Do whole body vibration exercises affect lower limbs neuromuscular activity in populations with a medical condition? A systematic review

Abstract

Background:

The use of surface electromyography (sEMG) to evaluate muscle activation when executing whole body vibration exercises (WBVE) in studies provide neuromuscular findings, in healthy and diseased populations.

Objectives:

Perform a systematic review of the effects of WBVE by sEMG of lower limbs in non-healthy populations.

Methods:

The search using the defined keywords was performed in PubMed, PEDRo and EMBASE databases by three independent researchers. Applying the PRISMA statement several studies were selected according to eligibility criteria and organized for the review. Full papers were included if they described effects of WBVE for the treatment of illnesses, evaluated by sEMG of lower limbs independently on the year of the publication; in comparison or associated with other treatment and evaluation techniques.

Results:

Seven publications were selected; two in spinal cord injury patients, one in Friedreich’s ataxia patients, three in stroke patients and one study in breast cancer survivors. Reported effects of WBV in were muscle activation by sEMG and also on strength, blood flow and exercise resistance; even in paretic limbs.

Conclusion:

By the use of sEMG it was verified that WBVE elicits muscle activation in diseased population. These results may lead to the definition of exercise protocols to maintain or increase muscular activation. However, due to the heterogeneity of methods among studies, there is currently no consensus on the sEMG signal processing. These strategies might also induce effects on muscle strength, balance and flexibility in these and other illnesses.

Keywords

Electromyography muscle whole body vibration rehabilitation

1 Introduction

The guidance of the practice of exercises to the treatment of an illness must consider the effectiveness and safety of the physical activity and the capacity of the diseased individuals in performing what is suggested (Alvarez-Barbosa et al., 2014; Burke, Franca, Meneses, Pereira, & Marques, 2012).

The whole body vibration exercises (WBVE) have been extensively studied and are considered effective and safe when practiced by healthy and non-healthy people and different age groups (Cardinale, Soiza, Leiper, Gibson, & Primrose, 2010; Cochrane et al., 2008; Lee et al., 2017; Santin-Medeiros, Santos-Lozano, Cristi-Montero, & Garatachea Vallejo, 2017). The oscillating/vibratory platforms (OVP) can transmit mechanical vibrations to the body when in contact with the platform, generating WBVE (Cardinale & Bosco, 2003; Cardinale & Rittweger, 2006; Cardinale & Wakeling, 2005; Dionello et al., 2016; Swe, Benjamin, Tun, & Sugathan, 2016). The WBVE, in adequate biomechanical parameters such as frequency (f), amplitude (A), peak-to-peak displacement (D), and peak acceleration (apeak) have a broad range of effects being safe and easy to perform (Anwer, Alghadir, Zafar, & Al-Eisa, 2016; Rauch, 2009; Rauch et al., 2010).

The WBVE may increase muscular strength and power while acting on neuromuscular function (Dionello et al., 2016; Iwamoto, Sato, Takeda, & Matsumoto, 2012). Several mechanisms of these exercises may be responsible for the prevention of muscle mass decline, muscle function’s increase or maintenance, with consequences to bone mass (Osugi, Iwamoto, Yamazaki, & Takakuwa, 2014; Raimundo, Gusi, & Tomas-Carus, 2009).

Neuronal and muscular effects of WBVE may be accessed by the surface electromyography (sEMG), since this test measures muscle response to nervous stimulation and is a tool to investigate muscular damage (Mosier, Herda, Trevino, & Miller, 2017).

The evaluation through sEMG may provide neuromuscular findings while performing, before or after the execution of WBVE. It has been suggested that mechanical vibrations causes reflex muscle contractions due to tonic vibration reflex (TVR) (Bosco et al., 1999; Cardinale & Bosco, 2003; Gillies, Burke, & Lance, 1971a, 1971b). The use of similar and different protocols regarding biomechanical parameters as well as magnitude of effects has provided information of its effects on healthy young (Marin, Bunker, Rhea, & Ayllon, 2009; Marin, Garcia-Gutierrez, Da Silva-Grigoletto, & Hazell, 2015; Marin, Garcia Rioja, Bernardo-Filho, & Hazell, 2015) and on aging populations (Marin, Herrero, et al., 2012; Marin, Santos-Lozano, et al., 2012). Especially in diseased and aging individuals sEMG has been used to determine the muscular activity obtained from different types of exercises with the purpose of enhancing balance, decreasing risk factors for falls and affecting mobility to perform daily activities (Machado, Garcia-Lopez, Gonzalez-Gallego, & Garatachea, 2010; Ochi et al., 2014).

There is an increasing interest in the evaluation of WBVE in different situations and illnesses, irrespective of the compromised part or system of the body (Tankisheva et al., 2013). Some examples of the evaluation of WBVE effects on diseases are the studies in cancer (Salhi et al., 2015; Van Ruymbeke, Boone, Coorevits, Vanderstraeten, & Bourgois, 2014), neurologic diseases (Ness & Field-Fote, 2009; Pang, Lau, & Yip, 2013) rheumatoid arthritis (Prioreschi, Tikly, & McVeigh, 2014), osteoporosis (Bemben, Palmer, Bemben, & Knehans, 2010; Dionello et al., 2016; Gomez-Cabello et al., 2014), knee osteoarthritis (Anwer et al., 2016; Wang et al., 2015), vascular disease (Arashi et al., 2010; Sanudo et al., 2013), metabolic syndrome (Alfonso-Rosa, Del Pozo-Cruz, Del Pozo-Cruz, Sanudo, & Abellan-Perpinan, 2015; del Pozo-Cruz, Alfonso-Rosa, del Pozo-Cruz, Sanudo, & Rogers, 2014; Sa-Caputo Dda et al., 2014; Sanudo et al., 2013) and chronic obstructive pulmonary disease (Furness, Bate, Welsh, Naughton, & Lorenzen, 2012; Furness, Joseph, Naughton, Welsh, & Lorenzen, 2014).

By using sEMG, the acquired and processed signal obtained during muscle activation while performing WBVE may guide proper strategies to maintain or increase muscle strength, flexibility and prevent complications such as falls, fractures or other morbidities also in populations with a medical condition.

The aim of this study was to perform a systematic review of the effects of whole body vibration exercises on neuromuscular activation of lower limbs in diseases, if evaluated by sEMG associated or not to other interventions and outcomes.

2 Material and methods

2.1 Search strategy used to find the publications

Three reviewers (CFD, PLS, DSC) independently accessed publications of PubMed, PEDro and EMBASE databases in the Universidade do Estado do Rio de Janeiro(UERJ), Brazil up to April of 2017.

The medical subject headings (MeSH) were accessed as terms resource for the definition of keywords. The first search was performed on PubMed, the second on EMBASE and the third on PEDro. The databases were chosen due to their large and open access to medical and rehabilitation literature.

A PICO question (population, intervention, comparator, outcome) was elaborated to inform keywords. The PICO question was: (i) population = diseased population, presence of a medical condition. The definition of illness was according to the International Classification of Diseases, of 2003; (ii) intervention = WBVE; (iii) comparator = placebo or no treatment; and (iv) outcome = muscle activation pattern evaluated by sEMG of lower limbs.

The first search used the keywords “electromyography” or “EMG” and “WBV” or “whole body vibration” on the databases.

The second search used the keywords “vibration” and “muscle” and “lower limbs” on the same databases. All the pooled publications were screened following the inclusion and exclusion criteria, described as follows.

2.2 Eligibility criteria

In both the keywords searches, all the publications found on the databases were preliminarily considered to be included in this systematic review. Papers from personal files of the authors were selected first.

After the three reviewers carried out searches for publications independently, they agreed on which publications should be excluded from the search results. Full papers were included for this systematic review if they met the search criteria.

The studies, independently on the year of the publication, were selected if they: (i) were randomized controlled trial (RCT), (ii) were a single group experimental study (crossover design) in the absence of RCT, (iii) were published in English language, (iv) described WBVE generated by an OVP effects for the treatment of a medical condition, and (v) evaluated neuromuscular effects in lower limbs by sEMG. The included studies might also evaluate (vi) performed static or dynamic exercises on OVP, and (vii) if other associated techniques evaluating WBV effects were used.

2.3 Exclusion criteria

Exclusion criteria allowed the elimination of unnecessary articles identified in the search.

Papers were excluded if they were (i) published in a language different of the English; (ii) review articles; (iii) case reports; (iv) related to upper limbs; (v) with healthy volunteers or sports activities; (vi) using stochastic vibration methods; (vii) studies in physiological phenomena (aging, andropause and menopause); (viii) with muscular outcomes related to strength and flexibility exclusively; (ix) with questionnaires or qualitative outcomes exclusively; (x) with evaluation of recovery of structural damage or post-surgery exclusively; (xi) duplicate papers.

The studies with WBVE and sEMG in healthy, andropause and menopause populations were excluded since the objective of the search was to identify studies in diseased population. This specific search could collect possible effects of WBVE on muscular activation in rehabilitation programs.

Then a flowchart (Fig. 1), based in the Preferred Reporting Items for Systematic Reviews and Meta-analysis (PRISMA) analysis, was created to show the steps in the selection of the full papers analyzed in this review (Liberati et al., 2009).

Fig.1

Flowchart indicating the steps to select the full papers analyzed in this review.

2.4 Levels of evidence (LE) of the selected papers

The National Health and Medical Research Council Hierarchy of Evidence (NHMRC, 2003–2007) (Merlin, Weston, & Tooher, 2009) and the Physiotherapy Evidence Database (PEDro) scale (Maher, Sherrington, Herbert, Moseley, & Elkins, 2003) were used to classify the included studies in this systematic review (Figs. 2 and 3).

Fig.2

Designation of levels of evidence according to the intervention research question.

Fig.3

Methodological quality of evidence according PEDRo scale.

Each article was assigned to one reviewer, crosschecked by a second reviewer and when there was disagreement, a third researcher was consulted and the issue discussed until consensus was reached.

2.5 Data analysis

Data was not comparable and statistical pooling was not appropriate, therefore, a metanalysis could not be performed.

3 Results

The Fig. 1 shows the flowchart (Liberati et al., 2009) of the steps to select the full papers analyzed in this systematic review. Of the 386 papers initially screened, only 7 have reached the inclusion criteria.

Of the seven included papers, two were Level II (RCT), three were level III-1, and two were level IV according to the NHMRC (Merlin et al., 2009) (Table 1). The Fig. 2 describes NHMRC levels of evidence (LE). The included studies consisted mainly of comparative studies against other interventions or controls, or pre-post-tests. Several studies asserted to be randomized controlled trials, but the descriptions indicated that these studies had not adequate randomization of groups, and therefore could not be classified as level II evidence. The less strict designs included were of pre-posttest design with no concurrentcomparison groups (two studies).

Table 1
Illnesses, aims, methods, LE and results of included studies

Disease Objectives Patients Muscles sEMG technique WBVE protocol f/A/D/a_peak Associated techniques and evaluations LE^*^,^** Results

Van Ruymbeke et al. Breast cancer Evaluate muscle activity and RPE during WBVE in breast cancer survivors 20 breast cancer survivors and 20 healthy controls RF, VM, BF, TA, G Acquisition through MyoSystem 1400 (Noraxon, Scottsdale, Arizona, USA). The raw EMG signals were band-pass filtered between 10–500 Hz, amplified and analogue-digital converted (12 bit) at a sampling rate of 1000 Hz. Amplified raw sEMG signals were converted to an average RMS signal through MyoResearch X (Noraxon USA, Inc., Scottsdale, AZ) Warm-up activity of 5 minutes (unloaded cycling). Isometric squats (knee angle of 55°) on a vertical OVP. RPE and sEMG were recorded under the following conditions: non-vibration and vibration conditions 0, 20, 30, 40, 50 Hz/D = 4 mm/0; 3.2; 7.2; 12.8; 20 g Combination of VAS score and revised Borg RPE III-1^* fair ^** Muscle activation did not differ between breast cancer survivors and healthy controls. Regarding VAS scores no significant group versus f interaction was found. RPE increased with increasing frequencies. EMG RMS responses of all muscles were higher in the presence of vibration compared to non-vibration condition.

Herrero et al. FA Investigate the effects of WBVE on BFV and muscular activity after different vibration protocols in FA patients 10 FA patients VL, VM Acquisition sEMG through ME6999 Biomonitor, Mega electronics, Kuopio, Finland. Total common mode rejection was of 110 dB, and data was low pass filtered (8–500 Hz) and sampled at 200 Hz before stored. A band-width of 0.8 Hz around each harmonic was excluded from the RMS calculation. Processing through MegaWin software, Mega electronics, Kuopio, Finland. Two familiarization sessions Patients on a squat position received six 3 min WBVE on a vertical OVP depending on a combination of different f 10, 20 or 30 Hz/D = 5 mm/1; 4; 9 g Femoral artery BFV through Doppler USS, and RPE IV^* fair^** PBF velocity was increased with respect to basal values after 1, 2 and 3 min of WBVE. Mean BFV was increased with respect to basal values after 1, 2 and 3 min of WBVE EMG amplitude of VL and VM was increased and EMG frequencies decreased during the application of WBVE. Higher f (30 Hz) produced a greater increase in BFV and RPE.

Tihanyi et al. Acute stroke Determine the effect of WBVE on isometric and eccentric torque and EMG variables of knee extensors on the affected side of stroke patients 16 acute stroke patients BF, VL Acquisition of data through the TeleMyo telemetric hardware system (Noraxon US, Inc, Scotsdale, AZ, USA. Notch filters information was not provided. Signals were processed using the Myosoft software (Noraxon Myoclinical 2.10) 3 days of familiarization VG received WBVE with 20 Hz f 3xweek standing on a vertical OVP in half squat position meanwhile flexing and extending the joints and placing the weight from one leg to the other. 20 Hz/D = 5 mm/4 g Maximum isometric and eccentric torque with dynamometer, rate of torque, development and co-activation of knee flexors II^*high^** Isometric and eccentric knee extension torque increased in CG. WBVE increased EMG A and the median f in the VL without changes in the CG. WBVE improved the ability to generate mechanical work during eccentric contraction. WBVE reduced BF co-activation during isometric and eccentric contraction.

Liao et al. Chronic stroke Determine the influence of WBVE on the activity of the VL and G muscles during the performance of different exercises in chronic stroke patients 45 chronic stroke patients G, VL Acquisition through Bagnoli-8 EMG Systems; DelSys, Inc. Data was filtered with a band-pass butterworth filter, and the infinite impulse response rejector was implemented to eliminate rhe associated harmonics at the frequencies of 20, 30 and 60 Hz. Processing was performed through MyoResearch XP, Master Package version 1.06 (Noraxon USA, Inc., Scottsdale, AZ) (a) no WBVE, (b) low-intensity WBVE (c) high-intensity WBVE in a vertical OVP while performing the eight different static exercises: upright standing, semi squat, deep squat, weight shifted forward, weight shifted backward, weight shifted to the side, forward lunge, and single-leg standing 20, 30 Hz/A = 0.60; 0.44 mm/0.96 and 1.61 g Modified Ashworth Scale for the severity of spasticity III-1^* fair ^** Exposure to WBVE (low- and high-intensity protocols) significantly increased VL and GS EMG A on both the paretic and non-paretic sides in different exercise conditions compared with no WBVE. No significant difference in EMG magnitude was found between the high- and the low-intensity WBVE protocols. With a few exceptions, WBVE enhanced EMG activity in the paretic and non-paretic leg muscles to a similar extent in different exercise conditions.

Silva et al. Chronic stroke The aim of this study was to investigate the acute effects of WBVE on the motor function of patients with stroke 43 stroke patients RF, TA A 4 channel device (EMG System of Brazil Ltda), model EMG-800 C, 20- to 500-Hz signals were collected with a sampling frequency of 2 KHz. Analog bandpass filter of 20–500 Hz with a common rejection ratio of greater than 100 dB was used. Signals were processed using MATLAB software routines (MathWorks Inc, Natick, MA) The protocol had 4 occasions: analysis of the intervention group clinical data and after of the CGclinical data; familiarization and Intervention – WBVE on a triplanar OVP (sEMG signal record, tests before and after WBVE) 50 Hz/A = 2 mm/20 g Different pedal stances during recordings; 6MWT, SCT, TUGT II^* high^** There was no evidence of effects on the group and time interaction relative to variables affected side RF, unaffected side RF, affected side TA, unaffected side TA, and the SCT. There was evidence of effects on the group interaction relative to variables 6MWT and TUGT.

Herrero et al. SCI To investigate the effects WBVE on muscular activity and BFV after different vibration treatments in patients with SCI 8 SCI patients VL, VM Myoelectric raw signals were acquired with a two channel sEMG device (MyoTrac Infiniti, Thought Technology, Montreal, Canada). A bandwidth of±0.8 Hz around each harmonic was excluded from the RMS calculation. EMG data processing was performed with a specific software (BioGraph Infiniti, Thought Technology, Montreal, Canada) Six 3-min WBV treatments depending on a combination of f and protocol (constant or fragmented) in a vertical OVP 10, 20 or 30 Hz/D = 5 mm/1; 4; 9 g Femoral artery BFV was registered with color Doppler USS IV^* fair^** Peak BFV increased after 1, 2 and 3 min of WBVE. The 20 Hz f increased peak BFV after 2 and 3 min of WBVE. The 30 Hz f increased peak BFV after 1, 2 and 3 min of WBVE and during the first minute after the end of the stimulus. No protocol effect was observed for blood parameters. EMG activity of VL and VM increased independently of the applied f or protocol.

Alizadeh -Meghrazi et al. SCI To investigate whether WBVE could evoke lower extremity EMG activity in AB and SCI individuals 10 SCI patients TA, S, GM, RF, VL Acquisition of signals using an sEMG system AMT-8 (Bortec Biomedical Ltd, Calgary, Alberta, Canada). Frequency band-width of 10–1000 Hz, common rejection mode of 115 dB (at 60 Hz) The processing was obtained with MATLAB (R2008a, Mathworks, Natick, MA, USA) 2 days of evaluation on two different manufacturers’ vertical OVP (WAVE® and Juvent™) were evaluated. The effects of vibration A, f and subject posture on lower extremity EMG activation were determined. 25, 35, 45 Hz/D = 0.2, 0.6 or 1.2 mm/0.2; 0.4; 0.8 g0.7; 1.4; 2.4 g1.5; 2.9; 4.8 g Different knee angles during the recordings (140°, 160°, 180°) III-1^* fair^** WBVE can elicit EMG activity among subjects with chronic SCI. The A of vibration had the greatest influence on EMG activation, while the f of vibration had lesser but significant impact on the measured lower extremity EMG activity.

	Disease	Objectives	Patients	Muscles	sEMG technique	WBVE protocol	f/A/D/a_peak	Associated techniques and evaluations	LE^^,^*	Results
Van Ruymbeke et al.	Breast cancer	Evaluate muscle activity and RPE during WBVE in breast cancer survivors	20 breast cancer survivors and 20 healthy controls	RF, VM, BF, TA, G	Acquisition through MyoSystem 1400 (Noraxon, Scottsdale, Arizona, USA). The raw EMG signals were band-pass filtered between 10–500 Hz, amplified and analogue-digital converted (12 bit) at a sampling rate of 1000 Hz. Amplified raw sEMG signals were converted to an average RMS signal through MyoResearch X (Noraxon USA, Inc., Scottsdale, AZ)	Warm-up activity of 5 minutes (unloaded cycling). Isometric squats (knee angle of 55°) on a vertical OVP. RPE and sEMG were recorded under the following conditions: non-vibration and vibration conditions	0, 20, 30, 40, 50 Hz/D = 4 mm/0; 3.2; 7.2; 12.8; 20 g	Combination of VAS score and revised Borg RPE	III-1^* fair ^**	Muscle activation did not differ between breast cancer survivors and healthy controls. Regarding VAS scores no significant group versus f interaction was found. RPE increased with increasing frequencies. EMG RMS responses of all muscles were higher in the presence of vibration compared to non-vibration condition.
Herrero et al.	FA	Investigate the effects of WBVE on BFV and muscular activity after different vibration protocols in FA patients	10 FA patients	VL, VM	Acquisition sEMG through ME6999 Biomonitor, Mega electronics, Kuopio, Finland. Total common mode rejection was of 110 dB, and data was low pass filtered (8–500 Hz) and sampled at 200 Hz before stored. A band-width of 0.8 Hz around each harmonic was excluded from the RMS calculation. Processing through MegaWin software, Mega electronics, Kuopio, Finland.	Two familiarization sessions Patients on a squat position received six 3 min WBVE on a vertical OVP depending on a combination of different f	10, 20 or 30 Hz/D = 5 mm/1; 4; 9 g	Femoral artery BFV through Doppler USS, and RPE	IV^* fair^**	PBF velocity was increased with respect to basal values after 1, 2 and 3 min of WBVE. Mean BFV was increased with respect to basal values after 1, 2 and 3 min of WBVE EMG amplitude of VL and VM was increased and EMG frequencies decreased during the application of WBVE. Higher f (30 Hz) produced a greater increase in BFV and RPE.
Tihanyi et al.	Acute stroke	Determine the effect of WBVE on isometric and eccentric torque and EMG variables of knee extensors on the affected side of stroke patients	16 acute stroke patients	BF, VL	Acquisition of data through the TeleMyo telemetric hardware system (Noraxon US, Inc, Scotsdale, AZ, USA. Notch filters information was not provided. Signals were processed using the Myosoft software (Noraxon Myoclinical 2.10)	3 days of familiarization VG received WBVE with 20 Hz f 3xweek standing on a vertical OVP in half squat position meanwhile flexing and extending the joints and placing the weight from one leg to the other.	20 Hz/D = 5 mm/4 g	Maximum isometric and eccentric torque with dynamometer, rate of torque, development and co-activation of knee flexors	II^high^*	Isometric and eccentric knee extension torque increased in CG. WBVE increased EMG A and the median f in the VL without changes in the CG. WBVE improved the ability to generate mechanical work during eccentric contraction. WBVE reduced BF co-activation during isometric and eccentric contraction.
Liao et al.	Chronic stroke	Determine the influence of WBVE on the activity of the VL and G muscles during the performance of different exercises in chronic stroke patients	45 chronic stroke patients	G, VL	Acquisition through Bagnoli-8 EMG Systems; DelSys, Inc. Data was filtered with a band-pass butterworth filter, and the infinite impulse response rejector was implemented to eliminate rhe associated harmonics at the frequencies of 20, 30 and 60 Hz. Processing was performed through MyoResearch XP, Master Package version 1.06 (Noraxon USA, Inc., Scottsdale, AZ)	(a) no WBVE, (b) low-intensity WBVE (c) high-intensity WBVE in a vertical OVP while performing the eight different static exercises: upright standing, semi squat, deep squat, weight shifted forward, weight shifted backward, weight shifted to the side, forward lunge, and single-leg standing	20, 30 Hz/A = 0.60; 0.44 mm/0.96 and 1.61 g	Modified Ashworth Scale for the severity of spasticity	III-1^* fair ^**	Exposure to WBVE (low- and high-intensity protocols) significantly increased VL and GS EMG A on both the paretic and non-paretic sides in different exercise conditions compared with no WBVE. No significant difference in EMG magnitude was found between the high- and the low-intensity WBVE protocols. With a few exceptions, WBVE enhanced EMG activity in the paretic and non-paretic leg muscles to a similar extent in different exercise conditions.
Silva et al.	Chronic stroke	The aim of this study was to investigate the acute effects of WBVE on the motor function of patients with stroke	43 stroke patients	RF, TA	A 4 channel device (EMG System of Brazil Ltda), model EMG-800 C, 20- to 500-Hz signals were collected with a sampling frequency of 2 KHz. Analog bandpass filter of 20–500 Hz with a common rejection ratio of greater than 100 dB was used. Signals were processed using MATLAB software routines (MathWorks Inc, Natick, MA)	The protocol had 4 occasions: analysis of the intervention group clinical data and after of the CGclinical data; familiarization and Intervention – WBVE on a triplanar OVP (sEMG signal record, tests before and after WBVE)	50 Hz/A = 2 mm/20 g	Different pedal stances during recordings; 6MWT, SCT, TUGT	II^* high^**	There was no evidence of effects on the group and time interaction relative to variables affected side RF, unaffected side RF, affected side TA, unaffected side TA, and the SCT. There was evidence of effects on the group interaction relative to variables 6MWT and TUGT.
Herrero et al.	SCI	To investigate the effects WBVE on muscular activity and BFV after different vibration treatments in patients with SCI	8 SCI patients	VL, VM	Myoelectric raw signals were acquired with a two channel sEMG device (MyoTrac Infiniti, Thought Technology, Montreal, Canada). A bandwidth of±0.8 Hz around each harmonic was excluded from the RMS calculation. EMG data processing was performed with a specific software (BioGraph Infiniti, Thought Technology, Montreal, Canada)	Six 3-min WBV treatments depending on a combination of f and protocol (constant or fragmented) in a vertical OVP	10, 20 or 30 Hz/D = 5 mm/1; 4; 9 g	Femoral artery BFV was registered with color Doppler USS	IV^* fair^**	Peak BFV increased after 1, 2 and 3 min of WBVE. The 20 Hz f increased peak BFV after 2 and 3 min of WBVE. The 30 Hz f increased peak BFV after 1, 2 and 3 min of WBVE and during the first minute after the end of the stimulus. No protocol effect was observed for blood parameters. EMG activity of VL and VM increased independently of the applied f or protocol.
Alizadeh -Meghrazi et al.	SCI	To investigate whether WBVE could evoke lower extremity EMG activity in AB and SCI individuals	10 SCI patients	TA, S, GM, RF, VL	Acquisition of signals using an sEMG system AMT-8 (Bortec Biomedical Ltd, Calgary, Alberta, Canada). Frequency band-width of 10–1000 Hz, common rejection mode of 115 dB (at 60 Hz) The processing was obtained with MATLAB (R2008a, Mathworks, Natick, MA, USA)	2 days of evaluation on two different manufacturers’ vertical OVP (WAVE® and Juvent™) were evaluated. The effects of vibration A, f and subject posture on lower extremity EMG activation were determined.	25, 35, 45 Hz/D = 0.2, 0.6 or 1.2 mm/0.2; 0.4; 0.8 g0.7; 1.4; 2.4 g1.5; 2.9; 4.8 g	Different knee angles during the recordings (140°, 160°, 180°)	III-1^* fair^**	WBVE can elicit EMG activity among subjects with chronic SCI. The A of vibration had the greatest influence on EMG activation, while the f of vibration had lesser but significant impact on the measured lower extremity EMG activity.

Abbreviations: A = Amplitude, a _peak = peak of acceleration; AB = able-bodied; BF = biceps femoris; BFV = blood flow velocity; CG = control group; D = peak-to-peak displacement; BFV = blood flow velocity; EMG = electromyography; FA = ‘Friedreich’s ataxia; f = frequency; G = gastrocnemius; GM = gastrocnemius medialis; LE = levels of evidence (NHMRC ^*/PEDRo scale^**); OVP = oscillating/vibratory platform; PBF = peak blood flow; RPE = rating of perceived exertion; RF = rectus femoris; RMS = root mean square; SCT = Stair-Climb Test; SCI = spinal cord injury; S = soleus; sEMG = surface electromyography; TA = tibialis anterior; TUGT = Timed Get-Up and- Go Test; USS = ultrasound system; VG = vibration group; VL = vastus lateralis; VM = vastus medialis; VAS = visual analogue scale; USS = ultrasound system; WBVE = whole body vibration; 6MWT = Six-Minute Walk Test.

By PEDro scale’scoring two studies were ‘high’ in methodological quality, five were ‘fair’. No ‘poor’ quality studies were obtained on the search nor were included in this systematic review (Maher et al., 2003), as described in Table 1.

According to both LE, two studies had better methodological design (Silva et al., 2014; Tihanyi, Horvath, Fazekas, Hortobagyi, & Tihanyi, 2007).

The publications’ aims, participants’ characteristics, details on the sEMG evaluation of the applied WBVE protocols as well as the LE, methodological quality and results are demonstrated in Table 1.

The search did not narrow the studies to neurological diseases; every medical condition in a study that met the eligibility criteria could be appraised.

The diseases of the included studies were breast cancer (Van Ruymbeke et al., 2014), Friedreich’s ataxia (Herrero, Martin, et al., 2011), acute and chronic stroke (Liao, Ng, Jones, Huang, & Pang, 2016; Silva et al., 2014; Tihanyi et al., 2007) and spinal cord injury (Alizadeh-Meghrazi et al., 2014; Herrero, Menendez, et al., 2011), with different variables and methods (Table 1).

Regardless of the diverse outcomes, the common objective of the all the selected papers was to evaluate neuromuscular effects of WBVE in lower limbs through sEMG analysis, and if these exercises demonstrate gains in the functional aspects of these illnesses.

The mostly used OVP in the papers were vertical type (Alizadeh-Meghrazi et al., 2014; Herrero, Martin, et al., 2011; Herrero, Menendez, et al., 2011; Liao et al., 2016; Tihanyi et al., 2007; Van Ruymbeke et al., 2014); but one study used a triplanar model (Silva et al., 2014).

In relation to the biomechanical parameters for evaluation of WBVE effects recommended by the International Society of Musculoskeletal and Neuronal Interactions (ISMNI) (Rauch et al., 2010), these were added and/or calculated when other data was provided. The ISMNI recommendations were not completely followed in all the studies where the methods were described.

In reference to the sEMG method in the articles, related to acquisition, filtering and processing, there was no uniformity. The description was that raw signals were acquired with vibration, band pass filters were used to delete mechanical vibration frequencies and signals were processed (Abercromby et al., 2007). The descriptions of the protocols were not totally according to the SENIAM (Surface EMG for a Non-Invasive Assessment of Muscles) or the ISEK (International Society of Electrophysiology and Kinesiology) orientations in all studies. One study did not provide information about filters used (Tihanyi et al., 2007).

Although the sEMG was mostly used in neurologic diseases as a tool for evaluation of WBVE effects, it was not exclusive to this group of illnesses.

The study in breast cancer survivors (Van Ruymbeke et al., 2014) evaluated sEMG in rectus femuris (RF), vastus medialis (VM), biceps femuris (BF), tibialis anterior (TA) and gastrocnemius (G). It was found no significant differences between groups (study and control) concerning muscle activity or rate of perceived exertion (RPE) (p = 0.471 and p = 0.629, respectively). The muscle interaction versus f was significant (p < 0.001) and RPE increased directly related to increasing vibration f (p < 0.05); however, no difference was found between 20 and 30 Hz (p = 0.088). The authors suggested the use of those frequencies in WBVE for this group of patients, as part of a rehabilitationprogram.

The only session evaluation in patients with acute stroke, with patients with less than a month of acute cerebral ischemia (Tihanyi et al., 2007) has demonstrated that myoelectrical activity in the VL increased significantly in the vibration group (VG) (44%; p = 0.0122) after vibration during isometric knee extension without changes in the EMG root mean square (EMGrms) in the control group (CG). The EMG activity was not affected by vibration in the BF in either group, nor in fast isometric contractions. The EMGrms associated with maximum eccentric torque (MET) decreased in BF activation and increased significantly in VL activation (33.2%; p = 0.0013), and decreased in BF, an antagonist muscle, in the VG, under the same circumstances (22.5%; p = 0.0013). The MET EMGrms in the CG remained unchanged. It was concluded that under eccentric conditions, WBVE increased median f in the VG but not in the CG.

The study from Silva et al. (Silva et al., 2014) randomly assigned 43 chronic stroke patients with hemiparesis to the VG (n = 33) or CG (n = 10), with reduce motor function by the Fugl-Meyer Assessment scale. The individuals, after familiarization, were submitted to one session of high magnitude WBVE (a peak = 20 g), while performing three body positions: bipedal stances with two degrees of knee flexion (30° or 90°) and a unipedal stance of the paretic limb. The sEMG of RF and TA were performed during WBVE, to establish muscle activation pattern during voluntary isometric contraction (VIC). The patients were evaluated through six-minute walk test (6MWT), stair-climb test (SCT) and the timed-up-and-go test (TUGT). It was only observed differences among VG and CG regarding 6MWT (p = 0.01) and TUGT (p = 0.02). No differences in muscle activation between affected and not-affected limbs were elucidated in sEMG.

Also in patients with chronic stroke, the paper from Liao et al. (Liao et al., 2016) exposed them to three WBVE conditions. The protocol comprised “no WBV”, “low magnitude” (less than 1 g) and “high magnitude” while positioning subjects in different positions: upright standing, semi squat, deep squat, weight shifted forward, weight shifted backward, weight shifted to the side, forward lunge, and single-leg standing. Bilateral VL and G muscle activity were evaluated whilst executing of WBVE in maximal voluntary contraction (MVC) of muscles. Differently from Silva et al. [51] it was demonstrated that exposure to WBVE, irrespectively to magnitude or paresis status, significantly increased VL and G sEMG activity on both the limbs compared with no WBV. Regarding VL on WBVE, the deep squat position induced higher activation in paretic limb (p < 0.001), but not on the non-paretic limb. The most activating position to paretic GS was the weight-shifted forward while on vibration (p < 0.001), but not when there was no vibration added, similar to VL. With a few exceptions, WBV enhanced EMG activity in leg muscles to a consonant extent in different positioning. No relationship was found between normalized EMGrms and spasticity of the paretic knee and ankle.

Although in different anatomic level of neurological compromise, the patients with spinal cord injury (SCI) had WBVE effects evaluated by sEMG for different purposes. The protocol applied by Alizadeh-Meghrazi et al. investigated the ability of WBVE to evoke EMG activation in resting lower-limb muscles of SCI patients (Alizadeh-Meghrazi et al., 2014). Although significance and magnitude of effects were not provided, EMG activity was successfully produced in both able-bodied (AB) subjects and subjects with SCI. These results provided the first demonstration that WBVE can induce activation even in resting muscles with low levels of TVR activity, related to biomechanical parameters that were employed. The WBVE could induce muscle activity in the resting muscles at the same level as what was observed during standing. Increasing the amplitude of vibration had the most evident impact on EMG activation in opposition to the postures that the patients were submitted to.

The article by Herrero et al. evaluated eight patients that had SCI and used wheelchair for their locomotion. All subjects were classified by the American Spinal Injury Association (ASIA) as “A”, which means that patients had no sensory or motor function preserved in the sacral segments S4-S5. It was performed sEMG of VM and VL along with the evaluation of blood flow velocity (BFV) using a pulsed color Doppler with a linear array transducer (7.5–12 MHz; length, 50 mm) in the femoral artery to analyze WBVE effects. The main findings of the present study were that WBVE alone can significantly increase leg BFV in SCI patients, with proportional increases to the minutes of intervention (11.3±10.3%, p < 0.05; 19±13.5% and 23±14.4%, p < 0.01 respectively). Higher f, especially 30 Hz, produced greater increase in leg BFV (more than 35% in the third minute). Regarding VM and VL sEMG activity, the increasing activation was obtained with passing of time, especially after the third minute in respect to baseline values (VM = 26±9.9 in respect to 18.9±2.8 mV, p < 0.05; VL = 26.2±5.8 in respect to 15.2±1.1 mV, p < 0.05). No difference was observed regarding the application of the WBVE in a constant or fragmented protocol.

Although being a rare genetic disease, patients with Friedreich’s ataxia (FA) suffer from consequences of progressive neuromuscular impairment (Aranca et al., 2016). The group of Herrero et al. (Herrero, Martin, et al., 2011) evaluated muscle activation during WBVE of FA patients. The protocol consisted of two familiarization sessions and one working session that comprised six bouts of 3 min WBVE treatments on a tilt-table combining 3 f (10, 20 or 30 Hz) in a constant or fragmented way. Femoral artery BFV with doppler, VL and VM sEMG, and RPE were registered. The peak and the mean BFV were increased with respect to baseline values after the fragmented session of WBVE. There was a time effect for PBF (p < 0.001) and MBF (p < 0.001). A time-f effect for MBV (p < 0.05) was observed especially for 30 Hz. The sEMG amplitude of VL and VM was increased with time effect for VM and VL (increase of 23% after 3 min, p < 0.05 and 39.4% after 3 min, p < 0.05 respectively). Since sEMG frequencies decreased during the working sessions proportionally to decreases in applied WBVE f, it was suggested that higher frequencies (30 Hz) produce a greater increase in BFV, VL and VM muscle activation and RPE.

4 Discussion

The neuromuscular activation of lower limbs with WBVE evaluated by sEMG in different populations with a medical condition was observed, independently of the pathophysiological mechanism. Patients with diverse illness were able to adequately perform the exercises (Van Ruymbeke et al., 2014). There was increased muscular activity in lower limbs, even paretic (Liao et al., 2016), mostly related to higher a_peak either by augmenting A or f (Alizadeh-Meghrazi et al., 2014).

When other techniques were evaluated along with sEMG, it was evidenced that other outcomes were achieved. The blood flow was enhanced by mechanical vibrations (Herrero, Martin, et al., 2011; Herrero, Menendez, et al., 2011), as well as functionality, when evaluated by TUGT or 6MWT (Silva et al., 2014). The vibration had influence also on maximal voluntary strength (Tihanyi et al., 2007) of agonists and reduction in antagonistic muscle activity, which might possibly reduce spasticity.

To our knowledge, this is the first systematic review to point out the potential use of sEMG on the evaluation of muscle activity concerning WBVE in non-healthy populations, which may serve as stimulus to increase the fields of study of muscle activation pattern by WBVE in other diseasedpopulations.

The recommendation of WBVE with appropriate parameters may be a safe and effective intervention to prevent and treat muscle/bone complications. Increased sEMG activity after WBVE indicates that patients were able to recruit more motor units than before. Of importance, all these results might have an effect on functionality regarding standing, walking and climbing stairs (Liao et al., 2016; Silva et al., 2014), as part of an exercises program effects evaluation.

The augmentation in muscle activity detected by sEMG during WBVE can be attributed to TVR, a reflex described as similar to the stretch reflex (Alizadeh-Meghrazi et al., 2014; Silva et al., 2014). The actions in soft tissues caused by vibration are capable of activating muscle spirals that leads to an enhancement of the stretch–reflex loop (Cardinale & Bosco, 2003), as the reflex activation of the a motor neuron. The intensification in muscle strength and power after vibration can consecutively be attributed to the increased muscle activity and loading of the musculoskeletal system as a result. There might subsequently be a turn into morphological adjustment and/or modifications in concentrations of hormones, such as testosterone, cortisol, and growth hormone, leading to muscle growth and strength (Giunta et al., 2012; Sartorio et al., 2010).

Weakness as a consequence of imposed rest or disease has been identified as a major contributing factor to disability in many diseases (de Andrade et al., 2012), being exercises a common and effective way of reducing this damage (Seo et al., 2016). Muscular impairments affect transfer capacity, ability to climb stairs, balance as well as gait and walking. Due to its ability to enhance muscle activity, increasing research has explored whether WBVE for short or longer periods can lead to benefits in populations who often suffer from these undesired neuromuscular consequences (Marin et al., 2009; Marin, Ferrero, Menendez, Martin, & Herrero, 2013; Marin & Hazell, 2014; Marin, Herrero, et al., 2012; Masani et al., 2014; Ness & Field-Fote, 2009). The evaluation of muscular activity through sEMG before, during and after the exercise programs, provides effectiveness and safety informations.

Regardless of the type of platform, protocols and vibration parameters used in WBVE, this modality of exercises has been shown to affect strength, power and functionality in healthy and non-healthy populations (Alvarez-Barbosa et al., 2014; Aminian-Far, Hadian, Olyaei, Talebian, & Bakhtiary, 2011; Bogaerts et al., 2011), and are safe under adequate supervision. Better balance and ambulation, independence, ability to perform daily activities are common desired outcomes when performing an exercise. But when there is an impairment of the loco motor system there is a tendency to avoid such challenges, therefore developing maximal voluntary force of muscles in the lower limbs is important (Lo et al., 2017).

All the described effects add information to specific rehabilitation programs, and are not dependent on the area that the person lives or other conditions such as weather or safety, which may affect the possibility of jogging or cycling.

5 Limitations

Caution should be taken when generalizing the results since the publications reviewed describe different sEMG hardware and software technology (acquiring, band-pass filtering and processing methods), diverse diseases and different WBVE treatment protocols.

Currently there is no consensus on the sEMG signal filtration and processing to recommend. This is a relevant point to compare effects between studies, since it limits the direct comparison of results and pooling of data in a metanalysis. Although the researchers have tried to retrieve all the publications with the selected keywords, it is not possible to affirm that all papers on this topic have been included; there may be articles that were not published in English and/or journals that were not indexed in the databases searched.

6 Conclusions

The WBVE may provoke muscular activation in lower limbs in populations with a medical condition. The use of sEMG is an adequate and proper tool to evaluate neuromuscular effects of these exercises. According to this systematic review, it appears that protocols with higher magnitude of effects (a_peak) provide significant muscle activation and increases blood circulation, being safe and well tolerated in these illnesses.

Putting together those findings, it can be affirmed that these exercises are an effective, safe and appropriate strategy recommended to elicit muscle activity and for the management of sequel, to amend bone, neuronal, muscle and vascular consequences of chronic illnesses that may or may not impose limbs misuse.

Regarding the use of the ISMNI recommendations of biomechanical parameters to WBVE, as well as ISEK or SENIAM orientations on sEMG, they are important measures to enhance quality of studies in the use of both techniques. Signal acquisition, raw signals filtering and processing in sEMG must be properly described, since results might differ with different methodologies.

It is important to determine the relationship between individual characteristics regarding genetics and epigenetics, biochemical factors, pathophysiology of diseases, individuals’ muscle and bone structure, and biomechanical parameters with therapy with WBVE. If other studies associating WBVE and sEMG are performed with non-healthy populations, it will be possible to determine the most adequate protocol to induce muscular activity during the treatments. These programs may take to other relevant outcomes, and demonstrate the behavior of mechanical vibrations in different conditions.

Therefore, the influence of WBVE in lower limbs of diseased individuals should be studied by sEMG to a greater extent.

Competing interests

The authors declare that there are not financial competing interests (political, personal, religious, ideological, academic, intellectual, commercial or any other) in relation to this manuscript.

Author’s Contributions

CFD, PLS, DSC, and MBF participated in the conception and design of the study, as well, preparing the manuscript. CD, PLS, DSC, and MBF coordinated the clinical approaches of the study. CFD, PLS, DSC performed the searches in the databases and aided in the selection of the papers to be discussed in the manuscript. EMM, DSM, EHFFF, EOGA, LLPD, PCP, RT, XC and PJM aided in the corrections of text, figures and tables. MBF has done the final version of the manuscript. MBF conceived the protocol, obtained funding and oversaw the study. All the authors read and approved the finalmanuscript.

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