- Email: [email protected]
Changes in distal muscle timing may contribute to slowness during sit to stand in Parkinsons disease
Clinical Biomechanics 20 (2005) 112–117 www.elsevier.com/locate/clinbiomech
Changes in distal muscle timing may contribute to slowness during sit to stand in Parkinsons disease Mark Bishop a
a,*
, Denis Brunt b, Neeti Pathare a, Mansoo Ko a, Jill Marjama-Lyons
c
Department of Physical Therapy, University of Florida, P.O. Box 100154, Gainesville, FL 32610-0154, USA b Department of Physical Therapy, East Carolina University, North Carolina, USA c Parkinson Center (PADRECC), Veterans Affairs Hospital, Albuquerque, NM, USA Received 13 November 2003; accepted 4 August 2004
Abstract Objective. To compare patterns of muscle activation in the lower extremity and subsequent forces during sit to stand in persons with Parkinsonism. Background. There is an interruption of the tibialis anterior/soleus interaction during forward oriented movements in some subjects with Parkinsonism, including sit to stand. This task is a major determinant of independence and 44% of those with Parkinsonism report difficulty. Methods. 41 subjects with Parkinsonism were asked to stand up from a bench. Peak acceleration and vertical ground reaction forces, the slopes to these peaks, and the timing of events were measured. Surface electrodes were placed on tibialis anterior and soleus. Results. The slower group produced force at slower rate than the fast group. The slower group spent 64% of the time taken to stand to complete the flexion-momentum phase, and the fast group spent 56%. The slower group had a larger proportion of co-contraction trials than the other groups. Conclusions. Slower subjects took longer to perform the task due to a longer time for seat off. Deficits recruiting tibialis anterior may contribute to the decreased rate of production of the acceleration forces and the longer time required for seat off. Relevance Decreased rate of rise of force is used to identify fallers in the elderly and subjects with stroke. Decreased rates of force production may therefore assist in identifying those with Parkinsonism at risk of falls. Treatment strategies designed to facilitate tibialis anterior activation may improve the functional performance of this task. 2004 Elsevier Ltd. All rights reserved. Keywords: Reciprocal inhibition; EMG
1. Introduction Rising from a sitting to a standing position (STS) is a common skill of daily living and an important measure of physical function (Kelly et al., 1976; Rodosky et al., 1989). During STS the bodyÕs center of mass is shifted *
Corresponding author. E-mail address: [email protected]fl.edu (M. Bishop).
0268-0033/$ - see front matter 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.clinbiomech.2004.08.002
forward and vertical from a relatively large, stable base of support created by contact with the chair and the ground to a much smaller base under the feet (Riley et al., 1991). The central nervous system is challenged to simultaneously control both the whole body movement and equilibrium (Hirschfield et al., 1999). Schenkman et al. (1990) have provided an adequate description of the successive phases of STS. First, the trunk is flexed (flexion-momentum phase) followed by the initiation of
M. Bishop et al. / Clinical Biomechanics 20 (2005) 112–117
vertical momentum as the buttocks are lifted off the chair (momentum transfer phase). The extension phase follows which ends when the hips are in extension and body sway must then be controlled (stabilization phase). Consequently, completing this seemingly simple task becomes a challenge for those with functional limitations. While there have been studies on stroke patients (Brunt et al., 2002; Cheng et al., 1998; Yoshida et al., 1983), research on other patient populations, such as those with ParkinsonÕs disease (PD) has been limited. This is somewhat surprising as 44.2% of persons with PD have difficulty with STS (Mano et al., 1988) and STS transfers appear to be one of the major determinants for independence and quality of life for those with PD (Hobson, 1999). That the risk of falling exists in elderly who have difficulty rising from a chair (Campbell et al., 1989; Nevitt et al., 1989) and impairments in mobility and falls are a characteristic of PD, reinforces the need to further study the STS task in persons with PD. Studies in the elderly (Yoshida et al., 1983) and patients who are stroke survivors (Brunt et al., 2002; Cheng et al., 1998; Yoshida et al., 1983) show that they perform the sit to stand task slowly. Slowness of movement in PD has clearly been demonstrated in gait initiation (Gantchev et al., 1996; Halliday et al., 1998), and upper extremity tasks (Corcos et al., 1996; Ikeda et al., 1991). The investigation of differences in activities of daily living or locomotor skills among groups of patients with PD based on slowness of movement is important for three reasons. First, expected speed of movement may provide a means to evaluate change following therapeutic intervention. Second, understanding what components of a skill contribute to overall slowness of the movement may well guide rehabilitation strategies. The selected strategy and functional status of an individual are closely connected and identification of the former allows for the modification of the latter. Third, understanding the sub-clinical mechanisms of slowness of movement could further guide rehabilitation strategies. We were specifically interested in the interaction of the soleus (SOL) and tibialis anterior (TA) muscles. It is well documented that during the initiation of gait activation of the TA and inhibition of the SOL begins the backward movement of the center of pressure and the initiates forward momentum (Breniere et al., 1987; Brenie`re et al., 1981; Brunt et al., 1991, 1999). Studies have shown a deficit in this pattern in PD patients and thus their gait initiation is slow (Gantchev et al., 1996; Halliday et al., 1998). The same mechanism of TA and SOL interaction is present at the beginning of STS (Goulart and Valls-Sole, 1999; Khemlani et al., 1999). The primary aim of this study was to compare the characteristics of STS in two groups of persons with PD. We speculated that there would be differences in
113
the patterns of muscle activation in the lower extremity when comparing fast and slower moving persons with PD. Specifically, we first hypothesized that there would be an interruption of the normal TA and SOL interaction in slower moving subjects. Second, it was hypothesized that the first phase of STS would be prolonged in those subjects that showed the alteration of the TA and SOL interaction. That is, we expect that the there will be an increase in the proportion of the total time taken to stand spent in the flexion momentum phase or first stage of STS.
2. Methods 2.1. Subjects Forty-one subjects (21 male and 20 female) with PD participated in this study. SubjectÕs ages were between 50 and 79 years (66, SD 8.3). Subjects were within Stages I–III of the Hoehn and Yahr classification and their United Parkinsons disease Rating Scale (UPDRS) Motor part III score ranged from 4 to 58. Subject characteristics within groups are summarized in Table 1. All subjects were able to stand up and walk independently. Subjects were on levodopa medication and were tested approximately 1.5 h following the administration of their medication, the timing of which was determined by the patientÕs physician. All subjects read and signed an informed consent form approved by the University Institutional Review Board. 2.2. Equipment After appropriate skin preparation, surface electrodes were applied to the muscle belly of the TA and to the muscle belly medial to the tendoachilles and distal to the medial gastrocnemius. Placement was confirmed by comparing the myoelectric signal during resisted ankle plantar flexion to that during resisted knee flexion. Each electromyographic (EMG) recording electrode consisted of two silver–silver chloride 1 cm diameter electrodes embedded in an epoxy-mounted preamplifier system (·35) spaced 2 cm apart. A reference electrode was attached to the medial aspect of the tibia. The EMG signals were band-pass filtered, (20 Hz–4 kHz; Table 1 Patient characteristics for Groups A and B
Age (years) Disease duration (years) Hoehn and Yahr UPDRS (III)
Group A
Group B
66.1 4.8 2 21
66.5 7.4 2.5 19
(55–80) (0.5–8) (1–2.5) (13–40)
(53–79) (0.5–14) (1–3.5) (4–36)
Values represent mean (range), or median (range). UPDRS—United Parkinsons Disease Rating Scale.
114
M. Bishop et al. / Clinical Biomechanics 20 (2005) 112–117
Therapeutics Unlimited, Iowa City, Iowa, USA) full wave rectified, and low pass filtered (350 Hz) on-line. Final amplification was 10 K. Two force platforms, (Advanced Mechanical Technology Inc., Watertown, MA, USA) were situated on the floor to measure ground reaction forces. Processed EMG and amplified force platform signals were sampled online at 1000 Hz for 8 s (BIOPAC Systems, Goleta, CA, USA). 2.3. Procedure Seat height was adjusted such that subjectsÕ knees were placed in approximately 90 of flexion. Arms were kept folded across the trunk with the palms of the hands flat against the rib cage. Subjects were instructed to look straight ahead at the light signal and stand, at their selfselected pace, when the light signal came on. Five satisfactory trials were completed. 2.4. Data analysis We have noted previously that scores on the Hoehn and Yahr Scale are not sensitive enough to discriminate between groups during a functional task, such as gait termination (Bishop et al., 2003). Subjects were divided into two groups based upon their time from the onset of movement to peak vertical ground reaction force (Fz; see Fig. 1). The mean time to complete STS was (807.35, SD 223.85 ms). Patients with mean times equal to or less than half a standard deviation below the population mean were placed in Group A (n = 12, 6695.43 ms).
Fx
Those patients with a mean time equal to or greater than half a standard deviation above the population mean were placed in Group B (n = 10, 6919.28 ms) leaving the data from 22 subjects for analysis. Fig. 1 shows the force plate data from a single trial of STS for a patient from Group A. The first vertical line represents movement onset at the first detectable shift in force plate activity. The peak anterior/posterior ground reaction force (Fx) is indicated by the second vertical line and represents the transition between the flexion-momentum and momentum-transfer stages of STS. The momentum-transfer stage ends approximately at peak Fz (third vertical line). These parameters have been described elsewhere (Brunt et al., 2002; Vander Linden et al., 1994). Although there appeared to be some asymmetry observed during experimental trials, no attempt was made to modify the patients preferred strategy during STS. Data were then analyzed from the task dependent limb as determined by peak vertical ground reaction forces generated during the extension phase. Dependent measures of temporal events were the absolute and relative time required to complete the flexion-momentum (phase I) and momentum transfer (phase II) stages of STS. Analysis of variance techniques were used to make comparisons of dependent variables between the two groups. Type I error was maintained at 5%. The dependent measures for the EMG data included the onset of TA with respect to movement onset. Muscle onset was determined as the point at which the EMG signal was two standard deviations above the mean background activity for 30 ms. The mean time of TA onset was considered for each subject. As we were uncertain of the nature of the distribution from which this data was drawn, a distribution-free rank sum test was used to compare the location of the groups. Reciprocal inhibition of the SOL muscle was also noted by visual inspection of the SOL muscle activity during or prior to the flexion momentum phase. Absence of SOL activity was categorized as presence of reciprocal inhibition.
Fz
3. Results Phase I
Phase I I
Fig. 1. Vertical (Fz) and horizontal (Fx) ground reaction forces from a single representative trial of the sit to stand task from a subject in Group A. The circles indicate the peak forces of both Fx and Fz. The first dashed vertical line represents movement onset, peak anterior/ posterior ground reaction force (Fx) is indicated by the second vertical line and represents the transition between the flexion-momentum and momentum-transfer stages of STS. The momentum-transfer stage ends approximately at peak Fz (third vertical line). The short vertical line = 20% body weight, the arrow indicates the direction of movement and 250 ms.
The two groups did not differ significantly in their Hoehn and Yahr and UPDRS scores, age and disease duration. The patient characteristics for both the groups are shown in Table 1. 3.1. Temporal events A summary of the results appears in Table 2. The end of the transfer-momentum stage (phase I + phase II) occurred 1056 ms (SD 254 ms) ms after the onset of movement for Group B and 644 ms (SD 65 ms) for Group A.
M. Bishop et al. / Clinical Biomechanics 20 (2005) 112–117
29.9
0.000
also resulted in a difference between groups that was statistically significant. Phase I took 64% of the total time for the slow group and 56% of the total time for the fast group (P < 0.001).
107.9
0.000
3.2. Muscle activity
1.5
0.230
0.6
0.446
11.3
0.003
Table 2 Mean (1 SEM) each of the dependent variables
Time to sit to stand (ms) Phase I (ms) Phase II (ms) Peak Fz (% BW) Slope Fz (% BWs 1) Peak Fx (% BW) Slope Fx (% BWs 1)
Group A
Group B
1055.87 (80.32) 663.41 (20.41) 392.45 (75.94) 37.43 (1.94) 137.71 (20.01) 9.66 (1.01) 15.95 (2.82)
643.53 (17.37) 341.88 (22.52) 301.65 (22.74) 39.52 (1.84) 218.06 (14.15) 13.04 (1.01) 40.76 (3.91)
115
F
P-value
5.43 24.5
0.030 0.000
Fz—vertical ground reaction force, Fx—anterior posterior ground reaction force.
For phase I alone, Group B took 663 ms (SD 20 ms) to complete the phase and Group A 341 ms (SD 23 ms). To determine if those in the slow group were slower across all phases of the task, or one phase in isolation, the timing of phase I was considered relative to the total time taken to complete both phases. This comparison
The onset of TA with respect to movement time was categorized into three patterns. These patterns were operationally defined for this study and single trial examples of these patterns of EMG activity are shown in Fig. 2. In the first pattern (Fig. 2A), the soleus is inhibited and TA is clearly active before the onset of phase II and the increase in Fz. Second, TA onset occurred after movement onset (Fig. 2B) and third, there was tonic activity of TA (Fig. 2C). The first pattern occurred in 91% of the trials for subjects in Group A and 70% of Group B. The second pattern occurred in 9% of the trials for subjects in Group A and 10% of the trials subjects in Group B. The third pattern occurred in none of the subjects in Group A and in 20% of the trials for Group B. When TA timing was considered as continuous data, a significant difference was noted between groups (Mann–Whitney U = 21, P = 0.037). TA onset occurred
Fig. 2. (A) Vertical ground reaction forces and EMG data depicting EMG Pattern 1. Note the TA onset with movement onset and the inhibition of the soleus. (B) Vertical ground reaction forces and EMG data depicting EMG Pattern 2. Note the late TA onset. (C) Vertical ground reaction forces and EMG data depicting EMG Pattern 3. Note the tonic TA activity. (D) Alternating bursts of TA and SOL activity. The dotted vertical line indicates movement onset. Solid vertical line indicates peak Fx. The arrow indicates the direction of travel and 250 ms. The short vertical line = 20% body weight and 0.10 mV.
116
M. Bishop et al. / Clinical Biomechanics 20 (2005) 112–117
more often prior to movement onset for Group A (median 67 ms, interquartile range (IQR) 60 ms), and after movement onset for Group B (median 40 ms, IQR 300 ms). Reciprocal inhibition of SOL was noted in all the subjects in the fast group and all but one subject in the slow group. However, this inhibition did not occur at movement onset as expected (Brunt et al., 2002, 1991, 1999, 2000) if the TA did not come on until after movement onset. In addition, those subjects that demonstrated tonic TA activity had multiple trials in which co-contraction occurred between the TA and SOL. This phenomenon was observed in about 30% of the trials in which tonic TA activity occurred.
4. Discussion The average time taken to complete the STS movement for all subjects with PD in our study was 807.35 (SD 223.85) ms. This is consistent with other work examining STS in those with PD (Mak and Hui-Chan, 2002). By comparison, in a previous study in our lab, healthy older adults (average age 66 years, SD 5.6 years) took an average of 798.8 (SD 166.4) ms to complete both phases during STS at their self-selected speed (Vander Linden et al., 1994). For the current investigation, we grouped subjects related to the speed with which they performed the movement. Group B took 1056 ms and Group A 644 ms to complete both phases I and II. For phase I alone, Group B took 663 ms (SD 20 ms) to complete the phase and Group A 341 ms (SD 23 ms). Mak and Hui-Chan (2002) report that the time to seat off is prolonged in absolute terms when comparing those with PD to able-bodied subjects. However, we previously found that healthy older adults took 522.5 ms (SD 704 ms) to complete phase I of STS (Vander Linden et al., 1994) thus, subjects in Group A in our current study completed STS more rapidly than healthy older adults. We speculate that the group of subjects with PD who were fast movers represents part of the population of persons with PD in whom hypokinesia is not clinically present (sub-clinical) but other clinical manifestations of PD maybe. For example, they may have had tremor or tone but not demonstrable slowness of movement on other clinical assessment batteries. We believe that this is more likely the case rather than the subjects having other dyskinesias. Deficits in TA recruitment patterns (onset after movement onset, or tonic activity) were more prevalent in the slower group of subjects (Fig. 2). In addition, trials occurred showing co-contraction between soleus and tibialis anterior. Both these events would decrease the net dorsiflexion torque at the ankle. Mak and Hui-Chan (2002) indicated that slowness in STS might be attrib-
uted to small ankle dorsiflexion torques produced. This was confirmed by a more recent study by Mak and colleagues in which net peak dorsiflexion torques were also lower in those with PD than able-bodied subjects (Mak et al., 2003). However, Pai and Rogers (1991) indicate that when healthy subjects modulated the speed at which they perform STS, that is, move as slowly as possible, dorsifexion torque at the ankle decreased. Therefore, it is difficult to determine whether the decreased dorsiflexion torques cause slower motion or if the torques are smaller because the movement is slower. Similarly, we are unable to say whether delayed onset of TA was the result of the slowness of movement, or the cause thereof. Based on our current findings it would seem that ankle activation strategies alone are not sufficient to account for differences in the time taken to perform STS. Nonetheless, 30% of the subjects in the slower moving group did not exhibit the expected pattern of TA activation. Gait initiation is another task in which difficulty coordinating the TA and SOL interaction presents limitations to those with PD (Burleigh-Jacobs et al., 1997; Crenna et al., 1990). In addition to a decrease in the ability to inhibit SOL, alternating bursts of TA and SOL have been identified in those with PD during gait initiation (Crenna et al., 1990) and other ballistic upper extremity motions (Berardelli et al., 1986). This pattern of multiple short bursts was also seen during STS in our current study and is shown in Fig. 2D. The alternating bursts of muscle activity occur after the signal to stand and prior to the initiation of movement. We speculate that this represents an impaired ability to generate enough muscle force with the initial activation of TA and subsequent bursts are required to generate the required movement pattern.
5. Conclusion Hypokinesia is related to decreased rates of force in upper extremity (Corcos et al., 1996). It would appear that this is likewise the case in the STS task. Those slow moving persons with PD, generated acceleration forces and vertical forces at slower rates. Decreased rate of rise of force is used to identify fallers in the elderly and subjects with stroke. Decreased rates of force production may assist in identifying those at risk of falls amongst those persons with PD and may imply greater functional impairment in performance of the STS than is indicated by traditional systems of rating impairment. Additionally, we speculate that improvement of TA recruitment during rehabilitation may facilitate change in rates of force production at the ankle and result in improvement in transitional tasks such as sit-to-stand.
M. Bishop et al. / Clinical Biomechanics 20 (2005) 112–117
References Berardelli, A., Dick, J.P., Rothwell, J.C., Day, B.L., Marsden, C.D., 1986. Scaling the size of the first agonist EMG burst during rapid wrist movements in patients with ParkinsonÕs disease. J. Neurol. Neurosurg. Psychiat. 49, 1273–1279. Bishop, M.D., Brunt, D., Fiolkowski, P., Pathare, N., Ko, M., Marjama-Lyons, J., 2003. Gait termination in parkinsonism: a review. J. Korean Acad. Phys. Therap. Assoc. 10, 43–60. Brenie`re, Y., Do, M.C., Sanchez, J., 1981. A biomechanical study of the gait initiation process. J. Biophys. Med. Nucl. 5, 197–205. Brenie`re, Y., Do, M.C., Bousset, S., 1987. Are dynamic phenomena prior to stepping essential to walking?. J. Mot. Behav. 19, 62–76. Brunt, D., Lafferty, M.J., Mckeon, A., 1991. Invariant characteristics of gait initiation. Am. J. Phys. Med. Rehab. 70, 206–212. Brunt, D., Liu, S.M., Trimble, M.H., Bauer, J., Short, M., 1999. Principles underlying the organization of movement initiation from quiet stance. Gait Posture 10, 121–128. Brunt, D., Short, M., Trimble, M., Liu, S.M., 2000. Control strategies for initiation of human gait are influenced by accuracy constraints. Neurosci. Lett. 285, 228–230. Brunt, D., Greenberg, B., Wankadia, S., Trimble, M.H., Shechtman, O., 2002. The effect of foot placement on sit to stand in healthy young subjects and patients with hemiplegia. Arch. Phys. Med. Rehab. 83, 924–929. Burleigh-Jacobs, A., Horak, F.B., Nutt, J.G., Obeso, J.A., 1997. Step initiation in parkinsonÕs disease: influence of levodopa and external sensory triggers. Movement Disord. 12, 206–215. Campbell, A.J., Borrie, M., Speras, G.F., 1989. Risk factors for falls in a community based prospective study of people 70 years and over. J. Gerontol. Med. Sci. 44 (M), 112–117. Cheng, P.T., Liaw, M.Y., Wong, M.K., Tang, F.T., Lee, M.Y., Lin, P.S., 1998. The sit-to-stand movement in stroke patients and its correlation with falling. Arch. Phys. Med. Rehab. 79, 1043– 1046. Corcos, D.M., Chen, C.M., Quinn, N.P., McAuley, J., Rothwell, J.C., 1996. Strength in parkinsonÕs disease: relationship to rate of force generation and clinical status. Ann. Neurol. 39, 79–88. Crenna, P., Friggo, C., Giovannini, P., Piccolo, I., 1990. The initiation of gait in parkinsonÕs disease. In: Berardelli, A. (Ed.), Motor Disturbances II. Academic Press, Orlando, pp. 161–173. Gantchev, N., Viallet, F., Aurenty, R., Massion, J., 1996. Impairment of posturo-kinetic co-ordination during initiation of forward oriented stepping movements in parkinsonian patients. Electroencephalogr. Clin. Neurophysiol. 101, 110–120. Goulart, F.R., Valls-Sole, J., 1999. Patterned electromyographic activity in the sit-to-stand movement. Clin. Neurophysiol. 110, 1634–1640.
117
Halliday, S.E., Winter, D.A., Frank, J., Patla, A., Prince, F., 1998. The initiation of gait in young, elderly, and parkinsonÕs disease subjects. Gait Posture 8, 8–14. Hirschfield, H., Thorsteinsdottir, M., Olsson, E., 1999. Coordinated ground forces exerted by buttocks and feet are adequately programmed for weight transfer during sit-to-stand. J. Neurophysiol. 82, 3021–3029. Hobson, P., 1999. Measuring the impact of parkinsonÕs disease with the parkinsonÕs disease quality of life questionnaire. Age Ageing 28, 341–346. Ikeda, E.R., Schenkman, M.L., Riley, P.O., Lin, S., 1991. Influence on dynamics of rising from a chair. Phys. Ther. 71, 473–481. Kelly, D.L., Dainis, A., Wood, G.K., 1976. Mechanics and muscular dynamics of rising from a seated position. In: Komi, P.V. (Ed.), International Series on Biomechanics, Biomechanics V-B. University Park Press, Baltimore, MD, pp. 127–134. Khemlani, M.M., Carr, J.H., Crosbie, W.J., 1999. Muscle synergies and joint linkages in sit-to-stand under two initial foot positions. Clin. Biomech. 14, 236–246. Mak, M.K., Hui-Chan, C.W., 2002. Switching of movement direction is central to parkinsonian bradykinesia in sit-to-stand. Movement Disord. 17, 1188–1195. Mak, M.K., Levin, O., Mizrahi, J., Hui-Chan, C.W., 2003. Joint torques during sit-to-stand in healthy subjects and people with parkinsonÕs disease. Clin. Biomech. 18, 197–206. Mano, Y., Sakakibara, T., Takayanagi, T., 1988. Kinesiological analysis of standing-up movement. Excerpta Medica International Congress Series 804, 503–512. Nevitt, M.C., Cummings, S.R., Kidd, S., 1989. Risk factors for recurrent nonsyncopial falls: a prospective study. J. Am. Med. Assoc. 261, 2663–2668. Pai, Y.C., Rogers, M.W., 1991. Speed variation and relevant joint torques during sit-to-stand. Arch. Phys. Med. Rehabilitation. 72, 881–885. Riley, P.O., Schenkman, M.L., Mann, R.W., Hodge, W.A., 1991. Mechanics of a constrained chair rise. J. Biomech. 24, 77–85. Rodosky, M.W., Andriacchi, T.P., Anderson, G.B., 1989. The influence of chair height on lower limb mechanics during rising. J. Orthop. Res. 7, 266–271. Schenkman, M., Berger, R.A., Riley, P.O., Mann, R.W., Hodge, W.A., 1990. Whole-body movements during rising to standing from sitting. Phys. Ther. 70, 638–648. Vander Linden, D.W., Brunt, D., McCulloch, M., 1994. Variant and invariant characteristics of the sit- to-stand task in healthy elderly adults. Arch. Phys. Med. Rehab. 75, 653–660. Yoshida, K., Iwakura, H., Inoue, F., 1983. Motion analysis in the movements of standing up from and sitting down on a chair. Scan. J. Rehab. Med. 15, 133–140.
Changes in distal muscle timing may contribute to slowness during sit to stand in Parkinsons disease Mark Bishop a
a,*
, Denis Brunt b, Neeti Pathare a, Mansoo Ko a, Jill Marjama-Lyons
c
Department of Physical Therapy, University of Florida, P.O. Box 100154, Gainesville, FL 32610-0154, USA b Department of Physical Therapy, East Carolina University, North Carolina, USA c Parkinson Center (PADRECC), Veterans Affairs Hospital, Albuquerque, NM, USA Received 13 November 2003; accepted 4 August 2004
Abstract Objective. To compare patterns of muscle activation in the lower extremity and subsequent forces during sit to stand in persons with Parkinsonism. Background. There is an interruption of the tibialis anterior/soleus interaction during forward oriented movements in some subjects with Parkinsonism, including sit to stand. This task is a major determinant of independence and 44% of those with Parkinsonism report difficulty. Methods. 41 subjects with Parkinsonism were asked to stand up from a bench. Peak acceleration and vertical ground reaction forces, the slopes to these peaks, and the timing of events were measured. Surface electrodes were placed on tibialis anterior and soleus. Results. The slower group produced force at slower rate than the fast group. The slower group spent 64% of the time taken to stand to complete the flexion-momentum phase, and the fast group spent 56%. The slower group had a larger proportion of co-contraction trials than the other groups. Conclusions. Slower subjects took longer to perform the task due to a longer time for seat off. Deficits recruiting tibialis anterior may contribute to the decreased rate of production of the acceleration forces and the longer time required for seat off. Relevance Decreased rate of rise of force is used to identify fallers in the elderly and subjects with stroke. Decreased rates of force production may therefore assist in identifying those with Parkinsonism at risk of falls. Treatment strategies designed to facilitate tibialis anterior activation may improve the functional performance of this task. 2004 Elsevier Ltd. All rights reserved. Keywords: Reciprocal inhibition; EMG
1. Introduction Rising from a sitting to a standing position (STS) is a common skill of daily living and an important measure of physical function (Kelly et al., 1976; Rodosky et al., 1989). During STS the bodyÕs center of mass is shifted *
Corresponding author. E-mail address: [email protected]fl.edu (M. Bishop).
0268-0033/$ - see front matter 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.clinbiomech.2004.08.002
forward and vertical from a relatively large, stable base of support created by contact with the chair and the ground to a much smaller base under the feet (Riley et al., 1991). The central nervous system is challenged to simultaneously control both the whole body movement and equilibrium (Hirschfield et al., 1999). Schenkman et al. (1990) have provided an adequate description of the successive phases of STS. First, the trunk is flexed (flexion-momentum phase) followed by the initiation of
M. Bishop et al. / Clinical Biomechanics 20 (2005) 112–117
vertical momentum as the buttocks are lifted off the chair (momentum transfer phase). The extension phase follows which ends when the hips are in extension and body sway must then be controlled (stabilization phase). Consequently, completing this seemingly simple task becomes a challenge for those with functional limitations. While there have been studies on stroke patients (Brunt et al., 2002; Cheng et al., 1998; Yoshida et al., 1983), research on other patient populations, such as those with ParkinsonÕs disease (PD) has been limited. This is somewhat surprising as 44.2% of persons with PD have difficulty with STS (Mano et al., 1988) and STS transfers appear to be one of the major determinants for independence and quality of life for those with PD (Hobson, 1999). That the risk of falling exists in elderly who have difficulty rising from a chair (Campbell et al., 1989; Nevitt et al., 1989) and impairments in mobility and falls are a characteristic of PD, reinforces the need to further study the STS task in persons with PD. Studies in the elderly (Yoshida et al., 1983) and patients who are stroke survivors (Brunt et al., 2002; Cheng et al., 1998; Yoshida et al., 1983) show that they perform the sit to stand task slowly. Slowness of movement in PD has clearly been demonstrated in gait initiation (Gantchev et al., 1996; Halliday et al., 1998), and upper extremity tasks (Corcos et al., 1996; Ikeda et al., 1991). The investigation of differences in activities of daily living or locomotor skills among groups of patients with PD based on slowness of movement is important for three reasons. First, expected speed of movement may provide a means to evaluate change following therapeutic intervention. Second, understanding what components of a skill contribute to overall slowness of the movement may well guide rehabilitation strategies. The selected strategy and functional status of an individual are closely connected and identification of the former allows for the modification of the latter. Third, understanding the sub-clinical mechanisms of slowness of movement could further guide rehabilitation strategies. We were specifically interested in the interaction of the soleus (SOL) and tibialis anterior (TA) muscles. It is well documented that during the initiation of gait activation of the TA and inhibition of the SOL begins the backward movement of the center of pressure and the initiates forward momentum (Breniere et al., 1987; Brenie`re et al., 1981; Brunt et al., 1991, 1999). Studies have shown a deficit in this pattern in PD patients and thus their gait initiation is slow (Gantchev et al., 1996; Halliday et al., 1998). The same mechanism of TA and SOL interaction is present at the beginning of STS (Goulart and Valls-Sole, 1999; Khemlani et al., 1999). The primary aim of this study was to compare the characteristics of STS in two groups of persons with PD. We speculated that there would be differences in
113
the patterns of muscle activation in the lower extremity when comparing fast and slower moving persons with PD. Specifically, we first hypothesized that there would be an interruption of the normal TA and SOL interaction in slower moving subjects. Second, it was hypothesized that the first phase of STS would be prolonged in those subjects that showed the alteration of the TA and SOL interaction. That is, we expect that the there will be an increase in the proportion of the total time taken to stand spent in the flexion momentum phase or first stage of STS.
2. Methods 2.1. Subjects Forty-one subjects (21 male and 20 female) with PD participated in this study. SubjectÕs ages were between 50 and 79 years (66, SD 8.3). Subjects were within Stages I–III of the Hoehn and Yahr classification and their United Parkinsons disease Rating Scale (UPDRS) Motor part III score ranged from 4 to 58. Subject characteristics within groups are summarized in Table 1. All subjects were able to stand up and walk independently. Subjects were on levodopa medication and were tested approximately 1.5 h following the administration of their medication, the timing of which was determined by the patientÕs physician. All subjects read and signed an informed consent form approved by the University Institutional Review Board. 2.2. Equipment After appropriate skin preparation, surface electrodes were applied to the muscle belly of the TA and to the muscle belly medial to the tendoachilles and distal to the medial gastrocnemius. Placement was confirmed by comparing the myoelectric signal during resisted ankle plantar flexion to that during resisted knee flexion. Each electromyographic (EMG) recording electrode consisted of two silver–silver chloride 1 cm diameter electrodes embedded in an epoxy-mounted preamplifier system (·35) spaced 2 cm apart. A reference electrode was attached to the medial aspect of the tibia. The EMG signals were band-pass filtered, (20 Hz–4 kHz; Table 1 Patient characteristics for Groups A and B
Age (years) Disease duration (years) Hoehn and Yahr UPDRS (III)
Group A
Group B
66.1 4.8 2 21
66.5 7.4 2.5 19
(55–80) (0.5–8) (1–2.5) (13–40)
(53–79) (0.5–14) (1–3.5) (4–36)
Values represent mean (range), or median (range). UPDRS—United Parkinsons Disease Rating Scale.
114
M. Bishop et al. / Clinical Biomechanics 20 (2005) 112–117
Therapeutics Unlimited, Iowa City, Iowa, USA) full wave rectified, and low pass filtered (350 Hz) on-line. Final amplification was 10 K. Two force platforms, (Advanced Mechanical Technology Inc., Watertown, MA, USA) were situated on the floor to measure ground reaction forces. Processed EMG and amplified force platform signals were sampled online at 1000 Hz for 8 s (BIOPAC Systems, Goleta, CA, USA). 2.3. Procedure Seat height was adjusted such that subjectsÕ knees were placed in approximately 90 of flexion. Arms were kept folded across the trunk with the palms of the hands flat against the rib cage. Subjects were instructed to look straight ahead at the light signal and stand, at their selfselected pace, when the light signal came on. Five satisfactory trials were completed. 2.4. Data analysis We have noted previously that scores on the Hoehn and Yahr Scale are not sensitive enough to discriminate between groups during a functional task, such as gait termination (Bishop et al., 2003). Subjects were divided into two groups based upon their time from the onset of movement to peak vertical ground reaction force (Fz; see Fig. 1). The mean time to complete STS was (807.35, SD 223.85 ms). Patients with mean times equal to or less than half a standard deviation below the population mean were placed in Group A (n = 12, 6695.43 ms).
Fx
Those patients with a mean time equal to or greater than half a standard deviation above the population mean were placed in Group B (n = 10, 6919.28 ms) leaving the data from 22 subjects for analysis. Fig. 1 shows the force plate data from a single trial of STS for a patient from Group A. The first vertical line represents movement onset at the first detectable shift in force plate activity. The peak anterior/posterior ground reaction force (Fx) is indicated by the second vertical line and represents the transition between the flexion-momentum and momentum-transfer stages of STS. The momentum-transfer stage ends approximately at peak Fz (third vertical line). These parameters have been described elsewhere (Brunt et al., 2002; Vander Linden et al., 1994). Although there appeared to be some asymmetry observed during experimental trials, no attempt was made to modify the patients preferred strategy during STS. Data were then analyzed from the task dependent limb as determined by peak vertical ground reaction forces generated during the extension phase. Dependent measures of temporal events were the absolute and relative time required to complete the flexion-momentum (phase I) and momentum transfer (phase II) stages of STS. Analysis of variance techniques were used to make comparisons of dependent variables between the two groups. Type I error was maintained at 5%. The dependent measures for the EMG data included the onset of TA with respect to movement onset. Muscle onset was determined as the point at which the EMG signal was two standard deviations above the mean background activity for 30 ms. The mean time of TA onset was considered for each subject. As we were uncertain of the nature of the distribution from which this data was drawn, a distribution-free rank sum test was used to compare the location of the groups. Reciprocal inhibition of the SOL muscle was also noted by visual inspection of the SOL muscle activity during or prior to the flexion momentum phase. Absence of SOL activity was categorized as presence of reciprocal inhibition.
Fz
3. Results Phase I
Phase I I
Fig. 1. Vertical (Fz) and horizontal (Fx) ground reaction forces from a single representative trial of the sit to stand task from a subject in Group A. The circles indicate the peak forces of both Fx and Fz. The first dashed vertical line represents movement onset, peak anterior/ posterior ground reaction force (Fx) is indicated by the second vertical line and represents the transition between the flexion-momentum and momentum-transfer stages of STS. The momentum-transfer stage ends approximately at peak Fz (third vertical line). The short vertical line = 20% body weight, the arrow indicates the direction of movement and 250 ms.
The two groups did not differ significantly in their Hoehn and Yahr and UPDRS scores, age and disease duration. The patient characteristics for both the groups are shown in Table 1. 3.1. Temporal events A summary of the results appears in Table 2. The end of the transfer-momentum stage (phase I + phase II) occurred 1056 ms (SD 254 ms) ms after the onset of movement for Group B and 644 ms (SD 65 ms) for Group A.
M. Bishop et al. / Clinical Biomechanics 20 (2005) 112–117
29.9
0.000
also resulted in a difference between groups that was statistically significant. Phase I took 64% of the total time for the slow group and 56% of the total time for the fast group (P < 0.001).
107.9
0.000
3.2. Muscle activity
1.5
0.230
0.6
0.446
11.3
0.003
Table 2 Mean (1 SEM) each of the dependent variables
Time to sit to stand (ms) Phase I (ms) Phase II (ms) Peak Fz (% BW) Slope Fz (% BWs 1) Peak Fx (% BW) Slope Fx (% BWs 1)
Group A
Group B
1055.87 (80.32) 663.41 (20.41) 392.45 (75.94) 37.43 (1.94) 137.71 (20.01) 9.66 (1.01) 15.95 (2.82)
643.53 (17.37) 341.88 (22.52) 301.65 (22.74) 39.52 (1.84) 218.06 (14.15) 13.04 (1.01) 40.76 (3.91)
115
F
P-value
5.43 24.5
0.030 0.000
Fz—vertical ground reaction force, Fx—anterior posterior ground reaction force.
For phase I alone, Group B took 663 ms (SD 20 ms) to complete the phase and Group A 341 ms (SD 23 ms). To determine if those in the slow group were slower across all phases of the task, or one phase in isolation, the timing of phase I was considered relative to the total time taken to complete both phases. This comparison
The onset of TA with respect to movement time was categorized into three patterns. These patterns were operationally defined for this study and single trial examples of these patterns of EMG activity are shown in Fig. 2. In the first pattern (Fig. 2A), the soleus is inhibited and TA is clearly active before the onset of phase II and the increase in Fz. Second, TA onset occurred after movement onset (Fig. 2B) and third, there was tonic activity of TA (Fig. 2C). The first pattern occurred in 91% of the trials for subjects in Group A and 70% of Group B. The second pattern occurred in 9% of the trials for subjects in Group A and 10% of the trials subjects in Group B. The third pattern occurred in none of the subjects in Group A and in 20% of the trials for Group B. When TA timing was considered as continuous data, a significant difference was noted between groups (Mann–Whitney U = 21, P = 0.037). TA onset occurred
Fig. 2. (A) Vertical ground reaction forces and EMG data depicting EMG Pattern 1. Note the TA onset with movement onset and the inhibition of the soleus. (B) Vertical ground reaction forces and EMG data depicting EMG Pattern 2. Note the late TA onset. (C) Vertical ground reaction forces and EMG data depicting EMG Pattern 3. Note the tonic TA activity. (D) Alternating bursts of TA and SOL activity. The dotted vertical line indicates movement onset. Solid vertical line indicates peak Fx. The arrow indicates the direction of travel and 250 ms. The short vertical line = 20% body weight and 0.10 mV.
116
M. Bishop et al. / Clinical Biomechanics 20 (2005) 112–117
more often prior to movement onset for Group A (median 67 ms, interquartile range (IQR) 60 ms), and after movement onset for Group B (median 40 ms, IQR 300 ms). Reciprocal inhibition of SOL was noted in all the subjects in the fast group and all but one subject in the slow group. However, this inhibition did not occur at movement onset as expected (Brunt et al., 2002, 1991, 1999, 2000) if the TA did not come on until after movement onset. In addition, those subjects that demonstrated tonic TA activity had multiple trials in which co-contraction occurred between the TA and SOL. This phenomenon was observed in about 30% of the trials in which tonic TA activity occurred.
4. Discussion The average time taken to complete the STS movement for all subjects with PD in our study was 807.35 (SD 223.85) ms. This is consistent with other work examining STS in those with PD (Mak and Hui-Chan, 2002). By comparison, in a previous study in our lab, healthy older adults (average age 66 years, SD 5.6 years) took an average of 798.8 (SD 166.4) ms to complete both phases during STS at their self-selected speed (Vander Linden et al., 1994). For the current investigation, we grouped subjects related to the speed with which they performed the movement. Group B took 1056 ms and Group A 644 ms to complete both phases I and II. For phase I alone, Group B took 663 ms (SD 20 ms) to complete the phase and Group A 341 ms (SD 23 ms). Mak and Hui-Chan (2002) report that the time to seat off is prolonged in absolute terms when comparing those with PD to able-bodied subjects. However, we previously found that healthy older adults took 522.5 ms (SD 704 ms) to complete phase I of STS (Vander Linden et al., 1994) thus, subjects in Group A in our current study completed STS more rapidly than healthy older adults. We speculate that the group of subjects with PD who were fast movers represents part of the population of persons with PD in whom hypokinesia is not clinically present (sub-clinical) but other clinical manifestations of PD maybe. For example, they may have had tremor or tone but not demonstrable slowness of movement on other clinical assessment batteries. We believe that this is more likely the case rather than the subjects having other dyskinesias. Deficits in TA recruitment patterns (onset after movement onset, or tonic activity) were more prevalent in the slower group of subjects (Fig. 2). In addition, trials occurred showing co-contraction between soleus and tibialis anterior. Both these events would decrease the net dorsiflexion torque at the ankle. Mak and Hui-Chan (2002) indicated that slowness in STS might be attrib-
uted to small ankle dorsiflexion torques produced. This was confirmed by a more recent study by Mak and colleagues in which net peak dorsiflexion torques were also lower in those with PD than able-bodied subjects (Mak et al., 2003). However, Pai and Rogers (1991) indicate that when healthy subjects modulated the speed at which they perform STS, that is, move as slowly as possible, dorsifexion torque at the ankle decreased. Therefore, it is difficult to determine whether the decreased dorsiflexion torques cause slower motion or if the torques are smaller because the movement is slower. Similarly, we are unable to say whether delayed onset of TA was the result of the slowness of movement, or the cause thereof. Based on our current findings it would seem that ankle activation strategies alone are not sufficient to account for differences in the time taken to perform STS. Nonetheless, 30% of the subjects in the slower moving group did not exhibit the expected pattern of TA activation. Gait initiation is another task in which difficulty coordinating the TA and SOL interaction presents limitations to those with PD (Burleigh-Jacobs et al., 1997; Crenna et al., 1990). In addition to a decrease in the ability to inhibit SOL, alternating bursts of TA and SOL have been identified in those with PD during gait initiation (Crenna et al., 1990) and other ballistic upper extremity motions (Berardelli et al., 1986). This pattern of multiple short bursts was also seen during STS in our current study and is shown in Fig. 2D. The alternating bursts of muscle activity occur after the signal to stand and prior to the initiation of movement. We speculate that this represents an impaired ability to generate enough muscle force with the initial activation of TA and subsequent bursts are required to generate the required movement pattern.
5. Conclusion Hypokinesia is related to decreased rates of force in upper extremity (Corcos et al., 1996). It would appear that this is likewise the case in the STS task. Those slow moving persons with PD, generated acceleration forces and vertical forces at slower rates. Decreased rate of rise of force is used to identify fallers in the elderly and subjects with stroke. Decreased rates of force production may assist in identifying those at risk of falls amongst those persons with PD and may imply greater functional impairment in performance of the STS than is indicated by traditional systems of rating impairment. Additionally, we speculate that improvement of TA recruitment during rehabilitation may facilitate change in rates of force production at the ankle and result in improvement in transitional tasks such as sit-to-stand.
M. Bishop et al. / Clinical Biomechanics 20 (2005) 112–117
References Berardelli, A., Dick, J.P., Rothwell, J.C., Day, B.L., Marsden, C.D., 1986. Scaling the size of the first agonist EMG burst during rapid wrist movements in patients with ParkinsonÕs disease. J. Neurol. Neurosurg. Psychiat. 49, 1273–1279. Bishop, M.D., Brunt, D., Fiolkowski, P., Pathare, N., Ko, M., Marjama-Lyons, J., 2003. Gait termination in parkinsonism: a review. J. Korean Acad. Phys. Therap. Assoc. 10, 43–60. Brenie`re, Y., Do, M.C., Sanchez, J., 1981. A biomechanical study of the gait initiation process. J. Biophys. Med. Nucl. 5, 197–205. Brenie`re, Y., Do, M.C., Bousset, S., 1987. Are dynamic phenomena prior to stepping essential to walking?. J. Mot. Behav. 19, 62–76. Brunt, D., Lafferty, M.J., Mckeon, A., 1991. Invariant characteristics of gait initiation. Am. J. Phys. Med. Rehab. 70, 206–212. Brunt, D., Liu, S.M., Trimble, M.H., Bauer, J., Short, M., 1999. Principles underlying the organization of movement initiation from quiet stance. Gait Posture 10, 121–128. Brunt, D., Short, M., Trimble, M., Liu, S.M., 2000. Control strategies for initiation of human gait are influenced by accuracy constraints. Neurosci. Lett. 285, 228–230. Brunt, D., Greenberg, B., Wankadia, S., Trimble, M.H., Shechtman, O., 2002. The effect of foot placement on sit to stand in healthy young subjects and patients with hemiplegia. Arch. Phys. Med. Rehab. 83, 924–929. Burleigh-Jacobs, A., Horak, F.B., Nutt, J.G., Obeso, J.A., 1997. Step initiation in parkinsonÕs disease: influence of levodopa and external sensory triggers. Movement Disord. 12, 206–215. Campbell, A.J., Borrie, M., Speras, G.F., 1989. Risk factors for falls in a community based prospective study of people 70 years and over. J. Gerontol. Med. Sci. 44 (M), 112–117. Cheng, P.T., Liaw, M.Y., Wong, M.K., Tang, F.T., Lee, M.Y., Lin, P.S., 1998. The sit-to-stand movement in stroke patients and its correlation with falling. Arch. Phys. Med. Rehab. 79, 1043– 1046. Corcos, D.M., Chen, C.M., Quinn, N.P., McAuley, J., Rothwell, J.C., 1996. Strength in parkinsonÕs disease: relationship to rate of force generation and clinical status. Ann. Neurol. 39, 79–88. Crenna, P., Friggo, C., Giovannini, P., Piccolo, I., 1990. The initiation of gait in parkinsonÕs disease. In: Berardelli, A. (Ed.), Motor Disturbances II. Academic Press, Orlando, pp. 161–173. Gantchev, N., Viallet, F., Aurenty, R., Massion, J., 1996. Impairment of posturo-kinetic co-ordination during initiation of forward oriented stepping movements in parkinsonian patients. Electroencephalogr. Clin. Neurophysiol. 101, 110–120. Goulart, F.R., Valls-Sole, J., 1999. Patterned electromyographic activity in the sit-to-stand movement. Clin. Neurophysiol. 110, 1634–1640.
117
Halliday, S.E., Winter, D.A., Frank, J., Patla, A., Prince, F., 1998. The initiation of gait in young, elderly, and parkinsonÕs disease subjects. Gait Posture 8, 8–14. Hirschfield, H., Thorsteinsdottir, M., Olsson, E., 1999. Coordinated ground forces exerted by buttocks and feet are adequately programmed for weight transfer during sit-to-stand. J. Neurophysiol. 82, 3021–3029. Hobson, P., 1999. Measuring the impact of parkinsonÕs disease with the parkinsonÕs disease quality of life questionnaire. Age Ageing 28, 341–346. Ikeda, E.R., Schenkman, M.L., Riley, P.O., Lin, S., 1991. Influence on dynamics of rising from a chair. Phys. Ther. 71, 473–481. Kelly, D.L., Dainis, A., Wood, G.K., 1976. Mechanics and muscular dynamics of rising from a seated position. In: Komi, P.V. (Ed.), International Series on Biomechanics, Biomechanics V-B. University Park Press, Baltimore, MD, pp. 127–134. Khemlani, M.M., Carr, J.H., Crosbie, W.J., 1999. Muscle synergies and joint linkages in sit-to-stand under two initial foot positions. Clin. Biomech. 14, 236–246. Mak, M.K., Hui-Chan, C.W., 2002. Switching of movement direction is central to parkinsonian bradykinesia in sit-to-stand. Movement Disord. 17, 1188–1195. Mak, M.K., Levin, O., Mizrahi, J., Hui-Chan, C.W., 2003. Joint torques during sit-to-stand in healthy subjects and people with parkinsonÕs disease. Clin. Biomech. 18, 197–206. Mano, Y., Sakakibara, T., Takayanagi, T., 1988. Kinesiological analysis of standing-up movement. Excerpta Medica International Congress Series 804, 503–512. Nevitt, M.C., Cummings, S.R., Kidd, S., 1989. Risk factors for recurrent nonsyncopial falls: a prospective study. J. Am. Med. Assoc. 261, 2663–2668. Pai, Y.C., Rogers, M.W., 1991. Speed variation and relevant joint torques during sit-to-stand. Arch. Phys. Med. Rehabilitation. 72, 881–885. Riley, P.O., Schenkman, M.L., Mann, R.W., Hodge, W.A., 1991. Mechanics of a constrained chair rise. J. Biomech. 24, 77–85. Rodosky, M.W., Andriacchi, T.P., Anderson, G.B., 1989. The influence of chair height on lower limb mechanics during rising. J. Orthop. Res. 7, 266–271. Schenkman, M., Berger, R.A., Riley, P.O., Mann, R.W., Hodge, W.A., 1990. Whole-body movements during rising to standing from sitting. Phys. Ther. 70, 638–648. Vander Linden, D.W., Brunt, D., McCulloch, M., 1994. Variant and invariant characteristics of the sit- to-stand task in healthy elderly adults. Arch. Phys. Med. Rehab. 75, 653–660. Yoshida, K., Iwakura, H., Inoue, F., 1983. Motion analysis in the movements of standing up from and sitting down on a chair. Scan. J. Rehab. Med. 15, 133–140.