JRRD Volume 47, Number 7, 2010

Pages 617–628

Journal of Rehabilitation Research & Development

Influence of gravity compensation on kinematics and muscle activation

patterns during reach and retrieval in subjects with cervical spinal cord
injury: An explorative study

Marieke G. M. Kloosterman, PT, MSc;1–2* Govert J. Snoek, MD, PhD;2–3 Mirjam Kouwenhoven, MD;2–3
Anand V. Nene, MD, PhD;2–3 Michiel J. A. Jannink, PhD2,4
1
Center for Human Movement Sciences, University Medical Center Groningen, University of Groningen, Groningen,
the Netherlands; 2Roessingh Research and Development, Enschede, the Netherlands; 3Roessingh Rehabilitation Cen-
ter, Enschede, the Netherlands; 4Laboratory of Biomechanical Engineering, University of Twente, Faculty of Engineer-
ing Technology, Enschede, the Netherlands

Abstract—Many interventions in upper-limb rehabilitation INTRODUCTION

after cervical spinal cord injury (CSCI) use arm support (grav-
ity compensation); however, its specific effects on kinematics Damage to the spinal cord causes loss of motor and
and muscle activation characteristics in subjects with a CSCI sensory function of the body parts below the level of the
are largely unknown. We conducted a cross-sectional explor- lesion. In patients with a cervical spinal cord injury
ative study to study these effects. Nine subjects with a CSCI
(CSCI), the arm and hand function is affected to varying
performed two goal-directed arm movements (maximal reach,
reach and retrieval) with and without gravity compensation.
degrees according to the level and completeness of the
Angles at elbow and shoulder joints and muscle activation lesion [1]. Compared with other spinal cord injury-related
were measured and compared. Seven subjects reduced elbow impairments, improvement in upper-limb function is one
extension (range 1.8°–4.5°) during the maximal reaching task of the highest priorities in patients with a CSCI [2]. Exer-
with gravity compensation. In the reach and retrieval task with cise therapy integrated in an intensive rehabilitation pro-
gravity compensation, all subjects decreased elbow extension gram to learn or relearn motor functions is considered
(range 0.1°–11.0°). Eight subjects executed movement closer very important in optimizing the remaining upper-limb
to the body. Regarding muscle activation, gravity compensa- function [1,3]. Even in the chronic stage, intensive exer-
tion did not influence timing; however, the amplitude of activa- cise therapy positively affects upper-limb motor control
tion decreased, especially in antigravity muscles, namely mean and functional abilities in patients with a CSCI [4].
change +/– standard deviation of descending part of trapezius
(18.2% +/– 37.5%), anterior part of deltoid (37.7% +/– 16.7%),
posterior part of deltoid (32.0% +/– 13.9%), and long head
biceps (49.6% +/– 20.0%). Clinical implications for the use of Abbreviations: 3-D = three dimensional, ADL = activity of
gravity compensation in rehabilitation (during activities of daily living, CSCI = cervical spinal cord injury, MRC = Medi-
daily living or exercise therapy) should be further investigated cal Research Council, sEMG = surface electromyography.
with a larger population. *
Address all correspondence to Marieke G. M. Kloosterman,
PT, MSc; Roessingh Research and Development, Roessingh-
sbleekweg 33b, 7522 AH Enschede, the Netherlands; +31-
Key words: electromyography, goal-directed movements, 53-487-5777; fax: +31-53-434-0849. 
gravity compensation, kinematics, rehabilitation, robot-assisted Email: m.kloosterman@rrd.nl
therapy, robotics, spinal cord injury, tetraplegia, upper limb. DOI:10.1682/JRRD.2010.02.0014

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JRRD, Volume 47, Number 7, 2010

Literature indicates that motor learning or relearning is Apparatus

influenced by several key elements: active movements, A mechanical, passive device called Freebal [17]
intensity of practice (frequency, repetitions, and duration), (University of Twente, Enschede, the Netherlands; now avail-
use of feedback, task specificity, goal-orientated practice, able commercially as ArmeoBoom, Hocoma; Volketswil,
and variation [5–6]. Exercise therapy based on these motor Switzerland) was used to counteract the effect of gravity
learning or relearning principles asks great physical effort on the upper limb (Figure 1). The device has two
from patients with a CSCI who have impaired upper-limb slings—one is applied at the elbow and the other around
function. We presume that during goal-directed move-
ments, a large part of the preserved muscle force is
required to hold the arm against gravity; consequently, less
muscle force is available to perform the actual movements.
To facilitate goal-directed arm movements during activi-
ties of daily living (ADLs) [7] or exercise therapy, thera-
peutic devices are often used to support the weight of the
arm (e.g., with the Swedish Help Arm [Kinsman Enter-
prises, Inc; West Frankfort, Illinois]). In the last decade,
several innovative therapeutic devices, including robotics,
have been developed to support the affected upper limb
during exercise therapy [8–9]. In these robotic devices, dif-
ferent treatment modalities have been implemented, such
as passive, active-assisted, and active-resisted movements
[8]; consequently, gravity compensation is incorporated in
the design [8–9]. Until now, the effect of gravity compen-
sation on motor control and functional abilities has mainly
been investigated in nondisabled elderly [10] and stroke
patients [11–15]. Although many applications in rehabili-
tation after a spinal cord injury include gravity compensa-
tion during ADLs or exercise therapy, the specific effects
on kinematics and muscle activation characteristics
(amplitude and timing) in patients with a CSCI are largely
unknown. A cross-sectional explorative study that meas-
ured kinematics and surface electromyography (sEMG)
during goal-directed movements with and without gravity
compensation was conducted to study the effects of gravity
compensation in subjects with a CSCI.

METHODS

Subjects
Nine subjects with a CSCI (at least 1 year since
injury) were recruited from a local rehabilitation center. Figure 1.
Inclusion criteria for participation were motor injury Freebal device for gravity compensation of upper limb. Source: Stienen
level C5–C7 (cervical) and age between 18 and 65 years. AH, Hekman EE, Van der Helm FC, Prange GB, Jannink MJ, Aalsma
AM, Van der Kooij H. Freebal: Dedicated gravity compensation for the
Exclusion criteria were extreme shoulder pain, contrac- upper extremities. In: Proceedings of the 2007 IEEE 10th International
tures of the upper limb, and/or spasticity preventing per- Conference on Rehabilitation Robotics; 2007 Jun 13–15; Noordwijk
formance of the required tasks. All subjects were assessed aan Zee, the Netherlands. Piscataway (NJ): IEEE Press. p. 804–8.
according to the standard neurological classification [16]. DOI:10.1109/ICORR.2007.4428517
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KLOOSTERMAN et al. Gravity compensation in cervical SCI

the wrist. Each sling is connected to an independent

adjustable spring by way of an overhead cable and pul-
leys. During the goal-directed movements, this system
enables a constant amount of support throughout the
three-dimensional (3-D) working volume, irrespective of
the position and orientation of the arm [17].

Procedures
During the measurements, subjects sat in their own
wheelchairs (one subject was not wheelchair-dependent
and sat on a normal chair) in front of a height adjustable
table. In the starting position, subjects sat with their fore-
arm flat on the tabletop, elbow flexed at 90°, and hand on
the starting dot. Subjects performed two goal-directed
movements with and without the Freebal:
1. Maximal reaching task. This task consisted of three
maximum reaches in front of the subjects, without
gliding the hand and arm along the tabletop.
2. Reach and retrieval task. Subjects were instructed to
move at their own comfortable speed between a start-
ing dot and target dot on the table for 30 seconds. Both
dots were 10 cm in diameter, and the distance between
the dots was 35 cm (Figure 2(a)).

Measurement and Data Analysis

Kinematics
Kinematics were recorded with a 3-D optical move-
ment tracking system with six cameras (Vicon Nexus
1.3.109, Oxford Metrics Ltd; Oxford, United Kingdom). Figure 2.
Reflective markers were placed on 10 bony landmarks of (a) Tabletop with start and target dots and (b) experimental setup. S =
the arm and trunk: processus spinosus of the seventh cer- starting dot, T = target dot.
vical and eighth thoracic vertebra, incisura jugularis, pro-
cessus xiphoideus, acromioclavicular joint, medial and
lateral epicondyle, radial and ulnar styloid, and distal replaced missing marker trajectories over a short period
head third metacarpal (Figure 2(b)). Six cameras at (less than 10 samples) by linear interpolation. If data
100 Hz recorded the 3-D marker trajectories. The acro- were missing for longer periods or at the end of the reach
mion marker was used for estimating the glenohumeral or retrieval movement, the movement cycle was removed.
rotation center. Scapular motion was disregarded because Marker position data were converted to limb seg-
scapular motion was not likely to participate in the ante- ments data according to the guidelines of the Interna-
flexion movement if the angle of elevation remains tional Society of Biomechanics [18]; thereafter, joint
below 60°. angles were calculated with Euler rotation. The elbow
The marker trajectories were visually inspected for joint angle (Figure 3(a)) was specified as the angle
recording errors and missing marker data. If one trunk between the longitudinal axis of the upper arm and the
marker was missing, we replaced it using the Vicon forearm (full elbow extension was defined as 0°; forearm
BodyBuilder model (Metrics Ltd; Oxford, United King- perpendicular to upper arm, 90°). We calculated two
dom). This model estimated the position of the missing angles to describe the position of the upper arm related to
marker by the position of the other three markers. We the thorax: (1) the angle of elevation (Figure 3(b)),
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Figure 3.
Representations of calculated angles to express position of elbow and shoulder in accordance with recommendations of International Society of
Biomechanics: (a) elbow angle (), (b) angle of elevation (), and (c) plane of elevation ().

defined as the angle between the upper arm and trunk preparation, and recording protocol were in accordance
(upper arm parallel with thorax, 0°; upper arm parallel with the SENIAM guidelines [19].
with horizontal; 90°), and (2) the plane of elevation (Fig- sEMG signals were synchronized with the marker
ure 3(c)), defined as the angle between the thorax and the trajectories (Figure 4). The time axis was normalized
upper arm in the transversal plane (arm extended forward, from 0 to 100 percent: reach 0 to 50 percent and retrieval
0°; arm extended to the lateral, –90°). 51 to 100 percent.
For the maximal reaching task, we compared the We converted the band-pass filtered sEMG signals to
maximum elbow extension with and without gravity smooth rectified sEMG using a second-order Butterworth
compensation. To quantify the differences between the filter with frequency at 25 Hz. To visualize the differ-
reach and retrieval task with and without gravity com- ences in smooth rectified sEMG, we plotted movement
pensation, we derived joint rotations (in degrees) of the trajectories (averaged data over all cycles) for two subjects
angles just mentioned and parameters of the movement with and without gravity compensation plotted in the same
cycles (mean duration of one movement cycle, number of graph (Figure 5). Changes in the amplitude of muscle
repetitions within 30 seconds). Cycle parameters were activation during movements with gravity compensation
averaged over all movement cycles within a series; the were expressed as a percentage of the change of the area
first two cycles were excluded for analysis. A movement under the curve of the same movement without gravity
cycle consisted of two parts, namely reach (maximum to compensation. The area under the curve is calculated as
minimum elbow angle) and retrieval (minimum to maxi- the integral of the smooth rectified sEMG.
mum elbow angle). Timing of muscle activation was analyzed visually.
The primary investigator assessed the sEMG recordings,
Electromyography and a coauthor with extensive experience in sEMG analysis
Bipolar sEMG of eight superficial muscles (descend- checked it.
ing parts of the trapezius, anterior and posterior parts of
the deltoid, pectoralis major, long head of the biceps, Statistical Analysis
long head and lateral head of the triceps, and latissimus This study had an explorative character; therefore,
dorsi) was recorded with circular, wet gel, silver/silver- the effect of gravity compensation was described separately
chloride electrodes (ARBO, type S93SG, Tyco/Health- for each individual subject. Because of the small sample
care Deutschland; Neustadt/Donau, Germany) at a sam- size and a heterogeneous population, a Wilcoxon signed
ple frequency of 1,000 Hz. Electrode placement, skin rank test was performed and the median or ranges were
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KLOOSTERMAN et al. Gravity compensation in cervical SCI

Figure 4.
Elbow and shoulder joint angles (°) during 15 s repetitive reach and retrieval tasks with Freebal, performed by subject with identification number 2,
simultaneously displayed with smooth rectified surface electromyography values (microvolt) of eight measured muscles.
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JRRD, Volume 47, Number 7, 2010

Figure 5.
Mean muscle activation pattern of reach and retrieval task with and without Freebal (Fb). Conditions with (dotted line) and without (solid line)
gravity compensation were plotted in same graph. Smooth rectified surface electromyography (sEMG) (microvolt) of eight measured muscles and
corresponding joint angles (°) was plotted against average movement cycle, divided into reach (1%–50%) and retrieval (51%–100%). (a) Activation
patterns of subject with identification (ID) number 9. Amplitude of sEMG of antigravity muscles decreased with use of Fb, except descending part of
trapezius. (b) Activation pattern of subject with ID number 2. Amplitude of sEMG of antigravity muscles decreased and amplitude of sEMG in
triceps increased with use of Fb.

found. From the Wilcoxon test, the test statistic T (smallest Kinematics
of the two sums of ranks), its significance (p), and the Movement parameters are presented in Table 2. During
effect size (r) were reported. the maximal reaching task with and without gravity com-
pensation, the maximum elbow angle was significantly
lower with gravity compensation (median 33.3°) than
RESULTS
without gravity compensation (median 29.4°), T = 2, p =
Subjects 0.021, r = –0.77.
A complete data set was available for nine partici- During the reach and retrieval task with gravity com-
pants. The physical characteristics of each of the nine pensation, all subjects showed decreased elbow extension
subjects are displayed in Table 1. (range 0.1°–11.0°). At the shoulder joint, seven subjects
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KLOOSTERMAN et al. Gravity compensation in cervical SCI

Table 1.
Physical characteristics of subjects (N = 9).
Subject ID Number
Variable
1 2 3 4 5 6 7 8 9
Sex M M M M F M F M M
Age (yr) 28 55 47 59 39 40 26 53 36
Time Since Injury (mo) 58 29 282 209 66 221 161 170 198
Motor Level of Lesion C5 C6 C6 C6 C5 C5 C6 C6 C7
ASIA Impairment Scale A C B D B C A A A
Measured Arm R L R L R L L L R
ASIA Motor Score of Measured Arm (MRC score)
C5 (elbow flexors) 4 5 5 5 4 5 5 5 5
C6 (wrist extensors) 0 4 4 4 5 2 5 5 5
C7 (elbow extensors) 0 2 0 5 4 4 0 0 3
C8 (finger extensors) 0 0 0 4 1 0 0 0 0
T1 (finger abductors) 0 0 0 4 0 0 0 0 0
ASIA = American Spinal Injury Association, C = cervical (fifth to eighth vertebra), F = female, ID = identification, L = left, M = male, MRC = Medical Research
Council, R = right, T = thoracic.

had decreased plane (0.3°–6.9°) and six subjects had 3. In three of the five subjects with active triceps function
reduced angle of elevation (0.1°–15.1°). The movement (MRC score of at least 2), the amplitude of sEMG in
times increased in four subjects (range 0.1–0.4 s), the long head of triceps increased (25.2%, 1.2%, and
decreased in two subjects (0.2–0.4 s), and remained the 16.9%) and decreased in the other two subjects (16.4%
same in three subjects. None of these parameters differs and 56.6%). On a group level, a significant difference
significantly between movements performed with and between the conditions with and without gravity com-
without gravity compensation (elbow extension: T = 2, p = pensation was found for the following muscles:
0.214, r = –0.41; shoulder plane of elevation: T = 3, p = descending part of trapezius during reach: T = 1, p =
0.767, r = –0.10; shoulder angle of elevation: T = 4, p = 0.038, r = –0.69; posterior part of deltoid during reach: T =
0.515, r = –0.22; and cycle duration: T = 2, p = 0.484, r = 1, p = 0.015, r = –0.81, and during retrieval: T = 0, p =
–0.23). 0.008, r = –0.89; and anterior part of deltoid and long
head biceps for reach as well as retrieval: T = 0, p =
Electromyography 0.008, r = –0.89.
Based on the plotted smooth rectified sEMG (Figure 5) Within subjects, the timing of muscle activation did
and calculated differences (in terms of percentage) in the not change visibly with gravity compensation. With
areas under the curves (Table 2), we made three observa- respect to the patterns of timing between subjects, we
tions: found various different patterns. Some alternating activa-
1. With gravity compensation, the amplitude of the tion patterns were found between agonists and antagonists.
sEMG decreased especially in the antigravity muscles. All subjects with at least some triceps function showed
In six subjects, amplitude of the sEMG decreased in an alternating activation pattern between the long head of
the descending part of the trapezius (range 17.5%– biceps and triceps (Figure 6(a)). We found a simulta-
60.6%) and increased in three subjects (4.1%, 6.5%, neous activation pattern in four subjects between the acti-
and 59.7%). In all subjects, amplitude of the sEMG vation of the anterior and posterior parts of the deltoid
was decreased in the posterior part of deltoid (range: muscle (Figure 6(b)) and in six subjects between the ante-
12.8%–54.1%), the anterior part of deltoid (17.4%– rior part of deltoid and pectoral muscles (Figure 6(c)).
73.6%), and the long head of biceps (22.9%–80.0%). Furthermore, the descending part of the trapezius
2. In four subjects (identification numbers 1, 3, 7, and 8) was used in various different patterns. In one subject, an
without triceps activity (Medical Research Council alternating activation pattern between the anterior and
[MRC] score of 0), sEMG activity was recorded dur- posterior parts of the deltoid occurred, and in another
ing flexion of the elbow. subject, an alternating activation pattern between the
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JRRD, Volume 47, Number 7, 2010

Table 2.
Influence of gravity compensation on kinematic parameters during maximal reaching task on kinematic and surface electromyography (sEMG)
parameters during reach and retrieval task of participants (N = 9) with and without Freebal (Fb).
Subject ID Number
Task Fb
1 2 3 4 5 6 7 8 9
Maximal Reach
No 47.9 19.0 47.5 36.9 22.3 24.3 21.1 46.2 29.4
Elbow Angle (°)
Yes 52.2 20.8 47.4 36.1 25.3 28.8 23.6 49.4 33.3
Reach and Retrieval
Angles of Elbow and Shoulder at Target Dot (°)
No 47.5 29.0 47.8 54.9 40.4 25.7 43.1 56.7 36.6
Elbow Angle
Yes 57.5 29.4 58.8 64.0 47.5 32.9 43.2 65.3 39.6
No –71.6 –42.7 –50.0 –66.4 –49.3 –39.8 –43.3 –56.7 –54.0
Plane of Elevation
Yes –64.7 –40.3 –49.7 –66.7 –48.4 –50.5 –41.4 –54.7 –51.2
No 30.6 23.0 37.8 51.3 29.1 27.2 44.6 44.7 40.4
Angle of Elevation
Yes 15.5 30.3 34.2 40.5 31.8 32.2 35.3 44.6 39.5
Parameters of Movement Cycles
No 2.7 2.1 1.4 2.4 1.3 1.6 1.5 2.9 1.3
Cycle Duration (s)
Yes 3.1 2.2 1.4 2.0 1.3 1.6 1.6 2.7 1.4
No 11 14 21 13 23 19 20 10 23
Repetitions (n in 30 s)
Yes 10 14 21 15 23 19 19 11 21
sEMG Parameters: Change of Area Under Curve (%)*
Descending Part of Trapezius — –17.5 –41.2 4.1 –60.6 –46.8 –48.3 59.7 6.5 –19.3
Posterior Part of Deltoid — –43.0 –54.1 –29.5 –16.0 –47.2 –26.1 –32.9 –26.3 –12.8
Anterior Part of Deltoid — –54.5 –31.9 –17.4 –73.6 –27.0 –33.2 –39.8 –30.6 –31.6
Pectoralis Major — –30.4 –51.2 –14.7 –40.6 –38.1 –11.3 –4.2 –39.0 22.2
Long Head Biceps — –57.0 –78.0 –42.9 –80.0 –41.6 –52.7 –44.4 –26.4 –22.9
Lateral Head Triceps — –55.7 46.6 –37.3 –24.8 –10.7 115.5 –43.4 –29.6 –13.8
Long Head Triceps — –47.2 25.2 –37.7 1.2 –16.4 –56.6 12.1 –24.5 16.9
Latissimus Dorsi — –17.5 –6.6 –13.1 –28.6 –23.5 –17.8 –5.5 45.4 –4.8
*Negative value means decrease in area under curve during movement with Fb, compared with same movement without Fb.
ID = identification.

posterior parts of the deltoid solely. These two combina- sEMG characteristics of the upper limb during goal-
tions were also observed in a simultaneous pattern: in one directed movements of subjects with a CSCI.
subject, the descending part of the trapezius and anterior With gravity compensation, most of the subjects
and posterior parts of the deltoid were simultaneously showed less elbow extension and movement execution
activated, and in another subject, the descending part of the closer to the midline. Based on previous studies with
trapezius was activated with the posterior deltoid solely. stroke patients, one can expect that gravity compensation
increases range of motion of the upper limb [12,14] because
of the positive effect on pathological muscle synergies
DISCUSSION between shoulder abduction and elbow flexion [14]. In
patients with a CSCI, this pathological coupling does
The objective of the present study was to study the not occur. However, an effect on kinematics is expected
influence of gravity compensation on kinematics and because less muscle force is necessary to overcome
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KLOOSTERMAN et al. Gravity compensation in cervical SCI

results of this study showed less elbow extension during

maximal reaching with gravity compensation in seven
subjects. During reach and retrieval with gravity compen-
sation, all subjects showed less elbow extension and, in
eight subjects, a decrease in shoulder angle and/or plane
of elevation.
Plausible explanations could be given for these
results. First, subjects with a CSCI who have a lack of tri-
ceps function use their anterior part of the deltoid and
upper pectoral muscles to produce an isometric extension
torque in their elbow [20] or make a trick movement with
their shoulder muscles to achieve passive elbow exten-
sion [21]. They use gravity to maintain the arm in exten-
sion below the horizontal plane [22] and to perform a
passive elbow extension with a trick movement. In both
compensation strategies, gravity is used to maintain
elbow extension. Therefore, movement execution with
gravity compensation might decrease elbow extension.
Second, during goal-directed movements without gravity
compensation, subjects use a large part of the preserved
muscle force to hold the arm against gravity. If the pri-
mary agonists alone are not capable of generating the
required anteflexion and extension torques, additional
agonist muscles are recruited [23]. For example, the mid-
dle part of the deltoid might contribute to lift the arm, if
the anterior part of the deltoid cannot generate enough
force. The middle part of the deltoid also has an abduc-
tion function that can result in a reaching movement not
truly in the sagittal plane [23]. Third, because of a
decreased plane of elevation, the hand moves more in a
direct line to the target dot. If the arm is extended closer
to the midline, less elbow extension and angle of eleva-
tion are necessary to reach the target dot. Finally, with
gravity compensation, the pectoral muscles can move the
arm more easily to a position in front of the patient
because the weight of the arm is counteracted.
Figure 6. The results of the sEMG data during the reach and
Examples of muscle activation patterns and corresponding elbow
angle: (a) Alternating activation pattern between biceps and triceps
retrieval task showed a decrease in sEMG activity during
(subject identification [ID] number 2), (b) simultaneous pattern movements with the use of the Freebal, particularly in
between anterior and posterior part of deltoid (subject ID number 3), muscles that counteracted gravity, while timing remained
and (c) simultaneous pattern between anterior deltoid and pectoralis unaffected. The results confirmed our presumption based
major (subject ID number 11). on previous studies with nondisabled elderly [10] and
stroke patients [11,13,15] that also showed a decreased
sEMG in antigravity muscles and unaffected timing.
gravity. A larger part of the muscle force could be used to Remarkably, despite subjects with an MRC score of 0 in
perform goal-directed movements, possibly leading to the triceps, sEMG activity was seen mainly during elbow
increased elbow extension during maximal reaching and flexion. A plausible explanation for this sEMG activity is
more repetitions during reach and retrieval. However, the stretch or cocontraction. In the sEMG signal, however,
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JRRD, Volume 47, Number 7, 2010

one cannot differentiate between activity because of in CSCI. A larger study is needed to firmly conclude
stretch and voluntary motor activity [24]. whether training with gravity compensation is clinically
A large variety in muscle activation patterns was relevent.
seen between subjects because of heterogeneity of the
study population. After a CSCI, the functional anatomy
of the upper limb had to be redefined. Muscle synergies ACKNOWLEDGMENTS
as seen in nondisabled subjects are often inappropriate
for subjects with a CSCI [20]. The central nervous sys- Author Contributions:
Study concept and design: G. J. Snoek, M. Kouwenhoven, A. V. Nene,
tem is challenged to use a motor strategy to adjust to the
M. J. A. Jannink.
new functional anatomy and biomechanics, with a Recruitment of study population: G. J. Snoek, M. Kouwenhoven, 
reduced repertoire of innervated muscles to deal with the A. V. Nene.
mechanics [21], leading to different movement patterns Data collection and analysis: M. G. M. Kloosterman, 
between subjects with a CSCI [20]. M. Kouwenhoven.
Interpretation of data: M. G. M. Kloosterman, G. J. Snoek, 
To our knowledge, our study was the first explorative
M. Kouwenhoven, A. V. Nene, M. J. A. Jannink.
study about the effect of gravity compensation on kine- Drafting of manuscript: M. G. M. Kloosterman.
matics and sEMG in subjects with a CSCI. Another type Critical revision of manuscript: G. J. Snoek, M. Kouwenhoven, 
of arm support by subjects with a CSCI was studied by A. V. Nene, M. J. A. Jannink.
Atkins et al. [7]. They reported about the effect of mobile Financial Disclosures: The authors have declared that no competing
arm support on ADLs. Based on Delphi questionnaires, interests exist.
Funding/Support: This material was based on work supported by the
they concluded that some ADLs were possible with the
Ministry of Economic Affairs (EZ) Overijssel and Gelderland, the
use of a mobile arm support, which without the use of Netherlands, grant 1-5160. The study sponsor was not involved in any
such a device, patients with very weak biceps and deltoid aspect of this research.
muscles were unable to perform. Additional Contributions: Ms. Kloosterman is now only affiliated
Besides being used for compensating lost functions, with Roessingh Research and Development, Enschede, the 
Netherlands.
gravity compensation can be used for training purposes. Institutional Review: The study was approved by the local medical
Further studies should be performed with a larger popula- ethics committee. Subjects provided written informed consent before
tion because of the small effect size, especially on kine- being admitted to the study.
matic parameters, and should be able to test the following Participant Follow-Up: The authors do not plan to inform partici-
hypotheses: (1) patients with an MRC score of at least 2 pants of the publication of this study.
in the triceps muscle can train their primary agonists of
the shoulder and elbow in goal-directed movements more
intensively and, (2) for patients without active triceps REFERENCES
function (MRC score of 0 or 1), gravity compensation
may not seem useful to train extension movements 1. Kirshblum S, Ho CH, House JG, Druin E, Nead C, Drastal
because they perform these movements with the use of S. Rehabilitation of spinal cord injury. In: Kirshblum S,
Campagnolo DI, DeLisa JA, editors. Spinal cord medicine.
gravity. However, gravity compensation might be benefi-
Philadelphia (PA): Lippincott Williams & Wilkins; 2001.
cial for training muscles required to cross the midline or p. 275–98.
to perform bimanual tasks. Also, the influence of gravity 2. Snoek GJ, IJzerman MJ, Hermens HJ, Maxwell D, Biering-
compensation on the patients’ ability to stabilize the Sorensen F. Survey of the needs of patients with spinal cord
shoulder in a certain position would be an interesting injury: Impact and priority for improvement in hand func-
parameter. tion in tetraplegics. Spinal Cord. 2004;42(9):526–32.
[PMID: 15224087] 
DOI:10.1038/sj.sc.3101638
CONCLUSIONS 3. Jacobs PL, Nash MS. Exercise recommendations for indi-
viduals with spinal cord injury. Sports Med. 2004;34(11):
727–51. [PMID: 15456347] 
This explorative study showed that gravity compen- DOI:10.2165/00007256-200434110-00003
sation influenced the kinematics and amplitude of the 4. Kloosterman MG , Snoek GJ, Jannink MJ. Systematic
sEMG of the upper limb during goal-directed movements review of the effects of exercise therapy on the upper
 627

KLOOSTERMAN et al. Gravity compensation in cervical SCI

extremity of patients with spinal-cord injury. Spinal Cord. lands. Piscataway (NJ): IEEE Press. p. 467–71.
2009;47(3):196–203. [PMID: 18825160]  DOI:10.1109/ICORR.2007.4428467
DOI:10.1038/sc.2008.113 14. Dewald J, Yao J. The effect of generating anti-gravity
5. Schmidt RA, Lee TD. Condition of practice. In: Schmidt RA, shoulder torques on upper limb discoordination following
Lee TD, editors. Motor control and learning: A behavioural hemiparetic stroke. In: Proceedings of the ISB XXth Con-
emphasis. 4th ed. Champaign (IL): Human Kinetics; 2005. gress—ASB 29th Annual Meeting; 2005 Jul 31–Aug 5.
p. 321–63. Cleveland, OH. International Society of Biomechanics. 973 p.
6. Powers SK, Howley ET. The physiology of training: Effect Available from: http://isbweb.org/o/content/view/280/1/.
on VO2 max, performance, homeostasis, and strength. In: 15. Jannink MJ, Prange GB, Stienen AH, Van der Kooij H,
Powers SK, Howley ET, editors. Exercise physiology, the- Kruidbosch JM, IJzerman MJ, Hermens HJ. Reduction of
ory and application to fitness and performance. 5th ed. muscle activity during repeated reach and retrieval with
New York (NY): McGraw-Hill; 2004. p. 249–75. gravity compensation in stroke patients. In: Proceedings of
7. Atkins MS, Baumgarten JM, Yasuda YL, Adkins R, Waters the 2007 IEEE 10th International Conference on Rehabili-
RL, Leung P, Requejo P. Mobile arm supports: Evidence- tation Robotics; 2007 Jun 13–15; Noordwijk aan Zee, the
based benefits and criteria for use. J Spinal Cord Med. 2008; Netherlands. Piscataway (NJ): IEEE Press. p. 472–76.
31(4):388–93. [PMID: 18959356] DOI:10.1109/ICORR.2007.4428468
8. Prange GB, Jannink MJ, Groothuis-Oudshoorn CG, Her- 16. Maynard FM Jr, Bracken MB, Creasey G, Ditunno JF Jr,
mens HJ, IJzerman MJ. Systematic review of the effect of Donovan WH, Ducker TB, Garber SL, Marino RJ, Stover
robot-aided therapy on recovery of the hemiparetic arm SL, Tator CH, Waters RL, Wilberger JE, Young W. Interna-
after stroke. J Rehabil Res Dev. 2006;43(2):171–84.  tional standards for neurological and functional classifica-
[PMID: 16847784]  tion of spinal cord injury. American Spinal Injury
DOI:10.1682/JRRD.2005.04.0076 Association. Spinal Cord. 1997;35(5):266–74. 
9. Kwakkel G, Kollen BJ, Krebs HI. Effects of robot-assisted [PMID: 9160449] 
therapy on upper limb recovery after stroke: A systematic DOI:10.1038/sj.sc.3100432
review. Neurorehabil Neural Repair. 2008;22(2):111–21. 17. Stienen AH, Hekman EE, Van der Helm FC, Prange GB,
[PMID: 17876068]  Jannink MJ, Aalsma AM, Van der Kooij H. Freebal: Dedi-
DOI:10.1177/1545968307305457 cated gravity compensation for the upper extremities. In:
10. Prange GB, Kallenberg LA, Jannink MJ, Stienen AH, Van Proceedings of the 2007 IEEE 10th International Confer-
der Kooij H, IJzerman MJ, Hermens HJ. Influence of gravity ence on Rehabilitation Robotics; 2007 Jun 13–15; Noord-
compensation on muscle activity during reach and retrieval wijk aan Zee, the Netherlands. Piscataway (NJ): IEEE
in healthy elderly. J Electromyogr Kinesiol. 2009;19(2): Press. p. 804–8. DOI:10.1109/ICORR.2007.4428517
e40–49. [PMID: 17911029]  18. Wu G, Van der Helm FC, Veeger HE, Makhsous M, Van
DOI:10.1016/j.jelekin.2007.08.001 Roy P, Anglin C, Nagels J, Karduna AR, McQuade K,
11. Prange GB, Jannink MJ, Stienen AH, Van der Kooij H, IJzer- Wang X, Werner FW, Buchholz B; International Society of
man MJ, Hermens HJ. Influence of gravity compensation Biomechanics. ISB recommendation on definitions of joint
on muscle activation patterns during different temporal coordinate systems of various joints for the reporting of
phases of arm movements of stroke patients. Neurorehabil human joint motion—Part II: Shoulder, elbow, wrist and
Neural Repair. 2009;23(5):478–85. [PMID: 19190089] hand. J Biomech. 2005;38(5):981–92. [PMID: 15844264]
DOI:10.1177/1545968308328720 DOI:10.1016/j.jbiomech.2004.05.042
12. Stienen AH, Van der Helm FC, Prange GB, Jannink MJ, 19. Hermens HJ, Freriks B, Merletti R, Stegeman D, Blok J,
Van der Kooij H. Effects of gravity compensation on the Tau G, Disselhorst-Klug C, Hagg G. SENIAM: European
range-of-motion of the upper extremities in robotic rehabili- recommendations for surface electromyography. Results of
tation after stroke. In: Proceedings of the International the SENIAM project. 2nd ed. Enschede (the Netherlands):
Shoulder Group (ISG). 2006 Oct 9–10; Chicago, IL; [about Roessingh Research and Development; 1999.
4 screens]. Available from: http://www.arnostienen.net/ 20. Marciello MA, Herbison GJ, Cohen ME, Schmidt R.
articles/stienen06.pdf/. Elbow extension using anterior deltoids and upper pectorals
13. Prange GB, Stienen AH, Jannink MJ, Van der Kooij H, IJzer- in spinal cord-injured subjects. Arch Phys Med Rehabil.
man MJ, Hermens HJ. Increased range of motion and 1995;76(5):426–32. [PMID: 7741612] 
decreased muscle activity during maximal reach with grav- DOI:10.1016/S0003-9993(95)80571-0
ity compensation in stroke patients. In: Proceedings of the 21. Koshland GF, Galloway JC, Farley B. Novel muscle pat-
2007 IEEE 10th International Conference on Rehabilitation terns for reaching after cervical spinal cord injury: A case
Robotics; 2007 Jun 13–15; Noordwijk aan Zee, the Nether- for motor redundancy. Exp Brain Res. 2005;164(2):133–47.
628

JRRD, Volume 47, Number 7, 2010

[PMID: 16028034]  and noninvasive applications. New York (NY): John Wiley
DOI:10.1007/s00221-005-2218-9 & Sons; 2004. p. 1–25. DOI:10.1002/0471678384
22. Acosta AM, Kirsch RF, Van der Helm FC. Three-dimen-
sional shoulder kinematics in individuals with C5–C6 spinal Submitted for publication February 9, 2010. Accepted in
cord injury. Proc Inst Mech Eng H. 2001;215(3):299–307. revised form June 1, 2010.
[PMID: 11436273] 
DOI:10.1243/0954411011535894 This article and any supplementary material should be
23. McCrea PH, Eng JJ, Hodgson AJ. Saturated muscle activa- cited as follows:
tion contributes to compensatory reaching strategies after Kloosterman MGM, Snoek GJ, Kouwenhoven M, Nene
stroke. J Neurophysiol. 2005;94(5):2999–3008.  AV, Jannink MJA. Influence of gravity compensation on
[PMID: 16014786]  kinematics and muscle activation patterns during reach
DOI:10.1152/jn.00732.2004 and retrieval in subjects with cervical spinal cord injury:
24. Moritani T, Stegeman D, Merletti R. Basic physiology and An explorative study. J Rehabil Res Dev. 2010;47(7):
biophysics of EMG signal regeneration. In: Merletti R, Parker 617–28. 
PA, editors. Electromyography. physiology, engineering, DOI:10.1682/JRRD.2010.02.0014