Center of Pressure Measures during Standing Tasks in Minimally Impaired Persons with Multiple Sclerosis

Abstract

Background and Purpose 

Balance impairments are common in persons with multiple sclerosis (MS), but clinical balance tests may not detect subtle deficits in adults with MS who are not yet experiencing functional limitations or disability. The purpose of this study was to determine if center of pressure (COP) displacement during standing tasks could be a useful performance-based evaluative measure for adults with MS who have minimal or no balance deficits on clinical examination using the Berg Balance Scale (BBS).

Subjects and Methods 

Twenty-one adults with MS were compared with 21 age- and gender-matched healthy adults. Subjects with MS were tested with the BBS, Mini-mental State Exam, Expanded Disability Status Scale (EDSS), and Multiple Sclerosis Functional Composite (MSFC). They also performed voluntary leaning and reaching movements while kinematic and kinetic data were collected. Control subjects performed the same tasks with the exception of the EDSS and MSFC.

Results 

COP displacement during reaching and leaning was less in adults with MS when compared to control subjects. There were no differences in anthropometric, kinematic, or foot position variables that could account for this difference. Furthermore, there was no difference between groups when COP displacement during reaching was expressed as a percentage of the maximum COP displacement during leaning.

Discussion and Conclusion 

COP measures show clear differences when comparing healthy adults with minimally impaired adults with MS. The lack of between-group differences when COP displacement during reaching was expressed as a percentage of the maximum COP displacement during leaning suggests that the subjects with MS adopt a reaching strategy that allows them to stay within their reduced limits of stability. COP measures during standing tasks appear well-suited to quantifying changes in postural control over time or in response to intervention for minimally impaired persons with MS.

INTRODUCTION

Multiple sclerosis (MS) is a chronic neurological disease characterized by demyelination and inflammation of the central nervous system (CNS).^1–4 The often progressive nature and variable sites of CNS involvement lead to varied presentations of neurological dysfunction.^1–3 People with MS often experience difficulty with mobility, extremity function, somatosensation, vestibular function, vision, cognition, and bowel and bladder control.^1–3 Balance is the result of complex interactions between musculoskeletal and neuromuscular systems, including sensory, motor, and integrative compo-nents.^{5, 6} Because these components are frequently affected by MS, many persons with MS have balance deficits.^{2, 3, 7–11}

One objective of rehabilitative interventions for persons with MS is to address balance impairment.^12–14 Clinically based tests such as the Berg Balance Scale (BBS), Tinetti Performance Oriented Mobility Assessment, and Functional Reach test, among others, have been used to test balance impairment and functional mobility in persons with MS.^{9, 11, 12, 15, 16} These measures indicate whether or not an individual can perform a given task and can identify individuals at risk for falls. However, they may not be sensitive to minimal impairments of balance in those persons not yet experiencing functional limitations or disability. An assessment of balance that could identify subtle impairments before they lead to functional decline could promote earlier intervention and possibly prevent or delay functional limitation and disability.

Laboratory measures offer the potential to identify subtle deficits in postural control that may not be otherwise apparent based on clinical tests.¹⁷ Force platforms are one laboratory assessment tool that have been used to assess postural control in individuals with MS during quiet stance conditions^{7–10, 18} or in dynamic conditions, namely in response to external perturbations such as support surface movements.^{8, 10, 19} In individuals with MS who demonstrate minimal or no balance impairment on clinical exam, some studies have shown force plate measures in static and dynamic conditions to be sensitive to subtle balance impair-ments.^{8, 10, 18, 19} However, some studies have shown static stance to be less discriminating than dynamic testing. Nelson et al identified abnormal scores with sensory organization testing in only 30% of subjects with MS in a ‘high function’ group (defined as those who scored at least 24 out of 26 points on the Tinetti Performance Oriented Mobility Assessment).⁹ Similarly, Daley and Swank found only 6% of subjects with MS who were free from functional limitations had abnormal sway in quiet stance with eyes open, and this percentage increased to only 15% when the same subjects stood with eyes closed.⁷ These results suggest that force plate measures under static conditions may not be a very sensitive measure in minimally impaired persons with MS,^7–9 but that dynamic testing shows promise.^{8, 10, 19}

In contrast to testing postural control in response to external perturbations of the support surface, no studies to date have used a force platform to assess postural control in persons with MS during voluntary movements such as those used during performance of daily activities. Voluntary upper extremity movements cause internally-generated perturbations to balance due to inertial effects and changes in the position of the center of mass. It has been well documented that there is an anticipatory phase of postural activity in the trunk and lower extremities prior to the initiation of arm movements in standing.^20–27 These anticipatory postural adjustments (APAs) include EMG activity in the trunk and legs^{20–25, 27} and changes in kinetic variables measured by a force platform.^{20–22, 24, 26} Researchers have hypothesized that the CNS employs APAs to provide postural control in anticipation of the potentially destabilizing effects of the arm movement.^20–23

One laboratory measure that can reflect an attempt by the CNS to maintain an upright posture is the center of pressure (COP).^{22, 24–27} Center of pressure is the point of application of the vertical ground reaction force.²⁸ The COP displacement can be determined while subjects stand quietly on the force platform, or as they respond to perturbations, either internal or external, imposed on their bodies. Assessing COP displacement during a task such as standing and reaching provides a means for assessing postural control in response to internally-generated perturbations in the context of a common functional activity.

The purpose of this study was to determine if the laboratory measure of COP displacement during standing reaches could identify subtle changes in postural control in a group of individuals with MS who showed minimal or no balance deficits on clinical examination using the BBS. The task we analyzed consisted of standing and reaching to various distances, both within and beyond arms' length. We also examined limits of stability as reflected by the maximum COP excursion in the sagittal plane while the subjects voluntarily leaned as far anterior and posterior as possible without loss of balance. We hypothesized that the COP displacement variables during rapid, bilateral reaching movements and leaning movements would be different in minimally impaired subjects with MS when compared to a control group consisting of age- and gender-matched adults with no known orthopedic or neurological impairments. A preliminary report of these results has been published in abstract form.²⁹

METHODS

Subjects

Subjects with MS were recruited through the University of Nebraska Medical Center (UNMC) MS clinic. Potential subjects were required to have a definite diagnosis of MS,³⁰ be able to stand unassisted for 5 minutes, and be able to reach forward with both arms in standing without assistance. (Although there are newer criteria for the diagnosis of MS,³¹ our subjects were recruited before these criteria were published.) We operationally defined ‘minimal or no balance impairment’ as a score of 48 or greater on the BBS based on our desire to have some heterogeneity in our sample of subjects with MS while avoiding subjects likely to require an assistive device.¹⁵ As such, exclusion criteria included a score on the BBS less than 48 out of 56, a score on the Mini-mental State Exam (MMSE) less than 20 out of 30, the presence of coexisting neurological or orthopedic conditions that limited the subjects' ability to perform the testing protocol, or the use of an assistive device while standing or walking. Twenty-one subjects with MS, 15 women (44.1 ± 8.38 years) and 6 men (50.2 ± 8.61 years) met the criteria for the study and were tested.

Control subjects were recruited through advertisements on the UNMC campus and website, and the local newspaper. Recruitment of control subjects followed the recruitment and testing of subjects with MS, so that control subjects could be age-(± 2 years) and gender-matched. Control subjects were eligible to participate if they met the same inclusion criteria as the subjects with MS, with the exception of having a diagnosis of MS. The same exclusion criteria also applied to the control group. Twenty-one control subjects, 15 women (45.3 ± 8.56 years) and 6 men (49.7 ± 8.41 years) met the criteria for the study and were tested.

The study protocol was approved by the UNMC Institutional Review Board. All subjects provided written informed consent prior to participating in testing procedures, and all subjects participated in 2 testing sessions.

Clinical Measures Berg Balance Scale

The performance-based BBS consists of 14 tasks, with performance rated on each task from 0 (cannot perform) to 4 (normal performance) for a total of 56 possible points.³² The BBS has been shown to be a reliable³² and valid³³ predictor of fall status in older adults and patients with acute stroke. When combined with fall history, it has been shown to be a powerful predictor of fall risk in community-dwelling older adults.³⁴ Reliability and validity of the BBS have not been established in persons with MS. However, the BBS has been found to change in response to rehabilitation in adults with clinically stable MS.¹² Also, a preliminary study found a modest correlation (r = −0.498) between the BBS score and self-reported falls in this population, as well as a difference in mean BBS score between adults with MS who used an assistive device (mean = 42.1) and those who did not (mean = 49.3).¹⁵

Mini-mental State Exam

The MMSE is a 7-item test of general cognitive ability.³⁵ Possible scores range from 0 to 30, with higher scores indicating better cognition.

Expanded Disability Status Scale

The Expanded Disability Status Scale (EDSS) is an 11-point scale (0 = normal neurological examination; 10 = death due to MS) of general impairment and disability specific to persons with MS.³⁶ The EDSS has been widely used for many years to classify disease severity,³⁷ but it has been criticized because it is an ordinal scale based on subjective evaluation,³⁸ it has poor inter-rater reliability,^{39, 40} and it mixes components of impairment and disability.^{39, 40} Additionally, the EDSS appears to be less sensitive to changes in function than other scales.^41–43 W e included the EDSS, despite its limitations, to allow for comparison with prior studies that have characterized persons with MS in terms of EDSS scores.

Multiple Sclerosis Functional Composite

Due to the limitations of the EDSS, the Multiple Sclerosis Functional Composite (MSFC) was devised as a multidimensional tool to reflect the varied clinical presentations of MS.³⁷ It consists of 3 performance tests that measure 3 clinical dimensions of function: a Timed 25-Foot Walk (leg function), the 9-Hole Peg Test (arm and hand function), and the Paced Auditory Serial Addition Test (cognitive function). The scores from these 3 dimensions are combined to form a composite Z-score that can be used to detect change over time relative to the general population of persons with MS.

Laboratory Measures Accelerometry

The TSD 109C triaxial piezoelectric accelerometer (output ± 5g, 400 mV/g; BIOPAC Systems, Inc., Santa Barbara, Calif) was calibrated prior to data collection according to its manufacturer. The accelerometer was attached to the radial side of each subject's left wrist, with one of its axes oriented in the sagittal plane and perpendicular to the long axis of the forearm. Onset of arm movement was determined from the signal from this axis.

Target

The target consisted of two 7.6 cm by 15.2 cm carbon rubber electrodes mounted individually to a flexible foam bar attached to a free-standing, lightweight metal frame. The frame could be adjusted so that the target was at shoulder height and at appropriate distances for each subject. Two targets were used to promote symmetrical reaching with both hands, however contact data were collected from only the left target. Subjects wore a metal thimble on their left index finger. Touching the thimble to the target closed a low-voltage circuit to indicate target acquisition.

Force platform

During the leaning and reaching movements, subjects stood on a strain gauge force platform (Advanced Mechanical Technology, Inc., Watertown, Mass) with their feet in a comfortable stance and arms resting at their sides with their palms facing medially. Subjects were barefoot to minimize variability in performance that may occur due to differences in footwear. The position of each subject's feet on the force platform was marked to maintain consistent foot position during testing and so that individual characteristics such as foot length and position could be determined. A research assistant stood by the subject during testing to ensure maintenance of foot position as well as to assist the subject in the event of a loss of balance. Signals were collected for the vertical ground reaction force (Fz) and the moment of force about the mediolateral axis (Mx). Center of pressure movement in the sagittal plane (COPy) was calculated using the following equation: COPy = Mx/Fz.

Kinematic data

In order to assess movement velocity, 3-dimensional kinematics of the hand were recorded using the WATS-MART 2-camera infrared motion analysis system (Northern Digital, Waterloo, ON, Canada) with an infrared emitting diode (IRED) placed on the left index fingertip. The 2 cameras were placed approximately 3 m away from the subjects and oriented at approximately 60° apart. The cameras were calibrated prior to data collection according to the manufacturer's specifications using a cubic calibration frame, and calibration parameters were deemed acceptable if the overall root-mean-square error for marker positions was less than 5 mm.

Data capture

MP100 Workstation hardware and Acknowledge® software (BIOPAC Systems, Inc., Santa Barbara, Calif) were used with one computer system to collect and store signals from the accelerometer, target circuit, and force platform amplifier. These signals were all sampled at a rate of 1000 Hz using a 16-bit analog-to-digital converter. Electromyographic data were collected simultaneously, but will be reported in a separate communication. A second computer system was used to collect and store kinematic data from the infrared motion analysis system using WATSMART hardware and software. These signals were sampled at 250 Hz. Data collection was synchronized between the two systems using a 5-volt electronic trigger signal.

Testing Procedure Test sessions for subjects with multiple sclerosis

During the first test session, each subject with MS underwent a neurological examination consisting of the administration of the EDSS and the MMSE by a board-certified neurologist. The neurologist determined subjects' ability to perform the standing and reaching task, and interviewed them about current medications, age of onset, recent (within 6 months) fall history, and relevant orthopedic conditions. Additional clinical tests during the first test session included the BBS and MSFC, both conducted by a licensed physical therapist.

Within 7 days of the clinical test session, subjects with MS returned for a second testing session to collect laboratory data. Three items from the BBS were repeated to determine the stability of the subject's balance performance across test sessions. These items were: Item 1, sitting to standing; Item 8, reaching forward with outstretched arm; and Item 14, standing on one foot. Arm's length (AL) was measured from the acromion to the tip of the index finger, and height measurements were taken.

The first laboratory task consisted of anterior and posterior leans. The subjects stood on the force platform and were instructed to lean as far forward and backward as possible without falling and to hold this position for 5 seconds. Subjects were asked to keep their feet flat on the floor and aligned with respect to the frontal plane, but stance width and toe-out were not dictated to the subjects. Center of pressure movement in the sagittal plane measurements were recorded for a total of 4 leaning trials, 2 backward and 2 forward.

The second laboratory task consisted of a series of reaching movements performed from the same stance position as the leaning trials with the eyes open. Following the indication that the subject was ready, data collection was initiated after a random interval of 1 to 3 seconds. Five hundred milliseconds (ms) after the initiation of data collection, an audible tone was generated as the signal for the subject to perform the movement. The subject was instructed to reach forward with both arms to touch a target placed at shoulder height. The subject was told to move as fast as possible to minimize variation in the reaching activity,⁴⁴ but that reaction time in response to the tone was not important. The final reach position was held until the 3 second data collection period was complete. Subjects were provided opportunities to rest at any point during testing.

Five reaches were performed to each of 7 different target distances, some within and some beyond AL. In order to place the target at AL and control for differences in the amount of scapular protraction the subjects may have used to reach the target, a rigid yardstick was used to measure from the anterior aspect of each subject's acromion to the target as the subject stood on the force platform with their arms held at their side. Distances of the target beyond and within AL were then determined from the AL position using a tape measure placed on the floor under the frame on which the target was mounted. Target distance varied by 5 cm increments from AL minus 10 cm to AL plus 20 cm (AL-10, AL-5, AL, AL+5, AL+10, AL+15, AL+20). A Latin Square design⁴⁵ was used to vary the order of target distance across subjects. One subject with MS (subject M13) was unable to safely reach the furthest target distance, and therefore performed only 30 reaches to 6 target distances. Subjects were allowed up to 5 practice reaches to the AL+10 distance prior to data collection. If visible movement of the subject's arms or trunk occurred prior to the auditory ‘go’ signal, if the movement appeared markedly slower than other trials at the same distance, or if the target was missed, the trial was repeated.

Test sessions for control subjects

Control subjects also participated in 2 testing sessions. During the first session, the control subjects' orthopedic and neurologic health was confirmed by the same board-certified neurologist that examined the subjects with MS. The second testing session occurred within 60 days of the first test session. At the second test session, a licensed physical therapist administered the BBS and the MMSE. Testing of leaning and reaching movements for control subjects involved the same instrumentation and protocol as that described for subjects with MS.

Data Reduction Foot position data

Figure 1 provides operational definitions for foot position characteristics from one representative control subject. The following variables were determined from the foot tracings for all subjects: foot length (the distance from the great toe to the mid-point of the calcaneus), toe distance (the distance between the great toes), heel distance (the distance between the mid-points of the calcanei), and anterior-posterior base of support (AP BOS; the sagittal plane distance between the most anterior and most posterior point of contact on the force plate). Foot position was defined as the ratio of in- or out-toeing determined by dividing the toe distance by the heel distance, with ratios greater than one indicating a toe-out position.

Figure 1: Foot tracing for a representative control subject with operational definitions for foot placement characteristics. Foot length is defined as the distance from the great toe to the mid-point of the calcaneus. Heel distance is defined as the distance between the mid-point of the calcanei. Toe distance is defined as the distance between the great toes. Anterior-posterior base of support (AP BOS) is defined as the sagittal plane distance between the most anterior and most posterior point of contact on the force plate.

Kinematic data

Three-dimensional position data from the IRED placed at the tip of the index finger were low pass filtered (12 Hz) and differentiated to determine peak tangential velocity of the fingertip and time to peak tangential velocity relative to movement onset for each trial. Averages of peak tangential velocity and time to peak tangential velocity for each reach distance for each subject were calculated. The two groups were compared across distances.

Arm movement onsets were identified for each trial for each subject from the accelerometer signal using a computer algorithm. The algorithm identified peak wrist acceleration, and then searched backwards in time to when the acceleration trace first exceeded the baseline. Baseline of the acceleration trace was defined as the mean value of the signal over the first 250 ms of the sampling period (the sampling period having started 500 ms prior to the tone). The onsets identified by the computer were visually confirmed by one of the investigators. If the onset was uncertain because of artifacts that may have been due to backward movement of the hand or slow hand movement prior to onset of the reach, the trial was rejected. Out of a total of 1465 trials, 27 (2%) were rejected because of difficulties in identifying the onset of arm movement.

Kinetic data

Center of pressure movement in the sagittal plane data were averaged for the reaching trials to each distance (maximum of 5 trials, minimum of 3 trials to each distance) relative to the onset of arm movement and examined for peak-to-peak and net displacement in the sagittal plane. Figure 2A shows the change in COPy position over time (0 cm = initial starting position of the subject) during reaching to distance AL+20 for one representative healthy subject. This trace represents the average of 5 reaches, aligned to the onset of arm movement (time = 0 ms), and illustrates how COPy displacements were calculated. Negative values (COPy-) represent movement of COPy in the posterior direction, and positive values (COPy+) represent movement of COPy in the anterior direction. Peak-to-peak COPy displacement was defined as the difference between the maximum COPy- and COPy+ positions. Net COPy displacement was defined as the difference between the COPy position in the subject's initial resting posture and the COPy position in the final reach posture. Initial COPy position was calculated as the mean value over 250 ms prior to the ‘go’ signal and final COPy position was based on the mean value over 250 ms after the subject had attained the final reach posture. When comparing groups, the peak-to-peak and net COPy displacements were adjusted for each subject to account for differences in foot length and placement by dividing these values by the subject's AP BOS.

Figure 2: A. Change in center of pressure in the sagittal plane (COPy) position over time during reaching to a distance of arm's length plus 20 cm (AL+20). Data are from a representative control subject. The trace represents the average of five trials to this distance. The x-axis depicts time in ms, with the five trials aligned so that zero ms is the point in time that arm movement began. The y-axis shows COPy position in cm relative to the initial starting position (0 cm) of the subject. Negative values (COPy-) indicate movement of the subject's COPy in the posterior direction, while positive values (COPy+) indicate movement in the anterior direction. The dotted lines indicate the initial and final COPy positions. The initial COPy position was calculated as the mean value over 250 ms prior to the “go” signal. The final COPy position was determined from the mean value over 250 ms after the subject had attained the final reach posture. COPy net is the difference between the initial and final positions of COPy. Dashed lines indicate the maximum COPy- and COPy+ positions. COPy peak-to-peak is the difference between the maximal COPy- and COPy+ positions. COPy+ and COPy- are calculated relative to the initial COPy position. B. Changes in COPy position for a representative subject with MS during leaning trials. Data are shown for 2 leans, one anterior and one posterior. Data were collected for a total of 5 seconds (x-axis). The y-axis depicts COPy position relative to the initial starting position (0 cm) of the subject. The limit of stability in the anterior-posterior direction (LOSAP) is defined as the difference between the most anterior and most posterior position of the COPy during the leaning trials.

Figure 2B shows COPy position data from one representative subject with MS during 2 leaning trials (1 backward and 1 forward). Zero on the x-axis represents the initial starting position of the subject. Changes in COPy position in the positive direction on the y-axis represent anterior leans, while posterior leans result in negative values of COPy position. The limit of stability in the anterior-posterior direction (LOSAP) was defined as the difference between a subject's most anterior and most posterior position of the COPy during the leaning trials. The percentage of the LOSAP used during the reaching task was also calculated as: (peak-to-peak COPy/LOSAP) × 100.

Statistical Analysis

Paired two-tailed t-tests were used to compare the 2 groups of subjects on the following variables that may have had an influence on the task: height, arm length, foot length, foot position, and AP BOS. Paired two-tailed t-tests were also used to compare groups on LOSAP during the leaning trials. Two-way ANOVAs (group x target distance) with one repeated measure (target distance) were used to evaluate group differences and the effects of target distance on COPy net, COPy+, COPy- and COPy peak-to-peak displacement, percentage of LOSAP used during the reaching task, peak tangential velocity of the fingertip, and time to peak tangential velocity of the fingertip. Tukey's test was used for post-hoc multiple comparisons for the variable of reach distance. The alpha level was set at P < 0.05. Microsoft® Excel 2002 (Microsoft Corporation, Redmond, WA) and SigmaStat for Windows Version 2.03 (SPSS, Inc., Chicago, III) were used for data analysis.

RESULTS

Subject Characteristics

Descriptive characteristics (mean ± SD) for all subjects are listed in Table 1. Subjects were matched for age (± 2 years) and gender. Paired two-tailed t-tests revealed that subjects with MS did not differ from control subjects on any of the other variables listed in Table 1.

Table 1: General Characteristics of Subjects. Subjects were matched for (± 2 years) and gender. Groups did not differ on other variables listed.

Table 2 provides clinical characteristics for all subjects with MS. These subjects scored well on the various clinical tests. Ten out of the 21 subjects scored the maximum number of points (56) on the BBS, with a median score of 55 (one control subject scored 55, all other control subjects scored 56 on the BBS). The median score on the EDSS was 2.0 on a scale of 0 to 10, with lower scores indicating better function. Fifteen of the 21 subjects with MS had a positive MSFC overall z-score, indicating function better than the average of the general population of persons with MS. The subjects with MS also appeared stable in their performance between sessions on the BBS. During the second test session, only 4 subjects differed on the 3 items that were repeated, and only by one point each.

Table 2: Clinical Characteristics of Subjects with Multiple Sclerosis

Kinematic variables

There were significant main effects of reach distance on peak tangential velocity of the fingertip and time-to-peak tangential velocity (P < 0.001 for each variable). There was no between-group difference in peak tangential velocity or time-to-peak tangential velocity, and no group x distance interaction.

Center of Pressure Movement in the Sagittal Plane: Lean Trials

Table 3 shows the mean (± SD) of LOS_AP during the maximum anterior and posterior lean trials for both groups. When leaning, the control subjects moved their COPy over a greater (P = 0.008) distance (14.2 ± 2.6 cm) than the subjects with MS (11.9 ± 2.9 cm). There was also a difference (P = 0.002) between groups when the AP BOS was taken into account and the LOS_AP was expressed as a percentage of the base of support.

Table 3: Group Differences During Lean Trials. Control subjects demonstrated a larger LOS_AP (p = 0.008) than subjects with MS. This difference was also apparent when the AP BOS was taken into account (p = 0.002).

Center of Pressure Movement in the Sagittal Plane: Reach Trials

Figure 3A depicts mean (± SD) net and Figure 3B shows mean (± SD) peak-to-peak COPy displacements for both groups of subjects across reach distances after AP BOS was taken into account. For both groups, COPy net displacement increased as target distance increased (P < 0.001), but there was no difference between groups and no group x distance interaction. Figure 3B illustrates that there was a difference in peak-to-peak COPy displacement between groups (P < 0.001), with control subjects showing greater peak-to-peak COPy displacement. The greater peak-to-peak COPy displacement in the control group was primarily due to a significant difference in COPy+, while COPy-did not differ significantly between groups. Peak-to-peak COPy displacement increased as target distance increased (P < 0.001), but there was no group x distance interaction.

Figure 3: A. Mean net COPy displacement for both groups during reaches to each distance. Reach distance in cm relative to arm's length is depicted along the x-axis. Reach distances varied by 5 cm increments and ranged from 10 cm short of arm's length to 20 cm beyond arm's length. (AL-10, AL-5, AL, AL+5, AL+10, AL+15, AL+20). COPy displacement is expressed as a percentage of each subject's AP BOS AND is represented along the y-axis as means (±SD) of each group. The black bars represent subjects with MS AND the white bars represent control subjects. B. Mean peak-to-peak COPy displacement for both groups during reaches to each distance. Axes are the same as in Fig 3A. The black bars represent subjects with MS, while the white bars represent control subjects. C. Mean percentage of LOS_AP used during reaching for both groups to all target distances. The x-axis is as in Figure 3A. The percentage of LOS_AP used during reaching was calculated by dividing the COPy peak-to-peak displacement during reaching by the LOS_AP determined from the leaning trials for each subject. These values are expressed as means (±SD) for each group along the y-axis. The black bars represent subjects with MS, while the white bars represent control subjects.

The percentage of the LOS_AP used during the reaching task was evaluated for each group. Figure 3C illustrates the mean (± SD) percentage of the LOSAP used for peak-to-peak COPy displacement during the reaching task to each distance. Percentage of LOS_AP used increased as target distance increased, with means approaching 100% for both groups for the longest distance. For the longest reaches, some individual subjects in each group demonstrated peak-to-peak COPy displacement greater than the LOS_AP they demonstrated during the leaning task. There was an effect for distance on the percentage of LOS_AP used during reaching (p < 0.001), but there was no difference between groups and no group x distance interaction.

Secondary Analysis of Center of Pressure Movement in the Sagittal Plane During Reaching

A secondary analysis was performed in order to determine if significant differences in COPy measures could still be seen when comparing healthy subjects to those subjects with MS who had the least balance impairments based on BBS scores. To do this, we divided the subjects into 3 groups: Healthy subjects with a BBS score of 55 or 56 (n = 21; 1 with a BBS score of 55), subjects with MS AND a BBS score of 55 or 56 (n = 12;2 with a BBS score of 55), and subjects with MS AND a BBS score < 55 (n = 9; mean ± SD BBS score of 52 ± 2). Both groups with MS still differed significantly (P < .02) from the Healthy group on COPy peak-to-peak and COPy+ measures. The mean values for 2 groups with MS did not differ significantly, but the test was underpowered after dividing the subjects with MS into 2 groups.

DISCUSSION

We found differences in COPy measurements between a group of minimally impaired adults with MS AND age- and gender-matched control subjects, during rapid reaches to various target distances and during leaning movements. These differences persisted even when the control subjects were compared only to the 12 subjects with MS who scored the highest (55 or 56) on the BBS. Specific variables that these groups differed on included their LOS_AP during maximum leans and their peak-to-peak COPy and anterior (COPy+) displacement during the reaching tasks. These differences cannot be explained by differences in anthropometric variables, differences in foot position, or differences in movement kinematics as assessed by peak tangential velocity of the fingertip and time to peak tangential velocity.

Variations in foot position in quiet standing have been found to affect postural sway and mean position of COP.⁴⁶ Kaminski and Simpkins²⁶ found increases in COPy displacements in healthy subjects using a step stance (right foot ahead of the left at a distance equal to 40% of leg length), when compared to subjects in parallel stance during standing reaches to distances greater than AL. They suggested the increase in COPy displacement occurred to assist whole body motion to the target. We examined AP BOS in our study and did not find a difference between groups. We further controlled for this variable by dividing each subject's LOS_AP AND COPy displacements by their AP BOS before comparing groups. Additionally, there was no difference between groups in foot position variables (heel distance, toe distance, or ratio of toe distance to heel distance). Therefore, differences in stance configuration cannot account for differences in LOS_AP or peak-to-peak COPy between the two groups.

Greater arm velocity during reaching movements is associated with earlier activation of postural muscles and greater response magnitude.⁴⁴ However, in our study, kinematic variables of peak tangential velocity of the fingertip and time to reach peak tangential velocity did not differ between groups. Consequently, the greater COPy excursions observed in healthy individuals do not appear to be due to differences in movement speed.

The Functional Reach (FR) was developed as a test of balance in response to the voluntary movement of reaching, and was found to correlate with COP excursion (r = 0.71).⁴⁷ Frzovic et al found that the FR was a useful test to differentiate between adults with MS AND control subjects.¹¹ In contrast to the relatively slow, unilateral reaches performed in the FR test, the reaching task used in this study was intended to produce greater postural control demands during a task of reaching while standing. Horak et al found that postural muscle activity was more variable, was sometimes absent, and did not always precede arm movement when subjects were asked to raise their arms slowly compared to quick arm movements.⁴⁴ They speculated that less stabilization force is necessary during low velocity movements. While the FR is destabilizing in that subjects must displace their center of mass to perform reaches to their maximal distance, the rapid arm movements used in this study would generate larger inertial forces in addition to displacing the body center of mass. Furthermore, consistent with previous findings,^{20–22, 24, 26} changes in COPy occurred prior to the internal perturbation of rapid arm movement, indicating anticipatory behavior. Thus, we would suggest that the rapid, goal-directed reaching paradigm used in this study provides additional information not gained with the FR alone.

Subjects with MS demonstrated smaller LOS_AP than our control group. The smaller LOS_AP demonstrated by subjects with MS in our study suggests that our subjects were less willing and/or able to deviate from their initial COP position in the sagittal plane when compared to individuals with no neurological impairment, indicating a voluntary or involuntary self-limiting strategy. Interestingly, there were no differences between groups in the percent of LOS_AP used for peak-to-peak COPy displacement during the reaching tasks. For both groups, percent of LOS_AP used during reaching increased as target distance increased, nearing 100% for the longest distances. The fact that there was no difference between groups on this variable suggests that the subjects with MS were instinctively aware of their limitations, and were able to find a strategy to achieve the same task as the controls, despite their decreased were able to find a strategy to achieve the same task as the controls, despite their decreased LOS_AP.

Reach distance had a main effect for many of the variables in our study, including net COPy displacement, peak-to-peak COPy displacement, COPy+ and COPy-displacement, percentage of LOS_AP.used during reaching, peak tangential velocity of the fingertip, and time to peak tangential velocity of the fingertip. Systematic differences in COPy displacement with reach distance have been previously found in healthy young adults^25–27 as well as healthy elderly.²⁵ In these studies, COPy trajectories were qualitatively similar across reach distances, with COPy initially moving posteriorly, then anteriorly, then to a relatively steady final position. In addition, these authors found that as target distance increased, net and peak-to-peak COPy displacement increased. Our findings are consistent with these qualitative patterns of COPy during reaching as well as the main effect of reach distance on net and peak-to-peak COPy displacement. In addition, we found the qualitative pattern of the COPy displacement during reach to be identical in all subjects tested, regardless of whether or not they had a diagnosis of MS.

In the interest of simplicity, we chose not to report each pair-wise difference found with post-hoc testing. In general, differences were found between most pairs of reach distances for all of the COPy variables, with the exception of the two shortest distances (AL-10 and AL-5). This finding is in agreement with previous studies of healthy sub-jects.^{25, 27} We suggest that in future studies, the task could be streamlined to include only one short and one long distance without losing the salient features of the data. Furthermore, because of the complex and multidimensional nature of balance, there is no single test that adequately assesses bal-ance.⁵ Streamlining this reaching task would allow more time to assess patients or subjects with other types of balance tests such as sensory manipulation, external perturbations, or functional scales.

Our study found that healthy subjects demonstrated significantly more peak-to-peak COPy displacement than subjects with MS during reaching movements. However, no differences were found between groups in net COPy displacement (the difference between the initial and final COPy positions). The fact that there was no difference in net COPy between groups indicates that both groups were able to successfully reach the target and maintain contact with it. Since the peak-to-peak COPy gives insight into the pattern of COPy movement prior to reaching the target, the significant difference in peak-to-peak COPy displacement suggests that subjects with MS used different movement strategies to achieve target acquisition.

The adults with MS in this study appeared minimally affected when assessed with standard clinical tests (see Ta b le 2). For instance, a clinician scoring most of these subjects on the BBS would not document a substantial balance impairment based on their scores. However, the subjects with MS demonstrated differences from healthy control subjects on COPy variables, implying that the BBS had a ceiling effect and failed to detect subtle balance deficits in this population. Other studies have suggested a ceiling effect in the BBS with elderly persons.^{48, 49} Furthermore, the BBS may lack sensitivity to change for subjects such as those in our study, with little room left for improvement in response to intervention.

The instrumented measures used here may be more sensitive than common clinical tests for objectively documenting both deficits and improvements in balance. With force plate technology becoming more common in physical therapy clinics, these variables would be easy to capture as part of a physical therapy examination. Because MS is a progressive disease, tools to measure balance impairments during early stages of the disease may lead to identification of persons at risk for future decline and lead to earlier intervention.

CONCLUSION

Our data demonstrate that peak-to-peak COPy and COPy+ displacement during reaching, as well LOS_AP. during leaning, are less in minimally impaired adults with MS than in age- and gender-matched control subjects. However, there was no difference between these groups when the COPy displacement during reaching was expressed as a percentage of the LOS_AP during leaning. This suggests that persons with minimal impairments due to MS were instinctively aware of their limitations, and were able to find a strategy to achieve the same task as the controls, while staying within their decreased LOS_AP. These center of pressure measures show clear differences in persons with MS who show little or no deficit on clinical measures such as the BBS when compared to a healthy control group. The usefulness of COP-related variables to measure change, either over time or in response to intervention, is worth further exploration.

ACKNOWLEDGEMENTS

This work was supported in part by a Pilot Research Award from the National Multiple Sclerosis Society. The Nebraska Bankers Association provided funding for the force platform. We would also like to thank Eliad Culcea, MD; Grace Johnson, PT, OCS; Janis McCullough, PT, DPT; Wade Lucas, PT, DPT; and Thomas Spray, PT, DPT for assistance with data collection and analysis.