1531
Increasing Muscle Mass in Spinal Cord Injured Persons
With a FUnctional Electrical Stimulation Exercise Program
A.M. Erika Scremin, MD, Lyvia Kurta, PT, Amilcare Gentili, MD, Barbara Wiseman, BSc, Karen Perell, PhD,
Charles Kunkel, ~ID, Oscar U. Scremin, MD, PhD
ABSTRACT. Scremin AME, Kurta L, Gentili A, Wiseman B,
Perell K, Kunkel C, Scremin OU. Increasing muscle mass in
spinal cord injured persons with a functional electrical stimulation
exercise program. Arch Phys Med Rehabil 1999;80:1531-6.
Objective: To determine the magnitude of changes in muscle
mass and lower extremity body composition that could be
induced with a regular regimen of functional electrical stimula-
tion (FES)-induced lower-extremity cycling, as well as the
distribution of changes in muscle mass among the thigh
muscles in personslwith spinal cord injury (SCI).
Study Design: Thirteen men with neurologically complete
motor sensory SCI!underwent a 3-phase, FES-induced, ergom-
etry exercise program: phase 1, quadriceps strengthening; phase
2, progressive sequential stimulation to achieve a rhythmic
pedaling motion (sOrface electrodes placed over the quadriceps,
hamstrings, and gl~teal muscles); phase 3, FES-induced cycling
for 30 minutes. Participants moved from one phase to the next
when they met the bbjectives for the current phase.
Measures: Computed tomography of legs to assess muscle
cross-sectional arda and proportion of muscle and adipose
tissue. Scans were [done at baseline (before subjects started the
program), at first follow-up, typically after 6 5 . 4 _+ 5.6 (SD)
weekly sessions, and at second follow-up, typically after 98.1 _+
9.1 sessions.
Results: Increases in cross-sectional areas were found in the
following musclesi rectus femoris (31%, p < .001), sartorius
(22%, p < .025), adductor magnus-hamstrings (26%, p < .001),
vastus lateralis (39%, p = .001), vastus medialis-intermedius
(31%, p = .025). Gross-sectional area of adductor longus and
gracilis muscles di~t not change. The ratio of muscle to adipose
tissue increased significantly in thighs and calves. There was no
correlation among the total number of exercise sessions and the
magnitude of musdle hypertrophy.
Conclusions: Muscle cross-sectional area and the muscle to
adipose tissue ratio of the lower extremities increased during a
regular regimen of 2.3 FES-induced lower extremity cycling
sessions weekly. The distribution of changes was related to the
proximity of muscles to the stimulating electrodes.
© 1999 by the American Congress of Rehabilitation Medi-
cine and the Am&ican Academy of Physical Medicine and
Rehabilitation
i
i
From the Department o~ Physical Medicine and Rehabilitation (Dr. A. Scremin, Ms.
/ subluxation, presence of plates, screws, or pins in femurs,
Kurta.Ms. Wiseman,Dr. Perell)and ResearchDepartment(Dr.O. Scremin),WestLos
AngelesVeteransAffairsMedicalCenter, and the Departmentof Medicine(Dr. A.
Scremin)and Departmen~of Physiology(Dr.O. Scremin),Universityof Californiaat
Los AngelesSchoolof Medicine,Los Angeles,CA; and the AlbuquerqueVeterans
AffairsMedicalCenter.Albuquerque,NM(Dr.Kunkel).
Submittedfor publicationJanuary5, 1999.Acceptedin revisedformMay 20, 1999.
No commercialpartyhavinga directfinancialinterestin the resultsof the research
supporting this articlehas or will confer a benefit upon the authors or upon any
organizationwithwhichthe authorsare associated,
Reprintrequeststo A.rv~.ErikaScremin,MD, WestLosAngelesVAMedicalCenter,
Building115,Room319,11301 WilshireBoulevard,Los Angeles,CA90073.
© 1999 by the AmericanCongressof RehabilitationMedicineand the American
Academyof PhysicalMedicineand Rehabilitation
0003-9993/99/8012-538753.00/0
UNCTIONAL ELECTRICAL stimulation (FES) is poten-
F tially useful in the rehabilitation of patients with spinal cord
injury (SCI). Claimed benefits include improvement of contrac-
tures, neurogenic osteoporosis, deep venous thrombosis, and
edema, as well as amelioration of spasticity.l-9 Another poten-
tial use of FES is as an aid in standing and ambulation. L°-13
Many of these applications require development of adequate
muscle power, which must be preceded by at least a partial
reversal of the profound muscle atrophy that occurs at levels
below the SCI lesion.
Resistive exercise increases muscle mass in human subjects
and experimental animals. 14-21 FES has been reported to
prevent disuse atrophy of the quadriceps in able-bodied patients
after surgery. 22,2~ Baldi and colleagues 24 reported prevention of
muscle atrophy in SCI subjects by FES cycle ergometry when it
was used within 3 months after injury. Information on effects of
FES on muscle mass in long-term SCI subjects, however, is
fragmentaryfl 5,26 and the persistence of changes and the rela-
tions of these changes to the duration of FES training have not
been established.
This work was designed to test if a prolonged exercise
regime of FES-induced lower-extremity cycling (FESILEC)
could improve muscle mass, and to determine the magnitude
and distribution of the effect in the thigh and leg. We used
computed tomography (CT) of the lower extremity to evaluate
muscle cross-sectional area and the proportion of muscle to
adipose tissue, a method validated against cadaver informa-
tion 27 and the standard against which other techniques are
evaluated. 28
MATERIAL AND METHODS
Subjects
Admission criteria for the study included a neurologically
complete SCI lesion (American Spinal Injury Association
[ASIA] Impairment Scale A29), presence of spasticity, and
range of motion of hip, knee, and ankle within limits compat-
ible with safe operation of the Regys ergometer, a Characteris-
tics of the 13 men admitted to the study are summarized in table
1. All subjects gave informed consent on a protocol approved
by the Human Subjects Committee of the West Los Angeles VA
Medical Center.
Exclusion criteria were: implanted pacemaker, unhealed
lower extremity fracture, history of hip or knee dislocation or
poorly controlled autonomic dysreflexia, active heterotopic
ossification, extreme osteoporosis with positive history of
fracture, severe uncontrollable spasticity in lower extremities,
presence of pressure sores in areas of treatment, acute medical
intercurrence, recent history of alcohol abuse for which treat-
ment was recommended, cardiovascular disease, and moderate
to severe puhnonary disease. Twelve potential subjects were
excluded from the study on the basis of these criteria.
At admission to the study, subjects received a complete
physical examination and, after informed consent, the follow-
ing evaluations: x-rays of spine, hip, femur, tibia, fibula, and
Arch Phys Med Rehabil Vol 80, December 1999
1532 FES-INDUCED CYCLING TO INCREASE MUSCLE MASS, Scremin

Table 1: Patient Characteristics exercise continued until the total of 30min was accomplished.
Maximum Two subjects could only cycle without load and are listed with a
"time Since Injury Age Body Mass Training maximum training workload of 0 in table 1. In phase 3b, the
Subject Injury (yrs) Level (yrs) (kg) Workload (W) protocol was similar to 3a, except that simultaneous arm
1 14 T8 31 72.7 0
ergometry was performed. This phase was initiated after
2 3 T5 24 82.7 12.2 completion of phase 3a with at least 24 sessions of 30-minute
3 14 T6 31 64.1 12.2 cycling completed. Average durations (in weeks) of each phase
4 2 T10 36 68.2 6.1 were: phase 1, 7.5; phase 2, 8.9; phase 3a, 14.4; Phase 3b, 21.9.
5 12 T4 33 72.6 12.2 The average protocol duration (sum of all phases' average
6 4 T5-6 46 91.4 12.2 durations listed above) was 52.8 weeks.
7 8 T4-5 45 95.5 6.1
Analysis of CT Scans
8 10 T12-L1 28 63.6 24.4
9 8 T6-7 42 79.2 18.3 CT scans were performed before phase 1 began and then as
10 15 C5-6 33 63.3 6.1 close as possible to the end of phase 3a (on average, after 65
11 12 T8 25 65.6 12.2 sessions) and at midpoint within phase 3b (on average, after 98
12 19 C6-7 36 106.3 0 sessions) of FESILEC (fig 1): the first CT was done to obtain a
13 9 T6 32 61.1 12.2 baseline (pre-FESILEC) measurement before the exercise pro-
tocol started; the second CT was done when workload reached a
Mean (SD) 10.0 (5.0) 34.0 (6.9) 75.9 (14.3) 10.3 (6.8) stable level (first follow-up CT); and the third CT was done
during the maintenance regime of phase 3b (second follow-up
CT). Three CT planes perpendicular to the limb major axis were
feet; blood tests, including complete blood count, chemistry defined in the thigh. One (midthigh) was at the midpoint
panel, and hematocrit and hemoglobin levels, routine urinaly- between the anterior superior iliac spine and the knee joint line.
sis; and a resting 12-lead electrocardiogram and cardiopulmo- Two other planes were 5cm above (proximal thigh) and 5cm
nary exercise stress test by arm crank ergometry. below (distal thigh) the first plane (midthigh). Two planes were
defined in the leg. One (proximal leg) was at the point of
FESILEC Protocol maximal circumferential distance, and another (distal leg) 2cm
Patients were treated with muscle stimulation in sessions of below. Three methods quantified these images. (1) Tracing of
30 minutes' duration, performed 2.32 _+ .26 (SD) times per areas with density levels of muscle tissue in digitized CT scans
week in a Regys 1 System? Stimulation was applied with with subtraction of intramuscular areas with density levels of
carbon-filled silastic surface electrodes taped to the skin. A adipose tissue (adipose tissue-free muscle area). In this
conducting jelly was applied between the skin and the elec- analysis, the three levels in the thigh (defined above) were
trode. Stimulation parameters were as follows: pulse frequency, studied; (2) A tracing of areas with density levels of muscle
30Hz; pulse duration, 300~sec; on/off ramp duration, lsec; train tissue was done without subtraction of intramuscular fat
duration, 10sec. These parameters were controlled by a micro- (anatomical muscle area). Individual muscles were identified
processor modulating six channels of stimulation. A set of with anatomic data from Eycleshymer and Schoemaker. 3° This
sensors provided feedback on leg position to the control unit. analysis was limited to the midthigh level. (3) Semiautomatic
FESILEC was implemented in three phases. In phase 1 (muscle calculation of area occupied by muscle tissue, adipose tissue,
strengthening), stimulation was applied to the quadriceps only. and bone was done using standard software available on the GE
Three electrodes were placed across the skin surface over the Highlight Advantage CT scanner, b The range of densities used
quadriceps: a reference electrode was placed in the center; the to differentiate tissues were: adipose tissue, - 1 9 0 to - 2 0 ;
other two electrodes were active. Stimulation was applied muscle tissue, +20 to + 100; bone, +200 to +2,000. In this
sequentially between the reference and one of the active analysis three levels in the thigh and two levels in the leg
electrodes to produce 45 ° of active extension followed, during (defined above) were studied. The first two analyses were
relaxation, by passive flexion. Treatment began without load. performed after CT scan films were digitized in a Hewlett-
After completion of 45 extension/flexion sequences in two Packard Scanjet 4C/T scanner5 Images were analyzed using
consecutive sessions, l lb of external weight was added and SigmaScan Pro 4 software, d Only one operator performed each
stimulation continued until the subject was able to reproduce 45
successful extension/flexion sequences.
This procedure was repeated until the patient could lift 3 to
51bs. In phase 2 (pedaling progression to 30 minutes), stimula- Phase 0 Phase 1 Phase 2 Phase 3
tion was applied sequentially to the quadriceps, the gluteus
maximus, and the semitendinosus, long head of the biceps, and Screening Strengthening Cycling
Progression
semimembranosus, to achieve a rhythmical pedaling motion. L
Initially, subjects pedalled against 0 kilopond (kp) resistive load
for 5 minutes or as long as the subject could tolerate (up to a X-ray Quadriceps ;tart 30 minutes
30-minute maximum). This was followed until the schedule Lab Tests Strengthening Cycling Continuous
Physical Exam Cycling
was completed and then each succeeding session increased bStressTest
progressively until the subject was able to pedal for 30min in
two consecutive sessions. In phase 3a (training protocol),
subjects performed three 30-minute of FESILEC per week,
initially unloaded (0 kp). Once the patient could complete two
First
f
Second Third
CT 65.4 _+5.6 (SE) Training Sessions CT CT
consecutive 30-minute sessions at a given workload, the load
I 98.1 +-9.1 (SE) Trainiug Sessions
I I|
was increased by 6.1W (l/8kp). If during the training session
the patient fatigued (ie, revolutions per minutes decreased to
<35), then the workload was reduced to the previous level and Fig 1. FESILEC training protocol and timing of CT measurements.

Arch Phys Med Rehabil Vol 80, December 1999

 FES-INDUCED CYCLING TO INCREASE MUSCLE MASS, Scremin 1533

methodology, and this person was blind to the treatment and to

subject identity. Not all the subjects were included in all three
analysis methods because some of the software was not
available in the initial stages of the study and some of the CT
scans had characteristics that did not permit anatomic delinea-
tion of the individual muscles.

Statistical Analysis
Ratios of cross4sectional area of the first and second fol-
low-up CT scans and that of baseline (pre-FESILEC) were
calculated to cancel out the variance between subjects. Statisti-
cal significance of[ these ratios against l were calculated from
the t distribution. A Bonferroni correction for two simultaneous
contrasts (first arid second intervals against baseline) was
applied to the perbentage increases in anterior and posterior
muscle mass. Sta[istical significance of differences was as-
sumed for probapilities <.05. Results were presented as
percentage of baseline (ratio × 100).

RESULTS
100%
Initial analysis !indicated that there were no statistically
significant side to :side differences within individual subjects;
therefore, cross-sectional areas from both sides were averaged
for each subject.
Cross-sectional ~cans of the thigh (fig 2) showed that adipose
tissue-free skeletal muscle increased significantly in anterior
(fig 3) and posteric~r (fig 4) compartments when measured at the
first follow-up interval. No further increase was observed at the
second follow-up ihterval.
Analysis of individual muscles' cross-sectional areas (ana-
tomic skeletal muscle) is shown in figure 5. The percent
increases over baseline (before FESILEC started) were: rectus
femoris, 31% (p <~ .001); sartorius, 22% (p < .025); adductor
magnus-hamstringS, 26% (p < .00l); vastus lateralis, 39%
(p = .001); vastus medialis-intermedius, 31% (p = .025). Cross-
sectional area of adductor longus and gracilis muscles did not
change. There were no correlations among the total number of
FESILEC sessions! and the magnitude of muscle hypertrophy.
Evaluation of the areas occupied by different tissues (fig 6) 178%
indicated statistically significant increases in muscle tissue in
thigh and leg, no Changes in adipose tissue, and a significant
increase in the ratio of muscle to adipose tissue.

DISCUSSION
This study found a generalized increase in skeletal muscle
cross-sectional arqa, with no change in adipose tissue, and a
consequent increase in the ratio of muscle to adipose tissue.
This phenomenon iwas present in both the thigh and the leg.
Although no electi1odes were applied over the leg, proximity of
the posterior eleqtrodes to the sciatic nerve activated leg
muscles. The greater effect observed in the anterior compart-
ment may relate tO the fact that only the quadriceps muscles
were stimulated in the strengthening period in phase 1. In
addition, the post{rior compartment included the gracilis and
adductor longus muscles, which did not increase in mass,
probably because ~otor points for these muscles were not close
to the stimulating electrodes.
Increased muscle mass was observed at the first follow-up
evaluation, after completion of the resistive part of the training.
159%
This type of exercise has been shown to induce greater muscle Fig 2. Midthigh CT scans of one SCI subject taken before and during
hypertrophy in animals and humans than aerobic exercise. 3~ FESILEC training: the top is a pre-FESILEC scan, the middle is at 83
The lack of further increase in muscle mass beyond the first days, and the scan on the bottom is at 395 days within the FESILEC
follow-up CT is p{obably related to the fact that workload was program. Cross-sectional area data are expressed as percentages of
pre-FESILEC (ie, pre-FESILEC = 100%). The vertical bar to the right of
not incremented after that time. each image represents 5cm.
FES has been shown previously to prevent decreases in leg

Arch Phys Med Rehabil Vol 80, December 1999

1534 FES-INDUCED CYCLING TO INCREASE MUSCLE MASS, Scremin

160 ** 160
,.'X--X,.

140

120

1--100 71oo -- . . . . . . . . . . . .
Z
ILl
(O 80
n'-
ILl
m_ 6O
o. oo i
4O 4o }
2O

0 I

PROXIMAL MIDDLE DISTAL Rect.F. Sart. Add.L. Grac. Add-Hams. Vast&. Vast.M.

Fig 3. Thigh anterior compartment: percentage change in cross-
sectional area of adipose tissue-free skeletal muscle in 8 subjects.
Left and right sides were averaged because no side differences were
present. Results are expressed as percentage of baseline (c], pre-
FESILEC [100%]). The first follow-up CT measurement (1~) was taken
after 65 -+ 5 sessions. The second follow-up CT measurement (11)
was taken after 98 - 9 sessions. * p < .025; * * p < .001.
lean body mass in SCI subjects when it is applied within 3
months after injury; Baldi and associates24 observed a decrease
of 21% in lean lower limb mass after a 6-months postinjury
period in untreated patients, whereas patients treated with
FESILEC (three times a week) showed a small but statistically
significant increase compared with pretreatment mass. The
smaller increase (9%) found by Baldi than found in the present
study (about 30% increase in the thigh) may be attributable to
differences in time after injury or underestimations in the Baldi
study because of the indirect estimates of muscle mass recorded
by x-ray absorptiometry.
In our study, muscle cross-sectional area increases were
comparable to those described with resistance exercise in
able-bodied subjects. In healthy men of ages comparable to
160
140
120
1--100
Z
w
0 80
rr
W ~ 6o
a. 60
40
20
0 T1
PROXIMAL MIDDLE DISTAL
Fig 4. Thigh posterior compartment: percentage change in cross-
sectional area of adipose tissue-free skeletal muscle in 8 subjects.
Left and right sides were averaged because no side differences were
present. Results are expressed as percentage of baseline (rT, pre-
FESILEC [100%]), The first follow-up CT measurement (~]) was taken
after 65 +- 5 sessions. The second follow-up CT measurement (11)
was taken after 98 -+ 9 sessions. * p < .025; * * p < .001.
Fig 5. Individual skeletal muscles (thigh): percent change in cross-
sectional area between baseline and first follow-up CT in 9 subjects.
Results are expressed as percent of baseline (pre-FESILEC, 100%).
*p < .025; * * p < .001.
those of our subjects, after 6 months of weight training on
alternate days with six series of eight unilateral leg extensions
at 80% of one repetition maximum, cross-sectional area in-
creased by 13% to 19.3% at different sectors of the quadriceps
muscle. 14 In subjects over the age of 55 years, 6 months of
isometric quadriceps strength training induced a 4% to 4.9%
increase in thigh circumferenceJ 5 In the upper arm, cross-
sectional areas of biceps and triceps increased by 12.6% and
25.1%, respectively, after 12 weeks of intensified resistance
training in college men. 16 The cross-sectional area of medial
and lateral knee extensors of bodybuilders has been reported to
be 29% and 49% greater, respectively, than that of nontrained
controls of comparable ages. 32
The ability of the presently reported FES exercise program to
increase muscle mass in men with SCI may be related to the
strength training characteristics of phases 1 and 3a, in which
160
140 ** * * **
120
Z~100 . . . . . . . . . . .
40
20
0
T2 T3 L1 L2
Fig 6. Cross-sectional area occupied by muscle (R) and by adipose
tissue ([]), and the ratio of muscle to adipose tissue (11): percent
changes between baseline and first follow-up CT in 6 subjects.
~ssue components were calculated by segmenting image density
levels into Hounsfield unit ranges: adipose tissue, -190 to -20;
muscle tissue, - 1 9 to +150. T1, proximal thigh; T2, midthigh; T3,
distal thigh; L1, proximal leg; L2, distal leg. Results are expressed as
percentage of baseline (pre-FESlLEC, 100%). * p < .025.

Arch Phys Med Rehabil Vol 80, December 1999

 FES-INDUCED CYCLING TO INCREASE MUSCLE MASS, Scremin
progressive loads are used. The fact that the gain in muscle
cross-sectional area was recorded at the end of phase 3a, with
no further gain at a later follow up seems to support this
interpretation. The anaerobic nature of FESILEC training may
also contribute to its effect on muscle mass. In young subjects,
when the quadriceps performs long, fatiguing contractions, a
significantly greater increase in cross-sectional area is observed
than when short contractions are performed followed by longer
intervals--a difference that has been attributed to a greater
metabolite accumulation during the first type of exercise. 33
FESILEC inducesa large increase in blood lactate. 34 Moreover,
our previous studids of muscle blood flow in SCI subjects on
FES-induced exercise showed a larger increase in blood flow
and a slower return lto preexercise blood flow levels than in able
bodied subjects performing a mechanically equivalent volun-
tary exercise. 35 Th~se findings suggest a greater accumulation
and slower washout of metabolites in this type of FES exercise.
The phenomenon may relate to the tetanic and synchronous
nature of FESILEC!muscle contraction that interferes with local
circulation.
Our results in the present study showed no change in adipose
tissue cross-sectional area in the legs after FESILEC. Only one
study has examined this issue before and it claimed that adipose
tissue area decreased in one of the studied FES regimens.36 This
conclusion was based on the analysis of a small group of
patients (n = 4) ahd use of nonadjusted multiple contrast
statistics. In the presence of an increase in muscle cross-
sectional area, the ~nuscle to adipose tissue ratio of the lower
extremities in our ekperiments was enhanced by FESILEC.
CONCLUSION
FESILEC increased muscle mass of thighs and legs, and
enhanced the muscle to adipose tissue ratio of SCI subjects.
These effects were Sustained by continuous training over 1 year.
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Suppliers
a. Therapeutic Alliances, 333 North Broad Street, Fairborn, OH
45324.
b. GE Medical Systems, 25925 Telegraph Road, Southfield, Milwau-
kee, W148034.
c. Hewlett-Packard, 3000 Hanover Street, Palo Alto, CA 94304- l 185.
d. Jandel Scientific, PO Box 7005, San Rafael, CA 94912-7005.