Gait and Posture 21 (2005) 369–378

A comparison of gait in spinal muscular atrophy, type II and Duchenne muscular dystrophy Stéphane Armand a,b,∗ , Mo¨ıse Mercier b,e , Eric Watelain a,c , Karine Patte b , Jacques Pelissier d , François Rivier e a

d

Laboratoire d’Automatique, de Mécanique et d’Informatique industrielles et Humaines, Université de Valenciennes et du Hainaut-Cambrésis, Le Mont Houy, 59313 Valenciennes Cedex 9, France b Unité Clinique d’Analyse de la Marche du Mouvement, Institut Saint-Pierre, 34250 Palavas-Les-Flots, France c Département de Médecine Physique et de Réadaptation, Centre Hospitalier Régionale Universitaire de Lille, Hˆopital Swynghedauw, 59037 Lille Cedex, France Département de Médecine Physique et de Réadaptation, Centre Hospitalier Carémeau, 5, rue Hoche, BP 26, 30029 Nˆımes Cedex 04, France e Service de Neuropédiatrie, Centre Hospitalier Saint-Eloi, 2, avenue Bertin-Sans, 34295 Montpellier Cedex, France Received 23 December 2003; accepted 10 April 2004

Abstract This study investigated and compared the gait of two patients with spinal muscular atrophy, type II (SMA II) and two patients with Duchenne muscular dystrophy (DMD). These diseases cause a progressive and proximal to distal muscular weakness resulting in the loss of ambulation. The DMD cases had comparable muscle weakness with the SMA II cases on manual muscle testing and patients were assessed using kinematics, kinetics, electromyography and video analysis. SMA II and DMD patients employed different gait strategies for forward movement. SMA II patients used pelvic rotation initiated by the upper body to propel the leg forward and produce the necessary step-length whereas the DMD patients tended to use hip flexion and plantar flexion. Management of SMA II patients would include preservation of hip abductor and flexor strength to maintain mobility. © 2004 Elsevier B.V. All rights reserved. Keywords: Gait analysis; Duchenne muscular dystrophy; Spinal muscular atrophy

1. Introduction Preserving gait autonomy is a major goal in the management of neuromuscular disease [1] and an understanding of the disorder facilitates patient management. Spinal muscular atrophy (SMA) is a neuromuscular disorder caused by degeneration of the anterior horn cells of the spinal cord. This hereditary disease is characterised by muscular weakness, abnormal spinal development and a disease-related deterioration of respiratory function. The underlying genetic defect on chromosome 5q13 has been identified and characterised [2]. There are at least three forms of SMA, often referred to as type I–III. These common forms are classified according to the patient’s age at the onset of the disease and the maximum motor function achieved [3]. In type I, the most severe

∗

Corresponding author. Tel.: +33-467-077-578. E-mail address: [email protected] (S. Armand).

0966-6362/$ – see front matter © 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.gaitpost.2004.04.006

form, the onset appears in the patient’s first 6 months, and affected individuals never manage to sit unsupported. Type II, the intermediate form, appears before 18 months, and in most cases, the patients never stand or walk independently. In type III, the mildest form, the disease can appear anytime after 18 months and even during adulthood. Type III individuals can learn to walk without support [4]. The prevalence rate for types II and III is around 12 per million [5]. Duchenne muscular dystrophy (DMD) is an X-linked muscle disease caused by an absence of the protein, dystrophin. DMD is also hereditary, and is characterised by progressive muscular weakness that can compromise ambulatory status as well as cardiopulmonary function. The prevalence rate for DMD is around 63 per million [5]. Both SMA II and DMD patients exhibit progressive muscular weakness. In both cases, this weakness is more proximal than distal, affects lower limbs more often than upper limbs, and is characterised more by extensor weakness than flexor weakness [6,7]. Despite these similarities

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Table 1 Manual muscular testing, graded according to the Medical Research Council’s criteria [12] Muscles

SMA II

DMD

Subject 1

Ilio-psoas Gluteus maximus Gluteus medius Rectus femoris Semi-tendinosus Biceps Tibialis anterior Peroneus Gastrocnemius Tibialis posterior Mean ± S.D.

Mean ± S.D.

Subject 2

Right

Left

Right

Left

3− 3− 3− 3+ 3 3− 3− 4− 3+ 3+ 3.0 ± 0.4

2+ 3− 3− 3+ 3 3 3 4− 3+ 3+ 3.0 ± 0.4

2+ 2+ 2+ 3 3− 3− 3+ 3+ 3 3 2.8 ± 0.4

3− 3− 2+ 3 3− 3− 3+ 3+ 3 3 2.9 ± 0.3

2.5 2.6 2.5 3.1 2.8 2.8 3.1 3.5 3.1 3.1 2.9

± ± ± ± ± ± ± ± ± ± ±

0.2a 0.2a 0.2 0.2a 0.2 0.1 0.3 0.2 0.2 0.2 0.4

Subject 3

Mean ± S.D.

Subject 4

Right

Left

Right

Left

3 2+ 2+ 3− 3+ 3+ 4 4 3+ 4+ 3.2 ± 0.7

3 2+ 2− 3− 3− 3+ 3+ 3+ 3+ 4+ 3.0 ± 0.7

3 2− 1+ 2+ 3 3 3+ 4 3 3 2.8 ± 0.8

3− 2− 2+ 1+ 2+ 2+ 2+ 2 2+ 4− 2.3 ± 0.6

2.9 2.0 1.9 2.2 2.8 3.0 3.2 3.3 3.0 3.8 2.8

± ± ± ± ± ± ± ± ± ± ±

0.1 0.3 0.5 0.7 0.4 0.5 0.7 0.9 0.4 0.6 0.6

For the purpose of mean and standard deviation calculations, a grade marked “−” was considered to be the number of the grade minus 0.33, and a grade marked “+” was considered to be the number of the grade plus 0.33 (for example: 3− = 2.67 and 2+ = 2.33). a It indicates muscle strength that are considered “different” between SMA II and DMD according to our criteria.

in muscle weakness distribution, a different gait pattern can be observed. To our knowledge, the number of SMA II patients who are able to walk without assistance is very small [4,7]. Souchon et al. [11] and Kroksmark et al. [4] have described gait in SMA III gait that was similar to that in DMD. Patte et al. [8] have described gait in DMD. Hip extensor weakness forces DMD patients to maintain an internal flexion moment at the hip, with a vector posterior to the hip joint centre [8]. They maintain this flexion moment by increasing pelvic tilt. When the knee extensors become too weak to resist an external flexion moment, they use progressive equinus that is also associated with fibrosis of the plantar flexors. This permits the vector to be maintained anterior to the knee throughout single-limb support [9]. Sufficient plantar flexor strength is needed to maintain this gait [10], and if surgery weakens these muscles, DMD patients can lose the ability to walk. The aim of this gait study was to analyse and compare the gait patterns of SMA II and DMD patients, to explain the

differences that exist between the two gait patterns, despite the similarities in muscle weakness in these two diseases, and to discuss the implications of our results for clinical management.

2. Materials and methods 2.1. Subjects Two children, one male (6.1 years, 111.5 cm and 12 kg) and one female (5.9 years, 104.5 cm and 15 kg) with SMA type II had deletions of gene SMN on chromosome 5q and had the onset of symptoms aged 12 and 13 months, respectively. They had been classified as type II by the Department of Neuropaediatrics at the Centre Hospitalier Saint-Eloi, Montpellier. Their gait was very unstable. The two male DMD subjects (8 years, 118 cm, 19 kg and 9.7 years, 129 cm, 24 kg) were selected from the patients pool in the Patte et al. study [8]. Our selection was based

Fig. 1. Ground reaction force curves: fore-aft (a), medio-lateral (b) and vertical (c). Mean (continue thick line) and standard deviation (dashed line) for SMA II (black) and DMD (grey) are represented for both lower limbs. The thick vertical line indicates toe-off. The characteristic curve instances referred to in the discussion are indicated with arrows.

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on muscle strength, which had to be comparable with those of the two SMA II patients. The difference between the mean manual muscular testing (MMT) results for the SMA II and DMD patients was less than 0.2 (Table 1). A physical therapist graded the muscle strength of hip extensors and flexors, knee extensors and flexors, and ankle plantar and dorsal flexors, according to the Medical Research Council’s criteria [12].

femoris, semi-membranosus, gastrocnemius and tibialis anterior muscles of both limbs was recorded by a ten-channel EMG system (MA-100, Motion-Lab® , LA, USA), set at a sampling frequency of 1000 Hz. Pre-amplified surface electrodes with a signal bandwidth of 10 Hz to 30 kHz (−3 dB) and a gain of 380 (±3%) were positioned according to SENIAM’s recommendations [14]. Three to six trials were used for subsequent analysis.

2.2. Gait analysis

2.3. Data processing and data analysis

Subjects were asked to walk the length (12 m) of the laboratory walkway, barefoot and at their usual speed, with rest periods provided between each trial to prevent fatigue. Markers were placed according to the Davis et al. protocol [13]. A five-camera motion analysis system (Vicon® 512, Oxford Metrics, Oxford, UK), set at a sampling frequency of 50 Hz, and two force platforms (AMTI® , Watertown, MA, USA) sampling frequency of 1000 Hz were used. The activity of the gluteus maximus, rectus

Spatio-temporal parameters, joint angle motion, internal joint moments and powers were computed using Vicon Clinical Manager (Vicon® , Oxford Metrics, Oxford, UK). Joint moments and powers were normalised for body weight and are reported in Newtonmetres per kilogram. All the moments described in this study express the resultant effect of the forces exerted by muscles crossing a joint [15]. All the kinematic and kinetic curves (Figs. 1–5) were normalised with respect to 100% of the gait cycle duration.

Fig. 2. EMG envelope curves for gluteus maximus (a, b), rectus femoris (c, d), semi-membranosus (e, f), gastrocnemius (g, h) and tibialis anterior (i, j). Mean (continue thick line) and standard deviation (dashed line) for SMA II (black) and DMD (grey) are represented for both lower limbs.

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Fig. 3. Kinematic curves in the sagittal (a, d, g, j), frontal (b, e, h) and horizontal (c, f, i, k, l) planes for the pelvis (a, b, c), hip (d, e, f), knee (g, h, i) and ankle (j, k, l). Mean (continue thick line) and standard deviation (dashed line) for SMA II (black) and DMD (grey) are represented for both lower limbs. The thick vertical line indicates toe-off. The characteristic curve instances referred to in the discussion are indicated with arrows.

Ground reaction forces (Fig. 1) were normalised for body weight. For each trial, the kinematic and kinetic parameters suggested by Benedetti et al. [16] (Tables 2–4) were extracted automatically using Matlab (The MathWorks, USA), and were manually validated. These parameters were customised to fit the specifications of the two neuromuscular diseases under consideration. Since not all Benedetti et al.’s [16] parameters were applicable to this study, we chose more appropriate ones for some variables. The mean and the standard deviation were calculated for SMA II and DMD. Because we had only two subjects per group, it was impossible to calculate the statistical difference. Therefore, we considered a parameter to be different, if the difference in this parameter’s value for the two groups was superior to the sum of the standard deviation of both groups, for both sides. Electromyographic data were full-wave rectified and smoothed using a fourth-order Butterworth low pass filter with a cut-off frequency of 10 Hz [17], and then normalised according to signal amplitude (Fig. 2).

Global movement was described using sagittal and frontal video views, synchronised with the motion analysis system. For simplicity, the results cited below are those observed for the right-hand side.

3. Results 3.1. Visual assessment SMA II patients had rotational movements of the lower limb, and had a wide base of support. DMD patients displayed lower limb movements in the sagittal plane, with a marked elevation of the foot in the swing. Both SMA II and DMD cases showed signs of hyperlordosis, with the trunk tilted backward. SMA II patients shifted the trunk towards the supporting limb and held the head to the contralateral side in stance, while DMD patients displayed movements of smaller amplitude in the frontal plane. SMA II patients moved their arms essentially in the frontal plane,

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Fig. 4. Joint moment curves in the sagittal (a, d, g), frontal (b, e, h) and horizontal (c, f, i) planes for the hip (a, b, c), knee (d, e, f) and ankle (g, h, i). Mean (continue thick line) and standard deviation (dashed line) for SMA II (black) and DMD (grey) are represented for both lower limbs. The thick vertical line indicates toe-off. The characteristic curve instances referred to in the discussion are indicated with arrows.

whereas DMD patients moved their arms in the sagittal plane. 3.2. Time–distance parameters and ground reaction force The time–distance parameters are summarised in Table 2. Speed and step length values were lower for SMA II than for DMD patients. Although DMD patients exhibited a higher cadence and a lower relative stance phase these parameters were not appreciably different in terms of our criteria. The ground reaction forces (Fig. 1) and parameters shown in Table 2 indicate a higher medio-lateral force in the loading response phase for SMA II than for DMD. Though the computed parameter values did not represent an appreciable difference in vertical force (Fig. 1c) on visual inspection the curve for SMA II was a simple hump, rather than the expected “M”.

3.3. Manual muscular testing Manual muscular testing indicated similar overall muscular weaknesses for SMA II and DMD (Table 1), although there were some variations. SMA II patients appeared to have stronger gluteus maximus and rectus femoris but weaker ilio-psoas. For agonist/antagonists in DMD the hip gluteus maximus were weaker than ilio-psoas, whereas there was no difference in SMA II. Rectus femoris appeared slightly stronger than semi-tendinosus and biceps for SMA II and slightly weaker for DMD. 3.4. Electromyography Mean EMG envelopes with standard deviations are shown in Fig. 2. The standard deviation for SMA II and DMD EMG was significant. Visual inspection indicated an adequate degree of similarity between the right and the left

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Fig. 5. Joint power curves in the sagittal (a, d, g), frontal (b, e, h) and horizontal (c, f, i) planes for the hip (a, b, c), knee (d, e, f) and ankle (g, h, i). Mean (continue thick line) and standard deviation (dashed line) for SMA II (black) and DMD (grey) are represented for both lower limbs. The thick vertical line indicates toe-off. Table 2 Means and standard deviations for time–distance and ground reaction force gait parameters Code

Variables

Parameters

Phase

Unit

DMD

SMA II

Right Mean F1 F2 F3 F8 F7 F9 F4 F5 F6 P6 P7 P4 P5 P1

Vertical force Vertical force Vertical force Medio-lateral force Medio-lateral force Medio-lateral force Fore-aft force Fore-aft force Fore-aft force Cadence Speed Step length Time cycle Stance phase

Max. Max. Max. Max. Min. Max. Min. Max. Min.

LR MS TS LR LR TS LR LR TS

N/kg N/kg N/kg N/kg N/kg N/kg N/kg N/kg N/kg steps/s m/s m s %gait cycle

115.00 86.19 108.11 8.85 −0.44 6.20 −0.29 15.08 −16.62 0.94 0.75 0.42 1.07 63.97

Left S.D. 5.31 6.32 4.89 2.24 0.62 1.28 0.95 1.45 2.39 0.08 0.14 0.04 0.09 2.56

Mean 110.78 87.93 111.15 6.99 −2.74 6.34 −1.61 16.13 −15.95 0.94 0.74 0.39 1.07 62.36

Right S.D. 6.65 5.51 5.49 1.52 1.43 2.17 2.41 2.41 2.05 0.08 0.14 0.07 0.09 4.10

Mean 106.03 89.00 109.83 14.75 0.20 12.48 3.26 16.79 −10.38 0.84 0.43 0.26 1.20 68.19

Considered “different”

Left S.D. 8.98 2.80 14.05 3.61 2.85 1.23 3.43 7.90 2.28 0.09 0.09 0.06 0.14 6.38

Mean 102.72 86.45 117.23 10.96 −1.38 11.82 0.24 14.32 −8.10 0.86 0.45 0.25 1.18 67.91

Max.—maximum; min.—minimum; S.D.—standard deviation; LR—loading response; MS—mid-stance; TS—terminal stance. a Parameters that are considered “different” according to our criteria (see Section 2.3).

S.D. 4.47 7.89 4.06 1.20 1.25 2.98 0.18 4.00 5.82 0.09 0.13 0.04 0.15 5.06

a a

a a

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Table 3 Means and standard deviations for kinematic gait parameters Code

Variables

Parameters

Phase

DMD

SMA II

Right

HR1 HR2 HR3 HR4 HR5 H1 H2 H3 H4 H5 H6 H7 H8 H10 H11 K1 K2 K3 K4 K5 K6 K7 K8 K10 K11 A1 A2 A3 A4 A5 A6 A7 A8 A9

Pelvis tilt Pelvis tilt Pelvis obliquity Pelvis obliquity Pelvis rotation Hip flexion/extension Hip flexion/extension Hip flexion/extension Hip flexion/extension Hip flexion/extension Hip flexion/extension Hip abduction/adduction Hip abduction/adduction Hip rotation Hip rotation Knee flexion/extension Knee flexion/extension Knee flexion/extension Knee flexion/extension Knee flexion/extension Knee flexion/extension Knee valgus/varus Knee valgus/varus Knee rotation Knee rotation Ankle plantar/dorsiflexion Ankle plantar/dorsiflexion Ankle plantar/dorsiflexion Ankle plantar/dorsiflexion Ankle plantar/dorsiflexion Ankle plantar/dorsiflexion Ankle rotation Ankle rotation Foot progression angle

Mean Range Range Max. down Range Value Max. flex. Max. ext. Value Max. flex. Range Range Mean Range Mean Value Range Max. ext. Value Max. flex. Range Range Mean Range Mean Value Max. plantar. Max. dorsi Value Max. plantar. Range Range Mean Mean

AC AC AC AC AC IC LR StP TO SwP AC AC AC AC AC IC StP TS TO SwP AC AC AC AC AC IC LR StP TO SwP AC AC AC AC

Left

Right

Considered “different”

Left

Mean

S.D.

Mean

S.D.

Mean

S.D.

Mean

S.D.

24.34 5.99 20.08 −14.32 23.88 40.23 39.46 3.16 14.41 53.01 49.84 21.94 9.33 27.74 −11.00 2.60 17.51 −3.06 29.02 65.26 68.49 15.59 −13.87 18.82 2.34 −15.31 −15.32 −4.72 −26.28 −29.73 25.01 28.56 1.84 −3.93

1.16 0.92 2.71 2.32 7.83 1.14 1.79 4.94 9.91 2.44 6.31 4.13 5.97 7.44 2.51 3.61 5.14 1.04 7.95 5.40 5.11 4.45 5.65 2.13 10.29 2.04 2.03 3.17 6.16 5.36 3.71 7.04 5.44 6.38

24.55 6.47 20.53 −14.41 24.73 41.78 41.00 2.55 10.01 50.19 47.64 23.19 4.33 28.73 −7.71 2.96 20.69 −1.02 25.37 63.35 65.20 18.40 −11.26 25.28 6.25 −16.79 −16.89 −5.75 −24.85 −29.11 23.36 21.11 −10.84 −6.92

0.89 1.35 1.60 1.42 8.78 3.12 3.62 4.15 7.04 3.63 7.47 2.65 2.86 6.52 3.45 3.72 8.51 0.92 5.21 7.10 6.57 5.43 5.46 3.76 2.54 3.17 2.99 6.22 9.60 7.14 4.61 2.02 2.42 8.42

21.77 6.39 29.11 −12.23 37.36 30.74 30.05 5.94 7.39 32.14 27.01 14.97 −5.37 28.23 5.08 3.11 13.50 5.64 18.58 24.99 24.75 20.11 1.20 20.41 −13.06 −3.95 −4.07 15.30 0.23 −4.18 20.30 13.08 −21.91 −29.54

2.00 1.95 6.11 4.52 9.99 2.71 3.41 4.20 4.06 3.92 4.37 4.69 3.07 10.68 4.77 5.39 7.14 8.24 2.92 7.94 10.55 3.80 2.17 4.34 6.72 2.80 2.85 1.25 4.59 2.32 2.10 3.58 3.67 17.33

20.87 7.05 28.83 −13.34 39.02 33.08 32.19 6.87 9.24 31.59 26.23 15.82 −7.80 26.84 −14.14 −2.06 13.86 2.19 21.21 32.90 35.96 16.50 −1.60 18.30 −10.69 −5.23 −6.18 11.83 −1.87 −7.70 20.21 15.30 −5.07 −28.73

2.08 1.90 5.61 5.32 9.34 2.98 4.40 2.74 4.06 7.00 6.72 3.14 4.46 4.14 7.46 3.04 7.66 3.98 8.10 11.51 12.08 6.18 1.61 3.92 8.74 3.94 3.83 3.78 6.98 5.45 3.19 3.41 5.19 6.74

a

a a

a a a

a a a

a a a a a a a

All parameters are expressed in degrees. Max.—maximum; min.—minimum; flex.—flexion; ext.—extension; plantar.—plantarflexion; dorsi—dorsiflexion; S.D.—standard deviation.; AC—all cycles; StP—stance phase; SwP—swing phase; IC—initial contact; LR—loading response; TS—terminal stance. a Parameters that are considered “different” according to our criteria (see Section 2.3).

side, except for gluteus maximus at 60% of the gait cycle (Fig. 2a and b). Between 40 and 75% of the gait cycle, SMA II rectus femoris demonstrated less activity than those of DMD (Fig. 2c and d), but semi-membranosus activity was higher (Fig. 2e and f). SMA II gastrocnemius exhibited more premature activity than those of DMD (Fig. 2g and h). The pattern of activity for tibialis anterior was the same for the two groups (Fig. 2i and j).

tients whereas it was adducted in the DMD patients. Maximum knee flexion in swing was lower for SMA II as was the knee flexion/extension range. Neither SMA II nor DMD displayed knee flexion during the loading response phase (Fig. 3g). Knee valgus was greater for DMD patients who also exhibited a permanent ankle plantarflexion that was not observed in the SMA II patients (Fig. 3j). The foot progression angle throughout the gait cycle was more external for SMA II than for DMD patients (Fig. 3k).

3.5. Kinematics 3.6. Kinetics Kinematic variables are shown in Table 3 and Fig. 3. When comparing SMA II with DMD, the pelvic obliquity range was higher, hip flexion was lower in loading response and in swing and the hip flexion/extension range was also lower. The hip was abducted in stance phase of SMA II pa-

The internal moments are represented in Fig. 4, and the kinetic variables appear in Table 4. Generally, values for SMA II were lower: SMA II had a lower maximum hip extensor moment during loading response as well as a lower

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Table 4 Means and standard deviations for kinetic gait parameters Code

Variables

Parameters

Phase

DMD

SMA II

Right

HM1 HM2 HM3 HM4 HM4m HM5 HM6 HM7 KM1 KM2 KM3 KM4 KM5 KM6 KM7 KM8 KM9 AM1 AM2 AM3 AM4 AM5 AM6

Hip flexor/extensor Hip flexor/extensor Hip abductor/adductor Hip abductor/adductor Hip abductor/adductor Hip rotator Hip rotator Hip rotator Knee flexor/extensor Knee flexor/extensor Knee flexor/extensor Knee valgus/varus Knee valgus/varus Knee valgus/varus Knee rotation Knee rotation Knee rotation Ankle dor-plantaflexor Ankle dor-plantaflexor Ankle abductor–adductor Ankle abductor–adductor Ankle rotation Ankle rotation

Max. ext. Max. flex. Max. abd. Max. add. Mean Max. exter. Max. inter. Mean Max. flex. Max. ext. Max. flex. Max. var. Max. valg. Mean Max. inter. Max. exter. Mean Max. flex. Max. flex. Max. abd. Max. add. Max. exter. Mean

LR AC StP StP StP StP StP StP LR MS TS StP StP StP StP StP StP LR TS StP StP StP StP

Left

Right

Considered “different”

Left

Mean

S.D.

Mean

S.D.

Mean

S.D.

Mean

S.D.

0.47 −0.81 0.94 −0.09 0.53 −0.01 0.09 0.05 −0.37 −0.11 −0.24 −0.07 0.20 0.08 −0.03 0.06 0.02 0.82 0.91 0.11 −0.11 0.07 0.02

0.15 0.07 0.39 0.06 0.28 0.01 0.03 0.02 0.07 0.06 0.12 0.08 0.14 0.12 0.02 0.04 0.02 0.33 0.09 0.14 0.10 0.05 0.04

0.46 −0.71 0.73 0.09 0.46 −0.02 0.07 0.03 −0.34 −0.17 −0.27 −0.12 0.09 −0.02 −0.04 0.04 0.00 0.84 1.02 0.06 −0.07 0.04 −0.02

0.10 0.07 0.22 0.13 0.17 0.01 0.01 0.00 0.08 0.03 0.08 0.05 0.07 0.04 0.02 0.02 0.02 0.27 0.09 0.06 0.09 0.03 0.03

0.19 −0.19 0.11 −0.18 −0.01 −0.02 0.03 0.00 −0.17 −0.05 −0.20 −0.22 −0.02 −0.15 −0.04 0.02 −0.01 0.48 0.70 0.08 −0.05 0.04 0.01

0.06 0.05 0.03 0.08 0.05 0.02 0.01 0.01 0.09 0.16 0.12 0.06 0.05 0.06 0.02 0.02 0.02 0.06 0.09 0.04 0.03 0.02 0.02

0.21 −0.28 0.07 −0.20 −0.12 −0.08 0.01 −0.05 −0.11 0.01 −0.13 −0.35 0.06 −0.24 −0.11 0.01 −0.07 0.37 0.52 0.03 −0.19 0.01 −0.05

0.12 0.12 0.12 0.17 0.16 0.08 0.01 0.07 0.09 0.08 0.03 0.21 0.05 0.18 0.06 0.01 0.06 0.11 0.05 0.05 0.16 0.01 0.07

a a a a a a a

a

All parameters are expressed in Nm/kg. Max.—maximum; min.—minimum; flex.—flexion; ext.—extension; add.—adductor; abd.—abductor; exter.—external; inter.—internal; var.—varus; valg.—valgus; S.D.—standard deviation; AC—all cycles; StP—stance phase; LR—loading response; MS—mid-stance; TS—terminal stance. a Parameters that are considered “different” according to our criteria (see Section 2.3).

maximum hip flexor moment. They also had a lower mean and maximum abductor moments, a lower mean hip rotator moment, a lower maximum flexor moment at the knee and a lower plantarflexor moment at the ankle in terminal stance. Only the visual aspect of joint power curves was used to compare SMA II and DMD (Fig. 5). In the sagittal plane there was a lower absorption/generation power for SMA II (Fig. 5a, d and g), especially at the hip (Fig. 5a) and in the frontal plane hip power generation was higher for DMD (Fig. 5b). For other plane/joints, the standard deviation was significant, making it difficult to compare the two groups.

4. Discussion The major finding of this study is that, despite similar overall muscular weakness, SMA II and DMD patients had different gait strategies for forward movement. SMA II patients maintained stance by limiting all joint moments requiring the counteraction of muscular contraction, and moved forward using pelvic rotation that pulled the swing limb ahead. The upper body operated like a pendulum to permit standing and to initiate the rotational movement. DMD patients, on the other hand, maintained stance through use of

the equinus and lordosis and to advance the limb in swing they flexed their hip and circumducted the leg. SMA II patients widened their base of support through hip abduction to maintain balance when standing in double support (Fig. 3e). In single support all their moments were very close to zero (Fig. 4). Given a muscular strength close to grade 3, they had to minimise joint moments to maintain balance. Abductor muscle strength of less than grade 3+ creates an unstable pelvis in stance [18]. A functioning gluteus medius has a high predictive value for mobility [19]. Duffy et al. [20] found that the strength/weakness of hip abductors is the most important factor in efficient ambulation in spina bifida. Perry [18] assumed that trunk shift toward the supporting limb is a deliberate action to reduce the abductor moment (Fig. 4b) and observed that the amount of lateral lean varies with the strength of the hip musculature. We observed head movements toward the non-supporting limb (the reverse of the trunk movement), which appear to align the ground reaction force with the hip joint centre in the frontal plane. To compensate for weak quadriceps during the loading response phase before toe-off, SMA II patients deliberately avoided knee flexion (Fig. 3g). In the presence of a permanent knee flexor moment (Fig. 4d), SMA II patients stabilised the knee against the posterior capsule and the

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cruciate ligament by contracting the hip extensors (Fig. 2a and b), knee extensors (Fig. 2c and d) and plantarflexors (Fig. 2g and h). They obtained a flexor moment at the knee by placing the foot to the floor at a point in front of the ankle’s centre of rotation, with the knee extended (Fig. 3g). SMA II patients demonstrated a backward tilt of the trunk; Perry [18] considers that this backward tilt is an adaptation for weak hip extensors, which situates the body vector behind the hip joint axis. Foot position relative to the plane of progression, as well as the use of hip abductors and the lateral muscles of the spine, has been shown to help patients control their balance medio-laterally [21]. The extremely external foot position depicted in Fig. 3k enabled SMA II patients to balance themselves in a medio-lateral direction. The easiest way to advance the limb in swing is to flex the hip with the help of ankle plantarflexion. When hip flexors are very weak, as in SMA II, an increase in step length (P4 in Table 2) was obtained from pelvic rotation combining backward/forward (Fig. 3c) and downward/upward (Fig. 3b) movement. External rotation of the hip (Fig. 3f), external foot progression (Fig. 3k) and raising the pelvis (Fig. 3b) on the swing side permitted foot clearance in swing. The combined pelvic rotation pulled the swing limb forward, with the help of upper body movement (arms, trunk, head) essentially in the frontal plane. Similarities in gait adaptations to muscular weakness include an excessive pelvic tilt (Fig. 3a) with lordosis. According to Do [22], this lordosis is created by hip extensor weakness and the absence of knee flexion in the stance phase (Fig. 3g), leading to a permanent knee flexor moment (Fig. 4d) that prevents the knee from collapsing [1,18]. A flexor moment at the hip (Fig. 4a) produced by the backward tilt of the trunk compensated for weak hip extensors [18]. The major differences between SMA II and DMD patients in the stance phase include the pelvic instability of SMA II patients, and the equinus foot position of DMD patients (Fig. 3j). The pelvic instability can be seen in the rapid drop of the pelvis in SMA II patients during stance, as compared to DMD patients (Fig. 3b). Despite this instability, the abductor muscles of the hip were stronger in SMA II patients (Table 1). One possible explanation is a contracture of the hip abductors and particularly the ilio-tibial band in DMD [22]. Unfortunately, our study cannot confirm this hypothesis because range of movement was not measured. Another possible explanation for the differences may be because it is easier to create a forward momentum when initiating a gait cycle from a toe-standing position [23]. Such a position could lead to a higher abductor moment (Fig. 4b) and greater speed (P7 in Table 2). DMD and SMA II patients used a different forward movement strategy. SMA II patients rotated their pelvis (Fig. 3b and c) and pulled their lower limb forward, whereas DMD patients, who had stronger hip flexors, used hip flexion (Fig. 3d) and circumducted slightly the leg (Fig. 3e and f). Our results concerning the difference in the DMD agonist/antagonists agree with those of McDonald et al. [6].

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Some SMA II studies [7,24] have reported stronger flexor muscles than extensor, but our results did not show this difference for gluteus maximus and ilio-psoas. However, we did find this difference for rectus femoris, semi-tendinosus and biceps (Table 1). In neuromuscular disease, it is important to conserve walking ability to slow down the disease’s progression. As soon as patients lose their ambulatory capacity, muscle strength begins to diminish more rapidly, joint contractures increase, scoliosis appears or increases, and cardio-pulmonary function diminishes [4,24]. Any therapeutic strategy should try to maintain maximum hip flexor and abductor strength and locomotor power in both pathologies. Given the muscular weaknesses, particularly in DMD, the equinus position seemed to provide an advantage for walking. Therefore, it is also important for DMD patients to preserve optimal plantarflexor muscle strength as well.

Acknowledgements We wish to thank Matthieu Jouvet for his help in processing the data, and Professor François-Xavier Lepoutre for his advice.

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