Effects of vibration rolling on ankle range of motion and ankle muscle stiffness in stroke patients: a crossover study

Background: Vibration stimulation has emerged as a treatment tool to aid spasticity during physical therapy. However, the benets of vibration rolling (VR) on interventions for stroke patients are unclear. This study aimed to investigate the effect of VR intervention on the range of motion (ROM) and ankle stiffness in stroke patients. Methods: In this crossover design study, seven stroke patients completed two test sessions (one VR and one non-VR [NVR]) in a randomized order, with 48 h of rest between each session. Participants completed intervention and its measurements on the same day. The measurements included ankle dorsiexion and plantarexion ROM and stiffness of ankle muscles, including the tibialis anterior and gastrocnemius lateral and medial muscles. Results: After VR, ankle dorsiexion ROM, gastrocnemius lateral stiffness, and gastrocnemius medial stiffness improved signicantly (all P < 0.05). After NVR, only gastrocnemius lateral stiffness improved signicantly (P < 0.05). Furthermore, compared with the change values for ankle dorsiexion ROM and gastrocnemius lateral stiffness, VR showed a more signicant difference than NVR (P < 0.05). Conclusions: VR improved ankle ROM and muscle stiffness. Therefore, we suggest that practitioners should consider VR as an intervention to increase dorsiexion ROM and gastrocnemius stiffness in stroke patients. and the other exercise performed two days later. The paretic leg of the participants was assessed using ROM of ankle dorsiexion and plantarexion, muscle stiffness of the tibial anterior muscle, and medial and lateral gastrocnemius muscles. After the completion of the pre-test assessments, each participant performed the intervention. Each intervention was performed in three sessions for 1 minute per session, and a 30-second rest was taken between each session.


Background
Stroke is caused by cerebral infarction and cerebral hemorrhage [1]. Stroke may result in several problems including poor balance and gait, spasticity, weakness, and contractures, as well as sensory and cognitive impairments, all of which require much effort in terms of patient care [2,3]. Among these problems, spasticity results in worse motor function, greater pain and stiffness, and reduced range of motion (ROM) of joints [4,5]. Spasticity can be de ned as a sensorimotor disorder related to some level of involuntary muscle activation, and it is a consequence of upper motor neuron syndrome [6,7]. Physical therapy, such as static stretching, transcutaneous electric nerve stimulation, extracorporeal shock wave therapy, electromyography biofeedback, and vibratory stimulation, can be used to treat post-stroke spasticity [8][9][10][11][12]. However, among the various treatment methods, most vibration stimulation studies have been wholebody vibration studies, and local vibration studies are lacking.
Among the various local vibration tools, vibration rolling (VR) is a combination of foam roller and vibration function. VR has been reported to improve ROM, exibility, pain, strength, proprioception, balance, and muscle tone in adults [13][14][15]. Recently, VR has been reported to improve athletic performance in athletes [16]. These effects are necessary not only for adults or athletes but also for stroke patients. Despite this, VR intervention has not yet been studied in stroke patients. Therefore, the purpose of this study was to investigate the effect of VR intervention on the ROM and stiffness of the ankle joint in stroke patients and to present the VR as one of the treatment and exercise methods of possible intervention for stroke patients.

Participants
The study was approved by the Institutional Review Board of Nambu University (IRB: 1041478-2020-HR-031). Eight stroke patients participated; however, one patient in poor condition was removed during the study. Therefore, seven patients (sex male/female: 6/1; paralyzed side left/right: 3/4; age: 71.43 ± 9.64 years, body mass: 67.00 ± 9.47 kg, height: 170.71 ± 6.52 cm; onset period: 12.57 ± 3.10 month; mini mental state examination, MMSE: 24.86 ± 0.90 score; modi ed Ashworth scale, MAS: 1.21 ± 0.27 grade) completed the study. The inclusion criteria were a diagnosis of stroke over 6 months ago, ability to move ankles without assistance, and ankle MAS below Grade 2. The exclusion criteria were as follows: cardiovascular or respiratory disease, orthopedic diseases in the legs, vision or hearing disabilities, and skin diseases of the feet. All participants were informed of the bene ts and risks of this study, and written informed consent was obtained from all participants.

Study procedures
This study was a crossover study. Assessments performed by each participant were assessed in a physical therapy room at the Department of Rehabilitation Medicine, Suwan Medical Center. Prior to the assessment, participants received instruction on how to perform VR and non-VR (NVR) exercises. During this orientation, participants were familiarized with the procedures, assessment tools, and VR equipment of the study. One day after the orientation session, each participant completed two assessment sessions in a randomized order, with 48 h of rest between each session. Before the assessment session, each participant completed general physical therapy and rehabilitation exercises. Participants rested before the assessment session. An assessment session was conducted in the afternoon. An assessor prepared randomly shu ed sticks (A stick: VR; and B stick: NVR) and sealed each stick in an opaque envelope. Each participant looked for an envelope and opened the envelope to identify the exercise of assignment. The identi ed exercise was performed rst, and the other exercise was performed two days later. The paretic leg of the participants was assessed using ROM of ankle dorsi exion and plantar exion, muscle stiffness of the tibial anterior muscle, and medial and lateral gastrocnemius muscles. After the completion of the pre-test assessments, each participant performed the intervention. Each intervention was performed in three sessions for 1 minute per session, and a 30-second rest was taken between each session. Immediately after the intervention, post-test assessments were conducted in the same order as pre-test measures. Participants completed the intervention and its measurements on the same day. One participant in the poor condition was lost to follow-up for the second session. A owchart of the experimental design is shown in Figure 1.

ROM of ankle
The ROM of the ankle was measured using a plastic goniometer. The angle of ankle dorsi exion in the prone position with 90 ° of knee exion was measured. The angle of ankle plantar exion in the supine position and the ankles outside the bed were measured. The axis of the plastic goniometer was placed on the lateral malleolus. The xed arm was placed parallel to the line connecting the bular head, and the moving arm was placed parallel to the line connecting the metatarsal bone of the fth toe [17]. The measurements were performed by a physical therapist who was blinded to the measured values. The measurer told the recorder when the measurement was complete. The recorder visually con rmed and recorded the measured value. The data used the average of the two measured values. The plastic goniometer showed high interrater reliability (ICC = 0.87) and intrarater reliability (ICC = 0.91) [17].

Muscle stiffness of ankle
The stiffness of the ankle muscles of the tibialis anterior, gastrocnemius lateral, and medial muscles was measured using the myotonPro (Myoton AS, Tallinn, Estonia). The stiffness of the tibialis anterior in the supine position was measured [18]. The stiffness of the gastrocnemius lateral and medial muscle was measured with the patient in the prone position and with feet hanging over the end of the bed [19]. The measurements were performed by a physical therapist who was blinded to the measured values. The measurer told the recorder when the measurement was complete. The recorder visually con rmed and recorded the measured value. The data used the average of the two measured values. The myotonPro showed high interrater reliability (ICC = 0.93) and intrarater reliability (ICC = 0.95) [20,21].
Exercise protocols VR Participants performed VR using a vibrating foam roller (Vyper, Hyperice, Irvine, CA, US). Participants positioned the vibrating foam roller below the gastrocnemius of their paretic side leg. The frequency of VR was 28 Hz, which has been used in many prior studies [13,22]. Thereafter, patients performed 60 s of dorsi exion and plantar exion of their ankle (Fig. 2). The physical therapist observed and encouraged the patient to continuously move through the entire ROM. Patients engaged in 30 s of rest in between exercises. Each exercise was performed three times.

NVR
The exercise protocols were the same as those used for the VR exercise, except vibration (vibration button off).

Statistical analyses
All data analyses were performed using SPSS version 25 (Chicago, IL, USA). Data are presented as the mean ± standard deviation (SD). Data were not observed statistically for normality (Shapiro-Wilk's test, p < 0.05), and a few variables were normally distributed. Therefore, nonparametric tests were used. Descriptive statistics were performed for the characteristics of the participants. A Mann-Whitney U test was performed to analyze the differences between VR and NVR by comparing the differences between preand post-treatment measurements. The Wilcoxon test was performed to compare pre-and postintervention results in each group. The effect size (Cohen's d), which is the difference between the pre-and post-means divided by their common SD, was calculated and interpreted as small (d = 0.2), medium (d = 0.5), or large (d = 0.8) to present the magnitude of the effect [23]. The signi cance level (α) was considered to be p < 0.05.

Stiffness of ankle muscle
For tibialis anterior stiffness, all groups showed no signi cant improvement in post hoc test measures (P > 0.05) ( Table 1) compared with pre-test measures. In addition, compared groups in change values, and the two groups showed no signi cant difference (P > 0.05) ( Fig. 3; C).
For gastrocnemius lateral stiffness, all groups showed signi cant improvement in post hoc test measures (P < 0.05) ( Table 1) compared with pre-test measures. In addition, compared with the change values, VR showed a more signi cant difference than NVR (P < 0.05) ( Fig. 3; D).
For gastrocnemius medial stiffness, VR showed signi cant improvement in post hoc test measures (P < 0.05) ( Table 1) compared with pre-test measures. NVR showed no signi cant improvement in post hoc test measures (P > 0.05) ( Table 1) compared with pre-test measures. In addition, compared groups in change values, and the two groups showed no signi cant difference (P > 0.05) (Fig. 3; E).

Discussion
This is the rst study to investigate the immediate effects of VR combined with dynamic muscle contraction as an intervention to improve ankle ROM and ankle stiffness in stroke patients. In terms of the effects on ankle ROM, VR signi cantly improved ankle dorsi exion ROM. In addition, the amount of angle change for dorsi exion ROM was greatly improved after VR. These results are supported by those of previous studies in which VR increased ankle ROM [22,24]. This effective result is thought to be the result of vibration stimulation leading to an increase in blood ow and temperature, which could provoke ROM improvements [25].
Next, our study revealed that VR signi cantly decreases gastrocnemius lateral and medial stiffness. These results were similar to those of previous studies in which VR decreased ankle stiffness in athletes [16].
However, as stroke patients experience upper motor neuron syndrome, spasticity occurs as a clinical characteristic of movement disorder. Spasticity can increase muscle stiffness due to exacerbation of stretch re exes [26]. The stretch re exes increase in proportion to the speed of movement [27]. This study is thought to suppress the stretch re ex, and the stiffness did not increase because the dynamic movement was slowly maintained during exercise. Additionally, it is thought that the stiffness was improved because the vibration caused a change in the viscoelastic properties of the muscle and increased stretch tolerance [28,29].
Finally, this study showed that improvements in stiffness of the gastrocnemius lateral muscle were signi cantly better than that of the medial muscle. This is thought to be because the gastrocnemius lateral muscle receives direct vibrational stimulation because the hip joint external rotation occurs when the stroke patient is in a supine position.
This study had several limitations. First, the number of participants in the study was small. Second, only one vibration frequency was used. The effects of other vibration frequencies could not be con rmed.
Third, the patient's ankle movement speed and frequency within the intervention time were different. In the future, follow-up studies should be conducted to compensate for these limitations.

Conclusions
The ndings suggest that VR intervention for stroke patients can signi cantly improve dorsi exion ROM and gastrocnemius stiffness. Therefore, we suggest that practitioners consider VR as an intervention to increase dorsi exion ROM and gastrocnemius stiffness in stroke patients. This study was approved by the Ethics Committee of Nambu University (IRB1041478-2020-HR-031), and it conformed to the ethics guidelines of the Declaration of Helsinki. All the written consents were signed voluntarily. For this study, a privacy regulation applies. This privacy regulation is compliant with the rules of South Korea.

Consent for Publication
Not applicable.

Availability of Data and Materials
All data generated or analysed during this study are included in this published article.  Changes from pre-test to post-intervention in ankle range of motion (ROM) and ankle muscle stiffness after vibration rolling (VR) and non-vibration rolling (NVR) * Change is statistically signi cant at p < 0.05.