Research Report

The Effect of Electrical Stimulation on Quadriceps Femoris Muscle Torque in Children with Spina Bifida

The effects of neuromuscular electrical stimulation (NMES) on the torque production of the quadncepsfemonk muscles were examined in five children with spina bzJida. Two male subjects, aged 5 and 12 years, and three female subjects, aged 5, 12, and 21 years, participated in the study. Suqace stimulation was applied to the quudricepsfemons muscles of one lower extremityfor 30 minutes each day over an 8-week period. At 0, 4, and 8 weeks, muximum isometric voluntary knee extension torques were measured for both control and stimulated lower extremities with a dynamometer at 0, 15,30, 45, and 60 degrees of knee Jm'on. The three oldest subjects had torque measurements of acceptable reliability (intraclass cowelation coeficient B.72). Two of these three subjects also had signiJcant increases in the torque produced by the stimulated limb relative to the torque produced by the control limb. The data were unreliablefrom the two youngest subjects. Completion timesfor finctional tasks (walking and step ascemion/descension)were also recorded before and a)er the 8 weeks of stimulation. The completion times were lower following stimulation for four subjects. [Karmel-RossY Cooperman DR, Van Dorm CL. The effect of electrical stimulation on quadncepsfemoris muscle torque in children with spina biJda. Phys Ther. 1992;72:723-730.1

Karen Karmel-Ross Danlel R Cooperman Clayton L Van Doren

Key Words: Function, Neuromuscular electncal stimulation, Pedia~~cs, Spina biJida, Torque.

Spina bifida is a complex disorder that occurs in 1 per 1,000 live births in the United States.' In spina bifida, the spinal cord and vertebrae are malformed, usually leaving the lower limbs partially or completely paralyzed.' As a result, 30% of those with spina bifida use a wheelchair alone to

ambulate, 20% use a wheelchair frequently, 20% ambulate with crutches and braces or braces alone, and only 30% walk without any assistive devices.' Quadriceps femoris muscle strength generally determines the extent of orthotic support and the type of ambulatory aid needed by a

K Karmel-Ross, FT,is Pediatric Clinical Specialist, Depanment of Rehabilitation Services, University Hospitals of Cleveland, 2074 Abington Rd, Cleveland, OH 44106-9961 (USA). Address all correspondence to Ms Karmel-Ross. ~

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DR Cooperman, MD, is Assistant Professor of Onhopaedics, Case Western Reserve University, University Hospitals of Cleveland. CL Van Doren, PhD, is Assistant Professor of Onhopaedics, Case Western Reserve University, University Hospitals of Cleveland. This research was Funded by the Young Investigator Research Grant supported by the Rainbow Babies and Childrens Hospital Board Trustees. The study protocol was approved by the Universicy Hospitals of Cleveland Institutional Review Board for Human Investigation.

of

child with spina bifida.2.3 Poor quadriceps femoris muscle strength and endurance adversely affect ambulation. One potential method for strengthening the quadriceps femoris muscles and thereby improving ambulation is the application of neuromuscular electrical stimulation (NMES). Over the last 15 years, research has shown that NMES is useful in strengthening the muscles of people with spinal cord injury." Peckham et ale investigated the force and fatigability of skeletal muscle in . people with quadri. plegia following exercise by chronic electrical stimulation. They concluded that electrical stimulation altered the contractile properties of muscle toward a state usable for func-

induced

This article was submitted Janualy 14, 1992, and was accepted June 10, 1992,

42 /723

Physical Therapy/Volume 72, Number 10/0ctober 1992

Table 1.

subject Informution

MMTa Subject No.

Sex

1

M

2

3

Age (y)

Left

Rlght

Orthosesb

5

Fair

Fairt

Bilateral AFOs with contoured sole plates; Lofstrand crutches for walking >10 minutes

F

5

Fair+'

Good

Bilateral AFOs with contoured sole plates; right AFO with femoral-condylar extensions

M

12

Fair-'

Good

Left side, floor-reaction AFO; right side, AFO with femoral-condylar extensions

4

F

12

Fair

Fair+t

None

5

F

21

Fair

Fair+t

Bilateral conventional metal orthoses with ring locks, split stirrups, and 90" plantar-flexion stops; left knee always locked with ambulation; Lofstrand crutches for walking

"MMT=prestimulation manual muscle test grade12 for strength of subject's quadriceps femoris muscles. Asterisk indicates side receiving neuromuscular electrical stimulation. b ~ lsubjects l were community ambulators.2 (AFO=ankle-foot orthosis.)

tional movements in otherwise paralyzed limbs (ie, forearm and finger flexor muscles) by increasing the muscles' strength and fatigue. Other investigators have demonstrated that NMES can induce changes in normal muscles. Laughman et a19 showed that NMES can strengthen normal quadriceps femoris muscles without voluntary effort. SnyderMackler et all0 reported stronger quadriceps femoris muscles and more normal gait patterns in patients who received NMES and volitional exercise after antt:rior cruciate ligament reconstruction compared with patients who performed volitional exercise alone. Mazliah et alu conducted a pilot study of three children with spina bifida to investigate the effects of NMES on the torque produced by the quadriceps femoris ~nusclesin relation to decreasing knee flexion contractures. Surface stimulation was applied bilaterally to the quadriceps femoris muscles for :L to 2 hours per day over a 6-month period. The subjects were seated during stimulation, and con-

tractions were isometric. The results varied considerably across subjects. One subject showed no changes in thigh girth o r maximal voluntary torque. Another subject showed no changes for one limb, but had a 3-cm increase in girth and a 44% increase in torque in the other limb. The third subject had no change in girth, but did have increased torques in both limbs. The results from the study by Mazliah et all1 are variable, but suggest that NMES may enhance the strength of the quadriceps femoris muscles in children with spina bifida. The purpose of our study was to measure the effects of NMES on both quadriceps femoris muscle strength and functional tasks in a similar group of subjects, using unilateral stimulation over an 8-week period.

Method

Two male subjects, aged 5 and 12 years, and three female subjects, aged

'Medical-Surgical Division/3M, 3M Center, St Paul, MN 55144-1000.

Physical Therapy /Volume 72, Number 10/0ctober 1992

5, 12, and 21 years, participated in the study. All subjects had lesions at the L2-3 spinal cord level and had at least a Fair strength grade of the quadriceps femoris muscles bilaterally when tested using the manual muscle test (MMT) as described by Kendall and McCreary.lz There is no muscle activity below the knee in individuals with lesions at the L2-3 level.lJ3 All subjects were community ambulators; that is, they can walk indoors and outdoors for most of their activities and may need crutches o r braces, o r both. They use a wheelchair only for .~ long trips out of the c o m m ~ n i t yThe adult participant and the parents of the four minors signed informed consent forms. The subject information is summarized in Table l .

The stimulated lower limb was selected randomly, and the other lower limb served as the control. One pregelled 4.4x 8.9-cm (1% X 3% in) electrode* was placed proximally over the belly of the vastus lateralis and rectus femoris muscles, and a second electrode was placed distally over the rectus femoris and vastus medialis muscles superior to the patella. The long axis of each electrode was placed perpendicular to the longitudinal direction of the muscle fibers. Parents of subjects 1, 2, 3, and 4 positioned the electrodes for each use. Subject 5 applied her own electrodes. Parents and subject 5 were given written instructions with landmarks to measure from so that they could duplicate electrode placements established by the tester (KK-R). These locations were chosen such that electrical stimulation produced a Fair involuntary contraction.12Stimuli were produced with a Myocare portable neuromuscular stimulator.*The stimulator was programmed to produce rectangular, biphasic, symmetrical pulses with durations of 347 microseconds per phase; a maximum current of 50 mA delivered at 35 pulses per second; and a 2-second up ramp and 5-second down ramp. The odoff times varied over the duration of the study, from 1:3 (8 seconds on, excluding the ramp times; 24 seconds off)for

structed to avoid changing their normal activities during the study.

50

.be*

3 ~qm..am.a..

Torque Measurements

.. ..-....-.. -.. .

Subject

1

0 n.

0-0

.we--.

owe..

amamamamaD .am

C L

5

50

*am a# a8

. .." am.

O..aa

a-

-amwe

.-a

0..

3

4

0 .Current

Week

8

V Torque Measurement

Flgure 1. Currents used during each 30-minute stimulation session over the expen'mental period. Each point represents the current used on I day. Occasionally, subjects would use more than one current level in a single session, resulting in two or more points on a single day. No points are plotted for days when no stimulation was used. Tbe triangles represent dates when knee extension torques were measured in the laboratoty. Subjects I and 2 had only one measurement session at the 4-week interval. Note that two subjects (subjects 3 and 4) continued beyond the nominal &week period because of scheduling conflicts. week 1 to 1:2 (8 seconds on, 16 seconds oft) for week 2 to 1:1 (8 seconds on, 8 seconds oft) for weeks 3 through 8.

(Tab. 1). Only one subject (subject 5) had braces that crossed the knee joint, and the braces were unlocked during stimulation.

The current was adjusted daily to each subject's tolerance, not as a percentage of each subject's maximal voluntary contraction. In each instance, the electrical stimulation elicited a visible, sustained muscular contraction. For 6 days each week over the 8-week period, all subjects were instructed to follow a routine of 30 minutes of stimulation while standing or moving around in an upright position using their regular orthosis

Parents kept daily journals to record the time of stimulation, current, skin integrity, and activity in which their children were engaged during stimulation. The parents described their perceptions of the quality of contractions (ie, whether the knee appeared to fully extend during stimulation or remained flexed). Subject 5, the 21-year-old, maintained her own daily journal. The subjects' current levels are illustrated in Figure 1. All subjects were in-

'universal Gym Equipment Inc, PO Box 1270, 930 27th Ave SW, Cedar Rapids, 1.4 52404.

44 / 725

The maximal knee extension torques were measured using a MERAC dynamometer,+ and all measurements were taken by one of the authors (KK-R). At the beginning of each test session, the dynamometer was calibrated in accordance with the manufacturer's guidelines. During the course of the study, subjects 1 and 2 each completed five test sessions and subjects 3, 4, and 5 each completed six test sessions. Each lower limb was tested in two ways during each session. First, the trials were performed with, at most, a 1-second rest between trials at different angles. The sequence of trials was then repeated with a 4-minute rest between trials. A 30-minute rest was allowed between the two sequences of trials. Nominally, subjects were tested 2 to 3 days apart at the same time of day. The actual test dates are shown in Figure 1. Once the NMES sessions began, testing was repeated in the same manner after approximately 4 weeks and 8 weeks of stimulation. The test schedule and length of stimulation varied according to the subjects' availability. The limb tested first was chosen randomly. Subjects thereafter were always tested with the same limb first. All subjects' braces were left on during testing, except for subiect 5. Subjects were tested in the prone position. The nontested lower limb was positioned in hip and knee extension, and the tested lower limb was positioned with the hip at 0 degrees of extension and the knee at 0, 15, 30, 45, and 60 degrees of flexion. The trunk, thigh, and ankle of the tested side were stabilized by straps to prevent position changes during contractions. The subjects were asked to sustain an isometric contraction greater than o r equal to a preset torque level of 0 newtonmeters over 5 seconds. Preliminary testing showed that a hold time of 5 seconds was necessary to accommodate variability in response times.

Physical Therapy /Volume 72, Number 10/0ctober 1992

-

Results and Discussion

Table 2. Intraclass Correlation Coeficientsa Sublect No. Week

1

2

3

4

5

"Type 2,2 b~ubjectcompleted only one test session.

Some subjects took up to 3 seconds to achieve their peak torques. The same 5-second sampling window has been used by previous investigatorsl6l6 for similar reasons. Comparison of data was based on the peak torque produced within this 5-second window. Each subject was encoura,ged repeatedly by the examiner (KK-R) to push as hard as he or she cou1.d.

Functional Tests In addition to the peak torque measurements, three timed functional tasks were assessed before and after the 8 weeks of stimulation: (1) freewalking 24.4 m (80 ft) on a level surface, (2) descending 20 steps, and (3) ascending 20 steps. All subjects wore their customary assistive devices (Tab. 1) during timed functional tasks. In free-walking, the subject was asked to walk 24.4 m as he or she normally would. ?'he tester (KK-R) started a timer and said "go," then stopped the timer when the subject crossed over a line 24.4 m from the starting line. The subject repeated this task two or three times, depending on his or her endurance. There was no rest period between trials. For step-climbing,the subject was instructed to descend and then to ;ascend 20 steps as he or she normally would. Each subject began the test by standing at the top step, holding on to the railing. The tester started the timer and said "go," then stopped the timer when the subject had both feet on the last step. The same procedure was followed for ascending the stairs. This entire cycle

was repeated twice with no rest between trials. Data Analysls To assess reliability of the torque measurements, intraclass correlation coeficients QCC[2,2])I7were calculated for each subject at 0, 4, and 8 weeks of stimulation. The ICCs were calculated using the peak torques (both rest paradigms and all five angles) from the two test sessions at 0, 4, and 8 weeks. The ICCs could not be calculated in two instances in which the second test session was not completed (week 4, subjects 1 and 2). The ICCs are listed in Table 2. No attempt was made to assess the reliability of the time measurements for the functional tasks. The data for subjects with reliable torque measurements (subjects 3, 4, and 5) were analyzed using a four-way repeated-measures analysis of variance (ANOVA) to assess the effects of the factors limb (control or stimulated), knee angle (0°, 15", 30°, 45", and 604, rest pmdigm (no wait and 4-minute wait between trials), and weeks of stimulation (0, 4, and 8 weeks) and their interactions. Note that the interaction between limb and weeks of stimulation is particularly important because it reflects any change in the relative strength of the control and stimulated limbs over time.

Physical Therapy /Volume 72, Number 10/0ctober 1 9 2

All subjects complied with the NMES protocol. The current levels for each day are shown in Figure 1, along with the dates for torque measurements. The variations from the nominal schedule were due to conflicts with the subjects' personal schedules. All subjects continued with the stimulation sessions until the final test date. As a result, all subjects received stimulation for at least 8 weeks, but as much as 10.5 weeks (subject 4). The ICCs for torque measurements for the three oldest subjects (subjects 3, 4, and 5) were calculated at 0, 4, and 8 weeks across two test sessions each and are presented in Table 2. The ICCs for subjects 4 and 5 were all greater than 90,and s u b ject 3 had only one marginal ICC QCC=.72, week 8). In contrast, the ICCs for the two 5-year-old subjects (subjects 1 and 2) were very poor at week 0 and could not be calculated at week 4 because the two subjects did not complete two test sessions. Their ICCs were marginal at week 8 QCCs =.58 and .78, respectively). The torque measurements from both stimulated and control limbs are plotted as functions of knee angle in Figure 2 (no rest between trials) and Figure 3 (4-minute rest between trials) for each subject. Each point represents the average of two torque measurements from pairs of test sessions, except in those instances in which only one session was completed. Subjects 1 and 2 were much weaker than subjects 3, 4, and 5 for either the stimulated or the control limb. Subjects 1 and 2 showed little change in torque with knee angle, whereas the other three subjects showed pronounced angle effects. The relative strengths of the stimulated and control limbs changed for subjects 4 and 5 over the 8-week stimulation period. For both subjects, the stimulated limb was weaker than the control limb at week 0. By week 8, however, the situation was reversed-the stimulated limb was the stronger of the two limbs. There was

726 / 45

WEEK 0

ent torque-angle relations for both lower extremities, as indicated by the significant interaction between the knee angle and limb factors (P< .01).

WEEK 8

WEEK 4

ldJ-!eL ;;ppp "LL~

The most interesting effect, however, was the interaction between limb and weeks of stimulation. For subjects 4 and 5, this interaction was significant (P