing test)

5 Conclusion

The results of this study show that NMES (presented parame-ters in experiment) is useful for strengthening the quadricepsmuscle in soccer athletes There is an evidence the benefit ofthe NMES in restoring quadriceps muscle mass and strengthof soccer players In our study the neuromuscular electricalstimulation appeared to be safe for biomechanics of kneejoint The pathological changes in knee function were notobserved

Conflict of Interests

The authors would like to certify that they have no commer-cial associations with the manufacturers of the equipmentdescribed in the paper or other conflict of interests

References

[1] S C Petterson R L Mizner J E Stevens et al ldquoImprovedfunction from progressive strengthening interventions aftertotal knee arthroplasty a randomized clinical trial with animbedded prospective cohortrdquo Arthritis Care and Research vol61 no 2 pp 174ndash183 2009

[2] C Krishnan and G N Williams ldquoFactors explaining chronicknee extensor strength deficits after ACL reconstructionrdquo Jour-nal of Orthopaedic Research vol 29 no 5 pp 633ndash640 2011

[3] D Adams D S Logerstedt A Hunter-Giordano M J Axeand L Snyder-Mackler ldquoCurrent concepts for anterior cruciateligament reconstruction a criterion-based rehabilitation pro-gressionrdquo Journal of Orthopaedics and Sports Physical Therapyvol 42 no 7 pp 601ndash614 2012

[4] J E Stevens-Lapsley J E Balter P Wolfe D G Eckhoff andW M Kohrt ldquoEarly neuromuscular electrical stimulation toimprove quadriceps muscle strength after total knee arthro-plasty a randomized controlled trialrdquo Physical Therapy vol 92no 2 pp 210ndash226 2012

[5] G J Yun M H Chun J Y Park and B R Kim ldquoThesynergic effects of mirror therapy and neuromuscular electricalstimulation for hand function in stroke patientsrdquo Annals ofRehabilitation Medicine vol 35 no 3 pp 316ndash322 2011

[6] R J Walls G McHugh D J OrsquoGorman N M Moyna and JM OrsquoByrne ldquoEffects of preoperative neuromuscular electricalstimulation on quadriceps strength and functional recovery intotal knee arthroplasty A pilot studyrdquo BMC MusculoskeletalDisorders vol 14 no 11 article 119 2010

[7] Y Guan P W Wacnik F Yang et al ldquoSpinal cord stimulation-induced analgesia electrical stimulation of dorsal column anddorsal roots attenuates dorsal horn neuronal excitability inneuropathic ratsrdquo Anesthesiology vol 113 no 6 pp 1392ndash14052010

[8] T Arakawa A Katada H Shigyo et al ldquoElectrical stimulationprevents apoptosis in denervated skeletal musclerdquo NeuroReha-bilitation vol 27 no 2 pp 147ndash154 2010

[9] M R Gersh Electrotherapy in Rehabilitation ContemporaryPerspectives in Rehabilitation (Book 7) FA Davis CompanyPhiladelphia Pa USA 1994

[10] J H Kim M L Trew A J Pullan and O Rohrle ldquoSimulatinga dual-array electrode configuration to investigate the influence

BioMed Research International 9

of skeletal muscle fatigue following functional electrical stim-ulationrdquo Computers in Biology and Medicine vol 42 no 9 pp915ndash924 2012

[11] T Paillard F Noe N Bernard P Dupui and C HazardldquoEffects of two types of neuromuscular electrical stimulationtraining on vertical jump performancerdquo Journal of Strength andConditioning Research vol 22 no 4 pp 1273ndash1278 2008

[12] I Vivodtzev R Debigare P Gagnon et al ldquoFunctional andmuscular effects of neuromuscular electrical stimulation inpatients with severe COPD a randomized clinical trialrdquo Chestvol 141 no 3 pp 716ndash725 2012

[13] L Snyder-Mackler A Delitto S L Bailey and S W StralkaldquoStrength of the quadriceps femoris muscle and functionalrecovery after reconstruction of the anterior cruciate ligamentA prospective randomized clinical trial of electrical stimula-tionrdquo Journal of Bone and Joint Surgery A vol 77 no 8 pp 1166ndash1173 1995

[14] M G Parker M J Bennett M A Hieb A C Hollar and A ARoe ldquoStrength response in human quadriceps femoris muscleduring 2 neuromuscular electrical stimulation programsrdquo Jour-nal of Orthopaedic and Sports Physical Therapy vol 33 no 12pp 719ndash726 2003

[15] J W Bellew Z Beiswanger E Freeman C Gaerte and JTrafton ldquoInterferential and burst-modulated biphasic pulsedcurrents yield greater muscular force than Russian currentrdquoPhysiotherapy Theory and Practice vol 28 no 5 pp 384ndash3902012

[16] A Mysliwiec E Saulicz M Kuszewski M Kokosz and TWolny ldquoAssessment of the influence of Saunders tractionand transcutaneous electrical nerve stimulation on hand gripforce in patients with neck painrdquo Ortopedia TraumatologiaRehabilitacja vol 13 no 1 pp 37ndash44 2011

[17] M Vanderthommen M Triffaux Ch Demoulin J MCrielaard and J L Croisier ldquoAlteration of muscle functionafter electrical stimulation bout of knee extensors and flexorsrdquoJournal of Sports Science andMedicine vol 11 pp 592ndash599 2012

[18] L Bax F Staes and A Verhagen ldquoDoes neuromuscular electri-cal stimulation strengthen the quadriceps femoris A systematicreview of randomised controlled trialsrdquo SportsMedicine vol 35no 3 pp 191ndash212 2005

[19] P Banerjee B Caulfield L Crowe and A Clark ldquoProlongedelectrical muscle stimulation exercise improves strength andaerobic capacity in healthy sedentary adultsrdquo Journal of AppliedPhysiology vol 99 no 6 pp 2307ndash2311 2005

[20] E Błaszczak A Franek J Taradaj JWiduchowski and J Klim-czak ldquoAssessment of the efficacy and safety of low frequencylow intensity magnetic fields in patients after knee endopros-thesis plasty Part 2 a clinical studyrdquo Bioelectromagnetics vol30 no 2 pp 152ndash158 2009

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 6: Clinical Study The Effect of NeuroMuscular Electrical Stimulation …downloads.hindawi.com/journals/bmri/2013/802534.pdf · 2019. 7. 31. · (ii) single-leg plyometrics, cutting/pivoting

6 BioMed Research International

Table 1 Characteristics of individuals from group A and B

Group A Group B Level ofsignificance

Number ofparticipants 40 40 lowastlowast

119875 gt 005

Age (years)Range 17ndash29 17ndash29

lowast

119875 gt 005Mean 224 213SD 578 567

Operated kneeRight 26 23

lowastlowast

119875 gt 005

Left 14 17Height (cm)

Range 171ndash193 170ndash186lowast

119875 gt 005Mean 1803 1765SD 754 811

Weight (kg)Range 71ndash80 63ndash100

lowast

119875 gt 005Mean 738 709SD 576 712

BMI (kgm2)Range 192ndash258 203ndash289

lowast

119875 gt 005Mean 224 234SD 422 303

Muscle strength(N)

Operated 5784ndash7013 5675ndash6899

lowastlowast

119875 gt 005

Range 6459 6486Mean 346 386SD

NonoperatedRange 8214ndash8798 8315ndash8897Mean 8401 8404SD 234 279

Duration of career(how long soccerplayers practicetheir discipline) inyears

Range 34ndash105 33ndash85lowast

119875 gt 005Mean 54 48SD 246 189

lowastthe 119905-test lowastlowastthe 1205942-test

phase of the studyThe training effect was evaluated bymeansof a treadmill test to determine peak aerobic capacity peakoxygen consumption Vo

2 a 6-minutes walking distance test

and measurement of body mass index (BMI) and quadricepsmuscle strength At baseline the mean values for peak Vo

2

6-min walking distance quadriceps strength and BMI were

246 lmin 4933m 3608N and 269 kgm2 respectivelyAfter training subjects demonstrated statistically significantimprovements in all variables except BMI PeakVo

2increased

by an average of 024 lmin (119875 lt 005) walking distanceincreased by 366m (119875 lt 0005) and quadriceps strengthincreased by 875N (119875 lt 0005) These results suggest thatNMES can be used in sedentary adults to improve musclestrength

Snyder-Mackler et al [13] included 85 patients to treatwith highintensity NMES high-level volitional exercise low-intensity NMES or combined high and lowintensity NMESAll treatment was performed isometrically with the knee in65 degrees of flexion All of the patients participated in anintensive programof closed-kinetic-chain exercise After fourweeks of treatment the strength of the quadriceps femorismuscle and the kinematics of the knee during stance phasewere measured Quadriceps strength averaged 70 or moreof the strength on the uninvolved side in the two groupsthat were treated with high-intensity NMES (either aloneor combined with low-intensity NMES) 57 in the groupthat was treated with high-level volitional exercise and 5in the group that was treated with low-intensity NMES Thekinematics of the knee joint were directly and significantly(119875 lt 005) correlated with the strength of the quadriceps

Other researchers [14] presented 27 healthy subjects(mean age 234 years) volunteered for the study and wererandomly assigned to 1 of 3 groups control group (noNMES)group 2 (NMES 2 times per week) and group 3 (NMES3 times per week) Groups 2 and 3 received NMES (10minutes per session) over a 4-week period for a total of 8and 12 NMES training sessions respectively The isometricquadriceps femoris muscle force produced during NMESwas monitored during each treatment minute The force ofthe quadriceps femoris was assessed prior to the first weekand at the start of weeks 2 3 and 4 of the 4-week trainingprogram with a final measurement after the fourth week (5total measurements) for all subjects Only the mean percentchange in quadriceps power before and after the 4 weeks oftraining with NMES between the control group and group 3was significantly different (119875 = 0021)

In our research we studied motion and function param-eters in knee without analysis of inflammatory reaction orquadriceps muscle damage

A review of the literature can be found to have onlyone article about muscle pathologies after NMES applicationVanderthommen et al [17] studied the effects on musclefunction of an electrical stimulation bout applied unilaterallyon thigh muscles in healthy male volunteers One group(ES group 119899 = 10) received consecutively 100 isometriccontractions of quadriceps and 100 isometric contractions ofhamstrings (on-off ratio 6-6 s) induced by neuromuscularelectrical stimulations (NMES) Changes in muscle torquemuscle soreness (VAS) muscle stiffness and serum creatinekinase (CK) activity were assessed before the NMES exercise(preex) as well as 24 h 48 h and 120 h after the bout Asecond group (control group 119899 = 10) was submitted tothe same test battery as the stimulation group and with thesame time-frame The between group comparison indicateda significant increase in VAS scores and in serum levels of CK

BioMed Research International 7

Table 2 Goniometry pendulum test in group A

Parameter Before therapy After therapyFollowup

Level of significance1 month 3 monthsMean SD Mean SD Mean SD Mean SD

120582

Operated 057 019 056 016 055 020 055 022 119875 gt 005

Nonoperated 047 018 045 019 046 022 046 022 lowast(in all comparisons)120573 [sminus1]

Operated 077 030 077 028 074 022 075 030 119875 gt 005

Non-operated 057 030 056 031 053 023 054 030 lowast(in all comparisons)119879 [s]

Operated 089 030 094 030 095 027 093 030 119875 gt 005

Non-operated 095 022 099 019 099 019 098 021 lowast(in all comparisons)119899

Operated 332 122 332 143 331 121 332 125 119875 gt 005

Non-operated 478 122 487 145 486 121 487 121 lowast(in all comparisons)119905 [s]

Operated 207 122 207 152 212 110 213 121 119875 gt 005

Non-operated 304 120 304 145 301 113 301 113 lowast(in all comparisons)lowastAnalysis of variance ANOVALegends120582 logarithm decrement of suppression (more than 065 is pathology of I Outebridge degree of the articular cartilage) 120573 suppression index (more than 085is pathology of I Outebridge degree of the articular cartilage) 119879 period of oscillations (less than 075 is pathology of I Outebridge degree of the articularcartilage) 119899 number of oscillations (less than 300 is pathology of I Outebridge degree of the articular cartilage) and 119905 whole time of oscillations (less than150 is pathology of I Outebridge degree of the articular cartilage)

Table 3 Goniometry pendulum test in group B

Parameter Before therapy After therapyFollowup

Level of significance1 month 3 monthsMean SD Mean SD Mean SD Mean SD

120582

Operated 055 021 058 019 056 022 055 020 119875 gt 005

Nonoperated 048 021 043 019 044 022 045 020 lowast(in all comparisons)120573 [sminus1]

Operated 075 032 076 021 075 022 075 028 119875 gt 005

Non-operated 058 027 057 028 055 025 054 028 lowast(in all comparisons)119879 [s]

Operated 087 034 090 035 090 029 090 030 119875 gt 005

Non-operated 095 019 097 019 097 019 099 020 lowast(in all comparisons)119899

Operated 335 131 333 138 333 130 333 130 119875 gt 005

Non-operated 475 131 479 139 480 141 480 141 lowast(in all comparisons)119905 [s]

Operated 211 103 209 104 210 111 211 101 119875 gt 005

Non-operated 310 128 311 125 311 111 310 109 lowast(in all comparisons)lowastAnalysis of variance ANOVALegends120582 logarithm decrement of suppression (more than 065 is pathology of I Outebridge degree of the articular cartilage) 120573 suppression index (more than 085is pathology of I Outebridge degree of the articular cartilage) 119879 period of oscillations (less than 075 is pathology of I Outebridge degree of the articularcartilage) 119899 number of oscillations (less than 300 is pathology of I Outebridge degree of the articular cartilage) and 119905 whole time of oscillations (less than150 is pathology of I Outebridge degree of the articular cartilage)

8 BioMed Research International

only in the ES group In the ES group changes were morepronounced in hamstrings than in quadriceps and peakedat 48 h (quadriceps VAS scores = 220 plusmn 1 (0 at preex)hamstrings VAS scores = 315 plusmn 214 (0 at preex) hip flexionangle = 62 plusmn 5∘ (75 plusmn 6∘ at preex) CK activity = 3021 plusmn2693 IU sdot l minus 1 (136 plusmn 50 IU sdot l minus 1 at preex) The results of thestudy suggested the occurrence of muscle damage that couldhave been induced by the physiologically incorrect musclerecruitment inNMES and the resulting overratedmechanicalstress

In our study the NMES appeared to be safe for biome-chanics of knee joint Based on our previous experience wecan strongly recommend the goniometry pendulum test asuseful diagnostic method in physical therapy process [20]The purpose of this clinical study was to assess low frequencylow intensity magnetic fields in the enhancement of thephysical rehabilitation of patients after knee endoprosthesissurgery The study included 62 patients who underwent totalknee arthroplasty Group A consisted of 32 patients who werephysically rehabilitated Group B consisted of 30 patients whowere physically rehabilitated and treated additionally withpulsing magnetic fields (5mT 30Hz 20min once a day 5days weekly)Therapy lasted for 3 weeks for both groupsTherehabilitation process was evaluated using a goniometer ten-someter goniometry pendulum test Lysholm scale for kneefunction and a visual analogue scale (VAS) questionnaire forpain and activityThe pendulum test appeared very useful forprecise observation of biomechanical changes in knee jointduring therapy process The physical therapy decreased thelogarithm decrement of suppression (120582) by about 79 ingroup A and 96 in group B suppression index (120573) decreasedabout 11 in group A and 133 in group B The period ofoscillations increased by 49 in group A and 4 in group Bnumber of oscillations (119899) increased by 221 in group A and206 in group B The whole time of oscillations increased of298 in group A and 245 in group B

In our study we did not observe both early and longterm results (goniometry pendulum testour research is thefirst attempt in literature of using this apparatus in sport)any pathological changes in knee function after increasingthe strength and mass of quadriceps in use of NMESThe progress in muscle parameters did not have influencepathologically on knee function

41 Limitations of Study In our study soccer players aftera month of therapy with NMES + rehabilitation or onlyrehabilitation program (7 months after ACL reconstruc-tion) returned to sport and league competition what couldinterfere with follow-up observation We were not able todemonstrate a relationship between the pendulum test andmuscle dysfunction either in the study or from previousresearch using a similar protocol correlated with markersof muscle damage We tried to use objective measurementmethods but we did not collect data related to functionaloutcomes of which there are some they could have chosen(triple-hop crossover-hop and jump-landing test)

5 Conclusion

The results of this study show that NMES (presented parame-ters in experiment) is useful for strengthening the quadricepsmuscle in soccer athletes There is an evidence the benefit ofthe NMES in restoring quadriceps muscle mass and strengthof soccer players In our study the neuromuscular electricalstimulation appeared to be safe for biomechanics of kneejoint The pathological changes in knee function were notobserved

Conflict of Interests

The authors would like to certify that they have no commer-cial associations with the manufacturers of the equipmentdescribed in the paper or other conflict of interests

References

[1] S C Petterson R L Mizner J E Stevens et al ldquoImprovedfunction from progressive strengthening interventions aftertotal knee arthroplasty a randomized clinical trial with animbedded prospective cohortrdquo Arthritis Care and Research vol61 no 2 pp 174ndash183 2009

[2] C Krishnan and G N Williams ldquoFactors explaining chronicknee extensor strength deficits after ACL reconstructionrdquo Jour-nal of Orthopaedic Research vol 29 no 5 pp 633ndash640 2011

[3] D Adams D S Logerstedt A Hunter-Giordano M J Axeand L Snyder-Mackler ldquoCurrent concepts for anterior cruciateligament reconstruction a criterion-based rehabilitation pro-gressionrdquo Journal of Orthopaedics and Sports Physical Therapyvol 42 no 7 pp 601ndash614 2012

[4] J E Stevens-Lapsley J E Balter P Wolfe D G Eckhoff andW M Kohrt ldquoEarly neuromuscular electrical stimulation toimprove quadriceps muscle strength after total knee arthro-plasty a randomized controlled trialrdquo Physical Therapy vol 92no 2 pp 210ndash226 2012

[5] G J Yun M H Chun J Y Park and B R Kim ldquoThesynergic effects of mirror therapy and neuromuscular electricalstimulation for hand function in stroke patientsrdquo Annals ofRehabilitation Medicine vol 35 no 3 pp 316ndash322 2011

[6] R J Walls G McHugh D J OrsquoGorman N M Moyna and JM OrsquoByrne ldquoEffects of preoperative neuromuscular electricalstimulation on quadriceps strength and functional recovery intotal knee arthroplasty A pilot studyrdquo BMC MusculoskeletalDisorders vol 14 no 11 article 119 2010

[7] Y Guan P W Wacnik F Yang et al ldquoSpinal cord stimulation-induced analgesia electrical stimulation of dorsal column anddorsal roots attenuates dorsal horn neuronal excitability inneuropathic ratsrdquo Anesthesiology vol 113 no 6 pp 1392ndash14052010

[8] T Arakawa A Katada H Shigyo et al ldquoElectrical stimulationprevents apoptosis in denervated skeletal musclerdquo NeuroReha-bilitation vol 27 no 2 pp 147ndash154 2010

[9] M R Gersh Electrotherapy in Rehabilitation ContemporaryPerspectives in Rehabilitation (Book 7) FA Davis CompanyPhiladelphia Pa USA 1994

[10] J H Kim M L Trew A J Pullan and O Rohrle ldquoSimulatinga dual-array electrode configuration to investigate the influence

BioMed Research International 9

of skeletal muscle fatigue following functional electrical stim-ulationrdquo Computers in Biology and Medicine vol 42 no 9 pp915ndash924 2012

[11] T Paillard F Noe N Bernard P Dupui and C HazardldquoEffects of two types of neuromuscular electrical stimulationtraining on vertical jump performancerdquo Journal of Strength andConditioning Research vol 22 no 4 pp 1273ndash1278 2008

[12] I Vivodtzev R Debigare P Gagnon et al ldquoFunctional andmuscular effects of neuromuscular electrical stimulation inpatients with severe COPD a randomized clinical trialrdquo Chestvol 141 no 3 pp 716ndash725 2012

[13] L Snyder-Mackler A Delitto S L Bailey and S W StralkaldquoStrength of the quadriceps femoris muscle and functionalrecovery after reconstruction of the anterior cruciate ligamentA prospective randomized clinical trial of electrical stimula-tionrdquo Journal of Bone and Joint Surgery A vol 77 no 8 pp 1166ndash1173 1995

[14] M G Parker M J Bennett M A Hieb A C Hollar and A ARoe ldquoStrength response in human quadriceps femoris muscleduring 2 neuromuscular electrical stimulation programsrdquo Jour-nal of Orthopaedic and Sports Physical Therapy vol 33 no 12pp 719ndash726 2003

[15] J W Bellew Z Beiswanger E Freeman C Gaerte and JTrafton ldquoInterferential and burst-modulated biphasic pulsedcurrents yield greater muscular force than Russian currentrdquoPhysiotherapy Theory and Practice vol 28 no 5 pp 384ndash3902012

[16] A Mysliwiec E Saulicz M Kuszewski M Kokosz and TWolny ldquoAssessment of the influence of Saunders tractionand transcutaneous electrical nerve stimulation on hand gripforce in patients with neck painrdquo Ortopedia TraumatologiaRehabilitacja vol 13 no 1 pp 37ndash44 2011

[17] M Vanderthommen M Triffaux Ch Demoulin J MCrielaard and J L Croisier ldquoAlteration of muscle functionafter electrical stimulation bout of knee extensors and flexorsrdquoJournal of Sports Science andMedicine vol 11 pp 592ndash599 2012

[18] L Bax F Staes and A Verhagen ldquoDoes neuromuscular electri-cal stimulation strengthen the quadriceps femoris A systematicreview of randomised controlled trialsrdquo SportsMedicine vol 35no 3 pp 191ndash212 2005

[19] P Banerjee B Caulfield L Crowe and A Clark ldquoProlongedelectrical muscle stimulation exercise improves strength andaerobic capacity in healthy sedentary adultsrdquo Journal of AppliedPhysiology vol 99 no 6 pp 2307ndash2311 2005

[20] E Błaszczak A Franek J Taradaj JWiduchowski and J Klim-czak ldquoAssessment of the efficacy and safety of low frequencylow intensity magnetic fields in patients after knee endopros-thesis plasty Part 2 a clinical studyrdquo Bioelectromagnetics vol30 no 2 pp 152ndash158 2009

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 7: Clinical Study The Effect of NeuroMuscular Electrical Stimulation …downloads.hindawi.com/journals/bmri/2013/802534.pdf · 2019. 7. 31. · (ii) single-leg plyometrics, cutting/pivoting

BioMed Research International 7

Table 2 Goniometry pendulum test in group A

Parameter Before therapy After therapyFollowup

Level of significance1 month 3 monthsMean SD Mean SD Mean SD Mean SD

120582

Operated 057 019 056 016 055 020 055 022 119875 gt 005

Nonoperated 047 018 045 019 046 022 046 022 lowast(in all comparisons)120573 [sminus1]

Operated 077 030 077 028 074 022 075 030 119875 gt 005

Non-operated 057 030 056 031 053 023 054 030 lowast(in all comparisons)119879 [s]

Operated 089 030 094 030 095 027 093 030 119875 gt 005

Non-operated 095 022 099 019 099 019 098 021 lowast(in all comparisons)119899

Operated 332 122 332 143 331 121 332 125 119875 gt 005

Non-operated 478 122 487 145 486 121 487 121 lowast(in all comparisons)119905 [s]

Operated 207 122 207 152 212 110 213 121 119875 gt 005

Non-operated 304 120 304 145 301 113 301 113 lowast(in all comparisons)lowastAnalysis of variance ANOVALegends120582 logarithm decrement of suppression (more than 065 is pathology of I Outebridge degree of the articular cartilage) 120573 suppression index (more than 085is pathology of I Outebridge degree of the articular cartilage) 119879 period of oscillations (less than 075 is pathology of I Outebridge degree of the articularcartilage) 119899 number of oscillations (less than 300 is pathology of I Outebridge degree of the articular cartilage) and 119905 whole time of oscillations (less than150 is pathology of I Outebridge degree of the articular cartilage)

Table 3 Goniometry pendulum test in group B

Parameter Before therapy After therapyFollowup

Level of significance1 month 3 monthsMean SD Mean SD Mean SD Mean SD

120582

Operated 055 021 058 019 056 022 055 020 119875 gt 005

Nonoperated 048 021 043 019 044 022 045 020 lowast(in all comparisons)120573 [sminus1]

Operated 075 032 076 021 075 022 075 028 119875 gt 005

Non-operated 058 027 057 028 055 025 054 028 lowast(in all comparisons)119879 [s]

Operated 087 034 090 035 090 029 090 030 119875 gt 005

Non-operated 095 019 097 019 097 019 099 020 lowast(in all comparisons)119899

Operated 335 131 333 138 333 130 333 130 119875 gt 005

Non-operated 475 131 479 139 480 141 480 141 lowast(in all comparisons)119905 [s]

Operated 211 103 209 104 210 111 211 101 119875 gt 005

Non-operated 310 128 311 125 311 111 310 109 lowast(in all comparisons)lowastAnalysis of variance ANOVALegends120582 logarithm decrement of suppression (more than 065 is pathology of I Outebridge degree of the articular cartilage) 120573 suppression index (more than 085is pathology of I Outebridge degree of the articular cartilage) 119879 period of oscillations (less than 075 is pathology of I Outebridge degree of the articularcartilage) 119899 number of oscillations (less than 300 is pathology of I Outebridge degree of the articular cartilage) and 119905 whole time of oscillations (less than150 is pathology of I Outebridge degree of the articular cartilage)

8 BioMed Research International

only in the ES group In the ES group changes were morepronounced in hamstrings than in quadriceps and peakedat 48 h (quadriceps VAS scores = 220 plusmn 1 (0 at preex)hamstrings VAS scores = 315 plusmn 214 (0 at preex) hip flexionangle = 62 plusmn 5∘ (75 plusmn 6∘ at preex) CK activity = 3021 plusmn2693 IU sdot l minus 1 (136 plusmn 50 IU sdot l minus 1 at preex) The results of thestudy suggested the occurrence of muscle damage that couldhave been induced by the physiologically incorrect musclerecruitment inNMES and the resulting overratedmechanicalstress

In our study the NMES appeared to be safe for biome-chanics of knee joint Based on our previous experience wecan strongly recommend the goniometry pendulum test asuseful diagnostic method in physical therapy process [20]The purpose of this clinical study was to assess low frequencylow intensity magnetic fields in the enhancement of thephysical rehabilitation of patients after knee endoprosthesissurgery The study included 62 patients who underwent totalknee arthroplasty Group A consisted of 32 patients who werephysically rehabilitated Group B consisted of 30 patients whowere physically rehabilitated and treated additionally withpulsing magnetic fields (5mT 30Hz 20min once a day 5days weekly)Therapy lasted for 3 weeks for both groupsTherehabilitation process was evaluated using a goniometer ten-someter goniometry pendulum test Lysholm scale for kneefunction and a visual analogue scale (VAS) questionnaire forpain and activityThe pendulum test appeared very useful forprecise observation of biomechanical changes in knee jointduring therapy process The physical therapy decreased thelogarithm decrement of suppression (120582) by about 79 ingroup A and 96 in group B suppression index (120573) decreasedabout 11 in group A and 133 in group B The period ofoscillations increased by 49 in group A and 4 in group Bnumber of oscillations (119899) increased by 221 in group A and206 in group B The whole time of oscillations increased of298 in group A and 245 in group B

In our study we did not observe both early and longterm results (goniometry pendulum testour research is thefirst attempt in literature of using this apparatus in sport)any pathological changes in knee function after increasingthe strength and mass of quadriceps in use of NMESThe progress in muscle parameters did not have influencepathologically on knee function

41 Limitations of Study In our study soccer players aftera month of therapy with NMES + rehabilitation or onlyrehabilitation program (7 months after ACL reconstruc-tion) returned to sport and league competition what couldinterfere with follow-up observation We were not able todemonstrate a relationship between the pendulum test andmuscle dysfunction either in the study or from previousresearch using a similar protocol correlated with markersof muscle damage We tried to use objective measurementmethods but we did not collect data related to functionaloutcomes of which there are some they could have chosen(triple-hop crossover-hop and jump-landing test)

5 Conclusion

The results of this study show that NMES (presented parame-ters in experiment) is useful for strengthening the quadricepsmuscle in soccer athletes There is an evidence the benefit ofthe NMES in restoring quadriceps muscle mass and strengthof soccer players In our study the neuromuscular electricalstimulation appeared to be safe for biomechanics of kneejoint The pathological changes in knee function were notobserved

Conflict of Interests

The authors would like to certify that they have no commer-cial associations with the manufacturers of the equipmentdescribed in the paper or other conflict of interests

References

[1] S C Petterson R L Mizner J E Stevens et al ldquoImprovedfunction from progressive strengthening interventions aftertotal knee arthroplasty a randomized clinical trial with animbedded prospective cohortrdquo Arthritis Care and Research vol61 no 2 pp 174ndash183 2009

[2] C Krishnan and G N Williams ldquoFactors explaining chronicknee extensor strength deficits after ACL reconstructionrdquo Jour-nal of Orthopaedic Research vol 29 no 5 pp 633ndash640 2011

[3] D Adams D S Logerstedt A Hunter-Giordano M J Axeand L Snyder-Mackler ldquoCurrent concepts for anterior cruciateligament reconstruction a criterion-based rehabilitation pro-gressionrdquo Journal of Orthopaedics and Sports Physical Therapyvol 42 no 7 pp 601ndash614 2012

[4] J E Stevens-Lapsley J E Balter P Wolfe D G Eckhoff andW M Kohrt ldquoEarly neuromuscular electrical stimulation toimprove quadriceps muscle strength after total knee arthro-plasty a randomized controlled trialrdquo Physical Therapy vol 92no 2 pp 210ndash226 2012

[5] G J Yun M H Chun J Y Park and B R Kim ldquoThesynergic effects of mirror therapy and neuromuscular electricalstimulation for hand function in stroke patientsrdquo Annals ofRehabilitation Medicine vol 35 no 3 pp 316ndash322 2011

[6] R J Walls G McHugh D J OrsquoGorman N M Moyna and JM OrsquoByrne ldquoEffects of preoperative neuromuscular electricalstimulation on quadriceps strength and functional recovery intotal knee arthroplasty A pilot studyrdquo BMC MusculoskeletalDisorders vol 14 no 11 article 119 2010

[7] Y Guan P W Wacnik F Yang et al ldquoSpinal cord stimulation-induced analgesia electrical stimulation of dorsal column anddorsal roots attenuates dorsal horn neuronal excitability inneuropathic ratsrdquo Anesthesiology vol 113 no 6 pp 1392ndash14052010

[8] T Arakawa A Katada H Shigyo et al ldquoElectrical stimulationprevents apoptosis in denervated skeletal musclerdquo NeuroReha-bilitation vol 27 no 2 pp 147ndash154 2010

[9] M R Gersh Electrotherapy in Rehabilitation ContemporaryPerspectives in Rehabilitation (Book 7) FA Davis CompanyPhiladelphia Pa USA 1994

[10] J H Kim M L Trew A J Pullan and O Rohrle ldquoSimulatinga dual-array electrode configuration to investigate the influence

BioMed Research International 9

of skeletal muscle fatigue following functional electrical stim-ulationrdquo Computers in Biology and Medicine vol 42 no 9 pp915ndash924 2012

[11] T Paillard F Noe N Bernard P Dupui and C HazardldquoEffects of two types of neuromuscular electrical stimulationtraining on vertical jump performancerdquo Journal of Strength andConditioning Research vol 22 no 4 pp 1273ndash1278 2008

[12] I Vivodtzev R Debigare P Gagnon et al ldquoFunctional andmuscular effects of neuromuscular electrical stimulation inpatients with severe COPD a randomized clinical trialrdquo Chestvol 141 no 3 pp 716ndash725 2012

[13] L Snyder-Mackler A Delitto S L Bailey and S W StralkaldquoStrength of the quadriceps femoris muscle and functionalrecovery after reconstruction of the anterior cruciate ligamentA prospective randomized clinical trial of electrical stimula-tionrdquo Journal of Bone and Joint Surgery A vol 77 no 8 pp 1166ndash1173 1995

[14] M G Parker M J Bennett M A Hieb A C Hollar and A ARoe ldquoStrength response in human quadriceps femoris muscleduring 2 neuromuscular electrical stimulation programsrdquo Jour-nal of Orthopaedic and Sports Physical Therapy vol 33 no 12pp 719ndash726 2003

[15] J W Bellew Z Beiswanger E Freeman C Gaerte and JTrafton ldquoInterferential and burst-modulated biphasic pulsedcurrents yield greater muscular force than Russian currentrdquoPhysiotherapy Theory and Practice vol 28 no 5 pp 384ndash3902012

[16] A Mysliwiec E Saulicz M Kuszewski M Kokosz and TWolny ldquoAssessment of the influence of Saunders tractionand transcutaneous electrical nerve stimulation on hand gripforce in patients with neck painrdquo Ortopedia TraumatologiaRehabilitacja vol 13 no 1 pp 37ndash44 2011

[17] M Vanderthommen M Triffaux Ch Demoulin J MCrielaard and J L Croisier ldquoAlteration of muscle functionafter electrical stimulation bout of knee extensors and flexorsrdquoJournal of Sports Science andMedicine vol 11 pp 592ndash599 2012

[18] L Bax F Staes and A Verhagen ldquoDoes neuromuscular electri-cal stimulation strengthen the quadriceps femoris A systematicreview of randomised controlled trialsrdquo SportsMedicine vol 35no 3 pp 191ndash212 2005

[19] P Banerjee B Caulfield L Crowe and A Clark ldquoProlongedelectrical muscle stimulation exercise improves strength andaerobic capacity in healthy sedentary adultsrdquo Journal of AppliedPhysiology vol 99 no 6 pp 2307ndash2311 2005

[20] E Błaszczak A Franek J Taradaj JWiduchowski and J Klim-czak ldquoAssessment of the efficacy and safety of low frequencylow intensity magnetic fields in patients after knee endopros-thesis plasty Part 2 a clinical studyrdquo Bioelectromagnetics vol30 no 2 pp 152ndash158 2009

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 8: Clinical Study The Effect of NeuroMuscular Electrical Stimulation …downloads.hindawi.com/journals/bmri/2013/802534.pdf · 2019. 7. 31. · (ii) single-leg plyometrics, cutting/pivoting

8 BioMed Research International

only in the ES group In the ES group changes were morepronounced in hamstrings than in quadriceps and peakedat 48 h (quadriceps VAS scores = 220 plusmn 1 (0 at preex)hamstrings VAS scores = 315 plusmn 214 (0 at preex) hip flexionangle = 62 plusmn 5∘ (75 plusmn 6∘ at preex) CK activity = 3021 plusmn2693 IU sdot l minus 1 (136 plusmn 50 IU sdot l minus 1 at preex) The results of thestudy suggested the occurrence of muscle damage that couldhave been induced by the physiologically incorrect musclerecruitment inNMES and the resulting overratedmechanicalstress

In our study the NMES appeared to be safe for biome-chanics of knee joint Based on our previous experience wecan strongly recommend the goniometry pendulum test asuseful diagnostic method in physical therapy process [20]The purpose of this clinical study was to assess low frequencylow intensity magnetic fields in the enhancement of thephysical rehabilitation of patients after knee endoprosthesissurgery The study included 62 patients who underwent totalknee arthroplasty Group A consisted of 32 patients who werephysically rehabilitated Group B consisted of 30 patients whowere physically rehabilitated and treated additionally withpulsing magnetic fields (5mT 30Hz 20min once a day 5days weekly)Therapy lasted for 3 weeks for both groupsTherehabilitation process was evaluated using a goniometer ten-someter goniometry pendulum test Lysholm scale for kneefunction and a visual analogue scale (VAS) questionnaire forpain and activityThe pendulum test appeared very useful forprecise observation of biomechanical changes in knee jointduring therapy process The physical therapy decreased thelogarithm decrement of suppression (120582) by about 79 ingroup A and 96 in group B suppression index (120573) decreasedabout 11 in group A and 133 in group B The period ofoscillations increased by 49 in group A and 4 in group Bnumber of oscillations (119899) increased by 221 in group A and206 in group B The whole time of oscillations increased of298 in group A and 245 in group B

In our study we did not observe both early and longterm results (goniometry pendulum testour research is thefirst attempt in literature of using this apparatus in sport)any pathological changes in knee function after increasingthe strength and mass of quadriceps in use of NMESThe progress in muscle parameters did not have influencepathologically on knee function

41 Limitations of Study In our study soccer players aftera month of therapy with NMES + rehabilitation or onlyrehabilitation program (7 months after ACL reconstruc-tion) returned to sport and league competition what couldinterfere with follow-up observation We were not able todemonstrate a relationship between the pendulum test andmuscle dysfunction either in the study or from previousresearch using a similar protocol correlated with markersof muscle damage We tried to use objective measurementmethods but we did not collect data related to functionaloutcomes of which there are some they could have chosen(triple-hop crossover-hop and jump-landing test)

5 Conclusion

The results of this study show that NMES (presented parame-ters in experiment) is useful for strengthening the quadricepsmuscle in soccer athletes There is an evidence the benefit ofthe NMES in restoring quadriceps muscle mass and strengthof soccer players In our study the neuromuscular electricalstimulation appeared to be safe for biomechanics of kneejoint The pathological changes in knee function were notobserved

Conflict of Interests

The authors would like to certify that they have no commer-cial associations with the manufacturers of the equipmentdescribed in the paper or other conflict of interests

References

[1] S C Petterson R L Mizner J E Stevens et al ldquoImprovedfunction from progressive strengthening interventions aftertotal knee arthroplasty a randomized clinical trial with animbedded prospective cohortrdquo Arthritis Care and Research vol61 no 2 pp 174ndash183 2009

[2] C Krishnan and G N Williams ldquoFactors explaining chronicknee extensor strength deficits after ACL reconstructionrdquo Jour-nal of Orthopaedic Research vol 29 no 5 pp 633ndash640 2011

[3] D Adams D S Logerstedt A Hunter-Giordano M J Axeand L Snyder-Mackler ldquoCurrent concepts for anterior cruciateligament reconstruction a criterion-based rehabilitation pro-gressionrdquo Journal of Orthopaedics and Sports Physical Therapyvol 42 no 7 pp 601ndash614 2012

[4] J E Stevens-Lapsley J E Balter P Wolfe D G Eckhoff andW M Kohrt ldquoEarly neuromuscular electrical stimulation toimprove quadriceps muscle strength after total knee arthro-plasty a randomized controlled trialrdquo Physical Therapy vol 92no 2 pp 210ndash226 2012

[5] G J Yun M H Chun J Y Park and B R Kim ldquoThesynergic effects of mirror therapy and neuromuscular electricalstimulation for hand function in stroke patientsrdquo Annals ofRehabilitation Medicine vol 35 no 3 pp 316ndash322 2011

[6] R J Walls G McHugh D J OrsquoGorman N M Moyna and JM OrsquoByrne ldquoEffects of preoperative neuromuscular electricalstimulation on quadriceps strength and functional recovery intotal knee arthroplasty A pilot studyrdquo BMC MusculoskeletalDisorders vol 14 no 11 article 119 2010

[7] Y Guan P W Wacnik F Yang et al ldquoSpinal cord stimulation-induced analgesia electrical stimulation of dorsal column anddorsal roots attenuates dorsal horn neuronal excitability inneuropathic ratsrdquo Anesthesiology vol 113 no 6 pp 1392ndash14052010

[8] T Arakawa A Katada H Shigyo et al ldquoElectrical stimulationprevents apoptosis in denervated skeletal musclerdquo NeuroReha-bilitation vol 27 no 2 pp 147ndash154 2010

[9] M R Gersh Electrotherapy in Rehabilitation ContemporaryPerspectives in Rehabilitation (Book 7) FA Davis CompanyPhiladelphia Pa USA 1994

[10] J H Kim M L Trew A J Pullan and O Rohrle ldquoSimulatinga dual-array electrode configuration to investigate the influence

BioMed Research International 9

of skeletal muscle fatigue following functional electrical stim-ulationrdquo Computers in Biology and Medicine vol 42 no 9 pp915ndash924 2012

[11] T Paillard F Noe N Bernard P Dupui and C HazardldquoEffects of two types of neuromuscular electrical stimulationtraining on vertical jump performancerdquo Journal of Strength andConditioning Research vol 22 no 4 pp 1273ndash1278 2008

[12] I Vivodtzev R Debigare P Gagnon et al ldquoFunctional andmuscular effects of neuromuscular electrical stimulation inpatients with severe COPD a randomized clinical trialrdquo Chestvol 141 no 3 pp 716ndash725 2012

[13] L Snyder-Mackler A Delitto S L Bailey and S W StralkaldquoStrength of the quadriceps femoris muscle and functionalrecovery after reconstruction of the anterior cruciate ligamentA prospective randomized clinical trial of electrical stimula-tionrdquo Journal of Bone and Joint Surgery A vol 77 no 8 pp 1166ndash1173 1995

[14] M G Parker M J Bennett M A Hieb A C Hollar and A ARoe ldquoStrength response in human quadriceps femoris muscleduring 2 neuromuscular electrical stimulation programsrdquo Jour-nal of Orthopaedic and Sports Physical Therapy vol 33 no 12pp 719ndash726 2003

[15] J W Bellew Z Beiswanger E Freeman C Gaerte and JTrafton ldquoInterferential and burst-modulated biphasic pulsedcurrents yield greater muscular force than Russian currentrdquoPhysiotherapy Theory and Practice vol 28 no 5 pp 384ndash3902012

[16] A Mysliwiec E Saulicz M Kuszewski M Kokosz and TWolny ldquoAssessment of the influence of Saunders tractionand transcutaneous electrical nerve stimulation on hand gripforce in patients with neck painrdquo Ortopedia TraumatologiaRehabilitacja vol 13 no 1 pp 37ndash44 2011

[17] M Vanderthommen M Triffaux Ch Demoulin J MCrielaard and J L Croisier ldquoAlteration of muscle functionafter electrical stimulation bout of knee extensors and flexorsrdquoJournal of Sports Science andMedicine vol 11 pp 592ndash599 2012

[18] L Bax F Staes and A Verhagen ldquoDoes neuromuscular electri-cal stimulation strengthen the quadriceps femoris A systematicreview of randomised controlled trialsrdquo SportsMedicine vol 35no 3 pp 191ndash212 2005

[19] P Banerjee B Caulfield L Crowe and A Clark ldquoProlongedelectrical muscle stimulation exercise improves strength andaerobic capacity in healthy sedentary adultsrdquo Journal of AppliedPhysiology vol 99 no 6 pp 2307ndash2311 2005

[20] E Błaszczak A Franek J Taradaj JWiduchowski and J Klim-czak ldquoAssessment of the efficacy and safety of low frequencylow intensity magnetic fields in patients after knee endopros-thesis plasty Part 2 a clinical studyrdquo Bioelectromagnetics vol30 no 2 pp 152ndash158 2009

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 9: Clinical Study The Effect of NeuroMuscular Electrical Stimulation …downloads.hindawi.com/journals/bmri/2013/802534.pdf · 2019. 7. 31. · (ii) single-leg plyometrics, cutting/pivoting

BioMed Research International 9

of skeletal muscle fatigue following functional electrical stim-ulationrdquo Computers in Biology and Medicine vol 42 no 9 pp915ndash924 2012

[11] T Paillard F Noe N Bernard P Dupui and C HazardldquoEffects of two types of neuromuscular electrical stimulationtraining on vertical jump performancerdquo Journal of Strength andConditioning Research vol 22 no 4 pp 1273ndash1278 2008

[12] I Vivodtzev R Debigare P Gagnon et al ldquoFunctional andmuscular effects of neuromuscular electrical stimulation inpatients with severe COPD a randomized clinical trialrdquo Chestvol 141 no 3 pp 716ndash725 2012

[13] L Snyder-Mackler A Delitto S L Bailey and S W StralkaldquoStrength of the quadriceps femoris muscle and functionalrecovery after reconstruction of the anterior cruciate ligamentA prospective randomized clinical trial of electrical stimula-tionrdquo Journal of Bone and Joint Surgery A vol 77 no 8 pp 1166ndash1173 1995

[14] M G Parker M J Bennett M A Hieb A C Hollar and A ARoe ldquoStrength response in human quadriceps femoris muscleduring 2 neuromuscular electrical stimulation programsrdquo Jour-nal of Orthopaedic and Sports Physical Therapy vol 33 no 12pp 719ndash726 2003

[15] J W Bellew Z Beiswanger E Freeman C Gaerte and JTrafton ldquoInterferential and burst-modulated biphasic pulsedcurrents yield greater muscular force than Russian currentrdquoPhysiotherapy Theory and Practice vol 28 no 5 pp 384ndash3902012

[16] A Mysliwiec E Saulicz M Kuszewski M Kokosz and TWolny ldquoAssessment of the influence of Saunders tractionand transcutaneous electrical nerve stimulation on hand gripforce in patients with neck painrdquo Ortopedia TraumatologiaRehabilitacja vol 13 no 1 pp 37ndash44 2011

[17] M Vanderthommen M Triffaux Ch Demoulin J MCrielaard and J L Croisier ldquoAlteration of muscle functionafter electrical stimulation bout of knee extensors and flexorsrdquoJournal of Sports Science andMedicine vol 11 pp 592ndash599 2012

[18] L Bax F Staes and A Verhagen ldquoDoes neuromuscular electri-cal stimulation strengthen the quadriceps femoris A systematicreview of randomised controlled trialsrdquo SportsMedicine vol 35no 3 pp 191ndash212 2005

[19] P Banerjee B Caulfield L Crowe and A Clark ldquoProlongedelectrical muscle stimulation exercise improves strength andaerobic capacity in healthy sedentary adultsrdquo Journal of AppliedPhysiology vol 99 no 6 pp 2307ndash2311 2005

[20] E Błaszczak A Franek J Taradaj JWiduchowski and J Klim-czak ldquoAssessment of the efficacy and safety of low frequencylow intensity magnetic fields in patients after knee endopros-thesis plasty Part 2 a clinical studyrdquo Bioelectromagnetics vol30 no 2 pp 152ndash158 2009

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 10: Clinical Study The Effect of NeuroMuscular Electrical Stimulation …downloads.hindawi.com/journals/bmri/2013/802534.pdf · 2019. 7. 31. · (ii) single-leg plyometrics, cutting/pivoting

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom