Effects of muscle tendon vibration on balance after stroke: systematic review

ABSTRACT

After cerebrovascular accident (CVA), people have complex combinations of sensory, motor, cognitive, and emotional deficits, which can affect static and dynamic balance. This study aimed to compile and summarize the main features and findings of protocols used in research that investigated the effects of muscle tendon vibration on static and dynamic balance in adults with stroke. This is a systematic review, registered in PROSPERO (CRD42022303874), in which searches were performed in the databases PubMed, Cochrane, LILACS, SciELO, MEDLINE, Science Direct, and PEDro, during the month of January 2022, using the combination of keywords related to “stroke,” “balance,” “muscle tendon vibration,” “randomized controlled trial.” Methodological quality was assessed using the PEDro scale. A total of 1,560 studies were identified, 11 of which were included, between the years 1994 to 2020, involving 242 post-stroke adults. Only five studies used vibration as an intervention and found an improvement in static and dynamic balance. Six studies analyzed the interference of vibration on postural control, showing that balance was affected during the application of vibration and that individuals needed more time to recover or did not experience significant differences. We found that the effects of muscle tendon vibration may be able to improve balance in people with stroke and influence postural control by proprioceptive mechanisms of vibration. However, more studies of high methodological quality are needed to reach a consensus regarding muscle tendon vibration treatment protocols and their recommendation in clinical practice.

Keywords
Postural Control; Balance; Muscle Tendon Vibration

RESUMO

Após o acidente vascular cerebral (AVC), as pessoas apresentam combinações complexas de déficits sensoriais, motores, cognitivos e emocionais que podem afetar o equilíbrio estático e dinâmico. O objetivo do estudo foi compilar e resumir as principais características e achados de protocolos utilizados em pesquisas que investigaram os efeitos da vibração no tendão muscular no equilíbrio estático e dinâmico em adultos com AVC. Trata-se de uma revisão sistemática, registrada na PROSPERO (CRD42022303874), em que foram realizadas buscas nas bases de dados PubMed, Cochrane, LILACS, SciELO, MEDLINE, Science Direct e PEDro, durante o mês de janeiro de 2022, por meio da combinação de palavras-chave relacionadas a “stroke”, “balance”, “muscle tendon vibration” e “randomized controlled trial”. A qualidade metodológica foi avaliada através da escala PEDro. Foram identificados 1.560 estudos, dos quais 11 foram incluídos, publicados entre 1994 e 2020, envolvendo 242 adultos pós-AVC. Apenas cinco estudos utilizaram a vibração como intervenção e verificaram melhora no equilíbrio estático e dinâmico. Seis estudos analisaram a interferência da vibração no controle postural, observando que o equilíbrio foi afetado durante a aplicação da vibração e que os indivíduos precisaram de mais tempo para se recuperar ou não sofreram diferenças significativas. Verificou-se que os efeitos da vibração do tendão muscular podem melhorar o equilíbrio em pessoas com AVC e influenciar o controle postural através de mecanismos proprioceptivos da vibração. Entretanto, são necessários mais estudos de alta qualidade metodológica para atingir um consenso em relação aos protocolos de tratamento com vibração do tendão muscular e sua recomendação na prática clínica.

Descritores
Controle Postural; Equilíbrio; Vibração do Tendão Muscular

RESUMEN

Después del accidente cerebrovascular, las personas tienen combinaciones complejas de déficits sensoriales, motores, cognitivos y emocionales que pueden afectar el equilibrio estático y dinámico. El objetivo de este estudio fue recopilar y resumir las principales características y hallazgos de los protocolos utilizados en los estudios que investigaron los efectos de la vibración del tendón muscular sobre el equilibrio estático y dinámico en adultos con accidente cerebrovascular. Se trata de una revisión sistemática, registrada en PROSPERO (CRD420223874), en la que se realizaron búsquedas en las Bases de Datos PubMed, Cochrane, LILACS, SciELO, MEDLINE, Science Direct y PEDro, durante el mes de enero de 2022, mediante la combinación de palabras clave relacionadas con “stroke”, “balance”, “muscle tendon vibration” y “randomized controlled trial”. La calidad metodológica se evaluó mediante la escala PEDro. Se identificaron un total de 1.560 estudios, de los cuales se incluyeron 11, publicados entre 1994 y 2020, con 242 adultos después del accidente cerebrovascular. Solo cinco estudios utilizaron la vibración como intervención y verificaron la mejoría en el equilibrio estático y dinámico. Seis estudios analizaron la interferencia de la vibración en el control postural, señalando que el equilibrio se vio afectado durante la aplicación de la vibración y que los individuos necesitaron más tiempo para recuperarse o no sufrieron diferencias significativas. Se encontró que los efectos de la vibración del tendón muscular pueden mejorar el equilibrio en personas con accidente cerebrovascular e influir en el control postural a través de mecanismos propioceptivos de vibración. Sin embargo, se necesitan más estudios de alta calidad metodológica para llegar a un consenso con respecto a los protocolos de tratamiento con vibración del tendón muscular y su recomendación en la práctica clínica.

Palabras clave
Control Postural; Equilibrio; Vibración del Tendón Muscular

INTRODUCTION

A cerebrovascular accident (CVA), or stroke, consists of a cerebrovascular disease with clinical signs of focal (or global) brain function disorder, which develops rapidly and persists for more than 24 hours¹. Worldwide, stroke was considered the second leading cause of death and the third leading cause of disability in 2019². One of these disabilities is imbalance, affecting about 70% of stroke survivors, who report falling at home within one year after the stroke, and up to 15.9 out of every 1,000 people with stroke, who have falls daily^3,4.

Postural balance is the position in which an optimal distribution of body mass is achieved and that provides the body with stability and conditions for functionality in a stationary or moving position, with strategies that may include “reaction” (feedback), “anticipation” (feed-forward) or a combination of both⁵. Therefore, postural control represents a complex sensory-motor ability, whose body orientation is based on the internal representation of the body scheme derived from interactions between multiple sensorimotor processes, including peripheral and central components of the visual, somatosensory, and vestibular systems⁶.

However, post-stroke individuals present complex combinations of sensory, motor, cognitive, and emotional deficiencies that can affect static and dynamic balance⁷. In the uncompromised nervous system, descending supraspinatus control regulates spinal reflex activity, but, after stroke injuries, this supraspinatus control is interrupted. Thus, the affected threshold of the stretch reflex pathway and impaired reflex adaptations are observed in people after a stroke⁸. The balance impairment can increase the risk of falls, reduce the individual’s confidence in their mobility, decrease functional independence, activity, and participation, negatively impacting the quality of life⁹.

Therefore, several rehabilitation therapies have been used to improve the balance capacity of people who have had a stroke, for example, proprioceptive stimuli such as whole-body vibration (WBV). Reviews performed with WBV use, in which the individual stands or makes vigorous movements on a vibration platform placed on a static surface, indicated an improvement in the body balance of people with stroke in the short-term⁴ or with little effect^10,11. Another similar therapy is the use of Flexibar, a stick that when moved quickly with the hands reaches vibrations of approximately 5Hz, which are transferred to the arm and the rest of the body¹². Other procedures are more directed to a certain region of the body, such as muscle tendon vibration, in which a vibratory stimulus is applied to a specific muscle or to its tendon by a device¹³. In addition to facilitating muscle contraction, reducing spasticity, improving postural control and functional recovery, this technique stimulates proprioceptive afferent pathways, thus increasing the sensory influence on cortical motor control systems^9,14.

Although previous evidence has highlighted the use of WBV to improve balance, gait, and mobility outcomes^11,15, a systematic review of the findings and protocols used for the use of tendon vibration in post-stroke individuals is of scientific interest. To advance this theme, this systematic review aimed to compile and summarize the main characteristics and findings of protocols used in research that investigated the effects of muscle tendon vibration on static and dynamic balance in adults with stroke. The hypothesis of the study is that the use of WBV improves outcomes related to balance in adults with stroke.

METHODS

This is a systematic review based on the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines (^{Supplementary Material A}). For the methodological procedures, the recommendations of the Cochrane collaboration were followed to elaborate systematic reviews of intervention studies¹⁶. The review was recorded on the PROSPERO database (CRD42022303874), and the complete search strategy is available in ^{Supplemental Material B}.

During January 2022, the databases: PubMed, Cochrane Central Register of Controlled Trials, Latin America and the Caribbean Health Sciences Literature (LILACS), Scientific Electronic Library Online (SciELO), MEDLINE, Science Direct and Physiotherapy Evidence Database (PEDro) were searched. For the search structure, the PICO method (Population, Intervention, Comparison and Outcome) was used, with P: people with stroke; I: vibration of the muscular tendon; C: comparison between periods, group without vibration or other intervention; and O: static or dynamic balance outcome. Thus, the combination of keywords related to “stroke,” “balance,” “muscle tendon vibration” and “randomized controlled trial” was used for the research (^{Supplemental Material B}).

Inclusion criteria

Randomized clinical trials were included, both with randomized participants for an experimental group or a control group and with randomized participants for different experimental groups. There was no restriction of date of publication and language of the studies. Study participants, regardless of gender, should be older than 18 years, with clinical diagnosis of stroke, at any stage of the disease (acute, subacute, chronic). Studies that used muscle tendon vibration as an intervention, which had static or dynamic balance after the intervention as an outcome, which compared periods or groups without vibration in the muscular tendon, which compared muscle tendon vibration between people with and without stroke, and which compared muscle tendon vibration with another rehabilitation technique were also included.

Exclusion criteria

Exclusion criteria were: reviews, cohort studies or case-control; study protocols; studies published in books and as summaries of events; studies unavailable in full; and studies with duplicate information in another randomized clinical trial. Studies that analyzed other diseases or mixed population groups were excluded, except for those whose results were reported separately for each diagnosis. In this case, only the specific stroke results were included.

Selection of studies

The titles and abstracts were independently evaluated by two reviewers (PJV and AYS) according to the inclusion and exclusion criteria. Then, all studies potentially relevant to the evaluation were read in full. Rayyan free software¹⁷ was used to gather the results obtained in the databases and delete duplicate articles. Disagreements were resolved by consulting a third reviewer.

Data extraction

The information extracted included the characteristics of the study (author and year of publication) and the participants (sample size, gender, age, type of stroke and its stage), methodological details related to interventions (location of vibration, frequency, duration, balance assessment) and results (before, during and after the intervention, intra- or intergroup analysis). These data were extracted and presented in a table.

Assessment of the risk of bias (quality)

The risk of bias and methodological quality were evaluated by two evaluators (PJV and AYS), independently, using the PEDro scale. The items were classified as “yes” or “no” (receiving scores 1 or 0, respectively) according to the satisfaction analysis of each of them, thus, the total score ranged from 0 to 10, resulting in a PEDro score, in which: <4 was considered “bad,” 4 to 5 was “regular,” 6 to 8 was “good,” and 9 to 10 was “excellent” ⁽¹⁸.

RESULTS

The searches resulted in 1,560 articles, but 222 duplicate studies were excluded and another 1,322 after title and abstract analysis. Of the 16 studies selected for full reading, 5 were eliminated for not meeting the eligibility criteria, resulting in 11 articles included in this review, as shown in Figure 1.

Figure 1
Flowchart

After the analysis of the risk of bias (Table 1), all included studies presented a high risk of bias in one or more criteria, so that confidence in their result decreased substantially. Thus, the methodological quality ranged from 3 to 7, and six studies presented poor quality, three regular, and two good.

All clinical trials were published between 1994 and 2020 and, of these, 10 have been published in the last eight years. Note that different countries have conducted research using the muscle tendon vibration technique to investigate postural balance in people with stroke, most of them from France^7,23,24,26, followed by South Korea^20,22, Iran^9,25, Sweden¹⁹, Canada²¹, and Turkey²⁷.

Some of the studies analyzed the application of the muscle tendon vibration technique as a form of balance disturbance^7,19,23-25, whereas others as a proposal for balance rehabilitation^{9,20,22,26,27}. Vibration was used in different muscle tendons - fibular²³, tibialis anterior^7,20, plantar flexors of the foot^9,27, gluteus medius^7,24, posterior neck muscles^21,26 -, but mostly in the triceps surae^{7,19,20-23,25}. For the rehabilitation proposal, vibration was applied to the tendons of the plantar flexors^9,27, the triceps surae^20,22, and the posterior neck muscles²⁶. A total of 242 people with stroke participated in the clinical trials. Table 2 shows the characterization of the included studies.

Table 1
Bias risk analysis

Authors/Year	Criteria											Total
	1	2	3	4	5	6	7	8	9	10	11
Magnusson, Johansson, and Johansson, 199419	NO	YES	NO	NO	NO	NO	NO	NO	NO	YES	YES	3*/10
Bonan et al., 20137	YES	NO	NO	NO	NO	NO	NO	YES	NO	YES	YES	3/10
Lee, Cho, and Lee, 201320	NO	YES	YES	YES	NO	NO	YES	YES	NO	YES	YES	7*/10
Mullie and Duclos, 201421	NO	NO	NO	YES	NO	NO	NO	NO	NO	YES	YES	3/10
Afzal et al., 201522	YES	NO	NO	YES	NO	NO	NO	YES	NO	YES	YES	4/10
Duclos et al., 201523	YES	NO	NO	YES	NO	NO	NO	NO	NO	YES	YES	3/10
Bonan et al., 201724	YES	NO	NO	YES	NO	NO	NO	NO	NO	YES	YES	3/10
Karimi-AhmadAbadi et al., 20189	YES	NO	NO	YES	NO	NO	NO	YES	YES	YES	YES	5/10
Jamali et al., 201925	YES	NO	NO	YES	NO	NO	NO	NO	NO	YES	YES	3/10
Jamal et al., 202026	YES	NO	NO	YES	NO	NO	NO	YES	YES	YES	YES	5/10
Önal, Karaca, and Sertel, 202027	YES	YES	YES	YES	NO	NO	NO	YES	NO	YES	YES	6/10

• 1: non-specified eligibility criteria; 2: random allocation; 3: concealed allocation; 4: comparability of baseline; 5: blind subjects; 6: blind therapists; 7: blind assessors; 8: adequate follow-up (>85%); 9: analysis of the intention to treat; 10: statistical group-to-group comparisons; 11: point measures and variability measures.
• *Score provided by PEDro scale evaluators.

Table 2
Characterization of the included studies

Author/Year/Country	Groups	Characteristics of participants	Methodology	Parameters and vibration dosage	Evaluation	Results
Magnusson, Johansson, and Johansson, 199419	Healthy control group (n=23)	Sex: unreported	Application as balance disturbance: standing, eyes open and closed, use of vibrator in the tendon of the triceps surae muscle.	1st mode: five periods of vibration with frequencies of 20, 40, 60, 80, or 100Hz, and amplitude of 0.4mm.	Force platform.	The three groups showed no difference in equilibrium velocity and anteroposterior oscillation.
Sweden	CVA vibration/galvanic stimulation group (n=22)	Age: on average 74 years		2nd mode: constant frequency of 60Hz (PRBS programming) with pulses between 0.5 and 8sec. by 205sec., preceded by 30sec. rest.	Evaluation: before, during, and after vibration.	The CVA control group needed more time to reassume the initial balance after vibration than the other groups.
	CVA control group (n=26)	CVA stage: chronic
Bonan et al., 20137	CVA vibration group and control group (n=20)	Sex: 7F+13M;	Application as balance disturbance: standing, eyes open, with the use of perpendicular electromagnetic vibrators in the tibialis anterior and triceps surae tendons.	Frequency: 50Hz in the tibialis anterior and triceps surae and 90Hz in the gluteus medius, in this order and separately, with amplitude of 1mm.	Two force platforms with two inertia sensors (head and trunk).	About 65% of the subjects were sensitive to vibratory stimulation, which affected postural control.
France		Age: 51.4±10.5 years		Duration: 35sec., 1 session.	Evaluation: before, during, and after vibration.
		CVA stage: subacute
Lee, Cho, and Lee, 201320	CVA vibration group (n=16)	Sex: Vib.=3F+13M and Plac.=4F+11M	Application as intervention: weightlifting and weight change training in paretic LL with two vibrators fixed in the heel, in the triceps surae and tibialis anterior.	Frequency: 90Hz.	Force platform.	Significant improvement in balance in CVA vibration group.
South Korea	CVA placebo group (n=15)	Age: Vib.=53.31±8.37 years and Plac.=55.73±8.27 years		Amplitude: 15µm.	Rating: pre-test, one week before the start, and post-test, one day after the end.
		CVA stage: chronic		Duration: 30min./day, 3×/week, 6 weeks.
Mullie and Duclos, 201421	Healthy vibration group (n=12)	Sex: unreported	Application as balance disturbance: standing, eyes open, walking on the treadmill, using electromechanical vibrators in the posterior muscles of the neck and in the tendon of the triceps surae of the non-dominant/paretic side.	Mode: continuous or phasic (when heel was in contact with the ground).	Three-dimensional kinematic analysis of the whole body and the ground reaction force by using an instrumented treadmill.	The balance did not change during the gait in the CVA vibration group.
Canada	CVA vibration group (n=12)	Age: 47.8±11.8 years		Frequency: 80Hz.	Evaluation: before, during, and after vibration.
		CVA stage: not reported		Amplitude: 0.5 and 1mm.
				Duration: 1min., 1 session.
Afzal et al., 201522	Healthy vibration group (n=5)	Sex: 1F+3M	Application as intervention: use of Velcro belt with six vibrators attached between the knee and calf.	Modulation: CVMbp, CVMst, and PVMsr	Six meters walk test.	Significant improvement in the CVA vibration group in gait symmetry and gait speed.
South Korea	CVA vibration group (n=4)	Age: 64.75 years		Frequency: 200Hz.	Evaluation: before, during, and after vibration.
		CVA stage: chronic		Amplitude: 1.4G.
				Duration: time of the walk test 6m; 1 session.
Duclos et al., 201523	Healthy vibration group (n=20)	Sex: RBI=2F+10M and LBI=6F+8M	Application as balance disturbance: standing, eyes closed, with the use of perpendicular electromagnetic vibrators in the tibialis anterior and triceps surae tendons.	Application: separated, under three conditions (paretic, non-paretic, and bilateral limb).	Force platform.	Greater disturbance in the triceps surae tendon, and greater displacement in non-paretic LL than in the paretic.
France	CVA vibration group RBI (n=12) and LBI (n=14)	Age: RBI=69.2 years and LBI=65.4 years		Frequency: 80Hz.	Evaluation: before (4sec.), during, and after (24sec.) vibration.	RBI group suffered significant disruption and needed more time to restore balance.
		CVA stage: chronic		Amplitude: 0.2-0.5mm
				Duration: 20sec., 1 session.
Bonan et al., 201724	Healthy vibration group (n=40)	Sex: 16F+24M	Application as balance disturbance: standing, use of vibrator on the tendon of the non-paretic gluteus medius (right GM for left hemiparesis and left GM for right hemiparesis), maintained by a band around the waist.	Frequency: 90Hz.	Two force platforms.	Greater disturbance in the CVA vibration group on the right hemiparetic than on the left.
France	CVA vibration group in the right (n=21) and left (n=19) hemiparetic	Age: 54.7±10.6 years		Amplitude: 0.4mm.	Evaluation: initial and in the 4th and 6th week (session 2) after the first test (session 1).
		CVA stage: subacute		Duration: 35sec., 2 sessions.
Karimi-AhmadAbadi et al., 20189	Same placebo and vibration CVA group (n=22)	Sex: 8F+14M	Application as an intervention: in supine position, arms next to the torso, with flexed knees, and bare feet, supported and fastened with three Velcro straps on the upper surface of a box with two vibration panels, in the tendons of the plantar flexors of the ankle.	Frequency: 100Hz.	Mini-BESTest.	Significant improvement in balance in vibration group.
Iran		Age: 55.82±11.87 years		Duration: 5min., 1 session.	Evaluation before and immediately after placebo or active vibration.
		CVA stage: chronic
Jamali et al., 201925	Healthy vibration group (n=18)	Sex: LA and HA=4F+14 M	Application as balance disturbance: a pair of vibrators applied to the triceps surae tendon standing still and during a visual task of anticipation/virtual visual environment (they should avoid the collision of visual stimuli by moving the head and torso).	Frequency: 80Hz.	Force platform.	Significant reduction in the variability of postural oscillation in the healthy group.
Iran	CVA vibration group with low anxiety (LA) (n=18) and high anxiety (HA) (n=18)	Age: LA=55.11±10.93 years and HA=51.89±10.90 years		Amplitude: 0.3mm	Evaluation: before, during, and after vibration.	CVA LA needed more time to restore balance and CVA HA required even more time.
		CVA stage: chronic		Duration: 60sec. for each condition, 1 session.
Jamal et al., 202026	CVA vibration group with RBI (n=16) and LBI (n=16)	Sex: 6F+26M	Application as an intervention: seated and blindfolded, with vibrator device manually positioned by the examiner in the tendons of the neck muscles (semispinalis and splenius); site depended on the side of the lesion: left on RBI and right on LBI.	Frequency: 80Hz.	Two force platforms, BBE and TUG	Significant improvement in balance in both groups.
France		Age: 60.9±10 years		Amplitude: 0.4mm.	Evaluation: two weeks before, immediately before the 1st intervention, one week and one month after.
		CVA stage: chronic		Duration: 10min., 5 sessions/week, 2 weeks.
Önal, Karaca, and Sertel, 202027	CVA vibration group (n=15)	Sex: 7F+23M	Application as intervention: in supine position, using a vibration device in both plantar regions.	Frequency: 80Hz for 10sec. and 5sec. of rest.	Biodex balance system.	Immediate significant improvement in the vibration group.
Turkey	CVA placebo group (n=15)	Age: on average 58 years		Duration: 15min., 1 session.	Evaluation: before the intervention and up to 5min. after.
		CVA stage: chronic

• CVA: stroke; BBE: Berg balance scale; F: female; G: acceleration of gravity; GM: gluteus medius; Hz: Hertz; RBI: right brain injury; LBI: left brain injury; M: male; LL: lower limb; μm: micrometer; mm: millimeter; min.: minute; CVMbp: constant vibration mode of balance phase; CVMst: constant vibration mode of matching support time; PVMsr: proportional vibration mode of matching symmetry ratio; Plac.: placebo; PRBS: pseudorandom binary sequence programming; sec.: seconds; TUG: timed up and go test; Vib.: vibration.

DISCUSSION

Characterization of the studies

In this systematic review, studies from different countries and with different forms and regions of application of muscle tendon vibration were identified, allowing the determination of the main characteristics of protocols used in research investigating the stability of body balance in people with stroke after the application of muscle tendon vibration. However, due to the high risk of bias, outcomes related to the efficacy of this method as a rehabilitation resource to improve postural balance should be interpreted with caution.

In view of the recovery process approached by Bernhardt et al. ⁽²⁸, of the studies that reported the characterization of stroke patients, most were in the chronic stage of stroke (more than six months), and only in two studies the participants were in the subacute stage^7,24. Regarding the age of the participants, they were over 41 years old, most being in the 50-year-old age group^{7,9,20,24,25,27}. All studies showed a larger male population, which corroborates the study by Bensenor et al. ⁽²⁹, in which the punctual prevalence was 1.6% in men and 1.4% in women, and disability was 29.5% in men and 21.5% in women.

Vibration devices: application location and positioning of vibrators

The muscular tendon in which vibration was applied was not standardized in view of the two proposals: verifying the influence of proprioceptive mechanisms on the outcome of postural balance and, as an intervention strategy, improving postural balance.

When used to produce vibration interferences in postural control, the sites were chosen to provoke different amplitudes of instability in different directions: anteroposterior or mediolateral. Vibrations in the triceps surae^{7,19,21,23,25}, for example, may result in a backward postural response. Mulie and Duclos²¹ observed in a study that individuals were inclined towards the posterior direction during the vibration of the triceps surae. This can be explained by the fact that vibration is generally interpreted by the kinesthetic illusion of stretching of the vibrated muscle and the back-up compensatory reaction generated to restore body posture³⁰. Unlike the tibialis anterior tendon⁷, which causes an illusion of inclination to the back of the body, causing the subjects to tilt forward in a corresponding way to correct the perceived inclination³¹.

Fibular tendon vibration was applied in only one study²³, being the least used. This is because the vibration in this tendon causes a relatively small posterior displacement compared with the vibration of the triceps surae tendon³², which is insufficient to stimulate muscle stretching and induce a postural control reaction³³.

In addition, vibrations can generate lateral displacement in the paretic limb in individuals with stroke. According to Biger et al. ⁽³⁴, the neck muscles are directly linked to the vestibular and oculomotor systems and can play a crucial role in the perception of the body in space. Thus, when applying vibration in these muscles, the information obtained from proprioceptive receptors, alongside that of the oculomotor muscles and vestibular system, is involved in the location of objects in relation to the body and, consequently, in the balance of the individual²⁶. Thus, neck muscle vibrations can reduce lateral body weight asymmetry in individuals with hemiparesis. The same happens for vibratory stimulation in the tendon of the middle gluteus since in the standing position the pressure center is laterally displaced for the duration of the vibration, which produces the perception of a strong push at the level of the vibrated hip in the opposite direction³⁵ and, consecutively, the placement of more weight in the paretic leg^7,24. This can both interfere with balance proprioception²¹ and improve postural balance, as seen in the study by Jamal et al. ⁽²⁶.

However, for Liang et al. ⁽⁸, afferents of the plantar region of the foot and the motor neurons that supply the leg muscles show a strong synaptic coupling between, thus, the afferents inputs mediate their effect on motor functions by modulating the excitability of the motor cortex, being more effective in balance, as observed in the studies by Karimi-AhmadAbadi et al. ⁽⁹ and Önal, Karaca and Sertel²⁷ after applying vibration to plantar foot flexors as a balancing intervention.

The application forms were based on positioning the device on the muscle tendon or attaching it to the spot by a band around the waist²⁴, a Velcro belt²², or three Velcro straps on the top surface of a box with two panels, one for each foot, to apply vibratory stimulation⁹. Whereas one study used a vibrator device manually positioned by the examiner in the neck muscles²⁶, and another used manually adjusted electromagnetic vibrators perpendicular to the muscle tendon⁷.

Frequency of vibration, dosage, and application time

Dosage and application time are effective measures to achieve the best response to a given treatment. The two main parameters for defining the dosage include amplitude, which is the extent of oscillatory motion (peak-to-peak displacement in mm), and vibration frequency, which consists of the repetition rate of oscillation cycles. Studies indicate that the amplitude should be from 0.2 to 0.5mm, since a higher value tends to lead to the stimulus overflowing to the surrounding muscles and bones^36,37, which corroborates the use of this amplitude in most included studies^7,19,23-26. However, one study²⁰ used a lower amplitude of vibration in the muscular tendon: 15μm, which corresponds to 0.015mm. Although most studies used amplitude by displacement (mm), Afzal et al. ⁽²² applied it as gravity acceleration (G). Both are important units of measurement since the relationship between amplitude and acceleration depends on frequency, and the lower the frequency, the higher the peak-to-peak amplitude for a given peak-to-peak acceleration³⁸.

In the studies included in this review, the frequency ranged from 20Hz to 200Hz, but most used the application at 80Hz^21,23,25-27. According to Kavounoudias, Roll, and Roll³⁹, when vibration is applied to a frequency above 80Hz, it can generate specific electromyographic (EMGs) activities, followed by full-body oriented inclinations, whose direction is always opposite and whose amplitude varies linearly with the frequency of vibration. Thus, when generating an afferent signal, a postural reaction occurs to “restore” muscle length and avoid illusory fall, which corroborates the findings of these studies, which mostly used this frequency.

According to Duclos et al. ⁽³², at least 16 seconds of vibration are necessary to induce most postural effects in young adults, regardless of the vibration condition. However, the literature shows no support to indicate the time necessary to cause central sensory adaptations for the population after stroke, but, due to reduced motor production, they are slower and deficient regarding correction forces and present greater oscillation⁷. Of the studies included in this review that reported vibration time, most applied the vibration for more than 20 seconds^7,21,23-25.

Regarding the dosage of the intervention with muscle tendon vibration, the studies diverged, and dosages ranged from 18 sessions in six weeks²⁰, 10 sessions in two weeks²⁶, to only a single session^9,22,27. These studies only carried out a short-term assessment, which means that the results may not persist when verified in the long term, and a greater number of sessions are required.

Main results

Studies that analyzed the interferences of vibration in postural control observed that the participants had the balance affected during the application of vibration⁷ and needed more time to recover²⁵ or did not suffer significant differences¹⁹. The studies that separated the sample regarding the side of the brain injury observed that the time of balance recovery was longer when the lesion was on the right^23,24, with a stronger disturbance in the non-paretic hemibody²³. This is because an injury in the right hemisphere can induce a pronounced interruption in the processing of spatial information, impair the internal representation of the body in space, and induce distortions in the coordinates used to distribute body weight across the two lower limbs while standing⁴⁰. In addition, muscle tendon vibration was unable to disturb balance when analyzed during gait in most participants with stroke²¹. Therefore, tendon vibration is a useful tool to disturb proprioception in specific muscles - especially on the paretic side, in which somatosensory impairments are greater - considering that vibratory stimuli increase the sensitivity of the stretch reflex, stimulate cutaneous and proprioceptive receptors and afferent nerves and therefore generate positive effects on the sensory system, on neuromuscular responses and on the improvement of the central nervous system’s ability to process signals⁹.

Only five studies used muscle tendon vibration as an intervention and verified a possible improvement in balance^9,20,26,27, even during gait²². In individuals with hemiparesis, the selectivity of sensory information of the paretic limb is reorganized and, in the acute stage of the stroke, they may become unable or reluctant to bear weight on the paretic side due to weakness, impaired motor control, impaired proprioception, or erroneous perception of orientation^23,41,42. Therefore, in the chronic stages of a stroke, hemiparesis may cause disuse of the paretic limb, despite the improvement of motor function in the lower limb.

The balance deficit results from the asymmetry of body weight distribution characterized by unaffected leg overload and paretic leg underload and increased oscillation of the center of pressure⁴³. However, obtaining good results for the outcome of postural control in post-stroke individuals is possible, since vibration has been shown to activate and alter the central mechanisms in the nervous system impaired by stroke and, thus, improve motor functions, probably by the increased somatosensory cortex activity⁹. Thus, the vibration of the muscular tendon can reduce sensory loss and play an important role in somatosensory integration, mainly due to the increased sensation of the paretic side, which causes the transfer of weight to the paretic side to increase and provides a symmetrical weight transfer^20,44, which corroborates the improvement of balance in the chronic stages of a stroke, as verified in the five studies^{9,20,22,26,27}.

The muscle tendon vibration affects the reduction of balance deficit in individuals after stroke - a condition related to severe physical impairments, disability, and low quality of life - decreasing the rates of falls, which represent a great burden for these individuals, their families, and the society⁴⁵.

Limitations

In view of this review, precautions are needed regarding the conclusions drawn, due to the small number of studies included, low sample number, and methodologies with high risk of bias. In addition, the studies were heterogeneous, with different sites of application, dosages, and duration of vibration in the muscular tendon, which made the meta-analysis in this study impossible. Therefore, further studies of high methodological quality are necessary to achieve more conclusive results.

CONCLUSION

The effects of muscle tendon vibration can benefit static balance, decreasing postural oscillation, and dynamic balance, improving cadence, step length and increasing unipedal support time in gait in adults with stroke. In addition, they can influence postural control by proprioceptive vibration mechanisms. However, more high methodological quality studies are needed to establish a consensus regarding treatment protocols and their recommendation in clinical practice.

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• 4
  Work carried out at the Universidade Estadual do Norte do Paraná (UENP), Campus Jacarezinho, Centro de Ciências da Saúde, Jacarezinho (PR), Brazil.
• 5
  Financing source: nothing to declare

SUPPLEMENTARY MATERIAL A

Section and topic Item # Checklist item Location where item is reported Title Title 1 Identify the report as a systematic review. Page 1 Abstract Abstract 2 See the PRISMA 2020 for Abstracts checklist. Page 4-5 Introduction Rationale 3 Describe the rationale for the review in the context of existing knowledge. Page 7 Objectives 4 Provide an explicit statement of the objective(s) or question(s) the review addresses. Page 7 Methods Eligibility criteria 5 Specify the inclusion and exclusion criteria for the review and how studies were grouped for the syntheses. Page 8 Information sources 6 Specify all databases, registers, websites, organisations, reference lists and other sources searched or consulted to identify studies. Specify the date when each source was last searched or consulted. Page 7 Search strategy 7 Present the full search strategies for all databases, registers and websites, including any filters and limits used. Page 28 Selection process 8 Specify the methods used to decide whether a study met the inclusion criteria of the review, including how many reviewers screened each record and each report retrieved, whether they worked independently, and if applicable, details of automation tools used in the process. Page 8 Data collection process 9 Specify the methods used to collect data from reports, including how many reviewers collected data from each report, whether they worked independently, any processes for obtaining or confirming data from study investigators, and if applicable, details of automation tools used in the process. Page 8-9 Data items 10a List and define all outcomes for which data were sought. Specify whether all results that were compatible with each outcome domain in each study were sought (e.g. for all measures, time points, analyses), and if not, the methods used to decide which results to collect. Page 8 10b List and define all other variables for which data were sought (e.g. participant and intervention characteristics, funding sources). Describe any assumptions made about any missing or unclear information. Page 8 Study risk of bias assessment 11 Specify the methods used to assess risk of bias in the included studies, including details of the tool(s) used, how many reviewers assessed each study and whether they worked independently, and if applicable, details of automation tools used in the process. Page 9 Effect measures 12 Specify for each outcome the effect measure(s) (e.g. risk ratio, mean difference) used in the synthesis or presentation of results. Page 10-11 Synthesis methods 13a Describe the processes used to decide which studies were eligible for each synthesis (e.g. tabulating the study intervention characteristics and comparing against the planned groups for each synthesis (item #5)). Page 8 13b Describe any methods required to prepare the data for presentation or synthesis, such as handling of missing summary statistics, or data conversions. Page 8-9 13c Describe any methods used to tabulate or visually display results of individual studies and syntheses. Page 9 13d Describe any methods used to synthesize results and provide a rationale for the choice(s). If meta-analysis was performed, describe the model(s), method(s) to identify the presence and extent of statistical heterogeneity, and software package(s) used. Page 8 13e Describe any methods used to explore possible causes of heterogeneity among study results (e.g. subgroup analysis, meta-regression). - 13f Describe any sensitivity analyses conducted to assess robustness of the synthesized results. - Reporting bias assessment 14 Describe any methods used to assess risk of bias due to missing results in a synthesis (arising from reporting biases). Page 9 Certainty assessment 15 Describe any methods used to assess certainty (or confidence) in the body of evidence for an outcome. Page 9 Results Study selection 16a Describe the results of the search and selection process, from the number of records identified in the search to the number of studies included in the review, ideally using a flow diagram. Page 9 and 10 16b Cite studies that might appear to meet the inclusion criteria, but which were excluded, and explain why they were excluded. Page 10 Study characteristics 17 Cite each included study and present its characteristics. Page 13-16 Risk of bias in studies 18 Present assessments of risk of bias for each included study. Page 11 Results of individual studies 19 For all outcomes, present, for each study: (1) summary statistics for each group (where appropriate) and (2) an effect estimate and its precision (e.g. confidence/credible interval), ideally using structured tables or plots. - Results of syntheses 20a For each synthesis, briefly summarise the characteristics and risk of bias among contributing studies. Page 13-16 20b Present results of all statistical syntheses conducted. If meta-analysis was done, present for each the summary estimate and its precision (e.g. confidence/credible interval) and measures of statistical heterogeneity. If comparing groups, describe the direction of the effect. - 20c Present results of all investigations of possible causes of heterogeneity among study results. Page 13-16 20d Present results of all sensitivity analyses conducted to assess the robustness of the synthesized results. - Reporting biases 21 Present assessments of risk of bias due to missing results (arising from reporting biases) for each synthesis assessed. Page 11 Certainty of evidence 22 Present assessments of certainty (or confidence) in the body of evidence for each outcome assessed. Page 17-21 Discussion Discussion 23a Provide a general interpretation of the results in the context of other evidence. Page 17 23b Discuss any limitations of the evidence included in the review. Page 22 23c Discuss any limitations of the review processes used. Page 22 23d Discuss implications of the results for practice, policy, and future research. Page 22 Other information Registration and protocol 24a Provide registration information for the review, including register name and registration number, or state that the review was not registered. Page 7 24b Indicate where the review protocol can be accessed, or state that a protocol was not prepared. Page 7 24c Describe and explain any amendments to information provided at registration or in the protocol. Page 7 Support 25 Describe sources of financial or non-financial support for the review, and the role of the funders or sponsors in the review. Page 22 Competing interests 26 Declare any competing interests of review authors. Page 22 Availability of data, code and other materials 27 Report which of the following are publicly available and where they can be found: template data collection forms; data extracted from included studies; data used for all analyses; analytic code; any other materials used in the review. Page 7 Source: Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71. doi: 10.1136/bmj.n71. For more information, visit: http://www.prisma-statement.org/.

Section and topic	Item #	Checklist item	Location where item is reported
Title
Title	1	Identify the report as a systematic review.	Page 1
Abstract
Abstract	2	See the PRISMA 2020 for Abstracts checklist.	Page 4-5
Introduction
Rationale	3	Describe the rationale for the review in the context of existing knowledge.	Page 7
Objectives	4	Provide an explicit statement of the objective(s) or question(s) the review addresses.	Page 7
Methods
Eligibility criteria	5	Specify the inclusion and exclusion criteria for the review and how studies were grouped for the syntheses.	Page 8
Information sources	6	Specify all databases, registers, websites, organisations, reference lists and other sources searched or consulted to identify studies. Specify the date when each source was last searched or consulted.	Page 7
Search strategy	7	Present the full search strategies for all databases, registers and websites, including any filters and limits used.	Page 28
Selection process	8	Specify the methods used to decide whether a study met the inclusion criteria of the review, including how many reviewers screened each record and each report retrieved, whether they worked independently, and if applicable, details of automation tools used in the process.	Page 8
Data collection process	9	Specify the methods used to collect data from reports, including how many reviewers collected data from each report, whether they worked independently, any processes for obtaining or confirming data from study investigators, and if applicable, details of automation tools used in the process.	Page 8-9
Data items	10a	List and define all outcomes for which data were sought. Specify whether all results that were compatible with each outcome domain in each study were sought (e.g. for all measures, time points, analyses), and if not, the methods used to decide which results to collect.	Page 8
	10b	List and define all other variables for which data were sought (e.g. participant and intervention characteristics, funding sources). Describe any assumptions made about any missing or unclear information.	Page 8
Study risk of bias assessment	11	Specify the methods used to assess risk of bias in the included studies, including details of the tool(s) used, how many reviewers assessed each study and whether they worked independently, and if applicable, details of automation tools used in the process.	Page 9
Effect measures	12	Specify for each outcome the effect measure(s) (e.g. risk ratio, mean difference) used in the synthesis or presentation of results.	Page 10-11
Synthesis methods	13a	Describe the processes used to decide which studies were eligible for each synthesis (e.g. tabulating the study intervention characteristics and comparing against the planned groups for each synthesis (item #5)).	Page 8
	13b	Describe any methods required to prepare the data for presentation or synthesis, such as handling of missing summary statistics, or data conversions.	Page 8-9
	13c	Describe any methods used to tabulate or visually display results of individual studies and syntheses.	Page 9
	13d	Describe any methods used to synthesize results and provide a rationale for the choice(s). If meta-analysis was performed, describe the model(s), method(s) to identify the presence and extent of statistical heterogeneity, and software package(s) used.	Page 8
	13e	Describe any methods used to explore possible causes of heterogeneity among study results (e.g. subgroup analysis, meta-regression).	-
	13f	Describe any sensitivity analyses conducted to assess robustness of the synthesized results.	-
Reporting bias assessment	14	Describe any methods used to assess risk of bias due to missing results in a synthesis (arising from reporting biases).	Page 9
Certainty assessment	15	Describe any methods used to assess certainty (or confidence) in the body of evidence for an outcome.	Page 9
Results
Study selection	16a	Describe the results of the search and selection process, from the number of records identified in the search to the number of studies included in the review, ideally using a flow diagram.	Page 9 and 10
	16b	Cite studies that might appear to meet the inclusion criteria, but which were excluded, and explain why they were excluded.	Page 10
Study characteristics	17	Cite each included study and present its characteristics.	Page 13-16
Risk of bias in studies	18	Present assessments of risk of bias for each included study.	Page 11
Results of individual studies	19	For all outcomes, present, for each study: (1) summary statistics for each group (where appropriate) and (2) an effect estimate and its precision (e.g. confidence/credible interval), ideally using structured tables or plots.	-
Results of syntheses	20a	For each synthesis, briefly summarise the characteristics and risk of bias among contributing studies.	Page 13-16
	20b	Present results of all statistical syntheses conducted. If meta-analysis was done, present for each the summary estimate and its precision (e.g. confidence/credible interval) and measures of statistical heterogeneity. If comparing groups, describe the direction of the effect.	-
	20c	Present results of all investigations of possible causes of heterogeneity among study results.	Page 13-16
	20d	Present results of all sensitivity analyses conducted to assess the robustness of the synthesized results.	-
Reporting biases	21	Present assessments of risk of bias due to missing results (arising from reporting biases) for each synthesis assessed.	Page 11
Certainty of evidence	22	Present assessments of certainty (or confidence) in the body of evidence for each outcome assessed.	Page 17-21
Discussion
Discussion	23a	Provide a general interpretation of the results in the context of other evidence.	Page 17
	23b	Discuss any limitations of the evidence included in the review.	Page 22
	23c	Discuss any limitations of the review processes used.	Page 22
	23d	Discuss implications of the results for practice, policy, and future research.	Page 22
Other information
Registration and protocol	24a	Provide registration information for the review, including register name and registration number, or state that the review was not registered.	Page 7
	24b	Indicate where the review protocol can be accessed, or state that a protocol was not prepared.	Page 7
	24c	Describe and explain any amendments to information provided at registration or in the protocol.	Page 7
Support	25	Describe sources of financial or non-financial support for the review, and the role of the funders or sponsors in the review.	Page 22
Competing interests	26	Declare any competing interests of review authors.	Page 22
Availability of data, code and other materials	27	Report which of the following are publicly available and where they can be found: template data collection forms; data extracted from included studies; data used for all analyses; analytic code; any other materials used in the review.	Page 7

• Source: Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71. doi: 10.1136/bmj.n71.
• For more information, visit: http://www.prisma-statement.org/.

SUMPLEMENTAR MATERIAL B

Database search formulation - PubMed (121 results)

A. Condition of the disease: CVA

• (1) Stroke

• (2) Post-stroke

• (3) After stroke

• (4) Cerebrovascular disorders

• (5) Hemiparetic stroke

• (6) Hemiplegia

• (7) Brain ischemia

#1 OR #2 OR #3 OR #4 OR #5 OR #6 OR #7

B. Outcome: Balance

• (8) Balance

• (9) Postural balance

• (10) Postural control

• (11) Equilibrium

• (12) Sway

#8 OR #9 OR #10 OR #11 OR #12

C. Intervention:

• (13) Sensory feedback

• (14) Vibrotactile feedback

• (15) Vibratory feedback

• (16) Tendon vibration

• (17) Neck muscle vibration

• (18) Localized muscle vibration

• (19) Muscle tendon vibration

• (20) Vibration

• (21) Focal vibration

• (22) Focal Muscle Vibration

#13 OR #14 OR #15 OR #16 OR #17 OR #18 OR #19 OR #20 OR #21 OR #22

D. Study design:

• (23) Randomized controlled trial

• (24) Randomised controlled trial

• (25) Controlled clinical trial

• (26) Comparative study

• (27) Randomized

• (28) Randomly

• (29) Placebo

• (30) Control groups

• (31) Random allocation

• (32) Trial

• (33) Groups

#23 OR #24 OR #25 OR #26 OR #27 OR #28 OR #29 OR #30 OR #31 OR #32 OR #33

Database search formulation - Cochrane Central Register of Controlled Trials (CENTRAL) (110 results)

#1: Stroke OR post-stroke OR after stroke OR Cerebrovascular Disorders OR Hemiparetic Stroke OR Hemiplegia OR Brain Ischemia

#2: Balance OR postural balance OR postural control OR equilibrium OR Sway

#3: sensory feedback OR vibrotactile feedback OR vibratory feedback OR Tendon vibration OR Neck muscle vibration OR Localized muscle vibration OR muscle tendon vibration OR Vibration OR focal vibration OR Focal Muscle Vibration

Database search formulation - LILACS (3 results)

#1: Stroke OR post-stroke OR after stroke OR Cerebrovascular Disorders OR Hemiparetic Stroke OR Hemiplegia OR Brain Ischemia

#2: Balance OR postural balance OR postural control OR equilibrium OR Sway

#3: sensory feedback OR vibrotactile feedback OR vibratory feedback OR Tendon vibration OR Neck muscle vibration OR Localized muscle vibration OR muscle tendon vibration OR Vibration OR focal vibration OR Focal Muscle Vibration

#1 AND #2 AND #3

Database search formulation - MEDLINE (0 results)

#1: Stroke OR post-stroke OR after stroke OR Cerebrovascular Disorders OR Hemiparetic Stroke OR Hemiplegia OR Brain Ischemia

#2: Balance OR postural balance OR postural control OR equilibrium OR Sway

#3: sensory feedback OR vibrotactile feedback OR vibratory feedback OR Tendon vibration OR Neck muscle vibration OR Localized muscle vibration OR muscle tendon vibration OR Vibration OR focal vibration OR Focal Muscle Vibration

#4: randomized controlled trial OR randomised controlled trial OR controlled clinical trial OR comparative study OR randomized OR randomly OR placebo OR control groups OR Random Allocation OR trial OR groups

#1 AND #2 AND #3 AND #4

Database search formulation - PEDro (42 results)

Abstract & Title: vibration AND stroke

Therapy: no selection

Problem: no selection

Body part: no selection

Subdiscipline: neurology

Method: clinical trial

When searching: match all search terms (AND)

Database search formulation - ScienceDirect (1,284 results)

(Stroke OR Hemiplegia) AND (Balance OR postural control OR equilibrium OR Sway) AND (vibratory feedback OR Tendon vibration) AND (trial)

Database search formulation - SciELO (0 results)

#1: “Stroke” OR “post-stroke” OR “after stroke” OR “Cerebrovascular Disorders” OR “Hemiparetic Stroke” OR “Hemiplegia” OR “Brain Ischemia”

#2: “Balance” OR “postural balance” OR “postural control” OR “equilibrium” OR “Sway”

#3: “sensory feedback” OR “vibrotactile feedback” OR “vibratory feedback” OR “Tendon vibration” OR “Neck muscle vibration” OR “Localized muscle vibration” OR “muscle tendon vibration” OR “Vibration” OR “focal vibration” OR “Focal Muscle Vibration”

#4: “randomized controlled trial” OR “randomised controlled trial” OR “controlled clinical trial” OR “comparative study” OR “randomized” OR “randomly” OR “placebo” OR “control groups” OR “Random Allocation” OR “trial” OR “groups”

Database search formulation - Scopus (0 results)

( TITLE-ABS-KEY ( stroke OR post-stroke OR after AND stroke OR cerebrovascular AND disorders OR hemiparetic AND stroke OR hemiplegia OR brain AND ischemia ) AND TITLE-ABS-KEY ( balance OR postural AND balance OR postural AND control OR equilibrium OR sway ) AND TITLE-ABS-KEY ( sensory AND feedback OR vibrotactile AND feedback OR vibratory AND feedback OR tendon AND vibration OR neck AND muscle AND vibration OR localized AND muscle AND vibration OR muscle AND tendon AND vibration OR vibration OR focal AND vibration OR focal AND muscle AND vibration ) )

No documents were found.

Publication Dates

• Publication in this collection
  05 Dec 2022
• Date of issue
  Jul-Sep 2022

History

• Received
  09 June 2022
• Accepted
  09 Aug 2022