Professional Documents
Culture Documents
Reduced Plantar Sensation Causes A Cautious Walking Pattern: Cite This Paper
Reduced Plantar Sensation Causes A Cautious Walking Pattern: Cite This Paper
Effect s of changes in plant ar sensory feedback on human gait charact erist ics: a syst emat ic…
Diet er Rosenbaum
Changes in muscle act ivit y in children wit h hemiplegic cerebral palsy while walking wit h and wit hout a…
Reinald Brunner
See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/8510105
CITATIONS READS
92 144
6 authors, including:
Dieter Rosenbaum
University of Münster
287 PUBLICATIONS 5,566 CITATIONS
SEE PROFILE
Some of the authors of this publication are also working on these related projects:
KNEEMO, an Initial Training Network (ITN) for knee OA research (EU FP7 funding) View project
Early rehabilitation in pediatric oncology: objective assessment of physical activity levels and
evaluation of bone mass View project
All content following this page was uploaded by Dieter Rosenbaum on 12 May 2014.
The user has requested enhancement of the downloaded file. All in-text references underlined in blue are added to the original document
and are linked to publications on ResearchGate, letting you access and read them immediately.
Gait and Posture 20 (2004) 54–60
Received 9 April 2003; received in revised form 20 June 2003; accepted 8 July 2003
Abstract
The aim of this study was to investigate the influence of reduced plantar sensation on gait patterns during walking in 20 healthy subjects
(25.9 ± 1.2 years, 61.6 ± 11.5 kg, 178 ± 9.5 cm) with no history of sensory disorders. Force plate measurements, electromyography (EMG)
measurements and a three-dimensional movement analysis were performed simultaneously during barefoot walking before and after reduction
of plantar sensation using an ice immersion technique. The results show that reduced plantar sensation leads to significant changes in gait
patterns that are present at the ankle, knee and hip joint and indicate a more cautious ground contact and push-off with modified EMG and
motion patterns.
© 2003 Elsevier B.V. All rights reserved.
0966-6362/$ – see front matter © 2003 Elsevier B.V. All rights reserved.
doi:10.1016/S0966-6362(03)00095-X
E. Eils et al. / Gait and Posture 20 (2004) 54–60 55
forces, muscle activation patterns and segment movements brated space to detect motion was 2 m long, 1.5 m wide and
of the lower extremity in barefoot walking. Our hypothe- 1.8 m high.
sis was that reduced cutaneous information of the plantar A three-dimensional force plate was used to measure com-
surface of the foot results in a substantially modified gait ponents of the ground reaction force in walking (AMTI, Wa-
strategy by characteristic changes in the horizontal and tertown, MA, USA). The sampling frequency was 600 Hz
vertical components of the ground reaction forces, reduced and data was measured and analyzed using Motion Analysis
electromyography (EMG) activity of specific muscles of Eva 5.2 software. Synchronization of force plate, EMG and
the lower extremities, and modified segment angles of the motion data was performed using the vertical component of
lower extremities during the phases of walking. the ground reaction force that was measured by EMG and
Motion Analysis software simultaneously. The swing phase
was also defined by using a manual trigger that was set at
2. Materials and methods initial contact of the ipsilateral leg.
Characteristic values of the vertical component of the
Twenty healthy subjects (25.9 ± 1.2 years, 61.6 ± 11.5 kg, ground reaction force (vGRF) were used to subdivide phases
178 ± 9.5 cm) participated in the study. All subjects signed of the EMG and to define parameters of the motion analy-
an informed consent form and filled out a short questionnaire sis curves (Fig. 1). Angles in the sagittal plane of the ankle,
before participation. All experimental procedures were per- knee and hip were calculated at the occurrence of the first
formed in accordance to the principles of the Declaration of peak (loading response peak), relative minimum (mid-stance
Helsinki. Subjects with a history of neurological disease or valley) and second peak (terminal stance peak) of the vGRF.
diabetes were excluded. Force plate measurements; (EMG) Mean EMG activity of the muscles were calculated for four
measurements and three-dimensional movement analysis different phases of the vGRF, i.e. the phase between ground
were performed simultaneously during walking before and contact and first peak, the phase between first and second
after reduction of plantar sensation. peak, the phase between second peak and toe off and the
Surface EMG signals of 12 muscles of the right leg were phase between toe off and the end of the swing phase. The
recorded using bipolar electrodes (Blue sensor (N-50-K), maximum braking and acceleration force peaks of the hor-
Medicotest GmbH, Olsstykke, Denmark). The skin was izontal component of the ground reaction force were also
prepared with abrasive skin prepping gel and alcohol to used for analysis.
minimized impedance below 6 k. The electrodes were For the reduction of plantar sensation, the right foot was
placed with an inter-electrode distance of 2 cm on the mus- placed in a cold water container (0 ◦ C) for 10 min. The foot
cle bellies of the tibialis anterior, peroneus longus, soleus, was placed on a grid that was surrounded by iced water
gastrocnemius medialis, biceps femoris, vastus medialis so that only the plantar aspect of the foot was submerged.
and lateralis, rectus femoris, adductor longus, tensor faciae This cooling procedure was reported to sufficiently influ-
latae, gluteus medius and maximus. All electrode place- ence plantar sensation as confirmed with Semmes–Weinstein
ments were performed by the same investigator using the monofilaments [15].
SENIAM recommendation [16] and the correct placements A first-step walking method (subjects stood close enough
were checked by manual tests and voluntary contractions. to the platform and contacted the platform with their first
The Noraxon system and software were used to measure and step) was chosen to obtain a high repeatability of contact-
analyze EMG data (Noraxon Myosystem, Scottsdale, USA). ing the platform and to avoid targeting. Before the data
EMG signals were normalized to maximum voluntary con- collection, subjects performed several first-step walking tri-
traction values for each muscle. The raw EMG signal was als across the force platform with the complete EMG and
A/D converted and sampled with 1200 Hz and 12 bit resolu- marker setting to familiarize themselves with the equipment
tion, filtered (bandpass 10–1000 Hz), rectified and smoothed and the testing procedure. After the 10 min cooling proce-
(RMS 50). dure, the subjects performed two trials of first-step walking
Three-dimensional movement analysis was performed us- over the force platform. The high repeatability of contacting
ing a set of six cameras in combination with reflective mark- the platform in first-step walking was important because
ers that were placed on anatomical landmarks of the subjects of the foot warming up which only allowed few measure-
using the “Helen Hayes Marker Set”. The marker placements ments. Only two first-step walking trials were measured
were the anterior superior iliac spine (left and right), sacrum, directly after the cooling to prevent foot warm-up. The foot
mid-thigh (left and right—wand markers), lateral knee (left was then submerged for additional 10 min in ice water and
and right), mid-shank (left and right—wand markers), lat- the next two steps were recorded until six steps under iced
eral malleolus (left and right), calcaneus (left and right) and conditions were measured.
foot between second and third metatarsal heads (left and For statistical analysis, the mean of six trials was calcu-
right). The Motion Analysis system and software (Motion lated. Differences between normal and iced conditions were
Analysis, Santa Rosa, CA, USA) were used to measure and determined using the nonparametric dependent Wilcoxon
analyze three-dimensional motion data. The system had a signed rank test. The statistical level of significance was set
sampling frequency of 60 Hz and the dimension of the cali- at P < 0.05.
56 E. Eils et al. / Gait and Posture 20 (2004) 54–60
1.4
1.2
1
Bodyweight
0.8
0.6
0.4
normal iced
0.2
0
0 20 40 60 80 100
Ground contact [%]
Table 1
Ground reaction force parameters under normal and iced conditions
Ground reaction force parameters Normal Iced P-level
Table 2
Angles (sagittal plane) of the ankle, knee and hip at the beginning of ground contact, occurrence of first peak, minimum, second peak and end of ground
contact under normal and iced conditions
Kinematic parameters Ankle angles (◦ ) Knee angles (◦ ) Hip angles (◦ )
(sagittal plane)
Normal Iced P-level Normal Iced P-level Normal Iced P-level
Begin of contact 4.0 ± 3.5 2.3 ± 4.3 0.0025 17.7 ± 5.4 18.3 ± 5.1 n.s. 33.9 ± 7.4 33.9 ± 6.6 n.s.
First peak 9.5 ± 3.2 10.0 ± 3.0 n.s. 25.5 ± 6.8 24.6 ± 6.1 n.s. 24.1 ± 7.2 23.5 ± 7.2 n.s.
Minimum 13.4 ± 3.1 13.4 ± 2.9 n.s. 14.5 ± 4.2 14.8 ± 4.1 n.s. 7.4 ± 6.2 8.5 ± 5.2 n.s.
Second peak 16.2 ± 3.0 15.9 ± 3.1 n.s. 12.0 ± 4.4 11.9 ± 4.9 n.s. −8.7 ± 6.1 −6.7 ± 5.1 0.0005
End of contact −11.6 ± 5.6 −9.6 ± 6.3 0.008 43.8 ± 4.8 42.9 ± 5.8 0.0479 −1.0 ± 6.0 0.4 ± 6.2 0.0366
Neutral positions were derived from straight standing. For the ankle and the hip joint positive values indicate flexion (dorsiflexion at the ankle, hip
flexion), negative values indicate extension (plantar flexion at the ankle, hip extension). For the knee joint values indicate the angle between neutral
position and shank.
the thigh. The hip muscles showed no consistent tendency contact and push-off with accordingly modified EMG and
(Table 3). The mean amplitudes of the gastrocnemius medi- motion patterns. Furthermore, these results explain previous
alis (P = 0.0080) and tibialis anterior (P = 0.0015) were observations where a characteristically modified roll-over
significantly decreased under iced conditions. pattern from pressure distribution measurements was found
Mean amplitudes were decreased for the muscles of the under iced conditions [15].
shank and increased for the muscles of the thigh under Plantar sensation was reduced using a 10 min ice immer-
iced conditions in phase 3. Muscles of the hip showed sion technique. Although reduced sensitivity after cooling
an inconsistent behavior. The decreased amplitude under was not explicitly tested in this investigation, it is well doc-
iced conditions was significant for the medial gastrocne- umented that this technique reduces significantly plantar
mius (P = 0.0064), peroneus longus (P = 0.0003), biceps sensation by influencing mainly the mechanoreceptors of the
femoris (P = 0.0013), adductor longus (P = 0.00187) and skin [4,13,15]. Apart from reduction of sensory function, the
tensor faciae latae (P = 0.0111). cooling procedure may produce other effects such as hyper-
In the swing phase (phase 4) the mean amplitude of the or paraesthesia. In a previous investigation, different dura-
muscles of the shank, the thigh and most of the hip muscles tions of cooling were subsequently tested and sensation was
was increased under iced conditions. The increased ampli- evaluated after cooling with Semmes–Weinstein monofil-
tude under iced conditions was significant for the extensors aments. No signs of hyperaesthesia were found during or
of the thigh (vastus medialis (P = 0.0251) and lateralis directly after cooling and initial sensation returned between
(P = 0.0100), rectus femoris (P = 0.0304)) as well as for 5 and 10 min after cooling [15]. Concerning paraesthesia,
the tensor faciae latae (P = 0.0008). subjects did not report any sensation that would indicate
such an effect. After submerging the sole of the foot in ice
water, subjects initially reported a feeling of discomfort that
4. Discussion decreased and vanished after a few minutes. During and
after subsequent cooling, subjects did not report any further
This investigation has shown that altered plantar sensation discomfort.
using an ice immersion approach leads to a substantially A first-step walking method was used in this investigation.
modulated gait strategy indicating a more cautious ground It has to be considered that a first-step in walking will be
58
Table 3
Muscle activity parameters of 12 selected muscles of the lower extremity and the hip in different phases of the gait cycle under normal and iced conditions
different from a step during full gait due to differences in sult of the decreased activity at ground contact and weight
braking and accelerating the centre of mass of the body. A bearing (phase 1) that still affected the activity level in
different strategy between normal and iced conditions for phase 2. The decreased activity of medial gastrocnemius
first-step and full gait is certainly not expected. However, it in phase 2 indicates the start of the observed decreased
should be kept in mind that the presented results are based muscle activity in the push-off phase (phase 3). Although
on the first-step walking method. the above-mentioned differences between conditions were
The vertical and horizontal component of the ground found, the contact time did not differ significantly between
reaction force showed a comparable ground contact time the two conditions. This suggests that the observed changes
but marked changes under iced condition. In the loading during ground contact may be counterbalanced in the swing
response, a reduction of the first peak was measured under phase. The results of the EMG analysis in phase 4 reflects
iced condition that was not significantly different from nor- this assumption: the mean activity of the knee extensor in-
mal conditions but appeared significantly later in the gait creased significantly in this phase and indicated an acceler-
cycle. The braking force peak was also significantly reduced ated swing forward of the lower limb under iced conditions.
under iced condition. This suggests that the initial foot con- This study has shown that there were marked differences
tact with the ground was performed more cautiously than in gait affecting the whole lower limb under iced condi-
under normal conditions. A similar strategy is seen for the tions. In general, sensation from the sole of the foot has
second peak indicating a more cautious push-off. After ice been demonstrated to have an influence on posture and gait
immersion the second and the acceleration force peak were when using patients with diabetic neuropathy as a specific
significantly decreased and the second peak appeared signif- model, ischaemic block techniques or an ice immersion ap-
icantly earlier. In addition to the reduced peak force values, proach. For example, Sacco and Amadio, Katoulis et al. and
the significantly increased minimum suggests a diminished Mueller et al. studied gait parameters in patients with dia-
dynamic of the ground contact phase under iced conditions. betic neuropathy in comparison to healthy controls [17–19].
These results are in accordance with recently performed These authors found reduced peak forces of the vertical
plantar pressure distribution measurements. Nurse and Nigg ground reaction force at loading response and push-off,
and Eils et al. reported significantly reduced peak pres- decreased bracing and acceleration force peaks of the hor-
sures under the heel and the forefoot at ground contact and izontal ground reaction force and reduced plantar flexion
push-off after ice immersion of the sole of the foot [13,15]. angles in walking when compared with controls. Dickey
In addition, Eils et al. [15] reported a substantially modified and Winter reported substantial modifications in walking
pressure distribution pattern in walking that was also char- after inducing a unilateral ischaemic block [9]. Changes
acterized by a significant load shift to the lateral part of the in the tibio-talar joint angles as well as decreased activity
foot and a more even load distribution over the whole foot of tibialis anterior were found after inducing an ischaemic
by an early and prolonged foot-flat position. block. In diabetic polyneuropathy and ischaemia afferent
The three-dimensional movement and EMG analysis also information of different systems is impaired causing diffi-
supports the above-mentioned hypothesis of a more cautious culty of evaluating the influence of information from single
beginning and end of contact. Significant changes in ankle, systems. In the above-mentioned studies, the influence of
knee, and hip angles were found especially at the beginning impaired sensation on gait patterns (angles, muscle activity)
and end of ground contact. At the instant of ground contact, was more pronounced than in the present investigation un-
dorsiflexion of the ankle was significantly reduced leading derlining the decreased afferent input from several different
to a more flat touch down, whereas knee and hip angles were sensor systems. Ice immersion approaches have also been
similar under iced conditions. At the end of ground contact, used to study the influence of reduced plantar sensation
a significantly decreased plantar flexion, knee and hip flex- on posture and gait [13–15,20,21]. Magnusson et al. and
ion indicate a less pronounced push-off from the ground. In Asai et al. demonstrated that cutaneous information of the
the phase between initial contact and first peak of the verti- sole of the foot is important in balance regulation during
cal component of the ground reaction force as well as from standing [14,20]. Nurse and Nigg as well as Eils et al.
the second peak and end of contact, the mean muscle activ- have shown the important influence of plantar sensation
ity was significantly reduced for characteristic muscles. The on roll-over in walking and Perry et al. have shown that
decreased dorsiflexion at ground contact and the decreased cutaneous sensation contributes to the control of the centre
plantar flexion at push-off were caused by significantly de- of mass during gait termination [21]. Although different
creased amplitudes of tibialis anterior, gastrocnemius medi- aspects of reduced plantar sensation have been studied, a
alis and peroneus longus under iced conditions. At ground more complete analysis of the lower extremities has not
contact, the decreased amplitude of the extensors of the knee been performed previously and the present investigation
and all hip muscles under iced conditions indicated a more provides further insights into the control mechanisms of
smooth initial contact and weight bearing for the whole leg. gait and posture related to reduced plantar sensation.
There was a significant decrease in muscle activity for In general, decreased tactile sensation, poor balance, in-
the tibialis anterior and the medial gastrocnemius muscle in creased body sway, and impaired sensory function of the
phase 2. The decreased tibialis anterior activity is the re- lower limbs are strongly associated with falls in the elderly
60 E. Eils et al. / Gait and Posture 20 (2004) 54–60
[22,23]. In addition, there is evidence that the control of gait [11] van Deursen RW, Simoneau GG. Foot and ankle sensory neuropathy,
and posture is a clinically relevant problem in patients with proprioception, and postural stability. J Orthop Sports Phys Ther
1999;29:718–26.
diabetic neuropathy [24]. The results of the present study [12] Eils E, Tewes M, Nolte S, Rosenbaum D. Der Einfluss reduzierter
may be of importance concerning the risk of falling in the Fußsohlensensorik auf Schwankungs- und Druckverteilungsparame-
elderly population or in patients with diabetic neuropathy. ter beim Stehen und Gehen. Med Orth Tech 2003;4:46–54.
Elderly patients or those with diabetes mellitus were not in- [13] Nurse MA, Nigg BM. The effect of changes in foot sensation on
vestigated in the present study but the techniques used may plantar pressure and muscle activity. Clin Biomech 2001;16:719–
27.
be applicable to these patient groups for future research. In [14] Magnusson M, Enbom H, Johansson R, Pyykko I. Significance of
conclusion, the present investigation showed that short term pressor input from the human feet in anterior-posterior postural
reduced afferent information from the sole of the foot sub- control. The effect of hypothermia on vibration-induced body-sway.
stantially modifies the normal gait pattern. Acta Otolaryngol 1990;110:182–8.
[15] Eils E, Nolte S, Tewes M, Thorwesten L, Rosenbaum D. Modi-
fied pressure distribution patterns in walking following reduction of
plantar sensation. J Biomech 2002;35:1307–13.
References [16] Hermens HJ, Freriks B, Disselhorst-Klug C, Rau G. Development
of recommendations for SEMG sensors and sensor placement pro-
[1] Grillner S. Control of locomotion in bipeds, tetrapods, and fish. In: cedures. J Electromyogr Kinesiol 2000;10:361–74.
Brooks B, editor. Handbook of physiology, vol. II, part 2. Washington, [17] Sacco IC, Amadio AC. A study of biomechanical parameters in gait
DC: The American Physiological Society; 1981. p. 1179–236. analysis and sensitive cronaxie of diabetic neuropathic patients. Clin
[2] Gandevia SC, Burke D. Does the nervous system depend on kines- Biomech 2000;15:196–202.
thetic information to control natural limb movements? Behav Brain [18] Katoulis EC, Ebdon-Parry M, Lanshammar H, Vileikyte L, Kulkarni
Sci 1992;15:614–32. J, Boulton AJ. Gait abnormalities in diabetic neuropathy. Diabetes
[3] Patla AE. Understanding the roles of vision in the control of human Care 1997;20:1904–7.
locomotion. Gait Posture 1997;5:54–69. [19] Mueller MJ, Minor SD, Sahrmann SA, Schaaf JA, Strube MJ. Dif-
[4] Perry SD, Santos LC, Patla AE. Contribution of vision and cuta- ferences in the gait characteristics of patients with diabetes and pe-
neous sensation to the control of centre of mass (COM) during gait ripheral neuropathy compared with age-matched controls. Phys Ther
termination. Brain Res 2001;913(1):27–34. 1994;74:299–308, and discussion 309–13.
[5] Wade MG, Jones G. The role of vision and spatial orientation in the [20] Asai H, Fujiwara K, Yamashina T, Nara I, Tachino K. The influence
maintenance of posture. Phys Ther 1997;77:619–28. of foot soles cooling on standing posture control. In: Brandt T, Paulus
[6] Straube A, Paulus W, Brandt T. Influence of visual blur on W, editors. Disorders of posture and gait. Stuttgart: Thieme; 1990.
object-motion detection, self-motion detection and postural balance. p. 198–201.
Behav Brain Res 1990;40(1):1–6. [21] Perry SD, McIlroy WE, Maki BE. The role of plantar cutaneous
[7] Horak FB, Nashner LM, Diener HC. Postural strategies associated mechanoreceptors in the control of compensatory stepping reactions
with somatosensory and vestibular loss. Exp Brain Res 1990;82:167– evoked by unpredictable, multi-directional perturbation. Brain Res
77. 2000;877:401–6.
[8] Diener HC, Dichgans J, Guschlbauer B, Bacher M. Role of visual [22] Lord SR, McLean D, Stathers G. Physiological factors associated
and static vestibular influences on dynamic posture control. Hum with injurious falls in older people living in the community. Geron-
Neurobiol 1986;5:105–13. tology 1992;38:338–46.
[9] Dickey JP, Winter DA. Adaptations in gait resulting from unilateral [23] Sorock GS, Labiner DM. Peripheral neuromuscular dysfunction and
ischaemic block of the leg. Clin Biomech 1992;7:215–25. falls in an elderly cohort. Am J Epidemiol 1992;136:584–91.
[10] Simoneau GG, Ulbrecht JS, Derr JA, Cavanagh PR. Role of so- [24] Cavanagh PR, Simoneau GG, Ulbrecht JS. Ulceration, unsteadiness,
matosensory input in the control of human posture. Gait Posture and uncertainty: the biomechanical consequences of diabetes mellitus.
1995;3:115–22. J Biomech 1993;26(Suppl 1):23–40.