Yoga therapy and ambulatory multiple sclerosis Assessment of gait analysis parameters, fatigue and balance.

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Journal of Bodywork & Movement Therapies (2014) xx, 1e10

Available online at www.sciencedirect.com

ScienceDirect journal homepage: www.elsevier.com/jbmt

ORIGINAL CLINICAL RESEARCH

Yoga therapy and ambulatory multiple sclerosis Assessment of gait analysis parameters, fatigue and balance Senem Guner, PT a,*, Fatma Inanici, MD b a Department of Orthopedic Prosthetics and Orthotics, Vocational School of Health, Ankara University, Ankara, Turkey b Department of Physical and Rehabilitation Medicine, Hacettepe University Medical School, Ankara, Turkey

Received 3 September 2013; received in revised form 27 February 2014; accepted 3 March 2014

KEYWORDS Multiple sclerosis; Yoga therapy; Gait analysis; Balance; Fatigue

Summary Background and Objective: Gait impairment, falls due to balance problems and fatigue are among the most important complaints in patients with multiple sclerosis (MS) and cause significant functional limitation. Use of complementary and alternative medicine (CAM) to help symptom management and to improve quality of life is growing among MS patients. Yoga is widely used as one of these CAM interventions, however, the number of studies that show the efficacy of yoga training in MS is inadequate. In this study, we aimed to evaluate the effects of a short term yoga program on fatigue, balance and gait in patients with MS. Method: Eight volunteer ambulatory MS patients with clinically definite relapsing remitting MS whose Expanded Disability Status Score (EDSS) is less than or equal to 6.0, and eight healthy subjects were included in the study. Patients participated in 12 weeks of a bi-weekly yoga program under supervision. At their baseline and after yoga therapy, the Fatigue Severity Scale (FSS) and Berg Balance Scale (BBS) are used to assess fatigue and balance. Three dimensional gait analysis is done using the Vicon 612 system with six cameras and two Bertec force plates, before and after therapy. Results: After short term yoga therapy, statistically significant achievements were obtained in fatigue, balance, step length and walking speed. Although sagittal plane pelvis and hip angles, ankle plantar flexor moment, powers generated at the hip and ankle joints at the pre-swing were improved, the improvements were not statistically significant. Conclusion: Yoga therapy is a safe and beneficial intervention for improving fatigue, balance and spatiotemporal gait parameters in patients with MS. Further studies with a larger sample size and longer follow-up will be needed to evaluate the long term effects of yoga therapy. ª 2014 Elsevier Ltd. All rights reserved.

¨ niversitesi, Saglık Hizmetleri Meslek Yu * Corresponding author. Ankara U ¨lu ¨ksekokulu, Ortopedik Ortez Protez Bo ¨mu ¨, Fatih Caddesi 197/A, 06290 Kec ¸io ¨ren, Ankara. Tel.: þ90 312 357 32 42; fax: þ90 312 380 48 68. E-mail address: [email protected] (S. Guner). http://dx.doi.org/10.1016/j.jbmt.2014.04.004 1360-8592/ª 2014 Elsevier Ltd. All rights reserved.

Please cite this article in press as: Guner, S., Inanici, F., Yoga therapy and ambulatory multiple sclerosis Assessment of gait analysis parameters, fatigue and balance, Journal of Bodywork & Movement Therapies (2014), http://dx.doi.org/10.1016/j.jbmt.2014.04.004

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Introduction Fatigue, balance and gait disturbances are among the most common problems in patients with multiple sclerosis (MS) which cause important personal, social and economic burdens, such as difficulties in the activities of daily living, reduced productivity, unemployment and reduced quality of life (Chandraratna, 2010; Heesen et al., 2008; Paltamaa et al., 2007). Seventy-five to ninety percent of patients with MS report fatigue and 55% describe it as one of their worst symptoms, and 85% of patients report gait disturbance as their main complaint (Flachenecker et al., 2002; Fisk et al., 1994; Lerdal et al., 2007; Scheinberg et al., 1980). Within 15 years of the onset of MS, almost half of patients require walking assistance and 10% become wheelchair dependent (Weinshenker et al., 1989). Since currently there is no cure with pharmacological treatment, and drug therapy has a limited effect on the disability, symptomatic and supportive therapies are important (Bourdette et al., 2004; Riley et al., 2004). There is a progressive trend towards the use of yoga as a mind-body complementary and alternative medicine intervention, adjunct to medical treatment by MS patients (Esmonde et al., 2008; Oken et al., 2004; Winterholler et al., 1997). Although it is popular and reported as highly satisfactory by patients with MS, there are few yoga studies in MS using objective quantitative outcome measures. Exercise is extremely important for individuals with MS. Although findings are heterogeneous, many studies support the beneficial effects of different types of exercise, i.e. endurance and resistance training, combined programs, and aquatic exercises, on strength, endurance, fatigue, balance, walking, mood, and health-related quality of life in patients with MS (Andreasen et al., 2011; Dalgas et al., 2009; Garrett et al., 2009, 2013; Oken et al., 2004; Petajan et al., 1996; Sutherland et al., 2001). Since MS is characterized by various neurologic deficits, an optimal exercise modality does not exist. The benefits of yoga postures (asanas), working with the breath (pranayama) and meditation may include increased body awareness, release of muscular tension, increased coordination and balance, increased flexibility and strength, control over fatigue, improved circulation and breathing. Yoga focuses on improving a person’s physical, mental and spiritual wellbeing. The main aim of yoga is to harmonize the body, mind and spirit through a combination of poses, meditation and breathing exercises. Unifying body, mind and spirit allows one to achieve a sense of wholeness, peace and selfrealization. Yoga poses are constructed in a way that works towards a common goal, such as battling fatigue, reducing spasticity, improving cognitive function and increasing range of motion (Fishman et al., 2007; Velikonja et al., 2010). The purpose of this study was to determine the effects of 12 weeks of short term yoga therapy on fatigue, balance and gait parameters in people with multiple sclerosis (MS).

Methods After getting informed consent, eight volunteer ambulatory patients with multiple sclerosis (MS), with clinically definite relapsing remitting MS (which presents with fluctuations of

S. Guner, F. Inanici symptoms and mild disability), and whose Expanded Disability Status Score (EDSS) was less than or equal to 6.0, and eight age, gender and body mass index similar healthy subjects were included in the study. Three patients were on Interferon beta 1a; two on Glatiramer acetate; one on Tizanidine, and one on Escilatopram. Exclusion criteria were: being non-ambulatory, use of pharmacological agents to control fatigue (including major sleep disorder, clinical depression, anemia, hypothyroidizim and B12 deficiency), significant balance problems (including cerebral vascular accident and peripheral neuropathy), peripheral vestibular disorders (Meniere’s disease, benign positional paroxysmal vertigo, acoustic neuroma, unilateral/bilateral vestibular hypofunction), or had undergone steroid therapy within the last 4 weeks. Eight healthy subjects were assessed in gait analysis who had not taken yoga classes. Patients with MS participated in 12 weeks of bi-weekly yoga class under supervision at the University Hospital in the Yoga unit. The Yoga unit is nearly 20 square meters and 16e17 centigrade degrees. All poses (Table 1 and Fig. 1) were performed over the course of 60 min and were supported, either with a chair or by having the subject on the floor or against the wall. Where needed, poses were modified according to the capabilities of the individual patients. Specific adaptations of yoga postures for people with limited mobility due to neurological conditions such as multiple sclerosis and stroke have been described before (Eudora et al., 1990). Each pose was held for approximately 10e30 s, followed by a resting period lasting from 30 s to 1 min. Each class ended up with a 10-min deep relaxation period with the subjects lying supine (Savasana pose). Progressive relaxation and meditation techniques were introduced during this time. All patients’ took the same classes because our mind is psychologically supported by group sessions. Daily home practice was strongly encouraged, so that they could become able to do some poses without help. We were to assess the effects of yoga therapy in patients after 12 weeks yoga programs.

Fatigue and balance assessments Fatigue and balance of the patients with MS were assessed using the Fatigue Severity Scale (FSS) and Berg Balance Scale (BBS), respectively, at their baseline and after yoga therapy (Berg et al., 1992; Krupp et al., 1989). The reliability and validity of the Turkish version of both scales have been shown before (Armutlu et al., 2007; Sahin et al., 2008). The FSS, which was published in 1989 by Krupp, has nine items. For each question, the patient is asked to choose a number from 1 to 7 that indicates how much the patient agrees with each statement, where 1 indicates strong disagreement and 7 indicates strong agreement. A score of 4 or higher generally indicates severe fatigue. Flachenecker et al. reported a significant correlation between EDSS and FSS (Flachenecker et al., 2002). The BBS is a clinical scale that evaluates balance in sitting and standing and rates performance from 0 (cannot perform) to 4 (normal performance). The scale has fifteen items that explore the ability to sit, stand, lean, turn and maintain the upright position on one leg. The BBS has been


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Yoga therapy and ambulatory multiple sclerosis Table 1

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Yoga postures e asanas (Fishman et al., 2007; Lasater, 2009).

Asanas

Poses

Possible and claimed benefits

Tadasana

Mountain Pose

Dandasana

Staff Pose

Savasana

Corpse Pose

Uttanasana

Standing Forward Bend Triangle Pose

Establishes well-aligned posture, strengthens thighs, knees, and ankles, firms abdomen and buttocks, reduces flat feet Strengthens the back muscles, stretches the shoulders and chest, improves posture Relaxes, calms the brain and helps relieve stress and mild depression, reduces headache, fatigue, and insomnia, helps to lower blood pressure Stretches thoracic and lumbar spines, hamstrings, calves, and hips, strengthens the thighs and knees, reduces fatigue and anxiety Strengthens and stretches the legs, hips, and spine, stimulates the abdominal organs, helps relieve stress Stretches the adductor muscles, improve hip mobility, and coordinate these with foot eversion, stimulates abdominal organs, ovaries and prostate gland, bladder, and kidneys, Stimulates the heart and improves general circulation, helps relieve mild depression, anxiety and fatigue Calms the brain, stimulates the abdominal organs and the thyroid gland, stretches the shoulders and spine, reduces stress and fatigue Strengthens and extends the upper back and neck. Extends and strengthens the back of the body and open the chest and shoulder, extends the spinal range, stimulates abdominal organs, lungs, and thyroid, reduces anxiety, fatigue, backache, headache, and insomnia Laterally stretches the torso and one leg, improves lateral flexion, stretches hamstrings, opens the shoulders, stimulates abdominal organs and lungs. Mobilize the joints of the spine, strengthens transverse and oblique abdominal muscles, stretches the front of the shoulder. Calms the brain and helps relieve mild depression, stretches the spine, shoulders, hamstrings, stimulates the liver and kidneys, relieves anxiety, fatigue, headache, menstrual discomfort Passively flexes the lumbar and extends the thoracic spine and flexes the hips, calms the brain and helps relieve stress and fatigue Strengthens the abdomen, hip flexors, and spine, stimulates the kidneys, thyroid and prostate glands, and intestines, helps relieving stress. Uses the leverage of the arms and legs to align the sacroiliac joint, stretches the spine and shoulders, stimulates abdominal organs like the liver and kidneys Strengthens and stretches the legs, knees, and ankles, stretches the groins, spine, waist, chest and lungs, and shoulders, stimulates abdominal organs Strengthens the back and legs, calms the brain and helps relieve stress and mild depression, stretches the spine, shoulders, hamstrings, stimulates the liver, kidneys, ovaries, and uterus, soothes headache and anxiety and reduces fatigue Strengthens the abdomen, ankles, thighs, buttocks, and spine, stretches the groins, hamstrings and calves, shoulders, chest, and spine, improves coordination and sense of balance, helps relieving stress

Trikonasana Baddha Konasana

Cobbler’s Pose

Halasana

Plow Pose

Bhujangasana Setu Bandhasana

Cobra Pose Bridge Pose

Parighasana

Gate Pose

Jathara Parivartanasana Janu Sirsasana

Revolved Abdomen Pose Head to Knee Pose

Balasana

Child’s Pose

Navasana

Boat Pose

Marichyasana

Marichi’s Pose

Parsvakonasana

Extended Side Angle Pose Seated Forward Bend Pose

Paschimottanasana

Ardha Chandrasana

Half Moon Pose

validated for use in people with Multiple Sclerosis (Cattaneo D et al., 2007). The reliability of the BBS has also been examined with regards to MS (Smedal T et al., 2006, Lord S et al., 1998). The BBS is widely used by physiotherapists and takes approximately 15 min to complete. It is also used in other studies evaluating interventions in MS (Fisk J et al., 1994), therefore making it possible to compare results with other studies.

Gait analysis A three-dimensional quantitative gait evaluation was performed in the Motion Analysis Laboratory at Hacettepe

University Medical School, Department of Physical and Rehabilitation Medicine using the Vicon 612 System (Oxford Metrics, Oxford, UK) with six infrared JAI cameras at 50 Hz and two force plates (Bertec Co., Columbus, OH, USA) by the same experienced physiotherapist (SG). The standard Plug-in Gait marker set was used to capture kinematic data, i.e. 15 reflective markers were placed on anterior superior iliac spines, mid-lateral thighs, lateral knee joints, lateral shanks, lateral malleolus, second metatarsal heads, and over the posterior calcaneus bilaterally, and on sacrum mid-way between the posterior superior iliac spines. Force plates were embedded in the middle of a 10 m walkway. Before data collection, each camera and force plate were


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S. Guner, F. Inanici

calibrated. Patients were asked to walk at their comfortable self-selected walking speed when barefoot. At least 5 good trials with the subject’s footfalls landing completely within the force plates were captured. Between trials, patients rested for at least one minute to ensure that fatigue did not confound the results. Average pelvic and lower extremity joint kinematic and kinetic values for each subject were obtained from 5 trials (the average of both right and left lower extremities providing an average of 10 values for each condition). All data processing was performed using Vicon Workstation software. Kinetic data was normalized with respect to body mass. Data from MS patients was compared to those collected in the same laboratory, using the same protocol, from eight healthy subjects. All data was collected between 9 and 11 AM, MS patients feel better about themselves in the morning. Of these patients increased feelings of fatigue during the day. Statistical analyses were performed by using the SPSS software program, version 16. The Non-parametric ManneWhitney U test is used to compare patient and control groups, and the Wilcoxon test to compare baseline and after yoga measurements in patients with MS. The statistical significance level was set at p < 0.05.

Results Demographic and anthropometric features of the patients and healthy controls are shown in Table 2. All patients

Figure 1

attended every yoga session and completed the 12 week biweekly yoga program. Related to the intervention, no adverse effect is observed or reported. Compared to baseline measurements, fatigue and balance scales improved significantly in patients with MS (Table 3). Baseline spatiotemporal parameters of gait, i.e. cadence, step length and walking speed were lesser, while double support and step time were longer in patients with MS than healthy controls (Table 4). The kinematic data of all joints in all planes is shown in Fig. 2. The gait pattern among subjects with MS in the sagittal plane was characterized by an increased anterior pelvic tilt throughout the gait cycle, increased hip and knee flexion at the heel strike, lack of knee extension during the midstance, lack of hip extension during the terminal stance, reduced hip and knee extension and ankle plantar flexion at the toe off compared to controls. During the swing phase, a reduced ankle plantar flexion, knee flexion and slightly increased hip flexion were observed at baseline records in patients with MS compared to the controls. The overall sagittal plane excursion was increased at the pelvis and decreased at the hip, knee and ankle joints (see Table 5). Kinetic data is displayed in Fig. 3 and Table 6. Knee external extension moment at midstance (KM2) and ankle external dorsiflexion moment at terminal stance were significantly reduced in patients with MS at the baseline compared to the control group. In terms of power, concentric iliopsoas activity during the pre- and initial swing (HP3), eccentric rectus femoris activity during the

Pose(Asanas) and picture.


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Yoga therapy and ambulatory multiple sclerosis Table 2 controls.

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Characteristics of the MS patients and healthy

Balance and fatigue scale results. Baseline

MS patients Control group Gender (Female/Male) Age (years) (mean SD) Height (cm) (mean SD) Weigth (kg) (mean SD) BMI (mean SD) Disease duration (years) (mean SD) Time since last relapse (years) (mean SD) EDSS

Table 3

7/1 38.4 7.0

7/1 33.9 3.8

P value*

0.185

161.8 7.4 163.8 6.8 0.528 65.5 12.5 64.6 9.0

0.958

25.1 4.7 7.2 5.9

24.1 3.8 NA

0.674

3.3 2.0

NA

3.3 2.1

NA

BMI e Body mass index. EDSS e Expanded Disability Status Scale. * ManneWhitney test.

preswing (KP3) and concentric gastrosoleus activity during the preswing (AP2) were less than the control group. After the yoga program, cadence, step length and walking speed were increased distinctly; however, statistically significant improvements were obtained only in step length and walking speed when compared baseline data (see Table 4). After yoga therapy, pelvic tilt throughout the gait cycle and hip extension at the terminal stance, and among transverse plane kinematics, hip and ankle rotation angles improved (see Fig. 2). Compared to baseline, the peak plantar flexion moment (AM2), eccentric rectus femoris activity (KP3) and concentric burst of propulsive plantar flexor activity (AP2) were increased after the yoga program (see Table 6, Fig. 3). However, differences recorded in the kinematic and kinetic parameters of gait between baseline and after yoga therapy did not reach a statistically significant level (p > 0.05).

Discussion The objective of this study was to assess the effects of 12 weeks of yoga therapy on fatigue, balance and gait in ambulatory patients with MS. This is the first study that evaluates the effect of yoga on mobility by using threedimensional quantitative gait analysis in patients with multiple sclerosis. The gait analysis findings in patients with MS are in agreement with literature. Patients with MS have typically walked slowly, with a shorter stride length and prolonged double support phase, decreased cadence, and lesser joint motion than normal subjects, which results in reduced community mobility (Benedetti et al., 1999; Crenshaw et al., 2006; Gehlsen et al., 1986; Gijbels et al., 2010; Givon et al., 2009; Holden et al., 1984; Jones et al., 1994; Martin et al., 2006; Orsnes et al., 2000; Rodgers et al., 1999; Thoumie et al., 2005). Decreased walking velocity and step length are concluded as compensation for deficits in balance and postural control (Syndulko et al.,

After yoga

P value*

Fatigue Severity Scale 53.0 7.6 33.9 10.7 0.012 Berg Balance Scale 42.4 19.1 47.3 16.2 0.027 * Wilcoxon test.

1996). Gait variability might be more sensitive to dysfunction in MS than other elements such as walking velocity (Flegel et al., 2012). Michael et al. studied that gait variability is more closely related to dysfunction in MS than average gait parameters (Socie M. et al., 2013). The beneficial effects of various exercise programs on fatigue, balance and walking function in various neurologic and musculoskeletal diseases, and also in the elderly, have been reported before. Exercise is shown to promote neuroregeneration and plasticity and to improve learning and memory in rodents (Cotman et al., 2007). Our results showed that a short-term yoga program is effective on alleviating fatigue and enhancing balance in patients with MS. We evaluated fatigue by FSS. Since fatigue and depression have common symptoms, FSS is developed to differentiate fatigue from clinical depression. FSS is composed of 9 items inquiring after patients’ subjective perception of fatigue and its consequences on everyday activities (Krupp et al., 1989). Parallel to our findings, the effects of various exercise programs including yoga on improving fatigue have been published before, using different fatigue scales (McCullagh et al., 2008; Oken et al., 2004; Petajan et al., 1996; Sutherland et al., 2001; Stroud et al.,. 2009; Velikonja et al., 2010). In a recent review, the efficacy of exercise on fatigue is reported to be potentially positive, but yet unconfirmed (Andreasen et al., 2011). Hebert et al. studied that symptomatic fatigue is significantly related to balance, and is a significant predictor of balance as a function of central sensory integration in persons with MS. They support the theory that for those persons with MS who struggle to maintain steady balance during tasks that stimulate the central sensory integration process, complaints of significants levels of fatique are probable (Hebert et al., 2013). Many studies in the literature report the positive effects of yoga on gait and balance properties. Di Benedetto et al. observed significant improvements on gait in the elderly with excellent adherence rates (DiBenedetto et al., 2005). Ulger et al. showed that yoga has a positive effect on the balance and gait parameters of women with gait and balance disturbances that are caused by musculoskeletal problems (Ulger et al., 20011). Yoga would have the same effects on fatigue, because yoga exercises help build up muscle strength and endurance. Oken et al. showed the influence of yoga on fatigue, namely that there was a significant decrease of the impact of fatigue in patients with MS (Oken et al., 2004). Higher levels of fitness in MS patients are found to be correlated cross-sectionally with higher structural connectivity and higher gray matter density (Prakash et al., 2011). Some researchers have hypothesized that physiological conditioning might play a role in the development of walking and gait impairment and increased physiological conditioning might have beneficial


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S. Guner, F. Inanici Table 4

Spatiotemporal parameters. MS patients Baseline

Cadence (steps/min) Double support (sec) Foot off (%) Single support (sec) Step length (m) Step time (sec) Step width (m) Walking speed (m/sec)

Control group

P value*

P value**

0.010 0.007 0.038 0.050 0.007 0.010 NS 0.005

NS NS NS NS 0.043 NS NS 0.027

After yoga

Mean SD

Mean SD

Mean SD

95.0 22.7 0.5 0.6 66.7 7.6 0.43 0.04 0.45 0.16 0.7 0.3 0.2 0.0 0.8 0.3

99.6 27.1 0.5 0.4 65.7 6.1 0.42 0.05 0.49 0.3 0.7 0.3 0.2 0.1 1.0 0.3

117.7 9.6 0.2 0.0 62.1 2.2 0.39 0.04 0.61 0.06 0.5 0.0 0.2 0.0 1.2 0.2

* Comparison of patients with multiple sclerosis at baseline and control group by non-parametric Mann Whitney U test. ** Comparison of patients with multiple sclerosis at baseline and after yoga program by non-parametric Wilcoxon test.

Figure 2

Joint angles (degrees).


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Yoga therapy and ambulatory multiple sclerosis Table 5

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Sagittal plane joint angles (degrees).a MS patients

Max. Posterior Pelvic Tilt Max. Anterior Pelvic Tilt Pelvic Tilt ROM Max. Hip Extension Max. Hip Flexion Hip Flexion Extension ROM Max. Knee Extension Max. Knee Flexion Knee Flexion Extension ROM Max. Ankle Plantar flexion Max. Ankle Dorsiflexion Ankle Dorsi-Plantar flexion ROM a

Baseline

After yoga

Control

13.3 8.5 16.5 10.7 3.2 2.6 0.9 16.9 36.5 9.3 37.4 9.2 2.3 6.9 48.2 10.5 45.8 14.3 9.3 5.2 16.2 2.2 25.5 4.2

10.4 2.7 13.7 3.9 3.3 2.1 5.0 9.0 33.1 5.8 38.1 7.4 1.8 8.0 47.2 11.5 45.5 14.9 10.1 7.3 15.8 4.7 25.9 5.1

7.6 3.5 9.9 3.7 2.4 0.7 12.4 6.5 30.5 3.5 42.9 5.6 0.6 3.5 54.3 6.2 54.9 6.3 14.8 4.6 13.3 1.5 28.1 5.0

Differences are not statistically significant.

consequences for improving walking and gait (Molt RW et al., 2010). Sandroff et al. suggested that physiological deconditioning explains variability in walking disability in persons with MS and might multimodal exercises training interventions for improving mobility outcomes in this population. They found aerobic capacity, balance, and kneeextensor asymmetry were associated with walking performance and gait in persons with MS (Sandroff et al., 2013). Briken et al. indicated that aerobic training is feasible and could be beneficial for patients with MS, and exercise improved walking ability, depression symptoms, fatigue and several domains’ cognitive function (Briken et al., 2013). Most asanas are concerned with maintaining the health and movement of the spinal column, lower and upper extremities. For example, in Dandasana poses, one is working all spinal extensors, the psoas major and minor muscle, legs and arms. The hamstring, gluteus maximus, priformis, obturaor internus and gemelli muscles all lengthen

Figure 3

(Coulter, 2001). Stretching exercises which improve endurance, and might reduce fatigue (McCullagh et al., 2008; Stroud et al., 2009). We applied some stretching poses such as Bhujangasana, Uttasana, Paschimottasana, Janu Sirsana that might reduce fatigue in MS patients. Yoga exercises include weight-bearing balance and static postures such as Tadasana, Trikosana, Uttasana, Ardha Chandrasana that with standing movements incorporate both open and closed chain exercises for the upper and lower body. In a standing posture, only the plantar side of the foot makes contact with the ground. Cutaneous afferent inputs from the sole of the foot provide useful information to the central nervous system to assist balance (Meyer et al., 2004). Many studies showed that sensation of the sole of the foot was decreased and maintaining balance in standing is a marked problem in patients with MS (Cattaneo D et al., 2009, Van Emmerik RE et al., 2010). Yoga standing postures might improve balance, and the

Sagittal plane moments and powers.


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S. Guner, F. Inanici Table 6

Sagittal plane moments (Nmm/kg) and powers (W).

HM1 HM2 KM1 KM2 AM1 AM2 HP1 HP2 HP3 KP1 KP2 KP3 KP4 AP1 AP2

MS patients baseline

MS patients after yoga

Control group

P value*

P value**

674.4 498.2 779.7 315.4 333.6 222.1 85.7 98.6 68.1 66.1 1152.1 448.3 1.1 1.2 0.7 0.4 0.7 0.4 0.5 0.5 0.5 0.7 0.1 0.1 0.5 0.2 0.7 0.3 1.8 1.1

520.0 293.2 870.3 320.4 329.5 244.0 79.2 292.0 92.8 81.7 1234.2 418.3 0.7 0.5 0.8 0.5 0.7 0.4 0.4 0.4 0.3 0.3 0.2 0.2 0.5 0.2 0.7 0.3 2.1 1.3

843.3 250.8 834.6 200.0 309.7 203.8 296.9 159.5 81.9 36.6 1456.7 168.0 1.2 0.4 0.9 0.4 1.4 0.6 0.6 0.3 0.4 0.3 0.3 0.2 0.7 0.3 1.0 0.2 3.0 0.6

NS NS NS 0.015 NS NS NS NS 0.05 NS NS 0.021 NS NS 0.01

NS NS NS NS NS NS NS NS NS NS NS NS NS NS NS

HM1: Maximum hip flexion moment; HM2: Maximum hip extension moment. KM1: Maximum knee flexion moment; KM2: Maximum knee extension moment. AM1: Maximum ankle plantar flexion moment; AM2: Maximum ankle dorsiflexion moment. HP1: Concentric hip extensor activity during loading response; HP2: Eccentric hip flexor activity during mid-stance; HP3: Concentric activity in the hip flexors during pre-swing and initial swing. KP1: Eccentric knee extensor activity at during loading response; KP2: Concentric knee extensor activity during mid-stance; KP3: Eccentric activity in the rectus femoris during pre-swing; KP4: Eccentric activity in the hamstrings during terminal swing. AP1: Eccentric plantar flexor activity at the ankle during mid-stance and terminal stance; AP2: Concentric burst of propulsive plantar flexor activity during pre-swing. NS: not significant. * Comparison of patients with multiple sclerosis at baseline and control group by non-parametric Mann Whitney U test. ** Comparison of patients with multiple sclerosis at baseline and after yoga program by non-parametric Wilcoxon test.

effect is increased via foot sensation. C ¸ itaker et al. found the significant value of foot sensation in maintaining balance in patients with MS (Citaker et al., 2011). Yoga exercises are usually associated with isometric movements including both eccentric and concentric muscle contraction. Postures in yoga are thought to strengthen voluntary muscles and control via the autonomic nervous system. Studies in this area support claims of physiological benefits from yoga including improved strength and range of motion or flexibility (Coulter, 2001; Cowen et al., 2005; DiBenedetto et al., 2005; Hill et al., 2007; Lasater, 2009; McCullagh et al., 2008; Stroud et al., 2009; Ulger et al., 20011). Tran et al. examined the effects of the 8 week Hatha Yoga Training on muscular strength for elbow flexion, elbow extension, knee extension and knee flexion that increased isometric muscular endurance and isokinetic muscular strength in their study (Tran et al., 2001).

Conclusion Several limitations of this study should be noted. A major limitation of the present study is that the study group was relatively small. Despite the limitations of the small sample size and short term follow up, yoga therapy is found beneficial for improving fatigue, balance, step length and walking velocity in patients with MS in this study. Not significant, but visible improvements in peak pelvic tilt, peak hip extension and ankle power at push off are thought to be the resulting improvement of motor control. Future

research with larger samples and longer follow-up will be needed to evaluate the long term effects of yoga therapy. Future Yoga studies should assess isometric muscle strength and evaluate to compare combined resistance and endurance training with gait analysis.

Acknowledgments We wish to thank Yoga instructors Feride Gul Cakiroglu and Ece Akay for guidance and helping in this study.

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Fatigue induced changes to kinematic and kinetic gait parameters following six minutes of walking in people with multiple sclerosis.

Sustained-released fampridine in multiple sclerosis: effects on gait parameters, arm function, fatigue, and quality of life.

Therapeutic Yoga: Symptom Management for Multiple Sclerosis.

Fatigue and Comorbidities in Multiple Sclerosis.

Hypnotic use and fatigue in multiple sclerosis.

Objective assessment of motor fatigue in multiple sclerosis: the Fatigue index Kliniken Schmieder (FKS).

Editorial: Fatigue in Multiple Sclerosis.

Amantadine: multiple sclerosis-related fatigue.

Fatigue Management in Multiple Sclerosis.

BioKin: an ambulatory platform for gait kinematic and feature assessment.

Gait changes with balance-based torso-weighting in people with multiple sclerosis.

Effect of rhythmic auditory stimulation on gait kinematic parameters of patients with multiple sclerosis.

Examination of spatiotemporal gait parameters during the 6-min walk in individuals with multiple sclerosis.

Analysis of foot and ankle disorders and prediction of gait in multiple sclerosis rehabilitation.

Preliminary investigation of gait initiation and falls in multiple sclerosis.

Managing treatment fatigue in patients with multiple sclerosis on long-term therapy: the role of multiple sclerosis nurses.

Diagnosis and quantification of cognitive fatigue in multiple sclerosis.

Do textured insoles affect postural control and spatiotemporal parameters of gait and plantar sensation in people with multiple sclerosis?

The relationship between objective parameters of sleep and measures of fatigue, depression, and cognition in multiple sclerosis.

Body-worn sensors capture variability, but not decline, of gait and balance measures in multiple sclerosis over 18 months.

Gait impairment and optimizing mobility in multiple sclerosis.

Cognitive fatigue in individuals with multiple sclerosis undergoing immunoablative therapy and hematopoietic stem cell transplantation.

Predictors of exercise participation in ambulatory and non-ambulatory older people with multiple sclerosis.