Copyright Blackwell Munksgaard 2003
Acta Neurol Scand 2004: 109: 416–424 DOI: 10.1046/j.1600-0404.2003.00243.x Printed in UK. All rights reserved
ACTA NEUROLOGICA SCANDINAVICA
Load force during manual transport in Parkinson’s disease Guo X, Hosseini N, Hejdukova´ B, Olsson T, Johnels B, Steg G. Load force during manual transport in Parkinson’s disease. Acta Neurol Scand 2004: 109: 416–424. Blackwell Munksgaard 2003.
X. Guo1, N. Hosseini1,2, B. Hejdukov1,3, T. Olsson2, B. Johnels1, G. Steg1 1
Objectives – To search for a physiological method for the measurement of upper extremity dexterity during activities of daily life in Parkinson’s disease (PD). Materials and methods – We examined load force output during manual transport in seven patients with PD and 10 healthy controls. PD patients were measured in both the nonmedicated and medicated states. The test movement included two continuous sub-movements: an upward-forward transport of an object from the table to the stand, and a downward-backward transport of the object from the stand to the table. Hand movements were recorded using an optoelectronic camera, and load force was measured using a force sensor installed in the test object. Results – Compared with the controls, PD patients had a different pattern of load force output characterized by slower force development and release, lower peak force, and less dynamic force generation during movement. After medication, the speed of force development and the level of peak force increased in the patients. Conclusions – These findings suggest that PD impairs the production of preprogrammed movements. The movements observed in the PD patients may result from compensatory strategies relying more on feedback mechanisms.
In clinical practice the evaluation of the symptoms of Parkinson’s disease (PD) including tremor, bradykinesia and rigidity is usually based on subjective and qualitative rating scales, such as the United Parkinson’s Disease Rating Scale and the Hoehn and Yahr Stage Score. These scales classify the symptoms roughly into categories, which causes difficulties in assessing the progress of disease and the efficacy of treatment (1). Performance tests, based on the measurement of body positions and force during ongoing movement, are useful additive tools to these rating scales, because they can provide objective and precise indices for assessment, such as speed, acceleration, and force tremor frequency. We have previously developed the Postural–Locomotor– Manual (PLM) test to study the disturbance of postural control, locomotion and arm reaching, as well as the integration of individual movement into a purposeful and smooth body movement (2). Previous studies have shown that the PLM test gives useful information on documenting clinical 416
Department of Neurology, Institute of Clinical Neuroscience, Sahlgrenska University Hospital, G teborg, Sweden; 2Department of Signals and Systems, Chalmers University of Technology, G teborg, Sweden; 3Department of Neurology, University Hospital Bulovka, Charles University, Prague, Czech Republic
Key words: load force; manual transport; Parkinson's disease Xinxin Guo MD, PhD, Department of Neurology, Institute of Clinical Neuroscience, Sahlgrenska University Hospital, 413 45 G teborg, Sweden Tel.: 46-31-3421359 Fax: 46-31-3422467 e-mail:
[email protected] Accepted for publication October 3, 2003
symptom profiles and on evaluating pharmacotherapeutic efficacy in PD patients (3, 4). Impaired manual transport is one of the main causes of disability in activities of daily living in PD. Our group has, therefore, been working on a new performance test, the Manual Transport (MANTRA) test (5–7). Force and movement were recorded in a natural test movement consisting of an upward-forward transport followed by a downward-backward transport of a test object. Previous studies have revealed that PD patients suffered from difficulties in initiating, developing, regulating, maintaining and releasing forces in different motor tasks (8–15). Specifically, patients showed slower force onset (8, 11, 14), slower force development (8, 9, 15), more irregular force-time pattern (10), more force oscillations (14), larger force-time integral (9), and slower force release (11–13) than healthy subjects. Deficient force control in PD was also revealed by abnormal electromyographic (EMG) patterns. For example, patients were unable to appropriately scale the size
Manual transport in Parkinson’s disease of the first agonist EMG burst to produce the propulsive force for movement initiation (16). One study found an excessive number of late bursts of EMG activities after the termination of voluntary muscle contraction, the duration of which correlated with bradykinesia and rigidity score (17). The present study aimed at examining load force control during manual transport in PD patients. Load force is used against the weight of the object and accelerates the object during dynamic transportation. Isometric load force appears in the beginning of the movement before the object lifts up, and at the end of the movement when the object is released. Force production is a truer representation of the activity in the muscle and nervous systems than the resulting movement that is more influenced by biomechanical factors. Force analysis provides information not only on dynamic movements, but also on non-dynamic movements (isometric force production). Force analysis may help us to explore the pathophysiological mechanisms underlying PD symptoms, assess therapeutic effects, and evaluate the severity and progress of disease.
Subjects and methods Subjects
Seven subjects with diagnosed PD (mean age: 63 years) and 10 healthy volunteers (all females, age range: 46–64 years, mean age: 51 years) participated in the present study. The PD patients were examined in both non-medicated (OFF) and medicated (ON) states, always starting with the OFF state. The OFF state was defined as more than 12 h after withdrawing anti-Parkinsonian medication. The ON state was defined as more than 1.5 h after administration of regular medication. Clinical characteristics of patients are presented in Table 1. This study was approved by the Ethics Committee for Medical Research of the Go¨teborg University. All subjects gave their informed consent to the study.
Manual transport test
The subject sat with the forearm comfortably resting on a table, and with the hand on a pressure-sensitive pad. The test object was placed 10 cm in front of the resting hand, and a stand was located 40 cm in front of the test object and 40 cm above the table. The test movement included two sub-movements: an upward-forward transport of the object from the table to the stand; and a downward-backward transport of the object from the stand to the table (Fig. 1). During the upward-forward transport, the subject picked up the object using the precision grip at the tips of the thumb and index finger, and transported it to the stand. Once the object was placed on the stand, the hand returned to the resting position. During the downward-backward transport, the subject picked up the object from the stand, and transported it back to the table. Afterwards the hand returned to the resting position. The subjects were instructed to perform the upward-forward and the downward-backward transport in alternation and as fast as possible. All movements performed for a trial period of 30 s were recorded after which the subjects were instructed to terminate the test. Each subject performed two such trials and the second one was selected for further analysis. The task was performed with the dominant hand in healthy subjects, and with the more disabled hand in PD
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Table 1 The clinical characteristics of Parkinson's disease patients 40 cm
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LD, L-dopa; B, bromocriptine; T, tolcapone; P, pramipexol; S, selegiline; R, ropinirole.
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Figure 1. Manual Transport test. (A) Upward-forward transport of the object from the table to the stand; (B) downwardbackward transport of the object from the stand to the table. The arrows indicate direction of movement. The solid lines indicate the movement phases used for further analysis in the present study.
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Guo et al. patients. Detailed information about this test has been reported in our previous studies (5–7).
Grip force transducer
Data acquisition and movement analysis
An infrared light reflective marker was placed on the test object. The movements of the marker were recorded by an optoelectronic camera (Macreflex; Qualisys AB, Go¨teborg, Sweden) and a tracking program yielding a measurement frequency of 50 Hz that was re-sampled to match the sampling frequency of force measurement. A linear interpolation method was used. Data was not filtered. The test object used is a cubic box (75 mm · 75 mm · 75 mm) weighing 640 g (Fig. 2). The load force was measured by a force sensor installed inside the test object. Grip force during transportation was also measured, but was not studied in the present study. The sampling frequency of the force measurement was 400 Hz. The signals from the camera and the force sensors were analyzed by computer software. The upward-forward (U) transport was divided into five phases: U-loading, U-accelerating, U-decelerating, U-retarding and U-replacing (Fig. 3). The U-loading phase was defined as the time period when the load force increased from zero to the weight of test object. The U-accelerating
Load force transducer Exchangeable weight
Figure 2. The test object.
phase started when the load force exceeded the weight of the object, and ended when the object reached the maximal upward vertical velocity. The U-decelerating phase started at the maximal upward vertical velocity, and ended at the maximum downward vertical velocity of the object. The U-retarding phase started at the maximum downward vertical velocity of the object, and ended with the load force equal to the weight of the object. The U-replacing phase was the time period when the load force decreased from the object weight to zero. The downward-backward (D) transport was divided into five phases: D-loading, D-lifting,
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Manual transport in Parkinson’s disease
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Figure 4. Typical curves of load force, object vertical position and object vertical velocity in downward-backward transport in a healthy subject. D1, loading phase; D2, lifting phase; D3, accelerating phase; D4, decelerating phase; D5, replacing phase.
D-accelerating, D-decelerating, and D-replacing (Fig. 4). The D-loading phase started when the load force began to increase, and ended when the object was lifted off the stand. The D-lifting phase started when the object was lifted off the stand, and ended when the object reached the maximal upward vertical velocity. The D-accelerating phase started at the maximum upward vertical velocity of the object, and ended at the maximum downward vertical velocity. The D-decelerating phase started at the maximum downward vertical velocity of the object, and ended with the load force equal to the weight of the object. The D-replacing phase was the time period when the load force decreased from the weight of the object to zero. Statistics
Upward-forward transport and downward-backward transport were analyzed separately. As the load force was continuously changing during transport, the mean value in each phase was calculated. The Mann–Whitney test was used to examine the difference of load force between healthy subjects and PD patients in the OFF state. The Wilcoxon signed rank test was employed to study the differences of load force between OFF and ON state in patients. Two-tailed tests of significance were used in all
calculations; P < 0.05 was considered statistically significant.
Results Upward-forward transport
Fig. 5 shows the pattern of load force output during the upward-forward transport in healthy controls, PD patients in ON state, and PD patients in OFF state. Healthy controls displayed a peak–valley– peak pattern of force output. The load force reached a peak value immediately at the beginning of transport. It decreased during the period of movement, and increased again when the object approached the stand. In contrast, PD patients in the OFF state showed a more constant load force during the whole period of transport with many small oscillations. For PD patients in ON state, one patient had a constant pattern of load force, and the other six patients had a peak–valley–peak pattern although not as marked as in the controls. PD OFF patients took longer time to develop isometric load force in the U-loading phase, as well as to release isometric load force in the U-replacing phase than controls (Table 2). The peak force in the U-accelerating phase was on average lower in PD patients than in controls, and it was also delayed. 419
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Figure 5. Load force curves for all analyzed movements during upward-forward transport in healthy subjects (A), and PD patients in the ON state (B) and in the OFF state (C).
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Manual transport in Parkinson’s disease Table 2 Load force development and release during upward-forward (U) transport* in controls (n ¼ 10) and PD patients (n ¼ 7) in mediation ON and OFF state P-values Variables
Controls
U-loading phase (s) Peak load force in U-accelerating phase (N) Time to peak load force in U-accelerating phase (s) U-replacing phase (s)
0.08 11.28 0.20 0.07
0.02 4.47 0.03 0.02
PD ON 0.09 10.69 0.23 0.11
0.03 3.29 0.05 0.04
PD OFF
PD OFF vs controls
PD OFF vs PD ON
0.012 0.011 0.001 0.016
0.027 0.018 0.018 0.553
0.15 6.89 0.74 0.13
0.05 0.88 0.46 0.05
Data are presented as mean SD. * Force development is described as the time period when load force increased from zero to object weight (U-loading phase), as well as the time period when load force increased from zero to the peak value in U-accelerating phase. Force release is described as the time period when the load force decreased from object weight to zero (U-replacing phase).
Table 3 Mean load force in different phases during upward-forward (U) transport in controls (n ¼ 10) and PD patients (n ¼ 7) in medication ON and OFF state P-values Phase U-loading (N) U-accelerating (N) U-decelerating (N) U-retarding (N) U-replacing (N)
Controls 1.57 8.90 3.04 3.69 0.96
0.17 2.97 0.73 1.25 0.26
PD ON 1.69 8.19 4.77 5.48 1.43
0.11 1.79 1.47 0.80 0.13
PD OFF
PD OFF vs controls
PD OFF vs PD ON
0.006 0.025 0.001 0.015 0.001
0.063 0.018 0.176 0.876 0.028
1.88 6.05 5.51 5.37 1.67
0.22 0.81 0.97 0.77 0.27
Data are presented as mean SD.
Compared with the OFF state, PD patients in ON state showed a faster development of force in both the U-loading and the U-accelerating phases (Table 2). The mean load force during different phases in the upward-forward transport is presented in Table 3. Compared with healthy subjects, PD patients in the OFF state showed higher load force in the phases of U-loading, U-decelerating, U-retarding, and U-replacing. However, the patients showed lower load force than the controls in the U-accelerating phase. Furthermore, PD patients increased the mean load force during the phase of U-accelerating after medication. Downward-backward transport
Fig. 6 shows the pattern of load force output during the downward-backward transport in healthy controls and patients. For healthy controls, the load force decreased after the object was lifted off the stand, followed by a gradual increase as the object approached the table. For PD patients in the OFF state, the load force was at a high level during the whole period of transport, lacking the dynamic pattern observed in healthy controls. For the patients in the ON state, load force was also kept at a high level. The load force generation during movement was more varied in the ON state than in the OFF state.
Table 4 shows the mean load force of different phases in healthy subjects and PD patients in the OFF and ON state. PD patients at OFF state employed higher load force during the D-accelerating phase than controls. The load force was not statistically different before and after medication in PD patients. Discussion
Using an optoelectronic technique and force measurements, we assessed load force output during a transport task in seven PD patients and ten healthy controls. Compared with the controls, PD patients had a different pattern of load force output characterized by slower force development and release, lower peak force, and less dynamic force generation during movement. After medication, the speed of force development and the level of peak force increased in the patients. Slower force development and release
Our results confirm previous findings that PD patients have an impaired ability of rapid force development (8, 9, 15), and release (11–13). In the execution of upward-forward transport, PD patients showed a slower development of isometric load force in the U-loading phase, and a slower release of isometric load force in the U-retarding 421
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Figure 6. Load force curves for all analyzed movements during downward-backward transport in healthy subjects (A), and PD patients in the ON state (B) and in the OFF state (C).
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Manual transport in Parkinson’s disease Table 4 Mean load force in different phases during downward-backward (D) transport in controls (n ¼ 10) and PD patients (n ¼ 7) in medication ON and OFF state P-values Phase D-loading (N) D-lifting (N) D-accelerating (N) D-decelerating (N) D-replacing (N)
Controls 1.96 3.42 2.75 5.54 1.14
0.82 1.07 0.94 1.59 0.54
PD ON 2.02 4.38 4.86 7.57 2.27
0.59 1.03 1.15 3.02 0.99
PD OFF
PD OFF vs controls
PD OFF vs PD ON
0.143 0.558 0.002 0.283 0.050
0.053 0.310 0.735 0.237 0.612
1.42 3.71 4.83 5.91 2.52
0.46 1.25 0.94 0.75 1.48
Data are presented as mean SD.
phase compared to controls. Moreover, the peak load force in the U-accelerating phase was about two-third of controls for PD patients. However, patients took nearly a threefold longer time to reach the peak value than controls. Deficient force development is a reason for the clinical manifestation of bradykinesia, i.e. slowness in execution of purposive movement. The underlying mechanism of impaired fast force development in PD has been suggested to be a failure of motor planning and inappropriate scaling of muscle force to the movement parameters (18, 19). Less dynamic force generation
In contrast to a dynamic force output during movement in healthy controls, PD patients displayed a more constant elevation of load force in both the upward-forward transport and the downward-backward transport. On the one hand, the patients showed less force than the controls in the U-accelerating phase during upward-forward transport when load force was needed to overcome the object weight and accelerate the object. On the other hand, the patients showed more force than the controls in the U-decelerating phase during upward transport and the D-accelerating phase during downward transport, when the object was driven by its weight rather than by the load force. It should be noted that besides lacking a dynamically changed force pattern, patients showed an increased amount of small force oscillations compared with controls. A previous study reported action tremor during object manipulation in PD (20). The differences of load force generation between PD OFF patients and healthy controls are more remarkable in the upward-forward transportation than in the downward-backward transportation. This is mainly because of a higher demand of load force generation in the upwardforward transportation than in the downwardbackward transportation. Less dynamic force output and slow movement indicate an impaired ability to produce ballistic
movements in PD. To perform a ballistic movement, one needs to plan the whole movement in advance and release it as a whole. Impaired motor programming in PD has been confirmed by studying reaction time and EMG activities recorded before the onset of movement (16, 18, 19). Moreover, recent studies have consistently reported that the pre-supplementary motor cortex (pre-SMA), which is related to selection of and preparation for the specific movement required (21), is underactivated in PD patients (18, 22). It has been suggested that the impaired preprogrammed ballistic movement is compensated by corrective movements based on feedback mechanisms (8, 23). Constant force output, slow force generation and release, and long movement time might be expressions of a strategy adopted by the PD patients to compensate for impairments of preprogrammed ballistic movement. These compensatory strategies enable the patients to function sub-optimally, but relatively reliably, rather than risking a total failure. Besides impaired motor plan, increased stretch reflexes and abnormal coactivation of agonist-antagonist muscle groups in PD (24) are also possible explanations to our findings. The less dynamic force generation in PD was similar to the pattern observed in healthy subjects during slow movement in a previous study (6). It suggests that bradykinesia is related to the more constant force output in PD. Manual transport is a well-developed act trained daily since childhood. Healthy people perform this act in an energetically economic way, i.e. a largely preprogrammed movement with a shorter movement time and relatively less force utilization. In contrast, the failure of a preprogrammed ballistic movement as well as the consequential corrective movements may cause higher energy expenditure in PD. Medication effects
After medication, PD patients increased the speed of force development and the level of peak force in 423
Guo et al. the upward-forward transport, which is in line with previous findings in a reach-to-grasp movement (25). Moreover, the load force generation during movement was somewhat more varied in the ON state than in the OFF state in both upwardforward transport and downward-backward transport. These results confirm that medication improves movement in PD. However, medication did not revert PD impairment to normal. The patients in medication ON state still kept a higher level of mean load force than the controls in downward-backward transport. The pattern of force production during movement in patients in the ON state was less varied than controls. Such deficits may result from the inability of pharmacological treatment to restore the nigro-striatal circuitry or that the movement planning is hampered by dysfunction in other systems, such as loss of cortico-cortical neurons in the presupplementary motor areas (26). In summary, in spite of a comparably small patient sample, this study showed that PD patients had a slow and constant pattern of load force output during a manual transport task, in contrast to a fast and dynamic pattern in the healthy controls. These findings suggest that PD impairs the production of pre-programmed ballistic movement. The present study just like our earlier studies (5–7), suggests that the Manual Transport test is a useful tool to detect and quantify abnormalities in PD, and to help seek underlying pathophysiological mechanisms. Acknowledgements This study was supported by the Foundation for Neurological Movement Analysis Research, the Parkinsonfonden and the Medical Faculty of Go¨teborg University. We thank Stefan Piechnik for his suggestions on our work.
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