Posterior-anterior body weight shift during stance period studied by measuring sole-floor reaction forces during healthy and hemiplegic human walking

Neuroscience Letters 399 (2006) 141 146 Posterior-anterior body weight shift during stance period studied by measuring sole-floor reaction forces during healthy and hemiplegic human walking Nobuyoshi Kobayashi a,, Tateo Warabi a, Masamichi Kato a, Kiichi Kiriyama a, Toshikazu Yoshida a, Susumu Chiba b a Clinical Brain Research Laboratory, Toyokura Memorial Hall, Sapporo Yamanoue Hospital, Yamanote 6-9-1-1, Sapporo 063-0006, Japan b Department of Neurology, School of Medicine, Sapporo Medical University, Minami-1, Nishi 16, Sapporo 060-8543, Japan Received 7 December 2005; received in revised form 4 January 2006; accepted 24 January 2006 Abstract Posterior-anterior body weight shift during stance phase of human overground locomotion was investigated by recording sole-floor reaction force from five anatomically discrete points with strain gauge transducers of 14 mm diameter attached firmly to the sole of bare foot. At first the subject was asked to walk straight on the laboratory floor at his/her preferred velocity. Then the subject was asked to walk curved path of about 1 m radius. For kicking off the body at the end of stance phase, sole-floor reaction force from 3rd metatarsal was stronger than 1st metatarsal or 5th metatarsal during the straight walking, thus body weight shift is represented from heel to 3rd metatarsal line. When walking along a curved path, two types of strategies were recognized; a group of subjects walked leaning to inner leading foot during stance period as judged by stronger forces recorded from 5th metatarsal combined with stronger force from 1st metatarsal of outer trailing foot. Another group of subjects showed almost the same patterns either in the straight and curved walking, suggesting the subjects changed direction of the foot during the immediately previous swing phase to the tangent direction of the curve and placed the foot without leaning the body weight to either direction. Hemiplegic patients showed strikingly different distribution of sole-floor reaction forces from the five points; strongest forces were recorded from 3rd and 5th metatarsals combined with reduced reaction force from heel, therefore characteristic y-vector patterns were observed. 2006 Elsevier Ireland Ltd. All rights reserved. Keywords: Straight walking; Circular walking; Sole-floor reaction force; Healthy human subjects; Hemiplegic patient Locomotion along a straight path, either on laboratory floor or on treadmill, is studied in usual set-up of experiment. Previous reports from our laboratory [9,10,16,17] describe various aspects of human locomotion investigated by recording solefloor reaction force from anatomically discrete five points of sole. In everyday life humans are frequently faced with changes in path direction, which can be either anticipated or unexpected. Courtine and Schieppati [2,3] investigated human walking along a curved path, and mentioned that the increased duration of the stance phase of the inner foot was accompanied by leaning of the trunk towards the inner side of the walking path [2]. Furthermore the authors reported that the decreased duration of the stance Corresponding author. Tel.: +81 11 621 1200; fax: +81 11 644 0435. E-mail address: yamanoue@alles.or.jp (N. Kobayashi). phase of the outer limb was probably related to the obligatory overall higher velocity of the outer limb, given the longer path to be traveled with respect to the inner limb [3]. Hase and Stein [8] investigated the mechanisms involved in rapid turning during human walking, and found two walking strategies, spin turn and step turn, were used depending on which leg was placed in front for breaking. During walking along a curved path in the previous study from our laboratory posterior-anterior body weight shift during stance phase was estimated by obtaining y-vector which was calculated from force curves of calcaneus and 3rd metatarsal [10]. The aim of the present study is to investigate how humans select locomotor pattern under (1) straight walking, (2) clockwise turning, and (3) anti-clockwise turning. For this purpose, posterior-anterior shift of body weight during stance phase was systematically studied by obtaining y-vector from (1) calcaneus and 3rd metatarsal, (2) calcaneus and 1st 0304-3940/$ see front matter 2006 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.neulet.2006.01.042

142 N. Kobayashi et al. / Neuroscience Letters 399 (2006) 141 146 metatarsal, and (3) calcaneus and 5th metatarsal in the healthy subjects. Furthermore, posterior-anterior body weight shift during stance phase of hemiplegic patients was also investigated compared with healthy subjects. There are two subject groups: healthy control groups and hemiplegic patients. (1) Healthy control subjects are 10 adults without known neurological disorders or discrepancies between right and left lower limbs that could affect the experimental outcome (5 males: 21 31 years, average 24.2 ± 4.0 years; 5 females: 21 33 years, average 23.6 ± 5.2 years). These subjects are the same subjects who were studied on different aspects of locomotion in an earlier publication [10]. (2) Five patients showed hemiplegic limbs due to cerebral hemorrhage (47 71 years, 3 male and 2 female). Both groups of the subjects were fully informed of the purpose and procedures including estimated time of the measurement and consented voluntarily to participate the measurement. The study was in accordance with Declaration of Helsinki [18] and was approved by Ethics Committee of Yamanoue Hospital. The method to record the sole-floor reaction force was fully documented in the earlier publications [9,16] from our laboratory. Therefore, the method is briefly described here. Strain gauge load cells (NEC, San Ei, type 9E01-L42-500N, diameter 14 mm, thickness 4 mm, measuring range 0 500 Newton) were used. The load cells were securely adhered with double faced adhesive tape on the skin of five points of the sole: (1) medial process of calcaneus, (2) head of 5th metatarsal, (3) head of 3rd metatarsal, (4) head of 1st metatarsal and (5) middle of great toe. The subject wore a cotton socks to secure the load cells. Leading wires from the gauges were attached on foot and leg with surgical tapes and connected to the power supply (about 50 gr) which was held around waist with a belt. Outputs from the load cells were fed to multichannel pen oscillograph (NEC San Ei Rectiholy 8K20) through amplifiers and low-pass filters (frequency range; 0 200 Hz), simultaneously stored on magnetic tapes. The analogue outputs from the gauges were digitized with a microcomputer (NEC San Ei Signal Processor 7T18T) at a sampling frequency of 250 Hz and were fed into a personal computer. At first the subjects were asked to walk on the laboratory floor with the preferred velocity for 10 m. This walking was repeated for five or six times in order to collect experimental data from the five points along with obtaining the average walking velocity. The subjects were asked to maintain gaze straight ahead with head position about 15 downward during straight walking, as in our previous study [16]. Then the subjects were asked to walk on circular path with about the same speed. For walking along circular path, the radius of curvature was about 1 m, and the subject was asked to walk both clockwise and counter-clockwise for about 20 steps each. No specific instruction was given to the subjects regarding gaze or head or body orientation during circular walking. One subject complained feeble vertigo during circular walking, then measurement was instantly stopped for this subject. For the hemiplegic patients, only straight walking was investigated. Method of calculation of posterior-anterior balance (or y- vector) of body shift was described in an earlier publication from our laboratory [9,10]. As described above, the analogue outputs from the gauges were digitized at a sampling frequency of 250 Hz and were stored in a personal computer. After measurement session three or four y-vectors were obtained off-line by subtracting digitized force curve of the calcaneus from digitized force curve of (1) 3rd metatarsal (C M3), (2) 1st metatarsal (C M1) and (3) 5th metatarsal (C M5) for the healthy subjects and in some patients (4) great toe (C G). x-vector was evaluated by subtracting digitized force curve of 5th metatarsal from digitized force curve from 1st metatarsal. The preferred walking velocities were 3.5 km/h for two subjects, 3.6 km/h for one subject, 4.0 km/h for five subjects and 4.5 km/h for two subjects. In our earlier reports, posterior-anterior body weight shift was discussed by obtaining y-vector by subtracting force curves Fig. 1. Distribution of sole-floor reaction force from the five points of one representative step of straight walking at 100 ms intervals. Time points were selected since touchdown of calcaneus. Stance phase proceeds from the left lowest (100 ms) and kicks off from the right-upper (700 ms) foot prints. Lengths of columns represent relative strength of sole-floor reaction force (e.g. 17.1 kg at calcaneus of 100 ms). Subject, T.M. male 20 years, height 176 cm body weight 60 kg. Walking velocity 4.0 km/h.

N. Kobayashi et al. / Neuroscience Letters 399 (2006) 141 146 143 of calcaneus from force curves of 3rd metatarsal [9,10,17]. Rationale to estimate posterior-anterior body weight shift from obtaining y-vector by subtracting force curve of calcaneus from force curve of 3rd metatarsal during straight floor walking was investigated in detail, as a basis for comparing straight walking and circular walking. Chronological distribution of sole-floor reaction force from the five points of one representative step is shown in Fig. 1. At the initial stage of the stance phase, sole-floor reaction force from calcaneus dominates (100 and 200 ms), then force from 5th metatarsal increases (200 400 ms), followed by strongest force from 3rd metatarsal (500 and 600 ms) and finally stance phase ends (700 ms). The period from 0 to 300 ms roughly corresponds to rearfoot phase of y-vector and period from 400 to 700 ms corresponds to forefoot phase. In the following figures (Figs. 2 4A) mean peak values (n = 15 steps) of sole-floor reaction force from the five points during stance period are illustrated. As examples from two subjects are illustrated in Fig. 2 (straight) and Fig. 3 (straight), sole-floor reaction force from 3rd metatarsal is statistically significantly (p < 0.01) stronger than force of either 1st metatarsal or 5th metatarsal. This relation was confirmed from data obtained from all the 10 healthy subjects. This relation was also observed in unaffected side of a patient illustrated in Fig. 4A. Based on these data it is a fair conclusion that posterior-anterior body weight shift directed from heel to 3rd metatarsal in the subjects studied in this project. Hence, it is reasonable to obtain y-vector by calculating from force curves of calcaneus and 3rd metatarsal. The lower part of y-vector was due to the impact of the heel, hence designated as the rearfoot phase, and the upper part coincides with the period when the body shifts forward and push off, therefore it was designated as the forefoot phase [9]. From the investigation of temporal patterns of force curves of calcaneus Fig. 2. (A) Peak force values (kg) recorded from the five points on the sole are illustrated as relative heights of columns with mean values ± S.D. (n = 15 steps) at the corresponding points. (B) Averaged y-vectors (n = 10 steps) of C M1, C M3 and C M5 are illustrated with heavy line and x-vector is shown with dotted line. Relative values of areas of forefoot phase of y-vector compared to the largest value are indicated as percentage for all the records. Left column shows data of outer foot during circular walking, middle column shows data of straight walking and right column shows results from inner foot during circular walking. Same subject as Fig. 1.

144 N. Kobayashi et al. / Neuroscience Letters 399 (2006) 141 146 Fig. 3. Peak force values from the five points (A) and y-vectors (B) as illustrated in Fig. 2. Subject; Y.K. female, 22 years, height 156 cm, weight 48 kg. Walking velocity 4.0 km/h. and 3rd metatarsal, it is said amplitude of lower going rearfoot phase is about 10% smaller than the peak value of the calcaneus, while the upper going forefoot phase the peak value correspond to peak value of 3rd metatarsal [16]. As can be seen in the middle columns of Figs. 2 and 3B, amplitudes of forefoot phases of C M3 is larger than either C M5 or C M1 for straight walking. These observations were supplemented by comparing areas of the forefoot phase of y-vector at C M1, C M3 and C M5. When area of C M3, which is the biggest among C M1, C M3 and C M5, was taken as 100, C M5 was 65.3% and C M1 was 56.7% in Fig. 2B straight. For the subject in Fig. 3B straight, C M5 was 37.1% and C M1 was 18.2%, as compared with C M3 which showed the largest area. In Figs. 2 4B, relative values of areas of forefoot phase of y-vector as compared to the strongest point are indicated as %. These findings indicate that posterior-anterior body weight shift is reasonably represented in line from calcaneus to 3rd metatarsal during straight walking. Successful recording was made on 9 among the 10 subjects; the reason being mentioned above. Compared with straight walking the process of changing path consists of decelerating the forward motion, rotating the body and stepping out toward the new direction. Two types of walking strategy were recognized. As is illustrated in Fig. 2A, one type of subject shows sole-floor reaction force from 5th metatarsal increased (p < 0.01) in inner foot as compared to straight walking while forces from 3rd and 1st metatarsals decreased. These changes are reflected in the patterns of three y-vectors shown in Fig. 2B. In the inner foot, the amplitude of forefoot phase of C M5 y-vector is much larger than straight and outer foot as compared in terms of amplitudes as well as areas of the forefoot phase. Also amplitudes of the rearfoot phase at C M3 and C M1 increased and duration elongated, indicating forward body weight sway in C M3 and C M1 directions delayed. These data show that the subject adjusts the body weight shift by leaning to inner side during stance phase. In the outer foot, rearfoot phase is not so different in the three y-vectors, while the forefoot phase of C M3 is the largest. This means that in the trailing (or outer) foot leaning to the inner side is compensated to some extent. This type

N. Kobayashi et al. / Neuroscience Letters 399 (2006) 141 146 145 Fig. 4. Peak force values (mean ± S.D.) from the five points of left (unaffected side) and right foot (affected side) which showed typical equinovarus deformity (A), and y-vector of C M1, C M3 and C M5 of both sides (B). Patient; A.M., female, 63 years old, height 151 cm, body weight 55.7 kg. Walking velocity about 2.5 km/h. of walking was observed in five subjects (three male and two female). The other type of walking strategy shown by a subject is illustrated in Fig. 3. This subject shows almost no recognizable changes in either inner or outer foot as compared with straight walking. Change of direction was apparently planned and executed during the immediately previous swing phase. This strategy is easier and more stable for the subject because the base of support while changing direction is much more symmetric in the standing foot. This type of walking strategy was observed on four subjects (two males and two females). Central locomotor pattern generator in mammals such as carnivores and rodents is located mainly in the lumbosacral spinal cord [12]. Although normal walking is automatic, it is not necessarily stereotyped. Central pattern generators are quite flexible. Three important types of sensory information are used to regulate stepping; somatosensory input from the receptors of muscle and skin, input from the vestibular apparatus (for controlling balance), and visual input. Motor cortex is involved in the control of precise stepping movements in visually guided walking. The cerebellum fine-tunes the locomotor pattern by regulating the timing and intensity of descending signals [15]. Recent researches on the locomotor function of human subjects with a complete spinal cord injury at either lower cervical or upper thoracic cord [1,4 7], and of human infants [13,14] strongly suggest that essentially the same mechanisms exist in human spinal cord as do in carnivores or rodents. Lamb and Yang [11] argued that a common locomotor pattern generator controls walking in all different directions in human infants. The present experimental results suggest that humans adjust their locomotor pattern generator either for walking on straight as well as curved paths by presumably inputs from supraspinal structures, although the mechanisms are yet to be clarified. Fig. 4 illustrates data obtained from a patient. This female patient of 63 years old suffered subcortical hemorrhage at left hemisphere 15 months earlier. She showed Brunnstrom stage III spastic hemiplegia for both upper and lower limbs of right side, and showed equinovarus deformity during standing as well as walking. The patient walked straight at about 2.5 km/h without using a cane, however she could not walk curvilinear path. To change walking direction she once stopped walking and resumed walking after changing direction of her body. As can be seen from the figure, unaffected left foot showed the pattern which could not be differentiated from the healthy subjects illustrated in Figs. 2 (straight) and 3 (straight). On the contrary, affected right side reveal characteristic pattern of distribution of sole-floor reaction forces in the sole; extremely weak force from the calcaneus and unusually strong force from 5th metatarsal (Fig. 4A). These characteristic distribution of force is reflected on the pattern of y-vector obtained from C M3 and C M5 metatarsals, as are illustrated in Fig. 4B. The most characteristic feature of this patient is that rearfoot phase of y- vector is lacking. Among the other four hemiplegic patients, two patients could not walk curvilinear path as the patient described in Fig. 4, and the remaining patients could walk curvilinear path but with difficulty. Distribution of the peak values from the five points differed among the hemiplegic patients, hence patterns of y-vector are different. This point is in preparation for other report. Total peak values of sole-floor reaction forces of the five points are 52.6 kg for the affected side and 62.0 kg for the unaffected side, and the difference was statistically significant (p < 0.01) in this patient. This tendency was observed in all the present subjects. Stance period of the unaffected side was 1490.6 ± 93.1 ms (n = 15 steps) and that of the affected side was 1231.3 ± 84.5 ms, and the difference was statistically significant (p < 0.01). This difference was observed in all the hemiplegic patients (n = 10, including this patient) and the difference was statistically significant (paired t-test, p < 0.01). There was no difference in cadence of the unaffected and affected sides (p = 0.88). From these data it can be said that the hemiplegic patients use the affected side with short stance period and weaker solefloor reaction force, alongside with compensatory use of the

146 N. Kobayashi et al. / Neuroscience Letters 399 (2006) 141 146 unaffected side which showed longer stance period and stronger reaction force. Acknowledgements The authors would like to express their gratitude to Professor R. Makino of Ohio State University for improving English. Skillful technical assistance with data collection and illustration by Ms. Ayano Sasaki is greatly acknowledged. References [1] J.A. Beres-Jones, S.J. Harkema, The human spinal cord interprets velocity-dependent afferent input during stepping, Brain 127 (2004) 2232 2246. [2] G. Courtine, M. Schieppati, Human walking along a curved path. I. Body trajectory, segment orientation and the effect of vision, Eur. J. Neurosci. 18 (2003) 177 190. [3] G. Courtine, M. Schieppati, Human walking along a curved path. II. Gait features and EMG patterns, Eur. J. Neurosci. 18 (2003) 191 205. [4] V. Dietz, G. Colombo, L. Jensen, L. Baumgartner, Locomotor capacity of spinal cord in paraplegic patients, Ann. Neurol. 37 (1995) 574 582. [5] V. Dietz, R. Mueller, Degradation of neuronal function following a spinal cord injury: mechanisms and countermeasures, Brain 127 (2004) 2221 2231. [6] V. Dietz, R. Mueller, G. Colombo, Locomotor activity in spinal man: significance of afferent input from joint and load receptors, Brain 125 (2002) 2626 2634. [7] S.J. Harkema, S.L. Hurley, U.K. Patel, P.S. Requejo, B.H. Dobkin, R. Edgerton, Human lumbosacral spinal cord interprets loading during stepping, J. Neurophysiol. 77 (1997) 797 811. [8] K. Hase, R.B. Stein, Turning strategies during human walking, J. Neurophsyiol. 81 (1999) 2914 2922. [9] K. Kiriyama, T. Warabi, M. Kato, T. Yoshida, N. Kobayashi, Progression of human body sway during successive walking studied by recording sole-floor reaction forces, Neurosci. Lett. 359 (2004) 130 132. [10] K. Kiriyama, T. Warabi, M. Kato, T. Yoshida, N. Kobayashi, Mediallateral balance during stance phase of straight and circular walking of human subjects, Neurosci. Lett. 388 (2005) 91 95. [11] T. Lamb, J.F. Yang, Could different directions of infant stepping be controlled by the same locomotor central pattern generator? J. Neurophysiol. 83 (2000) 2814 2824. [12] G.N. Orlovsky, T.G. Deliagina, S. Grillner, Neuronal control of locomotion. From mollusk to man, Oxford University Press, Oxford, 1999. [13] M.Y.C. Pang, J.F. Yang, The initiation of the swing phase in human infant stepping: importance of hip position and leg loading, J. Physiol. 528 (2000) 389 404. [14] M.Y.C. Pang, J.F. Yang, Interlimb co-ordination in human infant stepping, J. Physiol. 533 (2001) 617 625. [15] K. Pearson, J. Gordon, Locomotion, in: E.R. Kandel, J.H. Schwartz, T.M. Jessell (Eds.), Principles of neural sciences, fourth ed., McGraw- Hill, Co, New York, 2000, pp. 737 755. [16] T. Warabi, M. Kato, K. Kiriyama, T. Yoshida, N. Kobayashi, Analysis of human locomotion by recording sole-floor reaction forces from anatomically discrete points, Neurosci. Res. 50 (2004) 419 426. [17] T. Warabi, M. Kato, K. Kiriyama, T. Yoshida, N. Kobayashi, Treadmill walking and overground walking of human subjects compared by recording sole-floor reaction force, Neurosci. Res. 53 (2005) 343 348. [18] World Medical Association, Declaration of Helsinki on Ethical principles for medical research involving human subjects. 2004 http://www. wma.net/.