NeuroRehabilitation 34 (2014) 323–335 DOI:10.3233/NRE-131044 IOS Press

323

Trunk muscle activity during walking in persons with multiple sclerosis: The influence of body weight support1 Eva Swinnena,d,∗ , Jean-Pierre Baeyensa,c , Seppe Pintensc , Johan Van Nieuwenhovenb , Stephan Ilsbroukxb , Ron Clijsenc , Ronald Buyle , Maggie Goossensf , Romain Meeusena,d and Eric Kerckhofsa,d a Vrije

Universiteit Brussel, Faculty of Physical Education and Physiotherapy, Advanced Rehabilitation Technology and Science (ARTS), Brussels, Belgium b National Multiple Sclerosis Centre, Melsbroek, Belgium c University College Physiotherapy Thim van der Laan, Landquart, Switzerland d Center for Neurosciences, Vrije Universiteit Brussel, Brussels, Belgium e Vrije Universiteit Brussel, Faculty of Medicine and Pharmacy, Biostatistics and Medical Informatics, Brussels, Belgium f University College Artesis, Antwerp, Belgium

Abstract. BACKGROUND: Although the trunk is important for maintaining balance during walking only very limited information about the trunk muscle activity during walking with body weight support (BWS) is reported in literature. OBJECTIVE: The aim of this study was to measure the effect of BWS on the trunk muscle activity during treadmill walking. METHODS: 14 persons with multiple sclerosis and 14 healthy persons walked on a treadmill with 0%, 10%, 20%, 30%, 50% and 70% BWS. Bilateral EMG measurements (surface electrodes) on the m. rectus abdominis, m. obliquus externus, m. erector spinae and m. multifidus were performed. The maximal muscle activation was presented as a percentage of a performance related reference contraction. A repeated measures ANOVA with simple contrasts was applied (SPSS20). RESULTS: In general when comparing walking with BWS with walking with 0% BWS there is an increase in m. obliquus externus activity and a decrease in back muscle activity. With increasing percentages of BWS an increase in activity of the abdominal muscles and a decrease in back muscle activity was found, with most changes in high percentages BWS. CONCLUSION: Based on the results, it is recommended to decrease the percentage BWS as fast as possible beneath 30% BWS. Keywords: Abdominal muscles, back muscles, body weight support, electromyography, EMG, gait, gait analysis, multiple sclerosis, rehabilitation, treadmill, walking 1 Institutional Review: The Ethical Committees of the University Hospital UZ Brussels (BUN B14320084299) and the National Multiple Sclerosis centre at Melsbroek (OG033) approved the protocol. The tests were carried out at the National Multiple Sclerosis centre, Melsbroek, Belgium Written informed consent was obtained from all study participants. ∗ Address for correspondence: Eva Swinnen, Vrije Universiteit Brussel, Faculty of Physical Education and Physiotherapy, Advanced Rehabilitation Technology and Science (ARTS), Laarbeeklaan 103, B-1090 Brussels, Belgium. Tel.:/Fax: +32 2 4774530; E-mail: [email protected].

1053-8135/14/$27.50 © 2014 – IOS Press and the authors. All rights reserved

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Abbreviations BWS: body weight support MS: multiple sclerosis PwMS: persons with multiple sclerosis TT: treadmill training BWSTT: body weight supported treadmill training EDSS: Expanded Disability Status Scale RoM: range of motion TCT: Trunk Control Test MAS: Modified Ashworth scale MMSE: Mini Mental State Examination VAS: Visual Analogue Scale RA: M. Rectus abdominus OE: M. Obiquus externus ES: M. Erector Spinae MF: M. Multifidus

1. Introduction Multiple sclerosis (MS) is a degenerative disease of the central nervous system (Zuvich et al., 2009). Because this disease can affect different regions in the central nervous system, the symptoms vary (Compston & Coles, 2008) but often lead to gait problems. 18 years after the onset of the disease persons with MS (PwMS) will on average be confronted with an Expanded Disability Status Scale (EDSS) score of 6, implying a dependency on aids to walk for 100 m (Scalfari et al., 2010). A treadmill with a body weight support (BWS) system can be used to start early with gait rehabilitation, particularly important for those patients not able to carry their full body weight. Early start of gait rehabilitation has been proven to have a positive prognostic effect (Visintin et al., 1998). In PwMS, it has been demonstrated that treadmill training (TT) with BWS has a beneficial effect on walking speed, maximum walking distance, EDSS score, spasticity, muscle strength, balance and quality of life (Giesser et al., 2007; Lo & Triche, 2008; Pilutti et al., 2011). However, the available literature does not present evidence that training with BWS is more effective than other methods of gait rehabilitation, neither for MS (Swinnen et al., 2012), nor for other neurological disorders such as hemiplegia and complete or incomplete spinal cord injury (Dobkin et al., 2006; Franceschini et al., 2009; Moseley et al., 2003; Swinnen et al., 2010). Gait on a treadmill with the use of a BWS system (with a minimum of 30% BWS) influences the trunk

motions during the gait with the trunk being more forward tilted of the trunk and limited anteroposterior, mediolateral and vertical accelerations of the trunk. This implies less need for active dynamic stabilization in mediolateral direction, resulting in a passive swing from one side to the other (Aaslund & Moe-Nilssen, 2008). A shift of the center of mass (CoM) upwards and a decrease in the maximal activity of the erector spinae (ES) has also been shown at 70% BWS (Finch et al., 1991). This indicates a gait pattern with the trunk passively suspended in the harness and with only the lower limbs participating actively. Consequently, the normal muscle activity and movements of the trunk that provide active dynamic trunk stability – important for the retention of the posture and balance during normal gait - will therefore be less well involved in the gait training session (Cromwell et al., 2001). In literature thus far only limited information has been found about the influence of the use of BWS during treadmill walking on the activity of the trunk muscles. Furthermore the range of gradations of BWS being used in the published studies is limited. Because there is insufficient evidence that BWS TT is more effective than other types of gait training the focus of this study is whether gait rehabilitation with the use of different levels of BWS sufficiently approximates the gait pattern when walking without BWS, more specifically to compare the effects of different degrees of BWS on the trunk muscle activity (bilateral measured) in PwMS and in healthy persons. Walking with different levels of BWS (10, 20, 30, 50 en 70% BWS) were compared to a reference walking trial with 0% BWS. We hypothesized that with increasing levels of BWS the muscle activity will decrease due to the passive suspension of the trunk in the harness.

2. Methods 2.1. Participants 14 PwMS (recruited from the rehabilitation centre) and 14 healthy persons participated. The selection criteria were: males or females between 20 and 60 years, an EDSS score between two (minimal disability in one functional system is present) and six (the person needs intermittent or unilateral constant assistance with a cane, crutch or brace to walk 100 meters with or without resting) (Kurtzke, 1983, 1984), no flare of the disease, no other neurological diseases or orthopedic problems and they have to be cognitively able to

SP RR SP SP PR RR RR RR PR SP PP RR RR RR

Type MS

F F F M F F F M F F F M M F

Male / Female

19 18 12 12 10 4 22 2 4 22 13 5 2 0.5 10.4 7.7 0.5–22

Time after diagnosis (years)

2.5 3.5 4 4 4.5 4.5 6 5 3.5 6 6 6 5.5 6 4.8 1.2 2.5–6

EDSS-score

Flexors 0 0 2 0 0 0 0 2 0 0 0 0 0 0 0.3 0.7 0–2

R 0 0 0 0 0 0 0 3 0 0 0 0 0 0 0.2 0.8 0–3

L 0 0 2 0 0 0 0 0 0 0 0 0 0 0 0.1 0.5 0–2

R 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

L

Extensors

MAS lower extremities

30 28 21 22 28 29 25 29 28 29 30 29 30 28 27.6 2.9 21–30

MMSE (max 30)

∗

60 71 87 16 88 51 64 23 47 50 59.6 26.4 16–99

∗

99 87 32

0 0 99 0 77 2 0 0 5 52 25.3 36.7 0–99

75 0 19

VAS SCORES (max 100 mm) Pain Fatigue

100 100 61 74 100 100 100 100 100 100 100 100 100 100 95.4 12.1 61–100

TCT (max 100)

PwMS: persons with multiple sclerosis, MS: multiple sclerosis, SP: secondary progressive, RR: relapsing remitting, PP: Primary Progressive, PR: Progressive Relapsing, EDSS: Expanded Disability Status Scale, MAS: Modified Ashworth Scale, L: left side, R: right side, MMSE: Mini Mental State Examination, TCT: Trunk Control Test, SD: Standard Deviation. ∗ Not possible to measure.

1 2 3 4 5 6 7 8 9 10 11 12 13 14 Mean score SD Range

PwMS

Table 1 Characteristics of the PwMS E. Swinnen et al. / Trunk muscle activity during walking in MS patients 325

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E. Swinnen et al. / Trunk muscle activity during walking in MS patients Table 2 Characteristics of the participants PwMS (n = 14)

Age (years) BMI (kg/m²) Body weight (kg) Body height (cm)

Healthy persons (n = 14)

Range

Mean (SD)

Range

Mean (SD)

21–59 20.1–31.9 57–90 160–187

45.8 (10.9) 24.3 (3.0) 72.8 (9.3) 172.7 (8.7)

22–60 19.0–28.7 50–87 160–188

44.5 (12.2) 22.4 (3.2) 65.9 (10.9) 171.1 (8.6)

BMI: Body Mass Index, kg/m2 : weight in kilograms divided by squared height in meters, SD: standard deviation, n: number of participants, kg: kilogram, cm: centimeters.

understand and carry out the instructions. The inclusion criteria for the healthy persons were a normal range of motion (RoM) and no history of injury or surgery in the last 6 months. Persons with orthopaedic or musculoskeletal deformations, osteoporosis and anomalies of the lower extremities or trunk were excluded. The eligibility of the participants was checked using a standardized questionnaire (personal information, sports, diseases, problems with muscles and joints, surgery, medication and experience with walking on a treadmill and/or BWS system). For the PwMS the type and duration of the MS were registered. Some additional clinical data of the PwMS were collected: the Trunk Control Test (TCT) to evaluate the trunk control of the patients (Verheyden et al., 2007); the Modified Ashworth scale (MAS) for the lower legs to determine the spasticity of the flexor and extensor muscles of the lower legs (Blackburn et al., 2002); the Mini Mental State Examination (MMSE) to detect cognitive problems (Swirsky-Sacchetti et al., 1992); and the Visual Analogue Scale (VAS) score for pain and fatigue (Table 1). All participants were able to walk on a treadmill without a harness, a BWS system or holding their hands on the side bars. The participants’ body weight and height were measured before starting the protocol (Table 2). All participants were informed about the purpose and protocol of the study, and they all signed the informed consent.

2.2. Test procedure A motorized treadmill (Trimline) and suspension system (LiteGait MX300) (Frey et al., 2006) were used (Fig. 1). The suspension system has two suspension points, one at each side of the person in the frontal plane, separated 38 cm from each other (see Fig. 1). From each suspension point two belts, one on the front and one on the back of the person ensure the suspen-

sion. The harness was suspended at four points, two on the front (25 cm separated from each other) and two on the back side (21 cm separated from each other). Before starting the tests, the BWS system was calibrated and the height of the suspension fork was set for each person individually in the horizontal plane of the top of the head. In the harness openings were made for placing the EMG electrodes. The Polhemus LibertyTM (16/240), an electromagnetic tracking device (intra-trial reliability: CMD = 0.942 (Mills et al., 2007)), registered the 3D kinematics (accuracy 0.03 inch or 0.08 cm for position and 0.15◦ for orientation) to determine the gait cycle. The electromagnetic transmitter was located on the left side of the treadmill and was not moved during the whole procedure. The electromagnetic sensor was applied with tape on the back of the shoe. The sensor and wires were firmly affixed with tape to diminish motion artifacts. No interference of the electromagnetic tracker system was presented with metal objects, such as the BWS system, harness and the treadmill. Also sensors were placed on the trunk and the pelvis of the participants. This kinematic data will be published in a subsequent publication. Self-selected walking speed was determined during walking on the treadmill with higher and lower speeds while the display was blinded for the participants. The PwMS walked with a self-selected walking speed of 1.6 kmph (SD 0.5, range 1–2.5 kmph) and the healthy persons with a self-selected walking speed of 3.4 kmph (SD 0.5, range 2.5–4 kmph). The PwMS walked 1 to 2 minutes and the healthy persons 2 to 4 minutes before each measurement (30 seconds) to get used to the new level of BWS. They were instructed to look forward and walk normally without using the sidebars. The participants were randomised in two groups by drawing lots. Both groups started walking on 0% BWS. Next, one group walked with increasing levels of BWS (10, 20, 30, 50 and 70% BWS) and one group walked with decreasing levels of BWS (70, 50, 30, 20 and 10% BWS). If necessary, the

E. Swinnen et al. / Trunk muscle activity during walking in MS patients

Fig. 1. Study equipment. A PwMS is walking on the treadmill with BWS system.

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E. Swinnen et al. / Trunk muscle activity during walking in MS patients

patients could rest a few minutes between the different levels of BWS. The EMG data were normalized. The reference for the abdominal muscles was with the participant laying supine, bringing up his stretched legs up to 10 cm three times during six seconds, for the back muscles the same procedure was used but the person laying prone. The mean of three contractions was used for analysis. Surface EMG data were captured with the ME6000 EMG-system (Mega Electronics Ltd) using Conmed Cleartrace electrodes (Ag/AgCl) with an active diameter of 10 mm. To create an optimal electrode-skin contact, the skin was shaved, brushed and cleaned with alcohol. Bilateral electrode placements were for the M. rectus abdominis (RA) at the level of the umbilicus, 1 to 3 cm lateral of the midline (Ng et al., 1998); for the M. extern obliquus (OE) below the rib cage on the line between the inferior part of the rib cage and the contralateral tubercle pubicum (Ng et al., 1998); for the M. ES 2 to 4 cm lateral to the spine (de Seze & Cazalets, 2008; Saunders et al., 2004), at L2 (Lamoth et al., 2006; Ng et al., 2001; Saunders, et al., 2004), parallel to the line between the posterior superior iliac spine and the lateral border of the muscle at the level of the 12th rib (Ng et al., 2001) for the M. multifidus (MF) at the level of L5 (Dankaerts et al., 2004; Hanada et al., 2008; Ng et al., 2001), parallel to the line between the posterior superior iliac spine and the interspinous space between L1 and L2 (Dankaerts et al., 2004; Ng et al., 2001). 2.3. Data analysis and outcome measurements Only the middle 70% of the total signal (±30 seconds) was used, this to exclude artefacts at the beginning and the end of the measurements. In each condition the maximal muscle activity of the RA, OE, ES and MF during the gait cycle, expressed as a percentage of the reference contraction, was determined. The maximum contraction was calculated combining a peak detection algorithm with a smoothing filter (Savitzky-Golay) to exclude artefacts. The obtained data on the different levels of BWS were compared to walking data without BWS. A synchronized electromagnetic sensor on the calcaneus (left) was used to determine the gait cycle. Peak detection was done to differentiate the swing and stance phase. Because the EMG measurements were on the trunk, the electrodes were placed near to the heart, leading to interference between the measurements of the muscles and the activity of the heart. To eliminate

the ECG artifact from the EMG signal, an EEMDICA filter (Ensemble Empirical Mode Decomposition – Independent Component Analysis) was used (Taelman et al., 2011). 2.4. Statistical analysis SPSS 20 was used to analyse the mean effects. A repeated measures ANOVA with simple contrasts was processed with the level of BWS as the within-subjects factor. The different levels of BWS were compared to the 0% level of BWS. The significance level was set at 5%.

3. Results In this study the maximal muscle activation was measured and presented as a percentage of the reference contraction (Tables 3 and 4). The different levels of BWS (10%, 20%, 30%, 50% en 70%) will be compared to the 0% BWS level and the data will be divided in the stance and swing phase of the gait cycle (left leg). 3.1. Differences in muscle activity compared to 0% BWS in healthy persons 3.1.1. Abdominal muscles (Fig. 2) No significant differences were found in RA muscle activity between the different levels of BWS and the reference 0% BWS level in healthy persons. For the OE significant increases in reference to the 0% BWS were only found for the left side of the body (during swing and stance phase): on 20% BWS (stance: ↑28.96% and swing: ↑27.71%), 30% BWS (stance: ↑42.26%, swing: ↑44.03%), 50% BWS (stance: ↑60.92% and swing: ↑63.98%) and 70% BWS (stance: ↑80.02% and swing: ↑94.56%) (p ≤ 0.01). 3.1.2. Back muscles (Fig. 3) Compared to 0% BWS, the activity of the left ES decreased during stance phase significantly at 20% (↓20.29%), 50% (↓38.04%) and 70% (↓35.86%) BWS (p ≤ 0.01). For the swing phase, significant decreases in activity were only found for ES muscle activity on the left side during 50% and 70% BWS with respectively 26.73% and 28.03% (p = 0.04 and p = 0.03). For the right side significant decreases in muscle activity were only found during stance phase at 50% (↓25.05%) and 70% (↓26.94%) BWS (p = 0.05 and p = 0.03).

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Table 3 Muscle activity during walking with different levels of BWS in healthy persons, calculated as a percentage of the reference contraction (mean ± standard deviation) Healthy persons M. Rectus abdominis left Stance Swing M. Rectus abdominis right Stance Swing M. Obliquus externus left Stance Swing M. Obliquus externus right Stance Swing M. Erector spinae left Stance Swing M. Erector spinae right Stance Swing M. Multifidus left Stance Swing M. Multifidus right Stance Swing

0% BWS

10% BWS

20% BWS

30% BWS

50% BWS

70% BWS

18.00 ± 32.04 13.86 ± 21.22

20.50 ± 37.60 16.21 ± 27.29

13.14 ± 13.79 11.79±13.24

11.57 ± 8.20 10.43 ± 7.43

12.21 ± 8.81 10.93 ± 7.42

13.14 ± 9.49 12.43 ± 9.89

11.43 ± 9.30 10.21 ± 7.58

10.64 ± 8.91 9.64 ± 7.81

9.71 ± 5.99 8.86 ± 5.57

10.43 ± 6.19 10.14 ± 6.61

11.43 ± 7.50 10.29 ± 7.26

12.50 ± 8.36 11.86 ± 8.89

33.29 ± 17.51 27.57 ± 14.86

36.14 ± 15.31 31.50 ± 14.22

42.93 ± 22.59 35.21 ± 15.39

47.36 ± 23.97 39.71 ± 18.79

53.57 ± 28.09 45.21 ± 20.89

59.93 ± 34.04 53.64 ± 30.69

21.64 ± 8.55 19.14 ± 8.37

21.29 ± 7.73 19.07 ± 6.94

22.43 ± 9.94 20.14 ± 10.06

23.21 ± 10.26 21.29 ± 9.59

24.29 ± 10.77 22.50 ± 10.82

25.79 ± 12.24 24.14 ± 13.29

39.43 ± 13.89 32.36 ± 10.04

34.07 ± 8.34 30.29 ± 9.37

31.43 ± 10.42 29.14 ± 12.26

32.21 ± 9.35 29.43 ± 8.10

24.43 ± 12.93 23.71 ± 12.24

25.29 ± 13.67 23.29 ± 12.44

37.64 ± 13.98 35.21 ± 16.17

39.07 ± 9.74 32.79 ± 8.38

36.29 ± 10.67 29.29 ± 9.77

32.64 ± 11.30 31.86 ± 13.43

28.21 ± 12.47 25.86 ± 11.75

27.50 ± 14.26 24.57 ± 13.72

36.57 ± 14.76 34.57 ± 14.77

29.71 ± 7.88 27.50 ± 8.89

29.00 ± 7.71 26.36 ± 7.43

31.57 ± 11.52 28.36 ± 13.04

24.50 ± 14.08 23.43 ± 13.17

23.93 ± 15.68 23.71 ± 14.94

35.50 ± 11.26 32.00 ± 12.88

29.86 ± 11.28 25.71 ± 11.58

26.64 ± 9.62 22.50 ± 8.71

25.86 ± 10.14 24.57 ± 8.39

21.00 ± 9.48 18.43 ± 8.52

25.21 ± 15.02 21.36 ± 12.33

Stance: stance phase left leg, swing: swing phase left leg.

Table 4 Muscle activity during walking with different levels of BWS in the PwMS, calculated as a percentage of the reference contraction (mean ± standard deviation) PwMS M. Rectus abdominis left Stance Swing M. Rectus abdominis right Stance Swing M. Obliquus externus left Stance Swing M. Obliquus externus right Stance Swing M. Erector spinae left Stance Swing M. Erector spinae right Stance Swing M. Multifidus left Stance Swing M. Multifidus right Stance Swing

0%BWS

10% BWS

20% BWS

30% BWS

50% BWS

70% BWS

20.50 ± 13.61 17.14 ± 10.14

21.14 ± 14.53 18.14 ± 12.79

23.36 ± 17.99 18.93 ± 13.41

24.36 ± 20.16 21.86 ± 17.64

26.64 ± 21.20 22.36 ± 17.46

27.86 ± 23.80 25.07 ± 20.44

15.71 ± 9.24 13.07 ± 6.71

14.93 ± 8.66 13.50 ± 7.01

17.50 ± 11.28 15.36 ± 7.79

18.43 ± 12.79 17.00 ± 11.67

21.36 ± 19.09 17.57 ± 11.29

20.43 ± 17.08 18.43 ± 14.59

57.50 ± 33.56 48.14 ± 29.99

64.93 ± 37.44 56.71 ± 38.69

78.86 ± 45.99 64.43 ± 36.21

86.71 ± 50.58 73.21 ± 44.92

95.86 ± 55.36 82.36 ± 49.39

97.36 ± 54.60 86.57 ± 50.63

29.00 ± 19.10 23.79 ± 12.32

27.50 ± 12.17 23.79 ± 11.83

30.21 ± 15.38 26.29 ± 13.18

31.71 ± 15.63 27.86 ± 14.02

31.14 ± 16.54 28.64 ± 15.03

31.36 ± 17.43 28.57 ± 15.73

42.86 ± 18.31 34.14 ± 13.61

40.71 ± 22.62 37.36 ± 20.59

41.86 ± 21.89 37.57 ± 19.92

41.79 ± 25.06 31.64 ± 19.52

34.36 ± 17.69 31.43 ± 18.24

34.79 ± 19.91 30.29 ± 17.87

42.93 ± 18.76 39.86 ± 18.25

38.43 ± 21.58 28.43 ± 14.95

37.36 ± 18.38 30.29 ± 17.60

36.21 ± 18.38 29.07 ± 14.22

34.29 ± 14.99 26.93 ± 12.38

31.36 ± 15.38 28.79 ± 17.79

40.71 ± 13.90 35.36 ± 14.17

35.21 ± 10.67 30.07 ± 8.05

31.14 ± 8.32 26.57 ± 9.06

28.00 ± 8.25 24.00 ± 5.97

25.93 ± 10.15 23.00 ± 9.98

30.43 ± 15.19 24.93 ± 12.62

40.71 ± 15.30 34.71 ± 16.03

33.57 ± 13.72 29.93 ± 10.63

32.57 ± 10.96 29.43 ± 10.73

28.07 ± 11.85 25.64 ± 11.96

28.79 ± 13.31 23.43 ± 10.42

27.29 ± 13.02 25.07 ± 13.01

PwMS: persons with multiple sclerosis, stance: stance phase left leg, swing: swing phase left leg.

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Fig. 2. Percentage differences in abdominal muscle activity for the different levels of BWS in comparison with 0% BWS in healthy persons: A. during stance phase, B. during swing phase. ∗ significant difference.

For the MF on the right side significant decreases were found for all levels of BWS during stance and swing phase: at 10% BWS 15.89% and 19.66%, at 20% BWS 24.96% and 29.69%, at 30% BWS 27.15% and 23.22%, at 50% BWS 40.85% and 42.41% and at 70% BWS 28.99% and 33.25% respectively (p between 0.05 and ≤0.01). On the left side a significant decrease in MF muscle activity was found when walking on 10% (↓18.76%), 20% (↓20.70%), 50% (↓33.01%) and 70% (↓34.56%) BWS during stance phase and when walking on 20% BWS during swing phase (↓23.75%) (p between 0.03 and 0.04). 3.2. Differences in muscle activity compared to 0% BWS in PwMS 3.2.1. Abdominal muscles (Fig. 4) For the RA an increase in muscle activity was only significant on the right side of the body during the

Fig. 3. Percentage differences in back muscle activity for the different levels of BWS in comparison with 0% BWS in healthy persons: A. during stance phase, B. during swing phase. ∗ significant difference.

swing phase while walking at 20% (↑17.52%), 30% (↑30.07%) and 50% (↑34.43%) BWS (p between 0.03 and 0.05). An increase, but only significant at the left side, in OE muscle activity was found during stance and swing phase when walking at 20% (stance: ↑37.15%, swing: ↑33.84%), 30% (stance: ↑50.8%, swing: 52.08%), 50% (stance: ↑66.71%, swing: ↑71.08%) and 70% BWS (stance: ↑69.32%, swing: ↑79.83%) (p ≤ 0.01). 3.2.2. Back muscles (Fig. 5) Significant differences were only found for the right ES at 30% (↓15.65%), 50% (↓20.13%) and 70% (↓26.95%) BWS during stance phase and during 10% (↓28.68%), 20% (↓24.01%), 30% (↓27.07%) and 50% (↓32.44%) BWS during swing phase (p between 0.05 and ≤0.01).

E. Swinnen et al. / Trunk muscle activity during walking in MS patients

Fig. 4. Percentage differences in abdominal muscle activity for the different levels of BWS in comparison with 0% BWS in PwMS. A. during stance phase, B. during swing phase. ∗ significant difference.

For the left MF, significant decreases in muscle activity were measured during walking at 20% (stance: ↓23.51%, swing: ↓24.86%), 30% (stance: ↓31.22%, swing: ↓32.13%), 50% (stance: ↓36.31%, swing: ↓34.95%) and 70% BWS (stance: ↓25.25%, swing: ↓29.50%) (p between 0.05 and ≤0.01). For the right MF a decrease was significant in stance phase at all levels of BWS (↓17.54%, ↓20%, ↓31.05%, ↓29.28%, ↓32.96% respectively) and in the swing phase at 30% (↓26.13%) and 50% (↓32.50%) BWS (p between 0.05 and ≤0.01).

4. Discussion The aim of this study was to determine the influence of varying percentages BWS on the trunk muscle activity during treadmill walking. Two different groups were analyzed, PwMS and healthy persons. Hitherto, no similar study was found in the literature.

331

Fig. 5. Percentage differences in back muscle activity for the different levels of BWS in comparison with 0% BWS in PwMS. A. during stance phase, B. during swing phase. ∗ significant difference.

4.1. Abdominal muscles Global comparison of the sEMG data collected during the different levels of BWS with the 0% BWS reference level, revealed for the stance phase as well as the swing phase an increase in activity of the abdominal muscles with an increase in BWS, while the activity of the back muscles decreased. Primarily being a mover (Anders et al., 2007), the RA has also been demonstrated to act as a stabilizer before the back muscles become active (Waters & Morris, 1972). In this study, an increase in activity of the RA in PwMS during swing phase suggests a certain need for forward stabilization of the trunk during gait with BWS. The OE is considered a global stabilizer (Anders et al., 2007), responsible for lateral stabilization of the trunk during balancing over the stance feet (Waters & Morris, 1972). An increase in activity of the OE was found in this study in the healthy persons and in the PwMS. Some participants reported also that during gait

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with 70% BWS it was difficult to place their whole feet on the ground. Because of this, some of the participants walked on their forefeet, while others compensated with larger lateral movements. This could be suggesting a larger need of active stabilization of the trunk in lateral direction during gait with 20%, 30%, 50% en 70% BWS. These findings are in accordance with the study of (Finch et al., 1991), who concluded that there is no decrease in balance control in lateral direction during 70% BWS and also reported an increase in lateral trunk movements. Aaslund et al (Aaslund & Moe-Nilssen, 2008) also described a passive swing from one side to the another during 30% BWS, but they concluded differently that during BWS less dynamic mediolateral balance control is necessitated. 4.2. Back muscles The back muscles are primary movers for extension of the trunk (Cromwell et al., 2001) and important for the rotations of the trunk and pelvis (Waters & Morris, 1972). The results of this study show that muscle activity of the MF and the ES in PwMS and healthy persons was decreased with increasing BWS. At the level of the MF, there was a significant decrease in almost all BWS conditions, while in the ES the most significant differences were found during 50 and 70% BWS. Also (Finch et al., 1991) reported a decrease in muscle activity of the ES with an increasing percentage of BWS but only significant at 70% BWS. The ES and the MF show mainly peaks in activity during ipsilateral and contralateral heel contact (Anders et al., 2007). During the single limb support an upward movement of the trunk exist, while during double limb support the trunk shows more flexion and a downward movement (Cromwell et al., 2001; Waters & Morris, 1972). This upward movement of the trunk during the single limb support is responsible for the anterior flexion of the trunk because the CoM of the body is in a relatively anterior position. The task of the ES and the MF is to decelerate the flexion movement during stance phase (Finch et al., 1991; Waters & Morris, 1972). At 30% BWS the vertical acceleration of the trunk is decreased and during swing phase less need of anterior and upward trunk movements should be necessary to move the center of mass forwards (Aaslund & Moe-Nilssen, 2008). These factors could be an explanation for the decrease in muscle activity of the ES and the MF found in this study. This decreased need of forward stability has also been confirmed by (Finch et al., 1991), who found a decrease in ES activity during stance phase. BWS seems to reduce balance control

in anterior direction, but not in lateral direction (Finch et al., 1991). This corresponds partly with the finding of Aaslund et al. (Aaslund & Moe-Nilssen, 2008). They found by the use of 30% BWS a decrease in anteroposterior acceleration of the trunk and changes in the sagittal plane. Hence, as described before they found that with BWS there is less need of mediolateral balance control, this in contrast with the findings of (Finch et al., 1991). 4.3. Methodological considerations An influence of the application itself of the treadmill and BWS system is possible. Wearing a harness has an influence on the vertical acceleration of the trunk. The gait on a treadmill has an influence on the gaits cadence with a possible influence on the activity of the RA. During gait on a treadmill a larger anterior tilt of the trunk is seen and persons hang more forwards because of the fear to fall backwards and/or to reach the speed on the treadmill (Aaslund & Moe-Nilssen, 2008). On a treadmill the step length is shorter in comparison with over ground gait and also anterior tilt of the trunk exist during gait on a treadmill. The vertical acceleration of the trunk increases significantly in comparison with over ground gait (Aaslund & Moe-Nilssen, 2008). Literature reported no significant changes in muscle activity of the ES due to the gait on a treadmill in comparison with over ground walking (Murray et al., 1985). About the influence of the harness of the BWS itself on the activity of the trunk muscles no information was found in literature. The BWS system used in this study had two suspension points. However, some other systems have only one suspension point. As is the case in most rehabilitation centres, this study encompassed a passive system were the suspension varied during the gait cycle (Finch et al., 1991). Hence, the results of this study cannot be extrapolated to other suspension systems. Especially for the OE differences in maximal muscle activity were found between the right and the left side of the body. The same trend was found in the data, but larger and significant values were found on the left side. Possible explanations for this could be that the BWS system was not balanced enough or the occurrence of ECG artefacts. Although before starting the protocol the BWS system was installed and calibrated on a standardised manner and a specific filter was used to eliminate ECG artefacts from the EMG signal. A previous literature study (Swinnen et al., 2012) concluded that there is no consensus about optimal

E. Swinnen et al. / Trunk muscle activity during walking in MS patients

electrode placement for the trunk muscles. In most of the studies evaluating EMG activity of the trunk muscles during gait there is only a vague description of the placement, differing in muscle specific (for example: on the muscle belly) or location specific (for example 3 cm lateral for midline) descriptions (Swinnen et al., 2012). In this study, location specific locations were used to eliminate as good as possible cross talk. The placements used in this study were based on earlier studies about the most accurate locations for surface electrodes (de Seze & Cazalets, 2008; Ng et al., 1998). As in the most other studies, in the present study also surface electrodes were used, more specific wet electrodes (Ag/AgCl). This kind of electrodes were suggested because of their good stability an there low levels of noise (Merletti et al., 2009). The preparing of the skin could influence the measurements. As suggested in literature, in this study shaving, rubbing and degreasing of the skin was done (Merletti et al., 2009). 4.4. Participants In the PwMS different questionnaires and tests were completed. A high level of spasticity has influence on postural control (Sosnoff et al., 2010) and the gait pattern (Balantrapu et al., 2012) in the PwMS. The MAS was taken to evaluate the spasticity in the lower extremities, and only two of the 14 included persons showed some low level of spasticity. Control of trunk motion is related to disorders of the gait pattern (Verheyden et al., 2006). Therefore, a TCT evaluation was included in this study. The PwMS scored a mean of 95.4% (±12.1), revealing good trunk control. On the MMSE, all participants scored between 21 and 30. Two participants had a score lower than 24, reported in literature as the limit for dementia (Swirsky-Sacchetti et al., 1992), but they were all able to understand and carry out the given instructions. At the beginning of the protocol, four PwMS presented a high fatigue score on the VAS-scale. Therefore, the opportunity was given to take a rest break between the different trials. In this study, only PwMS with an EDSS score between 2 and 6 were included to be able to compare them with a 0% BWS reference. A statistical comparison between the healthy group and the group of PwMS wasn’t adequate because of the large difference in self-selected walking speed. Changes between the two groups could be caused by the fact that the mean walking speed in the healthy group was two times faster compared to the group of PwMS, this instead of the changes in BWS level.

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4.5. Suggestions for the use of BWS Suggestions about the most optimal percentage of BWS for therapeutic application differ (Finch et al., 1991; Visintin & Barbeau, 1994). (Visintin & Barbeau, 1994) described that 40% BWS facilitates the gait in persons with a spastic paresis presenting asymmetric gait patterning. In persons with a symmetric gait pattern it trains the postural stability while the EMG activity of the lower extremities accessed the normal EMG activity as seen during gait without BWS. These authors concluded that the use of 40% BWS without side bars leads to a more normal gait patterns compared with using side bars with or without BWS. Finch et al (Finch et al., 1991) concluded that every percentage lower than 70% BWS can be used for gait rehabilitation, because from 70% BWS on significant differences were found in kinematics and muscle activity of the lower extremities in comparison with walking without BWS. In this study in general compared to no BWS, low levels of BWS (10 and 20%) did not alter muscle activity of the trunk. On the contrary, high levels of BWS (30 to 70%) show more significant differences in muscle activity. The trunk muscles contribute to active dynamic trunk stabilization, necessary to retain the balance throughout the gait over ground (Cromwell et al., 2001). The comfort of the BWS for the patient is also of importance. During this study different participants described walking on 50% en 70% BWS as not comfortable. Therefore, it must be sought during gait rehabilitation to proceed as quickly as possible to less than 50% BWS.

5. Conclusion The use of a BWS system has an influence on the muscle activity of the trunk muscles. Most of the differences in muscle activity as compared to walking without BWS were found during high percentages (30%, 50% en 70%) of BWS. For trunk muscle activity the conditions with 10% en 20% BWS are closer to walking without suspension. Because of this reason we suggest to decrease the percentage BWS as fast as possible beneath the 30% BWS.

Declaration of interest The authors have declared that no competing interests exist.

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Acknowledgments The authors would like to thank Droesja Pinte for her aid in the data input.

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