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Acute effects of whole-body vibration training on neuromuscular performance and mobility in hypoxia and normoxia in persons with multiple sclerosis: A crossover study

Published:October 18, 2019DOI:https://doi.org/10.1016/j.msard.2019.101454

      Highlights

      • There are no differences on neuromuscular variables, except EMG, after a WBVT session in both conditions.
      • A WBVT session does not acutely worsen functional variables.
      • EMG decreases after WBV session in hypoxia, which could show a greater stimulus in this condition.

      Abstract

      Background

      Whole-body vibration training (WBVT) has been used in people with relapsing-remitting multiple sclerosis (pwMS), showing improvements in different neuromuscular and mobility variables. However, the acute effects of this training are still unknown. The acute effects of WBVT on neuromuscular performance, mobility and rating of perceived exertion (RPE) were evaluated in 10 pwMS.

      Methods

      Maximal voluntary isometric contraction (MVIC), central activation ratio (CAR), electromyography (EMG) of the vastus lateralis during isometric knee extension, Timed Up and Go Test (TUG), walking speed and RPE were assessed before and immediately after a session of WBVT (twelve 60-s bout of vibration; frequency 35 Hz; amplitude 4 mm; 1-min rest intervals) in both hypoxic and normoxic conditions.

      Results

      EMG 0–100, 0–200 ms and peak EMG resulted in significant differences (p < 0.05) between normoxic and hypoxic sessions. The EMG activity tended to decrease in all phases after the hypoxic session, indicating possible influence of hypoxia on neuromuscular performance. No changes were found in CAR, MVIC, TUG and walking speed in both conditions.

      Conclusion

      Based on our results, as well as those obtained by other studies that have used WBVT with other populations, more studies with a higher sample and lower dose of vibration exposure should be conducted in pwMS.

      Keywords

      1. Introduction

      Numerous studies have examined the effects of resistance training in persons with MS (pwMS) to help alleviate the symptomology of multiple sclerosis (
      • White L.J.
      • Dressendorfer R.H.
      Exercise and multiple sclerosis.
      ;
      • White L.J.
      • McCoy S.C.
      • Castellano V.
      • Gutierrez G.
      • Stevens J.E.
      • Walter G.A.
      • Vandenborne K.
      Resistance training improves strength and functional capacity in persons with multiple sclerosis.
      ) and improve muscle strength (
      • Dodd K.J.
      • Taylor N.F.
      • Shields N.
      • Prasad D.
      • McDonald E.
      • Gillon A.
      Progressive resistance training did not improve walking but can improve muscle performance, quality of life and fatigue in adults with multiple sclerosis: a randomized controlled trial.
      ;
      • Filipi M.L.
      • Kucera D.L.
      • Filipi E.O.
      • Ridpath A.C.
      • Leuschen M.P.
      Improvement in strength following resistance training in ms patients despite varied disability levels.
      ;
      • White L.J.
      • Dressendorfer R.H.
      Exercise and multiple sclerosis.
      ;
      • White L.J.
      • McCoy S.C.
      • Castellano V.
      • Gutierrez G.
      • Stevens J.E.
      • Walter G.A.
      • Vandenborne K.
      Resistance training improves strength and functional capacity in persons with multiple sclerosis.
      ) and physical function (
      • Dodd K.J.
      • Taylor N.F.
      • Shields N.
      • Prasad D.
      • McDonald E.
      • Gillon A.
      Progressive resistance training did not improve walking but can improve muscle performance, quality of life and fatigue in adults with multiple sclerosis: a randomized controlled trial.
      ;
      • White L.J.
      • Dressendorfer R.H.
      Exercise and multiple sclerosis.
      ;
      • White L.J.
      • McCoy S.C.
      • Castellano V.
      • Gutierrez G.
      • Stevens J.E.
      • Walter G.A.
      • Vandenborne K.
      Resistance training improves strength and functional capacity in persons with multiple sclerosis.
      ). However, whole-body vibration training (WBVT) may be an alternative approach in obtaining physiological benefits (
      • Bautmans I.
      • Van Hees E.
      • Lemper J.C.
      • Mets T.
      The feasibility of whole body vibration in institutionalised elderly persons and its influence on muscle performance, balance and mobility: a randomised controlled trial [ISRCTN62535013].
      ;
      • Cochrane D.J.
      • Stannard S.R.
      • Sargeant A.J.
      • Rittweger J.
      The rate of muscle temperature increase during acute whole-body vibration exercise.
      ) while minimizing symptomatic fatigue. WBVT causes rapid muscle contraction and relaxation due to the mechanical multidimensional oscillations of the vibratory platform (
      • Lohman E.B.
      • Petrofsky J.S.
      • Maloney-Hinds C.
      • Betts-Schwab H.
      • Thorpe D.
      The effect of whole body vibration on lower extremity skin blood flow in normal subjects.
      ). This vibratory stimulus is effective in modulating the Ia-afferent motoneuron synaptic transmission via presynaptic inhibition (
      • Hong J.
      • Kipp K.
      • Johnson S.T.
      • Hoffman M.A.
      Effects of 4 weeks whole body vibration on electromechanical delay, rate of force development, and presynaptic inhibition.
      ). Previous studies have shown that mechanical vibrations stimulate the muscle-tendon complex and induce the tonic vibration reflex that increases α-motor neuron activation, thereby enhancing force production in healthy people (
      • Cardinale M.
      • Bosco C.
      The use of vibration as an exercise intervention.
      ;
      • Cochrane D.J.
      • Stannard S.R.
      • Firth E.C.
      • Rittweger J.
      Acute whole-body vibration elicits post-activation potentiation.
      ).
      Benefits of short and long-term WBVT in pwMS have shown improvement in muscle strength, functional capacity, resistance, coordination and balance (
      • Castillo-Bueno I.
      • Ramos-Campo D.J.
      • Rubio-Arias J.A.
      Effects of whole-body vibration training in patients with multiple sclerosis: a systematic review.
      ;
      • Kang H.
      • Lu J.
      • Xu G.
      The effects of whole body vibration on muscle strength and functional mobility in persons with multiple sclerosis: a systematic review and meta-analysis.
      ), as well as overall physical function (
      • Hilgers C.
      • Mündermann A.
      • Riehle H.
      • Dettmers C.
      Effects of whole-body vibration training on physical function in patients with multiple sclerosis.
      ). In addition, lower ratings of perceived exertion (RPE) during and after a WBVT session compared to other types of resistance training of similar intensities were observed (
      • Perchthaler D.
      • Grau S.
      • Hein T.
      Evaluation of a six-week whole-body vibration intervention on neuromuscular performance in older adults.
      ). Thus, the observed low RPE in WBVT may be ideal for pwMS, whose main limitation when exercising is symptomatic fatigue (
      • Amatya B.
      • Khan F.
      • Galea M.
      Rehabilitation for people with multiple sclerosis: an overview of Cochrane reviews.
      ). However, acute effects of WBVT on neuromuscular performance remain unclear in the MS population.
      Another alternative to enhance strength using lower intensity levels is exercising under hypoxic conditions. Hypoxia training has shown chronic improvements in strength and muscle size (
      • Ramos-Campo D.J.
      • Martínez-Guardado I.
      • Olcina G.
      • et al.
      Effect of high-intensity resistance circuit-based training in hypoxia on aerobic performance and repeat sprint ability.
      a), as well as aerobic and anaerobic capacity (
      • Ramos-Campo D.J.
      • Scott B.R.
      • Alcaraz P.E.
      • Rubio-Arias J.A.
      The efficacy of resistance training in hypoxia to enhance strength and muscle growth: a systematic review and meta-analysis.
      b).
      • Scott B.R.
      • Slattery K.M.
      • Sculley D.V.
      • Lockhart C.
      • Dascombe B.J.
      Acute physiological responses to moderate-load resistance exercise in hypoxia.
      found higher muscle activation during a moderate-load resistance exercise under hypoxic compared to normoxic conditions in young adults, suggesting improvements in neuromuscular performance with hypoxia. Training in hypoxia has shown to improve physical function, such as the Timed Up and Go Test (TUG), walking speed and dynamic balance in patients with incomplete spinal cord injury (
      • Navarrete-Opazo A.
      • Alcayaga J.J.
      • Sepúlveda O.
      • Varas G.
      Intermittent hypoxia and locomotor training enhances dynamic but not standing balance in patients with incomplete spinal cord injury.
      ).
      • Girard O.
      • Malatesta D.
      • Millet G.P.
      Walking in hypoxia: an efficient treatment to lessen mechanical constraints and improve health in obese individuals?.
      affirmed that the hypoxic condition, by itself, can be used as a tool to increase the training load, which may be advantageous for pwMS (i.e., working at lower intensities in hypoxia). However, no studies have analyzed the hypoxic effects with WBVT. Additionally, no studies have used hypoxia in pwMS during resistance training or WBVT. Thus, understanding the acute effects of WBVT under normoxic and hypoxic condition on neuromuscular function in pwMS may be useful in better ameliorating the symptomology of MS.
      Therefore, to our knowledge, little is known regarding the acute physiological benefits, particularly central and peripheral neural activation of the muscle, following a single session of WBVT in pwMS. Moreover, the effects of hypoxia during an exercise session of WBVT on neuromuscular performance in general, as well as pwMS, has not been investigated.
      The main objectives were to: (1) examine the acute effect of WBVT on neuromuscular performance in pwMS and (2) compare these effects between normoxia and hypoxia. We hypothesized that (1) WBVT would decrease maximal voluntary contraction, central activation ratio, walking speed and TUG in pwMS and (2) WBVT in hypoxia would further diminish the aforementioned variables due to the greater stimulus on the neuromuscular component.

      2. Methods

      2.1 Design

      All training and testing sessions were completed in the UCAM Research Center for High Performance Sports (Murcia, Spain). The present study used a cross-over design with blocked randomization (i.e., subjects signed to either a WBVT session under normoxic (WVBTnorm; FiO2 = 20,9%) or hypoxic (WBVThyp; FiO2 = 15%) condition. In visit 1, subjects were familiarized with all testing procedures and the different vibration frequency and amplitudes used for the training session. Subjects returned one week later for visit 2 at the same time of day to perform the first session of WBVT either in normoxia or hypoxia. Visit 3 occurred after one week of rest where participants repeated the same WBVT protocol with a second baseline assessment but under the condition that was not performed previously. For the hypoxia visit, a normobaric chamber (CAT 430, Colorado Altitude Training, USA) with reduced oxygen content to 15% via a generator (CAT-12, Colorado Altitude Training, USA) was used. The trial design followed Consort guidelines for randomized clinical trials. The trial was approved by the Catholic University of Murcia's Science Ethics Committee and was in accordance with the Declaration of Helsinki. This study was registered in ClinicalTrials.gov (identifier: NCT03856801: available from website).

      2.2 Participants

      Thirteen pwMS (male: 39%, age: 42,3 ± 9,6years, height: 164,2 ± 8,5 cm, body mass: 67,3 ± 12,7 kg, body mass index: 29,6 ± 5,6 kg.m−2) were recruited from the local MS association. Participants were diagnosed with relapsing-remitting MS, not using any assistive devices, and not involved in any resistance or endurance training programs. All participants were previously diagnosed with MS by a board-certified neurologist according to the McDonald criteria (
      • Thompson A.J.
      • Banwell B.L.
      • Barkhof F.
      • et al.
      Diagnosis of multiple sclerosis: 2017 revisions of the McDonald criteria.
      ). Participants were included if he/she: (1) had mild or moderate disability with clinical mild spastic-ataxic gait disorder, and (2) was in the stable phase of the disease. The exclusion criteria were: (1) Expanded Disability Status Scale (EDSS) <6, (2) relapse within the preceding 12 months, (3) corticosteroid treatment within the last 2 months before inclusion, and (4) involved in a training program in the prior two months. All participants provided a written and signed informed consent before starting the study.

      2.3 Training procedure

      WBVT was performed on the Power Plate Pro5 (Power Plate International, London, UK) in a static squat position (30° knee flexion) (
      • Hilgers C.
      • Mündermann A.
      • Riehle H.
      • Dettmers C.
      Effects of whole-body vibration training on physical function in patients with multiple sclerosis.
      ). Vibration frequency was set at 35 Hz with a 4 mm peak-to-peak amplitude (
      • Castillo-Bueno I.
      • Ramos-Campo D.J.
      • Rubio-Arias J.A.
      Effects of whole-body vibration training in patients with multiple sclerosis: a systematic review.
      ). All participants held on to the rail of the vibration unit for safety. The training session consisted of 12 sets of 1 min static squat with 1 min rest between sets. During the resting period, participants stood upright on the platform.

      2.4 Testing procedures

      Participants performed the testing measurements before and after WVBTnorm and WBVThyp training sessions. A standardized warm-up of 5 min on a cycle ergometer at 75 W and a dynamic stretching routine were performed. The order of the tests was the same for both conditions and each assessment was conducted by the same investigator. The primary outcomes of neuromuscular performance were MVIC, Time-to-MVIC, CAR and EMG amplitudes at time ranges of 0–30 ms, 0–50 ms, 0–100 ms and 0–200 ms, EMGpeak and Time-to-EMGpeak. The secondary outcomes were RPE, TUG and walking speed.

      2.4.1 Neuromuscular testing: MVIC, CAR and surface EMG

      Participants sat upright on an isokinetic dynamometer chair (Biodex Medical System, NY) with both right and left legs flexed at 90° and the ankle strapped directly to a customized apparatus that contained a load cell (Model SML500, Interface Scottsdale, AZ, USA). Participants performed 3 MVICs, each lasting for 5 s with 3 min of rest between contractions. To ensure maximal effort, participants were encouraged verbally and at least 2 MVICs had to be within 10% of one another. The highest trial was used for MVIC.
      Then, two bipolar 10 × 15 cm stimulating electrodes were placed over the proximal and distal portions of the quadriceps of the right leg and secured with a Velcro wrap. Signal 6.0 software (CED, Cambridge, England) was used to control the stimulating characteristics: 100 Hz, 50 pulses, length 0.009 s and interval 0.01 s. The intensity of the stimulus was set at 40–50% of MVIC. The electrical stimulator (Digitimer DS7A, England; 400 Vmax, 2000 ms) and the EMG receiver were synchronized using a CED Micro3 1401 Data Acquisition Unit (Cambridge, England).
      Afterwards, EMG electrodes (Ambu Blue Sensor SP, Ambu A/S, Denmark) were placed over the vastus lateralis following SENIAM Guidelines (

      Hermens, H.J., Rau, G., Disselhorst-Klug, C., Freriks, B., 1998. Surface electromyography application areas and parameters (SENIAM 3). Standards for Surface Electromyography: The European Project (SENIAM)108–112.

      ). Then, wireless DTS EMG sensors (2.4 × 3.4 × 1.4 cm; Noraxon EMG TeleMyo DTS Desk receiver, Scottsdale, AZ, USA) were connected to the EMG electrodes and taped to the skin. Noraxon MR 3.6.20 software (Noraxon, Scottsdale, AZ, USA) was used to record force and EMG activity simultaneously. Participants performed an MVIC with a superimposed 100 Hz train when maximal force was steady. This sequence was repeated 2 times. Peak MVIC and, peak force obtained by superimposed stimulation were determined. The CAR was calculated as follows: (
      • Kent-Braun J.A.
      Central and peripheral contributions to muscle fatigue in humans during sustained maximal effort.
      ).
      CAR=MVICMVIC+superimposedtrain·100


      A decrement in CAR was associated with central fatigue mechanisms (
      • Kent-Braun J.A.
      Central and peripheral contributions to muscle fatigue in humans during sustained maximal effort.
      ).

      2.4.2 TUG

      TUG was performed before and after both WBVThyp and WBVTnorm sessions to assess functional mobility. When indicated, participants stood up from a seated position, walked three meters, turned around, walked back, and sat down again as quickly as possible (
      • Podsiadlo D.
      • Richardson S.
      The timed “up and go”: a test of basic functional mobility for frail elderly persons.
      ). The same armchair and footwear were used for all tests. The fastest time of two trials was used for analysis.

      2.4.3 Walking speed

      Participants walked 10 m, marked with taped lines, as quickly as possible without running twice with 1 min of rest between each trial. Verbal encouragement was given to the participants. Walking time was recorded between 6 and 10 m with two photocells (Witty, Microgate, Italy) (
      • Estes S.
      • Iddings J.A.
      • Ray S.
      • Kirk-Sanchez N.J.
      • Field-Fote E.C.
      Comparison of single-session dose response effects of whole body vibration on spasticity and walking speed in persons with spinal cord injury.
      ), and walking speed was calculated. The fastest walking speed was used for analysis.

      2.4.4 Variables measured during the session

      Participants were instructed and familiarized on how to use the RPE scale in Visit 1. RPE was assessed before, during (after sets 4 and 8) and after the training session using the Borg Scale (
      • Borg G.A.
      Psychophysical bases of perceived exertion.
      ). Participants were asked “How was your workout?” and were presented with the scale. Arterial oxygen saturation was measured before, after set 6 and immediately after the training session using a finger pulseoximetry (Onyx-Nonin Medical Inc, Model 9500 Finger Pulse Oximeter, USA).

      2.5 Statistical analyses

      Data collection, treatment, and analysis were performed using the SPSS for Windows statistical package (version 20.0; SPSS, Inc., Chicago, IL, USA). Descriptive statistics (mean and SD) were calculated. Before using parametric tests, the assumption of normality and homoscedasticity was confirmed with the Shapiro-Wilks test. Student's t-test for pair samples was used to test if significant changes occurred in differences between pre and post training for each group separately. Analysis of covariance (ANCOVA) was performed with the EDSS score as a covariate to evaluate the differences between hypoxia and normoxia sessions. For all procedures, a level of p ≤ 0.05 was set to indicate statistical significance.

      3. Results

      Although 13 pwMS volunteered to participate in this clinical trial, 3 participants dropped out of the study for different reasons (injury outside of the study intervention and schedule incompatibility). Thus, a total of 10 pwMS completed the study, including all testing assessments (Fig. 1).
      Fig. 1
      Fig. 1Flow diagram of the progress of the crossover study.
      All participants had an Expanded Disability Status Scale between 1 and 6 (EDSS: 2.55 ± 1.30). Table 1 shows the participant characteristics.
      Table 1Participant characteristics.
      CharacteristicsMean ± SD (n = 10)
      General characteristics
      Age (yrs)44.4 ± 7.7
      Sex (men:women)3:7
      EDSS2.5 ± 1.3
      Weight (kg)65.2 ± 11.1
      Height (cm)164.3 ± 8.9
      Lean mass (kg)44.7 ± 7.7
      Fat mass (kg)18.0 ± 8.2
      BMI (kg.m−2)24.1 ± 4.0
      EDSS = expanded disability status scale; BMI = body mass index.
      Baseline measures of neuromuscular and mobility variables are shown in Table 2. During the hypoxic and normoxic sessions, patients showed an oxygen saturation of 92.51 ± 0.52% and 98.10 ± 1.13%, respectively.
      Table 2Baseline measures of variables.
      DescriptiveMean ± SD
      ConditionHypoxiaNormoxia
      CAR (%)91.50 ± 3.3090.00 ± 4.88
      MVIC_Right (N.m)342.00 ± 120.00345.00 ± 92.30
      MVIC_Left (N.m)306.00 ± 107.00327.00 ± 105.00
      Time-To-MVIC_Right (s)2.36 ± 0.992.59 ± 0.70
      Time-To-MVIC_Left (s)1.63 ± 0.912.43 ± 1.09
      EMG_0-30 (µV)131.00 ± 84.20168.00 ± 153.00
      EMG_0-50 (µV)131.00 ± 88.00167.00 ± 153.00
      EMG_0-100 (µV)131.00 ± 95.30174.00 ± 164.00
      EMG_0-200 (µV)126.00 ± 85.30179.00 ± 175.00
      EMG_Peak (µV)211.00 ± 205.00325.00 ± 369.00
      EMG_Time-To-Peak (s)2.39 ± 1.472.34 ± 1.13
      Walking speed (m.s−1)1.67 ± 0.641.74 ± 0.60
      RPE8.40 ± 2.959.20 ± 2.30
      TUG (s)8.15 ± 3.178.20 ± 3.58
      Saturation Hb (%)92.50 ± 0.5898.17 ± 1.17
      CAR = central activation ratio; MVIC = maximal voluntary isometric contraction; EMG = surface electromyography; RPE = rate of perceived exertion; TUG = timed up and go test.
      No significant pre-post differences were found in CAR in WBVTnorm (t = 0.361, p = 0.727) or WBVThyp (t = −0.77, p = 0.464). No significant differences were shown between conditions (F = 0.584, p = 0.457). There were no significant pre-post differences in MVIC in the right leg in normoxia (t = −0.557, p = 0.591) and hypoxia (t = −0.461, p = 0.656) nor in the left leg (t = 0.511, p = 0.621; t = −0.033, p = 0.974), respectively. No significant differences were found between conditions in right and left legs (F = 0.151, p = 0.702; F = 0.008, p = 0.930). EMG 0-30 and 0-50 V tended to decrease in WBVThyp. See Tables 3 and 4.
      Table 3Comparison of pre-post effect on primary outcomes.
      95% CI for Cohen's d
      Primary OutcomesPre (Mean ± SD)Post (Mean ± SD)Δ ± ΔSDtpEffect SizeLowerUpper
      CAR (%)
      Hyp91.46 ± 3.2992.54 ± 4.180.01 ± 0.04−0.770.464−0.257−0.9140.416
      Norm90.04 ± 4.8889.09 ± 8.26−0.01 ± 0.090.360.7270.120−0.5390.773
      MVIC_Right (Nm)
      Hyp341.50 ± 120.26349.10 ± 99.760.04 ± 0.14−0.4610.656−0.146−0.7650.482
      Norm345.40 ± 92.30350.70 ± 84.290.02 ± 0.08−0.5570.591−0.176−0.7960.453
      MVIC_Left (Nm)
      Hyp305.70 ± 106.80306.00 ± 115.20−0.01 ± 0.10−0.0330.974−0.011−0.6300.610
      Norm327.20 ± 104.65322.30 ± 95.90−0.01 ± 0.090.5110.6210.162−0.4670.781
      TimeToMVIC Right (s)
      Hyp2.35 ± 0.992.25 ± 0.900.05 ± 0.450.3260.7520.103−0.5210.722
      Norm2.59 ± 0.702.50 ± 1.03−0.03 ± 0.300.3560.7300.113−0.5120.732
      TimeToMVIC Left (s)
      Hyp1.63 ± 0.922.19 ± 0.730.83 ± 1.36−1.3400.213−0.424−1.0620.236
      Norm2.42 ± 1.092.24 ± 0.900.03 ± 0.370.6430.5360.203−0.4290.825
      EMG_030 (µV)
      Hyp131.30 ± 84.22110.20 ± 74.14−0.17 ± 0.182.0870.0670.660−0.0431.334
      Norm167.90 ± 153.40197.30 ± 190.500.12 ± 0.41−1.6410.135−0.519−1.1700.157
      EMG_050 (µV)
      Hyp131.00 ± 88.04110.60 ± 73.60−0.15 ± 0.181.9390.0840.613−0.0801.279
      Norm167.40 ± 153.30198.60 ± 194.700.12 ± 0.37−1.6980.124−0.5371.1910.142
      EMG_0100 (µV)
      Hyp130.60 ± 95.32110.90 ± 71.92−0.13 ± 0.171.6170.1400.511−0.1631.161
      Norm173.70 ± 164.10201.30 ± 199.000.12 ± 0.28−1.5590.153−0.493−1.1400.178
      EMG_0200 (µV)
      Hyp125.50 ± 85.35113.90 ± 73.39−0.90 ± 0.141.3460.2110.426−0.2341.064
      Norm179.20 ± 174.40194.00 ± 175.300.15 ± 0.26−1.6540.132−0.523−1.1750.153
      EMG_Peak (µV)
      Hyp210.90 ± 205.30193.20 ± 175.90−0.07 ± 0.121.6180.1400.512−0.1631.162
      Norm324.80 ± 369.50387.00 ± 474.800.13 ± 0.21−1.6820.127−0.532−1.1850.146
      EMG_TimeToPeak (s)
      Hyp2.38 ± 1.471.21 ± 1.47−0.15 ± 1.451.6850.1260.533−0.1451.186
      Norm2.33 ± 1.312.73 ± 1.500.24 ± 0.69−1.1810.268−0.373−1.0070.279
      Note: CAR = central activation ratio; MVIC = maximal voluntary isometric contraction; EMG = surface electromyography; Hyp = hypoxia; Norm = normoxia.
      Table 4Comparison of pre-post effect on secondary outcomes.
      95% CI for Cohen's d
      Secondary outcomesPre (mean ± SD)Post (mean ± SD)Δ ± ΔSDtpEffect SizeLowerUpper
      TUG (s)
      Hyp8.15 ± 3.178.05 ± 3.42−0.02 ± 0.041.0640.3150.337−0.3110.966
      Norm8.20 ± 3.588.10 ± 3.70−0.02 ± 0.050.7370.4800.233−0.4020.856
      Walking speed (m/s)
      Hyp1.67 ± 0.641.63 ± 0.69−0.04 ± 0.091.3070.2230.413−0.2451.051
      Norm1.74 ± 0.601.75 ± 0.66−0.01 ± 0.09−0.1070.917−0.034−0.6530.587
      RPE_Pre-4
      Hyp8.40 ± 2.959.60 ± 2.170.20 ± 0.23−2.7140.024
      = Significant changes p ≤ 0.05.
      −0.858−1.574−0.109
      Norm9.20 ± 2.3010.70 ± 1.890.20 ± 0.210−3.1430.012
      = Significant changes p ≤ 0.05.
      0.994−1.774−0.209
      RPE_Pre-8
      Hyp8.40 ± 2.9510.20 ± 2.100.28 ± 0.29−3.2500.01
      = Significant changes p ≤ 0.05.
      −1.028−1.787−0.234
      Norm9.20 ± 2.3010.60 ± 1.900.20 ± 0.26−2.2640.05
      = Significant changes p ≤ 0.05.
      −0.716−1.401−0.576
      RPE_Pre-Post
      Hyp8.40 ± 2.9510.70 ± 2.260.34 ± 0.32−3.5350.006
      = Significant changes p ≤ 0.05.
      −1.118−1.902−0.298
      Norm9.20 ± 2.3011.80 ± 2.300.35 ± 0.39−3.2840.009
      = Significant changes p ≤ 0.05.
      −1.039−1.800−0.242
      Note: TUG = Timed Up and Go Test; RPE = Rating of Perceived Exertion; Hyp = Hypoxia; Norm = Normoxia.
      low asterisk = Significant changes p ≤ 0.05.
      A significant increase in EMG 0-100, EMG 0-200 and EMG Peak (F = 5.33, p = 0.034; F = 6.049, p = 0.025; F = 6–652, p = 0.02) were observed in normoxia compared to hypoxia. Table 5 shows the comparison between conditions and EDSS effect for each primary outcome variable.
      Table 5Comparison between hypoxia and normoxia and EDSS effect on primary outcomes.
      Primary outcomesANCOVA interactions (F, p, ES η²)
      Conditioning EffectEDSS Effect
      FpES η²FpES η²
      CAR
      Hyp-Norm0.5840.4570.0341.3960.2560.082
      MVIC_Right
      Hyp-Norm0.1510.7020.0090.0390.8450.002
      MVIC_Left
      Hyp-Norm0.0080.9300.0000.8700.3640.049
      Time-To-MVIC_Right
      Hyp-Norm0.1830.6740.0100.4660.5040.026
      Time-To-MVIC_Left
      Hyp-Norm3.8500.0660.1691.9200.1840.084
      EMG_0-30
      Hyp-Norm3.5970.0750.1700.5790.4570.027
      EMG_0-50
      Hyp-Norm3.7280.0700.1740.7520.3980.035
      EMG_0-100
      Hyp-Norm5.3300.034
      p < 0.05 differences between hypoxia and normoxia condition.
      0.2241.5000.2370.063
      EMG_0-200
      Hyp-Norm6.0490.025
      p < 0.05 differences between hypoxia and normoxia condition.
      0.2520.9660.3390.040
      EMG_Peak
      Hyp-Norm6.6520.02
      p < 0.05 differences between hypoxia and normoxia condition.
      0.2770.3770.5470.016
      EMG_Time-To-Peak
      Hyp-Norm0.4080.5310.0193.7640.0690.178
      Note: CAR = central activation ratio; MVIC = maximal voluntary isometric contraction; EMG = surface electromyography; Hyp = hypoxia; Norm = Normoxia; EDSS = expanded disability status scale.
      low asterisk p < 0.05 differences between hypoxia and normoxia condition.
      No pre-post differences were found in TUG and walking speed after WBVTnorm (t = 0.737, p = 0.48; t=−0.107, p = 0.917) and WBVThyp (t = 1.064, p = 0.315; and t = 1.307, p = 0.223), respectively. No differences were found between conditions in TUG (f = 0.123, p = 0.730) and walking speed (F = 0.583, p = 0.456). An increase in RPE was found in both WBVThyp and WBVTnorm (p = 0.006 and p = 0.009, respectively). Table 6 shows the comparison between conditions and the EDSS effect on secondary outcome variables.
      Table 6Comparison between hypoxia and normoxia and EDSS effect on secondary outcomes.
      Secondary OutcomesANCOVA interactions (F, p, ES η²)
      Conditioning EffectEDSS Effect
      FpES η²FpES η²
      TUG
      Hyp-Norm0.1230.7300.0070.2810.6030.016
      Walking speed (m/s)
      Hyp-Norm0.5830.4560.0330.0970.7600.005
      RPE_Pre-4
      Hyp-Norm0.0010.9730.0000.0760.7870.004
      RPE_Pre-8
      Hyp-Norm0.4910.4930.0270.5690.4610.031
      RPE_Pre-Post
      Hyp-Norm0.0010.9730.0000.3420.5660.020
      Note: TUG = timed up and go test; RPE = rate of perceived exertion; Hyp = hypoxia; Norm = normoxia; EDSS = expanded disability status scale.

      4. Discussion

      The main finding of the current study was that acute WBVT exposure (12 sets, 1-min of rest, 35 Hz, 3 mm, squat position) did not produce changes in neuromuscular performance and mobility in pwMS, except for in EMG activity where significant differences were observed between conditions. The EMG activity tended to decrease after a hypoxic session of WBVT.
      • Cochrane D.J.
      • Stannard S.R.
      • Firth E.C.
      • Rittweger J.
      Acute whole-body vibration elicits post-activation potentiation.
      did not observe changes in Time-to-MVIC after a single bout of WBVT in normoxia (one 5-min bout of vibration; frequency 26 Hz; amplitude 6 mm; static squat position of 40º knee flexion) in athletes. However, they did find changes in other neuromuscular variables, such as Rate of Force Development. The authors suggested that an acute bout of WBVT induces a post-activation potentiation (PAP) of the twitch, indicating that this modality of training can be used as a warm-up. This finding is consistent with our results, since we have also found a slight increase in MVIC, in all moments of the EMG and EMG Peak, as well as a slight decrease in the Time-to-MVIC after a session of normoxia. There are several possible explanations for the results of
      • Cochrane D.J.
      • Stannard S.R.
      • Firth E.C.
      • Rittweger J.
      Acute whole-body vibration elicits post-activation potentiation.
      . One possible explanation might be that WBVT increases intramuscular temperature due to muscular activity (
      • Cochrane D.J.
      • Stannard S.R.
      • Sargeant A.J.
      • Rittweger J.
      The rate of muscle temperature increase during acute whole-body vibration exercise.
      ). In addition, another possible explanation could be the PAP, which can produce an increase in muscle performance due to a greater muscle contractile activity (
      • Sale D.G.
      Postactivation potentiation: role in human performance.
      ).
      • Laudani L.
      • Mira J.
      • Carlucci F.
      • et al.
      Whole body vibration of different frequencies inhibits H-reflex but does not affect voluntary activation.
      investigated the acute effects of WBVT in normoxia on MVIC and CAR in healthy people using a frequency spectrum from 20 to 50 Hz (position: 10º knee joint; bout of 1-min; amplitude: 4 mm). Neither MVC nor CAR changed after WBVT with the different frequency conditions.
      • Jackson K.J.
      • Merriman H.L.
      • Vanderburgh P.M.
      • Brahler C.J.
      Acute effects of whole-Body vibration on lower extremity muscle performance in persons with multiple sclerosis.
      studied the acute effects of WBV session in normoxia with two different frequencies (2 and 26 Hz) on muscle torque in pwMS. No significant pre-post differences was found in isometric torque production or between the different frequencies used (2 and 26 Hz; 30 s of vibration). The lack of changes from these studies may be due to low training dose (30 s to 1 min of vibration).
      Interestingly, in older women with sarcopenia,
      • Miller R.M.
      • Heishman A.D.
      • Freitas E.D.S.
      • Bemben M.G.
      Comparing the acute effects of intermittent and continuous whole-body vibration exposure on neuromuscular and functional measures in sarcopenia and nonsarcopenic elderly women.
      demonstrated improvements in jump height and strength with intermittent WBVT (six 60-s exposures with 60-s rest intervals) compared with continuous WBVT (one six-minute exposure). These results support the idea that intermittent WBVT may have a greater capacity to stimulate PAP than continuous WBVT. The improvements of neuromuscular performance after a bout of WBVT in normoxia is supported by previous research in healthy population (
      • Cochrane D.J.
      • Stannard S.R.
      Acute whole body vibration training increases vertical jump and flexibility performance in elite female field hockey players.
      ;
      • Torvinen S.
      • Kannus P.
      • Sievänen H.
      • et al.
      Effect of a vibration exposure on muscular performance and body balance. Randomized cross-over study.
      ).
      However, the improvement of neuromuscular performance in a population with neuromuscular diseases after a bout of WBVT is unclear (
      • Freitas E.D.S.
      • Frederiksen C.
      • Miller R.M.
      • Heishman A.
      • Anderson M.
      • Pardo G.
      • Bemben M.G.
      Acute and chronic effects of whole-body vibration on balance, postural stability, and mobility in women with multiple sclerosis.
      ). The findings from the current study could be due to the inability of muscle spindles of persons with MS to adapt to the stimulus vibration and react to the tonic reflex. The decrease in EMG activity during an isometric contraction after the WBVT session in hypoxia shows an interesting use of hypoxia training as a training load with a capacity to alter the neuromuscular component in force production, as it indicates a greater recruitment of muscle fibers of the vastus lateralis during a hypoxic session, according to
      • Scott B.R.
      • Slattery K.M.
      • Sculley D.V.
      • Lockhart C.
      • Dascombe B.J.
      Acute physiological responses to moderate-load resistance exercise in hypoxia.
      . During the normoxic session, there was a slight increase in the MVIC in the right knee extensors, EMG and EMG Peak and a slight decrease in the Time-to-MVIC in both legs, suggesting that WBVT in normal conditions can be performed as a warm-up to pre-activate the neuromuscular response (i.e., PAP).
      In a recent study,
      • Freitas E.D.S.
      • Frederiksen C.
      • Miller R.M.
      • Heishman A.
      • Anderson M.
      • Pardo G.
      • Bemben M.G.
      Acute and chronic effects of whole-body vibration on balance, postural stability, and mobility in women with multiple sclerosis.
      did not observe changes in balance, postural stability or mobility after a session of WBVT (five 30-s bouts of vibration; frequency 30 Hz; amplitude 3 mm; 1-min rest intervals) in pwMS. However,
      • Miller R.M.
      • Heishman A.D.
      • Freitas E.D.S.
      • Bemben M.G.
      Comparing the acute effects of intermittent and continuous whole-body vibration exposure on neuromuscular and functional measures in sarcopenia and nonsarcopenic elderly women.
      observed improvements in TUG Test in older women with sarcopenia following intermittent, and not continuous, WBVT. This indicates that intermittent WBVT has greater potential for improvement mobility than continuous WBVT. Along these lines,
      • Dickin D.C.
      • Faust K.A.
      • Wang H.
      • Frame J.
      The acute effects of whole-body vibration on gait parameters in adults with cerebral palsy.
      found increases in walking speed after an acute session of WBVT in adults with cerebral palsy, which is likely explained by the improvement in range of motion at the knee and ankle. However,
      • Salmon J.R.
      • Roper J.A.
      • Tillman M.D.
      Does acute whole-body vibration training improve the physical performance of people with knee osteoarthritis.
      did not observe changes in TUG after WBVT session (ten 60‑s of vibration with 60‑s rest periods; frequency 35 Hz; amplitude 4–6 mm; knees slightly flexed) in people with knee osteoarthritis. Therefore, the results related to mobility in different populations are inconsistent, which may be because of the different types of health predicaments. Regardless, more research is needed to understand the acute and chronic effects of WBVT on daily life activities. In the current study, no significant pre-post differences were found in the neuromuscular variables, which could contribute to the lack of differences in the mobility measures. However, significant increases in RPE during and after sessions were found in both hypoxic and normoxic conditions. RPE increases from the beginning of the session, without reaching to very high values, suggesting that the participants exerted effort during the WBVT session and supports WBVT as a valid training load.
      This study provides a preliminary understanding of the acute effects of a WBVT session under both normoxic and hypoxic conditions on neuromuscular performance in pwMS, which is essential for designing long-term training programs using WBVT in this population. One limitation of this study was the small sample size. In addition, more studies are needed to examine the effects of vibration exposure using lower dosage. Training under hypoxic condition in pwMS is a field that needs further study for its potential benefits.
      Based on the findings from this study, we conclude that acute WBVT in hypoxia and normoxia resulted in no significant changes in mobility and neuromuscular performance in persons with MS, with the exception of EMG activity during maximal voluntary isometric contraction, which decreased after WBVT in hypoxia. Thus, there were no observed negative effects of using WBVT and hypoxia in persons with MS.

      5. Conclusions

      The importance of this study is to understand the acute physiological changes that occur with Whole-body Vibration Training (WBVT) in persons with MS, from which a better methodological approach can be designed for chronic WBVT in this population. Furthermore, it also highlights that WBVT minimizes symptomatic fatigue during physical effort in persons with MS. The researchers of this study, knowledgeable in the area of hypoxia and exercise training, believe that hypoxia may serve to potentiate the effects of training (
      • Girard O.
      • Malatesta D.
      • Millet G.P.
      Walking in hypoxia: an efficient treatment to lessen mechanical constraints and improve health in obese individuals?.
      ) on strength with minimal training duration. Thus, hypoxic training in persons with MS may be a good alternative in improving strength and physical function without needing a high exercise load.

      Formatting of funding sources

      This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

      Declaration of Competing Interest

      None.

      Acknowledgements

      We are grateful to all the participants in this study.

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