Postural control involves the coordination and integration of multiple sensory and motor events. Sensory information about the body's position in space (including visual, vestibular, proprioceptive, and tactile) is received and integrated by the brain, and appropriate motor responses are generated to maintain balance. Impairments in any component of these systems may predispose an individual to diminished postural stability. Multiple sclerosis (MS), which is characterized by central nervous system lesions that can affect sensory and motor function, is frequently associated with postural instability (10,12,27,37). In fact, there is a high incidence of falls in persons with MS (8), and ~45% of persons with MS require assistive devices for mobility (7).
Many investigators have studied postural stability in MS (10,12,27,37). Clinical standing balance tests show that people with MS have difficulty holding tandem and single-limb stances for 30 s (10,37). The response to an external perturbation (i.e., shoulder tug test) is also poorly controlled in MS (10,37). Recently, balance performance has been shown to vary depending on the subtype of MS (primary progressive, relapsing-remitting, and secondary progressive) (37). Persons with MS have slower gait speeds (3,38,39), suggesting the presence of instability or fear of falling.
Individuals with MS exhibit greater postural instability under conditions that minimize visual and tactile sensory input, demonstrating an inability to compensate for induced sensory deficits and suggesting impairments in the vestibular system (12,27). There are limited numbers of posturography studies in persons with MS; however, it has been shown that persons with MS have altered trunk control during a reaching task while seated (22) and a smaller displacement of the center of pressure (CoP) relative to the base of support during a leaning task in the sagittal plane compared with healthy controls (14).
Muscle weakness in the lower extremities, which can also contribute to postural instability, has been shown by a number of investigators to occur in people with MS (15,21,28,29,31,34). Weakness and postural disturbances have been linked in other disorders of the central nervous system. It has been established in stroke patients that muscle strength plays a greater role in maintaining postural stability when somatosensory and visual cues are removed and heightened vestibular function is required (24). In patients with Parkinson disease, dynamic balance, movement velocity, gait velocity, and stride length are shown to be correlated with muscle strength at the ankle, hip, and trunk (26). Furthermore, strength deficits in individuals with MS are most apparent during dynamic contractions at high velocities (1,21,31), revealing the significant effect of the disease on lower extremity muscle power. Leg power is predictive of functional mobility and performance in the elderly (2,4), highlighting the importance of these deficits. In addition to muscle weakness, the extent of bilateral strength asymmetry in the locomotor muscles and its effects on balance are not known. Likewise, it is not known whether asymmetries in the distribution of limb loading, which could arise from bilateral strength asymmetry, contribute to postural instability in MS.
Symptomatic fatigue, identified as the single most disabling symptom (9), may also play an important role in postural control in persons with MS. Increasing body temperature and energy expenditure throughout the day may exacerbate symptomatic fatigue (19). Thus far, the relationship between symptomatic fatigue and postural control has not been explored. Alterations in sensory input, symptomatic fatigue (9,33), and muscle weakness (1,21,31), all of which are common in MS, may each contribute to postural instability and limitations in physical function.
The aim of this study was to quantify the magnitude of and the associations between bilateral strength and limb-loading asymmetries, postural control, and symptomatic fatigue in persons with MS. We studied the knee extensor (KE) and the dorsiflexor (DF) muscles due to their differing contributions to postural stability (6) and locomotion (23). We hypothesized that, compared with healthy controls, women with MS would 1) be weaker in both the KE and the DF muscle groups, 2) have greater between-limb isometric torque and power asymmetries, 3) have greater limb-loading asymmetry, and 4) have greater variability in the postural CoP. In addition, we were interested in examining the relationships between variables of postural control, symptomatic fatigue, bilateral isometric torque and power asymmetries in the KE and the DF muscles, and physical function.
Subject characteristics and functional assessments.
Twelve women with MS and 12 age-matched healthy female controls were recruited from the university, the surrounding communities, and the local MS support groups. All subjects provided signed informed consent, as approved by the institutional review board at the University of Massachusetts, Amherst. Medications taken by the patients with MS included immune modulators, antidepressants, and antispasticity drugs. Women with MS were excluded if they had less than 20/200 visual acuity, had oculomotor or cerebellar disorders, or were nonambulatory. All subjects were otherwise healthy, free from orthopedic injury of the lower extremities, and did not participate in more than 30 min of structured exercise for more than 3 d·wk−1. Subjects came in for a total of three visits: familiarization, strength testing, and postural stability testing. All MS volunteers also underwent a clinical evaluation by the study neurologists in a separate visit. This included medical history, neurological exam, and determination of each individual's disease severity using the Expanded Disability Status Scale (EDSS) (20).
In the familiarization session, measures of symptomatic fatigue, physical function, and sensory function were performed. The Fatigue Severity Scale (FSS) (18) and the Visual Analog Fatigue Scale (VAFS) (35) were used to assess recent (previous 2 wk) and acute (immediately before data collection) symptomatic fatigue, respectively. The FSS is a nine-item questionnaire, and the VAFS is a 100-mm scale on which the subject draws a mark indicating the current degree of fatigue. In addition to the measures of fatigue, two trials of the following measures were performed, and the best time was recorded for each measure. Ten seconds of rapid toe taps were counted on each foot and used as an index of central motor drive and coordination. Peripheral sensory function was assessed using a 128-Hz tuning fork, which was struck and then placed at the first metatarsal head of each foot, as is common in clinical evaluations of sensory function. The recorded time began upon the placement of the tuning fork and lasted until the subject no longer perceived the vibration. Walk time was measured as an index of physical function. Subjects were timed twice for a 25-ft (7.62 m) unaided walk; first at a brisk and then at a normal pace. Following these measures, subjects were familiarized with the dynamometer (Biodex Medical, Shirley, NY) setup and were given an opportunity to practice the contractions that they would perform in the strength session with each leg.
Strength measures were performed for each leg, with the subject seated on a dynamometer. Shoulder, waist, and thigh straps were used to stabilize the body. Velcro straps were also used to stabilize the leg or the foot during contractions. The joint axes at the knee and ankle were aligned with the axis of the dynamometer arm for knee extension and dorsiflexion, respectively. The knee angle was fixed at 90° flexion, and the ankle angle was fixed at 120° relative to the shank (which was parallel to the floor) during isometric contractions. During dynamic contractions, the range of motion (ROM) was 55° starting at 90° flexion for knee extension and the middle 30° of the total ROM for ankle dorsiflexion.
For each muscle group, subjects performed three maximal voluntary isometric contractions (MVIC), with 2 min of rest between trials. Subjects then performed three consecutive isotonic contractions with a resistive load of 45% of the peak isometric torque and 3 to 4 s of rest between contractions. Joint torque and velocity were collected at 500 Hz with LabView software (National Instruments, Austin, TX). Isometric torque (MVIC; N·m) and power (W) were determined for each subject for each trial using a customized program in MATLAB software (MathWorks, Inc., Natick, MA), and the highest values for isometric torque and isotonic power were recorded. Strength asymmetry scores were determined for both peak isometric torque and power as
where the strength ratio (either peak isometric torque or power) was the value for the weaker limb divided by the value for the stronger limb. Zero percent asymmetry indicated even distribution of isometric torque or power across limbs, and 100% indicated maximal asymmetry.
Two adjacent force plates (Advanced Mechanical Technology, Inc., Watertown, MA) were used to record ground reaction forces underneath each foot while subjects stood quietly for 20 s with their eyes directed forward and arms resting at their sides. Stance width was constrained to 30 cm, and subjects wore their own comfortable street shoes during data collection. Data were sampled at 100 Hz using Qualisys Track Manager (Qualysis Medical AB, Gothenburg, Sweden); CoP for each foot was computed from the vertical ground reaction forces in Visual 3D™ (C-Motion, Inc., Rockville, MD). The net CoP (CoPnet) was calculated as
and indicated whole-body CoP (43). The CoPnet variability (CoPv; SD of CoPnet over the time series) in the anteroposterior (AP) and mediolateral (ML) directions was used as a measure of postural control, where greater variability indicated greater postural sway.
The force plates were also used to assess the bilateral distribution of body mass during quiet stance. Loading asymmetry was calculated as
where Fz high indicated greater limb loading with respect to the other limb (Fz low). Zero percent loading asymmetry score indicated even distribution of body mass beneath the feet, and 100% indicated all of the body weight on one foot.
All analyses were performed using SAS software (Version 8.0; SAS Institute, Inc., Cary, NC). Unpaired t-tests were used to detect group differences in age, height, mass, EDSS, FSS, VAFS, toe-tap counts, timed vibration, normal and brisk walk times, stride numbers, MVIC, peak isotonic power and velocity, MVIC and power asymmetry scores, CoPv, and loading asymmetry scores. A paired t-test was used to compare across-limb differences for each group in toe-tap counts, timed vibration, isotonic velocity, and Fz. Linear correlation analyses were used to examine the associations between variables of strength asymmetry, symptomatic fatigue, walk times, and postural control. Data are expressed as mean ± SD. Precise P values and 95% confidence intervals for differences between groups are reported, as appropriate.
Subject characteristics and functional assessment.
The numbers of women with MS in the different subtypes were as follows: one primary progressive, four secondary progressive, and six relapsing-remitting. The disease classification of one woman was unknown by our neurologist's assessment. The duration of the disease was 15± 11 yr (range = 3-38 yr). Mean EDSS for the MS group was 4 ± 1 (range = 2-6; median = 4), indicating a mild-to-moderate degree of impairment in this study group. Women in the MS group (n = 11) reported an average of three falls in the preceding year (SD = 3; range = 0-12). The study groups' characteristics and physical function data are summarized in Table 1. Both groups were similar in age, height, and mass. Both acute (VAFS) and recent (FSS) measures of perceived fatigue were higher in MS compared with controls. Maximal toe-tap count was lower in MS compared with controls in the right foot; however, toe-tap count was similar across groups in the left foot. There werebetween-foot differences of toe-tap counts in controls (P = 0.01) but not in MS (P = 0.13). The time of perceived vibration was shorter in MS compared with that in controls, with no between-foot differences in either group (P ≥ 0.41). Women with MS had longer normal and brisk walk times and greater numbers of strides compared with controls (Table 1).
Table 2 summarizes the KE and the DF strength and power results. KE and DF peak isometric torque values were similar in MS and controls. Peak KE power was lower in MS compared with that in controls; but peak DF power was similar across groups (data include one woman with MS who dorsiflexed with an ROM of 23°). Power differences in KE were accompanied by differences in peak velocity (MS = 3.4 ± 0.5 rad·s−1; control = 4.3 ± 0.5 rad·s−1; P < 0.001).
Table 3 summarizes the strength asymmetry scores in the KE and the DF. No difference across groups in isometric strength asymmetry was observed for KE or DF. KE power asymmetry was greater in MS compared with that in controls, with no difference across groups in power asymmetry in the DF. There were no differences across limbs in KE peak velocity in either group (P ≥ 0.15).
Mean AP CoPv during quiet stance was greater in MS compared with that in controls (7.52 ± 3.02 and 4.33 ± 1.79 mm, respectively; P = 0.005; Fig. 1). However, mean ML CoPv during quiet stance was only modestly greater in MS compared with that in controls (4.15 ± 3.10 and 2.22± 1.70 mm, respectively; P = 0.07). The loading asymmetry score, which is based on bilateral differences in ground reaction forces for each foot, was greater in MS compared with that in controls (Table 3).
Symptomatic fatigue (VAFS and FSS) and normal and brisk walk times were each correlated to KE power asymmetry (Table 4), such that those with greater asymmetry reported more fatigue and had longer walk times. Table 5 summarizes the correlation coefficients and P values for the CoPv analyses. In general, the measures of symptomatic fatigue and physical function were better correlated with CoPv in the AP direction than in the ML direction. The AP CoPv was associated (r ≥ 0.55) with brisk walk time, KE power asymmetry, and loading asymmetry and only modestly correlated with FSS, VAFS, normal walk time, and DF power asymmetry. In contrast, the ML CoPv was strongly associated only with loading asymmetry. The loading asymmetry score was neither correlated with KE (r = 0.35, P = 0.09) nor DF (r = 0.06, P = 0.76) with power asymmetry scores. The FSS (r = 0.44, P = 0.03), but not the VAFS (r = 0.20, P = 0.34), was associated with loading asymmetry score.
The results of this study provide new evidence of asymmetries in KE power and postural control in people with MS and suggest a role for these disturbances in the symptomatic fatigue and physical limitations that are so common in this disease. Figure 2 shows a schematic representation summarizing how strength asymmetries may play a role in mediating fatigue, gait, and balance in MS. These results suggest that therapeutic interventions designed to ameliorate strength asymmetries may be useful in alleviating physiological, functional, and symptomatic problems in this population.
Functional mobility is essential for maintaining a high quality of life. Slower gait speed in the physically impaired elderly (4) and persons with MS has been associated with muscle weakness (38,39). Our women with MS required more time and more steps to walk 25 ft at both normal and brisk paces compared with controls. During locomotion, a prolonged double support phase has been observed in persons with MS (3), which is similar to that observed in the elderly (42). Slower walk speeds and altered gait may thus be characteristics of postural instability. Changes in these parameters may also indicate a fear of falling. The relationship between KE power asymmetry and walk times observed here also suggests that power asymmetry in the lower limb may negatively affect gait speed.
Fatigue in persons with MS is a complex, disabling symptom that worsens with increases in body temperature and energy expenditure throughout the day. In our effort to minimize symptomatic fatigue, subjects were scheduled for the early morning, when the environmental temperature was cooler and minimal energy was expended. Despite our attention to minimizing symptomatic fatigue, the MS group scored higher on the VAFS and the FSS compared with controls, which is consistent with the results of others (9,28). The FSS was used to assess recent symptomatic fatigue by evaluating the 2 wk before study participation, whereas the VAFS was used to assess acute (i.e., at the time of data collection) symptomatic fatigue. Although FSS may be a better indicator of symptomatic fatigue because it distinguishes fatigue from depression and cognitive maladies, VAFS has been shown to be well correlated with FSS (18). Interestingly, muscle fatigue (defined as the inability of a muscle or muscle group to sustain a required force) has been shown in MS not to be associated with symptomatic fatigue, as determined by the FSS (36).
The decline of muscle strength in persons with MS can be attributed to both central and peripheral factors. Reduced central activation in MS has been observed as lower maximal motor unit firing rates (32), as well as incomplete activation of motor units (28). Significant changes also occur to the skeletal muscle itself, including slower contraction speed (28), lower oxidative capacity (16), and atrophy (15). At the single-muscle fiber level, force deficits in type IIa fibers from the vastus lateralis muscle of subjects with MS were explained by the atrophy of those fibers, whereas lower force production in type I fibers was attributed to both atrophy and decreased specific tension (11).
Studies of muscle power in MS individuals have revealed progressively greater muscular weakness with increasing contraction velocity in the KE and the flexor muscles (1,21,31). Armstrong et al. (1) showed the greatest decrement in peak torque at the highest tested isokinetic velocity (275°·s−1) during knee extension and flexion. Ponichtera (31) showed similar results and, in addition, observed greater peak torque during eccentric compared with concentric contractions in individuals with MS. Given these results, as well as the slowing of contraction speed that has been observed in both electrically stimulated (17) and voluntary (28) contractions in MS, it is reasonable to hypothesize that the slowing of contractile velocity due to neural and muscular factors may play an important role in the reduced muscle power of persons with MS. More recent reports of improved strength, mobility, and symptomatic fatigue in persons with MS after resistance training interventions (5,41) indicate a promising direction for future research aimed at reversing some of the physical limitations of this disease.
In the present study, we observed similar isometric torques in MS and control groups for both the KE and the DF muscles, results that are consistent with previous reports (15,29). Likewise, DF power did not differ across groups despite the slowing of foot-tap speed in MS compared with control subjects. In conjunction with the decreased KE power and contractile velocity found in our women with MS, these results suggest that muscle weakness was detected in MS only under conditions that required high velocities, such as those generated by the KE muscles. Thus, it appears that the KE muscles may be more susceptible to changes in muscle power than the DF muscles. Because we did not measure muscle size in this study, we do not know the extent to which muscle atrophy contributed to the loss of KE power in our MS group. Clarification of the extent and the mechanisms of decreased muscle power in MS will require additional study.
In addition to the neural and muscular factors discussed above, the decline in contraction velocity during KE could be attributed in part to spasticity in persons with MS. Olgiati et al. (30) used knee flexion-extension time as an index for spasticity and observed a positive relationship between energy cost of walking and flexion-extension time in MS, suggesting that spasticity or poor neuromuscular coordination results in poor gait efficiency. The possibility that this inefficiency may become a factor in fatigue for persons with MS warrants further attention.
Although bilateral strength loss has been observed in MS (39), individuals with this disease often report unilateral muscle weakness. In their study of leg power in people with MS, Lambert et al. (21) suggested the presence of greater strength asymmetries between the dominant and the nondominant legs of subjects with MS compared with controls, although no significant difference was detected. In the present study, we observed significantly greater power asymmetry in the KE in women with MS than in controls, as well as asymmetry in an important indicator of postural stability, CoPv. To the best of our knowledge, these results provide novel evidence of functional asymmetries in MS. Although causality cannot be established, the relationship between fatigue and KE power asymmetry observed here suggests that power asymmetry may contribute to the symptom of fatigue. Thus, strength training to reduce power asymmetry in persons with MS may help to partially alleviate symptomatic fatigue in this population.
Adequate sensory and motor functions are critical components of postural control. Although standing on either stable or unstable support surfaces, with vision, MS subjects have shown greater sway velocities of the CoP in AP and ML directions compared with controls (12). Furthermore, sensory organization tests revealed that persons with MS had greater sway when required to rely mainly on their vestibular system (12,27). Thus, it appears that persons with MS perform balance tasks better when all sensory (i.e., visual, proprioception, vestibular) and motor functions are intact (12,27). It is plausible that the ability to integrate and interpret sensory input may be affected by symptomatic fatigue. However, two recent studies showed that balance perturbation responses (10) and gait pattern (25) were similar at different times of the day in subjects with MS, although symptomatic fatigue was different at these times.
Our measure of postural sway was CoPv. The variability in CoP has been shown to be a sensitive measure for detecting postural control changes in individuals who are minimally impaired by their MS (14). A traditional view of variability suggests that minimal CoPv would reflect a better ability to stand quietly and would therefore indicate better stability. We observed greater CoPv in the AP direction and a modest trend for greater CoPv in the ML direction in women with MS compared with age-matched controls. The observed increase in postural sway suggests that postural control is affected in people with mild to moderate MS even under quiet upright stance conditions.
Our observation of a modest increase in postural sway (CoPv) in the ML direction in the MS group is consistent with results from Gutierrez et al. (13). They found that higher EDSS scores were correlated with reduced lateral balance control. Observations of reduced lateral balance control in MS are consistent with results from research on Parkinson disease (40). As lateral balance control emerges from the weighting and unweighting of each limb (43), increased lateral sway may result from asymmetries in left and right limb loading. In the current study, we observed greater limb-loading asymmetry in women with MS compared with controls. Moreover, the high positive correlation observed in our study between limb-loading asymmetry and postural sway in both AP and ML directions (see Table 5) suggests that load distribution beneath the feet plays a role in postural control and stability. Favoring of one limb over the other may predispose individuals to imbalances and falls. Interestingly, no relations were found between limb-loading asymmetry and KE or DF power asymmetry, suggesting that bilateral peak power differences at the knee and ankle are not responsible for differences in limb loading.
We found a significant association between KE power asymmetry and CoPv in the AP direction. Edwards (6) examined the interaction of multiple joints on the minimum joint stiffness needed to provide adequate torque around the joints to maintain standing balance. When the knee joint was included in the "inverted pendulum" model, more stiffness at each joint was required when the ankle and the hip joints were permitted to rotate to maintain balance (6). This observation suggests that weakness at the knee joint could compromise the maintenance of balance during quiet, bilateral stance. Thus, the increased asymmetry of KE power of our MS group may contribute to their postural instability, particularly in the AP direction.
We also found modest relationships between CoPv in the AP direction and symptomatic fatigue, suggesting that more energy or effort may be expended under conditions of greater postural sway so that greater symptomatic fatigue could develop. Symptomatic fatigue (FSS) was modestly associated with limb-loading asymmetry, again demonstrating a potential link between postural alterations and generalized fatigue in MS. Finally, CoPv in the AP direction was associated with walk times, which support the notion that concerns about postural stability in people with compromised balance control may result in slower walk speeds. More thorough investigation of these novel results pertaining to the interactions between physiological, functional, and symptomatic disturbances in MS is needed.
In addition to the demonstration of bilateral power deficits and asymmetry of the KE muscles of women with MS, the results of this study provide new evidence of interactions between power asymmetry, postural stability, walk times, and symptomatic fatigue (Fig. 2). These results suggest that interventions designed to correct muscle power asymmetries may lead to improvement in several aspects of physical functioning that are important for maintaining quality of life in persons with MS.
The authors thank Steve Foulis and Molly Johnson for their assistance in recruitment and data collection; Brian Smith, M.D., and George Baquis, M.D., for clinical evaluations; Ross Miller, M.S., and Mike Tevald, P.T., Ph.D., for their insightful comments; and the volunteers for their participation in the study. This work was supported by the National Multiple Sclerosis Society Grant PP0934. The results of the present study do not constitute endorsement by ACSM.
1. Armstrong LE, Winant DM, Swasey PR, Seidle ME, Carter AL, Gehlsen G. Using isokinetic dynamometry to test ambulatory patients with multiple sclerosis. Phys Ther
2. Bean JF, Kiely DK, Herman S, et al. The relationship between leg power and physical performance in mobility-limited older people. J Am Geriatr Soc
3. Benedetti MG, Piperno R, Simoncini L, Bonato P, Tonini A, Giannini S. Gait abnormalities in minimally impaired multiple sclerosis patients. Mult Scler
4. Cuoco A, Callahan DM, Sayers S, Frontera WR, Bean J, Fielding RA. Impact of muscle power and force on gait speed in disabled older men and women. J Gerontol A Biol Sci Med Sci
5. DeBolt LS, McCubbin JA. The effects of home-based resistance exercise on balance
, power, and mobility in adults with multiple sclerosis. Arch Phys Med Rehabil
6. Edwards WT. Effect of joint stiffness on standing stability
. Gait Posture
7. Finlayson M, Guglielmello L, Liefer K. Describing and predicting the possession of assistive devices among persons with multiple sclerosis. Am J Occup Ther
8. Finlayson ML, Peterson EW, Cho CC. Risk factors for falling among people aged 45 to 90 years with multiple sclerosis. Arch Phys Med Rehabil
9. Freal JE, Kraft GH, Coryell JK. Symptomatic fatigue
in multiple sclerosis. Arch Phys Med Rehabil
10. Frzovic D, Morris ME, Vowels L. Clinical tests of standing balance
: performance of persons with multiple sclerosis. Arch Phys Med Rehabil
11. Garner DJ, Widrick JJ. Cross-bridge mechanisms of muscle weakness in multiple sclerosis. Muscle Nerve
12. Grigorova V, Ivanov I, Stambolieva K. Effect of sensory inputs alteration and central sensory disinteraction on postural sway and optokinetic reflex maintaining simultaneously body balance
. Acta Physiol Pharmacol Bulg
13. Gutierrez GM, Chow JW, Tillman MD, White LJ. Postural sway characteristics of multiple sclerosis (MS) individuals of different disability statuses. Med Sci Sports Exerc
. 2003;35(5 suppl):S232.
14. Karst GM, Venema DM, Roehrs TG, Tyler AE. Center of pressure
measures during standing tasks in minimally impaired persons with multiple sclerosis. J Neurol Phys Ther
15. Kent-Braun JA, Ng AV, Castro M, et al. Strength, skeletal muscle
composition, and enzyme activity in multiple sclerosis. J Appl Physiol
16. Kent-Braun JA, Sharma KR, Miller RG, Weiner MW. Postexercise phosphocreatine resynthesis is slowed in multiple sclerosis. Muscle Nerve
17. Kent-Braun JA, Sharma KR, Weiner MW, Miller RG. Effects of exercise on muscle activation and metabolism in multiple sclerosis. Muscle Nerve
18. Krupp LB, LaRocca NG, Muir-Nash J, Steinberg AD. The Fatigue
Severity Scale: application to patients with multiple sclerosis and systemic lupus erythematosus. Arch Neurol
19. Krupp LB, Alvarez LA, LaRocca NG, Scheinberg LC. Fatigue
in multiple sclerosis. Arch Neurol
20. Kurtzke JF. Rating neurologic impairment in multiple sclerosis: an Expanded Disability Status Scale (EDSS). Neurology
21. Lambert CP, Archer RL, Evans WJ. Muscle strength and fatigue
during isokinetic exercise in individuals with multiple sclerosis. Med Sci Sports Exerc
22. Lanzetta D, Cattaneo D, Pellegatta D, Cardini R. Trunk control in unstable sitting posture during functional activities in healthy subjects and patients with multiple sclerosis. Arch Phys Med Rehabil
23. Liu MQ, Anderson FC, Pandy MG, Delp SL. Muscles that support the body also modulate forward progression during walking. J Biomech
24. Marigold DS, Eng JJ, Tokuno CD, Donnelly CA. Contribution of muscle strength and integration of afferent input to postural instability in persons with stroke. Neurorehabil Neural Repair
25. Morris ME, Cantwell C, Vowels L, Dodd K. Changes in gait and fatigue
from morning to afternoon in people with multiple sclerosis. J Neurol Neurosurg Psychiatry
26. Nallegowda M, Singh U, Handa G, et al. Role of sensory input and muscle strength in maintenance of balance
, gait, and posture in Parkinson's disease: a pilot study. Am J Phys Med Rehabil
27. Nelson SR, Di Fabio RP, Anderson JH. Vestibular and sensory interaction deficits assessed by dynamic platform posturography in patients with multiple sclerosis. Ann Otol Rhinol Laryngol
28. Ng AV, Miller RG, Gelinas D, Kent-Braun JA. Functional relationships of central and peripheral muscle alterations in multiple sclerosis. Muscle Nerve
29. Ng AV, Miller RG, Kent-Braun JA. Central motor drive is increased during voluntary muscle contractions in multiple sclerosis. Muscle Nerve
30. Olgiati R, Burgunder JM, Mumenthaler M. Increased energy cost of walking in multiple sclerosis: effect of spasticity, ataxia, and weakness. Arch Phys Med Rehabil
31. Ponichtera JA. Concentric and eccentric isokinetic lower extremity strength in multiple sclerosis and able-bodied. J Orthop Sports Phys Ther
32. Rice CL, Vollmer TL, Bigland-Ritchie B. Neuromuscular responses of patients with multiple sclerosis. Muscle Nerve
33. Schwid SR, Covington M, Segal BM, Goodman AD. Fatigue
in multiple sclerosis: current understanding and future directions. J Rehabil Res Dev
34. Schwid SR, Thornton CA, Pandya S, et al. Quantitative assessment of motor fatigue
and strength in MS. Neurology
35. Scott PJ, Huskisson EC. Measurement of functional capacity with visual analogue scales. Rheumatol Rehabil
36. Sheean GL, Murray NM, Rothwell JC, Miller DH, Thompson AJ. An electrophysiological study of the mechanism of fatigue
in multiple sclerosis. Brain
. 1997;120(Pt 2):299-315.
37. Soyuer F, Mirza M, Erkorkmaz U. Balance
performance in three forms of multiple sclerosis. Neurol Res
38. Thoumie P, Mevellec E. Relation between walking speed and muscle strength is affected by somatosensory loss in multiple sclerosis. J Neurol Neurosurg Psychiatry
39. Thoumie P, Lamotte D, Cantalloube S, Faucher M, Amarenco G. Motor determinants of gait in 100 ambulatory patients with multiple sclerosis. Mult Scler
40. van Wegen EE, van Emmerik RE, Wagenaar RC, Ellis T. Stability
boundaries and lateral postural control in Parkinson's disease. Motor Control
41. White LJ, McCoy SC, Castellano V, et al. Resistance training improves strength and functional capacity in persons with multiple sclerosis. Mult Scler
42. Winter DA, Patla AE, Frank JS, Walt SE. Biomechanical walking pattern changes in the fit and healthy elderly. Phys Ther
43. Winter DA, Prince F, Frank JS, Powell C, Zabjek KF. Unified theory regarding A/P and M/L balance
in quiet stance. J Neurophysiol
Keywords:©2008The American College of Sports Medicine
SKELETAL MUSCLE; BALANCE; FATIGUE; STABILITY; CENTER OF PRESSURE