Effects of vibration on spasticity in individuals with spinal cord injury: a scoping systematic review.

Authors: Mahsa Sadeghi, MD Bonita Sawatzky, PhD

Spasticity

Affiliations: From the Departments of Medicine (MS) and Orthopaedics (BS), University of British Columbia, Vancouver, British Columbia, Canada; and International Collaboration on Repair Discoveries, Vancouver, British Columbia, Canada (MS, BS).

Correspondence: All correspondence and requests for reprints should be addressed to Bonita Sawatzky, PhD, Orthopaedics/ICORD, University of British Columbia, 818 West 10th Ave, Vancouver, British Columbia, Canada V5Z 1M9.

Disclosures: Funded in part by Natural Sciences and Engineering Research Council of Canada (NSERC). Financial disclosure statements have been obtained, and no conflicts of interest have been reported by the authors or by any individuals in control of the content of this article.

0894-9115/14/9311-0995 American Journal of Physical Medicine & Rehabilitation Copyright * 2014 by Lippincott Williams & Wilkins DOI: 10.1097/PHM.0000000000000098

LITERATURE REVIEW

Effects of Vibration on Spasticity in Individuals with Spinal Cord Injury A Scoping Systematic Review ABSTRACT Sadeghi M, Sawatzky B: Effects of vibration on spasticity in individuals with spinal cord injury: a scoping systematic review. Am J Phys Med Rehabil 2014;93:995Y1007. The objective of this systematic review was to evaluate how whole-body vibration (WBV) or focal vibration (FV) would change spasticity in individuals with spinal cord injury (SCI). A search was conducted of MEDLINE, EMBASE, CINAHL, and PsycINFO electronic databases. A hand search was conducted of the bibliographies of articles and journals relevant to the research question. The inclusion criteria were three or more individuals, 17 yrs or older, with SCI who experience spasticity, and WBV or FV application. The evidence level of all ten identified studies (195 SCI subjects) was low on the basis of Centre for Evidence Based Medicine level of evidence. WBV (n = 1) and FV (n = 9) were applied to assess the effects of vibration on different measures of spasticity in individuals with SCI. FV application resulted in a short-term spasticity reduction lasting for a maximum of 24 hrs. Neurophysiologic measures showed H-reflex inhibition in individuals with SCI after FV application. WBV resulted in a decrease in spasticity lasting for 6Y8 days after the last vibration session. WBV and FV might decrease spasticity for a short period, but no evidence-based recommendation can be drawn from the literature to guide rehabilitation medicine clinicians to manage spasticity with vibration application. Key Words:

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Muscle Spasticity, Vibration, Spinal Cord Injury, Spasm

Vibration Changes Spasticity in Patients with SCI Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

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pasticity, defined by Lance,1 is Ba velocitydependent increase in muscle tone with exaggerated tendon jerks, resulting from hyperexcitability of the stretch reflex.[ Although the definition of Lance has been accepted widely, there is discrepancy within the literature for the precise definition of spasticity.1Y6 Although spasticity is described specifically as an increased muscle tone, there are some other symptoms such as clonus, hyperactive tendon reflexes, and spasms that are included within the original definition by Lance.1,2,4Y6 Spasticity is a result of hyperexcitable stretch reflex in the spinal cord, but spasms are involuntary muscle contractions caused by hyperexcitable or disinhibited spinal reflexes such as flexor withdrawal reflexes.3 Individuals with spinal cord injury (SCI) experience significant challenges with spasticity during their daily routine.2 It is estimated that 67%Y78% of individuals with SCI experience spasticity at rehabilitation hospital discharge and follow-up.2 Spasticity can degrade quality-of-life by causing pain and fatigue, contributing to the development of contractures, pressure ulcers, infection, and negative selfimage, and may interfere with a wheelchair user’s seating, transfers, and wheeling.2,7 Spasticity management in individuals with SCI involves a wide range of approaches including antispastic pharmaceuticals given orally, through injections, or intrathecally. Medications produce a nontargeted release of pharmacologic agents, which results in a general suppression of neuronal activity in a population that already experiences reduced voluntary drive.7 In addition, these medications have unwanted pharmacologic-induced side effects. Potential side effects vary between medications but may include muscle weakness, sedation, drowsiness, dizziness, ataxia, hallucination, depression, hypotension, liver toxicity, and possible addiction.7 Botulinum toxin (Botox A) is an injectable neurotoxin that blocks the acetylcholine transfer across the neuromuscular junction, causing a weakness in that muscle. However, because of the eventual sprouting of new nervelets, the effect of Botox is not permanent.7Y9 A surgical technique known as the rhizotomy is an invasive approach with surgical risks along with significant weakness as a result of the muscle nerves being cut and usually reserves for spasticity complications such as contracture.10,11 The least invasive method involves physical therapy techniques, and these are often considered adjuvant essentials in the management of spasticity because these are often used to complement the pharmacologic and surgical strategies.12,13 The

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techniques include a wide range of treatments such as positioning, muscle strengthening, stretching, weight-bearing techniques, electrical stimulation, vibration, cold/heat application, splinting, and orthoses.7,14 The physical therapy techniques are intended to maintain the muscle length, prevent contractures, and change mechanical properties of the musculoskeletal system and change plasticity within the central nervous system.7 Both wholebody vibration (WBV) and focal vibration (FV) have been used for spasticity management in individuals with SCI.15Y20 In normal spinal pathways, prolonged muscle tendon vibration (30 secs to 15 mins) results in decreased resting discharge rate of the sensory receptors (muscle spindles) and decreased short latency of stretch reflex of lower extremity muscles.21Y23 These mechanisms are mainly caused by lower excitatory sensory inputs by Ia afferent neurons to the spinal cord and, consequently, lower activity of motor units during muscle contractions.21Y23 Vibration effects on Ia afferent neuron discharge might modulate motor units and muscle activity.21Y23 Although it is unknown how vibration, either WBV or FV, would change muscle spasticity, lower Ia afferent neuron discharge might be a decisive responsible mechanism. Although there is some literature to support the use of either WBV or FV for spasticity management in individuals with SCI, it is still not fully understood or adopted into clinical practice guidelines for spasticity management in SCI. For example, the appropriate frequency range, magnitude, or durations are largely unknown. In addition to the variables described above, understanding the difference between WBV and FV is important because WBV devices typically provide a significantly greater power because the motors are larger and the amplitudes are greater than through handheld devices that are smaller. There are considerably more variances in how handheld FV than WBV is administered. With FV, it can vary on the muscle depending upon location relative to musculotendinous junction, as well as force applied in holding it on a specific limb. For WBV, one can typically stand (knees typically flexed or sits in a chair or wheelchair). These are all issues that need to be addressed in studying vibration effects on spasticity. Theoretically, there may be a vibration frequency that might play an important role in therapeutic goals. However, there may also be a danger to exposing individuals to some vibration frequencies. On the basis of the International Organization for Standardization 2631-1, the vibration range of frequencies between 4 and 12.5 Hz is considered to

Am. J. Phys. Med. Rehabil. & Vol. 93, No. 11, November 2014

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

TABLE 1 Assessment of risk for bias Author Alaca et al.18 Ashby et al.27 Butler et al.20 Calancie et al.16 Laessoe et al.17 Murillo et al.19 Ness and Field-Fote15 Perez et al.28 Taylor et al.29 Hilgevoord et al.30

Selection Bias/ Confounding

Performance Bias

Attrition Bias

Detection Bias

Reporting Bias

Low risk Medium risk Low risk Medium risk Medium risk Low risk Low risk Medium risk Medium risk Medium risk

Low risk Low risk Low risk Low risk Low risk Low risk Low risk Low risk Low risk Low risk

N/A N/A N/A N/A Low risk N/A Low risk N/A Unclear N/A

Unclear Low risk Low risk Low risk Unclear Medium risk Low risk Low risk Low risk Low risk

Low risk Low risk Low risk Low risk Low risk Low risk Low risk Low risk Low risk Low risk

N/A, not applicable.

put humans at greatest physical risk mainly on the lumbar spine and connected nervous system.24 Before guidelines can be established or more research in this area can be suggested, a systematic review is needed of what is the current knowledge on the use of vibration (WBV or FV) and how it should be used in the SCI population. For this systematic review, the primary question was what was the effect on spasticity and spasms after WBV or FV application in those with SCI? However, to put the results into context, the authors also needed to know what was the frequency range of WBV or FV used in this population, how was the vibration applied to individuals with SCI, and what were the measurement tools used to evaluate spasticity and spasms?

METHODS Search Strategy The Preferred Reporting Items for Systematic Reviews and Meta-analysis checklist and guideline were used to develop this review.25 However, the meta-analysis checklist items were not applicable. The following electronic databases were searched: MEDLINE, EMBASE, CINAHL, and PsycINFO since 1946,1974, 1977, and 1887, respectively, until January 3, 2013. No data restrictions were applied when the databases were searched. Peer-reviewed articles were identified using the key words vibration, whole body vibration, spasticity, spasm, and spinal cord injury. Search terms were adjusted for each database. Additional adjusted search terms were spastic paraplegia and spastic paresis. The bibliographies of relevant studies and review articles were searched. A hand search of potential journals was undertaken for articles relevant to the research question regarding research key words. The corresponding authors of five of the articles www.ajpmr.com

included in the study were contacted by e-mail to identify any additional studies related to the study purpose. E-mail addresses of an additional five corresponding authors were not available. The title and abstracts of all identified articles were reviewed by both authors. Articles not related to the objectives were excluded. The studies reporting the spastic muscles changes in individuals with SCI after either WBV or FV were reviewed in full articles. Assessing the Risk of Bias of Individual Studies in Systematic Reviews of Health Care Interventions was used to assess the risk for bias for each of the reviewed articles (Table 1).26

Inclusion/Exclusion Criteria To be included in the review, the articles must have included three or more participants, participants 17 yrs or older, and participants with chronic SCI who had spasticity for at least 4 mos after their injury (stable spasticity). Because of the diverse nature of definition for spasticity used in clinical and rehabilitation settings, the following spasticity definitions were included: velocity-dependent hypertonia, significant resistance to passive movement, involuntary electromyography (EMG) muscle activity, Modified Ashworth Scale (MAS) score of greater than 1, spasm frequency scale grade 1, pendulum test first swing excursion, and abnormal H-reflex activity. Studies with and without spasticity medication management were included in the review. Studies that specifically applied either WBV or FV were included. The studies that did not report a specific frequency of vibration were excluded from the review.

Data Extraction All information related to the research question including the methods of applying vibration, spasticity outcome measures, and study results were Vibration Changes Spasticity in Patients with SCI


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extracted from each of the reviewed articles. The authors extracted the data from each study together. The extracted data comprised study type, level of evidence, number of participants, age, level of injury, American Spinal Injury Association Impairment Scale, complete/ incomplete, tetraplegia/paraplegia, medication, vibration type, and frequency.

Level of Evidence The Centre for Evidence Based Medicine (CEBM) level of evidence was used to determine the level of evidence for each of the reviewed articles. The level of evidence was determined on the basis of the type of study including systematic reviews, randomized controlled trials, cohort studies, casecontrol studies, and case series.31 The CEBM categorizes the level of evidence as 1 (A to C), 2 (A to C), 3 (A and B), 4, and 5 on the basis of the type of studies described above.31 The studies are then categorized from grades A to D on the basis of their level of evidence. Grade A is consistent with level 1 (A to C) studies, and grade B is consistent with either level 2 (A to C) or 3 (A and B) studies. Grade C and D studies are consistent with level 4 and 5 studies, respectively. Each study was graded by

two authors using CEBM levels (1, 2, 3, and 4) and grades (A, B, C, and D). Disagreements over the evidence level and grade of each study were resolved through discussion between the two authors.

RESULTS In total, 109 articles were found by the primary electronic and hand searches. The search retrieved a total of 64 articles after duplications were removed. After reviewing the titles and abstracts, 40 articles were excluded, and 24 full-text articles were assessed by the authors to assess for eligibility on the basis of the inclusion criteria. After review of the 24 full-text articles, 10 met the inclusion criteria, whereas 14 articles were excluded. The hand search uncovered one study,30 whereas electronic search identified the remaining nine studies.15Y20,27Y29 The study selection process is described in Figure 1.

Population Collectively, the studies involved 195 individuals with chronic SCI. Six studies included an able-bodied control population totaling 87 participants.16,19,27Y30 Two studies included all three groups: acute SCI, chronic SCI, and able-bodied population.16,27

FIGURE 1 Flow chart of the literature search and study selection.

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4 3b 4 3b 2b 3b 2c 3b 3b 3b Case series Case-control Case series Case-control Crossover Case-control Prospective experimental study Case-control Case-control Case-control

Effects on Spasticity Whole-Body Vibration

AIS, American Spinal Injury Association Impairment Scale; LoE, level of evidence; N/A, not applicable.

C8YT12 C4YT7 C4YT6 C4YT10 C2YT8 C3YT12 C3YT7 N/A N/A N/A 2005 1974 2006 1993 2004 2011 2009 2004 1984 1996 Alaca et al.18 Ashby et al.27 Butler et al.20 Calancie et al.16 Laessoe et al.17 Murillo et al.19 Ness and Field-Fote15 Perez et al.28 Taylor et al.29 Hilgevoord et al.30

10 7 8 22 9 19 16 14 57 33

N/A 6 N/A 16 N/A 9 N/A 5 21 30

27.8 (3.7) 21Y57 37 (3) 26.2 (2.3) 27Y67 36.0 (10.6) 28Y65 42.8 (10.2) 17Y77 18Y68

A N/A A, B N/A A, C, D C, D C, D C, D N/A N/A

N/A N/A 2 baclofen Baclofen/diazepam Yes (n = 8) Yes (n = 7) Yes (n = 7) N/A N/A No medication

LoE Type of Study Medication AIS Level of Injury Age, Mean (SD)/Range N (Control) N Year Author

TABLE 2 Characteristics of the studies

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However, the results of the individuals with acute SCI were not reported in this review because of lack of spasticity in this group. Six studies reported the American Spinal Injury Association Impairment Scale scores of the SCI participants including A, B, C, and D levels.15,17Y20,28 The level of injury (ranging from C2 to L1) and having complete or incomplete SCI were reported in seven15Y20,27 and six15Y18,27,29 studies, respectively. Six studies reported the spasticity medication taken by the participants.15Y17,19,20,30 In one study, the spasticity medication was washed out 12 hrs before the study.19 Participants were not taking any medication in one study,30 and in four studies, the participants maintained their previous antispasticity medication regimen during the study.15Y17,20 The characteristics of the studies are described in Table 2.

Only one study (Table 3) measured spasticity after using WBV in incomplete SCI.15 The pendulum test was used to measure quadriceps muscle spasticity after WBV (three times a week for 4 wks). The first swing excursion and number of oscillation were the two components of the pendulum test used to evaluate spasticity. The study reported a significant decrease in spasticity in all but 1 wk of WBV training. There was a statistically significant (P = 0.005) increase in first swing excursion from initial to final test, with no significant change in oscillation numbers (P = 0.195) in the 1-mo period. The similarities between the first swing excursion values measured 1Y4 days and 6Y8 days after the last vibration sessions suggested that the effects of WBV intervention persisted for at least 6Y8 days.15

Focal Vibration Nine articles (Table 4) reported the effects of FV on clinical and neurophysiologic spasticity measures. Three studies reported clinical spasticity reductions before and after applying FV.17Y19 Two studies applied FV by penile vibration stimulation (PVS) and found a short-term decrease in spasticity for a maximum of 3Y6 hrs after applying vibration.17,18 Murillo et al.19 found a significant decrease in spasticity after applying FV to the rectus femoris muscle. The other six articles, the main outcome was spasticity neurophysiologic measure changes after FV application. Butler et al.20 displayed inconsistent EMG muscle activity and spasticity changes after applying FV. Although most of the EMG recordings after FV application showed a reduction in muscle activation, some of the trials showed increased Vibration Changes Spasticity in Patients with SCI


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FSE (angle at which the swinging leg first reversed direction from flexion to extension, indicating the point in the knee range of motion at which a reflex contraction of the quadriceps caused the knee to extend. An increase in FSE was interpreted as a decrease in spasticity). FSE, first swing excursion; OSC, number of oscillations.

Within 5 mins after vibration (immediate), approximately 15 mins later (delayed post-WBV), last testing: 8 days after last vibration session Ness and Field-Fote


a

Initial to last testing: increase in FSE (P = 0.005); no significant change in OSC Significant weekly within-session immediate and delayed post-WBV FSE changes for weeks 1, 2, and 4 Final test; 13 participants tested within 1Y4 days and 3 participants tested 6Y8 days (mean [SD] changes, 12.05 [4.04] and 11.47 [18.31], respectively) Pendulum test; FSE, OSC

Results

Three days per week for 4 wks. Each session: four 45-sec bouts per 1 min seated rest, standing on platform with the knees slightly flexed (30 degrees from full extension)

a

Outcome Measures Testing Intervention

15

Author

TABLE 3 WBV study characteristics

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muscle activity. Exposure to FV decreased EMG activity in seven participants but evoked spasm in one of the participants.20 Five of the studies that reported the spasticity neurophysiologic measure changes had an able-bodied control group. Changes in H-reflex in individuals with SCI who experienced spasticity, measured as H-reflexvibration/H-reflexcontrol, demonstrated less reduction compared with control groups in four of the studies included in the review.16,27,29,30 The study of Ashby et al.27 revealed suppression in T-reflex after vibration with an increase in tension of the force applied by a tendon hammer in two SCI participants. The Achilles tendon reflex suppression was greater in that study compared with H-reflex suppression.27 Perez et al.28 reported a significant increase in strength of Ia inhibition for 5 mins after vibration in a population with spasticity, with no significant change in presynaptic inhibition measured by H-reflex.

Vibration Frequency The type and frequencies of vibration varied considerably between studies as well as the application point to the person. The vibration was applied as WBV15 or FV16Y20,27Y30 with different frequencies; however, each study used only one specific frequency. The frequency range was 50Y110 Hz with an amplitude range of 1Y4 mm. FV was applied with a frequency of 50 Hz,19 60 Hz,27Y29 80 Hz,20 100 Hz,17,18,30 and 110 Hz.16 The WBV frequency was 50 Hz.15 The FV was applied to different points on the body including the Achilles tendon,16,20,27,29,30 the penis,17,18 the tibialis anterior tendon,28 and the rectus femoris muscle.19 The testing was conducted in sitting, semireclined, or lying supine positions while the vibration was applied. Vibration characteristics are described in Table 5.

Spasticity Measurements Spasticity was measured by different outcome measurements in the included studies. One study used the Penn Spasm Frequency Scale selfassessment.17 The clinical measurements used in different studies included the MAS,17Y19 the Modified Tardieu Scale,19 the pendulum test,15 spasm frequency,18 spasm severity,18 painful spasm,18 plantar stimulus response,18 muscle stretch reflex,18 clonus,18,19 and effects on function.18 The neurophysiologic measurements were most common, and these included EMG,17,20 H-reflex,16,19,20,27Y30 and Treflex.16,19,27,29 Three studies15,28,30 measured spasticity with only one outcome measure, and the other seven studies16Y20,27,29 used more than one outcome



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18

Lay prone with fixed angle at 90 degrees. Vibration applied to Achilles tendon to evoke TVR. EMG recorded from SOL

Stimulate SPN nerve to evoke muscle spasm (5 pulses of 300 Hz), 30 secs for PAD recovery

Semireclined position, vibration applied to Achilles tendon, EMG recorded from SOL

24 hrs of EMG from QF and TA bilaterally, followed by either PVS or no treatment subsequently and 24-hr EMG recording. repeated protocol after at least 1 wk

Butler et al.20

Calancie et al.16,a

Laessoe et al.17

3-min PVS followed by 1-min rest intervals until ejaculation or maximum of six sessions

Intervention

Ashby et al.27,a

Alaca et al.

Author

TABLE 4 Characteristics of FV studies

EMG recording 24 hrs before and 24 hrs after PVS (48 hrs in total). MAS and PSFS 24 hrs before, after PVS, and 24 hrs later

EMG, MAS, PSFS

H-reflex, T-reflex

H-reflexb: 10 pairs (20 trials)

Unconditioned Baseline, after applying vibration

EMG: 10 pairs (20 trials) from TA, MG, LG, SOL muscles

H-reflex, T-reflex, TVR

MAS, frequency spasm severity, painful spasms, plantar stimulation response, MSR, clonus, effect on function

Outcome Measures

Conditioned (with vibration)

Baseline, after applying vibration

Baseline and 3, 6, 24, and 48 hrs after PVS

Testing

(Continued on next page)

MAS significantly decreased in 3 hrs (P = 0.001) and 6 hrs (P = 0.03) after PVS. Lower MAS after 24 and 48 hrs but not significant. No significant difference for other measurements H-reflex: vibration less effective to suppress H-reflex in established spasticity group compared with control and acute SCI group TVR: absent in established SCI group ATR: suppression was greater than H-reflex suppression EMG: 66% of trials decreased, 22% abolished, 28% increased, 6% no response; group mean peak EMG decreased between 36% and 45%; 7 participants with decreased EMG and 1 participant had spasm after vibration H-reflex: amplitude not significantly reduced after vibration except in 2 participants Hvib/Hnvib ratio: significantly higher than control (P G 0.05) and acute SCI (P G 0.01); showed less inhibition T-reflex: changes after vibration were not reported in the article MAS: knee and ankle flexor and extensors significantly decreased after PVS (P G 0.01) and reduction vanished after 24 hrs EMG: mean number of EMG decreased significantly for 3 hrs (P G 0.05) PSFS: relaxation in legs and reduction in spasm frequency with no significant difference

Results

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Measurement with and without vibration

Measurement with and without vibration

Baseline measurement (before); immediately after (time 0); and at 5, 10, 15, and 20 mins

Baseline Stimulation after vibration

Testing

H-reflex

H-reflex

H-reflex: Ia inhibition,d presynaptic inhibitione

MAS, ROM measured with Modified Tardieu scale, clonus, H-reflex, T-reflex

Outcome Measures

MAS: significant reduction in knee joint (P G 0.001) ROM: significant increase in ROM for knee extension (P = 0.001) Clonus: significant reduction in number of cycles and total duration of clonus (P G 0.006) H-reflex: significant reduction in Hmax/Mmax (P = 0.001), no change in Mmax T-reflex: significant inhibition of the T wave in SCI participants (P = 0.002) Ia inhibition: significant increase in Ia inhibition at time 0 (P = 0.04) and 5 mins (P = 0.01) after vibration in all SCI participants Baseline inhibition = 2% of control. After vibration: at time 0 = 10% and after 5 mins = 9% compared with baseline. Ia inhibition returned to baseline at 15 mins (4%) Presynaptic inhibition: 3% at baseline and 4% after 10 mins (not significant) Hvib/Hcontrol: greater in group with spasticity than healthy and acute SCI group No report of T-reflex after vibration Max H-response vibratory suppression: significantly less in SCI group (P G 0.001) Maximal H-response: evoked at higher stimulus intensity than without vibration Mean level to which vibration inhibited the H-reflex: 20% for controls, 50% for SCI group

Results

b

Data for control group and acute SCI are not reported (results from chronic SCI group after vibration are reported). H-reflex (H- and M-wave onset latency and peak-to-peak amplitude, Hmax, Mmax). c Results for control group and comparing complete and incomplete groups are not reported. d Two to 3 milliseconds to evoke Ia inhibition. e Ten and 15 milliseconds to evoke presynaptic inhibition. ATR, Achilles tendon reflex; LG, lateral gastrocnemius; MG, medial gastrocnemius; MSR, muscle stretch reflex; PAD, postactivation decrease; PSFS, Penn Spasm Frequency Scale; QF, quadriceps femoris; RF, rectus femoris; SOL, soleus; SPN, superficial peroneal nerve; TA, tibialis anterior; TVR, tonic vibration reflex.

a

Semirecline chair. EMG recorded from SOL muscle

Hilgevoord et al.30

Rest sitting position, TA tendon vibrated for 3 mins, vibrator pressed onto the tendon 5 cm above the ankle

Vibration applied to RF

Intervention

Lay prone with extended knee and 90-degree ankle

19,c

Taylor et al.29

Perez et al.28

Murillo et al.

Author

TABLE 4 (Continued)

TABLE 5 Vibration characteristics Author

WBV/ FV

Frequency/ Amplitude

Alaca et al.18 Ashby et al.27 Butler et al.20 Calancie et al.16 Laessoe et al.17 Murillo et al.19 Ness and Field-Fote15 Perez et al.28 Taylor et al.29 Hilgevoord et al.30

FV FV FV FV FV FV WBV FV FV FV

100 Hz, 2.5 mm 60 Hz, 3 mm 80 Hz 110 Hz, 2.2 mm 100 Hz, 3 mm 50 Hz 50 Hz, 2Y4 mm 60 Hz 60 Hz, 1.5 mm 100 Hz, 1 mm

FV Application

Position

Muscles Testing

PVS Supine Kneea Achilles tendon Lying prone SOL Achilles tendon Sitting SOL, MG, LG, TA Achilles tendon Semireclined SOL PVS N/A QF, TA RF Sitting SOL, knee N/A Stood with knee flexed QF TA tendon Sitting SOL Achilles tendon Lay prone SOL Achilles tendon Semirecline SOL

a

Knee: including flexion and extension. LG, lateral gastrocnemius; MG, medial gastrocnemius; N/A, not applicable; QF, quadriceps femoris; RF, rectus femoris; SOL, soleus; TA, tibialis anterior; WBV, whole body vibration; FV, focal vibration; PVS, penile vibratory stimulation.

measure to report the changes after applying vibration. Two studies used the clinical and neurophysiologic measurements at the same time to assess the effects of vibration on spasticity.17,19

Level of Evidence The level of evidence of studies included in the review differed from 2b to 4 on the basis of CEBM. Six studies were case-control studies with the level of evidence of 3b.16,19,27Y30 Two studies were case series with the level of evidence of 4.18,20 The other two studies were a crossover study and a prospective experimental study with the level of evidence of 2b17 and 2c,15 respectively. On the basis of CEBM grades of recommendation, eight of the reviewed studies were categorized as grade B and the other two reviewed studies were categorized as grade C.

DISCUSSION The main purpose of this review was to explore what is the current state of knowledge regarding the effects of WBV and FV on spasticity in individuals with SCI. Although there may be some encouraging results linking WBV and FV to improved spasticity from the existing evidence, this evidence is still relatively weak because of limited number of studies and lack of high-quality clinical studies.

Vibration Frequency This review showed the significant breadth of vibration frequencies and duration applied to individuals with SCI. Frequencies ranged from 50 to 100 Hz, from 30 to 60 secs. Although this seems to be a relatively wide range, the studies all showed some reduction of spasticity in individuals with SCI. Because vibration frequency range and duration might be factors that play a role in either FV or WBV www.ajpmr.com

application to manage spasticity, vibration research will need to undergo various stages of development, focusing on factors such as frequency level and frequency duration or dose. Similar to drug trials, dose-response trials are essential to isolate what is effective and what may be ineffective or possibly spasticity inducing.

Whole-Body Vibration The 50-Hz frequency used in WBV exposures demonstrated a decrease in spasticity through a 1-mo training in individuals with SCI, lasting 6Y8 days after the last training session.15 These results were consistent with the WBV application studies for ablebodied individuals as well as individuals with cerebral palsy and stroke.32Y34 Ahlborg et al.34 evaluated the effects of 8 wks (24 sessions) of WBV training on spasticity, muscle strength, and motor performance in adults with cerebral palsy, and they found a reduction in knee extensors spasticity without any significant changes in other muscle groups after the 8-wk training. Chan et al.33 applied a single session of WBV with a magnitude of 12 Hz and 4-mm amplitude in stroke patients with spasticity.33 This randomized controlled trial showed a significant decrease in spasticity measured by the MAS, selfreport visual analog scale, and the H-reflex measurement (Hmax/Mmax ratio). Pang et al.32 completed a randomized controlled trial study with WBV stimulation (20Y30 Hz) and exercise training during an 8-wk period (15 mins for 3 days per week) and showed a significant reduction in spasticity measured by the MAS in a stroke population. In their study, the spasticity reduction showed a decreasing pattern during the 8-wk training and a significant reduction after 1 mo in the group with vibration and exercise compared with the control group that Vibration Changes Spasticity in Patients with SCI


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performed only the exercise. Although the mechanism of spasticity might be different among different upper motor neuron disorders, the results of studies on cerebral palsy and stroke participants offer a change in spasticity by WBV application. Despite the evidence, although limited, in using vibration to help manage spasticity in individuals with SCI and other upper motor neuron disorders, there is still concern about the appropriate frequency to use. The International Organization for Standardization 2631-1 shows that WBV exposures of 4Y12 Hz may be subjecting individuals to health hazards.24 In this frequency range, it is not clear whether vibration, either WBV or FV, would trigger spasticity or spasm in individuals with SCI. All the abovementioned WBV studies, except one, used frequencies higher than the International Organization for Standardization 2631-1 WBV health hazard range.15,24,32Y34 Messenberg35 created a vibration platform that could vibrate individuals with SCI in a sitting position at frequency ranges from 8 to 100 Hz. With the sample of two participants, it was found that sufficient vibrations could be provided to induce spasticity. Some frequencies resulted in a decrease in muscle activities and spasticity, whereas others exacerbated spasticity. However, this was only a pilot study to show a proposed methodology.35 More work with a larger sample size is needed to understand range of frequencies and their impacts. This methodology may be a good way to apply various frequencies to individuals with SCI and examine the muscle responses in a systematic fashion.

Focal Vibration Nine studies used the FV with a frequency range of 50Y110 Hz to evaluate the effects of FV on spasticity.16Y20,27Y30 Two studies that used PVS found a short-term decrease in spasticity, using EMG and MAS, lasting for up to 6 hrs.17,18 Laesso et al.17 described two mechanisms including release of a humoral factor with a general muscle relaxant effect and the activation of pudendal afferent nerve generated by PVS procedure. Pudendal afferent nerve activation might result in changes in inhibitory spinal pathways including increased presynaptic inhibition, increased reciprocal inhibition, and decreased Ib interneuron excitation.17 These changes in spinal cord inhibitory pathways result in spasticity reduction after PVS application.17 Halstead et al.36 also proposed two mechanisms for the antispastic effect of rectal-probe electroejaculation. The periprostatic area nerve supply is rich, and the stimulation is close to the spinal cord. The stimulation provokes

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a humoral agent release. These mechanisms are proposed for PVS and rectal-probe electroejaculation, which cannot be generalized as the FV mechanism for spasticity and spasms reduction. However, SLnksen37 used PVS to assist ejaculation in individuals with SCI, which resulted in abdominal muscle contraction and leg spasms. Inducing abdominal muscle contraction and leg spasms by PVS application37 supports the probability of spasm triggering by FV application in individuals with SCI who experience spasticity, thus consistent with the other studies that showed spasticity and spasms reduction after PVS. FV application has been used to manage spasticity in other upper motor neuron disorders such as stroke and SCI. Caliandro et al.38 applied FV (100 Hz, 0.2Y0.5 mm) to muscles of the upper extremities for 3 consecutive days to assess the effects of vibration on stroke patients with spasticity. Spasticity outcome measures by the MAS and the visual analog scale showed no difference through three different measurements immediately, after 1 wk, and after 1 mo. The Wolf Motor Function Test score showed a significant difference in spasticity over time.38 Noma et al.39 applied FV (91 Hz, 1 mm) to the upper limbs of stroke patients to assess the effects of FV on spasticity. F-wave and MAS measurements found the application of direct vibration to significantly decrease spasticity for at least 30 mins. FV was seen to be less effective to suppress H-reflex in individuals with established spasticity compared with those in the able-bodied population.16,27,29,30 Perez et al.28 studied the effects of mechanical stimulation by vibration (60 Hz) on reciprocal inhibition in individuals with chronic SCI. Reciprocal inhibition is necessary between agonist and antagonist muscle pairs to perform smooth movement alteration during motor activities.40,41 Reciprocal inhibition is modulated by a number of polysynaptic pathways including Ia inhibition and presynaptic pathways.28,42Y44 Vibration induction increased the Ia inhibition (2- to 3-millisecond latency) significantly to inhibit the antagonist muscle after agonist muscle activation. The presynaptic inhibition (10- to 25-millisecond latency) did not change significantly in individuals with chronic SCI.28 The increase in Ia inhibition would play a role in muscle relaxation and spasticity reduction by vibration intervention in individuals with SCI.

Spasticity Measurement Alaca et al.18 showed that spasticity outcome measurements other than the MAS did not change



significantly after PVS. This raises the ongoing question as to what is the best method for assessing spasticity in the SCI population. Quantifying a precise spasticity outcome measure is challenging and complex for researchers and clinicians. Although there are some correlations among spasticity outcome measures, the lack of strong correlation among self-assessment, clinical, and neurophysiologic spasticity outcome measures makes it difficult to find a valid and reliable measurement tool to reveal the degree of spasticity.45,46 The included studies in the review chose a variety of outcome measures to assess spasticity that were not consistent among the studies.15Y20,27Y30 Most of the studies included only neurophysiologic measures, which reduces clinical validity of the findings.16,20,27Y30 Isokinetic dynamometers measure spasticity quantitatively by measuring the resistance of a joint while it is sinusoidally oscillated at different constant angular movements.47,48 The amount of force that is generated by the muscles is reported as spasticity. Although this measurement is a simple quantitative outcome measure,47,48 it was not used as a spasticity outcome measure in any of the included articles in the review. It has been recommended in future research to use a combination of the different outcome measures including the self-assessment scales, clinical, biomechanical, and neurophysiologic, to evaluate the degree of spasticity in individuals with different upper motor neuron disorders including individuals with SCI.45

Quality of Articles As mentioned earlier, the quality of studies in this topic is relatively poor for clinical interventionbased studies. The best evidence was two prospective studies, one being a crossover design.15,17 Sample size in these studies is small, as typical in many rehabilitation studies investigating SCI. Thus, from a CEBM analysis, although these are not of great quality, they may be on par with most of SCI literature, which often has a small sample size with a relatively heterogeneous population. Thus, the results of these studies should not be discarded too quickly. There does seem to be some evidence that WBV and FV may have some impact on spasticity. This evidence definitely suggests that larger prospective and multicenter studies need to be performed.

What Is Known and Future Direction of Research According to the results of the studies in this review, most of the individuals with SCI experiwww.ajpmr.com

enced a short-term reduction in spasticity for a short period when FV (50Y100 Hz and 2.5Y3 mm) was applied. The FV with a specific range might be helpful for individuals with SCI who experience spasticity. The impact of this research could potentially lead to individuals with SCI purchasing an appropriately adjusted vibrator with a defined vibration frequency and intensity range to use for their daily life to manage their spasticity. WBV may have an effect on spasticity; however, it is still unclear what frequencies would be more beneficial. More work using a WBV platform that can apply a wide frequency range would help to demonstrate the relationship between a variety of frequencies and the impact on spasticity with greater accuracy. Future randomized controlled trials with a larger sample size, using a wide range of frequencies, repetitive WBV and FV exposure, along with valid and reliable spasticity outcome measurements, would allow researchers to tease out better what are the advantages and disadvantages of vibration exposure for those with SCI who experienced spasticity. Finally, in future research, some functional changes that may result from using either form of vibration need to be addressed. What are the impacts of vibration on the ability to transfer, dress, or even walk in some individuals? For example, in 2009, Ness and Field-Fote49 studied the use of vibration for 4 wks (three times a week) and its effect on walking speed. They found that vibration increased walking speed by 0.062 m/sec (P G 0.001). This improvement corresponds to results from gait training protocols. Seven of the 17 participants were on medication for spasticity, although the authors did not specifically study spasticity. They suggested that consistent use of afferent input improves the motor output of the control mechanisms that are impaired after an SCI. Are motor control mechanisms responsible, too, for spasticity and muscle spasm changes in vibration application? Future research should probably not only examine muscle activity changes by either WBV or FV application but also include walking or other exercises to vibration trainings.

CONCLUSIONS In conclusion, this unique review of how vibration, both whole body and focal, affects spasticity in individuals with SCI provides some limited support for use of WBV and FV to manage spasticity in individuals with SCI. The support is limited to relatively low-quality articles, which indicates the need Vibration Changes Spasticity in Patients with SCI


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for further studies with larger sample sizes, wider frequency ranges from low to high, application of vibration with other exercise trainings, and randomized controlled trial designs to provide stronger evidence for vibration effects on spasticity. Having a better understanding of the role of vibration in individuals with SCI for managing spasms will lead to innovations in therapy and changes to assistive technology that may potentially decrease the use of antispasmodic medications, which often have significant side effects. However, this review clearly shows that the current knowledge is limited. Thus, clinicians and researchers need to be encouraged to perform randomized controlled trial studies on vibration to provide clinicians and patients with a more clear direction on the use of vibration to manage spasticity for those with SCI. REFERENCES 1. Lance JW: The control of muscle tone, reflexes, and movement: Robert Wartenberg Lecture. Neurology 1980;30:1303Y13 2. Maynard FM, Karunas RS, Waring WP III: Epidemiology of spasticity following traumatic spinal cord injury. Arch Phys Med Rehabil 1990;71:566Y9 3. Sheean G: The pathophysiology of spasticity. Eur J Neurol Off J Eur Fed Neurol Soc 2002;9(suppl):53Y61 4. Sko¨ld C, Levi R, Seiger A: Spasticity after traumatic spinal cord injury: Nature, severity, and location. Arch Phys Med Rehabil 1999;80:1548Y57 5. St George CL: Spasticity. Mechanisms and nursing care. Nurs Clin North Am 1993;28:819Y27 6. Dietz V: Spastic movement disorder. Spinal Cord 2000;38:389Y93 7. Adams MM, Hicks AL: Spasticity after spinal cord injury. Spinal Cord 2005;43:577Y86 8. Richardson D, Thompson AJ: Botulinum toxin: Its use in the treatment of acquired spasticity in adults. Physiotherapy 1999;85:541Y51 9. Yaraskavitch M, Leonard T, Herzog W: Botox produces functional weakness in non-injected muscles adjacent to the target muscle. J Biomech 2008;41:897Y902

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Vibration Changes Spasticity in Patients with SCI Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

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