Introduction

Multiple sclerosis (MS) is a chronic inflammatory autoimmune neurological disease that is characterized by myelin destruction in the central nervous system (CNS), grey matter, and axonal loss (1). The damage within the CNS slows the nerve conduction and decreases motor activation that coincides with impaired motor performance (2). Altered balance, walking dysfunction, muscle weakness, reduced core stabilization, and fatigue are symptoms of impaired motor performance (3,4). Especially, core muscle strength is necessary for skilled movement and function (5).Physiotherapy and rehabilitation training includes strength and stretch and balance and coordination exercises for patients with MS in the baseline. Recently, task-oriented training and whole‐body vibration have proved benefits in patients with MS (6). Perturbation training (PT) has been incorporated into balance training (7). Anticipatory (APAs) and compensatory postural adjustments (CPAs) are the two main postural mechanisms used by the CNS to maintain and restore balance during perturbations (8). APAs are responsible for postural muscle activation in a feed-forward manner before perturbations (9). Predicted or small perturbations can only be counteracted with APAs (10). Unexpected or large perturbations can be counteracted with CPAs (10). Perturbations develop an automatic postural response, which is known as the primary component of postural control (11). PT is aimed to improve reactive balance control, step quality, and reduce the risk of falling (12,13). The inefficient APAs cause fear of falling, slow mobility, and poor balance in older adults (14). The muscle activity during APAs was smaller and delayed than healthy persons, even in the early phase of MS (15). Additionally, few studies investigated the effect of PT on lumbar stabilization (16), which revealed that external perturbations increased intramuscular electromyography signals, especially the transversus abdominis (17). Unexpected perturbation to the transversus abdominis plays a key role in lumbar stabilization compared to other trunk muscles (16).

The effects of PT are shown in different areas in different diseases, in the elderly, e.g., stroke, Parkinson’s disease, and anterior cruciate ligament ruptures (12,18-20). PT stimulated the neuromotor system, improved sensorimotor skills, and prevented falling (21). Lateral perturbations were improved in the magnitude of CPAs for patients with Parkinson’s disease to develop balance and reduce falls (14). Perturbations provide information on the strategies of adjustments, but the effects of PT were not clearly understood in patients with MS (22). The effects of perturbations on the fear of falling are still unknown. Thus, investigating the effect of PT on MS is necessary. This study aimed to investigate the effect of PT on balance, walking, and lumbar stabilization.

Method

This is a pilot study that was approved by Gaziantep University, Clinical Researches Ethics Committee in June 2017 (number: 2017/255). Informed consent was obtained from all participants.

Participants

This study included 10 patients with MS between July and December 2017 (Figure 1). The inclusion criteria were (1) Mc Donald’s MS diagnosis following the 2010 criteria, (2) ages 18-45 years, (3) and Expanded Disability Status Scale (EDSS) score of 3-5.5. The exclusion criteria were (1) 3 or higher scores in spasticity according to Modified Ashworth Scale, (2) psychological, orthopedic, and other neurological disorders, and (3) attacks in the last 3 months.

Procedure

All patients attained a physiotherapy program. Perturbations were manually applied, and precautionary measures were taken to avoid the risk of injuries. PT was carried out in different positions that included standing, kneeling, and sitting. Manual perturbations in each position were applied 10-12 times, and individuals were allowed to rest for 10 s between each position at a sitting position. Perturbations were applied for 5 min, along with 10 s break between two successive sets. Perturbations were performed in both right and left sideways, backward and forward in each of positions, and at the pelvis and shoulders in different directions. The duration of one session was 45 min. Treatment was given twice a week for 6 weeks (23). Participants did not receive any other treatment or physiotherapy application. The treatment and assessment tests were carried out by the same physiotherapist.

Measurements

Statics Balance Tests

Romberg (RT), Sharpened Romberg (SR), and single leg stance test (SLST) were performed and their duration was recorded. RT was performed on patients with eyes closed and feet together. The test was terminated when the participant held it in one place, oscillations began or were likely to fall (24). RT maximum duration was 120 s. SR was performed on a straight line with one leg behind the other leg, eyes open, and leaving the arms sagging, without impairing the balance. Duration stop criteria were defined as the time that took a participant to dislocate the foot, reach the maximal duration of 30 s, and contact the observer to avoid falling (25). An SLST was measured in a standing position with dangling arms. The duration was stopped when the participant re-positioned his/her supportive foot, touched their feet to the ground, sought support from the observer, and reached the maximum duration of 30 s (16).

Dynamic Balance Tests

Dynamic balance was assessed with functional reach test (FRT), lateral reach test (LRT), and four square step test (FSST). FRT was performed by reaching forward and lateral without taking a step. The level of the metacarpal bone was marked in the start position and final position. The difference between these levels was measured (26). LRT was performed with both sides that included dominant and non-dominant sides (27). LRT is a reliable and valid measure for lateral stability limits and mediolateral balance in the MS population (28). FSST measured dynamic balance and included all directions, e.g., backward, forward, right, and left (29). The time of the test was recorded while the participant rapidly stepped in clockwise and counter-clockwise rotations (30).

Walking

A timed up and go (TUG) test was used for functional mobility that was related to falling risk. Individuals in TUG were asked to stand from the sitting position, walk 3 m, turn back, and sit back on the chair again (31).

Lumbar Stabilization Test

Core muscle performances were assessed with a Pressure Biofeedback Stabilizer (PBS) (Chattanooga, Australian) (32). Individuals were positioned to stand with their comfortable foot distance and their back resting on the wall. The stabilizer’s pressure cell was placed under L3-4 spinous processes and was inflated to a baseline pressure of 40 mmHg. All individuals were asked to have a stable baseline pressure. The duration without moving their spine or pelvis was recorded. Three trials were performed and the best scores were recorded (5).

Fear of Falling

Falls Efficacy Scale International (FES-I) was used to evaluate the level of concern related to falls during 16 activities of daily living. This questionnaire quantifies the level of concern about falling while performing each activity on a 4-point scale (1= not at all; 2= somewhat; 3= quite a lot; and 4= very). The total score is between 16 and 64, in which a higher score indicates more concern about falling (33).

Statistical Analysis

Statistical Package for the Social Sciences version 22.0 software was used for statistical analyses. G*power application was used to calculate the necessary minimum sample size. The sample size was calculated to be 19 subjects with 5% type 1 and 10% type 2 error limits before and after treatment to provide 90% working power, gain 0.80 of effect size, and 95% confidence interval. The frequency in percent (%) and mean ± standard deviation (X ± SD) of necessary variables were calculated for the descriptive analyses. Normality of distribution was tested with the Skewness-Kurtosis and histogram graphic. Paired samples t-test was used for the comparison of two measurements; pre and post-treatment. Differences were assumed significant at p-values of <0.05.

Results

The demographic characteristics of participants are shown in Table 1. All participants had a Relapsing-Remitting type of MS. The diagnosis period of participants varied between 2 and 15 years. The average EDSS score was 1.87. All participants were right-handed. Two participants have no history of falling, whereas three participants fell one time or two times in the last year and five participants have >2 histories of falls in the last year.

SR and SLST, which were used to test the static balance, significantly increased after the treatment (p<0.05) (Table 2); however, RT had no differences between the pre and post-treatment periods (p>0.05) (Table 2). Significant differences were found in FRT and LRT-ND (Table 2). FSST dynamic balance test was not changed with the treatment period (p>0.05) (Table 2). The fear of falling decreased after the treatment, without statistically significant analysis (p>0.05) (Table 2). After the treatment, TUG improved in participants (p=0.01) (Table 2). However, no differences were found in PBS between the pre- and post-treatment periods (p>0.05) (Table 2).

Discussion

This study aimed to investigate the effect of PT on balance, walking, and lumbar stabilization in patients with MS. A significant effect of PT was recorded on balance and walking. However, the improvement in fear of falling was observed to be clinically but not statistically significant. Investigating the effect of PT on balance, walking, lumbar stabilization, and fear of falling is effective in long-term MS.

Perturbations are known to improve CPAs and APAs and positively affect balance and walking in the elderly (19,34). Both gait and fear of falling are affected by gender. Functional walking categories revealed that walking performance changed according to age and gender in patients with MS (35). Therefore, the effects of PT according to age and gender should be compared in a larger sample. The range of age and the number of participants were limited in our study. As this is a pilot study, the effects of age or gender were not determined. Further studies might focus on investigating the response of PT according to age and gender.

Studies investigated the perturbation direction in the literature. Morrison et al. (36) showed that persons with MS exhibited greater sway in the mediolateral direction compared to the anteroposterior direction. The comparison of the elderly revealed that mediolateral sway was greater in MS, which increased the falling risk and affected the activity in daily life (36). Cortesi et al. (37) determined that their treatment improved not only the mediolateral balance but also the anteroposterior balance. Additionally, Salcı et al. (11) demonstrated that proprioceptive neuromuscular facilitation techniques should be applied for motor strategy training, and balance, and especially posterior perturbations should be preferred. This study performed perturbations in all directions. The mediolateral balance was thought to be more difficult to develop since it was more affected according to the FSST and LRT results. A more intensive treatment program may be required to improve the mediolateral balance.Perturbations disturb individual stability and supply feedback postural control, thus they improve the balance (38). However, perturbations should be sufficient to improve reactive balance control (39). The amount of perturbations is unclear. A study showed that it should be 24 perturbations at one session and another argued that it should include approximately 80 perturbations over four sessions (40,41). Some studies determined approximately 700-1,150 perturbation overall training (42,43). This study performed approximately 75 perturbations in one session that includes three positions (i.e., sitting, stand, and tandem positions) 10-12 times in each position for two successive sets. The number of perturbations was thought to be sufficient to improve the balance and gait of MS. More studies are needed to determine the exact amount in patients with MS.

van Duijnhoven et al. (13) determined that perturbations improved the quality of stepping in patients with chronic stroke but not the speed of gait. Another study applied PT on the treadmill and revealed that PT improved the dynamic balance and walking in the elderly (34). Further, another study investigated the effect of PT on gait in Parkinson’s disease using the 6-meter walk test and TUG (44). Compared with the control group, PT was determined to improve the performance in TUG but remained unchanged in the 6-meter walk test duration (44). Our primary findings indicate that PT might support improvements in walking performance in patients with MS. Our study findings were similar to the literature. To our knowledge, performing PT in MS is the original feature of our study. However, our study investigated only the speed of walking in MS. Other studies in literature investigated the gait in detail. Aruin et al. (22) determined that perturbations improved CPAs and APAs and changed gait initiation in MS. Tajali et al.  (14) showed that external perturbations change in core muscle activity during walking in MS. Thus, the effect of PT on walking can be investigated in detail like electromyography activity.

After perturbations, improved balance and accurate stepping are essential strategies to prevent falling and reduce the fear of falling (34). PT focuses on response to improve reactive balance and reduce the risk of falling (12). PT was performed in 10 sessions for patients with chronic stroke in a study and showed increased activity-specific confidence, but no statistically significant differences (13). However, the increased activity-specific confidence after 6 weeks was greater than the post-treatment. Thus, the effect of PT on the fear of falling became apparent in the follow-up period. Our study revealed a decreased fear of falling with PT training following the literature. However, the effect of treatment is thought to be better in the long term. Fear is known as a psychogenic composite parameter and fear is affected by psychosocial factors. Thus, the fear of falling is thought to be follow-up as long term in patients.

Freeman et al. (16) emphasized the effect of unexpected perturbations on core stabilization that is directly controlled by CNS and PT supplied feedback and proprioception for deficits in neuromuscular control of stabilization; therefore, PT improved lumbar stabilization (45). Vera-Garcia et al. (46) showed that trunk perturbations increased preactivation of core muscles and trunk stability and reduced lumbar displacement. Another study proved that high-intensity perturbations increased neuromuscular activity (47). However, no significant differences were found in PBS. Future studies are necessary to investigate the effect of PT on lumbar stabilization that includes more intense training. The effect of PT on patients with MS remains unclear.

Study Limitations

This study had several limitations, such as the small sample size that has no control group. Future studies that investigate the effect of PT in the long term are needed to understand the effect of PT on MS.

Conclusion

This study revealed that PT may improve static and dynamic balance, walking, and fear of falling. The balance was insufficiently developed in the mediolateral direction with the PT. Additionally, the effect of PT on lumbar stabilization in MS was not determined in our study. Major conclusions were limited by the small sample size; however, the observed results may contribute to designing future trials.

Ethics

Ethics Committee Approval: This is a pilot study that was approved by Gaziantep University, Clinical Researches Ethics Committee in June 2017 (number: 2017/255).

Informed Consent: Informed consent was obtained from all participants.

Peer-review: Externally peer reviewed.

Authorship Contributions

Surgical and Medical Practices: T.M., H.Y., Y.Y., A.A., Concept: T.M., H.Y., Design: T.M., H.Y., Data Collection or Processing: T.M., A.A., Analysis or Interpretation: T.M., H.Y., Y.Y., A.A., Literature Search: T.M., H.Y., Writing: T.M., H.Y., Y.Y., A.A.

Conflict of Interest: No conflict of interest was declared by the authors.

Financial Disclosure: The authors declared that this study received no financial support.