2001 a Focused Exercise Regimen Improves Clinical Measures of Balance in Patients With Peripheral...

8/9/2019 2001 a Focused Exercise Regimen Improves Clinical Measures of Balance in Patients With Peripheral Neuropathy

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A Focused Exercise Regimen Improves Clinical Measures of Balance in Patients With Peripheral Neuropathy

James K. Richardson, MD, David Sandman, BS, Steve Vela, BS

ABSTRACT. Richardson JK, Sandman D, Vela S. A fo-cused exercise regimen improves clinical measures of balancein patients with peripheral neuropathy. Arch Phys Med Rehabil2001;82:205-9.

Objective: To determine the effect of a specific exerciseregimen on clinical measures of postural stability and confi-dence in a population with peripheral neuropathy (PN).

Design: Prospective, controlled, single blind study.Setting: Outpatient clinic of a university hospital.Participants: Twenty subjects with diabetes mellitus and

electrodiagnostically confirmed PN.Intervention: Ten subjects underwent a 3-week intervention

exercise regimen designed to increase rapidly available distalstrength and balance. The other 10 subjects performed a controlexercise regimen.

Main Outcome Measures: Unipedal stance time, functionalreach, tandem stance time, and score on the activities-specificbalance and confidence (ABC) scale.

Results: The intervention subjects, but not the control subjects, showed significant improvement in all 3 clinical mea-sures of balance and nonsignificant improvement on the ABCscale.

Conclusion: A brief, specific exercise regimen improvedclinical measures of balance in patients with diabetic PN.Further studies are needed to determine if this result translatesinto a lower fall frequency in this high-risk population.

Key Words: Balance; Diabetes mellitus; Exercise; Periph-eral nervous system diseases; Rehabilitation.

© 2001 by the American Congress of Rehabilitation Medi-cine and the American Academy of Physical Medicine and

Rehabilitation

IN PREVIOUS WORK,1,2 we found that older persons withperipheral neuropathy (PN) are at a markedly increased risk

for falls when compared with older persons with healthy pe-ripheral nerves. This postural instability was confirmed in thelaboratory setting. Subjects with PN balanced less reliably on 1foot for 3 seconds than did matched control subjects withoutPN.3 In addition, a decreased unipedal stance time amongpersons with PN has, in 2 separate studies, been associated witha history of falls over the previous year.2,4 It has also beennoted that diabetic subjects with PN, as identified by decreased

distal vibratory thresholds, were 15 times more likely to reportan injury from a fall than a control diabetic group.5 Further-more, PN is common among older persons, particularly thosewith diabetes mellitus. Among people over 60 with type 2diabetes mellitus, the prevalence of PN is greater than 50%.6

Taken together, the data suggest that PN is common amongolder persons and markedly increases their fall risk.

We have identified specific, distal sensory and motor impair-ments in older persons with PN that appear to underlie theirpostural instability. The sensory impairments identified areincreases in ankle inversion and eversion proprioceptivethresholds, which are about 5 times greater in older personswith PN compared with older persons without PN (1.46° vs0.3°).7 As a result, older persons with PN are likely less able toperceive ground irregularities and subtle shifts in their centersof mass, and are, therefore, predisposed to falls. More recently,

we8 identified a distal motor impairment about the ankle inwomen who had PN and diabetes. These women showed asignificantly decreased ankle rate of torque development com-pared with the age-matched women with diabetes but no PN(78.2 50.8N m/s vs 152.7 54.6N m/s, p .016). Asecond outcome was the ability to recover balance on 1 footwhen released from a lateral leaning posture (quantified as apercentage of foot width). Three of the 6 women with diabetesbut no PN were able to recover from a 5% lean, whereas noneof the women with PN was able to recover her balance ( p .083). These findings suggest that older women with diabetesand PN have impaired ability to rapidly develop torque at theankle, which has an impact on balance.

It is not known if an exercise regimen will improve thebalance impairments identified in older persons with PN.

Therefore, our primary hypothesis was that older persons withPN who perform an exercise regimen designed to increaserapidly available ankle strength would show improved balance,as reflected by increased functional reach, as well as tandemand unipedal stance times, compared with those who perform acontrol exercise regimen. Our secondary hypothesis was thatsubjects who performed the intervention exercises would showgreater confidence, on a validated scale, in their mobility skills(vs the control group).

METHODS

Subjects

The study was approved by the institution’s review board.All subjects gave written and verbal consent.

Inclusion criteria included: (1) being between 50 and 80years old; (2) a known history of diabetes mellitus treated bydiet, oral hypoglycemic, or insulin therapy; (3) lower extremitysymptoms consistent with PN; (4) ability to walk householddistances without assistance or an assistive device (thoughsubjects may use a cane intermittently in the community); (5)willingness to participate in the study; (6) strength of ankledorsiflexors, invertors, and evertors at least antigravity (grade 3or greater by manual muscle testing); and (7) conclusive elec-trodiagnostic evidence of a diffuse, primarily axonal, periph-eral polyneuropathy as evidenced by:

From the Department of Physical Medicine and Rehabilitation (Richardson), Uni-versity of Michigan (Sandman, Vela), Ann Arbor, MI.Accepted in revised form May 23, 2000.Supported by the University of Michigan Department of Physical Medicine, Public

Health Service (grant no. AG-08808), and the University of Michigan GeriatricsResearch and Training Center.

No commercial party having a direct financial interest in the results of the researchsupporting this article has or will confer a benefit upon the authors or upon anyorganization with which the authors are associated.

Reprint requests to James K. Richardson, Dept of Physical Medicine and Rehabil-itation, 1500 E Medical Center Dr, D5200, University of Michigan Health Systems,Ann Arbor, MI 48109-0718, e-mail: [email protected].

0003-9993/01/8201-6014$35.00/0doi:10.1053/apmr.2001.19742

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Arch Phys Med Rehabil Vol 82, February 2001



(a) sural response: absent or decreased amplitude (6V)with a normal or minimally prolonged distal latency(5ms) stimulating 14cm from the recording site pos-terior to the lateral malleolus.9 If the sural response wasabsent bilaterally, the motor responses were not per-formed.

(b) peroneal or tibial responses: absent or decreased in am-plitude (2mV for peroneal, 3mV for tibial) with anormal distal latency (6.2ms stimulating 9 and 8cm

from recording sites over the extensor digitorum brevisand abductor hallicus muscles, respectively).9

Exclusion criteria included: (1) a history or evidence onphysical examination of significant central nervous systemdysfunction (ie, hemiparesis, myelopathy, cerebellar ataxia);(2) significant musculoskeletal deformity (ie, amputation, sco-liosis, abnormality of range of motion [ROM]) that wouldprevent participation (90° of humeral abduction, inability togrip, 10° of combined ankle inversion/eversion); (3) lowerextremity arthritis or pain that limits standing or weight-bear-ing exercise; (4) electrodiagnostic evidence of any diagnosisother than PN; (5) a history or evidence on physical examina-tion of vestibular dysfunction; (6) a history of angina or angina-equivalent symptoms (ie, nausea, diaphoresis, shortness of breath with exercise); (7) symptomatic postural hypotension

(postural lightheadedness that interferes with standing for5min); and (8) a history or evidence on physical examination of plantar skin pressure ulcer.

The subjects also were evaluated by using the MichiganDiabetes Neuropathy Score (MDNS).10 This is a 46-point scale(0–46, with higher score reflecting more severe PN) that hasbeen shown to correlate well with more extensive neuropathystaging scales. The scale includes muscle stretch reflexes at thebiceps, triceps, patella, and Achilles; pinprick sensation at thegreat toe; ability to perceive the touch of a 10-gram monofil-ament; ability to perceive a 128Hz tuning fork at the great toe;strength of hand dorsal interossei; great toe extension; andankle dorsiflexion. The first 10 subjects recruited were placedin the intervention group, and the next 10 subjects were placedin the control group.

Intervention ExercisesThe exercise interventions, performed daily on a firm surface

for 3 weeks, included:(1) Warm up (open chain active ankle ROM exercises).

Subjects wrote the alphabet in the air with each foot bymoving the ankle.

(2) Bipedal toe raises and heel raises (lifting the forefoot asone does to balance on a heel). Subjects did these asquickly as possible, using support as necessary. Subjectsstarted with 1 set of 10 and increased by 1 set every 5exercise sessions for a total of 3 sets.

(3) Bipedal inversion and eversion. In this exercise, subjects’ center of mass was shifted laterally as subjectsstrengthened ankle invertors and evertors via closedchain exercises. The goal was to do so without using the

upper extremities, but support was used as necessary.Subjects started with 10 repetitions in each direction andincreased to 2 sets of 10 repetitions after 5 exercisesessions.

(4) Unipedal toe raises and heel raises. Again, subjectsattempted to perform this quickly—even if that was notpossible. Subjects started with 5 repetitions of eachexercise and increased to 10 repetitions after 5 exercisesand then to 2 sets of 10 after 10 exercise sessions.

(5) Unipedal inversion and eversion. Subjects inverted andeverted the foot while standing on it to challenge balance

and to create a closed chain exercise of the ankle inver-tors and evertors. It was anticipated that most subjectswould find this task challenging and so they used theirhands for balance when needed. Subjects started with 1set of 5 repetitions in each direction and increased to 10repetitions after 5 exercise sessions.

(6) Wall slides. Subjects started with bipedal slides withknee flexion maximum of about 45°. They performed 3sets of 10. After 5 exercise sessions the first set was

performed on each foot.(7) Unipedal balance for time. Three tries on each foot.

Control Exercises

The control exercise regimen was performed in a seatedposition. Subjects performed neck flexion and rotation stretch-ing with eyes open and then closed. They then used a resistanceband to perform strengthening exercises for the scapular ab-ductors, shoulder external rotators, and elbow flexors. Theexercises were performed 5 or more times (if tolerated) perweek for 3 weeks. Control exercises were suggested at aslightly decreased frequency because of concern that theymight lead to an overuse injury, which was not felt to be anethical risk from a control intervention.

OutcomesAll subjects underwent 3 trials of tandem stance, functional

reach, and unipedal stance before and after their exerciseprograms. Tandem stance, functional reach, and unipedalstance were performed and graded as described else-where.2,11,12 In addition, all subjects filled out the activities-specific balance confidence (ABC) scale13 before and after theexercise regimen. The ABC scale lists 16 activities (eg, walk-ing up and down stairs, walking on an icy sidewalk) andsubjects describe their degree of confidence in performing eachactivity, on a scale from 0% (no confidence) to 100% (com-plete confidence). All subjects were evaluated before and aftertheir 3-week exercise programs by the same examiner (DS).

Statistical Analysis

A paired, 2-tailed t test was used to detect significantchanges in tandem stance, functional reach, and unipedalstance. A p value of less than .05 was considered significantand a p value of .05 or greater and less than .10 was considereda trend. A 2-tailed t test was also used for evaluating theresponses to the 16 activities on the ABC scale; however, tocompensate for making multiple comparisons, p less than .0125was considered significant and p .125 or greater and less than.025 was considered a trend.

RESULTS

Nine of the 10 intervention subjects and 7 of the 10 controlsubjects completed the study. The intervention subject droppedout because of foot-ankle pain, which was attributed to theexercise regimen aggravating an underlying arthritis. One of

the 3 control subjects developed an illness and 2 dropped outwithout specifying a reason. Subject characteristics of genderand age are listed in table 1. There was a trend toward anincreased MDNS score, representing more severe PN, amongthe intervention subjects compared with the control subjects(table 1). There was no significant difference between inter-vention and control subjects’ sural, peroneal motor, or tibialmotor response amplitudes.

The 2 groups showed grossly similar baseline values fortandem stance and functional reach. The shorter unipedalstance time at baseline in the intervention group, compared

206 NEUROPATHY, BALANCE, AND EXERCISE, Richardson




with the control group ( p .11), was consistent with the trendtoward an increased MDNS score in the intervention group;however, none of the baseline differences was significant. Theintervention subjects showed a significant improvement in all 3outcomes after the exercise regimen (table 2). In contrast, thecontrol subjects showed insignificant improvements in tandemstance and functional reach, and an insignificant decrease inunipedal stance time (table 2).

The intervention and control groups showed nearly identicalinitial composite confidence scores (table 3). Although theintervention group reported improved confidence, as reflectedby a greater composite ABC score postintervention, the differ-ence was not significant. There was no significant change in thecontrol group confidence scores. When confidence scores forisolated activities were considered, there was a trend towardthe intervention subjects reporting greater confidence in climb-ing and descending stairs after the intervention exercises (table3). The intervention group also reported a 10% or greaterimprovement in confidence for 3 other activities (bending overto pick up an object, standing on tip toes to reach overhead,walking on icy sidewalks), but the changes were not signifi-cant. The control group showed no significant changes or

trends toward a change after their exercise program. There wasa change of 10% toward greater confidence among the controlgroup for bending over to pick up an object.

DISCUSSION

The data from this study showed that an exercise regimendesigned to increase rapidly available ankle strength improved3 commonly used clinical measures of balance (functionalreach, tandem stance, unipedal stance) among older personswith mild to moderate PN. The study further showed that theseimprovements develop in a relatively short period of time andthat the exercise regimen is well tolerated. The data alsosuggested, but did not confirm, that the exercise regimen isassociated with improvements in subjects’ confidence in theirabilities to perform daily tasks that challenge balance.

There was evidence to suggest that exercise is a reasonableintervention, even in those with predominantly sensory PN.Aside from our study, which showed impaired ankle rate of torque development among subjects with clinically normalankle strength,8 other work suggests that patients with clini-cally mild or sensory-only PN likely have motor impairmentsabout the ankle. In an electrophysiologic study14 of subjectsselected for clinical evidence of sensory-only PN, most subjects (70%) had abnormalities during needle electromyographyof the anterior tibialis or medial gastrocnemius muscles, bothof which provide torque to the ankle. Those investigators14

concluded that “subclinical motor involvement is often de-tected on electrophysiologic studies in patients . . . who haveonly sensory signs.” Also, there is evidence in animal models15

and in humans16 that the number of type II muscle fibers notonly decreases with age, but that there is a preferential loss of type II motor units in the setting of denervation, particularlydistal denervation.17 Therefore, it appears likely that a gener-alized PN, even among patients with predominantly sensoryfindings, is associated with motor deficits characterized by

decreased rapidly available torque at the ankle. This impair-ment, though important for postural stability under challengingcircumstances, is likely difficult or impossible to detect onroutine physical examination and, therefore, remains subclini-cal.

Because functional reach and tandem stance were not part of the intervention exercise regimen, improvement in these out-comes suggests that some change occurred beyond a practiceeffect. It is possible that the intervention subjects increasedtheir ankle strength in response to the exercise regimen. Brownet al18 found that type II muscle fiber concentration signifi-cantly increased in older persons undergoing rigorous strength-ening programs. The intervention applied in our study wasdesigned to increase rapidly available torque about the ankle19

and recruit type II motor units.20 Brown18 tested the biceps, a

proximal upper extremity muscle, and, therefore, their findingsmay not apply to distal lower extremity muscles, which werethe target of strengthening in our study. Another mechanism of strengthening is possible. Early strength gains appear to berelated to neural changes—possibly improved synchronizationof motor units—rather than muscle hypertrophy.21 Strengthen-ing has, therefore, been found to occur in response to exercisein diseases such as hereditary motor and sensory neuropathytypes I and II22 and postpoliomyelitis syndrome,23 which de-crease available motor units in a manner similar to that of ageneralized PN. Given the brevity of the exercise intervention,any strengthening that occurred in the intervention group wasmore likely related to a synchronization of motor units ratherthan muscle hypertrophy.

An isolated improvement in the strength of the ankle mus-culature would likely be sufficient to lead to the improvementsnoted in this study. Others have found that increased musclestrength among older subjects was an independent predictor of a decreased risk for loss of balance during a difficult test of balance that reduced proprioceptive input, a condition thatmimics the patient with PN.24 Wolfson et al25 emphasized thestrong association between falls/loss of balance and decreasedankle strength among nursing home residents. However, animprovement in ankle muscle strength, and, therefore, muscletension, may also improve ankle proprioceptive thresholds. In

Table 2: Change in Clinical Measures of BalancePre- and Postexercise

Preexercise Postexercise p *

Intervention Group

Tandem stance (s) 17.5 13.4 23.5 10.9 .004

Functional reach (in) 10.5 2.1 11.5 2.2 .0012

Unipedal stance (s) 5.4 4.7 11.6 10.2 .0014

Control Group

Tandem stance (s) 19.0 11.8 22.0 12.0 .13

Functional reach (in) 11.3 3.6 11.9 2.8 .23

Unipedal stance (s) 9.3 8.6 7.9 5.9 .33

NOTE. Values presented as mean SD.* Two-tailed t test.

Table 1: Clinical Characteristics of Subjects

Intervention Group

(n 9)

Control Group

(n 7) p

Age (yr) (mean SD) 64.0 6.3 63.3 7.6 NS

Gender (% men) 8 (89%) 4 (57%) NS

MDNS score (SD)* 18.6 5.3 11.9 3.0 .060†

Response amplitudes

Sural (V) .25 .79 .15 .47 .34

Peroneal motor (mV) .57 .63 .33 .43 .11

Tibial motor (mV) .18 .33 .50 1.1 .27

Abbreviation: NS, not significant.* MDNS scores: higher score more severe neuropathy (maxi-mum 46).† Represents a trend toward more severe neuropathy in the inter-vention group versus the control group.

207NEUROPATHY, BALANCE, AND EXERCISE, Richardson




another study, perception of ankle plantar- and dorsiflexionimproved markedly when the calf musculature was tested un-der tension compared with when the musculature was re-laxed.26

Among the present study’s strengths is the careful subjectselection, using electrodiagnostic criteria to confirm the pres-ence of PN, and the use of a control group with a controlexercise regimen. In addition, the outcomes are thought to have

clinical meaning; impairments in 2 of the 3 outcomes—unipe-dal stance and functional reach—have been associated withinjurious falls.12,27 Our study was well controlled, with thecontrol subjects receiving attention equivalent to the interven-tion group. In addition, the control subjects showed their great-est improvement on the ABC scale for a task involving grosshead motion, similar to some of their exercises, suggesting thepossibility that those subjects found the control exercisesmeaningful.

Our study’s greatest limitation was its design: it was notdouble-blind. Although the tests were administered as objec-tively as possible, bias is possible. This seems less likely forunipedal stance, which requires little judgment on the examin-er’s part. The decreased MDNS score and increased unipedalstance time of the control subjects1 preexercise suggests that

they had less severe PN than the intervention subjects. How-ever, the control subjects still had much room to improve—particularly in tandem and unipedal stance—so that a ceilingeffect does not appear to be an explanation for their lack of improvement. Although the subjects were carefully selectedand had similar baseline characteristics, the relatively smallnumbers diminish the strength of the conclusions. A largerstudy is planned to confirm the findings of our work. A lastconcern is that most subjects were men. Therefore, translatingthese results to women should be performed with caution.

CONCLUSION

A brief, intense exercise regimen designed to improve distallower extremity strength was well tolerated and improved 3clinical parameters of balance in a group of older persons with

PN. Although increased confidence or distal lower extremitystrength may be responsible for these findings, the study pro-vided no clear insight into the mechanism of the improvementsseen in the intervention group. Whether the improvements inclinical balance noted in the intervention subjects translate intodecreased fall risk in daily life is unknown. However, given theminimal risk from the intervention exercises and the magnitudeof the benefit from preventing falls in the population studied, itappears reasonable for clinicians to consider prescribing theseexercises for their patients with postural instability causedby PN.

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Table 3: Change in Subject Responses on the ABC Scale

Intervention Group Control Group

Before After p Before After p

Question 2* 70 28 83 16 .022† 76 14 81 21 .36

Question 3 81 24 93 9 .093 76 29 86 18 .11

Question 5 78 26 90 13 .093 77 30 76 28 .36

Question 16 51 38 67 32 .048 60 36 62 32 .45

Mean of all questions 80 21 88 11 .14 80 21 80 20 .64

NOTE. Values presented as %, in mean SD.* 100% complete confidence for activity; 0% no confidence for activity. See text for activities.† Represents a trend toward intervention subjects reporting greater confidence after the exercise regimen.

208 NEUROPATHY, BALANCE, AND EXERCISE, Richardson




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209NEUROPATHY, BALANCE, AND EXERCISE, Richardson


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