Effects of whole body vibration on hormonal & functional indices in patients with multiple sclerosis

Exercise is beneficial for multiple sclerosis (MS) patients, especially on fatigue which is related to quality of life (QoL), as compared with a neurological rehabilitation protocol in subjects with mild to moderate disability12. Whole-body vibration (WBV) as a training method causes rapid contraction and relaxation in the muscles and is based on the mechanical multi-dimensional oscillations of muscle-nervous system3. The WBV increases the flow of blood, and lymphatic flow through the body3, and can also increase the force of muscles in the short duration of time with less fatigue4, which may improve some aspects of postural control in individuals with disability or impaired vision5. Schuhfried et al6 have demonstrated that WBV may have a positive effect on postural control and mobility in MS patients, and van Nes and colleagues7 have found WBV as more effective on spasticity, muscle strength and motor performance in adults with stroke by comparing WBV with resistance training.

One of the most common complications of MS is the sedentary lifestyle which is due to changes in body composition, decrease muscle mass, and increase fat mass1. Changes in adipose tissue also affect leptin secretion. Leptin concentrations correlated positively with expression in subcutaneous fat, and leptin expression was also correlated with BMI8. Ghrelin modulates energy stores and expenditure in the adipocytes6. Ghrelin gene expression has been detected in subcutaneous and visceral adipose tissue8. There are evidences that suggest certain hormones like leptin and ghrelin (natural antagonists of leptin) are involved in the pathogenesis of MS and also regulate food intake, energy expenditure and metabolism9.

Changes in hormonal concentrations in humans and rats have been described after WBV training1011. Moreover, a role for testosterone has been proposed in the pathophysiology of MS10, so it would be useful to determine the hormonal changes during WBV and their contributions to clinical response in MS patients. This study was designed to determine the effects of WBV training on expanded disability status scale (EDSS), fatigue, quality of life, functional and physical indices consisting of balance, walking speed, functional mobility, functional muscle endurance, and walking endurance and serum levels of ghrelin, leptin, and testosterone in MS patients.

Material & Methods

This study was conducted between February 2010 and February 2011 under the auspices of the Isfahan University of Medical Sciences, Alzahra Multiple Sclerosis Clinic (AMSC), Isfahan, Iran. The study protocol was approved by the Local Ethics Committee affiliated to the Isfahan University of Medical Sciences, Iran.

The study design was randomized controlled trial. Thirty four patients attending AMSC (age: 38.76 ± 9.66 yr, height: 162.00 ± 0.07 cm, weight: 62.38 ± 8.71 kg, BMI: 23.53 ± 3.34 kg/m², EDSS; 3.11± 0.99) with definite MS according to McDonald's criteria12, with relapsing- remitting (RR) form of the disease and EDSS 1.5-5 (from 40 patients as sample size) were enrolled in the study. The exclusion criteria included pregnancy, epilepsy, cancer, using prosthetic, diabetes, cardiovascular or pulmonary diseases, diplopia, and any type of orthopedic conditions including degenerative disc disease, back and spine conditions, arthritic conditions, degenerative hip or knee, paediatric injuries in hip, knee, and ankle, trauma, and osteoarthritis. All participants according to their sex were randomly assigned to a WBV training group (men=5, women=12) and a control group (men=4, women=13). Subjects in the experimental group participated in protocol of training for 10 wk. The control group continued their normal life, without adding physical activity to their lifestyle. Intended variables were measured during five days before starting the protocol as pretest and measured again 72 h after the end of the protocol. The weekdays of the test for each participant were the same. The time of blood sampling was between 0900 - 1200 h and each participant had specific times for blood sampling as pre- and post-test.

Variables consisted of EDSS, fatigue, quality of life, functional and physical indices including balance, walking speed, functional mobility, functional muscle endurance, and walking endurance. All tests of variables were done by the same investigator at the recording session of the post-tests who were blinded in the pre-tests. Peripheral blood samples were collected to determine the serum levels of ghrelin, leptin, and testosterone.

The training group completed supervised vibration training on the vibration platform for 10 consecutive weeks according to a progressive programme. Prior to testing, subjects were allowed to be familiar with the vibration procedures. The protocol of the training was designed with low intensity and gradually its intensity was increased. During the 10 wk training session each participant came for training three times a week with 48 h rest between each session. At the beginning of each training session the participants warmed-up by performing static stretching movements such as hamstring stretch, body twister, heel cord stretch, and quadriceps stretch, and then pedalling on a cycle ergometer for 5-10 min. The protocol of WBV (frequency and amplitude were set at 2-20 Hz and 2 mm, respectively) consisted of 15 sets of vibrations with three repetition. Duration of each set was one minute. Each participant stood on the vibration platform for 30 sec and consequently had rest for 30 sec. Between each set the patients had one minute to take rest. The breaks between the individual series were designed to prevent rapid fatigue. After the eighth set, patients had a five- minute rest on chair. As the protocol was incremental, the duration of each set was 30 sec in the first week, and then reached to two minutes in the last week. The 15 sets consisted of squat [R-L (Right- Left) foot forward with a knee angle of 120)], deep squat (R-L foot forward with a knee angle of 90), lunge (R-L foot forward), sitting forward bend, modified press up position, one leg stance (R-L foot elevated), deep lunge (R-L foot forward), hip raise (R-L foot forward with a knee angle of 90) and calf massage. The participants maintained a static position on the platform while performing the above positions. The calf massage was performed in the last set of training. The control group continued their normal lifestyle without any training.

Measurements: Vital signs (such as temperature, blood pressure, and breath rate) before and after each training session were monitored to assure patients΄ safety throughout the tests.

(i) Disability, fatigue, and quality of life - EDSS was determined by a neurologist who was blinded to this study. The Kurtz's EDSS is a method of quantifying disability in multiple sclerosis12. The presence and severity of fatigue were assessed by mean of the modified fatigue impact scale (MFIS)13. The Multiple Sclerosis Quality of Life-54 questionnaire (MSQOL-54) was used to assess health-related quality of life, which has been translated, culturally adapted and validated in an Iranian population14.

(ii) Functional and physical indices - Berg balance scale was used to measure balance15. Functional reach was also used to measure the standing balance16. Timed 10-meters walk test (10 MWT) was used to evaluate gait speed17. The Timed up and go (TUG) test was used to assess the functional mobility17. The timed chair rise test was used to evaluate the local functional muscle endurance lower body extremity1718. Modified press up position was used to assess upper body local functional muscle endurance18. The six minutes walk test (6MWT) measured the distance (in meters) walked within six minutes to assess an individual^’ s walking endurance level17.

(iii) Blood sample measurements - Venous blood samples (10 ml) were obtained from the antecubital vein of patients in a seated position. The serum samples were stored at -80°C for miximum 12 wk or until analysis. The concentrations of ghrelin, leptin, and testosterone were measured by enzyme immunoassay method19.

Statistical analysis: Relevant statistical analyses were performed using SPSS version 15 (SPSS, Inc., Chicago, USA). Descriptive analyses were adopted for demographic and clinical characteristics reported as means ± SD. Before the statistical analysis Levene's test was used to show homogeneity of variances between the two groups before the start of the protocol. Kolmogorov-Smirnov test was used for determination of the normality of the distributions. Differences among groups were assessed by using analysis of covariate (ANCOVA).

Results

Thirty of the 34 patients recruited for the investigation completed the study and 16 of 17 in the study group completed the training programme sessions (Figure). Demographic and clinical characteristics are shown in Table I. There were no significant differences in baseline of age, weight, BMI, form of disease, disease duration, and EDSS between the two groups. The EDSS scores and fatigue scale score before and after 10 wk of protocol of training for both the groups are presented in Table II. The experimental group had 15.06 per cent significant (P<0.01) decrease in EDSS. After the training, the participants in the experimental group expressed no significant changes in the MFIS scores. Functional and physical indices are presented in Table III. Our results revealed significant improvement in some of the variables of functional and physical indices like a significant increase in the balance (15.00%), and walking endurance (47.99%). Pre- and post-test mean values of experimental and control groups on all dimensions of the MSQOL-54 were adjusted in Table IV. There was no significant overall effect of training on quality of life. In addition, low intensity exercise and WBV training had not significantly changed the serum levels of leptin, ghrelin ghrelin/leptin ratio, testosterone, and testosterone/leptin ratio (P<0.05) (Table V).

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Figure

Study design flowchart.

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Table I Characteristics of the patients with multiple sclerosis (MS) who completed the study protocol and controls

Table II Before and after intervention values of expanded disability status scale (EDSS) and modified fatigue impact scale (MFIS) scores in patients

Table III Before and after intervention values for functional and physical indices in the studied patients

Table IV Before and after intervention values for Multiple Sclerosis Quality of Life-54 Questionnaire (MSQOL-54) scores in the studied patients

Table V Before and after intervention levels of hormones in patients

Discussion

The results of this study indicated that unlike the control group, participants in the experimental group had significant decrease in EDSS and in some variables of functional and physical indices that included significant increase in the balance and walking endurance.

Significant decrease in patients’ EDSS was not in line with an earlier study1 which showed no changes in the EDSS of patients after WBV training1. The result of our study showed WBV training had no significant decrease in fatigue in MS patients, which was similar to that shown by Alguacil Diego et al20 who demonstrated vibrotherapy had no significant effect on fatigue in multiple sclerosis patients.

Our results also showed no significant change in the MSQOL-54 scores. Schyns et al21 reported that whole body vibration had no significant effect on QoL as measured by MSIS-29, which was similar to what was observed in this study. Limited walking prevents MS patients from participating in family and social activities and is a major determinant of overall impairment in ambulatory MS patients22. However, Rampello et al1 showed that aerobic training significantly increased the emotional well-being, energy, and health distress scores. The mechanism of action of these changes is not clear and may not be related directly to the training programmes or baseline physical ability of patients. Aerobic and strength exercise showed an effect on the quality of life in patients with mild multiple sclerosis and it could improve the well-being of the participants23. Both intervention programmes facilitate the patient's socialization, which in itself may have contributed to some of the beneficial effects. Moreover, it has been demonstrated that exercise may enhance psychological well-being via a strong placebo effect24. The improvement observed in the quality of life could be explained by several reasons including improving socialization and decreasing isolation, promoting well-being and improving self-esteem, preventing symptoms secondary to MS (muscle atrophy, joint contractions, pressure sores), maintaining or improving range of motion and flexibility of joints, and endurance potential, and muscle strength23. Variable results from different studies could be due to different methodologies used for training and different scales used for measuring QoL. Moreover, factors like culture, and economic conditions may also contribute to quality of life and well-being of patients.

Our study showed significantly increased balance after training sessions. In our earlier study25, after eight weeks of WBV training on MS patients the training group showed a significant increase in balance. Claerbout et al15 demonstrated after three weeks WBV in hospitalized MS persons, the Berg balance score was larger in training group than in the control group, but not significant. Another study showed that the WBV had significant improvements in standing balance from baseline16. Previously, Schuhfried et al6 studied the effect of whole body vibration at low amplitude (2.0-4.4 HZ oscillations at 3-mm amplitude) on 12 MS patients with moderate disability (EDSS 2.5-5), and they showed that WBV training had a positive influence on mobility and postural control. Balance problems are caused by a limited capacity to integrate visual, proprioceptive and vestibular stimuli for determination of the position of the body in space5. Mason et al16 showed that the WBV caused significant improvements in the time of 10-m walk at eight weeks. Another study21 reported four weeks vibration therapy in multiple sclerosis causing non significant improvement in 10-m walk. The result of our study showed no significant effect on walking speed and endurance similar to other studies161721. Our study showed no significant effect on functional mobility (chair rise time). In a study three-week WBV training showed no significant effect on chair raise test17. Our study demonstrated no significant effect in muscle endurance but significantly increase in walking endurance (6MWT). Hilgers et al17 reported that three weeks of WBV caused significantly greater improvements in the 6-min walk test in MS patients. In addition, the walking distance (6MWT) was found to be inversely related to the EDSS scores126. Previous studies have shown that WBV is associated with an increase in lower limb muscle strength, which is essential for postural stability2126. Schyns et al21 studied the effects of WBV training in 16 MS patients, and observed that WBV could have positive effects on muscular force and muscle spasm of MS patients. Delecluse et al26 have suggested that WBV has a great potential in a therapeutic context where it may enhance muscular performance in patients and elderly, who are not able to perform standard exercise programme. WBV provides a strong sensory stimulus which activates the muscle spindles, which might enhance proprioception, which in turn might be the reason for improvement in balance with WBV training5. It seems that this increase in distance during six minutes walking in MS patients, obtained following WBV training may be due to the effects of the training on the recruitment of more motor units1.

Previous studies on WBV training in MS had not focused on the role of functional, physical, psychosocial, and hormonal changes in MS patients. Also, the results showed that WBV training had no significant changes in leptin, ghrelin, ghrelin/leptin ratio, testosterone, and testosterone/leptin ratio. Leptin, a cytokine-like hormone with T helper 1 (Th1) promoting effects, may play a pathogenic role in MS and can be a useful marker of disease activity and response to therapy92627. It has also been shown that ghrelin mediates opposite effects of leptin on peripheral immune responses. In fact, ghrelin blocks the leptin-induced secretion of proinflammatory cytokines9. Increase in levels of ghrelin due to improvement in physical fitness could also be responsible for the observed improvement in MS patients, which might be due to anti-inflammatory effects of ghrelin28.

Sicotte et al29 have suggested that testosterone treatment has potential neuroprotective effects in men with relapsing-remitting MS. Another study showed a significant increase in testosterone hormone concentration and neuromuscular performance following WBV in healthy men10 and suggested that WBV influenced proprioceptive feedback mechanisms and specific neural components, leading to improvement of neuromuscular performance46. In an earlier study no significant changes were identified in salivary concentration of testosterone in responses to a single session of whole body vibration exercise in healthy young men30.

In conclusion, our results showed that long term use of WBV might create positive effects on EDSS and some variables of physical fitness in MS patients, but no improvement in quality of life and fatigue. In addition, WBV showed no change in the serum levels of ghrelin, leptin, ghrelin/leptin ratio, testosterone, and testosterone/leptin ratio. These positive effects of WBV could be temporary, and related to the duration of the protocol and detraining could lead to a reduction or loss in the effects of WBV. However, the effects of this method of training can be valuable as effective factors in reducing patient's inability.