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How early reactions in the support limb contribute to balance
recovery after tripping
Mirjam Pijnappels*, Maarten F. Bobbert, Jaap H. van Die.en
Faculty of Human Movement Sciences, Institute for Fundamental and Clinical Human Movement Sciences, Vrije Universiteit Amsterdam,
Van der Boechorststraat 9, 1081 BT Amsterdam, The Netherlands
Accepted 24 March 2004
Abstract
Tripping causes a forward angular momentum that has to be arrested to prevent a fall. The support limb, contralateral to the
obstructed swing limb, can contribute to an adequate recovery by providing time and clearance for proper positioning of the
recovery limb, and by restraining the angular momentum of the body during push-off. The present study investigated how such a
contribution is achieved by the support limb in terms of response times and muscle moment generation, in order to provide more
insight in the requirements for successful recovery after tripping. Twelve young adults repeatedly walked over a platform in which 21
obstacles were hidden. Each subject was tripped over one of these obstacles during mid-swing in at least five trials. Kinematics,
dynamics and muscle activity were measured. Very rapid responses were seen in the muscles of the support limb (B65 ms), causing
fast increases in muscle moments in the joints during the primary phase of recovery. Especially a large ankle plantar flexion moment
(204 Nm), a knee flexion moment (54 Nm) and a hip extension moment (52 Nm), generated by triceps surae and hamstring muscle
activity, brought about the necessary push-off reaction and simultaneously caused a restraining of the forward angular momentum
of the body. These required joint moments could be a problem for the elderly, who might not be able to generate such powerful
moments. Strength training in these muscle groups may be indicated in elderly subjects to reduce the risk of falling after a trip.
r 2004 Elsevier Ltd. All rights reserved.
0021-9290/$ - see front matter r 2004 Elsevier Ltd. All rights reserved.
doi:10.1016/j.jbiomech.2004.03.029
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628 M. Pijnappels et al. / Journal of Biomechanics 38 (2005) 627–634
When properly placed, the recovery limb can generate a wearing walking shoes, were instructed to walk at a self-
force and moment that counteract the body angular selected speed over a 12 2.5 m platform. In the
momentum (Grabiner et al., 1993). However, other platform, a force plate was mounted and 21 aluminum
actions can also contribute substantially to an adequate obstacles (15 cm height) were hidden over a total
recovery during this primary phase. First of all, the distance of 1.5 m (Fig. 1). In about 10 of 60 walking
obstructed foot has to be released from the obstacle, trials, one of the obstacles suddenly appeared to catch
about which the body rotates during contact. Further- the swing leg of the subject. At the start of each trial,
more, while the recovery limb is positioned, but before it subjects did not know whether or where an obstacle
hits the ground, a strong push-off reaction is seen in the would appear. Online kinematic data was used to
support limb (Pijnappels et al., 2004). This response can calculate where and when an obstacle had to appear to
play a major role in recovery after tripping. By pushing- initiate a trip at mid-swing. A full-body safety harness,
off with the support limb, time and clearance is provided attached to a ceiling-mounted rail, prevented subjects
for proper positioning of the recovery limb. Moreover, from falling on the floor. The safety ropes provided
generation of adequate joint moments in the support enough slack for free motion and harness assistance
limb restrains the angular momentum of the body could be precluded visually, to which end all trials were
before the recovery limb hits the ground. recorded on video.
Although the importance of the role of the support Gait kinematics were recorded using four Optotrak
limb in recovery after tripping has been described cameras (Northern Digitalr). Motion of 12 infrared-
(Pijnappels et al., 2004), the characteristics of the light emitting markers was tracked. The markers were
primary reactions in this limb are still unknown. The placed bilaterally on the anatomical landmarks heel,
present study was designed to investigate how the fifth metatarso-phalangeal joint, lateral malleolus, lat-
support limb contributes to a successful recovery. eral epicondyle, major trochanter of the femur, and
Important factors for success are response time and acromial process. The coordinates of these landmarks
the quality of the executed response (Grabiner et al., defined seven body segments: two feet, two lower legs,
1993). Thus far, response quality was described in terms two upper legs and a head-arms-trunk segment. Ground
of activation patterns and kinematics, mainly of the reactions forces (GRF) and center of pressure of the
recovery limb (Eng et al., 1994; Grabiner et al., 1993, support limb were measured with a custom-made strain
1996; Pavol et al., 2001; Schillings et al., 1999, 2000). gauge force plate (1 1 m). Kinematic and ground
The present study will focus on muscle responses and reaction force data were collected and synchronized at
moment generation in the support limb, as these could a sample frequency of 100 Hz. Data were analyzed in the
be limiting factors for recovery in the elderly. sagittal plane after smoothing with a uni-directional
The purpose of this study was to determine how the second-order low-pass Butterworth filter with a cutoff
support limb contributes during push-off to recovery
after tripping, in order to provide more insight in the
requirements for successful recovery. For this purpose,
we had 12 young subjects walk over a platform, and
tripped them several times. Kinematics, ground reaction
forces and muscle activity were measured and the
response times and response mechanics during push-
off by the support limb were investigated. We hypothe-
sized that the support limb would show rapid responses,
high peak muscle moments and high rates of change in
moments generated during push-off. If rapid and strong
reactions are required, these could be limiting factors for
recovery in the elderly.
2. Methods
frequency of 8 Hz. Joint forces and moments were detecting timing of impact was validated using the
calculated using an inverse dynamics model. For each signal of an accelerometer on the obstacles, sampled at
segment, mass, center of mass position and the moment 1000 Hz. The detection method based on kinematic data
of inertia were calculated per subject, according to resulted in an acceptable mean error of 1.61 ms (SD
Plagenhoef et al. (1983). 5.82).
For measurement of muscle activity patterns, bipolar For onset detection of EMG activity bursts, we
Ag/AgCl (Medicotest A/S) surface electrodes were subtracted the averaged pattern of five walking trials
attached after cleaning and gentle abrasion of the skin. from the averaged pattern of five tripping trials for each
The center-to-center electrode distance was 2.5 cm. The muscle. Onset was determined on these subtracted
electromyogram (EMG) signals were recorded from m. signals by means of a dynamic process model in
gluteus maximus (GL), m biceps femoris (BF), m. combination with statistically optimal change detection,
semitendinosus (ST), m. rectus femoris (RF), m. vastus described by Staude and Wolf (1999). For a period of
lateralis (VL), m. gastrocnemius medialis (GM), m. 200 ms following trip initiation, this method searched
soleus (SO), and m. tibialis anterior (TA). The EMG for changes in the sequence by use of the likelihood
signals were amplified, high-pass filtered (5 Hz), sampled ratios over small time windows. The same method was
at 1000 Hz and stored on disk (Porti-17t, Twente used for onset detection of the perturbation effect on the
Medical Systems). Next, the signals were whitened (fifth moment generation. For each tripping trial, the aver-
order) (Clancy et al., 2002) to reduce the influence of aged joint moment pattern of five walking trials was
tissue filtering and movement artefacts, Hilbert trans- subtracted, and deviation of the signal following trip
formed and rectified and finally low-pass filtered (fifth initiation was determined. Over the period of 50 ms
order Savitzky-Golay filter, frame size of 21). This following onset of this perturbation effect, the rate of
filtering method preserves sudden activity onset without change in generating the joint moments was calculated.
producing a phase-lag. Fig. 2 illustrates the effects of Finally, peak values were quantified of the joint
these techniques. moments and of the GRF in vertical and horizontal
For each subject, five normal walking and five left leg (foreaft) direction over stance time of the support limb
tripping trials at mid-swing were randomly selected from for each walking and tripping trial. Differences in EMG
trials with complete kinematic and dynamic data. In two onsets of the tripping responses were tested between
subjects only complete data of three tripping trials were muscles by paired t-tests with a Bonferoni correction. In
available. Heel strike (HS) and toe-off (TO) were order to test for differences between normal walking and
detected on the basis of kinematic data (Pijnappels tripping reactions, within-subject averaged (across
et al., 2001). Impact of the foot with the obstacle trials) values of the variables were statistically tested in
coincided with a local peak in first derivative of a multivariate analysis of variance (MANOVA) for
acceleration, also known as jerk, of the toe marker in repeated measures (SPSS Inc. statistical software). The
the walking direction. This kinematic method of level of significance selected was set at p ¼ 0:05:
(A)
0.5
[mV]
0 3. Results
-0.5
The subjects walked at a velocity of 1.61 (SD 0.15) m/s
0.5 (B) and frequency of 117 (SD 4.5) steps/min. Tripping
[mV]
GL
0
0.5
BF
0
tripping 0.5
ST
0
0.5
RF
0
0.5
t= -0.1 s t=0 s t=0.1 s t=0.2 s t=0.3 s
VL
early trip obstacle push-off 0
stance initiation clearance 0.5
TA
Fig. 3. Stick figures of a typical walking trial (upper graph) and a 0
tripping trial (lower graph) for 5 instants of time (trip initiation at
0.5
GM
t ¼ 0) of one subject. Thin lines indicate the obstructed swing limb,
thick lines depict the support limb. Body center of mass (d), foot- 0
obstacle contact force vector at the toe, and ground reaction force 0.5
SO
vectors are drawn. Center of pressure of the GRF can be positioned
0
anteriorly of the foot because the toe marker is located at the -0.2 -0.1 0 0.1 0.2 0.3 0.4
metatarso-phalangeal joint.
stance time [s]
Fig. 4. Muscle activity patterns (mV) over stance time during normal
The responses and onsets seen in the support limb walking (dashed) and tripping (solid), averaged over trials, for the
same subject as Fig. 3. Vertical lines indicate trip initiation (solid, with
muscles during the primary phase of recovery after a shaded SD at t ¼ 0 s) and onset of the perturbation effect (dotted).
tripping are presented for a typical subject (Fig. 4) and
averaged over subjects (Table 1). The first muscle
responses were observed in the hamstring muscles (ST Table 1
Onset times (and SD) of muscle responses after tripping in the support
and BF) followed by responses of triceps surae (GM and
limb (contralateral) and swing limb (ipsilateral), averaged over subjects
SO) and gluteal muscles (GL). Subsequently, quadriceps
bursts were observed (VL and RF). No responses could Tripping
be detected in the TA within the first 200 ms after impact Support limb Swing limb
with the obstacle. The onsets of the hamstrings and
Gluteus maximus (GL) 79 (8) 82 (15)
triceps surae muscles were significantly shorter than the
Biceps femoris (BF) 65 (7) 90 (18)
onsets of the RF muscle (po0:002). The onset of the Semitendinosus (ST) 63 (4) 86 (18)
hamstring muscles were even significantly shorter than Rectus femoris (RF) 136 (38) 104 (38)
the onset of the GL muscle (po0:001). Vastus lateralis (VL) 96 (22) 115 (25)
The hamstring and gluteal bursts generated a hip Tibialis anterior (TA) 76 (8)
Gastrocnemius medialis (GM) 71 (12) 119 (12)
extension moment. Fig. 5 (typical subject) and Table 2
Soleus (SO) 73 (9) 101 (14)
(group averages) show that whereas normally during
push-off a flexion moment was observed at the hip joint, In TA of the support limb, no responses could be detected within
after tripping an extension moment was seen. This hip 200 ms after impact.
extension moment decelerated the forward angular
velocity of the trunk. The sudden hamstring activity also
generated a knee flexion moment, together with GM after tripping (po0:001; Table 2 and Fig. 5), whereas the
activity: whereas normally an extension moment was seen peak hip extension moment and knee flexion moment
in the knee during push-off, after tripping a clear flexion after tripping were found to be in the range of moments
moment was observed (Fig. 5 and Table 2). This flexion observed during normal walking, although at other
moment decelerated the angular velocity of knee exten- phases in the gait cycle than push-off (Fig. 5).
sion, and thus decelerated forward rotation of segments Joint rotations toward extension were seen in all
cranial to the knee. At the end of push-off, the flexion support limb joints during push-off, but the changes in
moment decreased and the knee was accelerated towards amplitudes were small (Fig. 6). Only in the knee, a
extension by the quadriceps activity. Finally, the rapid prolonged extension movement was seen. This was a
responses by the triceps surae muscles provided a large result of the knee flexion moment, which decelerated the
plantar flexion moment, needed for push-off, and a angular velocity of the knee extension. At the end of
reduction of angular momentum. The peak ankle push-off, the knee was further extended by the quad-
moment of the support limb was increased significantly riceps activity.
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M. Pijnappels et al. / Journal of Biomechanics 38 (2005) 627–634 631
ext flex
ext
Hi p
Hip
0 0
flex
-50
-40
80
50
ext
Knee
Knee
flex
0 40
flex
-50
0
200 40
plantarflex
ext flex
Ankle
Ankle
100 0
0
-40
-0.2 -0.1 0 0.1 0.2 0.3 0.4 -0.2 -0.1 0 0.1 0.2 0.3 0.4
stance time [s] stance time [s]
Fig. 5. Net joint moments for the hip, knee, and ankle of the support Fig. 6. Joint angles for the hip, knee and ankle of the support limb
limb for the same typical subject as Figs. 3 and 4. Graphs over stance over stance time for the same subject as Figs. 3–5, during normal
time for normal walking (dashed mean and shaded SD) and for walking (dashed mean and shaded SD) and for tripping (solid line with
tripping (solid line with error bars). Vertical lines indicate trip error bars). Vertical lines indicate trip initiation (solid, with a shaded
initiation (solid, with a shaded SD at t ¼ 0 s) and onset of the SD at t ¼ 0 s) and onset of the perturbation effect (dotted). Positive
perturbation effect (dotted). Positive values in the joint moment graphs values correspond with joint flexion; negative values indicate a joint
correspond with extension moment, negative values indicate a joint extension.
flexion moment.
off. If rapid and strong reactions are required, these moment, as observed, angular momentum of the body
could be limiting factors for recovery in the elderly. was decelerated. Consequently, stance duration and
Quick responses, with latencies of 60–80 ms, were seen time available for push-off was prolonged (by about
in the muscles of the support limb, especially in the 9%). The combination of a knee flexion moment and a
gluteal, hamstring and triceps surae muscles. These hip extension moment, together with an increased ankle
response times were about as fast as those observed in plantar flexion moment caused the ground reaction
the swing limb (Eng et al., 1994; Schillings et al., 2000). force vector to increase in magnitude and become
Crossed reflexes could account for these rapid reactions directed more forward. This indicates an attempt to
(Berger et al., 1984; Tax et al., 1995). Accounting for an prevent a further increase or even bring about a
electro-mechanical delay of about 100 ms (Vos et al., reduction of the forward angular momentum of the
1990, 1991), these rapid muscle activities caused fast body, in line with earlier findings (Pijnappels et al.,
increases in muscle moments in the joints during the 2004). The attempt to control forward angular momen-
primary phase of recovery. The peak values and rate of tum was observed in all subjects, although from the
change of these muscle moments were large. Especially a earlier findings it appeared that only some subjects were
large ankle plantar flexion moment, generated by triceps able to actually reduce the angular momentum to zero
surae muscles, and a hip extension moment, generated (Pijnappels et al., 2004).
by hamstring activity, brought about the necessary Contribution of the support limb in restraining the
push-off reaction. These net moments in the support angular momentum of the body, and the trunk in
limb were high in comparison to literature data on the particular, was suggested, but not explained before.
capacity of human subjects. This was true especially for Grabiner et al. (1996) suggested that in the primary
the moments about the ankle. The peak ankle moment phase of recovery, trunk control might be achieved by
of 204 Nm was substantially higher than the isometric generation of a hip extension moment by hamstring
maximum voluntary moments in a compilation of data and/or gluteus maximus muscle activity, as they did not
from the literature for both young adults (maximum find an influence of the capacities of the paraspinal
B150 Nm) and elderly adults (maximum B85 Nm) muscles (maximum effort eccentric trunk extension
(LeBlanc et al., 1988; Trappe et al., 1996; Porter and strength, voluntary-reaction time, automatic response
Vandervoort, 1997; Dowson et al., 1998; Gajdosik et al., latencies and activation levels) on trunk kinematics
1999; Trappe et al., 2001; Suzuki et al., 2001; Pavol et al., during the positioning phase. Others, who found
2002). The peak value and rate of change of the ankle increased activity in these muscles in the contralateral
moment exceed the isometric capacity of a group of support limb after perturbation, have also described the
elderly females (Pavol et al., 2002) by factors of about potential effect of the hamstring and gluteal muscles on
2.4 and 5.6, respectively. Of course, data derived using trunk extension (Dietz et al., 1986; Eng et al., 1994;
dynamometers cannot be compared directly with Schillings et al., 2000). The present study showed that
estimates of moments from kinematics. The above- indeed, a large hip extension moment was generated.
mentioned factors might be overestimated because no One should bear in mind that not only the hip joint
correction was made for joint angle, subject character- moment contributes in trunk control, but dynamic
istics, and the fact that voluntary activation in isometric control of the angular momentum of the body involves
conditions is not necessarily maximal. Nevertheless the all joints of the support limb (Zajac and Gordon, 1989).
data show that high ankle moments are required during In summary, during the primary phase of recovery
push-off, which could be a problem for the elderly who after tripping, an early and pronounced increase in
might not be able to generate such large moments. muscle activity was seen in the support limb. Extension
For the hip and knee, peak values and rate of change reactions were observed to achieve push-off and
of joint moments were less extreme. However, other simultaneously reduce the angular momentum of the
striking findings appeared in these joints: the hip and body. A reversal of joint moments in the hip and knee,
knee joint moments of the support limb were directed and very large ankle extension moments were required.
opposite to those during push-off in normal walking. These reactions in the support limb resulted in a push-
We found hip extension moment instead of hip flexion off reaction that provided time and clearance for
moment and knee flexion moment instead of knee adequate positioning of the recovery foot and contrib-
extension moment. Similar reversals in joint moments uted to a decrease of the angular momentum during
were observed in slipping (Cham and Redfern, 2001; push-off. The ability of hip and ankle extensor muscles
Redfern et al., 2001). During push-off, all joints of the to react quickly and generate large forces in the limb is
support limb needed to be extended, but simultaneously, therefore an important determinant for successful
the angular momentum of the body had to be restricted. recovery, at least, during the primary phase of recovery.
Hip and ankle extension moments meet these require- In the next phase of recovery, when landing on the
ments, but a knee extension moment would increase the recovery limb, one would expect high net moments in
angular momentum. By generating a knee flexion the hip and knee of this limb. Preliminary results
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M. Pijnappels et al. / Journal of Biomechanics 38 (2005) 627–634 633
indicate that indeed large hip and knee extension Grabiner, M.D., Feuerbach, J.W., Jahnigen, D.W., 1996. Measures of
moments are generated in the recovery limb during paraspinal muscle performance do not predict initial trunk
landing. Further research is required to investigate the kinematics after tripping. Journal of Biomechanics 29, 735–744.
LeBlanc, A., Gogia, P., Schneider, V., Krebs, J., Schonfeld, E.,
characteristics and requirements of the landing phase. Evans, H., 1988. Calf muscle area and strength changes after five
However, the inverse dynamics analysis in the present weeks of horizontal bed rest. American Journal of Sports Medicine
study shows that the support limb plays an important 16, 624–629.
role in adequate recovery after tripping. This contribu- Nevitt, M.C., Cummings, S.R., Hudes, E.S., 1991. Risk factors for
tion should not be underestimated, because the more injurious falls: a prospective study. Journal of Gerontology Series
A Biological Sciences and Medical Sciences 46, M164–M170.
angular momentum is taken away by the support limb
Owings, T.M., Pavol, M.J., Grabiner, M.D., 2001. Mechanisms of
during push-off, the less remains to be accomplished by failed recovery following postural perturbations on a motorized
the recovery limb after landing. The support limb treadmill mimic those associated with an actual forward trip.
contribution can be ascribed particularly to large ankle Clinical Biomechanics 16, 813–819.
moments (for push-off) and hip extension moments (for Pavol, M.J., Owings, T.M., Foley, K.T., Grabiner, M.D., 1999. The
trunk control). These results add to the identification of sex and age of older adults influence the outcome of induced trips.
Journal of Gerontology Series A Biological Sciences and Medical
factors predisposing for falls, as more falls could be Sciences 54, M103–M108.
expected in older adults who react less rapid and less Pavol, M.J., Owings, T.M., Foley, K.T., Grabiner, M.D., 2001.
strong than young adults. Strength training in the Mechanisms leading to a fall from an induced trip in healthy older
muscle groups responsible for push-off and trunk adults. Journal of Gerontology Series A Biological Sciences and
control may be indicated in older adults to reduce the Medical Sciences 56, M428–M437.
Pavol, M.J., Owings, T.M., Foley, K.T., Grabiner, M.D., 2002.
risk of falling after a trip.
Influence of lower extremity strength of healthy older adults on the
outcome of an induced trip. Journal of the American Geriatrics
Society 50, 256–262.
Acknowledgements Pijnappels, M., Bobbert, M.F., van Die.en, J.H., 2001. Changes in
walking pattern caused by the possibility of a tripping reaction.
The authors would like to thank Richard Casius and Gait & Posture 14, 11–18.
Pijnappels, M., Bobbert, M.F., van Die.en, J.H., 2004. Contribution of
Leon Schutte for developing the data acquisition soft- the support limb in control of angular momentum after tripping.
ware and for help with the experiments. Journal of Biomechanics, in press.
Plagenhoef, S., Evans, F.G., Abdelnour, T., 1983. Anatomical data for
analyzing human motion. Research Quarterly for Exercise and
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