1379

ORIGINAL ARTICLE

A Randomized Controlled Trial on the Effects of Cycling Withand Without Electrical Stimulation on Cardiorespiratory and
Vascular Health in Children With Spinal Cord Injury
Therese E. Johnston, PT, PhD, Brian T. Smith, MS, Mary J. Mulcahey, OTL/R, PhD, Randal R. Betz, MD,
Richard T. Lauer, PhD
ABSTRACT. Johnston TE, Smith BT, Mulcahey MJ, Betz
RR, Lauer RT. A randomized controlled trial on the effects ofcycling with and without electrical stimulation on cardiorespiratory and vascular health in children with spinal cord injury.
Arch Phys Med Rehabil 2009;90:1379-88.
Objective: To examine the cardiorespiratory/vascular effects of cycling with and without functional electrical stimulation (FES) in children with spinal cord injury (SCI).
Design: Randomized controlled trial.
Setting: Pediatric referral hospital.
Participants: Children with SCI (N⫽30), ages 5 to 13 years,
with injury levels from C4 to T11, and American Spinal Injury
Association grades A, B, or C.
Interventions: Children were randomly assigned to 1 of 3groups: FES leg cycling exercise, passive leg cycling, or noncycling control group receiving electrical stimulation therapy.
After receiving instruction on the use of the equipment, children exercised for 1 hour 3 times per week for 6 months athome with parental supervision.
Main Outcome Measures: Oxygen uptake (V̇O2) during an
incremental arm ergometry test, resting heart rate, forced vital
capacity, and a fasting lipid profile.
Results: There were no differences (P⬎.05) between groups
after 6 months of exercise when comparing pre- and postvalues. However, there were differences between groups for somevariables when examining percent change. The FES cyclinggroup showed an improvement (P⫽.035) in V̇O2 (16.2%⫾
25.0%) as compared with the passive cycling group (–28.7%⫾
29.1%). For lipid levels, the electrical stimulation– only group
showed declines (P⫽.032) in cholesterol levels (–17.1%⫾
8.5%) as compared with the FES cycling group (4.4%⫾
20.4%).
Conclusions: Cycling with FES led to gains in V̇O2, whereas
electrical stimulation alone led to improvements in cholesterol.

From the Department of Physical Therapy, University of the Sciences in Philadelphia (Johnston); Shriners Hospital for Children (Johnston, Smith, Mulcahey, Betz,
Lauer); and the Department of Physical Therapy, Temple University (Lauer), Philadelphia, PA.
Presented to the International Functional Electrical Stimulation Society, November
10 –14, 2007, Philadelphia, PA; World Confederation for Physical Therapy Congress,
June 2– 6, 2007, Vancouver, BC; Physical Therapy Combined Sections Meeting,February 14 –18, 2007, Boston, MA; and Injury and Dysfunction of the Spinal Cordin Children, November 30 –December 2, 2006, Orlando, FL.
Supported by the Shriners Hospitals for Children (grant no. 8540).
No commercial party having a direct financial interest in the results of the researchsupporting this article has or will confer a benefit on the authors or on any organization with which the authors are associated.
Clinical Trials Registration Number: NCT00245726.
Reprint requests to Therese E. Johnston, PT, PhD, MBA, University of the Sciencesin Philadelphia, 600 S 43rd St, Box 39, Philadelphia, PA 19104, e-mail: t.johnston@usp.edu.
0003-9993/09/9008-00997$36.00/0
doi:10.1016/j.apmr.2009.02.018

Key Words: Pediatrics; Rehabilitation; Spinal cord injuries.
© 2009 by the American Congress of Rehabilitation
Medicine
EROBIC FITNESS IS DEFINED as the capacity to perA
form endurance activities that mainly depend on aerobic
metabolism. One component of aerobic fitness is V̇ max
1

O2(mL/kg/min). High V̇O2max values reflect good function of the
cardiorespiratory system, making it possible to accomplish
submaximal tasks with less fatigue.1 For adults with SCI,
VO2peak during upper-extremity ergometry is 5% to 59% lessthan age- and sex-matched peers without disability duringlower-extremity exercise.2 This decrease is partially caused bydecreased lean body mass that occurs post-SCI, with greaterloss with higher levels of injury and complete SCI. With lesslean tissue, there is less muscle available to participate in
exercise that would maximally stress the cardiorespiratory system to obtain sufficient benefits.3 Despite the fact that dailyenergy expenditure is reduced with decreased muscle mass,4 1
out of 4 young people with SCI does not have the level offitness required to perform essential activities of daily living.5
These activities are compromised, in part, by an insufficient
circulatory response (decreased blood pressure and increased
resting heart rate) because of vascular atrophy, impaired
work capacity, and increased VO2peak in response to submaximal work.6
After an acute SCI, muscle atrophy occurs quickly, withdecreases in average lower-extremity muscle cross-sectional
area of up to 45% reported 6 weeks post-SCI.7 These values
then decrease approximately 3.2% per decade post-SCI as
compared with 1% per decade in the general male population.
In addition to impacting energy expenditure, decreased muscle
mass increases the risk of cardiovascular disease.8 Other factors such as increased adiposity, hyperlipidemia, and decreased
physical activity contribute to this increased risk8 and the riskof metabolic syndrome and diabetes.4,8 In fact, cardiovasculardisease is now the leading cause of mortality in persons withchronic SCI, with an earlier onset 9 and increased prevalence
than in the general population.10

List of Abbreviations
FES
FVC
HDL
LDL
rpm
SCI
V̇O2
V̇O2maxVO2peakfunctional electrical stimulation
forced vital capacity
high-density lipoprotein
low-density lipoprotein
revolutions per minutespinal cord injury
oxygen uptake
maximum oxygen consumption
peak oxygen uptake

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CARDIORESPIRATORY EFFECTS OF CYCLING, Johnston

Aerobic exercise may be used to reduce these risk factors
and improve life expectancy.11 One method, lower-extremity
FES cycling, has been proposed as an ideal means to address
long-term complications of SCI because it is an exercise that
can target the larger lower-extremity muscles.3 Numerous
studies12-24 have examined the effects of FES cycling on the
cardiovascular and respiratory systems of adults with SCI.
Studies involving cycling training 2 to 3 days per week for
12 to 16 weeks have shown increases in VO2peak,19,25
cardiac output,19,26 stroke volume,26 and pulmonary ventilation during FES cycling.19 Faghri et al26 reported thatheart rate and blood pressure during submaximal cycling
decreased, whereas stroke volume and cardiac output increased, suggesting an improvement in central cardiovascular fitness. Hooker et al22 examined respiratory change after
a program of FES cycling of 24 sessions over 19 weeks,showing improvement in VO2peak, indicating that gains canbe obtained with a less intense program. In addition, FES
cycling has led to improved circulatory responses to ischemia and the reversal of cardiac atrophy in people withtetraplegia.6 These studies show that improvements in cardiorespiratory fitness can be obtained by adults with SCI
after a program of FES cycling.
FES cycling may have an impact on the exercise capacity of
the upper body. Suggested mechanisms include improvements
in venous return and decreased blood pooling, which may thenincrease the upper-body exercise capacity.3,16 Both peripheral
muscular effects and central cardiovascular effects have beenreported after a program of FES cycling.26 Other reports suggest that the effects of FES cycling are more peripheral; however, they acknowledge that higher power outputs may have an
impact on the cardiorespiratory system.19
FVC is reduced in adults with SCI, with greater deficits withhigher injury levels.27 After a program of upper-extremity
exercise, adults with SCI showed increases in FVC and ventilatory endurance. These changes were possibly caused by improvements in strength and endurance of the diaphragm, abdominals, and more directly on the accessory muscles ofinspiration. The impact of lower-extremity exercise on FVC
post-SCI is not known. However, FVC has been shown toincrease in healthy children after a running program with thetheory that the activity could lead to increased strength andendurance of the respiratory muscles and changes in the structure of the respiratory system.28
Despite the focus on FES cycling with adults with SCI, thistechnique has not been studied in children with SCI. For
children with SCI, cardiorespiratory deficits are contributed torespiratory complications, which occur in up to 33% of persons
with pediatric-onset SCI29 and respiratory illness accounts for
22% of the deaths in persons with SCI.30 If FES cycling leads
to similar improvements in children with SCI as seen withadults, the potential exists to improve cardiorespiratory healthat an early age. The purpose of this study, therefore, was to
examine the effects of leg cycling exercise both with andwithout electrical stimulation to determine whether the same
cardiorespiratory changes that were reported in the adult population can be achieved in the pediatric population. It was
hypothesized that the FES cycling group would have the greatest cardiorespiratory and vascular improvements.

block randomization, children were randomly assigned to 1 of
3 groups: FES leg cycling exercise, passive leg cycling, and anoncycling control group receiving electrical stimulation therapy. The groups were balanced as to the amount of time theyreceived the specific therapy.
Parents and children signed an institutional review board–
approved informed consent and assent forms, respectively.
Inclusion criteria were 12 months postinjury; cervical or thoracic level SCI with an American Spinal Injury Association
grade A, B, or C classification (if C, nonambulatory or only able
to walk with long leg braces); age 5 to 13 years; and innervatedlower-extremity muscles. Exclusion criteria included chronic steroid treatment, history of seizures, cardiac disease, ventilator
dependency, severe spasticity in the legs, lower-limb stressfractures, lower-extremity fractures of unknown origin, uncontrolled autonomic dysreflexia, heterotopic ossification, and hip
dislocation. Children were also excluded if they had participated in activities involving electrical stimulation or activitybased therapy within the past 3 months.
Children exercised at home with parental assistance for 1
hour 3 times per week for 6 months. Parents received instruction on the use of the equipment from the same investigator.
The FES cycling group cycled at a target cadence of 50rpm byusing an RT300-P FES cyclea while seated in their wheelchairs(fig 1). The cycle provided 10 minutes of a passive warm-up,
40 minutes of FES cycling, and 10 minutes of a passive cool
down. FES to the quadriceps, hamstring, and gluteal muscles
was delivered by using the largest surface electrodesb appropriate for the child’s leg. Stimulation frequency was fixed at
33Hz, and pulse duration was set at 150, 200, 250, or 300␮s.
The current amplitude increased automatically up to a maximum of 140mA to generate sufficient force to maintain thecadence. This maximum was decreased for the smaller children
based on individual muscle response. At higher stimulationlevels, the quadriceps and hamstring muscles were often activated simultaneously by the quadriceps and/or the hamstrings
electrodes, likely because of the small muscle size of thesechildren. This cocontraction would cause the cycling cadence

METHODS
Subjects and Exercise Protocol
A controlled, randomized study with a pre-post within-subjects
repeated-measures design was conducted. Children were recruited through a hospital-based pediatric SCI clinic. By using
Arch Phys Med Rehabil Vol 90, August 2009

Fig 1. Child with paraplegia on the FES cycle.

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CARDIORESPIRATORY EFFECTS OF CYCLING, Johnston

to decrease. The resistance cycled against started at 1Nm andwas increased in increments of 0.14Nm once the child could
cycle for an entire session at the current resistance level. If thechildren’s cycling cadence dropped below 35rpm for greaterthan 30 seconds, the muscles were determined to be fatigued
and the cycle would go into the passive cool down mode.
The passive cycling group used the RT100a motorized cycle,
which passively moved the legs for the entire hour at 50 rpm
with children seated in their wheelchairs. The RT300 and
RT100 only differ in that the RT300 provides FES, whereas the
RT100 does not. Children in the electrical stimulation therapy
group used a portable, 2-channel surface stimulation unitc tobilaterally create strong muscle contractions of the hamstrings,
quadriceps, and gluteal muscles. Each muscle was stimulated
for 20 minutes with a duty cycle of 5:15 seconds for a total of
1 hour. Subjects exercised in the supine position, working
against zero resistance. Parents were instructed to increase thestimulation level delivered if the muscle response decreased
during the session.
For children performing either cycling exercise, adjustments
were made to accommodate each child’s size and wheelchairconfiguration. For example, crank arm length was shortened toaccommodate smaller legs, and the calf support could be manipulated to prevent it from hitting the wheelchair. The cycle’s
height was raised with a custom-made wooden platform so thechildren’s feet would reach the pedals. The goal was to position
the child to obtain a position of approximately 30° to 40° lessthan full knee extension during the extension phase of therevolution.
Before exercising, all children participated in lower-extremity muscle passive range of motion exercises. Children werepermitted to continue their previously established therapeutic
activities, such as standing and walking with braces, but were
not permitted to participate in nonstudy-related lower-extremity repetitive motion tasks or electrically stimulated exercise. It
was decided not to alter the prestudy exercise routine because
declines from baseline values might have occurred if these
activities were stopped.
Children were permitted to miss up to 12 sessions over the
6-month period. If a greater number of sessions were missed,parents were instructed to add 1 extra session per week to makeup for the missed sessions. Parents logged each session performed on a weekly log sheet that was sent to the investigators
on a monthly basis. In addition, telephone calls were made to
the parents every 2 weeks to receive information on how thechild was doing and if the required number of sessions was
being completed.
Data Collection
Data were collected before and after 6 months of at-home
exercise. Heart rate and V̇O2 (mL/kg/min) were measured during an incremental upper-extremity ergometry test31 by using abreath-by-breath technique with a SensorMedics VMax29 metabolic cart.d The measurement error for this test with children
is unknown. An upper-extremity test was chosen instead of alower-extremity FES cycling test because all subjects were nottrained with FES cycle. During the upper-extremity ergometry
test, subjects wore a small airtight facemaske over the mouthand nose that held the flow sensor that measured the volume ofoxygen per kilogram of body weight. Before each test, the flow
sensor and the gas analyzer were calibrated according to the
manufacturer’s guidelines. V̇O2 was measured under 4 consecutive conditions: (1) sitting quietly for 5 minutes (baseline), (2)upper-extremity cycling at 10W at a self-selected cadence for
1 minute (warm-up), (3) upper-extremity cycling at 10W withincreases of 10W every minute until self-determined fatigue,and (4) sitting quietly for 3 minutes (recovery). Each subject’s
heart rate was monitored during the test, but setting a heart ratecriterion based on adult recommendations for an exercise test
was not practical because growing children can reach an exercising heart rate between 195 and 210bpm.32 Oxygen saturation was monitored during the test to ensure that it did not drop
below 95%. Children were instructed to terminate the test if
they were not feeling well, such as feeling dizzy or nauseous orexperiencing pain; however, no child experienced these reactions to the test. On occasion, the mask was removed during therecovery phase because of a child feeling short of breath or hot
while wearing the mask. After the test, the resting heart rate
was averaged from baseline data, and VO2peak (mL/kg/min)
was calculated by determining the highest 15-second averagevalue.
FVC was assessed by using the same metabolic cart that wasused for upper-extremity ergometry testing by taking the bestof 3 trials. With the nose closed by a soft nose clip, children
were asked to breathe normally for at least 3 breaths through amouthpiece and then were instructed to take as deep of a breathin as possible and blast the air out as fast and long as possible(goal⫽6s). FVC was recorded as a percentage of the norm
based on age and height.33,34
Finally, cholesterol, HDLs, LDLs, and triglycerides levels
were obtained by a fasting lipid profile with children fasting atleast 10 hours before the test. The measurement error has beenreported to be 18.2mg/dL for triglycerides, 6.1mg/dL for cholesterol, 2.3mg/dL for HDL levels, and 7.4mg/dL for LDL
levels in a sample of 19 children.35
The same investigator, who was not blinded to group, performed all testing with the children, except the blood draw andblood histochemical analysis. The blood was collected andanalyzed by blinded personnel.
Data Analysis
Two-way analyses of variance were used to compare all data
across time (baseline and 6mo) and group. One-tailed paired t
tests were used to examine any differences within groups overtime. To allow for comparisons with published results forchildren with typical development, average percent change inV̇O2, and average change in values for the lipids were also
analyzed.
RESULTS
Subjects
Thirty children with C4 to T11 SCI, ages 5 to 13 years (table 1),
participated in the study. In total, 58 children were screened forpossible participation (fig 2). Of the children who participatedin the study, only 1 (passive cycling group) was involved inregular upper-extremity strengthening activities. Four children
were participating in other recreation activities (hand cycling, 1
FES cycling, 1 electrical stimulation) and wheelchair basketball (1 electrical stimulation, 1 passive cycling). These activities were not new to the children during the study.
Adherence values (percentage) were calculated with andwithout the allowance for up to 12 missed sessions over the 6months. With the allowance, adherence rates were 95.2%⫾
18.1%, 107.2%⫾16.2%, and 105.5%⫾19.6% for the FES cycling, passive cycling, and electrical stimulation groups, respectively. Without the allowance, this corresponded to 81.6%⫾
15.5%, 91.9%⫾13.9%, and 89.6%⫾17.4%, respectively. The
maximal resistances obtained by the FES cycling subjects ranged
from 1.28 to 2.25Nm. Using these resistance levels and a cadenceof 35 to 50rpm, the range of power outputs was 3.67 to 13.1W.
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CARDIORESPIRATORY EFFECTS OF CYCLING, Johnston
Table 1: Subject Demographics

Group

Age

Sex

Level of Injury

ASIA
Grade

Years Postinjury

Cause of Injury

Height (cm)Weight (kg)

FES
FES
FES
FES
FES
FES
FES
FES
FES
FES
PC
PC
PC
PC
PC
PC
PC
PC
PC
PC
ES
ES
ES
ES
ES
ES
ES
ES
ES
ES

7
7
7
8
8
9
11
12
12
13
5
7
7
7
8
8
8
11
11
12
6
11
11
12
12
12
12
12
13
13

F
M
M
M
M
F
M
F
F
F
F
F
M
M
F
M
M
F
M
F
F
F
M
F
M
M
M
M
M
M

T4
T1
C4
C8
T5
C7
T1
T11
T1
T10
C7
T8
T3
T7
C5
T1
C7
C8
C7
T4
T7
T5
T11
C7
T7
C7
T5
C7
T4
T5

A
A
B
B
B
A
A
A
A
C*
A
B
A
C†
A
A
A
B
A
A
A
A
B
A
A
A
A
A
A
A

5
5
6
6
8
5
5
2
1
3
4
7
3
1
7
5
6
7
8
1
1
7
7
2
8
12
2
10
7
1

MVC
MVC
Transverse myelitis
MVC
Atresia
MVC
MVC
MVC
MVC
MVC
MVC
Ischemia
MVC
MVC
MVC
MVC
MVC
MVC
MVC
MVC
MVC
MVC
Chemotherapy
MVC
MVC
Birth
MVC
MVC
MVC
Transverse myelitis

119
120.5
122
122.5
120
130
138.5
160.5
156.5
156
116.5
120
118.5
118.5
122
134.7
121.5
139
144.5
149
118
146
156
161.5
161.3
146
167
153
171.4
165.5

27.5
20.2
23.1
26.8
19.7
23.7
27.5
57.8
89.4
66
24
24.1
19.7
17.7
23.3
37
24.6
41.6
29.1
38
20.7
45
49.1
54.8
72.6
33.9
75.4
37.7
70.2
67.6

Abbreviations: ES, electrical stimulation; F, female; M, male; MVC, motor vehicle collision; PC, passive cycling.
*Hip flexion grade 2 only. No other lower-extremity movement.
†
Anal contraction only. No lower-extremity movement.

Baseline Measures
There were significant differences between groups in baseline height, weight, and age. In addition, the groups were
unbalanced in terms of injury levels, with the greatest numberof subjects with tetraplegia in the passive cycling group. However, there were no differences between groups for any of thebaseline measures (VO2peak, resting heart rate, FVC, lipid
values).
Oxygen Uptake (mL/kg/min) and Resting Heart Rate
There were no differences between groups over time forVO2peak when comparing baseline and 6-month values (fig 3).
However, when examining average percent change, there weresignificant differences between groups with Bonferroni post hoc
testing showing that the FES cycling group had a significant
change (16.2%⫾25%) as compared with the passive cyclinggroup (–28.7%⫾42%). In examining baseline and 6-monthvalues within each group, the changes did not reach statisticalsignificance. In addition, resting heart rate did not change whencomparing the groups over time (fig 4), and 1-tailed paired t
tests showed no changes within each group. Table 2 displays
each subject’s individual data for V̇O2 and resting heart rate.
Forced Vital Capacity
There were no differences between groups over time for
FVC when comparing baseline and 6-month values (fig 5).
Arch Phys Med Rehabil Vol 90, August 2009

One-tailed paired t tests also showed no changes within eachgroup. Table 2 displays each subject’s individual data.
LipidsThere were no differences between groups over time for anyof the lipids when comparing baseline and 6-month values(table 3). One-tailed paired t tests also showed no changes
within each group. When examining average change in lipid
values, there were significant differences between groups
for cholesterol and HDL levels. Bonferroni post hoc testing
showed that the electrical stimulation group had a decrease incholesterol as compared with the FES cycling group.
DISCUSSION
In this study, 30 children with SCI exercised at home for 6
months with an FES cycle or passive cycle or they used
noncycling electrical stimulation therapy. The results showed agreater percent change in VO2peak for the FES cycling group
and a greater percent decrease in cholesterol levels for theelectrical stimulation group. Therefore, our hypothesis waspartially supported because the FES cycling group showed
greater respiratory changes but not greater cardiovascularchanges.
Compliance with the exercise protocol was between 80%
and 92% for the 3 groups, suggesting that the exercise protocols were integrated successfully into the family routine. The

CARDIORESPIRATORY EFFECTS OF CYCLING, Johnston1383

Fig 2. Flowchart diagram for the study.

adherence rate for the FES cycling group was likely less thanthe other groups because of the added time for setup, occasional computer malfunctions, and the need for greater parental
supervision to advance resistance. Only 1 child (12y) complained of occasional discomfort with the FES; however, she
did not miss sessions because of this issue. During the study,
medications taken by the children were primarily for spasticity
and bladder management. These medications remained stablethroughout the study, other than occasional antibiotics becauseof urinary tract infections.
The FES cycling group showed improvements in VO2peakwith values improving from 9.9⫾5.4 to 12.7⫾7.6mL/kg/min.
A decline was observed in the passive cycling group, and aminimal increase was seen in the electrical stimulation group.
To interpret these findings, it is important to understand how

children with typical development respond to exercise because
children respond differently than do adults. One study examining V̇O2max changes after a 12-week aerobic exercise program for 10- to 12-year-old children with typical development
showed average VO2max increases of 6.5% (P⬍.05).36 In ourstudy, children in the FES cycling group showed averageincreases of 16.2%, suggesting that they experienced a clinically significant improvement in this measure. The percent
decrease in V̇O2 of 28.7% for the passive cycling group was
surprising. Children in the electrical stimulation group showedno overall change (2.5% increase). Overall, these results suggest that both types of exercise involving electrical stimulation
helped to improve or maintain V̇O2, whereas the passive exercise did not, indicating that active muscle contractions may be
important. These active contractions may have impacted theArch Phys Med Rehabil Vol 90, August 2009

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CARDIORESPIRATORY EFFECTS OF CYCLING, Johnston

Fig 3. (A) V̇O2 values and (B) average percent change in V̇O2 pergroup. There were no differences between groups in uptake values
over time (Pⴝ.588, powerⴝ.133); however, the FESC group showeda significant increase in average percent change as compared withthe passive cycling group (Pⴝ.033, powerⴝ.651) with Bonferroni
post hoc testing showing that the FESC group had a greater positive percent change than did the passive cycling group (Pⴝ.035)(FESC vs ES, Pⴝ1.00; PC vs ES, Pⴝ.185). In examining baseline and6-month values within each group, the changes did not reach statistical significance (FESC, Pⴝ.056; PC, Pⴝ.095; ES, Pⴝ.23). Abbreviations: ES, electrical stimulation; FESC, functional electrical stimulation cycling; PC, passive cycling.

central cardiorespiratory system through improvements in venous return and decreased blood pooling.3 One possible limitation to these findings is that the impact of the upper-extremity
exercise participation during the study for 5 (1 FES cycling, 2
passive cycling, 2 electrical stimulation) of the 30 children
cannot be determined. However, the children were participating in these activities regularly before enrolling in the study.
In children31 and adults with SCI,37 exercise responses vary
based on level of injury, with people with tetraplegia showing
the smallest changes in V̇O2 values with exercise because ofalterations in the sympathetic nervous system and differencesin lean body mass. These factors may have impacted the results
by decreasing the average change per group. Each group included
children with tetraplegia and children with paraplegia (3, 5, and 3
children with tetraplegia in the FES cycling, passive cycling, andelectrical stimulation groups, respectively). When re-examining the data based on level of injury, the average changes in
V̇O2 were –12.1%⫾22.8% for subjects with tetraplegia (n⫽9),41.2%⫾78% for subjects with T1 to T5 paraplegia (n⫽10), and–5.2%⫾35.5% for subjects with T7 to T11 paraplegia (n⫽7).
Therefore, the largest change was seen in the group with T1 to
T5 paraplegia. When only examining the children in the FES
cycling group, the average changes in V̇O2 were –7%⫾9.9%
for subjects with tetraplegia (n⫽2), 52.8⫾69.3% for subjects
with T1 to T5 paraplegia (n⫽4), and –32.4%⫾35.0% forsubjects with T7 to T11 paraplegia (n⫽2). These results suggest that lean body mass may have had an impact on the results
because greater improvements were seen in the children with
Arch Phys Med Rehabil Vol 90, August 2009

paraplegia. This finding must be viewed cautiously because of
the small sample size of the FES cycling group.
Adults with SCI have shown improvements in VO2peak
after upper-extremity38 and lower-extremity FES cycling39
exercise. A systematic review of VO2peak after a 3 or moretimes per week upper-extremity exercise program showed
average increases of 17.6%⫾11.2% over a period of 4 to 32
weeks.38 Our finding of an increase of 16.2% for subjects in
the FES cycling groups was comparable with their results. In
an FES cycling study for adults with SCI,39 statistically significant improvements were found in VO2peak during FES
cycling after a minimum of twenty-four 30-minute sessions
performed twice per week.
Resting heart rate decreased approximately 5 beats/min on
average for all groups. It is difficult to discern the exercise
effect because of the natural decline in resting heart rate that
occurs as children become older.32 A 2- to 3-beats/min decrease of over a 6-month period of time occurs in children withtypical development40; however, it is unknown if the similar
decrease occurs in children with SCI. In addition, adults with
SCI show variability in their resting heart rate41; therefore,
resting heart rate may not be a good indicator of fitness levels.
Variability in resting heart rate has not been reported forchildren with SCI.
FVC did not change over time for children in any group. The
baseline average FVC value for subjects in this study was
66.9%⫾24.7% (range, 22%–124%) of predicted based on children with typical development. Therefore, as a group, thesechildren have low values. In a study with prepubescent children
with typical development,28 FVC (in liters) increased by 7%(P⬍.05) after an 8-week running program, indicating thatexercise can increase FVC. However, in that study, it was
unknown if this training increased lung volume or if the increase was because of improvements in the expiratory muscles.28 For adults with SCI, 1 study showed that a 30-minute,3-times-per-week, 6-week upper-extremity aerobic program
could increase FVC. This change may have been because ofincreased strength and the endurance of accessory muscles thatwere impacted directly or indirectly by the exercise.27
Perhaps the children in our study did not reach sufficient
exercise intensity to realize significant changes in FVC, restingheart rate, and lipid levels. Resistance was increased for the
FES cycling group to increase overall power output; however,
the resistance may not have allowed subjects to reach power
output levels necessary to realize further gains. To reach higher
resistances, the cadence of 50rpm would likely have to be
decreased. Fornusek and Davis42 showed a higher average

Fig 4. Resting heart rate values per group. There were no changes
in resting heart rate over time for any group (Pⴝ.991, powerⴝ.051).
One-tailed paired t tests also showed no changes within each group(FESC, Pⴝ.12; PC, Pⴝ.16; ES, Pⴝ.18). The slight decline noted may
be because of children being 6 months older. Abbreviations: ES,electrical stimulation; FESC, functional electrical stimulation cycling; PC, passive cycling.

1385

CARDIORESPIRATORY EFFECTS OF CYCLING, Johnston

Table 2: Individual Data and Percent Change for the Upper-Extremity Ergometry Test (VO2peak, resting heart rate, peak heart rate, andmaximal power) and the FVC Test
VO2peak (mL/kg/min)Resting HR (beats/min)

HR Peak (beats/min)

Max Power Output
(W)

Group

Age

Sex

Pre

Post

%⌬

Pre

Post

%⌬

Pre

Post

%⌬

Pre

Post

%⌬

FES
FES
FES
FES
FES
FES
FES
FES
FES
FES
PC
PC
PC
PC
PC
PC
PC
PC
PC
PC
ES
ES
ES
ES
ES
ES
ES
ES
ES
ES

7
7
7
8
8
9
11
12
12
13
5
7
7
7
8
8
8
11
11
12
6
11
11
12
12
12
12
12
13
13

F
M
M
M
M
F
M
F
F
F
F
F
M
M
F
M
M
F
M
F
F
F
M
F
M
M
M
M
M
M

6.2
12.1

15.7
11.4
NT
7.4
NT
6.0
10.4
26.7
4.5
19.8
8.8
25.7
NT
15.3
NT
7.4
9.0
4.0
17.1
12.6
13.1
9.7
18.3
3.3
17.3
5.8
14.5
17.0
21.0
11.3

153.2
⫺5.8

105
76

⫺8.6
17.1

185
110

30
20

2.3
⫺27.0
⫺15.3
⫺7.6
⫺16.8
2.1
13.2
⫺24.1
⫺14.9
⫺2.0
28.4
3.7
⫺21.5
5.1
5.2
⫺7.1
⫺16.8
13.2
6.9
7.5
⫺10.3
11.5
⫺17.6
⫺22.2
⫺9.2
⫺9.6
10.3

134
170
132
100
170
100
159
143
200
136
146

⫺16.4
⫺19.4
⫺12.1
3.0
5.9
10.0
8.2
⫺9.1
⫺4.5
3.7
⫺43.8

20
20
10
30
180
40
130
10
60
20
30

3.1
0.0
16.4
11.8
⫺17.9
⫺9.8
5.0
1.2
⫺3.0
12.5
⫺8.6
⫺16.4
36.2
⫺15.1
⫺9.4

20
20
20
40
20
30
40
80
20
100
10
100
30
115
70

40
20
NT
10
20
10
30
100
50
115
10
70
20
30
NT
30
10
40
30
20
30
70
80
20
100
20
130
50
100
80

33.3
0.0

88
122
111
66
101
97
68
108
101
101
95
82
130
99
77
85
101
91
87
80
107
78
125
99
76
104
68

173
112
NT
112
137
116
103
180
110
172
130
191
141
82
NT
165
129
128
142
138
175
190
165
128
189
127
163
143
174
154

⫺6.5
1.8

⫺14.0

96
89
NT
90
89
94
61
84
99
77
82
86
99
122
85
102
104
81
79
84
103
93
86
96
87
103
77
69
94
75

8.6
6.0
7.7
17.0
3.5
18.4
9.9
25.4
19.7
14.0
14.4
7.0
13.6
10.7
33.8
9.1
20.5
4.5
18.8
7.0
4.7
14.8
20.0
10.3

0.0
35.1
57.1
28.6
7.6
⫺11.1
1.2
⫺22.3
⫺47.1
⫺37.5
⫺42.9
25.7
17.8
⫺61.2
6.6
⫺10.7
⫺26.7
⫺8.0
⫺17.1
208.5
14.9
5.0
9.7

160
129
110
127
168
194
181
163
132
168
139
195
105
205
170

⫺50.0
0.0
0.0
0.0
⫺44.4
25.0
⫺11.5
0.0
16.7
0.0
0.0
50.0
⫺50.0
100.0
⫺25.0
0.0
0.0
75.0
0.0
0.0
0.0
100.0
30.0
66.7
⫺13.0
14.3

FVC (% Predicted)
Pre

Post

%⌬

61
36
54
90
36
55
124
71
115
50
115
54
49
22
75
53
58
46
66
81
70
81
32
84
60
83
56
87
76

NT
52
50
55
99
35
59
111
63
119
56
96
67
60
20
60
49
69
46
69
41
73
84
35
85
55
83
55
84
6

⫺14.8
38.9
1.9
10.0
⫺2.8
7.3
⫺10.5
⫺11.3
3.5
12.0
⫺16.5
24.1
22.4
⫺9.1
⫺20.0
⫺7.5
19.0
0.0
4.5
⫺49.4
4.3
3.7
9.4
1.2
⫺8.3
0.0
⫺1.8
⫺3.4
⫺92.1

Abbreviations: ES, electrical stimulation; F, female; HR, heart rate; M, male; NT, not tested; PC, passive cycling; % ⌬, percent change.

power output in adults with SCI when cycling with FES at
30rpm as compared with 50rpm. Another option would be toperform upper- and lower-extremity exercise simultaneously.
Hooker et al19 reported an increase of 23% in V̇O2 after a
combined lower-extremity FES and arm-crank ergometry program for adults with SCI. This type of combined exercise has
not been tested in children with SCI. Future research should
examine these and other methods to increase exercise intensity

Fig 5. FVC per group. There were no differences between groups
over time for FVC when comparing baseline and 6-month values(Pⴝ.637, powerⴝ.098). One-tailed paired t tests also showed nochanges within each group (FESC, Pⴝ.50; PC, Pⴝ.45; ES, Pⴝ.10).
Abbreviations: ES, electrical stimulation; FESC, functional electricalstimulation cycling; PC, passive cycling.

in children with SCI to determine if greater cardiorespiratory
improvements can be realized. Additionally, future studies
should include a rating of perceived exertion to determine theintensity as related to each of the children because children willvary in their levels of fitness.
No significant changes in lipid levels were seen between
groups over time. However, it is important to consider how
lipids typically respond to exercise for children in general tobetter interpret our results. A meta-analysis43 of lipid profiles
after aerobic exercise in typically developing children (5–19y)reported changes only with triglyceride levels (average change12%). In this meta-analysis, the confidence intervals for lipidchanges were found to be –22.8 to 0.8mg/dL for triglycerides,– 4.4 to 3.3mg/dL for cholesterol, – 4.8 to 1.9mg/dL for HDL,
and – 4.3 to 6.7mg/dL for LDL levels.43 Using these confidence
intervals, the FES cycling group had a small increase in cholesterol levels, the passive cycling group had a decrease incholesterol levels (a positive change) but also a decrease in
HDL levels (a negative change), and the electrical stimulationgroup had decreases in cholesterol, HDL, and LDL (positivechange) levels. Therefore, the findings were mixed. In adults
with SCI, arm-cranking exercise training has been associatedwith positive changes in HDL levels but not in total cholesterol
or triglyceride levels.44 Another study45 reported that adults
with SCI with greater physical capacity had better lipid profiles, thus suggesting that physical activity can have an impact.
Arch Phys Med Rehabil Vol 90, August 2009

1386

Triglycerides
Group

FES
FES
FES
FES
FES
FES
FES
FES
FES
FES
FES group
averages
PC
PC
PC
PC
PC
PC
PC
PC
PC
PC
PC group
averages
ES
ES
ES
ES
ES
ES
ES
ES
ES
ES
ES group
averages

Cholesterol

HDL

LDL

Age Sex

Pre

Post

%⌬

Pre

Post

%⌬

Pre

Post

%⌬

Pre

Post

%⌬

7
7
7
8
8
9
11
12
12
13

F
M
M
M
M
F
M
F
F
F

96
59
56
52
67
45
136
111
150
66

103
63
44
38
52
48
77
50
144
152

7.3
6.8
⫺21.4
⫺26.9
⫺22.4
6.7
⫺43.4
⫺55.0
⫺4.0
130.3

188
144
140
143
126
143
188
164
210
114

231
124
158
128
130
147
169
165
211
141

22.9
⫺13.9
12.9
⫺10.5
3.2
2.8
⫺10.1
0.6
0.5
23.7

36
36
49
48
37
38
31
37
25
36

40
37
60
46
37
36
31
53
26
37

11.1
2.8
22.4
⫺4.2
0.0
⫺5.3
0.0
43.2
4.0
2.8

133
97
80
85
76
96
130
105
155
65

171
75
90
75
83
102
123
103
157
74

28.6
⫺22.7
12.5
⫺11.8
9.2
6.3
⫺5.4
⫺1.9
1.3
13.8

5
7
7
7
8
8
8
11
11
12

F
F
M
M
F
M
M
F
M
F

83.8⫾37.3
77
29
219
139
56
72
87
227
75
48

77.1⫾41.9
69
44
155
118
42
69
78
126
75
40

⫺6.7⫾40.6
⫺10.4
51.7
⫺29.2
⫺15.1
⫺25.0
⫺4.2
⫺10.3
⫺44.5
0.0
⫺16.7

156⫾30.1
164
149
181
80
152
202
102
204
219
124

160.4⫾35.8
172
156
182
74
140
215
101
154
181
112

4.4⫾20.4
4.9
4.7
0.6
⫺7.5
⫺7.9
6.4
⫺1.0
⫺24.5
⫺17.4
⫺9.7

37.3⫾7.1
43
55
30
33
40
57
36
33
65
44

40.3⫾10.1
44
48
26
23
41
55
33
24
53
36

3.0⫾5.9
2.3
⫺12.7
⫺13.3
⫺30.3
2.5
⫺3.5
⫺8.3
⫺27.3
⫺18.5
⫺18.2

102.2⫾28.8
106
89
108
20
101
131
49
126
139
71

105.3⫾34.7
115
100
125
28
91
147
53
105
113
69

3.1⫾15.8
8.5
12.4
15.7
40.0
⫺9.9
12.2
8.2
⫺16.7
⫺18.7
⫺2.8

6
11
11
12
12
12
12
12
13
13

F
F
M
F
M
M
M
M
M
M

102.9⫾69.5
35
100
60
101
342
65
23
56
148
97

81.6⫾39.1
63
50
74
77
258
55
99
45
97
76

⫺21.3⫾34.7
80.0
⫺50.0
23.3
⫺23.8
⫺24.6
⫺15.4
330.4
⫺19.6
⫺34.5
⫺21.6

157.7⫾45.7
205
140
138
260
237
175
123
225
115
155

148.7⫾42.8
173
129
132
240
218
152
98
220
102
138

⫺9.0⫾20.4
⫺15.6
⫺7.9
⫺4.3
⫺7.7
⫺8.0
⫺13.1
⫺20.3
⫺2.2
⫺11.3
⫺11.0

47⫾18.5
57
50
36
39
39
35
43
36
24
46

43.5⫾22.8
41
44
34
43
37
32
32
39
20
50

⫺3.5⫾6.8
⫺28.1
⫺12.0
⫺5.6
10.3
⫺5.1
⫺8.6
⫺25.6
8.3
⫺16.7
8.7

90.6⫾39.8
141
70
90
201
130
127
76
178
62
90

89.4⫾38.4
120
75
84
182
130
109
47
172
63
73

⫺1.2⫾14.8
⫺14.9
7.1
⫺6.7
⫺9.5
0.0
⫺14.2
⫺38.2
⫺3.4
1.6
⫺18.9

102.7⫾91.7

89.4⫾62.0⫺13.3⫾45.2

177.3⫾51.3

160.2⫾50.6⫺17.1⫾8.5

40.5⫾9.1

37.2⫾8.3⫺3.3⫾6.5

116.5⫾47.1

105.5⫾45.7⫺11⫾11.3

NOTE. There were no differences between groups over time for any of the lipids (triglycerides, P⫽.929, power⫽.061; cholesterol, P⫽.733, power⫽.097; HDL, P⫽.705, power⫽.103; and LDL,
P⫽.847, power⫽.075). One-tailed paired t tests also showed no changes within each group. When examining average change in lipid values, there were differences between groups forcholesterol (P⫽.032, power⫽.656) and HDL levels (P⫽.05, power⫽.579). Bonferroni post hoc testing showed that the ES group had a decrease in cholesterol as compared with the FES
cycling group.
Abbreviations: ES, electrical stimulation; F, female; HR, heart rate; M, male; NT, not tested; PC, passive cycling; % ⌬, percent change.

CARDIORESPIRATORY EFFECTS OF CYCLING, Johnston

Arch Phys Med Rehabil Vol 90, August 2009

Table 3: Baseline and 6-Month Lipid Values (in mg/dL)

CARDIORESPIRATORY EFFECTS OF CYCLING, Johnston

One limitation of our study is that diet was not controlled, anddiet is a key factor in cholesterol levels. Future research should
include a component focusing on nutrition to determine its
influence on lipid values in these children.
Study Limitations
There are several limitations of this study. First, a control
group not receiving any intervention was not included in the
randomized controlled trial; therefore, the results may havebeen influenced by the developmental stage and growth of thesubjects. Because of this, normative values for children without
disability and data from adults with SCI after exercise programs were used to assist in the understanding of the results.
The physical development of children with SCI for the measures tested is not known and warrants further investigation. A
second limitation is that we did not have a data-logging systemon the cycling or electrical stimulation equipment, so we reliedon the parents for providing the majority of the information on
program adherence through biweekly telephone calls and handwritten logs. The parents were very motivated to participate inthis study because of the potential benefits to their children, so
we believe that overall the parents were accurate in theirreports of adherence.
CONCLUSIONSFor the cardiorespiratory and vascular measures studied,
only children in the FES cycling group showed significant
differences in percent increase in VO2peak as compared withchildren in the passive cycling and electrical stimulationgroups. No differences were found with resting heart rate and
FVC among groups. The electrical stimulation group showed asignificant difference in cholesterol levels as compared with the
FES cycling and passive cycling groups. These findings suggest that an important respiratory change was observed forchildren in the FES cycling group. However, the lack of aneffect on the other variables suggests that an increased intensityof exercise may be needed. Passive cycling and electricalstimulated exercise alone led to no or minimal positive changes
in the cardiorespiratory or vascular measures studied.
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Suppliers
a. Restorative-Therapies Inc, 910 Binney St, Baltimore, MD 21224.
b. Axelgaard Manufacturing Co Inc, 520 Industrial Way, Fallbrook,
CA 92028.
c. Empi 300PV; Empi, 599 Cardigan Rd, St. Paul, MN 55126.
d. Viasys Healthcare, 22745 Savi Ranch Pkwy, Yorba Linda, CA
92887.
e. Hans Rudolph Inc, 7200 Wyandotte, Kansas City, MO 64114.