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

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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.
2014 Elsevier Ltd. All rights reserved.

niversitesi, Saglk Hizmetleri Meslek Yu


* Corresponding author. Ankara U
lu
ksekokulu, Ortopedik Ortez Protez Bo
mu
, Fatih Caddesi 197/A,
06290 Kec
io
ren, Ankara. Tel.: 90 312 357 32 42; fax: 90 312 380 48 68.
E-mail address: sguner@ankara.edu.tr (S. Guner).
http://dx.doi.org/10.1016/j.jbmt.2014.04.004
1360-8592/ 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 persons 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 (Menieres 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

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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Yoga therapy and ambulatory multiple sclerosis


Table 1

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

Cobblers 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

Childs Pose

Navasana

Boat Pose

Marichyasana

Marichis 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

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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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 subjects 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.

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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Yoga therapy and ambulatory multiple sclerosis


Table 2
controls.

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

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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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).

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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Yoga therapy and ambulatory multiple sclerosis


Table 5

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.

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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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.

References
Andreasen, A., Stenager, E., Dalgas, U., 2011. The effect of exercise therapy on fatigue in multiple sclerosis. Mult. Scler. 17,
1041e1054.
Armutlu, K., Korkmaz, N.C., Keser, I., et al., 2007. The validity and
reliability of the fatigue severity scale in Turkish multiple
sclerosis patients. Int. J. Rehabil. Res. 30 (1), 81e85.
Benedetti, M.G., Piperno, R., Simoncini, L., Bonato, P., Tonini, A.,
Giannini, S., 1999. Gait abnormalities in minimally impaired
multiple sclerosis patients. Mult. Scler. 5, 363e368.
Berg, K.O., Wood-Dauphinee, S.L., Williams, J.I., Maki, B., 1992.
Measuring balance in the elderly: validation of an instrument.
Can. J. Public Health 83 (Suppl. 2), S7eS11. JuleAug.
Bourdette, D., et al., 2004. COmplementary Therapies in
Neurology: an Evidence Based Approach. Parthenon Publishing,
New York, pp. 291e302.
Briken, S., Gold, S.M., Patra, S., Vettorazzi, E., Harbs, A.,
Ketels, G., et al., 2013. Effects of exercise on fitness and

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

MODEL

Yoga therapy and ambulatory multiple sclerosis


cognition in progressive MS: a randomized, controlled pilot trial.
Multiple Scler. J., 1e9. Oct 24.
Cattaneo, D., Jonsdottir, J., 2009. Sensory impairments in quiet
standing in subjects with multiple sclerosis. Mult. Scler. 15,
59e67.
Cattaneo, D., Jonsdottir, J., Repetti, S., 2007. Reliability of four
scales on balance disorders in persons with multiple sclerosis.
Disabil. Rehabil. 29, 1920e1925.
Chandraratna, D., 2010. MSIF Survey on Employment. Report.
Multiple Sclerosis International Federation, London, UK.
Citaker, S., Gunduz, A.G., Guclu, M.B., Nazliel, B., Irkec, C.,
Kaya, D., 2011. Relationship between foot and standing balance
in patients with multiple sclerosis. Gait Posture 34, 275e278.
Cotman, C.W., Berchtold, N.C., Christie, L.A., 2007. Exercise
builds brain health: key roles of growth factor cascades and
inflammation. Trends Neurosci. 30, 464e472.
Coulter, D., 2001. Anatomy of Hatha Yoga: a Manual for Students,
Teachers and Practitioners. Body and Breath, Honesdale, PA,
USA.
Cowen, V.S., Adams, T.B., 2005. Physical and perceptual benefits
of yoga asana practice: results of a pilot study. J. Bodyw. Mov.
Ther. 9 (3), 211e219.
Crenshaw, S.J., Royer, T.D., Richards, J.G., Hudson, D.J., 2006.
Gait variability in people with multiple sclerosis. Mult. Scler. 12,
613e619.
Dalgas, U., Stenager, E., Jakobsen, J., et al., 2009. Resistance
training improves muscle strength and functional capacity in
multiple sclerosis. Neurol 73, 1478e1484.
DiBenedetto, M., Innes, K.E., Taylor, A.G., Rodeheaver, P.F.,
Boxer, J.A., Wright, H.J., et al., 2005. Effect of a gentle iyengar
yoga program on gait in the elderly: an exploratory study. Arch.
Phys. Med. Rehabil. 86 (9), 1830e1837.
Esmonde, L., Long, A.F., 2008. Complementary therapy use by
persons with multiple sclerosis: benefits and research priorities.
Complement. Ther. Clin. Pract. 14 (3), 176e184. Aug.
Eudora, Seyfer, Lorna, Bell, 1990. Gentle Yoga: a Guide to Lowimpact Exercise. Celestial Arts, pp. 4e11.
Fishman, L., Small, Eric, 2007. Yoga and Multiple Sclerosis. Demos
Medical Publishing, New York.
Fisk, J.D., Pontefract, A., Ritvo, P.G., Archibald, C.J., Murray, T.J.,
1994a. The impact of fatigue on patients with multiple sclerosis. Can. J. Neurol. Sci. 21, 9e14.
Fisk, J., Ritvo, P., Ross, L., Haase, D., Marrie, T., Schlech, W.,
1994b. Measuring the functional impact of fatigue : initinal
validation of the fatigue impact scale. Clin. Infect. Dis. 18,
79e83.
Flachenecker, P., Kumpfel, T., Kallmann, B., et al., 2002. Fatigue
in multiple sclerosis: a comparison of different rating scales and
correlation to clinical parameters. Mult. Scler. 8, 523e526.
Flegel, M., Knox, K., Nickel, D., 2012. Step-length variability in
minimally disabled women with multiple sclerosis or clinically
isolated syndrome. Int. J. Multiple Scler. Care 14, 26e30.
Garrett, M., Coote, S., 2009. Multiple sclerosis and exercise in
people with minimal gait impairment: a review. Phys. Ther. Rev.
14, 169e180.
Garrett, M., Hogan, N., Larkin, A., Saunders, J., Jakeman, P.,
Coote, S., 2013. Exercise in the community for people with
minimal gait impairment due to MS: an assessor-blind randomized controlled trial. Mult. Scler. 19 (6), 782e789. May.
Gehlsen, G., Beekman, K., Assmann, N., Winant, D., Seidle, M.,
Carter, A., 1986. Gait characteristics in multiple sclerosis:
progressive changes and effects of exercise on parameters.
Arch. Phys. Med. Rehabil. 67, 536e539.
Gijbels, D., Alders, G., Van Hoof, E., et al., 2010. Predicting
habitual walking performance in multiple sclerosis: relevance of
capacity and self-report measures. Mult. Scler. 16, 618e626.
Givon, U., Zeilig, G., Achiron, A., 2009. Gait analysis in multiple
sclerosis: characterization of temporal-spatial parameters using

9
GAITRite functional ambulation system. Gait Posture 29,
138e142.
Hebert, J.R., Corboy, J.R., 2013. The association between multiple
sclerosis related fatigue and balance as a function of central
sensory. Gait Posture 38, 37e42.
Heesen, C., Bo
hm, J., Reich, C., et al., 2008. Patient perception of
bodily functions in multiple sclerosis: gait and visual function
are the most valuable. Mult. Scler. 14 (7), 988e991. Aug.
Hill, K., Smith, R., Fearn, M., Rydberg, M., Oliphant, R., 2007.
Physical and psychological outcames of a supported physical
activity program for older carers. J. Aging Phys. Act. 15 (3),
257e271.
Holden, M.K., Gill, K.M., Magliozzi, M.R., Nathan, J., PiehlBaker, L., 1984. Clinical gait assessment in the neurologically
impaired. Reliability and meaningfulness. Phys. Ther. 64,
35e40.
Jones, R., Rees, D.P., Campbell, M.J., 1994. Tibialis anterior surface EMG parameters change before force output in multiple
sclerosis patients. Clin. Rehabil. 8, 100e106.
Krupp, L.B., LaRocca, N.G., Muir-Nash, J., Steinberg, A.D., 1989.
The Fatigue Severity Scale. Application to patients with multiple sclerosis and systemic lupus erythematosus. Arch. Neurol.
46, 1121e1123.
Lasater, Hanson J., 2009. Yoga Body, Anatomy, Kinesiology, and
Asana, first ed. Rodmell Press, China.
Lerdal, A., Celius, E.G., Krupp, L., Dahl, A.A., 2007. 2007 A prospective study of patterns of fatigue in multiple sclerosis. Eur.
J. Neurol. 14, 1338e1343.
Lord, S., Wade, D., Halligan, P., 1998. A comparison of two physiotherapy treatment approaches to improve walking in multiple
sclerosis : a pilot randomized study. Clin. Rehabil. 12, 447e486.
Martin, C.L., Phillips, B.A., Kilpatrick, T.J., et al., 2006. Gait and
balance impairment in early multiple sclerosis in the absence of
clinical disability. Mult. Scler. 12, 620e628.
McCullagh, R., Fitzgerald, A.P., Murphy, R.P., 2008. Long-term
benefits of exercising on quality of life and fatigue in multiple
sclerosis patients with mild disability: a pilot study. Clin.
Rehabil. 22 (3), 206e214.
Meyer, P.F., Oddsson, L.I., De Luca, C.J., 2004. The role of plantar
cutaneous sensation in unperturbed stance. Exp. Brain Res. 156,
505e512.
Molt, R.W., Goldman, M.D., Benedict, R.H., 2010. Walking
impairment in patients with multiple sclerosis: exercise training
as a treatment option. Neuropsychiatr. Dis. Treat. 6, 767e774.
Oken, B.S., Kishiyama, S., Zajdel, D., Bourdette, D., Carlsen, J.,
Haas, M., et al., 2004. Randomized controlled trial of Yoga and
exercise in multiple sclerosis. Neurology 62, 2058e2064.
Orsnes, G.B., Sorensen, P.S., Larsen, T.K., Ravnborg, M., 2000.
Effect of baclofen on gait in spastic MS patients. Acta Neurol.
Scand. 101, 244e248.
Paltamaa, J., Sarasoja, T., Leskinen, E., et al., 2007. Measures of
physical functioning predict self-reported performance in selfcare, mobility, and domestic life in ambulatory persons with
multiple sclerosis. Arch. Phys. Med. Rehabil. 88, 1649e1657.
Petajan, J., Gappmaier, E., White, A.T., et al., 1996. Impact of
aerobic training on fitness and quality of life in multiple sclerosis. Ann. Neurol. 39, 432e441.
Prakash, R.S., Patterson, B., Janssen, A., et al., 2011. Physical
activity associated with increased resting-state functional
connectivity in multiple sclerosis. J. Int. Neuropsychol. Soc. 17,
986e997.
Riley, D., 2004. Complementary Therapies in Neurology: an
Evidence-based Approach. Parthenon Publishing, New York,
pp. 159e167.
Rodgers, M.M., Mulcare, J.A., King, D.L., Mathews, T., Gupta, S.C.,
Glaser, R.M., 1999. Gait characteristics of individuals with
multiple sclerosis before and after a 6-month aerobic training
program. J. Rehabil. Res. Dev. 36, 183e188.

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

MODEL

10
Sahin, F., Yilmaz, F., Ozmaden, A., et al., 2008. Reliability and
validity of the Turkish version of the Berg Balance Scale. J.
Geriart Phys. Ther. 31 (1), 32e37.
Sandroff, B.M., Sosnoff, J., Molt, R., 2013. Physical fitness, walking
performance, and gait in multiple sclerosis. J. Neurol. Sci. 328,
70e76.
Scheinberg, L., Holland, N., La Rocca, N.G., Laitin, P., Bennett, A.,
Hall, H., 1980. Multiple sclerosis. Earning a living. N Y State J.
Med. 80, 1395e1400.
Smedal, T., Lygren, H., Myhr, K., Moe-Nilssen, R., Gjelsvik, B.,
Gjelsvik, O., et al., 2006. Balance and gait improved in patients
with MS after physiotherapy based on the Bobath concept.
Physiother. Res. Int. 11 (2), 104e116.
Socie, M.J., Molt, R.W., Pula, J.H., Sandroff, B.M., Sosnoff, J.,
2013. Gait variability and disability in multiple sclerosis. Gait
Posture 38, 51e55.
Stroud, N.M., Minahan, C.L., 2009. The impact of regular physical
activity on fatigue, depression and quality of life in persons with
multiple sclerosis. Health Qual. Life Outcomes 7, 68.
Sutherland, G., Andersen, M.B., Stoove, M.A., 2001. Can aerobic
exercise training affect health-related quality of life for people
with multiple sclerosis? J. Sport Exerc. Psychol. 23, 122e125.
Syndulko, K., Ke, D., Ellison, G.W., Baumhefner, R.W., Myers, L.W.,
Tourtellotte, W.W., 1996. Comparative evaluations of neuro
performance and clinical outcome assessments in chronic progressive multiple sclerosis: I. Reliability, validity and sensitivity

S. Guner, F. Inanici
to disease progression. Multiple Sclerosis Study Group. Mult.
Scler. 2, 142e156.
Thoumie, P., Lamotte, D., Cantalloube, S., Faucher, M.,
Amarenco, G., 2005. Motor determinants of gait in 100 ambulatory patients with multiple sclerosis. Mult. Scler. 11, 485e491.
Tran, M.D., Holly, R.G., Lashbrook, J., Amsterdam, E.A., 2001.
Effect Hatha yoga practice on the health- related aspects of
physical fitness. Prev. Cardiol. 4, 165e170.
Ulger, O., Yagl, N., 2011. 2011 Effects of yoga on balance and gait
properties in women with musculoskeletal problems: a pilot
study. Complement. Ther. Clin. Pract. 17, 13e15.
Van Emmerik, R.E., Remelius, J.G., Johnson, M.B., Chung, L.H.,
Kent- Braun, J.A., 2010. Postural control in women with multiple sclerosis: effects of task, vision and symptomatic fatigue.
Gait Posture 32, 608e614.
Velikonja, O., Curic, K., Ozura, A., Jazbec, S.S., 2010. Influence of
sports climbing and yoga on spasticity, cognitive function, mood
and fatigue in patients with multiple sclerosis. Clin. Neurol.
Neurosurg. 112, 597e601.
Weinshenker, B.G., Bass, B., Rice, G.P., et al., 1989. The natural
history of multiple sclerosis: a geographically based study. I.
Clinical course and disability. Brain 112, 133e146.
Winterholler, M., Erbguth, F., Neundo
rfer, B., 1997. The use of
alternative medicine by multiple sclerosis patientsepatient
characteristics and patterns of use. Fortschr Neurol. Psychiatr.
65, 555e561.

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