Older Age Is Associated with Lower Optimal Vibration Frequency in Lower-Limb Muscles During...

Muscle

ORIGINAL RESEARCH ARTICLE

Older Age Is Associated with LowerOptimal Vibration Frequency inLower-Limb Muscles DuringWhole-Body Vibration

ABSTRACT

Carlucci F, Orlando G, Haxhi J, Laudani L, Giombini A, Macaluso A, Pigozzi F,

Sacchetti M: Older age is associated with lower optimal vibration frequency in

lower-limb muscles during whole-body vibration. Am J Phys Med Rehabil

2014;00:00Y00.

Objective: The aim of this study was to compare the optimal vibration fre-

quency (OVF), which corresponds to maximal electromyographic muscle response

during whole-body vibration, between young, middle-aged, and older women in four

muscles of the lower-limbs.

Design: OVF was measured as the frequency corresponding to maximal root

mean square of the surface electromyogram (RMSmax) during a continuous in-

cremental protocol, with a succession of vibration frequencies from 20 to 55 Hz

(A = 2 mm), on the vastus lateralis, vastus medialis, rectus femoris, and gastroc-

nemius lateralis muscles of the dominant lower-limb. Seventy-eight women were

divided into three age groups, that is, young, 21.6 T 2.4 yrs; middle aged, 43.0 T

5.2 yrs; and older, 74.2 T 6.0 yrs.

Results: OVF in the vastus medialis was lower in the older women than in the

middle-aged and young women, whereas OVF in the vastus lateralis was lower in

the older than in the young women. There were no differences in OVF between

muscles within each group. RMSmax was higher in the older than in the young

women in all muscles.

Conclusions: Age range should be taken into consideration when determining

OVF because it decreases with age. Properly individualizing the vibration protocol

might greatly influence neuromuscular effects of vibration training.

KeyWords: Whole-Body Vibration, Maximal Muscle Activity, Lower-LimbMuscles,Women

Authors:Flaminia Carlucci, PhDGiorgio Orlando, MScJonida Haxhi, MDLuca Laudani, PhDArrigo Giombini, MDAndrea Macaluso, MD, PhDFabio Pigozzi, MDMassimo Sacchetti, PhD

Affiliations:From the Department of Movement,Human and Health Sciences,University of Rome Foro Italico, Rome(FC, GO, JH, LL, AM, FP, MS); andDepartment of Medicine and HealthSciences, University of Molise,Campobasso, Italy (AG).

Correspondence:All correspondence and requests forreprints should be addressed to:Massimo Sacchetti, PhD, Departmentof Movement, Human and HealthSciences, University of RomeForo Italico.

Disclosures:Financial disclosure statements havebeen obtained, and no conflicts ofinterest have been reported by theauthors or by any individuals in controlof the content of this article.

0894-9115/14/0000-0000American Journal of PhysicalMedicine & RehabilitationCopyright * 2014 by LippincottWilliams & Wilkins

DOI: 10.1097/PHM.0000000000000193

www.ajpmr.com Lower Optimal Vibration Frequency 1

Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

Aging may lead to progressive disability and lossof independence because of a decrease in neuro-muscular function.1 In particular, the decline instrength, muscle power,2,3 skeletal muscle mass,and bone density1 could be addressed by trainingprograms based on whole-body vibration.4,5 Womenare more at risk than men for falls and the onset ofdisability with aging, and for this reason, they havebeen identified as the primary target group for in-tervention and rehabilitation studies.6Y8

Whole-body vibration (WBV) training hasrecently been incorporated into sport training inathletes and into rehabilitation programs aimed atmuscle conditioning in older individuals.9,10 Vibra-tion has been suggested to induce neuromuscu-lar facilitation, which results in improved musclestrength, power, and coordination as well as in-creased muscle fiber recruitment, synchronization,and proprioceptive responses.9 The mechanical vi-bration stimuli induce reflex muscle contractions,similar to the tonic vibration reflex,11 by activat-ing sensory receptors of skin and tendons and, mostimportantly, muscle spindles.12Y14 In turn, thesestimuli determine an excitatory influence on ago-nistic alpha motoneurons and an inhibitory influ-ence on antagonistic motor neurons.15 Although thismechanism has been experimentally demonstratedonly during exposure to focal vibration, it has beensuggested that mechanisms are similar in the case ofWBV.13,16 The magnitude of this neuromuscular re-sponse may depend on the type, frequency, ampli-tude, and duration of the vibration stimulus17Y21 aswell as on joint angle11,22 and body position on thevibration platform.17,20,23,24

Among all of these parameters, vibration fre-quency seems to have an important role on thebody’s response to vibration. Indeed, it is possiblethat some people are more sensitive than others toa given vibration frequency.19 Such a differencemight be caused by a greater level of muscle spindleactivation and, consequently, different surface elec-tromyographic (sEMG) responses.9,19,20 Although theunderlying mechanisms have not been identifiedyet, interindividual and intraindividual variabilitycaused by factors such as age, training status, thepercentage of fast-twitch muscle fibers, or Ia affer-ent sensitivity may play an important role. Suchvariables may affect the maximal excitability of spi-nal reflexes during vibration, which, in turn, mayalter electromechanical contractile proprieties ofthe alpha motor neurons.25Y28 Thus, the existence ofa specific frequency, referred to as optimal vibrationfrequency (OVF), has been proposed to characterize

the response of each individual to vibration.19 OVFhas been defined as the vibration frequency (hertz) atwhich maximal muscle activation, intended as max-imal root mean square (RMS) of the EMG signal,occurs.4,19 This individual OVF, which usually com-prises between 20 and 55 Hz for platforms trans-mitting the vibration along the vertical axis, has beensuggested to optimize the functional activation ofthe primary endings of the muscle spindle and in-duce the greatest neuromuscular activations.19

In WBV training, the application of the OVF,rather than a pre-established, nonindividualized vi-bration frequency, is always advisable because it po-tentially produces greater effects on neuromuscularperformance4,19,20 and in less time.19 Recent studiespointed out that vibrating at OVF results in a greaterincrease in explosive strength and flexibility in youngindividuals19,20 and in a greater increase in musclepower output of the lower-limbs in older women4

than vibrating at a fixed frequency of 30 Hz. Fur-thermore, high frequencies of vibration, as well asa prolonged exposure to vibration, could decreasesynchronization of motor units, hence resulting ina negative outcome on neuromuscular perfor-mance29,30 particularly with respect to elevated levelsof mechanical muscle power. This evidence suggeststhat special care must be taken on how the vibrationintervention is administered in terms of frequency.However, the identification of OVF might not alwaysbe feasible. In these cases, it may be useful to havesome frequency ranges of reference to empiricallyset the OVF. To date, the results of existing studiesare rather discordant in their findings relative toOVF reference values. In young individuals, OVFranged from 44 to 55 Hz in some studies,20,31

whereas other authors18 reported maximal muscleactivation at 30 Hz. To the best of the authors’knowledge, there is only one study reporting OVF inolder individuals, in which it has been suggested thatOVF values in this population range from30 to 35Hz,although generalization of these data may be limitedbecause of the small sample size taken into account.4

In addition, no studies have identified the OVF inmiddle-aged individuals. Taken together, the evidencefrom these studies suggests that there may be aninfluence of age onOVF. Nevertheless, this possibilityhas never been specifically addressed. Therefore, thefirst objective of the present study was to compareOVF between young, middle-aged, and older individ-uals, to detect any effect of age on OVF.

It has been suggested that muscles have dif-ferent levels of neuromuscular activation, depend-ing on their distance from the vibrating platform.20,24

However, previous studies have determined OVF

2 Carlucci et al. Am. J. Phys. Med. Rehabil. & Vol. 00, No. 00, Month 2014


mainly in the vastus lateralis (VL)muscle,4,18,19,31 butlower leg and thigh muscles might have differentvalues of OVF. Indeed, recent studies show that theVL and the gastrocnemius muscles are maximallyactivated at different vibration frequencies, approxi-mately 50 and 30 Hz, respectively.20 Thus, it could beargued that the OVF of the VL may not necessarily beoptimal for the gastrocnemiusmuscle. Therefore, thesecond objective of our study was to test the hypo-thesis of whether the WBV-induced neuromuscularactivation is dependent on the muscle group or theproximity to the WBV platform.

METHODS

ParticipantsA total of 78 women volunteered to partici-

pate in the study. The participants were divided intothree groups, young (21.6 T 2.4 yrs), middle aged(43.0 T 5.2 yrs), and older (74.2 T 6.0 yrs). Anthro-pometric characteristics of the participants are re-ported in Table 1. All volunteers were moderatelyactive and followed aerobic exercise programs. Thevolume of training was similar for all subjects: threetimes a week, 60 mins per session, and none of theparticipants had previous experience with vibratorytraining. Subjects were excluded if they had one ormore possible contraindications for a WBV inter-vention such as acute hernia, thrombosis, diabetes,epilepsy, metabolic or neuromuscular diseases, osteo-porosis, osteoarthritis, orthopedic injuries, prosthesis,menstrual irregularity, and cardiovascular diseases.The study was approved by the Local Ethical Com-mittee, and informed written consent was obtainedfrom the subjects before the experimental trials.

Experimental ProtocolEach participant underwent two experimental

sessions carried out in the midmorning and sepa-rated by at least 2 days to avoid any residual effect ofthe previous vibration session. In the first session,the subjects were informed about the study pro-cedures and familiarized with the use of the vibra-tion platform and with the experimental protocol.

On the same occasion, weight, height, and informedwritten consent were obtained. The subjects werealso instructed to maintain their usual dietary ha-bits and to refrain from consuming beverages con-taining caffeine and from training for at least 24 hrsbefore experimental sessions.

In the second experimental session, the par-ticipants arrived at the laboratory 3 hrs after con-suming a standard breakfast and were not allowedto eat or drink anything else during the tests. Op-timal frequency was determined as the frequencycorresponding to maximal RMS during a specificvibration protocol. Each subject underwent the samevibration protocol twice, with a resting period of10 mins between trials.

A vertical synchronous vibrating platform(nemeS Double Vibe, Bosco System; OMP, Rieti,Italy) was used for the vibration protocol. The peak-to-peak displacement of vibration was 2 mm. Thevertical component of acceleration was measuredusing an accelerometer during the incremental test(Type ET-Acc-02, Bosco System Technologies, Rieti)placed in the middle of the vibration platform. Thevibration protocol consisted of the continuous suc-cession, with no pause, of the following vibrationfrequencies: 0 (no vibration), 20, 25, 30, 35, 40, 45,50, and 55 Hz. The increase in frequency occurred insteps of 5 secs, with a total duration of 40 secs ofvibration and 10 secs in the squat position beforeand after the exposure to vibration. The authors re-cently demonstrated this continuous short protocolto yield OVF values similar to more time-consumingprotocols.31 To identify the OVF for each participant,neuromuscular activity (sEMG) was recorded onthe VL, vastus medialis (VM), rectus femoris (R), andgastrocnemius lateralis (GL) muscles of the domi-nant lower-limb, during the execution of the vibra-tion protocol. The vibration frequency at whichmaximal sEMG activation (RMSmax) was recordeddetermined the OVF. During exposure to vibration,the subjects were wearing only socks. They wereasked to maintain a static half-squat position withthe heels down and maintain an angle of 90 degreesat the ankle joint, 120 degrees at the knee joint, and

TABLE 1 Participants’ anthropometric characteristicsa

Young (n = 26) Middle Aged (n = 26) Older (n = 26)

Height, m 1.63 T 0.06 1.66 T 0.06 1.60 T 0.05Body mass, kg 58.3 T 11.6 58.7.8 T 7.5 57.7 T 6.5BMI, kg/m2 22.0 T 4.0 21.8 T 2.3 22.3 T 2.1

BMI, body mass index.aValues are given as mean T standard deviation.



140 degrees at the hip joint. The correct joint an-gle was ascertained using a goniometer. Before start-ing the experimental sessions, the participants wereinstructed to stand as still as possible, limiting thepossible oscillations of the trunk and avoiding vol-untary contraction of the muscles in the lower-limbsduring vibration. Investigators made sure that thisposition was held constant throughout the exposureto vibration. Five minutes of rest, during which thesubjects remained seated inside the laboratory, wereallowed between subsequent vibration interventions.During the exposure to the vibration, the subjectswere asked to report all sensations, both negativeand positive, and were instructed to interrupt the testwhenever discomfort was perceived.

EMG and Data ProcessingA portable eight-channel sEMG device (Model

4020E, Bosco System Lab S.p.A., Rome, Italy) wasused in this study. Firstly, the skin of the subjectswas carefully shaved, exfoliated, and cleaned withalcohol. Then, two self-adhesive silver/silver chlorideelectrodes, with a diameter of 4 mm (Blue SensorAmbu Ag/AgCl, type NF-00-S/12, Milano, Italy), wereplaced longitudinally over the belly of the muscleswith a 20-mm interelectrode distance. The place-ment and location of the electrodes were in accor-dance to recommendations by SENIAM project.32

The sEMG signals were recorded with bipolar elec-trodes including an amplifier (gain, 1000; samplingfrequency, 100 Hz; input impedance, 2 G.; commonmode rejection rate, 100 dB; input noise level [1-kHzband, 20 nV I Hzj2]) and a Butterworth band passfilter (3-dB low cutoff frequency, 8 Hz; 3-dB highcutoff frequency, 1200 Hz). A ground electrode wasfixed on a neutral area, away from the measuringelectrodes. Medical adhesive tape and an elasticband were used to fix the sEMG cables on the skinto minimize any motion artifacts that could be en-countered during the vibration. The preamplifiedsEMG raw signals were converted to mean RMS sig-nals via a built-in hardware circuit network. TheRMS signals were then sampled at 100 Hz. The meanRMS was collected at each vibration frequency andwas reported as a function of time (millivolts persecond). Finally, sEMG parameters were normalizedfor the respective values at maximal voluntary con-tractions (MVCs), assessed with a protocol previ-ously suggested in the literature.24 The MVCs wereperformed isometrically. MVCs of the quadriceps mus-cles were recorded during leg extension. The sub-jects were lying supine on a therapy table with theknees flexed at 120 degrees and hanging off the

table. MVC of the GL muscle was recorded duringplantar flexion of the foot with the ankle joint flexedto 90 degrees.

Statistical AnalysisStatistical analysis was performed using the

Statistical Package for the Social Sciences 19.0 forWindows (SPSS, Chicago, IL). Values are expressedas mean T standard deviation or standard error asspecified. Analysis of variance was used to analyzethe data, with age group as a between-subjects fac-tor and muscle as a within-subjects factor. OVF andRMSmax measured from the VL, VM, R, and GL mus-cles were defined as dependent variables. Multivariateanalysis of variance was used to detect significantdifferences in OVF and maximal activation in thighand calf muscles. Repeated-measures analysis of var-iance (within-between analysis of variance) was per-formed to assess the effect of muscle and age groupon OVF and maximal muscle activation (RMSmax).Data were checked for normality with the Shapiro-Wilk test and sphericity by the Mauchly test, andwhen the sphericity assumption was violated, theGreenhouse-Geisser adjustment was applied. The levelof significance was set at P e 0.05. Post hoc Student’st tests with Bonferroni correction were performedwhere appropriate. The effect size (partialG2) was alsocomputed for all parameters.

The intraclass correlation coefficient of the OVFand sEMG was quantified using reliability analysis inSPSS. A two-way mixed reliability model was chosen(type consistency). The intraclass correlation coeffi-cient values were interpreted as expressed by Cicchettiand Sparrow,33 1981. Intraclass correlation coeffi-cient values range from 0 (not reliable) to 1 (perfectlyreliable). Values from 0.00 to 0.39 were considered low;0.40Y0.59, discrete; 0.60Y0.74, good; and 0.75Y1.00,excellent.

Results of the statistical analysis are reportedin Table 2.

RESULTS

Age-Related DifferencesFigures 1 and 2 show the OVF and RMSmax in

the VL, VM, R, and GL muscles of the three agegroups, respectively. In the older subjects, OVFvalues were lower than in the young and middle-aged participants, for each muscle tested. The olderwomen showed lower OVF values of the VM (F =7.04, P = 0.002, G

2 = 0.16) compared with themiddle-aged (P G 0.01) and young (P G 0.01) groups.OVFs recorded on the VL were also lower (F = 4.37,



P = 0.016, G2 = 0.10) in the older compared with theyoung women (P = 0.012).

RMS during squat without vibration was notsignificantly different between the groups and in allmuscles considered (Table 3). RMSmax at OVF washigher in the older compared with the young andmiddle-aged women. Significant differences (P G

0.05) in muscle activity, between the older and theyoung group, were found in all muscles tested (VL,F = 4.40, G2 = 0.10; VM, F = 4.01, G2 = 0.10; R, F =4.12, G2 = 0.10; GL, F = 3.93, G2 = 0.09). RMSmax

in the VL, VM, and R muscles were 24%, 21%, and19% higher in the older than the young women,respectively. In the GL muscle, RMSmax was 17%higher in the older women than in the middle-agedwomen (P = 0.05). The same parameter was higherin the older compared with the young women, but itdid not reach statistical significance (P = 0.056).

Muscle-Related DifferencesThere were no significant muscle-related dif-

ferences in OVF values between the four musclesconsidered in each group (Fig. 1). On average,the OVF in muscles of the young women was 35.2 T7.6 Hz; in the middle-aged women, 33.7 T 6.0; andin the older women, 31.0 T 5.3 Hz.

The four muscles tested showed significantlydifferent RMSmax values (P G 0.01) in the young

(F = 16.52, G2 = 0.04), middle-aged (F = 27.94, G2 =0.053), and older women (F = 9.74, G2 = 0.28). In thegroup of young women, significantly lower percent-ages of muscular activation were recorded for theGL compared with the VL (P G 0.01), VM (P G 0.01),and R (P G 0.01) muscles. The same pattern wasevident in the group of middle-aged individuals, inwhich the GL muscle showed a significantly loweractivation in comparison with its three tested coun-terparts (P G 0.001). As for the older women, RMSmax

of the GL was significantly lower compared with theVL (P G 0.05) and R (P G 0.01) muscles.

DISCUSSIONTo the best of the authors’ knowledge, for the

first time, OVF was compared between young, middle-aged, and older women in four muscles of the lower-limb. The major finding was that OVF was lower inthe older women than in the middle-aged and youngwomen in the VL and VM muscles. There were nodifferences in OVF between muscles within eachgroup. RMSmax was higher in the older than theyoung women in all muscles.

To date, little is known about the mechanismsaccounting for the lower OVF in the older with re-spect to the young women. However, some clinicalevidence has shown that aging may be responsiblefor a selective reduction in the number of muscle

TABLE 2 Intraclass correlation coefficient

VL VM R GL

OVF Young 0.97 0.94 0.90 0.96Middle aged 0.95 0.97 0.84 0.63

Older 0.74 0.82 0.91 0.95RMSmax Young 0.87 0.93 0.96 0.79

Middle aged 0.82 0.93 0.85 0.77Older 0.90 0.93 0.90 0.85

FIGURE 1 Effect of age on OVF. Mean T SE OVF values, recorded in the VL, VM, R, and GL muscles of the young,middle-aged, and older individuals. *P G 0.05.



spindles, Ia afferent fibers, and muscle fibers.25,26

These alterations might lead to a change in vibra-tory sensitivity that could explain the differencesin the recorded values of OVF. The maximal sEMGresponse during exposure to incremental frequen-cies might have been altered from a change in thebalance between the excitatory stimuli coming fromIa afferents or skin receptors and the inhibitory stim-uli from Golgi tendon organ,20 as postulated by thetheoretical model proposed by Cardinale and Bosco.9

The older population of the present studyshowed greater levels of neuromuscular activity atOVF in the lower extremities than did the young ormiddle-aged populations. Apparently, the present re-sult has not been reported in previous studies. Be-cause of the novel nature of this result, the authorscan only speculate about the practical relevance ofit. It is known that a high EMG activity results froma high number of recruited muscle fibers and highmotor unit discharge frequencies.3 This may meanthat older women benefit the most from trainingat the OVF compared with younger women. Furtherresearch is necessary to confirm this finding andelucidate underlying mechanisms. As a practical ap-plication, the older women may benefit the mostfrom an individualized approach when designing avibration training, aiming at an optimal exposureto vibration. Indeed, this specific frequency has beensuggested to increase neuromuscular facilitationand improve neuromuscular performance.4 It is

interesting to note that, although there were differ-ences inmuscle activation between young andmiddle-aged individuals, maximal activation was reachedat similar frequencies, thus similar OVFs. As for theyoung participants tested in the present study, theOVF corresponding to the maximal activation ofthe VL was 35 Hz, which is in contrast with previousstudies.18,34,35 In a number of studies, a frequencyof 30 Hz during WBV resulted in a greater VL mus-cle activation as compared with higher or lowerfrequencies.18,34,35 In other studies using the sameprotocol as in the present study, OVF ranged from44 to 55 Hz.20,31 Different factors such as age, train-ing status, muscle fiber type, and Ia afferent sensitivityhave been suggested as important in determiningthe pattern of neuromuscular activation at a partic-ular frequency of vibration.25Y28 These factors maypotentially contribute to the variability of the resultsof this study, but the exact underlying mechanismsare still to be fully understood. For the GL muscle,the data of this study show a mean maximal activa-tion at 32 Hz, which is in line with the results ofanother study in which frequencies of vibration be-tween 25 and 35 Hz resulted inmaximal activation ofthis muscle.20 A muscle tuning mechanism has beensuggested as a possible reason for the highest sEMGmuscle response at these frequencies, which are closeto the resonance frequency for the GL muscle.36

The results of this study suggest that a fre-quency between 33 and 36 Hz could be optimal in

TABLE 3 Levels of muscle activity recorded during squatting without WBV

%RMS0Hz Young (n = 26) Middle Aged (n = 26) Older (n = 26)

VL 23.9 T15.0 27.3 T 15.2 26.6 T 17.6VM 25.7 T 14.9 27.7 T 12.9 25.8 T 19.1R 20.7 T 11.7 24.7 T 11.7 23.5 T 17.2GL 4.6 T 3.0 4.9 T 4.1 7.5 T 4.1

RMS values are represented as a percentage of MVC expressed as mean T standard deviation.

FIGURE 2 Muscle activation at OVF. Maximal muscle activity, expressed as a percentage of the muscle activityduring an MVC (RMSmax). Data are expressed as mean T SE. *P G0.05.



middle-aged adults who undergo WBV. So far, nostudy known to the authors determined the OVFin this age group; thus, comparison of this study’sdata is difficult. In the older women, OVF for the VLmuscle ranged between 30 and 35 Hz. Even thoughthe older women in this study were probably fitterthan the general population, which may not allowfor generalization of this result, OVF values deter-mined for them are similar to those previously re-ported in the literature for this age group.4

Special care must be taken on how the inter-vention is administered in terms of vibration fre-quencies because some people are more sensitivethan others to a given vibration frequency, and thefrequency inducing the greatest sEMG responsesin an individual might not necessarily yield thesame response in another person.19 For this reason,it would be advisable to plan a preliminary vibra-tion session for every person, to identify the OVF.The protocol used in this study could be useful inthe determination of the OVF because it is short,lasting only 50 secs, and it shows high reproduc-ibility (Table 2). Although the VL muscle would beusually preferred,4,18,20,31 the test for the identifi-cation of the OVF could be applied equally to the VM,R, or GL muscles. In those cases when it is not pos-sible to identify the OVF, the vibration frequency ofa training program may be empirically set using thedata of this study as reference values, that is, 35 Hzfor the young or the middle aged and 30 Hz forthe older.

In conclusion, the present study shows that theOVF decreases with age independent of the mus-cle tested. Therefore, determining OVF would be ad-visable before starting a vibration training programwhen dealing with different age groups. OVF may beset at 35 Hz for the young and middle-aged womenand at 30 Hz for the older. However, because fewstudies have used the OVF to set the vibration exer-cise, future longitudinal studies should be performedto evaluate this potential effect of WBV, especiallywith regard to the comparison between young andolder individuals.

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Older Age Is Associated with Lower Optimal Vibration Frequency in Lower-Limb Muscles During...

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