Clinical Study Whole-Body Electromyostimulation to Fight...

8
Clinical Study Whole-Body Electromyostimulation to Fight Osteopenia in Elderly Females: The Randomized Controlled Training and Electrostimulation Trial (TEST-III) Simon von Stengel, Michael Bebenek, Klaus Engelke, and Wolfgang Kemmler Institute of Medical Physics, University of Erlangen-N¨ urnberg, 91052 Erlangen, Germany Correspondence should be addressed to Simon von Stengel; [email protected] Received 7 October 2014; Revised 7 January 2015; Accepted 12 January 2015 Academic Editor: Harri Siev¨ anen Copyright © 2015 Simon von Stengel 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. Whole-body electromyostimulation (WB-EMS) has been shown to be effective in increasing muscle strength and mass in elderly women. Because of the interaction of muscles and bones, these adaptions might be related to changes in bone parameters. 76 community-living osteopenic women 70 years and older were randomly assigned to either a WB-EMS group ( = 38) or a control group (CG: = 38). e WB-EMS group performed 3 sessions every 14 days for one year while the CG performed gymnastics containing identical exercises without EMS. Primary study endpoints were bone mineral density (BMD) at lumbar spine (LS) and total hip (thip) as assessed by DXA. Aſter 54 weeks of intervention, borderline nonsignificant intergroup differences were determined for LS-BMD (WB-EMS: 0.6 ± 2.5% versus CG −0.7 ± 2.5%, = .051) but not for thip-BMD (WB-EMS: −1.1 ± 1.9% versus CG: −0.8 ± 2.3%, = .771). With respect to secondary endpoints, there was a gain in lean body mass (LBM) of 1.5% ( = .006) and an increase in grip strength of 8.4% ( = .000) in the WB-EMS group compared to CG. WB-EMS effects on bone are less pronounced than previously reported effects on muscle mass. However, for subjects unable or unwilling to perform intense exercise programs, WB-EMS may be an option for maintaining BMD at the LS. 1. Introduction Exercise maintains bone mass. But do people maintain exercise? [1]. Indeed, the majority of elderly subjects in Germany [2] or the US [3] fall far short of the exercise doses recommended for consistently impacting Bone Mineral Den- sity [46]. A novel training technology, called whole-body electromyostimulation (WB-EMS), may increase effects of moderate exercise on the musculoskeletal system and thus might be a time-saving and feasible option for subjects unable or unwilling to perform strenuous conventional exercise. Unlike local EMS application, WB-EMS technology simul- taneously stimulates up to 14–18 regions or 8–12 muscle groups with up to 2.800 cm 2 electrode area. Although EMS- technology primarily focuses on muscle by activating muscle contraction and directly stimulating muscle protein synthesis rate [7], there is some evidence that this mode of muscle stimulation also impacts bone [8]. However, human trials determined the effect of EMS- application on bone only in the case of disuse-induced bone loss in spinal cord injury (SCI) patients. In these studies EMS was applied either locally only on plantarflexors or as functional electrostimulation (FES) activating isolated thigh muscles to induce leg cycling movements on ergometry or knee extention movements on strength machines. One meta- analysis [9] and two reviews [10, 11] analyzed and discussed the effect of EMS and FES on BMD in SCI and found positive results. Basic mechanisms of bone adaptions to disuse aſter SCI and following EMS training are reviewed by Dudley- Javoroski and Shields [12]. However, conclusions drawn from studies determining the effect of EMS on bone in the specific situation of disuse in paralyzed patients are not valid for the normal population and, furthermore, the transferability of results of local EMS studies on the WB-EMS technology is rather questionable. Hindawi Publishing Corporation Journal of Osteoporosis Volume 2015, Article ID 643520, 7 pages http://dx.doi.org/10.1155/2015/643520

Transcript of Clinical Study Whole-Body Electromyostimulation to Fight...

Page 1: Clinical Study Whole-Body Electromyostimulation to Fight ...downloads.hindawi.com/journals/jos/2015/643520.pdf · e Training and Electrostimulation Trial (TEST) project is a series

Clinical StudyWhole-Body Electromyostimulation to Fight Osteopeniain Elderly Females The Randomized Controlled Trainingand Electrostimulation Trial (TEST-III)

Simon von Stengel Michael Bebenek Klaus Engelke and Wolfgang Kemmler

Institute of Medical Physics University of Erlangen-Nurnberg 91052 Erlangen Germany

Correspondence should be addressed to Simon von Stengel simonvonstengelimpuni-erlangende

Received 7 October 2014 Revised 7 January 2015 Accepted 12 January 2015

Academic Editor Harri Sievanen

Copyright copy 2015 Simon von Stengel et al This is an open access article distributed under the Creative Commons AttributionLicense which permits unrestricted use distribution and reproduction in any medium provided the original work is properlycited

Whole-body electromyostimulation (WB-EMS) has been shown to be effective in increasing muscle strength and mass in elderlywomen Because of the interaction of muscles and bones these adaptions might be related to changes in bone parameters 76community-living osteopenic women 70 years and older were randomly assigned to either a WB-EMS group (119899 = 38) or a controlgroup (CG 119899 = 38) The WB-EMS group performed 3 sessions every 14 days for one year while the CG performed gymnasticscontaining identical exercises without EMS Primary study endpoints were bone mineral density (BMD) at lumbar spine (LS)and total hip (thip) as assessed by DXA After 54 weeks of intervention borderline nonsignificant intergroup differences weredetermined for LS-BMD (WB-EMS 06 plusmn 25 versus CG minus07 plusmn 25 119875 = 051) but not for thip-BMD (WB-EMS minus11 plusmn 19versus CG minus08 plusmn 23 119875 = 771) With respect to secondary endpoints there was a gain in lean body mass (LBM) of 15(119875 = 006) and an increase in grip strength of 84 (119875 = 000) in the WB-EMS group compared to CG WB-EMS effects on boneare less pronounced than previously reported effects on muscle mass However for subjects unable or unwilling to perform intenseexercise programs WB-EMS may be an option for maintaining BMD at the LS

1 Introduction

Exercise maintains bone mass But do people maintainexercise [1] Indeed the majority of elderly subjects inGermany [2] or the US [3] fall far short of the exercise dosesrecommended for consistently impacting BoneMineral Den-sity [4ndash6] A novel training technology called whole-bodyelectromyostimulation (WB-EMS) may increase effects ofmoderate exercise on the musculoskeletal system and thusmight be a time-saving and feasible option for subjects unableor unwilling to perform strenuous conventional exerciseUnlike local EMS application WB-EMS technology simul-taneously stimulates up to 14ndash18 regions or 8ndash12 musclegroups with up to 2800 cm2 electrode area Although EMS-technology primarily focuses on muscle by activating musclecontraction and directly stimulatingmuscle protein synthesisrate [7] there is some evidence that this mode of musclestimulation also impacts bone [8]

However human trials determined the effect of EMS-application on bone only in the case of disuse-induced boneloss in spinal cord injury (SCI) patients In these studiesEMS was applied either locally only on plantarflexors or asfunctional electrostimulation (FES) activating isolated thighmuscles to induce leg cycling movements on ergometry orknee extentionmovements on strengthmachines Onemeta-analysis [9] and two reviews [10 11] analyzed and discussedthe effect of EMS and FES on BMD in SCI and found positiveresults Basic mechanisms of bone adaptions to disuse afterSCI and following EMS training are reviewed by Dudley-Javoroski and Shields [12] However conclusions drawn fromstudies determining the effect of EMS on bone in the specificsituation of disuse in paralyzed patients are not valid for thenormal population and furthermore the transferability ofresults of local EMS studies on the WB-EMS technology israther questionable

Hindawi Publishing CorporationJournal of OsteoporosisVolume 2015 Article ID 643520 7 pageshttpdxdoiorg1011552015643520

2 Journal of Osteoporosis

In the present study we evaluated the impact ofWB-EMSon BMD in sedentary lean and osteopenic elderly femalesa cohort at high risk for fractures The main hypothesis ofthis trial was that WB-EMS training significantly increasesBMD at the lumbar spine compared with a control groupOur secondary hypothesis was thatWB-EMS training signif-icantly impacts BMD at the proximal femur compared withthe control group Secondary endpoints concerning bodycomposition and strength are published elsewhere [13]

2 Materials and Methods

The Training and Electrostimulation Trial (TEST) projectis a series of studies that determine the effect of WB-EMSon parameters related to risk factors and diseases of elderlysubjects In the present study TEST-III is a randomizedcontrolled trial (RCT) that evaluated the effect of whole-body electromyostimulation (WB-EMS) on osteoporosis inlean sedentary elderly females with osteopenia To determinethe isolated effect of WB-EMS we implemented an activecontrol group which performed identical movements ascarried out during the WB-EMS session The study protocolwas approved by the Ethical Committee of the Friedrich-Alexander University Erlangen-Nuremberg (FAU) Germany(Ethik Antrag 4184) and the German Radiation SafetyAgency (Z 5-224622-2010-027) Written informed consentwas obtained from all subjects prior to the study entry TEST-III was conducted from November 2010 through July 2012 atthe Institute of Medical Physics FAU Germany and is fullyregistered under wwwclinicaltrialsgov (NCT01296776)

21 Participants All female subjects (9256 women) 70 yearsand older living in the area of Erlangen Germany werecontacted by personal letters Though eligibility criteria forthe trial (Figure 1) already had been listed in the letter 272subjects of the 451 women who responded had to be excludedafter phone interviews because they (a) did not meet ourcriteria for ldquoleannessrdquo (body weight (kg) gt (body height (cm)minus 100)) (b) had exercised more than 1 hour per week duringthe last 10 years (c) reported contraindications (ie totalendoprosthesis abdomengroin hernia epilepsy and cardiacarrhythmia) for WB-EMS intervention and (d) reporteddiseases or medication affecting our primary endpoints

179 women were invited to our lab to determine bodycomposition and bone status After measuring body weightand height with calibrated devices and determining BMD atthe lumbar spine and proximal femur 103 women had to beexcluded because they did not meet our inclusion criterionsof ldquoleannessrdquo or osteopenia (BMD lt 1 SD T-Score) (Figure 1)

The 76 remaining subjects were assigned into two studygroups using computerized block randomization stratifiedfor age (block size 119899 = 2) by an external statistician to ensureallocation concealment Table 1 lists baseline characteristicsof the WB-EMS and the control group No correspondingintergroup differences were observed

22 Interventions WB-EMS group performed 54 weeks ofconsecutive WB-EMS intervention while in parallel thecontrol group (CG) carried out an intermitted not strenuous

gymnastics program The underlying rationale for this pro-cedure was to validate the isolated effect of WB-EMS versusa motivated and ldquoblindedrdquo control group that performedgymnastics containing identical low intensitylow amplitudemovements as the WB-EMS group

Both interventions were performed at the Institute ofMedical Physics (IMP) which could be easily reached by thesubjects All the sessions were supervised by certified trainerswho recorded the attendance of the participants

In order to check for parameters that may impact ourstudy endpoints lifestyle parameters (ie dietary intakephysical activity etc) were inquired by questionnaires atbaseline and follow-up [16 17] After analyzing standard-ized dietary intake protocols over 4 days (Prodi-45 Wis-senschaftlicher Verlag Freiburg Germany) both groupswere provided with a maximum of 1200mgd calcium and800 IUd of cholecalciferol (RottapharmMadaus CologneGermany)

Apart from these interventions subjects were asked tomaintain their habitual life style

23 WB-EMS Intervention The WB-EMS exercise protocolis described in more detail in another publication [18] TheWB-EMS group performed supervised WB-EMS training(18-19minsession bipolar current frequency 85Hz pulse-breadth 350 120583sec) 3 times in 2 weeks (each Monday orTuesday and every second Thursday or Friday) for 54 weeksusing the WB-EMS technology of miha bodytec (AugsburgGermany) Eight muscle groups were simultaneously acti-vated by electrostimulation upper legs upper arms bottomabdomen chest lower back upper back and latissimus dorsiWB-EMS sessions consisted of easy not strenuous dynamicexercises performed in a standing position with 6 s dynamicmovements under EMS intermitted by 4 s of static restwithout current 10ndash14 exercises (eg dead lift with elbow-extension or arm-flexion squat with trunk flexion squat withlat pulleys or military press squat with crunch and butterflyor reverse fly squat with vertical chest press or verticalrowing) were structured in 1-2 sets of 8 repetitions Total timeunder load (current) averaged asymp11minsession during whichasymp110 stimulation intervals a 6 sec were completed Motionamplitude as well as corresponding intensity generated bythe movements was set low (ie squat leg-flexion lt35∘) toprevent effects from the exercise per se

In a WB-EMS session 3 subjects underwent supervisedand video-guided exercise (at three WB-EMS devices) at thesame time Strong emphasis was placed on adequate (current)intensity Current intensity was individually adapted for eachregion during the first sessions to a Rate of Perceived Exertion(RPE) of 14ndash16 of 20 (ldquosomewhat hardrdquo to ldquohardrdquo) Intensitieswere saved on chip cards that allowed fast and reliable settingof the devices in the subsequent sessions If necessary currentintensity was increased in the following sessions to maintainthe predefined rate of perceived exertion Figure 2 illustratesthe WB-EMS equipment and training

24 Control Group (CG) Subjects of the CG performed two10-week blocks of easy not strenuous gymnastics with 1

Journal of Osteoporosis 3

Received allocated intervention n = 38

Subjects with follow-up data included in the ITT finisher analysisWB-EMS 32 CG 28

Discontinued study due to personal reasons n = 2

Moved n = 1

Injuries diseases n = 2

Discontinued study due to personal reasons n = 3

Injuries diseases n = 4

Lost interest n = 1

ldquoLost to follow-uprdquo n = 6 ldquoLost to follow-uprdquo n = 10

Moved n = 1 deceased n = 1

Assessed for eligibility n = 451

Did not meet inclusion criteria n = 375

Randomized (stratified for age) n = 76

Received allocated intervention n = 38

Whole-body electromyostimulation n = 38 Control group (CG) n = 38

Figure 1 Flow chart of the ldquoTEST-IIIrdquo study (CONSORT scheme)

Table 1 Baseline characteristics of the WB-EMS and control group WB-EMS whole-body electromyostimulation 1As assessed by detailedquestionnaires (14 15) 2As assessed by 4-day protocol and analyzed using Prodi-4503 Expert software (Wissenschaftlicher Verlag FreiburgGermany) 3As assessed by Jamar dynamometer (dominant hand) according to Mathiowetz et al [14] 4Test according to Fritz und Lusardi[15] 5Prevalence of two and more diseases

Variable WB-EMS (119899 = 38) CG (119899 = 38)Age [years]1 747 plusmn 37 747 plusmn 44Body weight [kg] 579 plusmn 68 588 plusmn 57Body length [cm] 1616 plusmn 56 1629 plusmn 51Year postmenopausal [years] 243 plusmn 42 252 plusmn 47Total body fat DXA [] 316 plusmn 46 321 plusmn 37Appendicular skeletal muscle mass [kg] 158 plusmn 21 159 plusmn 17Energy uptake [MJd]2 663 plusmn 181 674 plusmn 167Calcium uptake [mgd]2 986 plusmn 276 966 plusmn 266Vitamin D uptake [IUd]2 244 plusmn 167 262 plusmn 211Exercise volume [minweek]1 341 plusmn 216 313 plusmn 193Grip strength3 [kg] 237 plusmn 40 235 plusmn 41Walking speed4 [kmh] 51 plusmn 14 53 plusmn 16Multimorbidity5 [119899] 22 (58) 25 (66)

session (60min)week with 10 weeks of rest between theblocks After 5min of walking variations subjects performedthe identical low intensitylow amplitude dynamic exercisesas during the EMS sessions After this flexibility generalcoordination and balance exercises were carried out for20min The session finished with 15min of relaxation andcommunication The aim of the CG protocol was to ensure aldquoblindingrdquo by carrying out a multifaceted attractive exerciseand relaxation program The program was designed not toimpact the study endpoints bone and muscle

25 Endpoints Primary and secondary endpoints weredetermined at baseline and after 54 weeks of intervention

Primary Outcome Measures

(i) Bone Mineral Density at the lumbar spine (LS)(ii) BoneMineralDensity at the proximal femur (total hip

region of interest (thip-ROI))

Secondary Outcome Measures

(i) Total lean body mass (LBM)(ii) grip strength

26 Testing Procedures All assessments and analysis werecarried out in a blinded mode Research assistants were not

4 Journal of Osteoporosis

Figure 2 Whole-body electromyostimulation equipment

informed about the status of the participants (WB-EMS orCG) and were not allowed to ask either

27 Anthropometry Bodyweightwasmeasured to the nearest01 kg on a digital scale (InBody 230 Seoul Korea) Heightwas determined barefoot to the nearest 01 cm with a sta-diometer (Holtain Crymych Dyfed Great Britain) Bodycomposition was assessed with Dual Energy X-Ray Absorp-tiometry (DXA QDR 4500a Discovery-upgrade HologicInc Bedford USA) using standard protocols Grip strengthof the dominant armwas assessedwith a Jamar dynamometer(Jamar Bolington IL)

Bone Mineral Density (BMD) was also determined byDXAat the lumbar spine (L1ndashL4 ap) and the proximal femur(total hip ROI) at baseline and after 1 year using standardprotocols specified by themanufacturer Long-term reliabilitywas 04 (coefficient of variation) as determined by 177 lum-bar spine phantom scans conducted during the study period

28 Statistical Analyses The sample size calculation wasbased on the study endpoint ldquoBone Mineral Density changesat the lumbar spinerdquo In order to detect a relevant between-group difference of 20 (Standard Deviation (SD) 28)31 subjectsgroup were required (5 error probability 80statistical power) Analyses were performed on an intention-to-treat basis for all the participants who completed thebaseline and at least one follow-up measurement (finisheranalysis) The treatment effect was defined as between-groupdifferences in changes from baseline to 12months In order toobtain normally distributed data all endpoints (BMD LBM)were log-transformed Analysis of covariance with baselinevalue age height and fat and muscle mass as covariateswere carried for statistical comparison of the two studygroups Statistical significance was accepted at 119875 lt 005 (2-tailed) Effect sizes were calculated using Cohenrsquos d [19] Weused SPSS 190 (SPSS Inc Chicago IL) for all the statisticalprocedures

3 Results

16 (WB-EMS 119899 = 6 CG 119899 = 10) of 76 subjects were unableor unwilling to visit the one-year control assessment andwerethus lost to follow-up (Figure 1) Altogether 6women sufferedfractures surgery andor serious diseases (cancer CHD)

One subject of the CG lost interest and five subjects listedpersonal reasons for their withdrawal two of them related tothe CG protocol one related to the WB-EMS protocol Oneparticipant of the CG died during the interventional periodand one woman of each groupmovedThus 28 subjects of theCG (74) and 32 subjects of the WB-EMS group (84) wereincluded in the analysis No serious training-related adverseeffects were observed during the sessions

Summing up as total attendance in the WB-EMS group61 out of 78 sessions (79 plusmn 18) were conducted Thecorresponding attendance rate in the CG was slightly lower(74 plusmn 18 149 of 20 sessions) Although the total numberof sessions was much lower in the CG the difference in totalexercise volumewas smaller with an average ofasymp24minweekin the WB-EMS group and asymp18min in the CG

No intergroup differences were recorded for anthropo-metric and clinical parameters at baseline (Table 1) Withrespect to confounding parameters no significant changesbetween baseline and follow-up were observed for lifestyleparameters (physical activity eg) andor medication asrecorded by questionnaires or dietary intake as assessed by 4-day dietary protocol and analyzed using Prodi-4503 Expertsoftware (Wissenschaftlicher Verlag Freiburg Germany)

31 Primary and Secondary Outcome Measures BMD atthe LS increased in the WB-EMS groups (06 plusmn 25) anddecreased in the CG (minus06 plusmn 24) At the total hip ROIBMD decreased in both groups (WB-EMS minus09 plusmn 19versus CG minus10 plusmn 23) Similar negative changes wereobserved for the proximal femur subregions (femoral necktrochanter) Differences between WB-EMS and CG-groupwere borderline nonsignificant for LS-BMD (119875 = 0051 ES1198891015840= 049) and not significant for BMD of the total hip ROI

(119875 = 0771 ES 1198891015840 = 004)Total LBM as assessed by total body DXA scans increased

in the WB-EMS group (07 plusmn 16) and decreased in the CG(minus08 plusmn 25) Corresponding differences between WB-EMSand CG-group were significant (119875 = 0006 ES 1198891015840 = 071)

The changes in grip strength were 105 plusmn 126 in theWB-EMS group and 22 plusmn 819 in the CG (119875 = 0000 ES1198891015840= 071) Table 2 lists the changes of BMD and strength

parameters in both groups

4 Discussion

This is the first trial that determined the effect of (WB-) EMSon BMD at lumbar spine orand proximal femur in elderlyfemales with osteopenia We found a borderline significanteffect (119875 = 0051) for the lumbar spine BMD but not forthe femoral neck site In view of the high effects of WB-EMSon muscle mass and strength in previous studies [20 21] andthe close interaction of muscle and bone [8] we had expectedstronger effects on bone In the present study the effect ofWB-EMS on LBMwas significant but rather moderate showing a15 net gain However maximum isometric leg and trunkextension strength significantly increased by more than 10as published elsewhere [13]

All the other studies examining the effect of EMS in BMDexclusively determined (functional) electromyostimulation

Journal of Osteoporosis 5

Table 2 Baseline and follow-up data of the WB-EMS and CG group for BMD lumbar spine (LS) total hip lean body mass (LBM) and gripstrength absolute treatment effects between training and control and 119875 value (covariance analysis baseline value age height lean bodymass and fat mass)

WB-EMS (119899 = 32) CG (119899 = 28) Treatment effectGroup Baseline 12 months Baseline 12 months Mean (95 CI) 119875 value

Mean (SD) Mean (SD)BMD LS [mgcm2] 882 plusmn 178 886 plusmn 173 835 plusmn 103 830 plusmn 105 104 (minus213 to 05) 0051BMD hip [mgcm2] 763 plusmn 81 756 plusmn 85 754 plusmn 95 746 plusmn 0097 12 (minus90 to 661) 0771LBM (Kg) 3515 plusmn 443 3542 plusmn 440 3542 plusmn 352 3512 plusmn 36 057 (016 to 098) 0006Grip strength (Kg) 239 plusmn 40 2641 plusmn 36 231 39 236 plusmn 45 207 (088 to 326) 0000

(FEMS) under disuse conditions (eg SCI) [22ndash32] In therecent meta-analysis by Chang et al [9] the authors found asignificant increase in BMD after 3 6 and 12 months of FESleg cycling or FES knee extension exercises in SCI patientsA longer period of exercise and a higher training frequencywere associated with higher effectiveness Dolbow et al [10]reviewed 10 studies determining the effect of FES leg cyclingon BMD taking into account the time after injury Two oftwo studies report effects of FES therapy in the first 2 monthsafter injury only one of three studies showed effects at anaverage of 3ndash6 years after injury and 4 out of five 9ndash13 yearsafter injury In line with the results of Dolbow et al Biering-Soslashrensen et al [11] concluded in a systematic review including19 EMS studies that there may be some effects of electricalstimulation especially in the early phaseThis review includesstudies with EMS of the lower limb (4 studies) leg cyclingFES (7 studies) knee extention FES (5 studies) FES duringtreadmill gait (1 study) or a combination of leg cycle andknee extension FES Consistent with the results of Chang etal improvement is seen in a longer period of training or withhigher training frequency

Although the studies included in the meta-analysis andreviews differ widely with respect to subjects or measure-ments the large majority of trials which ensured sufficienttime for bone adaption (6ndash12months) reported positive BMDchanges at skeletal sites stimulated and loaded by EMS orFES cycling or FES leg-extension exercises However it can beassumed that in paralyzed subjects the strain threshold is lowdue to inactivity and it remains unclear if the positive BMDchanges were caused more by EMS induced muscle con-traction producing joint reaction forces or just by resultingexternal reaction forces leading to axial loading of bones dur-ing exercises like leg-extension or FEMS cycling And againthe relevance of the results of these studies for older peoplewithout serve functional limitations is rather questionable

A comparison of the effect of WB-EMS with ldquogold-standard exercise protocolsrdquo might be helpful for estimatingthe relevance ofWB-EMSprograms for fighting osteoporosisReviewing the literature for exercise-induced BMD changesin subjects 60 years and older as assessed byDXA (review [3334]) shows that our WB-EMS effects were lower comparedwith conventional exercise effects in particular when specificresistance exercise was applied Comparing the results ofthe present WB-EMS results with data of our recent 18-month SEFIP exercise trial [35] that used identical measure-ments and included comparable subjects with respect to age

(69 plusmn 4 yrs) with higher BMI (26 plusmn 4 kgm2) revealed morefavorable data for the SEFIP cohort (net BMD difference EGversus CG at LS and thip asymp15ndash21 both 119875 = 0001) that hadcarried out a combined resistanceaerobicbalance protocol

Little is known about the optimum EMS protocol forimpacting bone and the low effect on Bone Mineral Den-sity in the present study might be due to a suboptimalsetting of current parameters Although the most favor-able composition of EMS parameters for triggering boneadaptation still has to be established a recent study thatdirectly compared different frequencies of EMS in an animaldisuse model [36] determined the most favorable effect onbone parameters (eg volume fraction connectivity andtrabecular numberthickness) especially at 20 and 50HzWith respect to stimulation intensity Dudley-Javoroski andShields [12] suggested supramaximal amperage (200mA) toelicit very strong contractions Because each pair of electrodeswas regulated separately with different intensities and dueto differences in electrode size we were unable to controland describe the stimulation intensity (mA) in the presentstudy In EMS studies in SCI patients where isolated muscleswere stimulated external forces were measured and put intorelation with body weight to estimate intensity [31] Becauseof the simultaneous activation of agonists and antagonistsand resulting co-contraction this method cannot be usedin WB-EMS We applied EMS for 3 times 20min in 2 weeksusing a bipolar current at 85Hz at a pulse width of 350 120583secwhereas 6 sec of stimulation was intermitted by 4 sec of restThe highly significant effect of this protocol on muscle massand strength and its acceptance [20 21 37] supported theapplication of this EMS protocol

Considering that enthusiasm for conventional exercise israther low in the cohort of elderly women one key factorfor the relative high compliance with EMS training [33] mayhave been the low total volume of the program (in total30minweek) Furthermore WB-EMS programs are appliedunder rather individualized conditions and it may be also theexclusiveness of the exercise program that resulted in a highcompliance

Some limitations may decrease the evidence of thepresent study (a)We evaluated the effect of EMS in the cohortof lean elderly females with osteopenia and the assignabilityof our results to other cohorts is questionable (b) AlthoughDXA is still the ldquogold standardrdquo technology for assessingBMD QCT technique may be the more appropriate methodfor assessing BMD at lumbar spine in the cohort of subjects

6 Journal of Osteoporosis

70 years and older due to degenerative changes of the spine(c) No X-ray examinations have been performed to detectvertebral body fractures However we presume that BMDincreases in WB-EMS group were not the result of ldquotraininginducedrdquo compression fractures In the analyzed LS-scans nodecrease of area of the vertebra as sign of vertebral deformitywas observed Further duringWB-EMS themechanical load-ing of vertebrae due to muscular tension is rather moderatecompared to classic high impact training contents (d) Asemiactive control group that performed a comparable exer-cise volume and identical movements was implemented toensure blinding and to determine the effect of WB-EMS perse For reasons of attractiveness and compliance the CG didnot carry out only identical movements but also performedexercises for mobility coordination and relaxation and thetraining schedule differed However the movements of theWB-EMS program and all the contents of the CG sessionswere not strenuous and designed not to impact our endpointThus in our opinion the influences of the differences inexercises contents and schedule on the validity of the studiesare rather low (e) Due to a lower number of subjects included(76 instead of 80) and a slightly higher drop-out rate thanexpected we failed to realize our estimated sample size of31 subjectsgroup (g) It is not possible to objectify intensityof muscle contraction during WB-EMS and it is not clear ifsubjects realized the requested high intensity

5 Conclusions

In summary we found a borderline nonsignificant effect ofWB-EMS on Bone Mineral Density at the lumbar spine andno effect at the hip However taking into account the highimpact of this technology on muscle mass and strengthWB-EMS may be an option for musculoskeletal preven-tionrehabilitation at least for (elderly) subjects unable orunwilling to exercise conventionally Nevertheless due to thehigher impact of mixed exercise programs on BMD and theircomprehensive effect on multiple risk factors and diseasesof advanced age [38] classic exercise should be favored forelderly subjects

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors gratefully acknowledge the support of mihabodytec (Augsburg Germany) that supplied the WB-EMStechnology and RottapharmMadaus (Cologne Germany)that supplied calcium and vitamin D

References

[1] D A Nelson and M L Bouxsein ldquoExercise maintains bonemass but do people maintain exerciserdquo Journal of Bone andMineral Research vol 16 no 2 pp 202ndash205 2001

[2] Statistisches-Bundesamt Gesundheit in Deutschland Statistis-ches-Bundesamt Berlin Germany 2006

[3] D O Clark ldquoPhysical activity and its correlates among urbanprimary care patients aged 55 years or olderrdquo The Journals ofGerontology Series B Psychological Sciences and Social Sciencesvol 54 no 1 pp S41ndashS48 1999

[4] W Kemmler and S von Stengel ldquoDose-response effect of exer-cise frequency on bone mineral density in post-menopausalosteopenic womenrdquo Scandinavian Journal of Medicine andScience in Sports vol 24 no 3 pp 526ndash534 2014

[5] WKemmler and SVon Stengel ldquoExercise frequency health riskfactors and diseases of the elderlyrdquoArchives of PhysicalMedicineand Rehabilitation vol 94 no 11 pp 2046ndash2053 2013

[6] E C Cussler S B Going L B Houtkooper et al ldquoExercisefrequency and calcium intake predict 4-year bone changes inpostmenopausal womenrdquoOsteoporosis International vol 16 no12 pp 2129ndash2141 2005

[7] B TWall M L Dirks L B Verdijk et al ldquoNeuromuscular elec-trical stimulation increases muscle protein synthesis in elderlytype 2 diabetic menrdquo The American Journal of PhysiologymdashEndocrinology and Metabolism vol 303 no 5 pp E614ndashE6232012

[8] Y-X Qin H Lam S Ferreri and C Rubin ldquoDynamic skeletalmuscle stimulation and its potential in bone adaptationrdquo Jour-nal of Musculoskeletal amp Neuronal Interactions vol 10 no 1 pp12ndash24 2010

[9] K-V Chang C-Y Hung W-S Chen M-S Lai K-L Chienand D-S Han ldquoEffectiveness of bisphosphonate analoguesand functional electrical stimulation on attenuating post-injuryosteoporosis in spinal cord injury patients a systematic reviewand meta-analysisrdquo PLoS ONE vol 8 no 11 Article ID e811242013

[10] J D Dolbow D R Dolbow A S Gorgey R A Adler and D RGater ldquoThe effects of aging and electrical stimulation exerciseon bone after spinal cord injuryrdquo Aging and Disease vol 4 no3 pp 141ndash153 2013

[11] F Biering-Soslashrensen B Hansen and B S B Lee ldquoNon-phar-macological treatment and prevention of bone loss after spinalcord injury a systematic reviewrdquo Spinal Cord vol 47 no 7 pp508ndash518 2009

[12] S Dudley-Javoroski and R K Shields ldquoMuscle and boneplasticity after spinal cord injury reviewof adaptations to disuseand to electrical muscle stimulationrdquo Journal of RehabilitationResearch and Development vol 45 no 2 pp 283ndash296 2008

[13] W Kemmler M Bebenek K Engelke and S von StengelldquoImpact of whole-body electromyostimulation on body com-position in elderly women at risk for sarcopenia the Trainingand ElectroStimulation Trial (TEST-III)rdquo Age vol 36 no 1 pp395ndash406 2014

[14] V Mathiowetz K Weber G Volland and N Kashman ldquoReli-ability and validity of grip and pinch strength evaluationsrdquoTheJournal of Hand SurgerymdashAmerican Volume vol 9 no 2 pp222ndash226 1984

[15] S Fritz andM Lusardi ldquoWhite paper lsquowalking speed the sixthvital signrsquordquo Journal of Geriatric Physical Therapy vol 32 no 2pp 46ndash49 2009

[16] W Kemmler D Lauber JWeineck J HensenW Kalender andK Engelke ldquoBenefits of 2 years of intense exercise on bone den-sity physical fitness and blood lipids in early postmenopausalosteopenic women results of the Erlangen Fitness OsteoporosisPrevention Study (EFOPS)rdquo Archives of Internal Medicine vol164 no 10 pp 1084ndash1091 2004

Journal of Osteoporosis 7

[17] W Kemmler J Weineck W A Kalender and K EngelkeldquoThe effect of habitual physical activity non-athletic exercisemuscle strength andVO2max on bonemineral density is ratherlow in early postmenopausal osteopenic womenrdquo Journal ofMusculoskeletal amp Neuronal Interactions vol 4 no 3 pp 325ndash334 2004

[18] W Kemmler and S von Stengel ldquoWhole-body electromyostim-ulation as a means to impact muscle mass and abdominal bodyfat in lean sedentary older female adults subanalysis of theTEST-III trialrdquo Clinical Interventions in Aging vol 8 pp 1353ndash1364 2013

[19] J Cohen Statistical Power Analysis for the Behavioral SciencesLawrence Erlbaum Associates Hillsdale NJ USA 2nd edition1988

[20] W Kemmler A Birlauf and S von Stengel ldquoEinfluss von Ganz-korper-Elektromyostimulation auf das Metabolische Syndrombei alteren Mannern mit metabolischem Syndromrdquo DeutscheZeitschrift fur Sportmedizin vol 61 no 5 pp 117ndash123 2010

[21] W Kemmler R Schliffka J L Mayhew and S von Sten-gel ldquoEffects of whole-body electromyostimulation on restingmetabolic rate body composition and maximum strength inpostmenopausal women the training and electrostimulationtrialrdquo The Journal of Strength amp Conditioning Research vol 24no 7 pp 1880ndash1887 2010

[22] M C Ashe J J Eng A V Krassioukov D E R WarburtonC Hung and A Tawashy ldquoResponse to functional electricalstimulation cycling in women with spinal cord injuries usingdual-energy X-ray absorptiometry and peripheral quantitativecomputed tomography a case seriesrdquoThe Journal of Spinal CordMedicine vol 33 no 1 pp 68ndash72 2010

[23] M Belanger R B Stein G D Wheeler T Gordon and BLeduc ldquoElectrical stimulation can it increase muscle strengthand reverse osteopenia in spinal cord injured individualsrdquoArchives of Physical Medicine and Rehabilitation vol 81 no 8pp 1090ndash1098 2000

[24] K K BeDell A M E Scremin K L Perell and C F KunkelldquoEffects of functional electrical stimulation-induced lowerextremity cycling on bone density of spinal cord-injuredpatientsrdquo American Journal of Physical Medicine amp Rehabilita-tion vol 75 no 1 pp 29ndash34 1996

[25] S-C Chen C-H LaiW P ChanM-HHuangH-WTsai andJ-J J Chen ldquoIncreases in bone mineral density after functionalelectrical stimulation cycling exercises in spinal cord injuredpatientsrdquo Disability and Rehabilitation vol 27 no 22 pp 1337ndash1341 2005

[26] JM ClarkM Jelbart H Rischbieth et al ldquoPhysiological effectsof lower extremity functional electrical stimulation in earlyspinal cord injury lack of efficacy to prevent bone lossrdquo SpinalCord vol 45 no 1 pp 78ndash85 2007

[27] P Eser E D de Bruin I Telley H E Lechner H Knecht andE Stussi ldquoEffect of electrical stimulation-induced cycling onbone mineral density in spinal cord-injured patientsrdquo EuropeanJournal of Clinical Investigation vol 33 no 5 pp 412ndash419 2003

[28] A Frotzler S Coupaud C Perret et al ldquoHigh-volume FES-cycling partially reverses bone loss in people with chronic spinalcord injuryrdquo Bone vol 43 no 1 pp 169ndash176 2008

[29] T N Hangartner M M Rodgers R M Glaser and P SBarre ldquoTibial bone density loss in spinal cord injured patientseffects of FES exerciserdquo Journal of Rehabilitation Research andDevelopment vol 31 no 1 pp 50ndash61 1994

[30] T Mohr ldquoElectric stimulation in muscle training of the lowerextremities in persons with spinal cord injuriesrdquo Ugeskrift forLaeligger vol 162 no 15 pp 2190ndash2194 2000

[31] R K Shields and S Dudley-Javoroski ldquoMusculoskeletal plas-ticity after acute spinal cord injury effects of long-term neuro-muscular electrical stimulation trainingrdquo Journal of Neurophys-iology vol 95 no 4 pp 2380ndash2390 2006

[32] R K Shields and S Dudley-Javoroski ldquoMusculoskeletal adap-tations in chronic spinal cord injury effects of long-term soleuselectrical stimulation trainingrdquo Neurorehabilitation and NeuralRepair vol 21 no 2 pp 169ndash179 2007

[33] E A Marques J Mota and J Carvalho ldquoExercise effectson bone mineral density in older adults a meta-analysis ofrandomized controlled trialsrdquo Age vol 34 no 6 pp 1493ndash15152011

[34] A Gomez-Cabello I Ara A Gonzalez-Aguero J A Casajusand G Vicente-Rodrıguez ldquoEffects of training on bone mass inolder adults a systematic reviewrdquo Sports Medicine vol 42 no4 pp 301ndash325 2012

[35] W Kemmler S von Stengel K Engelke L Haberle J LMayhew and W A Kalender ldquoExercise body compositionand functional ability a randomized controlled trialrdquoAmericanJournal of Preventive Medicine vol 38 no 3 pp 279ndash287 2010

[36] H Lam and Y-X Qin ldquoThe effects of frequency-dependentdynamic muscle stimulation on inhibition of trabecular boneloss in a disuse modelrdquo Bone vol 43 no 6 pp 1093ndash1100 2008

[37] W Kemmler S von Stengel J Schwarz and J L MayhewldquoEffect of whole-body electromyostimulation on energy expen-diture during exerciserdquo The Journal of Strength amp ConditioningResearch vol 26 no 1 pp 240ndash245 2012

[38] M Borjesson M L Hellenius E Jansson et al PhysicalActivity in the Prevention and Treatment of Disease ProfessionalAssociation for Physical Activity (Pafpa) Stockholm Sweden2010

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Page 2: Clinical Study Whole-Body Electromyostimulation to Fight ...downloads.hindawi.com/journals/jos/2015/643520.pdf · e Training and Electrostimulation Trial (TEST) project is a series

2 Journal of Osteoporosis

In the present study we evaluated the impact ofWB-EMSon BMD in sedentary lean and osteopenic elderly femalesa cohort at high risk for fractures The main hypothesis ofthis trial was that WB-EMS training significantly increasesBMD at the lumbar spine compared with a control groupOur secondary hypothesis was thatWB-EMS training signif-icantly impacts BMD at the proximal femur compared withthe control group Secondary endpoints concerning bodycomposition and strength are published elsewhere [13]

2 Materials and Methods

The Training and Electrostimulation Trial (TEST) projectis a series of studies that determine the effect of WB-EMSon parameters related to risk factors and diseases of elderlysubjects In the present study TEST-III is a randomizedcontrolled trial (RCT) that evaluated the effect of whole-body electromyostimulation (WB-EMS) on osteoporosis inlean sedentary elderly females with osteopenia To determinethe isolated effect of WB-EMS we implemented an activecontrol group which performed identical movements ascarried out during the WB-EMS session The study protocolwas approved by the Ethical Committee of the Friedrich-Alexander University Erlangen-Nuremberg (FAU) Germany(Ethik Antrag 4184) and the German Radiation SafetyAgency (Z 5-224622-2010-027) Written informed consentwas obtained from all subjects prior to the study entry TEST-III was conducted from November 2010 through July 2012 atthe Institute of Medical Physics FAU Germany and is fullyregistered under wwwclinicaltrialsgov (NCT01296776)

21 Participants All female subjects (9256 women) 70 yearsand older living in the area of Erlangen Germany werecontacted by personal letters Though eligibility criteria forthe trial (Figure 1) already had been listed in the letter 272subjects of the 451 women who responded had to be excludedafter phone interviews because they (a) did not meet ourcriteria for ldquoleannessrdquo (body weight (kg) gt (body height (cm)minus 100)) (b) had exercised more than 1 hour per week duringthe last 10 years (c) reported contraindications (ie totalendoprosthesis abdomengroin hernia epilepsy and cardiacarrhythmia) for WB-EMS intervention and (d) reporteddiseases or medication affecting our primary endpoints

179 women were invited to our lab to determine bodycomposition and bone status After measuring body weightand height with calibrated devices and determining BMD atthe lumbar spine and proximal femur 103 women had to beexcluded because they did not meet our inclusion criterionsof ldquoleannessrdquo or osteopenia (BMD lt 1 SD T-Score) (Figure 1)

The 76 remaining subjects were assigned into two studygroups using computerized block randomization stratifiedfor age (block size 119899 = 2) by an external statistician to ensureallocation concealment Table 1 lists baseline characteristicsof the WB-EMS and the control group No correspondingintergroup differences were observed

22 Interventions WB-EMS group performed 54 weeks ofconsecutive WB-EMS intervention while in parallel thecontrol group (CG) carried out an intermitted not strenuous

gymnastics program The underlying rationale for this pro-cedure was to validate the isolated effect of WB-EMS versusa motivated and ldquoblindedrdquo control group that performedgymnastics containing identical low intensitylow amplitudemovements as the WB-EMS group

Both interventions were performed at the Institute ofMedical Physics (IMP) which could be easily reached by thesubjects All the sessions were supervised by certified trainerswho recorded the attendance of the participants

In order to check for parameters that may impact ourstudy endpoints lifestyle parameters (ie dietary intakephysical activity etc) were inquired by questionnaires atbaseline and follow-up [16 17] After analyzing standard-ized dietary intake protocols over 4 days (Prodi-45 Wis-senschaftlicher Verlag Freiburg Germany) both groupswere provided with a maximum of 1200mgd calcium and800 IUd of cholecalciferol (RottapharmMadaus CologneGermany)

Apart from these interventions subjects were asked tomaintain their habitual life style

23 WB-EMS Intervention The WB-EMS exercise protocolis described in more detail in another publication [18] TheWB-EMS group performed supervised WB-EMS training(18-19minsession bipolar current frequency 85Hz pulse-breadth 350 120583sec) 3 times in 2 weeks (each Monday orTuesday and every second Thursday or Friday) for 54 weeksusing the WB-EMS technology of miha bodytec (AugsburgGermany) Eight muscle groups were simultaneously acti-vated by electrostimulation upper legs upper arms bottomabdomen chest lower back upper back and latissimus dorsiWB-EMS sessions consisted of easy not strenuous dynamicexercises performed in a standing position with 6 s dynamicmovements under EMS intermitted by 4 s of static restwithout current 10ndash14 exercises (eg dead lift with elbow-extension or arm-flexion squat with trunk flexion squat withlat pulleys or military press squat with crunch and butterflyor reverse fly squat with vertical chest press or verticalrowing) were structured in 1-2 sets of 8 repetitions Total timeunder load (current) averaged asymp11minsession during whichasymp110 stimulation intervals a 6 sec were completed Motionamplitude as well as corresponding intensity generated bythe movements was set low (ie squat leg-flexion lt35∘) toprevent effects from the exercise per se

In a WB-EMS session 3 subjects underwent supervisedand video-guided exercise (at three WB-EMS devices) at thesame time Strong emphasis was placed on adequate (current)intensity Current intensity was individually adapted for eachregion during the first sessions to a Rate of Perceived Exertion(RPE) of 14ndash16 of 20 (ldquosomewhat hardrdquo to ldquohardrdquo) Intensitieswere saved on chip cards that allowed fast and reliable settingof the devices in the subsequent sessions If necessary currentintensity was increased in the following sessions to maintainthe predefined rate of perceived exertion Figure 2 illustratesthe WB-EMS equipment and training

24 Control Group (CG) Subjects of the CG performed two10-week blocks of easy not strenuous gymnastics with 1

Journal of Osteoporosis 3

Received allocated intervention n = 38

Subjects with follow-up data included in the ITT finisher analysisWB-EMS 32 CG 28

Discontinued study due to personal reasons n = 2

Moved n = 1

Injuries diseases n = 2

Discontinued study due to personal reasons n = 3

Injuries diseases n = 4

Lost interest n = 1

ldquoLost to follow-uprdquo n = 6 ldquoLost to follow-uprdquo n = 10

Moved n = 1 deceased n = 1

Assessed for eligibility n = 451

Did not meet inclusion criteria n = 375

Randomized (stratified for age) n = 76

Received allocated intervention n = 38

Whole-body electromyostimulation n = 38 Control group (CG) n = 38

Figure 1 Flow chart of the ldquoTEST-IIIrdquo study (CONSORT scheme)

Table 1 Baseline characteristics of the WB-EMS and control group WB-EMS whole-body electromyostimulation 1As assessed by detailedquestionnaires (14 15) 2As assessed by 4-day protocol and analyzed using Prodi-4503 Expert software (Wissenschaftlicher Verlag FreiburgGermany) 3As assessed by Jamar dynamometer (dominant hand) according to Mathiowetz et al [14] 4Test according to Fritz und Lusardi[15] 5Prevalence of two and more diseases

Variable WB-EMS (119899 = 38) CG (119899 = 38)Age [years]1 747 plusmn 37 747 plusmn 44Body weight [kg] 579 plusmn 68 588 plusmn 57Body length [cm] 1616 plusmn 56 1629 plusmn 51Year postmenopausal [years] 243 plusmn 42 252 plusmn 47Total body fat DXA [] 316 plusmn 46 321 plusmn 37Appendicular skeletal muscle mass [kg] 158 plusmn 21 159 plusmn 17Energy uptake [MJd]2 663 plusmn 181 674 plusmn 167Calcium uptake [mgd]2 986 plusmn 276 966 plusmn 266Vitamin D uptake [IUd]2 244 plusmn 167 262 plusmn 211Exercise volume [minweek]1 341 plusmn 216 313 plusmn 193Grip strength3 [kg] 237 plusmn 40 235 plusmn 41Walking speed4 [kmh] 51 plusmn 14 53 plusmn 16Multimorbidity5 [119899] 22 (58) 25 (66)

session (60min)week with 10 weeks of rest between theblocks After 5min of walking variations subjects performedthe identical low intensitylow amplitude dynamic exercisesas during the EMS sessions After this flexibility generalcoordination and balance exercises were carried out for20min The session finished with 15min of relaxation andcommunication The aim of the CG protocol was to ensure aldquoblindingrdquo by carrying out a multifaceted attractive exerciseand relaxation program The program was designed not toimpact the study endpoints bone and muscle

25 Endpoints Primary and secondary endpoints weredetermined at baseline and after 54 weeks of intervention

Primary Outcome Measures

(i) Bone Mineral Density at the lumbar spine (LS)(ii) BoneMineralDensity at the proximal femur (total hip

region of interest (thip-ROI))

Secondary Outcome Measures

(i) Total lean body mass (LBM)(ii) grip strength

26 Testing Procedures All assessments and analysis werecarried out in a blinded mode Research assistants were not

4 Journal of Osteoporosis

Figure 2 Whole-body electromyostimulation equipment

informed about the status of the participants (WB-EMS orCG) and were not allowed to ask either

27 Anthropometry Bodyweightwasmeasured to the nearest01 kg on a digital scale (InBody 230 Seoul Korea) Heightwas determined barefoot to the nearest 01 cm with a sta-diometer (Holtain Crymych Dyfed Great Britain) Bodycomposition was assessed with Dual Energy X-Ray Absorp-tiometry (DXA QDR 4500a Discovery-upgrade HologicInc Bedford USA) using standard protocols Grip strengthof the dominant armwas assessedwith a Jamar dynamometer(Jamar Bolington IL)

Bone Mineral Density (BMD) was also determined byDXAat the lumbar spine (L1ndashL4 ap) and the proximal femur(total hip ROI) at baseline and after 1 year using standardprotocols specified by themanufacturer Long-term reliabilitywas 04 (coefficient of variation) as determined by 177 lum-bar spine phantom scans conducted during the study period

28 Statistical Analyses The sample size calculation wasbased on the study endpoint ldquoBone Mineral Density changesat the lumbar spinerdquo In order to detect a relevant between-group difference of 20 (Standard Deviation (SD) 28)31 subjectsgroup were required (5 error probability 80statistical power) Analyses were performed on an intention-to-treat basis for all the participants who completed thebaseline and at least one follow-up measurement (finisheranalysis) The treatment effect was defined as between-groupdifferences in changes from baseline to 12months In order toobtain normally distributed data all endpoints (BMD LBM)were log-transformed Analysis of covariance with baselinevalue age height and fat and muscle mass as covariateswere carried for statistical comparison of the two studygroups Statistical significance was accepted at 119875 lt 005 (2-tailed) Effect sizes were calculated using Cohenrsquos d [19] Weused SPSS 190 (SPSS Inc Chicago IL) for all the statisticalprocedures

3 Results

16 (WB-EMS 119899 = 6 CG 119899 = 10) of 76 subjects were unableor unwilling to visit the one-year control assessment andwerethus lost to follow-up (Figure 1) Altogether 6women sufferedfractures surgery andor serious diseases (cancer CHD)

One subject of the CG lost interest and five subjects listedpersonal reasons for their withdrawal two of them related tothe CG protocol one related to the WB-EMS protocol Oneparticipant of the CG died during the interventional periodand one woman of each groupmovedThus 28 subjects of theCG (74) and 32 subjects of the WB-EMS group (84) wereincluded in the analysis No serious training-related adverseeffects were observed during the sessions

Summing up as total attendance in the WB-EMS group61 out of 78 sessions (79 plusmn 18) were conducted Thecorresponding attendance rate in the CG was slightly lower(74 plusmn 18 149 of 20 sessions) Although the total numberof sessions was much lower in the CG the difference in totalexercise volumewas smaller with an average ofasymp24minweekin the WB-EMS group and asymp18min in the CG

No intergroup differences were recorded for anthropo-metric and clinical parameters at baseline (Table 1) Withrespect to confounding parameters no significant changesbetween baseline and follow-up were observed for lifestyleparameters (physical activity eg) andor medication asrecorded by questionnaires or dietary intake as assessed by 4-day dietary protocol and analyzed using Prodi-4503 Expertsoftware (Wissenschaftlicher Verlag Freiburg Germany)

31 Primary and Secondary Outcome Measures BMD atthe LS increased in the WB-EMS groups (06 plusmn 25) anddecreased in the CG (minus06 plusmn 24) At the total hip ROIBMD decreased in both groups (WB-EMS minus09 plusmn 19versus CG minus10 plusmn 23) Similar negative changes wereobserved for the proximal femur subregions (femoral necktrochanter) Differences between WB-EMS and CG-groupwere borderline nonsignificant for LS-BMD (119875 = 0051 ES1198891015840= 049) and not significant for BMD of the total hip ROI

(119875 = 0771 ES 1198891015840 = 004)Total LBM as assessed by total body DXA scans increased

in the WB-EMS group (07 plusmn 16) and decreased in the CG(minus08 plusmn 25) Corresponding differences between WB-EMSand CG-group were significant (119875 = 0006 ES 1198891015840 = 071)

The changes in grip strength were 105 plusmn 126 in theWB-EMS group and 22 plusmn 819 in the CG (119875 = 0000 ES1198891015840= 071) Table 2 lists the changes of BMD and strength

parameters in both groups

4 Discussion

This is the first trial that determined the effect of (WB-) EMSon BMD at lumbar spine orand proximal femur in elderlyfemales with osteopenia We found a borderline significanteffect (119875 = 0051) for the lumbar spine BMD but not forthe femoral neck site In view of the high effects of WB-EMSon muscle mass and strength in previous studies [20 21] andthe close interaction of muscle and bone [8] we had expectedstronger effects on bone In the present study the effect ofWB-EMS on LBMwas significant but rather moderate showing a15 net gain However maximum isometric leg and trunkextension strength significantly increased by more than 10as published elsewhere [13]

All the other studies examining the effect of EMS in BMDexclusively determined (functional) electromyostimulation

Journal of Osteoporosis 5

Table 2 Baseline and follow-up data of the WB-EMS and CG group for BMD lumbar spine (LS) total hip lean body mass (LBM) and gripstrength absolute treatment effects between training and control and 119875 value (covariance analysis baseline value age height lean bodymass and fat mass)

WB-EMS (119899 = 32) CG (119899 = 28) Treatment effectGroup Baseline 12 months Baseline 12 months Mean (95 CI) 119875 value

Mean (SD) Mean (SD)BMD LS [mgcm2] 882 plusmn 178 886 plusmn 173 835 plusmn 103 830 plusmn 105 104 (minus213 to 05) 0051BMD hip [mgcm2] 763 plusmn 81 756 plusmn 85 754 plusmn 95 746 plusmn 0097 12 (minus90 to 661) 0771LBM (Kg) 3515 plusmn 443 3542 plusmn 440 3542 plusmn 352 3512 plusmn 36 057 (016 to 098) 0006Grip strength (Kg) 239 plusmn 40 2641 plusmn 36 231 39 236 plusmn 45 207 (088 to 326) 0000

(FEMS) under disuse conditions (eg SCI) [22ndash32] In therecent meta-analysis by Chang et al [9] the authors found asignificant increase in BMD after 3 6 and 12 months of FESleg cycling or FES knee extension exercises in SCI patientsA longer period of exercise and a higher training frequencywere associated with higher effectiveness Dolbow et al [10]reviewed 10 studies determining the effect of FES leg cyclingon BMD taking into account the time after injury Two oftwo studies report effects of FES therapy in the first 2 monthsafter injury only one of three studies showed effects at anaverage of 3ndash6 years after injury and 4 out of five 9ndash13 yearsafter injury In line with the results of Dolbow et al Biering-Soslashrensen et al [11] concluded in a systematic review including19 EMS studies that there may be some effects of electricalstimulation especially in the early phaseThis review includesstudies with EMS of the lower limb (4 studies) leg cyclingFES (7 studies) knee extention FES (5 studies) FES duringtreadmill gait (1 study) or a combination of leg cycle andknee extension FES Consistent with the results of Chang etal improvement is seen in a longer period of training or withhigher training frequency

Although the studies included in the meta-analysis andreviews differ widely with respect to subjects or measure-ments the large majority of trials which ensured sufficienttime for bone adaption (6ndash12months) reported positive BMDchanges at skeletal sites stimulated and loaded by EMS orFES cycling or FES leg-extension exercises However it can beassumed that in paralyzed subjects the strain threshold is lowdue to inactivity and it remains unclear if the positive BMDchanges were caused more by EMS induced muscle con-traction producing joint reaction forces or just by resultingexternal reaction forces leading to axial loading of bones dur-ing exercises like leg-extension or FEMS cycling And againthe relevance of the results of these studies for older peoplewithout serve functional limitations is rather questionable

A comparison of the effect of WB-EMS with ldquogold-standard exercise protocolsrdquo might be helpful for estimatingthe relevance ofWB-EMSprograms for fighting osteoporosisReviewing the literature for exercise-induced BMD changesin subjects 60 years and older as assessed byDXA (review [3334]) shows that our WB-EMS effects were lower comparedwith conventional exercise effects in particular when specificresistance exercise was applied Comparing the results ofthe present WB-EMS results with data of our recent 18-month SEFIP exercise trial [35] that used identical measure-ments and included comparable subjects with respect to age

(69 plusmn 4 yrs) with higher BMI (26 plusmn 4 kgm2) revealed morefavorable data for the SEFIP cohort (net BMD difference EGversus CG at LS and thip asymp15ndash21 both 119875 = 0001) that hadcarried out a combined resistanceaerobicbalance protocol

Little is known about the optimum EMS protocol forimpacting bone and the low effect on Bone Mineral Den-sity in the present study might be due to a suboptimalsetting of current parameters Although the most favor-able composition of EMS parameters for triggering boneadaptation still has to be established a recent study thatdirectly compared different frequencies of EMS in an animaldisuse model [36] determined the most favorable effect onbone parameters (eg volume fraction connectivity andtrabecular numberthickness) especially at 20 and 50HzWith respect to stimulation intensity Dudley-Javoroski andShields [12] suggested supramaximal amperage (200mA) toelicit very strong contractions Because each pair of electrodeswas regulated separately with different intensities and dueto differences in electrode size we were unable to controland describe the stimulation intensity (mA) in the presentstudy In EMS studies in SCI patients where isolated muscleswere stimulated external forces were measured and put intorelation with body weight to estimate intensity [31] Becauseof the simultaneous activation of agonists and antagonistsand resulting co-contraction this method cannot be usedin WB-EMS We applied EMS for 3 times 20min in 2 weeksusing a bipolar current at 85Hz at a pulse width of 350 120583secwhereas 6 sec of stimulation was intermitted by 4 sec of restThe highly significant effect of this protocol on muscle massand strength and its acceptance [20 21 37] supported theapplication of this EMS protocol

Considering that enthusiasm for conventional exercise israther low in the cohort of elderly women one key factorfor the relative high compliance with EMS training [33] mayhave been the low total volume of the program (in total30minweek) Furthermore WB-EMS programs are appliedunder rather individualized conditions and it may be also theexclusiveness of the exercise program that resulted in a highcompliance

Some limitations may decrease the evidence of thepresent study (a)We evaluated the effect of EMS in the cohortof lean elderly females with osteopenia and the assignabilityof our results to other cohorts is questionable (b) AlthoughDXA is still the ldquogold standardrdquo technology for assessingBMD QCT technique may be the more appropriate methodfor assessing BMD at lumbar spine in the cohort of subjects

6 Journal of Osteoporosis

70 years and older due to degenerative changes of the spine(c) No X-ray examinations have been performed to detectvertebral body fractures However we presume that BMDincreases in WB-EMS group were not the result of ldquotraininginducedrdquo compression fractures In the analyzed LS-scans nodecrease of area of the vertebra as sign of vertebral deformitywas observed Further duringWB-EMS themechanical load-ing of vertebrae due to muscular tension is rather moderatecompared to classic high impact training contents (d) Asemiactive control group that performed a comparable exer-cise volume and identical movements was implemented toensure blinding and to determine the effect of WB-EMS perse For reasons of attractiveness and compliance the CG didnot carry out only identical movements but also performedexercises for mobility coordination and relaxation and thetraining schedule differed However the movements of theWB-EMS program and all the contents of the CG sessionswere not strenuous and designed not to impact our endpointThus in our opinion the influences of the differences inexercises contents and schedule on the validity of the studiesare rather low (e) Due to a lower number of subjects included(76 instead of 80) and a slightly higher drop-out rate thanexpected we failed to realize our estimated sample size of31 subjectsgroup (g) It is not possible to objectify intensityof muscle contraction during WB-EMS and it is not clear ifsubjects realized the requested high intensity

5 Conclusions

In summary we found a borderline nonsignificant effect ofWB-EMS on Bone Mineral Density at the lumbar spine andno effect at the hip However taking into account the highimpact of this technology on muscle mass and strengthWB-EMS may be an option for musculoskeletal preven-tionrehabilitation at least for (elderly) subjects unable orunwilling to exercise conventionally Nevertheless due to thehigher impact of mixed exercise programs on BMD and theircomprehensive effect on multiple risk factors and diseasesof advanced age [38] classic exercise should be favored forelderly subjects

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors gratefully acknowledge the support of mihabodytec (Augsburg Germany) that supplied the WB-EMStechnology and RottapharmMadaus (Cologne Germany)that supplied calcium and vitamin D

References

[1] D A Nelson and M L Bouxsein ldquoExercise maintains bonemass but do people maintain exerciserdquo Journal of Bone andMineral Research vol 16 no 2 pp 202ndash205 2001

[2] Statistisches-Bundesamt Gesundheit in Deutschland Statistis-ches-Bundesamt Berlin Germany 2006

[3] D O Clark ldquoPhysical activity and its correlates among urbanprimary care patients aged 55 years or olderrdquo The Journals ofGerontology Series B Psychological Sciences and Social Sciencesvol 54 no 1 pp S41ndashS48 1999

[4] W Kemmler and S von Stengel ldquoDose-response effect of exer-cise frequency on bone mineral density in post-menopausalosteopenic womenrdquo Scandinavian Journal of Medicine andScience in Sports vol 24 no 3 pp 526ndash534 2014

[5] WKemmler and SVon Stengel ldquoExercise frequency health riskfactors and diseases of the elderlyrdquoArchives of PhysicalMedicineand Rehabilitation vol 94 no 11 pp 2046ndash2053 2013

[6] E C Cussler S B Going L B Houtkooper et al ldquoExercisefrequency and calcium intake predict 4-year bone changes inpostmenopausal womenrdquoOsteoporosis International vol 16 no12 pp 2129ndash2141 2005

[7] B TWall M L Dirks L B Verdijk et al ldquoNeuromuscular elec-trical stimulation increases muscle protein synthesis in elderlytype 2 diabetic menrdquo The American Journal of PhysiologymdashEndocrinology and Metabolism vol 303 no 5 pp E614ndashE6232012

[8] Y-X Qin H Lam S Ferreri and C Rubin ldquoDynamic skeletalmuscle stimulation and its potential in bone adaptationrdquo Jour-nal of Musculoskeletal amp Neuronal Interactions vol 10 no 1 pp12ndash24 2010

[9] K-V Chang C-Y Hung W-S Chen M-S Lai K-L Chienand D-S Han ldquoEffectiveness of bisphosphonate analoguesand functional electrical stimulation on attenuating post-injuryosteoporosis in spinal cord injury patients a systematic reviewand meta-analysisrdquo PLoS ONE vol 8 no 11 Article ID e811242013

[10] J D Dolbow D R Dolbow A S Gorgey R A Adler and D RGater ldquoThe effects of aging and electrical stimulation exerciseon bone after spinal cord injuryrdquo Aging and Disease vol 4 no3 pp 141ndash153 2013

[11] F Biering-Soslashrensen B Hansen and B S B Lee ldquoNon-phar-macological treatment and prevention of bone loss after spinalcord injury a systematic reviewrdquo Spinal Cord vol 47 no 7 pp508ndash518 2009

[12] S Dudley-Javoroski and R K Shields ldquoMuscle and boneplasticity after spinal cord injury reviewof adaptations to disuseand to electrical muscle stimulationrdquo Journal of RehabilitationResearch and Development vol 45 no 2 pp 283ndash296 2008

[13] W Kemmler M Bebenek K Engelke and S von StengelldquoImpact of whole-body electromyostimulation on body com-position in elderly women at risk for sarcopenia the Trainingand ElectroStimulation Trial (TEST-III)rdquo Age vol 36 no 1 pp395ndash406 2014

[14] V Mathiowetz K Weber G Volland and N Kashman ldquoReli-ability and validity of grip and pinch strength evaluationsrdquoTheJournal of Hand SurgerymdashAmerican Volume vol 9 no 2 pp222ndash226 1984

[15] S Fritz andM Lusardi ldquoWhite paper lsquowalking speed the sixthvital signrsquordquo Journal of Geriatric Physical Therapy vol 32 no 2pp 46ndash49 2009

[16] W Kemmler D Lauber JWeineck J HensenW Kalender andK Engelke ldquoBenefits of 2 years of intense exercise on bone den-sity physical fitness and blood lipids in early postmenopausalosteopenic women results of the Erlangen Fitness OsteoporosisPrevention Study (EFOPS)rdquo Archives of Internal Medicine vol164 no 10 pp 1084ndash1091 2004

Journal of Osteoporosis 7

[17] W Kemmler J Weineck W A Kalender and K EngelkeldquoThe effect of habitual physical activity non-athletic exercisemuscle strength andVO2max on bonemineral density is ratherlow in early postmenopausal osteopenic womenrdquo Journal ofMusculoskeletal amp Neuronal Interactions vol 4 no 3 pp 325ndash334 2004

[18] W Kemmler and S von Stengel ldquoWhole-body electromyostim-ulation as a means to impact muscle mass and abdominal bodyfat in lean sedentary older female adults subanalysis of theTEST-III trialrdquo Clinical Interventions in Aging vol 8 pp 1353ndash1364 2013

[19] J Cohen Statistical Power Analysis for the Behavioral SciencesLawrence Erlbaum Associates Hillsdale NJ USA 2nd edition1988

[20] W Kemmler A Birlauf and S von Stengel ldquoEinfluss von Ganz-korper-Elektromyostimulation auf das Metabolische Syndrombei alteren Mannern mit metabolischem Syndromrdquo DeutscheZeitschrift fur Sportmedizin vol 61 no 5 pp 117ndash123 2010

[21] W Kemmler R Schliffka J L Mayhew and S von Sten-gel ldquoEffects of whole-body electromyostimulation on restingmetabolic rate body composition and maximum strength inpostmenopausal women the training and electrostimulationtrialrdquo The Journal of Strength amp Conditioning Research vol 24no 7 pp 1880ndash1887 2010

[22] M C Ashe J J Eng A V Krassioukov D E R WarburtonC Hung and A Tawashy ldquoResponse to functional electricalstimulation cycling in women with spinal cord injuries usingdual-energy X-ray absorptiometry and peripheral quantitativecomputed tomography a case seriesrdquoThe Journal of Spinal CordMedicine vol 33 no 1 pp 68ndash72 2010

[23] M Belanger R B Stein G D Wheeler T Gordon and BLeduc ldquoElectrical stimulation can it increase muscle strengthand reverse osteopenia in spinal cord injured individualsrdquoArchives of Physical Medicine and Rehabilitation vol 81 no 8pp 1090ndash1098 2000

[24] K K BeDell A M E Scremin K L Perell and C F KunkelldquoEffects of functional electrical stimulation-induced lowerextremity cycling on bone density of spinal cord-injuredpatientsrdquo American Journal of Physical Medicine amp Rehabilita-tion vol 75 no 1 pp 29ndash34 1996

[25] S-C Chen C-H LaiW P ChanM-HHuangH-WTsai andJ-J J Chen ldquoIncreases in bone mineral density after functionalelectrical stimulation cycling exercises in spinal cord injuredpatientsrdquo Disability and Rehabilitation vol 27 no 22 pp 1337ndash1341 2005

[26] JM ClarkM Jelbart H Rischbieth et al ldquoPhysiological effectsof lower extremity functional electrical stimulation in earlyspinal cord injury lack of efficacy to prevent bone lossrdquo SpinalCord vol 45 no 1 pp 78ndash85 2007

[27] P Eser E D de Bruin I Telley H E Lechner H Knecht andE Stussi ldquoEffect of electrical stimulation-induced cycling onbone mineral density in spinal cord-injured patientsrdquo EuropeanJournal of Clinical Investigation vol 33 no 5 pp 412ndash419 2003

[28] A Frotzler S Coupaud C Perret et al ldquoHigh-volume FES-cycling partially reverses bone loss in people with chronic spinalcord injuryrdquo Bone vol 43 no 1 pp 169ndash176 2008

[29] T N Hangartner M M Rodgers R M Glaser and P SBarre ldquoTibial bone density loss in spinal cord injured patientseffects of FES exerciserdquo Journal of Rehabilitation Research andDevelopment vol 31 no 1 pp 50ndash61 1994

[30] T Mohr ldquoElectric stimulation in muscle training of the lowerextremities in persons with spinal cord injuriesrdquo Ugeskrift forLaeligger vol 162 no 15 pp 2190ndash2194 2000

[31] R K Shields and S Dudley-Javoroski ldquoMusculoskeletal plas-ticity after acute spinal cord injury effects of long-term neuro-muscular electrical stimulation trainingrdquo Journal of Neurophys-iology vol 95 no 4 pp 2380ndash2390 2006

[32] R K Shields and S Dudley-Javoroski ldquoMusculoskeletal adap-tations in chronic spinal cord injury effects of long-term soleuselectrical stimulation trainingrdquo Neurorehabilitation and NeuralRepair vol 21 no 2 pp 169ndash179 2007

[33] E A Marques J Mota and J Carvalho ldquoExercise effectson bone mineral density in older adults a meta-analysis ofrandomized controlled trialsrdquo Age vol 34 no 6 pp 1493ndash15152011

[34] A Gomez-Cabello I Ara A Gonzalez-Aguero J A Casajusand G Vicente-Rodrıguez ldquoEffects of training on bone mass inolder adults a systematic reviewrdquo Sports Medicine vol 42 no4 pp 301ndash325 2012

[35] W Kemmler S von Stengel K Engelke L Haberle J LMayhew and W A Kalender ldquoExercise body compositionand functional ability a randomized controlled trialrdquoAmericanJournal of Preventive Medicine vol 38 no 3 pp 279ndash287 2010

[36] H Lam and Y-X Qin ldquoThe effects of frequency-dependentdynamic muscle stimulation on inhibition of trabecular boneloss in a disuse modelrdquo Bone vol 43 no 6 pp 1093ndash1100 2008

[37] W Kemmler S von Stengel J Schwarz and J L MayhewldquoEffect of whole-body electromyostimulation on energy expen-diture during exerciserdquo The Journal of Strength amp ConditioningResearch vol 26 no 1 pp 240ndash245 2012

[38] M Borjesson M L Hellenius E Jansson et al PhysicalActivity in the Prevention and Treatment of Disease ProfessionalAssociation for Physical Activity (Pafpa) Stockholm Sweden2010

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Behavioural Neurology

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Disease Markers

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Oxidative Medicine and Cellular Longevity

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Computational and Mathematical Methods in Medicine

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Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 3: Clinical Study Whole-Body Electromyostimulation to Fight ...downloads.hindawi.com/journals/jos/2015/643520.pdf · e Training and Electrostimulation Trial (TEST) project is a series

Journal of Osteoporosis 3

Received allocated intervention n = 38

Subjects with follow-up data included in the ITT finisher analysisWB-EMS 32 CG 28

Discontinued study due to personal reasons n = 2

Moved n = 1

Injuries diseases n = 2

Discontinued study due to personal reasons n = 3

Injuries diseases n = 4

Lost interest n = 1

ldquoLost to follow-uprdquo n = 6 ldquoLost to follow-uprdquo n = 10

Moved n = 1 deceased n = 1

Assessed for eligibility n = 451

Did not meet inclusion criteria n = 375

Randomized (stratified for age) n = 76

Received allocated intervention n = 38

Whole-body electromyostimulation n = 38 Control group (CG) n = 38

Figure 1 Flow chart of the ldquoTEST-IIIrdquo study (CONSORT scheme)

Table 1 Baseline characteristics of the WB-EMS and control group WB-EMS whole-body electromyostimulation 1As assessed by detailedquestionnaires (14 15) 2As assessed by 4-day protocol and analyzed using Prodi-4503 Expert software (Wissenschaftlicher Verlag FreiburgGermany) 3As assessed by Jamar dynamometer (dominant hand) according to Mathiowetz et al [14] 4Test according to Fritz und Lusardi[15] 5Prevalence of two and more diseases

Variable WB-EMS (119899 = 38) CG (119899 = 38)Age [years]1 747 plusmn 37 747 plusmn 44Body weight [kg] 579 plusmn 68 588 plusmn 57Body length [cm] 1616 plusmn 56 1629 plusmn 51Year postmenopausal [years] 243 plusmn 42 252 plusmn 47Total body fat DXA [] 316 plusmn 46 321 plusmn 37Appendicular skeletal muscle mass [kg] 158 plusmn 21 159 plusmn 17Energy uptake [MJd]2 663 plusmn 181 674 plusmn 167Calcium uptake [mgd]2 986 plusmn 276 966 plusmn 266Vitamin D uptake [IUd]2 244 plusmn 167 262 plusmn 211Exercise volume [minweek]1 341 plusmn 216 313 plusmn 193Grip strength3 [kg] 237 plusmn 40 235 plusmn 41Walking speed4 [kmh] 51 plusmn 14 53 plusmn 16Multimorbidity5 [119899] 22 (58) 25 (66)

session (60min)week with 10 weeks of rest between theblocks After 5min of walking variations subjects performedthe identical low intensitylow amplitude dynamic exercisesas during the EMS sessions After this flexibility generalcoordination and balance exercises were carried out for20min The session finished with 15min of relaxation andcommunication The aim of the CG protocol was to ensure aldquoblindingrdquo by carrying out a multifaceted attractive exerciseand relaxation program The program was designed not toimpact the study endpoints bone and muscle

25 Endpoints Primary and secondary endpoints weredetermined at baseline and after 54 weeks of intervention

Primary Outcome Measures

(i) Bone Mineral Density at the lumbar spine (LS)(ii) BoneMineralDensity at the proximal femur (total hip

region of interest (thip-ROI))

Secondary Outcome Measures

(i) Total lean body mass (LBM)(ii) grip strength

26 Testing Procedures All assessments and analysis werecarried out in a blinded mode Research assistants were not

4 Journal of Osteoporosis

Figure 2 Whole-body electromyostimulation equipment

informed about the status of the participants (WB-EMS orCG) and were not allowed to ask either

27 Anthropometry Bodyweightwasmeasured to the nearest01 kg on a digital scale (InBody 230 Seoul Korea) Heightwas determined barefoot to the nearest 01 cm with a sta-diometer (Holtain Crymych Dyfed Great Britain) Bodycomposition was assessed with Dual Energy X-Ray Absorp-tiometry (DXA QDR 4500a Discovery-upgrade HologicInc Bedford USA) using standard protocols Grip strengthof the dominant armwas assessedwith a Jamar dynamometer(Jamar Bolington IL)

Bone Mineral Density (BMD) was also determined byDXAat the lumbar spine (L1ndashL4 ap) and the proximal femur(total hip ROI) at baseline and after 1 year using standardprotocols specified by themanufacturer Long-term reliabilitywas 04 (coefficient of variation) as determined by 177 lum-bar spine phantom scans conducted during the study period

28 Statistical Analyses The sample size calculation wasbased on the study endpoint ldquoBone Mineral Density changesat the lumbar spinerdquo In order to detect a relevant between-group difference of 20 (Standard Deviation (SD) 28)31 subjectsgroup were required (5 error probability 80statistical power) Analyses were performed on an intention-to-treat basis for all the participants who completed thebaseline and at least one follow-up measurement (finisheranalysis) The treatment effect was defined as between-groupdifferences in changes from baseline to 12months In order toobtain normally distributed data all endpoints (BMD LBM)were log-transformed Analysis of covariance with baselinevalue age height and fat and muscle mass as covariateswere carried for statistical comparison of the two studygroups Statistical significance was accepted at 119875 lt 005 (2-tailed) Effect sizes were calculated using Cohenrsquos d [19] Weused SPSS 190 (SPSS Inc Chicago IL) for all the statisticalprocedures

3 Results

16 (WB-EMS 119899 = 6 CG 119899 = 10) of 76 subjects were unableor unwilling to visit the one-year control assessment andwerethus lost to follow-up (Figure 1) Altogether 6women sufferedfractures surgery andor serious diseases (cancer CHD)

One subject of the CG lost interest and five subjects listedpersonal reasons for their withdrawal two of them related tothe CG protocol one related to the WB-EMS protocol Oneparticipant of the CG died during the interventional periodand one woman of each groupmovedThus 28 subjects of theCG (74) and 32 subjects of the WB-EMS group (84) wereincluded in the analysis No serious training-related adverseeffects were observed during the sessions

Summing up as total attendance in the WB-EMS group61 out of 78 sessions (79 plusmn 18) were conducted Thecorresponding attendance rate in the CG was slightly lower(74 plusmn 18 149 of 20 sessions) Although the total numberof sessions was much lower in the CG the difference in totalexercise volumewas smaller with an average ofasymp24minweekin the WB-EMS group and asymp18min in the CG

No intergroup differences were recorded for anthropo-metric and clinical parameters at baseline (Table 1) Withrespect to confounding parameters no significant changesbetween baseline and follow-up were observed for lifestyleparameters (physical activity eg) andor medication asrecorded by questionnaires or dietary intake as assessed by 4-day dietary protocol and analyzed using Prodi-4503 Expertsoftware (Wissenschaftlicher Verlag Freiburg Germany)

31 Primary and Secondary Outcome Measures BMD atthe LS increased in the WB-EMS groups (06 plusmn 25) anddecreased in the CG (minus06 plusmn 24) At the total hip ROIBMD decreased in both groups (WB-EMS minus09 plusmn 19versus CG minus10 plusmn 23) Similar negative changes wereobserved for the proximal femur subregions (femoral necktrochanter) Differences between WB-EMS and CG-groupwere borderline nonsignificant for LS-BMD (119875 = 0051 ES1198891015840= 049) and not significant for BMD of the total hip ROI

(119875 = 0771 ES 1198891015840 = 004)Total LBM as assessed by total body DXA scans increased

in the WB-EMS group (07 plusmn 16) and decreased in the CG(minus08 plusmn 25) Corresponding differences between WB-EMSand CG-group were significant (119875 = 0006 ES 1198891015840 = 071)

The changes in grip strength were 105 plusmn 126 in theWB-EMS group and 22 plusmn 819 in the CG (119875 = 0000 ES1198891015840= 071) Table 2 lists the changes of BMD and strength

parameters in both groups

4 Discussion

This is the first trial that determined the effect of (WB-) EMSon BMD at lumbar spine orand proximal femur in elderlyfemales with osteopenia We found a borderline significanteffect (119875 = 0051) for the lumbar spine BMD but not forthe femoral neck site In view of the high effects of WB-EMSon muscle mass and strength in previous studies [20 21] andthe close interaction of muscle and bone [8] we had expectedstronger effects on bone In the present study the effect ofWB-EMS on LBMwas significant but rather moderate showing a15 net gain However maximum isometric leg and trunkextension strength significantly increased by more than 10as published elsewhere [13]

All the other studies examining the effect of EMS in BMDexclusively determined (functional) electromyostimulation

Journal of Osteoporosis 5

Table 2 Baseline and follow-up data of the WB-EMS and CG group for BMD lumbar spine (LS) total hip lean body mass (LBM) and gripstrength absolute treatment effects between training and control and 119875 value (covariance analysis baseline value age height lean bodymass and fat mass)

WB-EMS (119899 = 32) CG (119899 = 28) Treatment effectGroup Baseline 12 months Baseline 12 months Mean (95 CI) 119875 value

Mean (SD) Mean (SD)BMD LS [mgcm2] 882 plusmn 178 886 plusmn 173 835 plusmn 103 830 plusmn 105 104 (minus213 to 05) 0051BMD hip [mgcm2] 763 plusmn 81 756 plusmn 85 754 plusmn 95 746 plusmn 0097 12 (minus90 to 661) 0771LBM (Kg) 3515 plusmn 443 3542 plusmn 440 3542 plusmn 352 3512 plusmn 36 057 (016 to 098) 0006Grip strength (Kg) 239 plusmn 40 2641 plusmn 36 231 39 236 plusmn 45 207 (088 to 326) 0000

(FEMS) under disuse conditions (eg SCI) [22ndash32] In therecent meta-analysis by Chang et al [9] the authors found asignificant increase in BMD after 3 6 and 12 months of FESleg cycling or FES knee extension exercises in SCI patientsA longer period of exercise and a higher training frequencywere associated with higher effectiveness Dolbow et al [10]reviewed 10 studies determining the effect of FES leg cyclingon BMD taking into account the time after injury Two oftwo studies report effects of FES therapy in the first 2 monthsafter injury only one of three studies showed effects at anaverage of 3ndash6 years after injury and 4 out of five 9ndash13 yearsafter injury In line with the results of Dolbow et al Biering-Soslashrensen et al [11] concluded in a systematic review including19 EMS studies that there may be some effects of electricalstimulation especially in the early phaseThis review includesstudies with EMS of the lower limb (4 studies) leg cyclingFES (7 studies) knee extention FES (5 studies) FES duringtreadmill gait (1 study) or a combination of leg cycle andknee extension FES Consistent with the results of Chang etal improvement is seen in a longer period of training or withhigher training frequency

Although the studies included in the meta-analysis andreviews differ widely with respect to subjects or measure-ments the large majority of trials which ensured sufficienttime for bone adaption (6ndash12months) reported positive BMDchanges at skeletal sites stimulated and loaded by EMS orFES cycling or FES leg-extension exercises However it can beassumed that in paralyzed subjects the strain threshold is lowdue to inactivity and it remains unclear if the positive BMDchanges were caused more by EMS induced muscle con-traction producing joint reaction forces or just by resultingexternal reaction forces leading to axial loading of bones dur-ing exercises like leg-extension or FEMS cycling And againthe relevance of the results of these studies for older peoplewithout serve functional limitations is rather questionable

A comparison of the effect of WB-EMS with ldquogold-standard exercise protocolsrdquo might be helpful for estimatingthe relevance ofWB-EMSprograms for fighting osteoporosisReviewing the literature for exercise-induced BMD changesin subjects 60 years and older as assessed byDXA (review [3334]) shows that our WB-EMS effects were lower comparedwith conventional exercise effects in particular when specificresistance exercise was applied Comparing the results ofthe present WB-EMS results with data of our recent 18-month SEFIP exercise trial [35] that used identical measure-ments and included comparable subjects with respect to age

(69 plusmn 4 yrs) with higher BMI (26 plusmn 4 kgm2) revealed morefavorable data for the SEFIP cohort (net BMD difference EGversus CG at LS and thip asymp15ndash21 both 119875 = 0001) that hadcarried out a combined resistanceaerobicbalance protocol

Little is known about the optimum EMS protocol forimpacting bone and the low effect on Bone Mineral Den-sity in the present study might be due to a suboptimalsetting of current parameters Although the most favor-able composition of EMS parameters for triggering boneadaptation still has to be established a recent study thatdirectly compared different frequencies of EMS in an animaldisuse model [36] determined the most favorable effect onbone parameters (eg volume fraction connectivity andtrabecular numberthickness) especially at 20 and 50HzWith respect to stimulation intensity Dudley-Javoroski andShields [12] suggested supramaximal amperage (200mA) toelicit very strong contractions Because each pair of electrodeswas regulated separately with different intensities and dueto differences in electrode size we were unable to controland describe the stimulation intensity (mA) in the presentstudy In EMS studies in SCI patients where isolated muscleswere stimulated external forces were measured and put intorelation with body weight to estimate intensity [31] Becauseof the simultaneous activation of agonists and antagonistsand resulting co-contraction this method cannot be usedin WB-EMS We applied EMS for 3 times 20min in 2 weeksusing a bipolar current at 85Hz at a pulse width of 350 120583secwhereas 6 sec of stimulation was intermitted by 4 sec of restThe highly significant effect of this protocol on muscle massand strength and its acceptance [20 21 37] supported theapplication of this EMS protocol

Considering that enthusiasm for conventional exercise israther low in the cohort of elderly women one key factorfor the relative high compliance with EMS training [33] mayhave been the low total volume of the program (in total30minweek) Furthermore WB-EMS programs are appliedunder rather individualized conditions and it may be also theexclusiveness of the exercise program that resulted in a highcompliance

Some limitations may decrease the evidence of thepresent study (a)We evaluated the effect of EMS in the cohortof lean elderly females with osteopenia and the assignabilityof our results to other cohorts is questionable (b) AlthoughDXA is still the ldquogold standardrdquo technology for assessingBMD QCT technique may be the more appropriate methodfor assessing BMD at lumbar spine in the cohort of subjects

6 Journal of Osteoporosis

70 years and older due to degenerative changes of the spine(c) No X-ray examinations have been performed to detectvertebral body fractures However we presume that BMDincreases in WB-EMS group were not the result of ldquotraininginducedrdquo compression fractures In the analyzed LS-scans nodecrease of area of the vertebra as sign of vertebral deformitywas observed Further duringWB-EMS themechanical load-ing of vertebrae due to muscular tension is rather moderatecompared to classic high impact training contents (d) Asemiactive control group that performed a comparable exer-cise volume and identical movements was implemented toensure blinding and to determine the effect of WB-EMS perse For reasons of attractiveness and compliance the CG didnot carry out only identical movements but also performedexercises for mobility coordination and relaxation and thetraining schedule differed However the movements of theWB-EMS program and all the contents of the CG sessionswere not strenuous and designed not to impact our endpointThus in our opinion the influences of the differences inexercises contents and schedule on the validity of the studiesare rather low (e) Due to a lower number of subjects included(76 instead of 80) and a slightly higher drop-out rate thanexpected we failed to realize our estimated sample size of31 subjectsgroup (g) It is not possible to objectify intensityof muscle contraction during WB-EMS and it is not clear ifsubjects realized the requested high intensity

5 Conclusions

In summary we found a borderline nonsignificant effect ofWB-EMS on Bone Mineral Density at the lumbar spine andno effect at the hip However taking into account the highimpact of this technology on muscle mass and strengthWB-EMS may be an option for musculoskeletal preven-tionrehabilitation at least for (elderly) subjects unable orunwilling to exercise conventionally Nevertheless due to thehigher impact of mixed exercise programs on BMD and theircomprehensive effect on multiple risk factors and diseasesof advanced age [38] classic exercise should be favored forelderly subjects

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors gratefully acknowledge the support of mihabodytec (Augsburg Germany) that supplied the WB-EMStechnology and RottapharmMadaus (Cologne Germany)that supplied calcium and vitamin D

References

[1] D A Nelson and M L Bouxsein ldquoExercise maintains bonemass but do people maintain exerciserdquo Journal of Bone andMineral Research vol 16 no 2 pp 202ndash205 2001

[2] Statistisches-Bundesamt Gesundheit in Deutschland Statistis-ches-Bundesamt Berlin Germany 2006

[3] D O Clark ldquoPhysical activity and its correlates among urbanprimary care patients aged 55 years or olderrdquo The Journals ofGerontology Series B Psychological Sciences and Social Sciencesvol 54 no 1 pp S41ndashS48 1999

[4] W Kemmler and S von Stengel ldquoDose-response effect of exer-cise frequency on bone mineral density in post-menopausalosteopenic womenrdquo Scandinavian Journal of Medicine andScience in Sports vol 24 no 3 pp 526ndash534 2014

[5] WKemmler and SVon Stengel ldquoExercise frequency health riskfactors and diseases of the elderlyrdquoArchives of PhysicalMedicineand Rehabilitation vol 94 no 11 pp 2046ndash2053 2013

[6] E C Cussler S B Going L B Houtkooper et al ldquoExercisefrequency and calcium intake predict 4-year bone changes inpostmenopausal womenrdquoOsteoporosis International vol 16 no12 pp 2129ndash2141 2005

[7] B TWall M L Dirks L B Verdijk et al ldquoNeuromuscular elec-trical stimulation increases muscle protein synthesis in elderlytype 2 diabetic menrdquo The American Journal of PhysiologymdashEndocrinology and Metabolism vol 303 no 5 pp E614ndashE6232012

[8] Y-X Qin H Lam S Ferreri and C Rubin ldquoDynamic skeletalmuscle stimulation and its potential in bone adaptationrdquo Jour-nal of Musculoskeletal amp Neuronal Interactions vol 10 no 1 pp12ndash24 2010

[9] K-V Chang C-Y Hung W-S Chen M-S Lai K-L Chienand D-S Han ldquoEffectiveness of bisphosphonate analoguesand functional electrical stimulation on attenuating post-injuryosteoporosis in spinal cord injury patients a systematic reviewand meta-analysisrdquo PLoS ONE vol 8 no 11 Article ID e811242013

[10] J D Dolbow D R Dolbow A S Gorgey R A Adler and D RGater ldquoThe effects of aging and electrical stimulation exerciseon bone after spinal cord injuryrdquo Aging and Disease vol 4 no3 pp 141ndash153 2013

[11] F Biering-Soslashrensen B Hansen and B S B Lee ldquoNon-phar-macological treatment and prevention of bone loss after spinalcord injury a systematic reviewrdquo Spinal Cord vol 47 no 7 pp508ndash518 2009

[12] S Dudley-Javoroski and R K Shields ldquoMuscle and boneplasticity after spinal cord injury reviewof adaptations to disuseand to electrical muscle stimulationrdquo Journal of RehabilitationResearch and Development vol 45 no 2 pp 283ndash296 2008

[13] W Kemmler M Bebenek K Engelke and S von StengelldquoImpact of whole-body electromyostimulation on body com-position in elderly women at risk for sarcopenia the Trainingand ElectroStimulation Trial (TEST-III)rdquo Age vol 36 no 1 pp395ndash406 2014

[14] V Mathiowetz K Weber G Volland and N Kashman ldquoReli-ability and validity of grip and pinch strength evaluationsrdquoTheJournal of Hand SurgerymdashAmerican Volume vol 9 no 2 pp222ndash226 1984

[15] S Fritz andM Lusardi ldquoWhite paper lsquowalking speed the sixthvital signrsquordquo Journal of Geriatric Physical Therapy vol 32 no 2pp 46ndash49 2009

[16] W Kemmler D Lauber JWeineck J HensenW Kalender andK Engelke ldquoBenefits of 2 years of intense exercise on bone den-sity physical fitness and blood lipids in early postmenopausalosteopenic women results of the Erlangen Fitness OsteoporosisPrevention Study (EFOPS)rdquo Archives of Internal Medicine vol164 no 10 pp 1084ndash1091 2004

Journal of Osteoporosis 7

[17] W Kemmler J Weineck W A Kalender and K EngelkeldquoThe effect of habitual physical activity non-athletic exercisemuscle strength andVO2max on bonemineral density is ratherlow in early postmenopausal osteopenic womenrdquo Journal ofMusculoskeletal amp Neuronal Interactions vol 4 no 3 pp 325ndash334 2004

[18] W Kemmler and S von Stengel ldquoWhole-body electromyostim-ulation as a means to impact muscle mass and abdominal bodyfat in lean sedentary older female adults subanalysis of theTEST-III trialrdquo Clinical Interventions in Aging vol 8 pp 1353ndash1364 2013

[19] J Cohen Statistical Power Analysis for the Behavioral SciencesLawrence Erlbaum Associates Hillsdale NJ USA 2nd edition1988

[20] W Kemmler A Birlauf and S von Stengel ldquoEinfluss von Ganz-korper-Elektromyostimulation auf das Metabolische Syndrombei alteren Mannern mit metabolischem Syndromrdquo DeutscheZeitschrift fur Sportmedizin vol 61 no 5 pp 117ndash123 2010

[21] W Kemmler R Schliffka J L Mayhew and S von Sten-gel ldquoEffects of whole-body electromyostimulation on restingmetabolic rate body composition and maximum strength inpostmenopausal women the training and electrostimulationtrialrdquo The Journal of Strength amp Conditioning Research vol 24no 7 pp 1880ndash1887 2010

[22] M C Ashe J J Eng A V Krassioukov D E R WarburtonC Hung and A Tawashy ldquoResponse to functional electricalstimulation cycling in women with spinal cord injuries usingdual-energy X-ray absorptiometry and peripheral quantitativecomputed tomography a case seriesrdquoThe Journal of Spinal CordMedicine vol 33 no 1 pp 68ndash72 2010

[23] M Belanger R B Stein G D Wheeler T Gordon and BLeduc ldquoElectrical stimulation can it increase muscle strengthand reverse osteopenia in spinal cord injured individualsrdquoArchives of Physical Medicine and Rehabilitation vol 81 no 8pp 1090ndash1098 2000

[24] K K BeDell A M E Scremin K L Perell and C F KunkelldquoEffects of functional electrical stimulation-induced lowerextremity cycling on bone density of spinal cord-injuredpatientsrdquo American Journal of Physical Medicine amp Rehabilita-tion vol 75 no 1 pp 29ndash34 1996

[25] S-C Chen C-H LaiW P ChanM-HHuangH-WTsai andJ-J J Chen ldquoIncreases in bone mineral density after functionalelectrical stimulation cycling exercises in spinal cord injuredpatientsrdquo Disability and Rehabilitation vol 27 no 22 pp 1337ndash1341 2005

[26] JM ClarkM Jelbart H Rischbieth et al ldquoPhysiological effectsof lower extremity functional electrical stimulation in earlyspinal cord injury lack of efficacy to prevent bone lossrdquo SpinalCord vol 45 no 1 pp 78ndash85 2007

[27] P Eser E D de Bruin I Telley H E Lechner H Knecht andE Stussi ldquoEffect of electrical stimulation-induced cycling onbone mineral density in spinal cord-injured patientsrdquo EuropeanJournal of Clinical Investigation vol 33 no 5 pp 412ndash419 2003

[28] A Frotzler S Coupaud C Perret et al ldquoHigh-volume FES-cycling partially reverses bone loss in people with chronic spinalcord injuryrdquo Bone vol 43 no 1 pp 169ndash176 2008

[29] T N Hangartner M M Rodgers R M Glaser and P SBarre ldquoTibial bone density loss in spinal cord injured patientseffects of FES exerciserdquo Journal of Rehabilitation Research andDevelopment vol 31 no 1 pp 50ndash61 1994

[30] T Mohr ldquoElectric stimulation in muscle training of the lowerextremities in persons with spinal cord injuriesrdquo Ugeskrift forLaeligger vol 162 no 15 pp 2190ndash2194 2000

[31] R K Shields and S Dudley-Javoroski ldquoMusculoskeletal plas-ticity after acute spinal cord injury effects of long-term neuro-muscular electrical stimulation trainingrdquo Journal of Neurophys-iology vol 95 no 4 pp 2380ndash2390 2006

[32] R K Shields and S Dudley-Javoroski ldquoMusculoskeletal adap-tations in chronic spinal cord injury effects of long-term soleuselectrical stimulation trainingrdquo Neurorehabilitation and NeuralRepair vol 21 no 2 pp 169ndash179 2007

[33] E A Marques J Mota and J Carvalho ldquoExercise effectson bone mineral density in older adults a meta-analysis ofrandomized controlled trialsrdquo Age vol 34 no 6 pp 1493ndash15152011

[34] A Gomez-Cabello I Ara A Gonzalez-Aguero J A Casajusand G Vicente-Rodrıguez ldquoEffects of training on bone mass inolder adults a systematic reviewrdquo Sports Medicine vol 42 no4 pp 301ndash325 2012

[35] W Kemmler S von Stengel K Engelke L Haberle J LMayhew and W A Kalender ldquoExercise body compositionand functional ability a randomized controlled trialrdquoAmericanJournal of Preventive Medicine vol 38 no 3 pp 279ndash287 2010

[36] H Lam and Y-X Qin ldquoThe effects of frequency-dependentdynamic muscle stimulation on inhibition of trabecular boneloss in a disuse modelrdquo Bone vol 43 no 6 pp 1093ndash1100 2008

[37] W Kemmler S von Stengel J Schwarz and J L MayhewldquoEffect of whole-body electromyostimulation on energy expen-diture during exerciserdquo The Journal of Strength amp ConditioningResearch vol 26 no 1 pp 240ndash245 2012

[38] M Borjesson M L Hellenius E Jansson et al PhysicalActivity in the Prevention and Treatment of Disease ProfessionalAssociation for Physical Activity (Pafpa) Stockholm Sweden2010

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 4: Clinical Study Whole-Body Electromyostimulation to Fight ...downloads.hindawi.com/journals/jos/2015/643520.pdf · e Training and Electrostimulation Trial (TEST) project is a series

4 Journal of Osteoporosis

Figure 2 Whole-body electromyostimulation equipment

informed about the status of the participants (WB-EMS orCG) and were not allowed to ask either

27 Anthropometry Bodyweightwasmeasured to the nearest01 kg on a digital scale (InBody 230 Seoul Korea) Heightwas determined barefoot to the nearest 01 cm with a sta-diometer (Holtain Crymych Dyfed Great Britain) Bodycomposition was assessed with Dual Energy X-Ray Absorp-tiometry (DXA QDR 4500a Discovery-upgrade HologicInc Bedford USA) using standard protocols Grip strengthof the dominant armwas assessedwith a Jamar dynamometer(Jamar Bolington IL)

Bone Mineral Density (BMD) was also determined byDXAat the lumbar spine (L1ndashL4 ap) and the proximal femur(total hip ROI) at baseline and after 1 year using standardprotocols specified by themanufacturer Long-term reliabilitywas 04 (coefficient of variation) as determined by 177 lum-bar spine phantom scans conducted during the study period

28 Statistical Analyses The sample size calculation wasbased on the study endpoint ldquoBone Mineral Density changesat the lumbar spinerdquo In order to detect a relevant between-group difference of 20 (Standard Deviation (SD) 28)31 subjectsgroup were required (5 error probability 80statistical power) Analyses were performed on an intention-to-treat basis for all the participants who completed thebaseline and at least one follow-up measurement (finisheranalysis) The treatment effect was defined as between-groupdifferences in changes from baseline to 12months In order toobtain normally distributed data all endpoints (BMD LBM)were log-transformed Analysis of covariance with baselinevalue age height and fat and muscle mass as covariateswere carried for statistical comparison of the two studygroups Statistical significance was accepted at 119875 lt 005 (2-tailed) Effect sizes were calculated using Cohenrsquos d [19] Weused SPSS 190 (SPSS Inc Chicago IL) for all the statisticalprocedures

3 Results

16 (WB-EMS 119899 = 6 CG 119899 = 10) of 76 subjects were unableor unwilling to visit the one-year control assessment andwerethus lost to follow-up (Figure 1) Altogether 6women sufferedfractures surgery andor serious diseases (cancer CHD)

One subject of the CG lost interest and five subjects listedpersonal reasons for their withdrawal two of them related tothe CG protocol one related to the WB-EMS protocol Oneparticipant of the CG died during the interventional periodand one woman of each groupmovedThus 28 subjects of theCG (74) and 32 subjects of the WB-EMS group (84) wereincluded in the analysis No serious training-related adverseeffects were observed during the sessions

Summing up as total attendance in the WB-EMS group61 out of 78 sessions (79 plusmn 18) were conducted Thecorresponding attendance rate in the CG was slightly lower(74 plusmn 18 149 of 20 sessions) Although the total numberof sessions was much lower in the CG the difference in totalexercise volumewas smaller with an average ofasymp24minweekin the WB-EMS group and asymp18min in the CG

No intergroup differences were recorded for anthropo-metric and clinical parameters at baseline (Table 1) Withrespect to confounding parameters no significant changesbetween baseline and follow-up were observed for lifestyleparameters (physical activity eg) andor medication asrecorded by questionnaires or dietary intake as assessed by 4-day dietary protocol and analyzed using Prodi-4503 Expertsoftware (Wissenschaftlicher Verlag Freiburg Germany)

31 Primary and Secondary Outcome Measures BMD atthe LS increased in the WB-EMS groups (06 plusmn 25) anddecreased in the CG (minus06 plusmn 24) At the total hip ROIBMD decreased in both groups (WB-EMS minus09 plusmn 19versus CG minus10 plusmn 23) Similar negative changes wereobserved for the proximal femur subregions (femoral necktrochanter) Differences between WB-EMS and CG-groupwere borderline nonsignificant for LS-BMD (119875 = 0051 ES1198891015840= 049) and not significant for BMD of the total hip ROI

(119875 = 0771 ES 1198891015840 = 004)Total LBM as assessed by total body DXA scans increased

in the WB-EMS group (07 plusmn 16) and decreased in the CG(minus08 plusmn 25) Corresponding differences between WB-EMSand CG-group were significant (119875 = 0006 ES 1198891015840 = 071)

The changes in grip strength were 105 plusmn 126 in theWB-EMS group and 22 plusmn 819 in the CG (119875 = 0000 ES1198891015840= 071) Table 2 lists the changes of BMD and strength

parameters in both groups

4 Discussion

This is the first trial that determined the effect of (WB-) EMSon BMD at lumbar spine orand proximal femur in elderlyfemales with osteopenia We found a borderline significanteffect (119875 = 0051) for the lumbar spine BMD but not forthe femoral neck site In view of the high effects of WB-EMSon muscle mass and strength in previous studies [20 21] andthe close interaction of muscle and bone [8] we had expectedstronger effects on bone In the present study the effect ofWB-EMS on LBMwas significant but rather moderate showing a15 net gain However maximum isometric leg and trunkextension strength significantly increased by more than 10as published elsewhere [13]

All the other studies examining the effect of EMS in BMDexclusively determined (functional) electromyostimulation

Journal of Osteoporosis 5

Table 2 Baseline and follow-up data of the WB-EMS and CG group for BMD lumbar spine (LS) total hip lean body mass (LBM) and gripstrength absolute treatment effects between training and control and 119875 value (covariance analysis baseline value age height lean bodymass and fat mass)

WB-EMS (119899 = 32) CG (119899 = 28) Treatment effectGroup Baseline 12 months Baseline 12 months Mean (95 CI) 119875 value

Mean (SD) Mean (SD)BMD LS [mgcm2] 882 plusmn 178 886 plusmn 173 835 plusmn 103 830 plusmn 105 104 (minus213 to 05) 0051BMD hip [mgcm2] 763 plusmn 81 756 plusmn 85 754 plusmn 95 746 plusmn 0097 12 (minus90 to 661) 0771LBM (Kg) 3515 plusmn 443 3542 plusmn 440 3542 plusmn 352 3512 plusmn 36 057 (016 to 098) 0006Grip strength (Kg) 239 plusmn 40 2641 plusmn 36 231 39 236 plusmn 45 207 (088 to 326) 0000

(FEMS) under disuse conditions (eg SCI) [22ndash32] In therecent meta-analysis by Chang et al [9] the authors found asignificant increase in BMD after 3 6 and 12 months of FESleg cycling or FES knee extension exercises in SCI patientsA longer period of exercise and a higher training frequencywere associated with higher effectiveness Dolbow et al [10]reviewed 10 studies determining the effect of FES leg cyclingon BMD taking into account the time after injury Two oftwo studies report effects of FES therapy in the first 2 monthsafter injury only one of three studies showed effects at anaverage of 3ndash6 years after injury and 4 out of five 9ndash13 yearsafter injury In line with the results of Dolbow et al Biering-Soslashrensen et al [11] concluded in a systematic review including19 EMS studies that there may be some effects of electricalstimulation especially in the early phaseThis review includesstudies with EMS of the lower limb (4 studies) leg cyclingFES (7 studies) knee extention FES (5 studies) FES duringtreadmill gait (1 study) or a combination of leg cycle andknee extension FES Consistent with the results of Chang etal improvement is seen in a longer period of training or withhigher training frequency

Although the studies included in the meta-analysis andreviews differ widely with respect to subjects or measure-ments the large majority of trials which ensured sufficienttime for bone adaption (6ndash12months) reported positive BMDchanges at skeletal sites stimulated and loaded by EMS orFES cycling or FES leg-extension exercises However it can beassumed that in paralyzed subjects the strain threshold is lowdue to inactivity and it remains unclear if the positive BMDchanges were caused more by EMS induced muscle con-traction producing joint reaction forces or just by resultingexternal reaction forces leading to axial loading of bones dur-ing exercises like leg-extension or FEMS cycling And againthe relevance of the results of these studies for older peoplewithout serve functional limitations is rather questionable

A comparison of the effect of WB-EMS with ldquogold-standard exercise protocolsrdquo might be helpful for estimatingthe relevance ofWB-EMSprograms for fighting osteoporosisReviewing the literature for exercise-induced BMD changesin subjects 60 years and older as assessed byDXA (review [3334]) shows that our WB-EMS effects were lower comparedwith conventional exercise effects in particular when specificresistance exercise was applied Comparing the results ofthe present WB-EMS results with data of our recent 18-month SEFIP exercise trial [35] that used identical measure-ments and included comparable subjects with respect to age

(69 plusmn 4 yrs) with higher BMI (26 plusmn 4 kgm2) revealed morefavorable data for the SEFIP cohort (net BMD difference EGversus CG at LS and thip asymp15ndash21 both 119875 = 0001) that hadcarried out a combined resistanceaerobicbalance protocol

Little is known about the optimum EMS protocol forimpacting bone and the low effect on Bone Mineral Den-sity in the present study might be due to a suboptimalsetting of current parameters Although the most favor-able composition of EMS parameters for triggering boneadaptation still has to be established a recent study thatdirectly compared different frequencies of EMS in an animaldisuse model [36] determined the most favorable effect onbone parameters (eg volume fraction connectivity andtrabecular numberthickness) especially at 20 and 50HzWith respect to stimulation intensity Dudley-Javoroski andShields [12] suggested supramaximal amperage (200mA) toelicit very strong contractions Because each pair of electrodeswas regulated separately with different intensities and dueto differences in electrode size we were unable to controland describe the stimulation intensity (mA) in the presentstudy In EMS studies in SCI patients where isolated muscleswere stimulated external forces were measured and put intorelation with body weight to estimate intensity [31] Becauseof the simultaneous activation of agonists and antagonistsand resulting co-contraction this method cannot be usedin WB-EMS We applied EMS for 3 times 20min in 2 weeksusing a bipolar current at 85Hz at a pulse width of 350 120583secwhereas 6 sec of stimulation was intermitted by 4 sec of restThe highly significant effect of this protocol on muscle massand strength and its acceptance [20 21 37] supported theapplication of this EMS protocol

Considering that enthusiasm for conventional exercise israther low in the cohort of elderly women one key factorfor the relative high compliance with EMS training [33] mayhave been the low total volume of the program (in total30minweek) Furthermore WB-EMS programs are appliedunder rather individualized conditions and it may be also theexclusiveness of the exercise program that resulted in a highcompliance

Some limitations may decrease the evidence of thepresent study (a)We evaluated the effect of EMS in the cohortof lean elderly females with osteopenia and the assignabilityof our results to other cohorts is questionable (b) AlthoughDXA is still the ldquogold standardrdquo technology for assessingBMD QCT technique may be the more appropriate methodfor assessing BMD at lumbar spine in the cohort of subjects

6 Journal of Osteoporosis

70 years and older due to degenerative changes of the spine(c) No X-ray examinations have been performed to detectvertebral body fractures However we presume that BMDincreases in WB-EMS group were not the result of ldquotraininginducedrdquo compression fractures In the analyzed LS-scans nodecrease of area of the vertebra as sign of vertebral deformitywas observed Further duringWB-EMS themechanical load-ing of vertebrae due to muscular tension is rather moderatecompared to classic high impact training contents (d) Asemiactive control group that performed a comparable exer-cise volume and identical movements was implemented toensure blinding and to determine the effect of WB-EMS perse For reasons of attractiveness and compliance the CG didnot carry out only identical movements but also performedexercises for mobility coordination and relaxation and thetraining schedule differed However the movements of theWB-EMS program and all the contents of the CG sessionswere not strenuous and designed not to impact our endpointThus in our opinion the influences of the differences inexercises contents and schedule on the validity of the studiesare rather low (e) Due to a lower number of subjects included(76 instead of 80) and a slightly higher drop-out rate thanexpected we failed to realize our estimated sample size of31 subjectsgroup (g) It is not possible to objectify intensityof muscle contraction during WB-EMS and it is not clear ifsubjects realized the requested high intensity

5 Conclusions

In summary we found a borderline nonsignificant effect ofWB-EMS on Bone Mineral Density at the lumbar spine andno effect at the hip However taking into account the highimpact of this technology on muscle mass and strengthWB-EMS may be an option for musculoskeletal preven-tionrehabilitation at least for (elderly) subjects unable orunwilling to exercise conventionally Nevertheless due to thehigher impact of mixed exercise programs on BMD and theircomprehensive effect on multiple risk factors and diseasesof advanced age [38] classic exercise should be favored forelderly subjects

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors gratefully acknowledge the support of mihabodytec (Augsburg Germany) that supplied the WB-EMStechnology and RottapharmMadaus (Cologne Germany)that supplied calcium and vitamin D

References

[1] D A Nelson and M L Bouxsein ldquoExercise maintains bonemass but do people maintain exerciserdquo Journal of Bone andMineral Research vol 16 no 2 pp 202ndash205 2001

[2] Statistisches-Bundesamt Gesundheit in Deutschland Statistis-ches-Bundesamt Berlin Germany 2006

[3] D O Clark ldquoPhysical activity and its correlates among urbanprimary care patients aged 55 years or olderrdquo The Journals ofGerontology Series B Psychological Sciences and Social Sciencesvol 54 no 1 pp S41ndashS48 1999

[4] W Kemmler and S von Stengel ldquoDose-response effect of exer-cise frequency on bone mineral density in post-menopausalosteopenic womenrdquo Scandinavian Journal of Medicine andScience in Sports vol 24 no 3 pp 526ndash534 2014

[5] WKemmler and SVon Stengel ldquoExercise frequency health riskfactors and diseases of the elderlyrdquoArchives of PhysicalMedicineand Rehabilitation vol 94 no 11 pp 2046ndash2053 2013

[6] E C Cussler S B Going L B Houtkooper et al ldquoExercisefrequency and calcium intake predict 4-year bone changes inpostmenopausal womenrdquoOsteoporosis International vol 16 no12 pp 2129ndash2141 2005

[7] B TWall M L Dirks L B Verdijk et al ldquoNeuromuscular elec-trical stimulation increases muscle protein synthesis in elderlytype 2 diabetic menrdquo The American Journal of PhysiologymdashEndocrinology and Metabolism vol 303 no 5 pp E614ndashE6232012

[8] Y-X Qin H Lam S Ferreri and C Rubin ldquoDynamic skeletalmuscle stimulation and its potential in bone adaptationrdquo Jour-nal of Musculoskeletal amp Neuronal Interactions vol 10 no 1 pp12ndash24 2010

[9] K-V Chang C-Y Hung W-S Chen M-S Lai K-L Chienand D-S Han ldquoEffectiveness of bisphosphonate analoguesand functional electrical stimulation on attenuating post-injuryosteoporosis in spinal cord injury patients a systematic reviewand meta-analysisrdquo PLoS ONE vol 8 no 11 Article ID e811242013

[10] J D Dolbow D R Dolbow A S Gorgey R A Adler and D RGater ldquoThe effects of aging and electrical stimulation exerciseon bone after spinal cord injuryrdquo Aging and Disease vol 4 no3 pp 141ndash153 2013

[11] F Biering-Soslashrensen B Hansen and B S B Lee ldquoNon-phar-macological treatment and prevention of bone loss after spinalcord injury a systematic reviewrdquo Spinal Cord vol 47 no 7 pp508ndash518 2009

[12] S Dudley-Javoroski and R K Shields ldquoMuscle and boneplasticity after spinal cord injury reviewof adaptations to disuseand to electrical muscle stimulationrdquo Journal of RehabilitationResearch and Development vol 45 no 2 pp 283ndash296 2008

[13] W Kemmler M Bebenek K Engelke and S von StengelldquoImpact of whole-body electromyostimulation on body com-position in elderly women at risk for sarcopenia the Trainingand ElectroStimulation Trial (TEST-III)rdquo Age vol 36 no 1 pp395ndash406 2014

[14] V Mathiowetz K Weber G Volland and N Kashman ldquoReli-ability and validity of grip and pinch strength evaluationsrdquoTheJournal of Hand SurgerymdashAmerican Volume vol 9 no 2 pp222ndash226 1984

[15] S Fritz andM Lusardi ldquoWhite paper lsquowalking speed the sixthvital signrsquordquo Journal of Geriatric Physical Therapy vol 32 no 2pp 46ndash49 2009

[16] W Kemmler D Lauber JWeineck J HensenW Kalender andK Engelke ldquoBenefits of 2 years of intense exercise on bone den-sity physical fitness and blood lipids in early postmenopausalosteopenic women results of the Erlangen Fitness OsteoporosisPrevention Study (EFOPS)rdquo Archives of Internal Medicine vol164 no 10 pp 1084ndash1091 2004

Journal of Osteoporosis 7

[17] W Kemmler J Weineck W A Kalender and K EngelkeldquoThe effect of habitual physical activity non-athletic exercisemuscle strength andVO2max on bonemineral density is ratherlow in early postmenopausal osteopenic womenrdquo Journal ofMusculoskeletal amp Neuronal Interactions vol 4 no 3 pp 325ndash334 2004

[18] W Kemmler and S von Stengel ldquoWhole-body electromyostim-ulation as a means to impact muscle mass and abdominal bodyfat in lean sedentary older female adults subanalysis of theTEST-III trialrdquo Clinical Interventions in Aging vol 8 pp 1353ndash1364 2013

[19] J Cohen Statistical Power Analysis for the Behavioral SciencesLawrence Erlbaum Associates Hillsdale NJ USA 2nd edition1988

[20] W Kemmler A Birlauf and S von Stengel ldquoEinfluss von Ganz-korper-Elektromyostimulation auf das Metabolische Syndrombei alteren Mannern mit metabolischem Syndromrdquo DeutscheZeitschrift fur Sportmedizin vol 61 no 5 pp 117ndash123 2010

[21] W Kemmler R Schliffka J L Mayhew and S von Sten-gel ldquoEffects of whole-body electromyostimulation on restingmetabolic rate body composition and maximum strength inpostmenopausal women the training and electrostimulationtrialrdquo The Journal of Strength amp Conditioning Research vol 24no 7 pp 1880ndash1887 2010

[22] M C Ashe J J Eng A V Krassioukov D E R WarburtonC Hung and A Tawashy ldquoResponse to functional electricalstimulation cycling in women with spinal cord injuries usingdual-energy X-ray absorptiometry and peripheral quantitativecomputed tomography a case seriesrdquoThe Journal of Spinal CordMedicine vol 33 no 1 pp 68ndash72 2010

[23] M Belanger R B Stein G D Wheeler T Gordon and BLeduc ldquoElectrical stimulation can it increase muscle strengthand reverse osteopenia in spinal cord injured individualsrdquoArchives of Physical Medicine and Rehabilitation vol 81 no 8pp 1090ndash1098 2000

[24] K K BeDell A M E Scremin K L Perell and C F KunkelldquoEffects of functional electrical stimulation-induced lowerextremity cycling on bone density of spinal cord-injuredpatientsrdquo American Journal of Physical Medicine amp Rehabilita-tion vol 75 no 1 pp 29ndash34 1996

[25] S-C Chen C-H LaiW P ChanM-HHuangH-WTsai andJ-J J Chen ldquoIncreases in bone mineral density after functionalelectrical stimulation cycling exercises in spinal cord injuredpatientsrdquo Disability and Rehabilitation vol 27 no 22 pp 1337ndash1341 2005

[26] JM ClarkM Jelbart H Rischbieth et al ldquoPhysiological effectsof lower extremity functional electrical stimulation in earlyspinal cord injury lack of efficacy to prevent bone lossrdquo SpinalCord vol 45 no 1 pp 78ndash85 2007

[27] P Eser E D de Bruin I Telley H E Lechner H Knecht andE Stussi ldquoEffect of electrical stimulation-induced cycling onbone mineral density in spinal cord-injured patientsrdquo EuropeanJournal of Clinical Investigation vol 33 no 5 pp 412ndash419 2003

[28] A Frotzler S Coupaud C Perret et al ldquoHigh-volume FES-cycling partially reverses bone loss in people with chronic spinalcord injuryrdquo Bone vol 43 no 1 pp 169ndash176 2008

[29] T N Hangartner M M Rodgers R M Glaser and P SBarre ldquoTibial bone density loss in spinal cord injured patientseffects of FES exerciserdquo Journal of Rehabilitation Research andDevelopment vol 31 no 1 pp 50ndash61 1994

[30] T Mohr ldquoElectric stimulation in muscle training of the lowerextremities in persons with spinal cord injuriesrdquo Ugeskrift forLaeligger vol 162 no 15 pp 2190ndash2194 2000

[31] R K Shields and S Dudley-Javoroski ldquoMusculoskeletal plas-ticity after acute spinal cord injury effects of long-term neuro-muscular electrical stimulation trainingrdquo Journal of Neurophys-iology vol 95 no 4 pp 2380ndash2390 2006

[32] R K Shields and S Dudley-Javoroski ldquoMusculoskeletal adap-tations in chronic spinal cord injury effects of long-term soleuselectrical stimulation trainingrdquo Neurorehabilitation and NeuralRepair vol 21 no 2 pp 169ndash179 2007

[33] E A Marques J Mota and J Carvalho ldquoExercise effectson bone mineral density in older adults a meta-analysis ofrandomized controlled trialsrdquo Age vol 34 no 6 pp 1493ndash15152011

[34] A Gomez-Cabello I Ara A Gonzalez-Aguero J A Casajusand G Vicente-Rodrıguez ldquoEffects of training on bone mass inolder adults a systematic reviewrdquo Sports Medicine vol 42 no4 pp 301ndash325 2012

[35] W Kemmler S von Stengel K Engelke L Haberle J LMayhew and W A Kalender ldquoExercise body compositionand functional ability a randomized controlled trialrdquoAmericanJournal of Preventive Medicine vol 38 no 3 pp 279ndash287 2010

[36] H Lam and Y-X Qin ldquoThe effects of frequency-dependentdynamic muscle stimulation on inhibition of trabecular boneloss in a disuse modelrdquo Bone vol 43 no 6 pp 1093ndash1100 2008

[37] W Kemmler S von Stengel J Schwarz and J L MayhewldquoEffect of whole-body electromyostimulation on energy expen-diture during exerciserdquo The Journal of Strength amp ConditioningResearch vol 26 no 1 pp 240ndash245 2012

[38] M Borjesson M L Hellenius E Jansson et al PhysicalActivity in the Prevention and Treatment of Disease ProfessionalAssociation for Physical Activity (Pafpa) Stockholm Sweden2010

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 Whole-Body Electromyostimulation to Fight ...downloads.hindawi.com/journals/jos/2015/643520.pdf · e Training and Electrostimulation Trial (TEST) project is a series

Journal of Osteoporosis 5

Table 2 Baseline and follow-up data of the WB-EMS and CG group for BMD lumbar spine (LS) total hip lean body mass (LBM) and gripstrength absolute treatment effects between training and control and 119875 value (covariance analysis baseline value age height lean bodymass and fat mass)

WB-EMS (119899 = 32) CG (119899 = 28) Treatment effectGroup Baseline 12 months Baseline 12 months Mean (95 CI) 119875 value

Mean (SD) Mean (SD)BMD LS [mgcm2] 882 plusmn 178 886 plusmn 173 835 plusmn 103 830 plusmn 105 104 (minus213 to 05) 0051BMD hip [mgcm2] 763 plusmn 81 756 plusmn 85 754 plusmn 95 746 plusmn 0097 12 (minus90 to 661) 0771LBM (Kg) 3515 plusmn 443 3542 plusmn 440 3542 plusmn 352 3512 plusmn 36 057 (016 to 098) 0006Grip strength (Kg) 239 plusmn 40 2641 plusmn 36 231 39 236 plusmn 45 207 (088 to 326) 0000

(FEMS) under disuse conditions (eg SCI) [22ndash32] In therecent meta-analysis by Chang et al [9] the authors found asignificant increase in BMD after 3 6 and 12 months of FESleg cycling or FES knee extension exercises in SCI patientsA longer period of exercise and a higher training frequencywere associated with higher effectiveness Dolbow et al [10]reviewed 10 studies determining the effect of FES leg cyclingon BMD taking into account the time after injury Two oftwo studies report effects of FES therapy in the first 2 monthsafter injury only one of three studies showed effects at anaverage of 3ndash6 years after injury and 4 out of five 9ndash13 yearsafter injury In line with the results of Dolbow et al Biering-Soslashrensen et al [11] concluded in a systematic review including19 EMS studies that there may be some effects of electricalstimulation especially in the early phaseThis review includesstudies with EMS of the lower limb (4 studies) leg cyclingFES (7 studies) knee extention FES (5 studies) FES duringtreadmill gait (1 study) or a combination of leg cycle andknee extension FES Consistent with the results of Chang etal improvement is seen in a longer period of training or withhigher training frequency

Although the studies included in the meta-analysis andreviews differ widely with respect to subjects or measure-ments the large majority of trials which ensured sufficienttime for bone adaption (6ndash12months) reported positive BMDchanges at skeletal sites stimulated and loaded by EMS orFES cycling or FES leg-extension exercises However it can beassumed that in paralyzed subjects the strain threshold is lowdue to inactivity and it remains unclear if the positive BMDchanges were caused more by EMS induced muscle con-traction producing joint reaction forces or just by resultingexternal reaction forces leading to axial loading of bones dur-ing exercises like leg-extension or FEMS cycling And againthe relevance of the results of these studies for older peoplewithout serve functional limitations is rather questionable

A comparison of the effect of WB-EMS with ldquogold-standard exercise protocolsrdquo might be helpful for estimatingthe relevance ofWB-EMSprograms for fighting osteoporosisReviewing the literature for exercise-induced BMD changesin subjects 60 years and older as assessed byDXA (review [3334]) shows that our WB-EMS effects were lower comparedwith conventional exercise effects in particular when specificresistance exercise was applied Comparing the results ofthe present WB-EMS results with data of our recent 18-month SEFIP exercise trial [35] that used identical measure-ments and included comparable subjects with respect to age

(69 plusmn 4 yrs) with higher BMI (26 plusmn 4 kgm2) revealed morefavorable data for the SEFIP cohort (net BMD difference EGversus CG at LS and thip asymp15ndash21 both 119875 = 0001) that hadcarried out a combined resistanceaerobicbalance protocol

Little is known about the optimum EMS protocol forimpacting bone and the low effect on Bone Mineral Den-sity in the present study might be due to a suboptimalsetting of current parameters Although the most favor-able composition of EMS parameters for triggering boneadaptation still has to be established a recent study thatdirectly compared different frequencies of EMS in an animaldisuse model [36] determined the most favorable effect onbone parameters (eg volume fraction connectivity andtrabecular numberthickness) especially at 20 and 50HzWith respect to stimulation intensity Dudley-Javoroski andShields [12] suggested supramaximal amperage (200mA) toelicit very strong contractions Because each pair of electrodeswas regulated separately with different intensities and dueto differences in electrode size we were unable to controland describe the stimulation intensity (mA) in the presentstudy In EMS studies in SCI patients where isolated muscleswere stimulated external forces were measured and put intorelation with body weight to estimate intensity [31] Becauseof the simultaneous activation of agonists and antagonistsand resulting co-contraction this method cannot be usedin WB-EMS We applied EMS for 3 times 20min in 2 weeksusing a bipolar current at 85Hz at a pulse width of 350 120583secwhereas 6 sec of stimulation was intermitted by 4 sec of restThe highly significant effect of this protocol on muscle massand strength and its acceptance [20 21 37] supported theapplication of this EMS protocol

Considering that enthusiasm for conventional exercise israther low in the cohort of elderly women one key factorfor the relative high compliance with EMS training [33] mayhave been the low total volume of the program (in total30minweek) Furthermore WB-EMS programs are appliedunder rather individualized conditions and it may be also theexclusiveness of the exercise program that resulted in a highcompliance

Some limitations may decrease the evidence of thepresent study (a)We evaluated the effect of EMS in the cohortof lean elderly females with osteopenia and the assignabilityof our results to other cohorts is questionable (b) AlthoughDXA is still the ldquogold standardrdquo technology for assessingBMD QCT technique may be the more appropriate methodfor assessing BMD at lumbar spine in the cohort of subjects

6 Journal of Osteoporosis

70 years and older due to degenerative changes of the spine(c) No X-ray examinations have been performed to detectvertebral body fractures However we presume that BMDincreases in WB-EMS group were not the result of ldquotraininginducedrdquo compression fractures In the analyzed LS-scans nodecrease of area of the vertebra as sign of vertebral deformitywas observed Further duringWB-EMS themechanical load-ing of vertebrae due to muscular tension is rather moderatecompared to classic high impact training contents (d) Asemiactive control group that performed a comparable exer-cise volume and identical movements was implemented toensure blinding and to determine the effect of WB-EMS perse For reasons of attractiveness and compliance the CG didnot carry out only identical movements but also performedexercises for mobility coordination and relaxation and thetraining schedule differed However the movements of theWB-EMS program and all the contents of the CG sessionswere not strenuous and designed not to impact our endpointThus in our opinion the influences of the differences inexercises contents and schedule on the validity of the studiesare rather low (e) Due to a lower number of subjects included(76 instead of 80) and a slightly higher drop-out rate thanexpected we failed to realize our estimated sample size of31 subjectsgroup (g) It is not possible to objectify intensityof muscle contraction during WB-EMS and it is not clear ifsubjects realized the requested high intensity

5 Conclusions

In summary we found a borderline nonsignificant effect ofWB-EMS on Bone Mineral Density at the lumbar spine andno effect at the hip However taking into account the highimpact of this technology on muscle mass and strengthWB-EMS may be an option for musculoskeletal preven-tionrehabilitation at least for (elderly) subjects unable orunwilling to exercise conventionally Nevertheless due to thehigher impact of mixed exercise programs on BMD and theircomprehensive effect on multiple risk factors and diseasesof advanced age [38] classic exercise should be favored forelderly subjects

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors gratefully acknowledge the support of mihabodytec (Augsburg Germany) that supplied the WB-EMStechnology and RottapharmMadaus (Cologne Germany)that supplied calcium and vitamin D

References

[1] D A Nelson and M L Bouxsein ldquoExercise maintains bonemass but do people maintain exerciserdquo Journal of Bone andMineral Research vol 16 no 2 pp 202ndash205 2001

[2] Statistisches-Bundesamt Gesundheit in Deutschland Statistis-ches-Bundesamt Berlin Germany 2006

[3] D O Clark ldquoPhysical activity and its correlates among urbanprimary care patients aged 55 years or olderrdquo The Journals ofGerontology Series B Psychological Sciences and Social Sciencesvol 54 no 1 pp S41ndashS48 1999

[4] W Kemmler and S von Stengel ldquoDose-response effect of exer-cise frequency on bone mineral density in post-menopausalosteopenic womenrdquo Scandinavian Journal of Medicine andScience in Sports vol 24 no 3 pp 526ndash534 2014

[5] WKemmler and SVon Stengel ldquoExercise frequency health riskfactors and diseases of the elderlyrdquoArchives of PhysicalMedicineand Rehabilitation vol 94 no 11 pp 2046ndash2053 2013

[6] E C Cussler S B Going L B Houtkooper et al ldquoExercisefrequency and calcium intake predict 4-year bone changes inpostmenopausal womenrdquoOsteoporosis International vol 16 no12 pp 2129ndash2141 2005

[7] B TWall M L Dirks L B Verdijk et al ldquoNeuromuscular elec-trical stimulation increases muscle protein synthesis in elderlytype 2 diabetic menrdquo The American Journal of PhysiologymdashEndocrinology and Metabolism vol 303 no 5 pp E614ndashE6232012

[8] Y-X Qin H Lam S Ferreri and C Rubin ldquoDynamic skeletalmuscle stimulation and its potential in bone adaptationrdquo Jour-nal of Musculoskeletal amp Neuronal Interactions vol 10 no 1 pp12ndash24 2010

[9] K-V Chang C-Y Hung W-S Chen M-S Lai K-L Chienand D-S Han ldquoEffectiveness of bisphosphonate analoguesand functional electrical stimulation on attenuating post-injuryosteoporosis in spinal cord injury patients a systematic reviewand meta-analysisrdquo PLoS ONE vol 8 no 11 Article ID e811242013

[10] J D Dolbow D R Dolbow A S Gorgey R A Adler and D RGater ldquoThe effects of aging and electrical stimulation exerciseon bone after spinal cord injuryrdquo Aging and Disease vol 4 no3 pp 141ndash153 2013

[11] F Biering-Soslashrensen B Hansen and B S B Lee ldquoNon-phar-macological treatment and prevention of bone loss after spinalcord injury a systematic reviewrdquo Spinal Cord vol 47 no 7 pp508ndash518 2009

[12] S Dudley-Javoroski and R K Shields ldquoMuscle and boneplasticity after spinal cord injury reviewof adaptations to disuseand to electrical muscle stimulationrdquo Journal of RehabilitationResearch and Development vol 45 no 2 pp 283ndash296 2008

[13] W Kemmler M Bebenek K Engelke and S von StengelldquoImpact of whole-body electromyostimulation on body com-position in elderly women at risk for sarcopenia the Trainingand ElectroStimulation Trial (TEST-III)rdquo Age vol 36 no 1 pp395ndash406 2014

[14] V Mathiowetz K Weber G Volland and N Kashman ldquoReli-ability and validity of grip and pinch strength evaluationsrdquoTheJournal of Hand SurgerymdashAmerican Volume vol 9 no 2 pp222ndash226 1984

[15] S Fritz andM Lusardi ldquoWhite paper lsquowalking speed the sixthvital signrsquordquo Journal of Geriatric Physical Therapy vol 32 no 2pp 46ndash49 2009

[16] W Kemmler D Lauber JWeineck J HensenW Kalender andK Engelke ldquoBenefits of 2 years of intense exercise on bone den-sity physical fitness and blood lipids in early postmenopausalosteopenic women results of the Erlangen Fitness OsteoporosisPrevention Study (EFOPS)rdquo Archives of Internal Medicine vol164 no 10 pp 1084ndash1091 2004

Journal of Osteoporosis 7

[17] W Kemmler J Weineck W A Kalender and K EngelkeldquoThe effect of habitual physical activity non-athletic exercisemuscle strength andVO2max on bonemineral density is ratherlow in early postmenopausal osteopenic womenrdquo Journal ofMusculoskeletal amp Neuronal Interactions vol 4 no 3 pp 325ndash334 2004

[18] W Kemmler and S von Stengel ldquoWhole-body electromyostim-ulation as a means to impact muscle mass and abdominal bodyfat in lean sedentary older female adults subanalysis of theTEST-III trialrdquo Clinical Interventions in Aging vol 8 pp 1353ndash1364 2013

[19] J Cohen Statistical Power Analysis for the Behavioral SciencesLawrence Erlbaum Associates Hillsdale NJ USA 2nd edition1988

[20] W Kemmler A Birlauf and S von Stengel ldquoEinfluss von Ganz-korper-Elektromyostimulation auf das Metabolische Syndrombei alteren Mannern mit metabolischem Syndromrdquo DeutscheZeitschrift fur Sportmedizin vol 61 no 5 pp 117ndash123 2010

[21] W Kemmler R Schliffka J L Mayhew and S von Sten-gel ldquoEffects of whole-body electromyostimulation on restingmetabolic rate body composition and maximum strength inpostmenopausal women the training and electrostimulationtrialrdquo The Journal of Strength amp Conditioning Research vol 24no 7 pp 1880ndash1887 2010

[22] M C Ashe J J Eng A V Krassioukov D E R WarburtonC Hung and A Tawashy ldquoResponse to functional electricalstimulation cycling in women with spinal cord injuries usingdual-energy X-ray absorptiometry and peripheral quantitativecomputed tomography a case seriesrdquoThe Journal of Spinal CordMedicine vol 33 no 1 pp 68ndash72 2010

[23] M Belanger R B Stein G D Wheeler T Gordon and BLeduc ldquoElectrical stimulation can it increase muscle strengthand reverse osteopenia in spinal cord injured individualsrdquoArchives of Physical Medicine and Rehabilitation vol 81 no 8pp 1090ndash1098 2000

[24] K K BeDell A M E Scremin K L Perell and C F KunkelldquoEffects of functional electrical stimulation-induced lowerextremity cycling on bone density of spinal cord-injuredpatientsrdquo American Journal of Physical Medicine amp Rehabilita-tion vol 75 no 1 pp 29ndash34 1996

[25] S-C Chen C-H LaiW P ChanM-HHuangH-WTsai andJ-J J Chen ldquoIncreases in bone mineral density after functionalelectrical stimulation cycling exercises in spinal cord injuredpatientsrdquo Disability and Rehabilitation vol 27 no 22 pp 1337ndash1341 2005

[26] JM ClarkM Jelbart H Rischbieth et al ldquoPhysiological effectsof lower extremity functional electrical stimulation in earlyspinal cord injury lack of efficacy to prevent bone lossrdquo SpinalCord vol 45 no 1 pp 78ndash85 2007

[27] P Eser E D de Bruin I Telley H E Lechner H Knecht andE Stussi ldquoEffect of electrical stimulation-induced cycling onbone mineral density in spinal cord-injured patientsrdquo EuropeanJournal of Clinical Investigation vol 33 no 5 pp 412ndash419 2003

[28] A Frotzler S Coupaud C Perret et al ldquoHigh-volume FES-cycling partially reverses bone loss in people with chronic spinalcord injuryrdquo Bone vol 43 no 1 pp 169ndash176 2008

[29] T N Hangartner M M Rodgers R M Glaser and P SBarre ldquoTibial bone density loss in spinal cord injured patientseffects of FES exerciserdquo Journal of Rehabilitation Research andDevelopment vol 31 no 1 pp 50ndash61 1994

[30] T Mohr ldquoElectric stimulation in muscle training of the lowerextremities in persons with spinal cord injuriesrdquo Ugeskrift forLaeligger vol 162 no 15 pp 2190ndash2194 2000

[31] R K Shields and S Dudley-Javoroski ldquoMusculoskeletal plas-ticity after acute spinal cord injury effects of long-term neuro-muscular electrical stimulation trainingrdquo Journal of Neurophys-iology vol 95 no 4 pp 2380ndash2390 2006

[32] R K Shields and S Dudley-Javoroski ldquoMusculoskeletal adap-tations in chronic spinal cord injury effects of long-term soleuselectrical stimulation trainingrdquo Neurorehabilitation and NeuralRepair vol 21 no 2 pp 169ndash179 2007

[33] E A Marques J Mota and J Carvalho ldquoExercise effectson bone mineral density in older adults a meta-analysis ofrandomized controlled trialsrdquo Age vol 34 no 6 pp 1493ndash15152011

[34] A Gomez-Cabello I Ara A Gonzalez-Aguero J A Casajusand G Vicente-Rodrıguez ldquoEffects of training on bone mass inolder adults a systematic reviewrdquo Sports Medicine vol 42 no4 pp 301ndash325 2012

[35] W Kemmler S von Stengel K Engelke L Haberle J LMayhew and W A Kalender ldquoExercise body compositionand functional ability a randomized controlled trialrdquoAmericanJournal of Preventive Medicine vol 38 no 3 pp 279ndash287 2010

[36] H Lam and Y-X Qin ldquoThe effects of frequency-dependentdynamic muscle stimulation on inhibition of trabecular boneloss in a disuse modelrdquo Bone vol 43 no 6 pp 1093ndash1100 2008

[37] W Kemmler S von Stengel J Schwarz and J L MayhewldquoEffect of whole-body electromyostimulation on energy expen-diture during exerciserdquo The Journal of Strength amp ConditioningResearch vol 26 no 1 pp 240ndash245 2012

[38] M Borjesson M L Hellenius E Jansson et al PhysicalActivity in the Prevention and Treatment of Disease ProfessionalAssociation for Physical Activity (Pafpa) Stockholm Sweden2010

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 Whole-Body Electromyostimulation to Fight ...downloads.hindawi.com/journals/jos/2015/643520.pdf · e Training and Electrostimulation Trial (TEST) project is a series

6 Journal of Osteoporosis

70 years and older due to degenerative changes of the spine(c) No X-ray examinations have been performed to detectvertebral body fractures However we presume that BMDincreases in WB-EMS group were not the result of ldquotraininginducedrdquo compression fractures In the analyzed LS-scans nodecrease of area of the vertebra as sign of vertebral deformitywas observed Further duringWB-EMS themechanical load-ing of vertebrae due to muscular tension is rather moderatecompared to classic high impact training contents (d) Asemiactive control group that performed a comparable exer-cise volume and identical movements was implemented toensure blinding and to determine the effect of WB-EMS perse For reasons of attractiveness and compliance the CG didnot carry out only identical movements but also performedexercises for mobility coordination and relaxation and thetraining schedule differed However the movements of theWB-EMS program and all the contents of the CG sessionswere not strenuous and designed not to impact our endpointThus in our opinion the influences of the differences inexercises contents and schedule on the validity of the studiesare rather low (e) Due to a lower number of subjects included(76 instead of 80) and a slightly higher drop-out rate thanexpected we failed to realize our estimated sample size of31 subjectsgroup (g) It is not possible to objectify intensityof muscle contraction during WB-EMS and it is not clear ifsubjects realized the requested high intensity

5 Conclusions

In summary we found a borderline nonsignificant effect ofWB-EMS on Bone Mineral Density at the lumbar spine andno effect at the hip However taking into account the highimpact of this technology on muscle mass and strengthWB-EMS may be an option for musculoskeletal preven-tionrehabilitation at least for (elderly) subjects unable orunwilling to exercise conventionally Nevertheless due to thehigher impact of mixed exercise programs on BMD and theircomprehensive effect on multiple risk factors and diseasesof advanced age [38] classic exercise should be favored forelderly subjects

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors gratefully acknowledge the support of mihabodytec (Augsburg Germany) that supplied the WB-EMStechnology and RottapharmMadaus (Cologne Germany)that supplied calcium and vitamin D

References

[1] D A Nelson and M L Bouxsein ldquoExercise maintains bonemass but do people maintain exerciserdquo Journal of Bone andMineral Research vol 16 no 2 pp 202ndash205 2001

[2] Statistisches-Bundesamt Gesundheit in Deutschland Statistis-ches-Bundesamt Berlin Germany 2006

[3] D O Clark ldquoPhysical activity and its correlates among urbanprimary care patients aged 55 years or olderrdquo The Journals ofGerontology Series B Psychological Sciences and Social Sciencesvol 54 no 1 pp S41ndashS48 1999

[4] W Kemmler and S von Stengel ldquoDose-response effect of exer-cise frequency on bone mineral density in post-menopausalosteopenic womenrdquo Scandinavian Journal of Medicine andScience in Sports vol 24 no 3 pp 526ndash534 2014

[5] WKemmler and SVon Stengel ldquoExercise frequency health riskfactors and diseases of the elderlyrdquoArchives of PhysicalMedicineand Rehabilitation vol 94 no 11 pp 2046ndash2053 2013

[6] E C Cussler S B Going L B Houtkooper et al ldquoExercisefrequency and calcium intake predict 4-year bone changes inpostmenopausal womenrdquoOsteoporosis International vol 16 no12 pp 2129ndash2141 2005

[7] B TWall M L Dirks L B Verdijk et al ldquoNeuromuscular elec-trical stimulation increases muscle protein synthesis in elderlytype 2 diabetic menrdquo The American Journal of PhysiologymdashEndocrinology and Metabolism vol 303 no 5 pp E614ndashE6232012

[8] Y-X Qin H Lam S Ferreri and C Rubin ldquoDynamic skeletalmuscle stimulation and its potential in bone adaptationrdquo Jour-nal of Musculoskeletal amp Neuronal Interactions vol 10 no 1 pp12ndash24 2010

[9] K-V Chang C-Y Hung W-S Chen M-S Lai K-L Chienand D-S Han ldquoEffectiveness of bisphosphonate analoguesand functional electrical stimulation on attenuating post-injuryosteoporosis in spinal cord injury patients a systematic reviewand meta-analysisrdquo PLoS ONE vol 8 no 11 Article ID e811242013

[10] J D Dolbow D R Dolbow A S Gorgey R A Adler and D RGater ldquoThe effects of aging and electrical stimulation exerciseon bone after spinal cord injuryrdquo Aging and Disease vol 4 no3 pp 141ndash153 2013

[11] F Biering-Soslashrensen B Hansen and B S B Lee ldquoNon-phar-macological treatment and prevention of bone loss after spinalcord injury a systematic reviewrdquo Spinal Cord vol 47 no 7 pp508ndash518 2009

[12] S Dudley-Javoroski and R K Shields ldquoMuscle and boneplasticity after spinal cord injury reviewof adaptations to disuseand to electrical muscle stimulationrdquo Journal of RehabilitationResearch and Development vol 45 no 2 pp 283ndash296 2008

[13] W Kemmler M Bebenek K Engelke and S von StengelldquoImpact of whole-body electromyostimulation on body com-position in elderly women at risk for sarcopenia the Trainingand ElectroStimulation Trial (TEST-III)rdquo Age vol 36 no 1 pp395ndash406 2014

[14] V Mathiowetz K Weber G Volland and N Kashman ldquoReli-ability and validity of grip and pinch strength evaluationsrdquoTheJournal of Hand SurgerymdashAmerican Volume vol 9 no 2 pp222ndash226 1984

[15] S Fritz andM Lusardi ldquoWhite paper lsquowalking speed the sixthvital signrsquordquo Journal of Geriatric Physical Therapy vol 32 no 2pp 46ndash49 2009

[16] W Kemmler D Lauber JWeineck J HensenW Kalender andK Engelke ldquoBenefits of 2 years of intense exercise on bone den-sity physical fitness and blood lipids in early postmenopausalosteopenic women results of the Erlangen Fitness OsteoporosisPrevention Study (EFOPS)rdquo Archives of Internal Medicine vol164 no 10 pp 1084ndash1091 2004

Journal of Osteoporosis 7

[17] W Kemmler J Weineck W A Kalender and K EngelkeldquoThe effect of habitual physical activity non-athletic exercisemuscle strength andVO2max on bonemineral density is ratherlow in early postmenopausal osteopenic womenrdquo Journal ofMusculoskeletal amp Neuronal Interactions vol 4 no 3 pp 325ndash334 2004

[18] W Kemmler and S von Stengel ldquoWhole-body electromyostim-ulation as a means to impact muscle mass and abdominal bodyfat in lean sedentary older female adults subanalysis of theTEST-III trialrdquo Clinical Interventions in Aging vol 8 pp 1353ndash1364 2013

[19] J Cohen Statistical Power Analysis for the Behavioral SciencesLawrence Erlbaum Associates Hillsdale NJ USA 2nd edition1988

[20] W Kemmler A Birlauf and S von Stengel ldquoEinfluss von Ganz-korper-Elektromyostimulation auf das Metabolische Syndrombei alteren Mannern mit metabolischem Syndromrdquo DeutscheZeitschrift fur Sportmedizin vol 61 no 5 pp 117ndash123 2010

[21] W Kemmler R Schliffka J L Mayhew and S von Sten-gel ldquoEffects of whole-body electromyostimulation on restingmetabolic rate body composition and maximum strength inpostmenopausal women the training and electrostimulationtrialrdquo The Journal of Strength amp Conditioning Research vol 24no 7 pp 1880ndash1887 2010

[22] M C Ashe J J Eng A V Krassioukov D E R WarburtonC Hung and A Tawashy ldquoResponse to functional electricalstimulation cycling in women with spinal cord injuries usingdual-energy X-ray absorptiometry and peripheral quantitativecomputed tomography a case seriesrdquoThe Journal of Spinal CordMedicine vol 33 no 1 pp 68ndash72 2010

[23] M Belanger R B Stein G D Wheeler T Gordon and BLeduc ldquoElectrical stimulation can it increase muscle strengthand reverse osteopenia in spinal cord injured individualsrdquoArchives of Physical Medicine and Rehabilitation vol 81 no 8pp 1090ndash1098 2000

[24] K K BeDell A M E Scremin K L Perell and C F KunkelldquoEffects of functional electrical stimulation-induced lowerextremity cycling on bone density of spinal cord-injuredpatientsrdquo American Journal of Physical Medicine amp Rehabilita-tion vol 75 no 1 pp 29ndash34 1996

[25] S-C Chen C-H LaiW P ChanM-HHuangH-WTsai andJ-J J Chen ldquoIncreases in bone mineral density after functionalelectrical stimulation cycling exercises in spinal cord injuredpatientsrdquo Disability and Rehabilitation vol 27 no 22 pp 1337ndash1341 2005

[26] JM ClarkM Jelbart H Rischbieth et al ldquoPhysiological effectsof lower extremity functional electrical stimulation in earlyspinal cord injury lack of efficacy to prevent bone lossrdquo SpinalCord vol 45 no 1 pp 78ndash85 2007

[27] P Eser E D de Bruin I Telley H E Lechner H Knecht andE Stussi ldquoEffect of electrical stimulation-induced cycling onbone mineral density in spinal cord-injured patientsrdquo EuropeanJournal of Clinical Investigation vol 33 no 5 pp 412ndash419 2003

[28] A Frotzler S Coupaud C Perret et al ldquoHigh-volume FES-cycling partially reverses bone loss in people with chronic spinalcord injuryrdquo Bone vol 43 no 1 pp 169ndash176 2008

[29] T N Hangartner M M Rodgers R M Glaser and P SBarre ldquoTibial bone density loss in spinal cord injured patientseffects of FES exerciserdquo Journal of Rehabilitation Research andDevelopment vol 31 no 1 pp 50ndash61 1994

[30] T Mohr ldquoElectric stimulation in muscle training of the lowerextremities in persons with spinal cord injuriesrdquo Ugeskrift forLaeligger vol 162 no 15 pp 2190ndash2194 2000

[31] R K Shields and S Dudley-Javoroski ldquoMusculoskeletal plas-ticity after acute spinal cord injury effects of long-term neuro-muscular electrical stimulation trainingrdquo Journal of Neurophys-iology vol 95 no 4 pp 2380ndash2390 2006

[32] R K Shields and S Dudley-Javoroski ldquoMusculoskeletal adap-tations in chronic spinal cord injury effects of long-term soleuselectrical stimulation trainingrdquo Neurorehabilitation and NeuralRepair vol 21 no 2 pp 169ndash179 2007

[33] E A Marques J Mota and J Carvalho ldquoExercise effectson bone mineral density in older adults a meta-analysis ofrandomized controlled trialsrdquo Age vol 34 no 6 pp 1493ndash15152011

[34] A Gomez-Cabello I Ara A Gonzalez-Aguero J A Casajusand G Vicente-Rodrıguez ldquoEffects of training on bone mass inolder adults a systematic reviewrdquo Sports Medicine vol 42 no4 pp 301ndash325 2012

[35] W Kemmler S von Stengel K Engelke L Haberle J LMayhew and W A Kalender ldquoExercise body compositionand functional ability a randomized controlled trialrdquoAmericanJournal of Preventive Medicine vol 38 no 3 pp 279ndash287 2010

[36] H Lam and Y-X Qin ldquoThe effects of frequency-dependentdynamic muscle stimulation on inhibition of trabecular boneloss in a disuse modelrdquo Bone vol 43 no 6 pp 1093ndash1100 2008

[37] W Kemmler S von Stengel J Schwarz and J L MayhewldquoEffect of whole-body electromyostimulation on energy expen-diture during exerciserdquo The Journal of Strength amp ConditioningResearch vol 26 no 1 pp 240ndash245 2012

[38] M Borjesson M L Hellenius E Jansson et al PhysicalActivity in the Prevention and Treatment of Disease ProfessionalAssociation for Physical Activity (Pafpa) Stockholm Sweden2010

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 Whole-Body Electromyostimulation to Fight ...downloads.hindawi.com/journals/jos/2015/643520.pdf · e Training and Electrostimulation Trial (TEST) project is a series

Journal of Osteoporosis 7

[17] W Kemmler J Weineck W A Kalender and K EngelkeldquoThe effect of habitual physical activity non-athletic exercisemuscle strength andVO2max on bonemineral density is ratherlow in early postmenopausal osteopenic womenrdquo Journal ofMusculoskeletal amp Neuronal Interactions vol 4 no 3 pp 325ndash334 2004

[18] W Kemmler and S von Stengel ldquoWhole-body electromyostim-ulation as a means to impact muscle mass and abdominal bodyfat in lean sedentary older female adults subanalysis of theTEST-III trialrdquo Clinical Interventions in Aging vol 8 pp 1353ndash1364 2013

[19] J Cohen Statistical Power Analysis for the Behavioral SciencesLawrence Erlbaum Associates Hillsdale NJ USA 2nd edition1988

[20] W Kemmler A Birlauf and S von Stengel ldquoEinfluss von Ganz-korper-Elektromyostimulation auf das Metabolische Syndrombei alteren Mannern mit metabolischem Syndromrdquo DeutscheZeitschrift fur Sportmedizin vol 61 no 5 pp 117ndash123 2010

[21] W Kemmler R Schliffka J L Mayhew and S von Sten-gel ldquoEffects of whole-body electromyostimulation on restingmetabolic rate body composition and maximum strength inpostmenopausal women the training and electrostimulationtrialrdquo The Journal of Strength amp Conditioning Research vol 24no 7 pp 1880ndash1887 2010

[22] M C Ashe J J Eng A V Krassioukov D E R WarburtonC Hung and A Tawashy ldquoResponse to functional electricalstimulation cycling in women with spinal cord injuries usingdual-energy X-ray absorptiometry and peripheral quantitativecomputed tomography a case seriesrdquoThe Journal of Spinal CordMedicine vol 33 no 1 pp 68ndash72 2010

[23] M Belanger R B Stein G D Wheeler T Gordon and BLeduc ldquoElectrical stimulation can it increase muscle strengthand reverse osteopenia in spinal cord injured individualsrdquoArchives of Physical Medicine and Rehabilitation vol 81 no 8pp 1090ndash1098 2000

[24] K K BeDell A M E Scremin K L Perell and C F KunkelldquoEffects of functional electrical stimulation-induced lowerextremity cycling on bone density of spinal cord-injuredpatientsrdquo American Journal of Physical Medicine amp Rehabilita-tion vol 75 no 1 pp 29ndash34 1996

[25] S-C Chen C-H LaiW P ChanM-HHuangH-WTsai andJ-J J Chen ldquoIncreases in bone mineral density after functionalelectrical stimulation cycling exercises in spinal cord injuredpatientsrdquo Disability and Rehabilitation vol 27 no 22 pp 1337ndash1341 2005

[26] JM ClarkM Jelbart H Rischbieth et al ldquoPhysiological effectsof lower extremity functional electrical stimulation in earlyspinal cord injury lack of efficacy to prevent bone lossrdquo SpinalCord vol 45 no 1 pp 78ndash85 2007

[27] P Eser E D de Bruin I Telley H E Lechner H Knecht andE Stussi ldquoEffect of electrical stimulation-induced cycling onbone mineral density in spinal cord-injured patientsrdquo EuropeanJournal of Clinical Investigation vol 33 no 5 pp 412ndash419 2003

[28] A Frotzler S Coupaud C Perret et al ldquoHigh-volume FES-cycling partially reverses bone loss in people with chronic spinalcord injuryrdquo Bone vol 43 no 1 pp 169ndash176 2008

[29] T N Hangartner M M Rodgers R M Glaser and P SBarre ldquoTibial bone density loss in spinal cord injured patientseffects of FES exerciserdquo Journal of Rehabilitation Research andDevelopment vol 31 no 1 pp 50ndash61 1994

[30] T Mohr ldquoElectric stimulation in muscle training of the lowerextremities in persons with spinal cord injuriesrdquo Ugeskrift forLaeligger vol 162 no 15 pp 2190ndash2194 2000

[31] R K Shields and S Dudley-Javoroski ldquoMusculoskeletal plas-ticity after acute spinal cord injury effects of long-term neuro-muscular electrical stimulation trainingrdquo Journal of Neurophys-iology vol 95 no 4 pp 2380ndash2390 2006

[32] R K Shields and S Dudley-Javoroski ldquoMusculoskeletal adap-tations in chronic spinal cord injury effects of long-term soleuselectrical stimulation trainingrdquo Neurorehabilitation and NeuralRepair vol 21 no 2 pp 169ndash179 2007

[33] E A Marques J Mota and J Carvalho ldquoExercise effectson bone mineral density in older adults a meta-analysis ofrandomized controlled trialsrdquo Age vol 34 no 6 pp 1493ndash15152011

[34] A Gomez-Cabello I Ara A Gonzalez-Aguero J A Casajusand G Vicente-Rodrıguez ldquoEffects of training on bone mass inolder adults a systematic reviewrdquo Sports Medicine vol 42 no4 pp 301ndash325 2012

[35] W Kemmler S von Stengel K Engelke L Haberle J LMayhew and W A Kalender ldquoExercise body compositionand functional ability a randomized controlled trialrdquoAmericanJournal of Preventive Medicine vol 38 no 3 pp 279ndash287 2010

[36] H Lam and Y-X Qin ldquoThe effects of frequency-dependentdynamic muscle stimulation on inhibition of trabecular boneloss in a disuse modelrdquo Bone vol 43 no 6 pp 1093ndash1100 2008

[37] W Kemmler S von Stengel J Schwarz and J L MayhewldquoEffect of whole-body electromyostimulation on energy expen-diture during exerciserdquo The Journal of Strength amp ConditioningResearch vol 26 no 1 pp 240ndash245 2012

[38] M Borjesson M L Hellenius E Jansson et al PhysicalActivity in the Prevention and Treatment of Disease ProfessionalAssociation for Physical Activity (Pafpa) Stockholm Sweden2010

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 Whole-Body Electromyostimulation to Fight ...downloads.hindawi.com/journals/jos/2015/643520.pdf · e Training and Electrostimulation Trial (TEST) project is a series

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